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Crystal Resolution in Raman Spetctoscopy for Pharmaceutical Analysis, Volume 2 (Volume Two: Latest in Genomics Methodologies for Therapeutics: Gene Editing, NGS and BioInformatics, Simulations and the Genome Ontology), Part 1: Next Generation Sequencing (NGS)

Crystal Resolution in Raman Spetctoscopy for Pharmaceutical Analysis

Curator: Larry H. Bernstein, MD, FCAP

 

Investigating Crystallinity Using Low Frequency Raman Spectroscopy: Applications in Pharmaceutical Analysis

http://images.alfresco.advanstar.com/alfresco_images/pharma/2016/01/21/52099838-6354-4ad4-b6f9-9c7c8061f307/Gordon-figure01_web.jpg

Figure 1: Illustration of an exemplar low-frequency Raman setup with a 785-nm laser.

The second system is based on a pre-built SureBlock XLF-CLM THz-Raman system from Ondax Inc. The laser (830 nm, 200 mW), cleanup filters, and laser line filters are all self-contained inside of the instrument but operate on the same principles as the 785-nm system. The sample is arranged in a 180° backscattering geometry relative to a 10× microscope lens. This system is then coupled via a fiber-optic cable to a Princeton Instruments SP2150i spectrograph and PIXIS 100 CCD camera. The 0.15-m spectrograph is used in conjunction with either a 1200- or 1800-groove/mm blazed diffraction grating to adjust the resolution and spectral range.

Crystalline Versus Amorphous Samples

The Raman spectrum of crystalline and amorphous solids differ greatly in the low-frequency region (see Figure 2) because of the highly ordered and highly disordered molecular environments of the respective solids. However, the mid-frequency region can also be noticeably altered by the changing environment (Figure 3).

 

 

http://images.alfresco.advanstar.com/alfresco_images/pharma/2016/01/21/52099838-6354-4ad4-b6f9-9c7c8061f307/Gordon-figure03_web.jpg

Figure 3: Raman spectra of griseofulvin

Ensuring Accuracy

A potential issue is optical artifacts, and these may be identified by the analysis of both Stokes and anti-Stokes spectra. One advantage of the experimental setups described is that signal from the sample may be measured within minutes and it is nondestructive, thus allowing Raman spectra to be collected from a single sample using both techniques at virtually the same time. This approach permits the examination of low-frequency Raman data with 785-nm and 830-nm excitation and allows comparison with Fourier transform (FT)-Raman spectra, in which it is possible to collect meaningful data down to a Raman shift of 50 cm-1. The benefits are demonstrated in Figure 4. In this data, each technique produces consistent bands with similar Raman shifts and relative intensities. While Raman data were not collected below 50 cm-1 using the 1064-nm system, the bands at 69 and 96 cm-1 are consistent with the 785- and 830-nm data. Furthermore, the latter two methods show consistency with bands appearing around 32 and 46 cm-1 for both techniques.

http://images.alfresco.advanstar.com/alfresco_images/pharma/2016/01/21/52099838-6354-4ad4-b6f9-9c7c8061f307/Gordon-figure04_web.jpg

Figure 4: Comparison of the low-frequency region of three Raman spectroscopic techniques.

Case Studies

So far there have been few studies to utilize low-frequency Raman spectroscopy in the analysis of pharmaceutical crystallinity. Despite this, the literature does contain articles that demonstrate the promising applicability of the technique.

Mah and colleagues (38) studied the level of crystallinity of griseofulvin using low-frequency Raman spectroscopy with PLS analysis. In this study a batch of amorphous griseofulvin (which was checked using X-ray powder diffractometry) was prepared by melting the griseofulvin and rapidly cooling it again using liquid nitrogen. Condensed water was removed by placing the sample over phosphorus pentoxide and the glassy sample was then ground using mortar and pestle. Calibrated samples of 2%, 4%, 6%, 8%, and 10% crystallinity were then created though geometric mixing of the amorphous and crystalline samples; following this mixing, the samples were then pressed into tablets. Many tablets were then stored in differing temperatures (30 °C, 35 °C, and 40 °C) at 0% humidity. Low-frequency 785-nm, mid-frequency 785-nm, and FT-Raman spectroscopies were performed simultaneously on each sample. After PLS analysis, limits of detection (LOD) and limits of quantification (LOQ) were calculated. The results of this research showed that each of these three techniques were capable of quantifying crystallinity. It also showed that FT-Raman and low-frequency Raman techniques were able to both detect and quantify crystallinity earlier than the mid-frequency 785 nm Raman technique. The respective LOD and LOQ values for FT-Raman, low-frequency Raman, and mid-frequency Raman are as follows: LOD values: 0.6%, 1.1%, and 1.5%; LOQ values: 1.8%, 3.4%, and 4.6%. The root mean squared errors of prediction (RMSEP) were also calculated and, like the LOD and LOQ values, indicated that the FT-Raman data had the lowest error, followed by the low-frequency Raman, and mid-frequency Raman had the largest errors of the three techniques. The recrystallization tests that were performed indicated that higher temperatures showed a distinct increase in the rate of recrystallization and that each technique provided similar results (within experimental error). It is also important to note that each technique gave similar spectra (where applicable), which provides supporting evidence that the data is meaningful. Overall, the conclusions of this research were that low-frequency predictions of crystallinity are at least as accurate as the predictions made using mid-frequency Raman techniques. It is arguable that low-frequency Raman is better because of the presence of stronger spectral features and because they are intrinsically linked with crystallinity.

Hédoux and colleagues (36) investigated the crystallinity of indomethacin using low-frequency Raman spectroscopy and compared the results with high frequency data. The ranges of interest were indicated to be 5–250 cm-1and 1500–1750 cm-1 regions. Samples of indomethacin were milled using a cryogenic mill to avoid mechanical heating of the sample, with full amorphous samples being obtained after 25 min of milling. Methods used in this study include Raman spectroscopy, isothermal differential scanning calorimetry (DSC), and X-ray diffractometry as well as the milling technique. The primary objective of this research was to use all of these techniques to monitor the crystallization of amorphous indomethacin to the more stable γ-state while the sample was at room temperature–well below the glass transition temperature,Tg = 43 °C. The results of this research did in fact show that low-frequency Raman spectroscopy is a very sensitive technique for identifying very small amounts of crystallinity within mostly amorphous samples. The data was supported by the well-established methods for monitoring crystallinity: XRD and DSC. This paper particularly noted the benefit of low acquisition times associated with low-frequency Raman spectroscopy compared with the other techniques used.

Low-frequency Raman spectroscopy was also used to monitor two polymorphic forms of caffeine after grinding and pressurization of the samples (39). Pressurization was performed hydrostatically using a gasketed membrane diamond anvil cell (MDAC), while ball milling was used as the method of grinding the sample. Analysis methods used were low-frequency Raman and X-ray diffraction. Low-frequency Raman spectra revealed that, upon slight pressurization, caffeine form I transforms into a metastable state slightly different from that of form II and that a disordered (amorphous) state is achieved in both forms when pressurized above 2 GPa. In contrast, it is concluded that grinding results in the transformation of each form into the other with precise grinding times, thus also generating an intermediate form, which was found to only be observable using low-frequency Raman spectroscopy. The caffeine data, as well as the low-frequency data obtained for indomethacin were further discussed by Hédoux and colleagues (40).

Larkin and colleagues (41) used low-frequency Raman in conjunction with other techniques to characterize several different APIs and their various forms. The other techniques include FT-Raman spectroscopy, X-ray powder diffraction (XRPD), and single-crystal X-ray diffractometry. The APIs studied include carbamazepine, apixaban diacid co-crystals, theophylline, and caffeine and were prepared in various ways that are not detailed here. During this research, low-frequency Raman spectroscopy played an important role in understanding the structures while in their various forms. However, more importantly, low-frequency Raman spectroscopy produced information-rich regions below 200 cm-1 for each of the crystalline samples and noticeably broad features when the APIs were in solution.

Wang and colleagues (42) investigated the applicability of low-frequency Raman spectroscopy in the analysis of respirable dosage forms of various pharmaceuticals. The analyzed pharmaceuticals were involved in the treatment of asthma or chronic obstructive pulmonary disease (COPD) and include salmeterol xinafoate, formoterol fumarate, glycopyrronium bromide, fluticasone propionate, mometasone furoate, and salbutamol sulfate. Various formulations of amino acid excipients were also analyzed in this study. Results indicated that the use of low-frequency Raman analysis was beneficial because of the large features found in the region and allowed for reliable identification of each of the dosage forms. Not only this, it also allowed unambiguous identification of two similar bronchodilators, albuterol (Ventolin) and salbutamol (Airomir).

Heyler and colleagues (43) collected both the low-frequency and fingerprint region of Raman spectra from several polymorphs of carbamazepine, an anticonvulsant and mood stabilizer. This study found that the different polymorphs of this API could be distinguished effectively using these two regions. Similarly, Al-Dulaimi and colleagues (44) demonstrated that polymorphic forms of paracetamol, flufenamic acid, and imipramine hydrochloride could be screened using low-frequency Raman and only milligram quantities of each drug. In this study, paracetamol and flufenamic acid were used as the model compounds for comparison with a previously unstudied system (imipramine hydrochloride). Features within the low-frequency Raman regions of spectra were shown to be significantly different between forms of each drug. Therefore this study also indicated that the polymorphs were highly distinguishable using the technique. Hence, like all other previously mentioned case studies, these investigations further demonstrate the utility of low-frequency Raman spectroscopy as a fast and effective method for screening pharmaceuticals for crystallinity.

Conclusions

Low-frequency Raman spectroscopy is a new technique in the field of pharmaceuticals, as well as in general studies of crystallinity. This is despite indications in previous studies showing an innate ability of the technique for identifying crystalline materials and in some cases, quantifying crystallinity. Arguably one of the most beneficial aspects of this technique is the relatively small amount of time necessary to prepare and analyze samples when compared with XRD or DSC. This should ensure the growing use of low-frequency Raman spectroscopy in, not only pharmaceutical crystallinity studies, but also crystallinity studies of other substances as well.

References

  1. J.R. Ferraro and K. Nakamoto, Introductory Raman Spectroscopy, 1st Edition (Academic Press, San Diego, 1994).
  2. K.C. Gordon and C.M. McGoverin, Int. J. Pharm. 417, 151–162 (2011).
  3. D. Law et al., J. Pharm. Sci. 90, 1015–1025 (2001).
  4. G.H. Ward and R.K. Schultz, Pharm. Res. 12, 773–779 (1995).
  5. M.D. Ticehurst et al., Int. J. Pharm. 193, 247–259 (2000).
  6. M. Rani, R. Govindarajan, R. Surana, and R. Suryanarayanan, Pharm. Res. 23, 2356–2367 (2006).
  7. M.J. Pikal, in Polymorphs of Pharmaceutical Solids, H.G. Brittain, Ed. (Marcel Dekker, New York, 1999), pp. 395–419.
  8. M. Ohta and G. Buckton, Int. J. Pharm. 289, 31–38 (2005).
  9. J. Han and R. Suryanarayanan, Pharm. Dev. Technol. 3, 587–596 (1998).
  10. S. Debnath and R. Suryanarayanan, AAPS PharmSciTech. 5, 1–11 (2004).
  11. C.J. Strachan, T. Rades, D.A. Newnham, K.C. Gordon, M. Pepper, and P.F. Taday, Chem. Phys. Lett. 390, 20–24 (2004).
  12. Y.C. Shen, Int. J. Pharm. 417, 48–60 (2011).
  13. G.W. Chantry, in Submillimeter Spectroscopy: A Guide to the Theoretical and Experimental Physics of the Far Infrared, 1st Edition (Academic Press Inc. Ltd., Waltam, 1971).
  14. D. Tuschel, Spectroscopy 30(9), 18–31 (2015).
  15. P.M.A. Sherwood, Vibrational Spectroscopy of Solids (Cambridge University Press, Cambridge, 1972).
  16. L. Ho et al., J. Control. Release. 119, 253–261 (2007).
  17. V.P. Wallace et al., Faraday Discuss. 126, 255–263 (2004).
  18. F.S. Vieira and C. Pasquini, Anal. Chem. 84, 3780–3786 (2014).
  19. J. Darkwah, G. Smith, I. Ermolina, and M. Mueller-Holtz, Int. J. Pharm.455, 357–364 (2013).
  20. S. Kojima, T. Shibata, H. Igawa, and T. Mori, IOP Conf. Ser. Mater. Sci. Eng. 54, 1–6 (2014).
  21. T. Shibata, T. Mori, and S. Kojima, Spectrochim. Acta Part A Mol. Biomol. Spectrosc. 150, 207–211 (2015).
  22. S.P. Delaney, D. Pan, M. Galella, S.X. Yin, and T.M. Korter, Cryst. Growth Des. 12, 5017–5024 (2012).
  23. M.D. King, W.D. Buchanan, and T.M. Korter, Anal. Chem. 83, 3786–3792 (2011).
  24. C.J. Strachan et al., J. Pharm. Sci. 94, 837–846 (2005).
  25. C.M. McGoverin, T. Rades, and K.C. Gordon, J. Pharm. Sci. 97, 4598–4621 (2008).
  26. A. Heinz, C.J. Strachan, K.C. Gordon, and T. Rades, J. Pharm. Pharmacol. 971–988 (2009).,<>
  27. H.G. Brittain, J. Pharm. Sci. 86, 405–412 (1997).
  28. L. Yu, S.M. Reutzel, and G. A. Stephenson, Pharm. Sci. Technol. Today1, 118–127 (1998).
  29. M. Dracínský, E. Procházková, J. Kessler, J. Šebestík, P. Matejka, and P. Bour, J. Phys. Chem. B. 117, 7297–7307 (2013).
  30. P. Sharma et al., J. Raman Spectrosc. DOI 10.1002/jrs.4834, wileyonlinelibrary.com (2015).
  31. A.P. Ayala, Vib. Spectrosc. 45, 112–116 (2007).
  32. J.F. Scott, Spex Speak. 17, 1–12 (1972).
  33. D.P. Strommen and K. Nakamoto, in Laboratory Raman Spectroscopy, 1st Edition (John Wiley & Sons Inc., New York, 1984).
  34. A.L. Glebov, O. Mokhun, A. Rapaport, S. Vergnole, V. Smirnov, and L.B. Glebov, Proc. SPIE. 8428, 84280C1–84280C11 (2012).
  35. E.P.J. Parrott and J.A. Zeitler, Appl. Spectrosc. 69, 1–25 (2015).
  36. A. Hédoux, L. Paccou, Y. Guinet, J.F. Willart, and M. Descamps, Eur. J. Pharm. Sci. 38, 156–164 (2009).
  37. R.L. McCreery, in Raman Spectroscopy for Chemical Analysis, 1st Edition (John Wiley & Sons Inc., New York, 2000).
  38. P.T. Mah, S.J. Fraser, M.E. Reish, T. Rades, K.C. Gordon, and C.J. Strachan, Vib. Spectrosc. 77, 10–16 (2015).
  39. A. Hédoux, A.A. Decroix, Y. Guinet, L. Paccou, P. Derollez, and M. Descamps, J. Phys. Chem. B. 115, 5746–5753 (2011).
  40. A. Hédoux, Y. Guinet, and M. Descamps, Int. J. Pharm. 417, 17–31 (2011).
  41. P.J. Larkin, M. Dabros, B. Sarsfield, E. Chan, J.T. Carriere, and B.C. Smith, Appl. Spectrosc. 68, 758–776 (2014).
  42. H. Wang, M. A. Boraey, L. Williams, D. Lechuga-Ballesteros, and R. Vehring, Int. J. Pharm. 469, 197–205 (2014).
  43. R. Heyler, J. Carriere, and B. Smith, in “Raman Technology for Today’s Spectroscopists,” supplement to Spectroscopy (June), 44–50 (2013).
  44. S. Al-Dulaimi, A. Aina, and J. Burley, CrystEngComm. 12, 1038–1040 (2010).

 

The drawing in Figure 1 is that of a six-membered ring or hexagon. A carbon atom is located at each vertex of the hexagon and a hydrogen atom is attached to each carbon, although it is not written in. The circle inside the ring represents that the electrons are delocalized which is illustrated in Figure 2.

http://images.alfresco.advanstar.com/alfresco_images/pharma/2016/02/12/645ee751-2432-4444-8af1-ded62697ee27/IR-Spectral-figure02_web.jpg

Figure 2: Top: The P orbitals on each of the six carbon atoms in benzene that contribute an electron to the ring. Bottom: the collection of delocalized P orbital electrons forming a cloud of electron density above and below the benzene ring.

Each of the carbon atoms in a benzene ring contains two P orbitals containing a lone electron, and one of these orbitals is perpendicular to the benzene ring as seen in the top of Figure 2. There is enough orbital overlap that these electrons, rather than being confined between two carbon atoms as might be expected, instead delocalize and form clouds of electron density above and below the plane of the ring. This type of bonding is called aromatic bonding(2), and a ring that has aromatic bonding is called an aromatic ring. It is aromatic bonding that gives aromatic rings their unique structures, chemistry, and IR spectra. Benzene is simply a commonly found aromatic ring. Other types of aromatic molecules include polycyclic aromatic hydrocarbons (PAHs), such as naphthalene, that contain two or more benzene rings that are fused (which means adjacent rings share two carbon atoms), and heterocyclic aromatic rings which are aromatic rings that contain a noncarbon atom such as nitrogen. Pyridine is an example of one of these. The interpretation of the IR spectra of these latter aromatic molecules will be discussed in future articles.

The IR Spectrum of Benzene

The IR spectrum of benzene is shown in Figure 3.

http://images.alfresco.advanstar.com/alfresco_images/pharma/2016/02/12/645ee751-2432-4444-8af1-ded62697ee27/IR-Spectral-figure03_web.jpg

 

09:00

Super-Resolution Fluorescence Microscopy: Where To Go Now?
Bernd Rieger, Quantitative Imaging Group Leader, Delft University of Technology

09:30

Keynote Presentation

From Molecules To Whole Organs
Francesco Pavone, Principal Investigator, LENS, University of Florence

Some examples of correlative microscopies, combining linear and non linear techniques will be described. Particular attention will be devoted Alzheimer disease or to neural plasticity after damage as neurobiological application.

10:15

Super-Resolution Imaging by dSTORM
Markus Sauer, Professor, Julius-Maximilians-Universität Würzburg

10:45

Coffee and Networking in Exhibition Hall

11:15

Correlated Fluorescence And X-Ray Tomography: Finding Molecules In Cellular CT Scans
Carolyn Larabell, Professor, University of California San Francisco

11:45

Integrating Advanced Fluorescence Microscopy Techniques Reveals Nanoscale Architecture And Mesoscale Dynamics Of Cytoskeletal Structures Promoting Cell Migration And Invasion
Alessandra Cambi, Assistant Professor, University of Nijmegen

This lecture will describe our efforts to exploit and integrate a variety of advanced microscopy techniques to unravel the nanoscale structural and dynamic complexity of individual podosomes as well as formation, architecture and function of mesoscale podosome clusters.

12:15

Multi-Photon-Like Fluorescence Microscopy Using Two-Step Imaging Probes
George Patterson, Investigator, National Institutes of Health

12:45

Lunch & Networking in Exhibition Hall

14:15

Technology Spotlight

14:30

3D Single Particle Tracking: Following Mitochondria in Zebrafish Embryos
Don Lamb, Professor, Ludwig-Maximilians-University

15:00

Visualizing Mechano-Biology: Quantitative Bioimaging Tools To Study The Impact Of Mechanical Stress On Cell Adhesion And Signalling
Bernhard Wehrle-Haller, Group Leader, University of Geneva

15:30

Superresolution Imaging Of Clathrin-Mediated Endocytosis In Yeast
Jonas Ries, Group Leader, EMBL Heidelberg

We use single-molecule localization microscopy to investigate the dynamic structural organization of the east endocytic machinery. We discovered a striking ring-shaped pre-patterning of the actin nucleation zone, which is key for an efficient force generation and membrane invagination.

16:00

Coffee and Networking in Exhibition Hall

16:30

Optical Imaging of Molecular Mechanisms of Disease
Clemens Kaminski, Professor, University of Cambridge

17:00

3-D Optical Tomography For Ex Vivo And In Vivo Imaging
James McGinty, Professor, Imperial College London

17:30

End Of Day One

Wednesday, 15 June 2016

09:00

Imaging Gene Regulation in Living Cells at the Single Molecule Level
James Zhe Liu, Group Leader, Janelia Research Campus, Howard Hughes Medical Institute

09:30

Keynote Presentation

Super-Resolution Microscopy With DNA Molecules
Ralf Jungmann, Group Leader, Max Planck Institute of Biochemistry

10:15

A Revolutionary Miniaturised Instrument For Single-Molecule Localization Microscopy And FRET
Achillefs Kapanidis, Professor, University of Oxford

10:45

Coffee and Networking in Exhibition Hall

11:15

Democratising Live-Cell High-Speed Super-Resolution Microscopy
Ricardo Henriques, Group Leader, University College London

11:45

Democratising Live-Cell High-Speed Super-Resolution Microscopy

12:15

Information In Localisation Microscopy
Susan Cox, Professor, Kings College London

12:45

Lunch & Networking in Exhibition Hall

14:15

Technology Spotlight

14:30

High-Content Imaging Approaches For Drug Discovery For Neglected Tropical Diseases
Manu De Rycker, Team Leader, University of Dundee

The development of new drugs for intracellular parasitic diseases is hampered by difficulties in developing relevant high-throughput cell-based assays. Here we present how we have used image-based high-content screening approaches to address some of these issues.

15:00

High Resolution In Vivo Histology: Clinical in vivo Subcellular Imaging using Femtoseceond Laser Multiphoton/CARS Tomography
Karsten König, Professor, Saarland University

We report on a certified, medical, transportable multipurpose nonlinear microscopic imagingsystem based on a femtosecond excitation source and a photonic crystal fiber with multiple miniaturized time-correlated single-photon counting detectors.

15:30

Coffee and Networking in Exhibition Hall

16:00

Lateral Organization Of Plasma Membrane Constituents At The Nanoscale
Gerhard Schutz, Professor, Vienna University of Technology

It is of interest how proteins are spatially distributed over the membrane, and whether they conjoin and move as part of multi-molecular complexes. In my lecture, I will discuss methods for approaching the two questions, and provide biological examples.

16:30

Correlative Light And Electron Microscopy In Structural Cell Biology
Wanda Kukulski, Group Leader, University of Cambridge

17:00

Close of Conference

 

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CRISPR/Cas9, Familial Amyloid Polyneuropathy ( FAP) and Neurodegenerative Disease

CRISPR/Cas9, Familial Amyloid Polyneuropathy (FAP) and Neurodegenerative Disease, Volume 2 (Volume Two: Latest in Genomics Methodologies for Therapeutics: Gene Editing, NGS and BioInformatics, Simulations and the Genome Ontology), Part 2: CRISPR for Gene Editing and DNA Repair

CRISPR/Cas9, Familial Amyloid Polyneuropathy ( FAP) and Neurodegenerative Disease

Curator: Larry H. Bernstein, MD, FCAP

 

CRISPR/Cas9 and Targeted Genome Editing: A New Era in Molecular Biology

https://www.neb.com/tools-and-resources/feature-articles/crispr-cas9-and-targeted-genome-editing-a-new-era-in-molecular-biology

The development of efficient and reliable ways to make precise, targeted changes to the genome of living cells is a long-standing goal for biomedical researchers. Recently, a new tool based on a bacterial CRISPR-associated protein-9 nuclease (Cas9) from Streptococcus pyogenes has generated considerable excitement (1). This follows several attempts over the years to manipulate gene function, including homologous recombination (2) and RNA interference (RNAi) (3). RNAi, in particular, became a laboratory staple enabling inexpensive and high-throughput interrogation of gene function (4, 5), but it is hampered by providing only temporary inhibition of gene function and unpredictable off-target effects (6). Other recent approaches to targeted genome modification – zinc-finger nucleases [ZFNs, (7)] and transcription-activator like effector nucleases [TALENs (8)]– enable researchers to generate permanent mutations by introducing doublestranded breaks to activate repair pathways. These approaches are costly and time-consuming to engineer, limiting their widespread use, particularly for large scale, high-throughput studies.

The Biology of Cas9

The functions of CRISPR (Clustered Regularly Interspaced Short Palindromic Repeats) and CRISPR-associated (Cas) genes are essential in adaptive immunity in select bacteria and archaea, enabling the organisms to respond to and eliminate invading genetic material. These repeats were initially discovered in the 1980s in E. coli (9), but their function wasn’t confirmed until 2007 by Barrangou and colleagues, who demonstrated that S. thermophilus can acquire resistance against a bacteriophage by integrating a genome fragment of an infectious virus into its CRISPR locus (10).

Three types of CRISPR mechanisms have been identified, of which type II is the most studied. In this case, invading DNA from viruses or plasmids is cut into small fragments and incorporated into a CRISPR locus amidst a series of short repeats (around 20 bps). The loci are transcribed, and transcripts are then processed to generate small RNAs (crRNA – CRISPR RNA), which are used to guide effector endonucleases that target invading DNA based on sequence complementarity (Figure 1) (11).

Figure 1. Cas9 in vivo: Bacterial Adaptive Immunity

https://www.neb.com/~/media/NebUs/Files/Feature%20Articles/Images/FA_Cas9_Fig1_Cas9InVivo.png

In the acquisition phase, foreign DNA is incorporated into the bacterial genome at the CRISPR loci. CRISPR loci is then transcribed and processed into crRNA during crRNA biogenesis. During interference, Cas9 endonuclease complexed with a crRNA and separate tracrRNA cleaves foreign DNA containing a 20-nucleotide crRNA complementary sequence adjacent to the PAM sequence. (Figure not drawn to scale.)

https://www.neb.com/~/media/NebUs/Files/Feature%20Articles/Images/FA_Cas9_GenomeEditingGlossary.png

One Cas protein, Cas9 (also known as Csn1), has been shown, through knockdown and rescue experiments to be a key player in certain CRISPR mechanisms (specifically type II CRISPR systems). The type II CRISPR mechanism is unique compared to other CRISPR systems, as only one Cas protein (Cas9) is required for gene silencing (12). In type II systems, Cas9 participates in the processing of crRNAs (12), and is responsible for the destruction of the target DNA (11). Cas9’s function in both of these steps relies on the presence of two nuclease domains, a RuvC-like nuclease domain located at the amino terminus and a HNH-like nuclease domain that resides in the mid-region of the protein (13).

To achieve site-specific DNA recognition and cleavage, Cas9 must be complexed with both a crRNA and a separate trans-activating crRNA (tracrRNA or trRNA), that is partially complementary to the crRNA (11). The tracrRNA is required for crRNA maturation from a primary transcript encoding multiple pre-crRNAs. This occurs in the presence of RNase III and Cas9 (12).

During the destruction of target DNA, the HNH and RuvC-like nuclease domains cut both DNA strands, generating double-stranded breaks (DSBs) at sites defined by a 20-nucleotide target sequence within an associated crRNA transcript (11, 14). The HNH domain cleaves the complementary strand, while the RuvC domain cleaves the noncomplementary strand.

The double-stranded endonuclease activity of Cas9 also requires that a short conserved sequence, (2–5 nts) known as protospacer-associated motif (PAM), follows immediately 3´- of the crRNA complementary sequence (15). In fact, even fully complementary sequences are ignored by Cas9-RNA in the absence of a PAM sequence (16).

Cas9 and CRISPR as a New Tool in Molecular Biology

The simplicity of the type II CRISPR nuclease, with only three required components (Cas9 along with the crRNA and trRNA) makes this system amenable to adaptation for genome editing. This potential was realized in 2012 by the Doudna and Charpentier labs (11). Based on the type II CRISPR system described previously, the authors developed a simplified two-component system by combining trRNA and crRNA into a single synthetic single guide RNA (sgRNA). sgRNAprogrammed Cas9 was shown to be as effective as Cas9 programmed with separate trRNA and crRNA in guiding targeted gene alterations (Figure 2A).

To date, three different variants of the Cas9 nuclease have been adopted in genome-editing protocols. The first is wild-type Cas9, which can site-specifically cleave double-stranded DNA, resulting in the activation of the doublestrand break (DSB) repair machinery. DSBs can be repaired by the cellular Non-Homologous End Joining (NHEJ) pathway (17), resulting in insertions and/or deletions (indels) which disrupt the targeted locus. Alternatively, if a donor template with homology to the targeted locus is supplied, the DSB may be repaired by the homology-directed repair (HDR) pathway allowing for precise replacement mutations to be made (Figure 2A) (17, 18).

Cong and colleagues (1) took the Cas9 system a step further towards increased precision by developing a mutant form, known as Cas9D10A, with only nickase activity. This means it cleaves only one DNA strand, and does not activate NHEJ. Instead, when provided with a homologous repair template, DNA repairs are conducted via the high-fidelity HDR pathway only, resulting in reduced indel mutations (1, 11, 19). Cas9D10A is even more appealing in terms of target specificity when loci are targeted by paired Cas9 complexes designed to generate adjacent DNA nicks (20) (see further details about “paired nickases” in Figure 2B).

The third variant is a nuclease-deficient Cas9 (dCas9, Figure 2C) (21). Mutations H840A in the HNH domain and D10A in the RuvC domain inactivate cleavage activity, but do not prevent DNA binding (11, 22). Therefore, this variant can be used to sequence-specifically target any region of the genome without cleavage. Instead, by fusing with various effector domains, dCas9 can be used either as a gene silencing or activation tool (21, 23–26). Furthermore, it can be used as a visualization tool. For instance, Chen and colleagues used dCas9 fused to Enhanced Green Fluorescent Protein (EGFP) to visualize repetitive DNA sequences with a single sgRNA or nonrepetitive loci using multiple sgRNAs (27).

Figure 2. CRISPR/Cas9 System Applications

https://www.neb.com/~/media/NebUs/Files/Feature%20Articles/Images/FA_Cas9_Fig2_Cas9forGenomeEditing.png?device=modal

  1. Wild-type Cas9 nuclease site specifically cleaves double-stranded DNA activating double-strand break repair machinery. In the absence of a homologous repair template non-homologous end joining can result in indels disrupting the target sequence. Alternatively, precise mutations and knock-ins can be made by providing a homologous repair template and exploiting the homology directed repair pathway.
    B. Mutated Cas9 makes a site specific single-strand nick. Two sgRNA can be used to introduce a staggered double-stranded break which can then undergo homology directed repair.
    C. Nuclease-deficient Cas9 can be fused with various effector domains allowing specific localization. For example, transcriptional activators, repressors, and fluorescent proteins.

Targeting Efficiency and Off-target Mutations

Targeting efficiency, or the percentage of desired mutation achieved, is one of the most important parameters by which to assess a genome-editing tool. The targeting efficiency of Cas9 compares favorably with more established methods, such as TALENs or ZFNs (8). For example, in human cells, custom-designed ZFNs and TALENs could only achieve efficiencies ranging from 1% to 50% (29–31). In contrast, the Cas9 system has been reported to have efficiencies up to >70% in zebrafish (32) and plants (33), and ranging from 2–5% in induced pluripotent stem cells (34). In addition, Zhou and colleagues were able to improve genome targeting up to 78% in one-cell mouse embryos, and achieved effective germline transmission through the use of dual sgRNAs to simultaneously target an individual gene (35).

A widely used method to identify mutations is the T7 Endonuclease I mutation detection assay (36, 37) (Figure 3). This assay detects heteroduplex DNA that results from the annealing of a DNA strand, including desired mutations, with a wildtype DNA strand (37).

Figure 3. T7 Endonuclease I Targeting Efficiency Assay

https://www.neb.com/~/media/NebUs/Files/Feature%20Articles/Images/FA_Cas9_Fig3_T7Assay_TargetEfficiency.png

Genomic DNA is amplified with primers bracketing the modified locus. PCR products are then denatured and re-annealed yielding 3 possible structures. Duplexes containing a mismatch are digested by T7 Endonuclease I. The DNA is then electrophoretically separated and fragment analysis is used to calculate targeting efficiency.

Another important parameter is the incidence of off-target mutations. Such mutations are likely to appear in sites that have differences of only a few nucleotides compared to the original sequence, as long as they are adjacent to a PAM sequence. This occurs as Cas9 can tolerate up to 5 base mismatches within the protospacer region (36) or a single base difference in the PAM sequence (38). Off-target mutations are generally more difficult to detect, requiring whole-genome sequencing to rule them out completely.

Recent improvements to the CRISPR system for reducing off-target mutations have been made through the use of truncated gRNA (truncated within the crRNA-derived sequence) or by adding two extra guanine (G) nucleotides to the 5´ end (28, 37). Another way researchers have attempted to minimize off-target effects is with the use of “paired nickases” (20). This strategy uses D10A Cas9 and two sgRNAs complementary to the adjacent area on opposite strands of the target site (Figure 2B). While this induces DSBs in the target DNA, it is expected to create only single nicks in off-target locations and, therefore, result in minimal off-target mutations.

By leveraging computation to reduce off-target mutations, several groups have developed webbased tools to facilitate the identification of potential CRISPR target sites and assess their potential for off-target cleavage. Examples include the CRISPR Design Tool (38) and the ZiFiT Targeter, Version 4.2 (39, 40).

Applications as a Genome-editing and Genome Targeting Tool

Following its initial demonstration in 2012 (9), the CRISPR/Cas9 system has been widely adopted. This has already been successfully used to target important genes in many cell lines and organisms, including human (34), bacteria (41), zebrafish (32), C. elegans (42), plants (34), Xenopus tropicalis (43), yeast (44), Drosophila (45), monkeys (46), rabbits (47), pigs (42), rats (48) and mice (49). Several groups have now taken advantage of this method to introduce single point mutations (deletions or insertions) in a particular target gene, via a single gRNA (14, 21, 29). Using a pair of gRNA-directed Cas9 nucleases instead, it is also possible to induce large deletions or genomic rearrangements, such as inversions or translocations (50). A recent exciting development is the use of the dCas9 version of the CRISPR/Cas9 system to target protein domains for transcriptional regulation (26, 51, 52), epigenetic modification (25), and microscopic visualization of specific genome loci (27).

The CRISPR/Cas9 system requires only the redesign of the crRNA to change target specificity. This contrasts with other genome editing tools, including zinc finger and TALENs, where redesign of the protein-DNA interface is required. Furthermore, CRISPR/Cas9 enables rapid genome-wide interrogation of gene function by generating large gRNA libraries (51, 53) for genomic screening.

The Future of CRISPR/Cas9

The rapid progress in developing Cas9 into a set of tools for cell and molecular biology research has been remarkable, likely due to the simplicity, high efficiency and versatility of the system. Of the designer nuclease systems currently available for precision genome engineering, the CRISPR/Cas system is by far the most user friendly. It is now also clear that Cas9’s potential reaches beyond DNA cleavage, and its usefulness for genome locus-specific recruitment of proteins will likely only be limited by our imagination.

 

Scientists urge caution in using new CRISPR technology to treat human genetic disease

By Robert Sanders, Media relations | MARCH 19, 2015
http://news.berkeley.edu/2015/03/19/scientists-urge-caution-in-using-new-crispr-technology-to-treat-human-genetic-disease/

http://news.berkeley.edu/wp-content/uploads/2015/03/crispr350.jpg

The bacterial enzyme Cas9 is the engine of RNA-programmed genome engineering in human cells. (Graphic by Jennifer Doudna/UC Berkeley)

A group of 18 scientists and ethicists today warned that a revolutionary new tool to cut and splice DNA should be used cautiously when attempting to fix human genetic disease, and strongly discouraged any attempts at making changes to the human genome that could be passed on to offspring.

Among the authors of this warning is Jennifer Doudna, the co-inventor of the technology, called CRISPR-Cas9, which is driving a new interest in gene therapy, or “genome engineering.” She and colleagues co-authored a perspective piece that appears in the March 20 issue of Science, based on discussions at a meeting that took place in Napa on Jan. 24. The same issue of Science features a collection of recent research papers, commentary and news articles on CRISPR and its implications.    …..

A prudent path forward for genomic engineering and germline gene modification

David Baltimore1,  Paul Berg2, …., Jennifer A. Doudna4,10,*, et al.
http://science.sciencemag.org/content/early/2015/03/18/science.aab1028.full
Science  19 Mar 2015.  http://dx.doi.org:/10.1126/science.aab1028

 

Correcting genetic defects

Scientists today are changing DNA sequences to correct genetic defects in animals as well as cultured tissues generated from stem cells, strategies that could eventually be used to treat human disease. The technology can also be used to engineer animals with genetic diseases mimicking human disease, which could lead to new insights into previously enigmatic disorders.

The CRISPR-Cas9 tool is still being refined to ensure that genetic changes are precisely targeted, Doudna said. Nevertheless, the authors met “… to initiate an informed discussion of the uses of genome engineering technology, and to identify proactively those areas where current action is essential to prepare for future developments. We recommend taking immediate steps toward ensuring that the application of genome engineering technology is performed safely and ethically.”

 

Amyloid CRISPR Plasmids and si/shRNA Gene Silencers

http://www.scbt.com/crispr/table-amyloid.html

Santa Cruz Biotechnology, Inc. offers a broad range of gene silencers in the form of siRNAs, shRNA Plasmids and shRNA Lentiviral Particles as well as CRISPR/Cas9 Knockout and CRISPR Double Nickase plasmids. Amyloid gene silencers are available as Amyloid siRNA, Amyloid shRNA Plasmid, Amyloid shRNA Lentiviral Particles and Amyloid CRISPR/Cas9 Knockout plasmids. Amyloid CRISPR/dCas9 Activation Plasmids and CRISPR Lenti Activation Systems for gene activation are also available. Gene silencers and activators are useful for gene studies in combination with antibodies used for protein detection.    Amyloid CRISPR Knockout, HDR and Nickase Knockout Plasmids

 

CRISPR-Cas9-Based Knockout of the Prion Protein and Its Effect on the Proteome


Mehrabian M, Brethour D, MacIsaac S, Kim JK, Gunawardana C.G, Wang H, et al.
PLoS ONE 2014; 9(12): e114594. http://dx.doi.org/10.1371/journal.pone.0114594

The molecular function of the cellular prion protein (PrPC) and the mechanism by which it may contribute to neurotoxicity in prion diseases and Alzheimer’s disease are only partially understood. Mouse neuroblastoma Neuro2a cells and, more recently, C2C12 myocytes and myotubes have emerged as popular models for investigating the cellular biology of PrP. Mouse epithelial NMuMG cells might become attractive models for studying the possible involvement of PrP in a morphogenetic program underlying epithelial-to-mesenchymal transitions. Here we describe the generation of PrP knockout clones from these cell lines using CRISPR-Cas9 knockout technology. More specifically, knockout clones were generated with two separate guide RNAs targeting recognition sites on opposite strands within the first hundred nucleotides of the Prnp coding sequence. Several PrP knockout clones were isolated and genomic insertions and deletions near the CRISPR-target sites were characterized. Subsequently, deep quantitative global proteome analyses that recorded the relative abundance of>3000 proteins (data deposited to ProteomeXchange Consortium) were undertaken to begin to characterize the molecular consequences of PrP deficiency. The levels of ∼120 proteins were shown to reproducibly correlate with the presence or absence of PrP, with most of these proteins belonging to extracellular components, cell junctions or the cytoskeleton.

http://journals.plos.org/plosone/article/figure/image?size=inline&id=info:doi/10.1371/journal.pone.0114594.g001

http://journals.plos.org/plosone/article/figure/image?size=inline&id=info:doi/10.1371/journal.pone.0114594.g003

 

Development and Applications of CRISPR-Cas9 for Genome Engineering

Patrick D. Hsu,1,2,3 Eric S. Lander,1 and Feng Zhang1,2,*
Cell. 2014 Jun 5; 157(6): 1262–1278.   doi:  10.1016/j.cell.2014.05.010

Recent advances in genome engineering technologies based on the CRISPR-associated RNA-guided endonuclease Cas9 are enabling the systematic interrogation of mammalian genome function. Analogous to the search function in modern word processors, Cas9 can be guided to specific locations within complex genomes by a short RNA search string. Using this system, DNA sequences within the endogenous genome and their functional outputs are now easily edited or modulated in virtually any organism of choice. Cas9-mediated genetic perturbation is simple and scalable, empowering researchers to elucidate the functional organization of the genome at the systems level and establish causal linkages between genetic variations and biological phenotypes. In this Review, we describe the development and applications of Cas9 for a variety of research or translational applications while highlighting challenges as well as future directions. Derived from a remarkable microbial defense system, Cas9 is driving innovative applications from basic biology to biotechnology and medicine.

The development of recombinant DNA technology in the 1970s marked the beginning of a new era for biology. For the first time, molecular biologists gained the ability to manipulate DNA molecules, making it possible to study genes and harness them to develop novel medicine and biotechnology. Recent advances in genome engineering technologies are sparking a new revolution in biological research. Rather than studying DNA taken out of the context of the genome, researchers can now directly edit or modulate the function of DNA sequences in their endogenous context in virtually any organism of choice, enabling them to elucidate the functional organization of the genome at the systems level, as well as identify causal genetic variations.

Broadly speaking, genome engineering refers to the process of making targeted modifications to the genome, its contexts (e.g., epigenetic marks), or its outputs (e.g., transcripts). The ability to do so easily and efficiently in eukaryotic and especially mammalian cells holds immense promise to transform basic science, biotechnology, and medicine (Figure 1).

http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4343198/bin/nihms659174f1.jpg

For life sciences research, technologies that can delete, insert, and modify the DNA sequences of cells or organisms enable dissecting the function of specific genes and regulatory elements. Multiplexed editing could further allow the interrogation of gene or protein networks at a larger scale. Similarly, manipulating transcriptional regulation or chromatin states at particular loci can reveal how genetic material is organized and utilized within a cell, illuminating relationships between the architecture of the genome and its functions. In biotechnology, precise manipulation of genetic building blocks and regulatory machinery also facilitates the reverse engineering or reconstruction of useful biological systems, for example, by enhancing biofuel production pathways in industrially relevant organisms or by creating infection-resistant crops. Additionally, genome engineering is stimulating a new generation of drug development processes and medical therapeutics. Perturbation of multiple genes simultaneously could model the additive effects that underlie complex polygenic disorders, leading to new drug targets, while genome editing could directly correct harmful mutations in the context of human gene therapy (Tebas et al., 2014).

Eukaryotic genomes contain billions of DNA bases and are difficult to manipulate. One of the breakthroughs in genome manipulation has been the development of gene targeting by homologous recombination (HR), which integrates exogenous repair templates that contain sequence homology to the donor site (Figure 2A) (Capecchi, 1989). HR-mediated targeting has facilitated the generation of knockin and knockout animal models via manipulation of germline competent stem cells, dramatically advancing many areas of biological research. However, although HR-mediated gene targeting produces highly precise alterations, the desired recombination events occur extremely infrequently (1 in 106–109 cells) (Capecchi, 1989), presenting enormous challenges for large-scale applications of gene-targeting experiments.

Genome Editing Technologies Exploit Endogenous DNA Repair Machinery

http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4343198/bin/nihms659174f2.gif

To overcome these challenges, a series of programmable nuclease-based genome editing technologies have been developed in recent years, enabling targeted and efficient modification of a variety of eukaryotic and particularly mammalian species. Of the current generation of genome editing technologies, the most rapidly developing is the class of RNA-guided endonucleases known as Cas9 from the microbial adaptive immune system CRISPR (clustered regularly interspaced short palindromic repeats), which can be easily targeted to virtually any genomic location of choice by a short RNA guide. Here, we review the development and applications of the CRISPR-associated endonuclease Cas9 as a platform technology for achieving targeted perturbation of endogenous genomic elements and also discuss challenges and future avenues for innovation.   ……

Figure 4   Natural Mechanisms of Microbial CRISPR Systems in Adaptive Immunity

http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4343198/bin/nihms659174f4.gif

……  A key turning point came in 2005, when systematic analysis of the spacer sequences separating the individual direct repeats suggested their extrachromosomal and phage-associated origins (Mojica et al., 2005Pourcel et al., 2005Bolotin et al., 2005). This insight was tremendously exciting, especially given previous studies showing that CRISPR loci are transcribed (Tang et al., 2002) and that viruses are unable to infect archaeal cells carrying spacers corresponding to their own genomes (Mojica et al., 2005). Together, these findings led to the speculation that CRISPR arrays serve as an immune memory and defense mechanism, and individual spacers facilitate defense against bacteriophage infection by exploiting Watson-Crick base-pairing between nucleic acids (Mojica et al., 2005Pourcel et al., 2005). Despite these compelling realizations that CRISPR loci might be involved in microbial immunity, the specific mechanism of how the spacers act to mediate viral defense remained a challenging puzzle. Several hypotheses were raised, including thoughts that CRISPR spacers act as small RNA guides to degrade viral transcripts in a RNAi-like mechanism (Makarova et al., 2006) or that CRISPR spacers direct Cas enzymes to cleave viral DNA at spacer-matching regions (Bolotin et al., 2005).   …..

As the pace of CRISPR research accelerated, researchers quickly unraveled many details of each type of CRISPR system (Figure 4). Building on an earlier speculation that protospacer adjacent motifs (PAMs) may direct the type II Cas9 nuclease to cleave DNA (Bolotin et al., 2005), Moineau and colleagues highlighted the importance of PAM sequences by demonstrating that PAM mutations in phage genomes circumvented CRISPR interference (Deveau et al., 2008). Additionally, for types I and II, the lack of PAM within the direct repeat sequence within the CRISPR array prevents self-targeting by the CRISPR system. In type III systems, however, mismatches between the 5′ end of the crRNA and the DNA target are required for plasmid interference (Marraffini and Sontheimer, 2010).  …..

In 2013, a pair of studies simultaneously showed how to successfully engineer type II CRISPR systems from Streptococcus thermophilus (Cong et al., 2013) andStreptococcus pyogenes (Cong et al., 2013Mali et al., 2013a) to accomplish genome editing in mammalian cells. Heterologous expression of mature crRNA-tracrRNA hybrids (Cong et al., 2013) as well as sgRNAs (Cong et al., 2013Mali et al., 2013a) directs Cas9 cleavage within the mammalian cellular genome to stimulate NHEJ or HDR-mediated genome editing. Multiple guide RNAs can also be used to target several genes at once. Since these initial studies, Cas9 has been used by thousands of laboratories for genome editing applications in a variety of experimental model systems (Sander and Joung, 2014). ……

The majority of CRISPR-based technology development has focused on the signature Cas9 nuclease from type II CRISPR systems. However, there remains a wide diversity of CRISPR types and functions. Cas RAMP module (Cmr) proteins identified in Pyrococcus furiosus and Sulfolobus solfataricus (Hale et al., 2012) constitute an RNA-targeting CRISPR immune system, forming a complex guided by small CRISPR RNAs that target and cleave complementary RNA instead of DNA. Cmr protein homologs can be found throughout bacteria and archaea, typically relying on a 5 site tag sequence on the target-matching crRNA for Cmr-directed cleavage.

Unlike RNAi, which is targeted largely by a 6 nt seed region and to a lesser extent 13 other bases, Cmr crRNAs contain 30–40 nt of target complementarity. Cmr-CRISPR technologies for RNA targeting are thus a promising target for orthogonal engineering and minimal off-target modification. Although the modularity of Cmr systems for RNA-targeting in mammalian cells remains to be investigated, Cmr complexes native to P. furiosus have already been engineered to target novel RNA substrates (Hale et al., 20092012).   ……

Although Cas9 has already been widely used as a research tool, a particularly exciting future direction is the development of Cas9 as a therapeutic technology for treating genetic disorders. For a monogenic recessive disorder due to loss-of-function mutations (such as cystic fibrosis, sickle-cell anemia, or Duchenne muscular dystrophy), Cas9 may be used to correct the causative mutation. This has many advantages over traditional methods of gene augmentation that deliver functional genetic copies via viral vector-mediated overexpression—particularly that the newly functional gene is expressed in its natural context. For dominant-negative disorders in which the affected gene is haplosufficient (such as transthyretin-related hereditary amyloidosis or dominant forms of retinitis pigmentosum), it may also be possible to use NHEJ to inactivate the mutated allele to achieve therapeutic benefit. For allele-specific targeting, one could design guide RNAs capable of distinguishing between single-nucleotide polymorphism (SNP) variations in the target gene, such as when the SNP falls within the PAM sequence.

 

 

CRISPR/Cas9: a powerful genetic engineering tool for establishing large animal models of neurodegenerative diseases

Zhuchi Tu, Weili Yang, Sen Yan, Xiangyu Guo and Xiao-Jiang Li

Molecular Neurodegeneration 2015; 10:35  http://dx.doi.org:/10.1186/s13024-015-0031-x

Animal models are extremely valuable to help us understand the pathogenesis of neurodegenerative disorders and to find treatments for them. Since large animals are more like humans than rodents, they make good models to identify the important pathological events that may be seen in humans but not in small animals; large animals are also very important for validating effective treatments or confirming therapeutic targets. Due to the lack of embryonic stem cell lines from large animals, it has been difficult to use traditional gene targeting technology to establish large animal models of neurodegenerative diseases. Recently, CRISPR/Cas9 was used successfully to genetically modify genomes in various species. Here we discuss the use of CRISPR/Cas9 technology to establish large animal models that can more faithfully mimic human neurodegenerative diseases.

Neurodegenerative diseases — Alzheimer’s disease(AD),Parkinson’s disease(PD), amyotrophic lateral sclerosis (ALS), Huntington’s disease (HD), and frontotemporal dementia (FTD) — are characterized by age-dependent and selective neurodegeneration. As the life expectancy of humans lengthens, there is a greater prevalence of these neurodegenerative diseases; however, the pathogenesis of most of these neurodegenerative diseases remain unclear, and we lack effective treatments for these important brain disorders.

CRISPR/Cas9,  Non-human primates,  Neurodegenerative diseases,  Animal model

There are a number of excellent reviews covering different types of neurodegenerative diseases and their genetic mouse models [812]. Investigations of different mouse models of neurodegenerative diseases have revealed a common pathology shared by these diseases. First, the development of neuropathology and neurological symptoms in genetic mouse models of neurodegenerative diseases is age dependent and progressive. Second, all the mouse models show an accumulation of misfolded or aggregated proteins resulting from the expression of mutant genes. Third, despite the widespread expression of mutant proteins throughout the body and brain, neuronal function appears to be selectively or preferentially affected. All these facts indicate that mouse models of neurodegenerative diseases recapitulate important pathologic features also seen in patients with neurodegenerative diseases.

However, it seems that mouse models can not recapitulate the full range of neuropathology seen in patients with neurodegenerative diseases. Overt neurodegeneration, which is the most important pathological feature in patient brains, is absent in genetic rodent models of AD, PD, and HD. Many rodent models that express transgenic mutant proteins under the control of different promoters do not replicate overt neurodegeneration, which is likely due to their short life spans and the different aging processes of small animals. Also important are the remarkable differences in brain development between rodents and primates. For example, the mouse brain takes 21 days to fully develop, whereas the formation of primate brains requires more than 150 days [13]. The rapid development of the brain in rodents may render neuronal cells resistant to misfolded protein-mediated neurodegeneration. Another difficulty in using rodent models is how to analyze cognitive and emotional abnormalities, which are the early symptoms of most neurodegenerative diseases in humans. Differences in neuronal circuitry, anatomy, and physiology between rodent and primate brains may also account for the behavioral differences between rodent and primate models.

 

Mitochondrial dynamics–fusion, fission, movement, and mitophagy–in neurodegenerative diseases

Hsiuchen Chen and David C. Chan
Human Molec Gen 2009; 18, Review Issue 2 R169–R176
http://dx.doi.org:/10.1093/hmg/ddp326

Neurons are metabolically active cells with high energy demands at locations distant from the cell body. As a result, these cells are particularly dependent on mitochondrial function, as reflected by the observation that diseases of mitochondrial dysfunction often have a neurodegenerative component. Recent discoveries have highlighted that neurons are reliant particularly on the dynamic properties of mitochondria. Mitochondria are dynamic organelles by several criteria. They engage in repeated cycles of fusion and fission, which serve to intermix the lipids and contents of a population of mitochondria. In addition, mitochondria are actively recruited to subcellular sites, such as the axonal and dendritic processes of neurons. Finally, the quality of a mitochondrial population is maintained through mitophagy, a form of autophagy in which defective mitochondria are selectively degraded. We review the general features of mitochondrial dynamics, incorporating recent findings on mitochondrial fusion, fission, transport and mitophagy. Defects in these key features are associated with neurodegenerative disease. Charcot-Marie-Tooth type 2A, a peripheral neuropathy, and dominant optic atrophy, an inherited optic neuropathy, result from a primary deficiency of mitochondrial fusion. Moreover, several major neurodegenerative diseases—including Parkinson’s, Alzheimer’s and Huntington’s disease—involve disruption of mitochondrial dynamics. Remarkably, in several disease models, the manipulation of mitochondrial fusion or fission can partially rescue disease phenotypes. We review how mitochondrial dynamics is altered in these neurodegenerative diseases and discuss the reciprocal interactions between mitochondrial fusion, fission, transport and mitophagy.

 

Applications of CRISPR–Cas systems in Neuroscience

Matthias Heidenreich  & Feng Zhang
Nature Rev Neurosci 2016; 17:36–44   http://dx.doi.org:/10.1038/nrn.2015.2

Genome-editing tools, and in particular those based on CRISPR–Cas (clustered regularly interspaced short palindromic repeat (CRISPR)–CRISPR-associated protein) systems, are accelerating the pace of biological research and enabling targeted genetic interrogation in almost any organism and cell type. These tools have opened the door to the development of new model systems for studying the complexity of the nervous system, including animal models and stem cell-derived in vitro models. Precise and efficient gene editing using CRISPR–Cas systems has the potential to advance both basic and translational neuroscience research.
Cellular neuroscience
, DNA recombination, Genetic engineering, Molecular neuroscience

Figure 3: In vitro applications of Cas9 in human iPSCs.close

http://www.nature.com/nrn/journal/v17/n1/carousel/nrn.2015.2-f3.jpg

a | Evaluation of disease candidate genes from large-population genome-wide association studies (GWASs). Human primary cells, such as neurons, are not easily available and are difficult to expand in culture. By contrast, induced pluripo…

  1. Genome-editing Technologies for Gene and Cell Therapy

Molecular Therapy 12 Jan 2016

  1. Systematic quantification of HDR and NHEJ reveals effects of locus, nuclease, and cell type on genome-editing

Scientific Reports 31 Mar 2016

  1. Controlled delivery of β-globin-targeting TALENs and CRISPR/Cas9 into mammalian cells for genome editing using microinjection

Scientific Reports 12 Nov 2015

 

Alzheimer’s Disease: Medicine’s Greatest Challenge in the 21st Century

https://www.physicsforums.com/insights/can-gene-editing-eliminate-alzheimers-disease/

The development of the CRISPR/Cas9 system has made gene editing a relatively simple task.  While CRISPR and other gene editing technologies stand to revolutionize biomedical research and offers many promising therapeutic avenues (such as in the treatment of HIV), a great deal of debate exists over whether CRISPR should be used to modify human embryos. As I discussed in my previous Insight article, we lack enough fundamental biological knowledge to enhance many traits like height or intelligence, so we are not near a future with genetically-enhanced super babies. However, scientists have identified a few rare genetic variants that protect against disease.  One such protective variant is a mutation in the APP gene that protects against Alzheimer’s disease and cognitive decline in old age. If we can perfect gene editing technologies, is this mutation one that we should be regularly introducing into embryos? In this article, I explore the potential for using gene editing as a way to prevent Alzheimer’s disease in future generations. Alzheimer’s Disease: Medicine’s Greatest Challenge in the 21st Century Can gene editing be the missing piece in the battle against Alzheimer’s? (Source: bostonbiotech.org) I chose to assess the benefit of germline gene editing in the context of Alzheimer’s disease because this disease is one of the biggest challenges medicine faces in the 21st century. Alzheimer’s disease is a chronic neurodegenerative disease responsible for the majority of the cases of dementia in the elderly. The disease symptoms begins with short term memory loss and causes more severe symptoms – problems with language, disorientation, mood swings, behavioral issues – as it progresses, eventually leading to the loss of bodily functions and death. Because of the dementia the disease causes, Alzheimer’s patients require a great deal of care, and the world spends ~1% of its total GDP on caring for those with Alzheimer’s and related disorders. Because the prevalence of the disease increases with age, the situation will worsen as life expectancies around the globe increase: worldwide cases of Alzheimer’s are expected to grow from 35 million today to over 115 million by 2050.

Despite much research, the exact causes of Alzheimer’s disease remains poorly understood. The disease seems to be related to the accumulation of plaques made of amyloid-β peptides that form on the outside of neurons, as well as the formation of tangles of the protein tau inside of neurons. Although many efforts have been made to target amyloid-β or the enzymes involved in its formation, we have so far been unsuccessful at finding any treatment that stops the disease or reverses its progress. Some researchers believe that most attempts at treating Alzheimer’s have failed because, by the time a patient shows symptoms, the disease has already progressed past the point of no return.

While research towards a cure continues, researchers have sought effective ways to prevent Alzheimer’s disease. Although some studies show that mental and physical exercise may lower ones risk of Alzheimer’s disease, approximately 60-80% of the risk for Alzheimer’s disease appears to be genetic. Thus, if we’re serious about prevention, we may have to act at the genetic level. And because the brain is difficult to access surgically for gene therapy in adults, this means using gene editing on embryos.

Reference https://www.physicsforums.com/insights/can-gene-editing-eliminate-alzheimers-disease/

 

Utilising CRISPR to Generate Predictive Disease Models: a Case Study in Neurodegenerative Disorders


Dr. Bhuvaneish.T. Selvaraj  – Scottish Centre for Regenerative Medicine

http://www.crisprsummit.com/utilising-crispr-to-generate-predictive-disease-models-a-case-study-in-neurodegenerative-disorders

  • Introducing the latest developments in predictive model generation
  • Discover how CRISPR is being used to develop disease models to study and treat neurodegenerative disorders
  • In depth Q&A session to answer your most pressing questions

 

Turning On Genes, Systematically, with CRISPR/Cas9

http://www.genengnews.com/gen-news-highlights/turning-on-genes-systematically-with-crispr-cas9/81250697/

 

Scientists based at MIT assert that they can reliably turn on any gene of their choosing in living cells. [Feng Zhang and Steve Dixon]  http://www.genengnews.com/media/images/GENHighlight/Dec12_2014_CRISPRCas9GeneActivationSystem7838101231.jpg

With the latest CRISPR/Cas9 advance, the exhortation “turn on, tune in, drop out” comes to mind. The CRISPR/Cas9 gene-editing system was already a well-known means of “tuning in” (inserting new genes) and “dropping out” (knocking out genes). But when it came to “turning on” genes, CRISPR/Cas9 had little potency. That is, it had demonstrated only limited success as a way to activate specific genes.

A new CRISPR/Cas9 approach, however, appears capable of activating genes more effectively than older approaches. The new approach may allow scientists to more easily determine the function of individual genes, according to Feng Zhang, Ph.D., a researcher at MIT and the Broad Institute. Dr. Zhang and colleagues report that the new approach permits multiplexed gene activation and rapid, large-scale studies of gene function.

The new technique was introduced in the December 10 online edition of Nature, in an article entitled, “Genome-scale transcriptional activation by an engineered CRISPR-Cas9 complex.” The article describes how Dr. Zhang, along with the University of Tokyo’s Osamu Nureki, Ph.D., and Hiroshi Nishimasu, Ph.D., overhauled the CRISPR/Cas9 system. The research team based their work on their analysis (published earlier this year) of the structure formed when Cas9 binds to the guide RNA and its target DNA. Specifically, the team used the structure’s 3D shape to rationally improve the system.

In previous efforts to revamp CRISPR/Cas9 for gene activation purposes, scientists had tried to attach the activation domains to either end of the Cas9 protein, with limited success. From their structural studies, the MIT team realized that two small loops of the RNA guide poke out from the Cas9 complex and could be better points of attachment because they allow the activation domains to have more flexibility in recruiting transcription machinery.

Using their revamped system, the researchers activated about a dozen genes that had proven difficult or impossible to turn on using the previous generation of Cas9 activators. Each gene showed at least a twofold boost in transcription, and for many genes, the researchers found multiple orders of magnitude increase in activation.

After investigating single-guide RNA targeting rules for effective transcriptional activation, demonstrating multiplexed activation of 10 genes simultaneously, and upregulating long intergenic noncoding RNA transcripts, the research team decided to undertake a large-scale screen. This screen was designed to identify genes that confer resistance to a melanoma drug called PLX-4720.

“We … synthesized a library consisting of 70,290 guides targeting all human RefSeq coding isoforms to screen for genes that, upon activation, confer resistance to a BRAF inhibitor,” wrote the authors of the Nature paper. “The top hits included genes previously shown to be able to confer resistance, and novel candidates were validated using individual [single-guide RNA] and complementary DNA overexpression.”

A gene signature based on the top screening hits, the authors added, correlated with a gene expression signature of BRAF inhibitor resistance in cell lines and patient-derived samples. It was also suggested that large-scale screens such as the one demonstrated in the current study could help researchers discover new cancer drugs that prevent tumors from becoming resistant.

More at –  http://www.genengnews.com/gen-news-highlights/turning-on-genes-systematically-with-crispr-cas9/81250697/

 

Susceptibility and modifier genes in Portuguese transthyretin V30M amyloid polyneuropathy: complexity in a single-gene disease
Miguel L. Soares1,2, Teresa Coelho3,6, Alda Sousa4,5, …, Maria Joa˜o Saraiva2,5 and Joel N. Buxbaum1
Human Molec Gen 2005; 14(4): 543–553   http://dx.doi.org:/10.1093/hmg/ddi051
https://www.researchgate.net/profile/Isabel_Conceicao/publication/8081351_Susceptibility_and_modifier_genes_in_Portuguese_transthyretin_V30M_amyloid_polyneuropathy_complexity_in_a_single-gene_disease/links/53e123d70cf2235f352733b3.pdf

Familial amyloid polyneuropathy type I is an autosomal dominant disorder caused by mutations in the transthyretin (TTR ) gene; however, carriers of the same mutation exhibit variability in penetrance and clinical expression. We analyzed alleles of candidate genes encoding non-fibrillar components of TTR amyloid deposits and a molecule metabolically interacting with TTR [retinol-binding protein (RBP)], for possible associations with age of disease onset and/or susceptibility in a Portuguese population sample with the TTR V30M mutation and unrelated controls. We show that the V30M carriers represent a distinct subset of the Portuguese population. Estimates of genetic distance indicated that the controls and the classical onset group were furthest apart, whereas the late-onset group appeared to differ from both. Importantly, the data also indicate that genetic interactions among the multiple loci evaluated, rather than single-locus effects, are more likely to determine differences in the age of disease onset. Multifactor dimensionality reduction indicated that the best genetic model for classical onset group versus controls involved the APCS gene, whereas for late-onset cases, one APCS variant (APCSv1) and two RBP variants (RBPv1 and RBPv2) are involved. Thus, although the TTR V30M mutation is required for the disease in Portuguese patients, different genetic factors may govern the age of onset, as well as the occurrence of anticipation.

Autosomal dominant disorders may vary in expression even within a given kindred. The basis of this variability is uncertain and can be attributed to epigenetic factors, environment or epistasis. We have studied familial amyloid polyneuropathy (FAP), an autosomal dominant disorder characterized by peripheral sensorimotor and autonomic neuropathy. It exhibits variation in cardiac, renal, gastrointestinal and ocular involvement, as well as age of onset. Over 80 missense mutations in the transthyretin gene (TTR ) result in autosomal dominant disease http://www.ibmc.up.pt/~mjsaraiv/ttrmut.html). The presence of deposits consisting entirely of wild-type TTR molecules in the hearts of 10– 25% of individuals over age 80 reveals its inherent in vivo amyloidogenic potential (1).

FAP was initially described in Portuguese (2) where, until recently, the TTR V30M has been the only pathogenic mutation associated with the disease (3,4). Later reports identified the same mutation in Swedish and Japanese families (5,6). The disorder has since been recognized in other European countries and in North American kindreds in association with V30M, as well as other mutations (7).

TTR V30M produces disease in only 5–10% of Swedish carriers of the allele (8), a much lower degree of penetrance than that seen in Portuguese (80%) (9) or in Japanese with the same mutation. The actual penetrance in Japanese carriers has not been formally established, but appears to resemble that seen in Portuguese. Portuguese and Japanese carriers show considerable variation in the age of clinical onset (10,11). In both populations, the first symptoms had originally been described as typically occurring before age 40 (so-called ‘classical’ or early-onset); however, in recent years, more individuals developing symptoms late in life have been identified (11,12). Hence, present data indicate that the distribution of the age of onset in Portuguese is continuous, but asymmetric with a mean around age 35 and a long tail into the older age group (Fig. 1) (9,13). Further, DNA testing in Portugal has identified asymptomatic carriers over age 70 belonging to a subset of very late-onset kindreds in whose descendants genetic anticipation is frequent. The molecular basis of anticipation in FAP, which is not mediated by trinucleotide repeat expansions in the TTR or any other gene (14), remains elusive.

Variation in penetrance, age of onset and clinical features are hallmarks of many autosomal dominant disorders including the human TTR amyloidoses (7). Some of these clearly reflect specific biological effects of a particular mutation or a class of mutants. However, when such phenotypic variability is seen with a single mutation in the gene encoding the same protein, it suggests an effect of modifying genetic loci and/or environmental factors contributing differentially to the course of disease. We have chosen to examine age of onset as an example of a discrete phenotypic variation in the presence of the particular autosomal dominant disease-associated mutation TTR V30M. Although the role of environmental factors cannot be excluded, the existence of modifier genes involved in TTR amyloidogenesis is an attractive hypothesis to explain the phenotypic variability in FAP. ….

ATTR (TTR amyloid), like all amyloid deposits, contains several molecular components, in addition to the quantitatively dominant fibril-forming amyloid protein, including heparan sulfate proteoglycan 2 (HSPG2 or perlecan), SAP, a plasma glycoprotein of the pentraxin family (encoded by the APCS gene) that undergoes specific calcium-dependent binding to all types of amyloid fibrils, and apolipoprotein E (ApoE), also found in all amyloid deposits (15). The ApoE4 isoform is associated with an increased frequency and earlier onset of Alzheimer’s disease (Ab), the most common form of brain amyloid, whereas the ApoE2 isoform appears to be protective (16). ApoE variants could exert a similar modulatory effect in the onset of FAP, although early studies on a limited number of patients suggested this was not the case (17).

In at least one instance of senile systemic amyloidosis, small amounts of AA-related material were found in TTR deposits (18). These could reflect either a passive co-aggregation or a contributory involvement of protein AA, encoded by the serum amyloid A (SAA ) genes and the main component of secondary (reactive) amyloid fibrils, in the formation of ATTR.

Retinol-binding protein (RBP), the serum carrier of vitamin A, circulates in plasma bound to TTR. Vitamin A-loaded RBP and L-thyroxine, the two natural ligands of TTR, can act alone or synergistically to inhibit the rate and extent of TTR fibrillogenesis in vitro, suggesting that RBP may influence the course of FAP pathology in vivo (19). We have analyzed coding and non-coding sequence polymorphisms in the RBP4 (serum RBP, 10q24), HSPG2 (1p36.1), APCS (1q22), APOE (19q13.2), SAA1 and SAA2 (11p15.1) genes with the goal of identifying chromosomes carrying common and functionally significant variants. At the time these studies were performed, the full human genome sequence was not completed and systematic singlenucleotide polymorphism (SNP) analyses were not available for any of the suspected candidate genes. We identified new SNPs in APCS and RBP4 and utilized polymorphisms in SAA, HSPG2 and APOE that had already been characterized and shown to have potential pathophysiologic significance in other disorders (16,20–22). The genotyping data were analyzed for association with the presence of the V30M amyloidogenic allele (FAP patients versus controls) and with the age of onset (classical- versus late-onset patients). Multilocus analyses were also performed to examine the effects of simultaneous contributions of the six loci for determining the onset of the first symptoms.  …..

The potential for different underlying models for classical and late onset is supported by the MDR analysis, which produces two distinct models when comparing each class with the controls. One could view the two onset classes as unique diseases. If this is the case, then the failure to detect a single predictive genetic model is consistent with two related, but different, diseases. This is exactly what would be expected in such a case of genetic heterogeneity (28). Using this approach, a major gene effect can be viewed as a necessary, but not sufficient, condition to explain the course of the disease. Analyzing the cases but omitting from the analysis of phenotype the necessary allele, in this case TTR V30M, can then reveal a variety of important modifiers that are distinct between the phenotypes.

The significant comparisons obtained in our study cohort indicate that the combined effects mainly result from two and three-locus interactions involving all loci except SAA1 and SAA2 for susceptibility to disease. A considerable number of four-site combinations modulate the age of onset with SAA1 appearing in a majority of significant combinations in late-onset disease, perhaps indicating a greater role of the SAA variants in the age of onset of FAP.

The correlation between genotype and phenotype in socalled simple Mendelian disorders is often incomplete, as only a subset of all mutations can reliably predict specific phenotypes (34). This is because non-allelic genetic variations and/or environmental influences underlie these disorders whose phenotypes behave as complex traits. A few examples include the identification of the role of homozygozity for the SAA1.1 allele in conferring the genetic susceptibility to renal amyloidosis in FMF (20) and the association of an insertion/deletion polymorphism in the ACE gene with disease severity in familial hypertrophic cardiomyopathy (35). In these disorders, the phenotypes arise from mutations in MEFV and b-MHC, but are modulated by independently inherited genetic variation. In this report, we show that interactions among multiple genes, whose products are confirmed or putative constituents of ATTR deposits, or metabolically interact with TTR, modulate the onset of the first symptoms and predispose individuals to disease in the presence of the V30M mutation in TTR. The exact nature of the effects identified here requires further study with potential application in the development of genetic screening with prognostic value pertaining to the onset of disease in the TTR V30M carriers.

If the effects of additional single or interacting genes dictate the heterogeneity of phenotype, as reflected in variability of onset and clinical expression (with the same TTR mutation), the products encoded by alleles at such loci could contribute to the process of wild-type TTR deposition in elderly individuals without a mutation (senile systemic amyloidosis), a phenomenon not readily recognized as having a genetic basis because of the insensitivity of family history in the elderly.

 

Safety and Efficacy of RNAi Therapy for Transthyretin Amyloidosis

Coelho T, Adams D, Silva A, et al.
N Engl J Med 2013;369:819-29.    http://dx.doi.org:/10.1056/NEJMoa1208760

Transthyretin amyloidosis is caused by the deposition of hepatocyte-derived transthyretin amyloid in peripheral nerves and the heart. A therapeutic approach mediated by RNA interference (RNAi) could reduce the production of transthyretin.

Methods We identified a potent antitransthyretin small interfering RNA, which was encapsulated in two distinct first- and second-generation formulations of lipid nanoparticles, generating ALN-TTR01 and ALN-TTR02, respectively. Each formulation was studied in a single-dose, placebo-controlled phase 1 trial to assess safety and effect on transthyretin levels. We first evaluated ALN-TTR01 (at doses of 0.01 to 1.0 mg per kilogram of body weight) in 32 patients with transthyretin amyloidosis and then evaluated ALN-TTR02 (at doses of 0.01 to 0.5 mg per kilogram) in 17 healthy volunteers.

Results Rapid, dose-dependent, and durable lowering of transthyretin levels was observed in the two trials. At a dose of 1.0 mg per kilogram, ALN-TTR01 suppressed transthyretin, with a mean reduction at day 7 of 38%, as compared with placebo (P=0.01); levels of mutant and nonmutant forms of transthyretin were lowered to a similar extent. For ALN-TTR02, the mean reductions in transthyretin levels at doses of 0.15 to 0.3 mg per kilogram ranged from 82.3 to 86.8%, with reductions of 56.6 to 67.1% at 28 days (P<0.001 for all comparisons). These reductions were shown to be RNAi mediated. Mild-to-moderate infusion-related reactions occurred in 20.8% and 7.7% of participants receiving ALN-TTR01 and ALN-TTR02, respectively.

ALN-TTR01 and ALN-TTR02 suppressed the production of both mutant and nonmutant forms of transthyretin, establishing proof of concept for RNAi therapy targeting messenger RNA transcribed from a disease-causing gene.

 

Alnylam May Seek Approval for TTR Amyloidosis Rx in 2017 as Other Programs Advance


https://www.genomeweb.com/rnai/alnylam-may-seek-approval-ttr-amyloidosis-rx-2017-other-programs-advance

Officials from Alnylam Pharmaceuticals last week provided updates on the two drug candidates from the company’s flagship transthyretin-mediated amyloidosis program, stating that the intravenously delivered agent patisiran is proceeding toward a possible market approval in three years, while a subcutaneously administered version called ALN-TTRsc is poised to enter Phase III testing before the end of the year.

Meanwhile, Alnylam is set to advance a handful of preclinical therapies into human studies in short order, including ones for complement-mediated diseases, hypercholesterolemia, and porphyria.

The officials made their comments during a conference call held to discuss Alnylam’s second-quarter financial results.

ATTR is caused by a mutation in the TTR gene, which normally produces a protein that acts as a carrier for retinol binding protein and is characterized by the accumulation of amyloid deposits in various tissues. Alnylam’s drugs are designed to silence both the mutant and wild-type forms of TTR.

Patisiran, which is delivered using lipid nanoparticles developed by Tekmira Pharmaceuticals, is currently in a Phase III study in patients with a form of ATTR called familial amyloid polyneuropathy (FAP) affecting the peripheral nervous system. Running at over 20 sites in nine countries, that study is set to enroll up to 200 patients and compare treatment to placebo based on improvements in neuropathy symptoms.

According to Alnylam Chief Medical Officer Akshay Vaishnaw, Alnylam expects to have final data from the study in two to three years, which would put patisiran on track for a new drug application filing in 2017.

Meanwhile, ALN-TTRsc, which is under development for a version of ATTR that affects cardiac tissue called familial amyloidotic cardiomyopathy (FAC) and uses Alnylam’s proprietary GalNAc conjugate delivery technology, is set to enter Phase III by year-end as Alnylam holds “active discussions” with US and European regulators on the design of that study, CEO John Maraganore noted during the call.

In the interim, Alnylam continues to enroll patients in a pilot Phase II study of ALN-TTRsc, which is designed to test the drug’s efficacy for FAC or senile systemic amyloidosis (SSA), a condition caused by the idiopathic accumulation of wild-type TTR protein in the heart.

Based on “encouraging” data thus far, Vaishnaw said that Alnylam has upped the expected enrollment in this study to 25 patients from 15. Available data from the trial is slated for release in November, he noted, stressing that “any clinical endpoint result needs to be considered exploratory given the small sample size and the very limited duration of treatment of only six weeks” in the trial.

Vaishnaw added that an open-label extension (OLE) study for patients in the ALN-TTRsc study will kick off in the coming weeks, allowing the company to gather long-term dosing tolerability and clinical activity data on the drug.

Enrollment in an OLE study of patisiran has been completed with 27 patients, he said, and, “as of today, with up to nine months of therapy … there have been no study drug discontinuations.” Clinical endpoint data from approximately 20 patients in this study will be presented at the American Neurological Association meeting in October.

As part of its ATTR efforts, Alnylam has also been conducting natural history of disease studies in both FAP and FAC patients. Data from the 283-patient FAP study was presented earlier this year and showed a rapid progression in neuropathy impairment scores and a high correlation of this measurement with disease severity.

During last week’s conference call, Vaishnaw said that clinical endpoint and biomarker data on about 400 patients with either FAC or SSA have already been collected in a nature history study on cardiac ATTR. Maraganore said that these findings would likely be released sometime next year.

Alnylam Presents New Phase II, Preclinical Data from TTR Amyloidosis Programs
https://www.genomeweb.com/rnai/alnylam-presents-new-phase-ii-preclinical-data-ttr-amyloidosis-programs

 

Amyloid disease drug approved

Nature Biotechnology 2012; (3http://dx.doi.org:/10.1038/nbt0212-121b

The first medication for a rare and often fatal protein misfolding disorder has been approved in Europe. On November 16, the E gave a green light to Pfizer’s Vyndaqel (tafamidis) for treating transthyretin amyloidosis in adult patients with stage 1 polyneuropathy symptoms. [Jeffery Kelly, La Jolla]

 

Safety and Efficacy of RNAi Therapy for Transthyretin …

http://www.nejm.org/…/NEJMoa1208760?&#8230;

The New England Journal of Medicine

Aug 29, 2013 – Transthyretin amyloidosis is caused by the deposition of hepatocyte-derived transthyretin amyloid in peripheral nerves and the heart.

 

Alnylam’s RNAi therapy targets amyloid disease

Ken Garber
Nature Biotechnology 2015; 33(577)    http://dx.doi.org:/10.1038/nbt0615-577a

RNA interference’s silencing of target genes could result in potent therapeutics.

http://www.nature.com/nbt/journal/v33/n6/images/nbt0615-577a-I1.jpg

The most clinically advanced RNA interference (RNAi) therapeutic achieved a milestone in April when Alnylam Pharmaceuticals in Cambridge, Massachusetts, reported positive results for patisiran, a small interfering RNA (siRNA) oligonucleotide targeting transthyretin for treating familial amyloidotic polyneuropathy (FAP).  …

  1. Analysis of 589,306 genomes identifies individuals resilient to severe Mendelian childhood diseases

Nature Biotechnology 11 April 2016

  1. CRISPR-Cas systems for editing, regulating and targeting genomes

Nature Biotechnology 02 March 2014

  1. Near-optimal probabilistic RNA-seq quantification

Nature Biotechnology 04 April 2016

 

Translational Neuroscience: Toward New Therapies

https://books.google.com/books?isbn=0262029863

Karoly Nikolich, ‎Steven E. Hyman – 2015 – ‎Medical

Tafamidis for Transthyretin Familial Amyloid Polyneuropathy: A Randomized, Controlled Trial. … Multiplex Genome Engineering Using CRISPR/Cas Systems.

 

Is CRISPR a Solution to Familial Amyloid Polyneuropathy?

Author and Curator: Larry H. Bernstein, MD, FCAP

Originally published as

https://pharmaceuticalintelligence.com/2016/04/13/is-crispr-a-solution-to-familial-amyloid-polyneuropathy/

 

http://scholar.aci.info/view/1492518a054469f0388/15411079e5a00014c3d

FAP is characterized by the systemic deposition of amyloidogenic variants of the transthyretin protein, especially in the peripheral nervous system, causing a progressive sensory and motor polyneuropathy.

FAP is caused by a mutation of the TTR gene, located on human chromosome 18q12.1-11.2.[5] A replacement of valine by methionine at position 30 (TTR V30M) is the mutation most commonly found in FAP.[1] The variant TTR is mostly produced by the liver.[citation needed] The transthyretin protein is a tetramer.    ….

 

 

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Glycobiology advances

Larry H. Bernstein, MD, FCAP, Curator

LPBI

 

The Evolution of the Glycobiology Space

The Nascent Stage of another Omics Field with Biomarker and Therapeutic Potential

Enal Razvi, Ph.D. , Gary Oosta, Ph.D

http://www.genengnews.com/insight-and-intelligence/the-evolution-of-the-glycobiology-space/77900638/

 

The Evolution of the Glycobiology Space

 

Glycobiology is an important field of study with medical applications because it is known that tumor cells alter their glycosylation pattern, which may contribute to their metastatic potential as well as potential immune evasion. [iStock/© vjanez]    http://www.genengnews.com/media/images/AnalysisAndInsight/Apr12_2016_iStock_41612310_PlasmaMembraneOfACell1211657142.jpg

There is growing interest in the field of glycobiology given the fact that epitopes with physiological and pathological relevance have glyco moieties.  We believe that another “omics” revolution is on the horizon—the study of the glyco modifications on the surface of cells and their potential as biomarkers and therapeutic targets in many disease classes. Not much industry tracking of this field has taken place. Thus, we sought to map this landscape by examining the entire ensemble of academic publications in this space and teasing apart the trends operative in this field from a qualitative and quantitative perspective. We believe that this methodology of en masse capture and publication and annotation provides an effective approach to evaluate this early-stage field.

Identifiation and Growth of Glycobiology Publications

http://www.genengnews.com/Media/images/AnalysisAndInsight/thumb_April12_2016_SelectBiosciences_Figure11935315421.jpg

For this article, we identified 7000 publications in the broader glycobiology space and analyzed them in detail.  It is important to frame glycobiology in the context of genomics and proteomics as a means to assess the scale of the field. Figure 1 presents the relative sizes of these fields as assessed by publications in from 1975 to 2015.

Note that the relative scale of genomics versus proteomics and glycobiology/glycomics in this graph strongly suggests that glycobiology is a nascent space, and thus a driver for us to map its landscape today and as it evolves over the coming years.

Figure 2. (A) Segmentation of the glycobiology landscape. (B) Glycobiology versus glycomics publication growth.

 

http://www.genengnews.com/Media/images/AnalysisAndInsight/thumb_April12_2016_SelectBiosciences_Figure2ab1917013624.jpg

To examine closely the various components of the glycobiology space, we segmented the publications database, presented in Figure 2A. Note the relative sizes and growth rates (slopes) of the various segments.

Clearly, glycoconjugates currently are the majority of this space and account for the bulk of the publications.  Glycobiology and glycomics are small but expanding and therefore can be characterized as “nascent market segments.”  These two spaces are characterized in more detail in Figure 2B, which presents their publication growth rates.

Note the very recent increased attention directed at these spaces and hence our drive to initiate industry coverage of these spaces. Figure 2B presents the overall growth and timeline of expansion of these fields—especially glycobiology—but it provides no information about the qualitative nature of these fields.

Focus of Glycobiology Publications

http://www.genengnews.com/Media/images/AnalysisAndInsight/April12_2016_SelectBiosciences_Figure2c1827601892.jpg

Figure 2C. Word cloud based on titles of publications in the glycobiology and glycomics spaces.

To understand the focus of publications in this field, and indeed the nature of this field, we constructed a word cloud based on titles of the publications that comprise this space presented in Figure 2C.

There is a marked emphasis on terms such as oligosaccharides and an emphasis on cells (this is after all glycosylation on the surface of cells). Overall, a pictorial representation of the types and classes of modifications that comprise this field emerge in this word cloud, demonstrating the expansion of the glycobiology and to a lesser extent the glycomics spaces as well as the character of these nascent but expanding spaces.

Characterization of the Glycobiology Space in Journals

Figure 3A. Breakout of publications in the glycobiology/glycomics fields.   http://www.genengnews.com/Media/images/AnalysisAndInsight/April12_2016_SelectBiosciences_Figure3a_5002432117316.jpg
Having framed the overall growth of the glycobiology field, we wanted to understand its structure and the classes of researchers as well as publications that comprise this field. To do this, we segmented the publications that constitute this field into the various journals in which glycobiology research is published. Figure 3A presents the breakout of publications by journal to illustrate the “scope” of this field.

The distribution of glycobiology publications across the various journals suggests a very concentrated marketplace that is very technically focused. The majority of the publications segregate into specialized journals on this topic, a pattern very indicative of a field in the very early stages of development—a truly nascent marketplace.

http://www.genengnews.com/Media/images/AnalysisAndInsight/thumb_April12_2016_SelectBiosciences_Figure3b1012091061.jpg

Figure 3B. Origin of publications in the glycobiology/glycomics fields.
We also sought to understand the “origin” of these publications—the breakout between academic- versus industry-derived journals. Figure 3B presents this breakout and shows that these publications are overwhelmingly (92.3%) derived from the academic sector. This is again a testimonial to the early nascent nature of this marketplace without significant engagement by the commercial sector and therefore is an important field to characterize and track from the ground up.

Select Biosciences, Inc. further analyzed the growth trajectory of the glycobiology papers in Figure 3C as a means to examine closely the publications trajectory. Although there appears to be some wobble along the way, overall the trajectory is upward, and of late it is expanding significantly.

In Summary

Figure 3C. Trajectory of the glycobiology space.   http://www.genengnews.com/Media/images/AnalysisAndInsight/April12_2016_SelectBiosciences_Figure3c1236921793.jpg
Glycobiology is the study of what coats living cells—glycans, or carbohydrates, and glycoconjugates. This is an important field of study with medical applications because it is known that tumor cells alter their glycosylation pattern, which may contribute to their metastatic potential as well as potential immune evasion.

At this point, glycobiology is largely basic research and thus it pales in comparison with the field of genomics. But in 10 years, we predict the study of glycobiology and glycomics will be ubiquitous and in the mainstream.

We started our analysis of this space because we’ve been focusing on many other classes of analytes, such as microRNAs, long-coding RNAs, oncogenes, tumor suppressor genes, etc., whose potential as biomarkers is becoming established. Glycobiology, on the other hand, represents an entire new space—a whole new category of modifications that could be analyzed for diagnostic potential and perhaps also for therapeutic targeting.

Today, glycobiology and glycomics are where genomics was at the start of the Human Genome Project. They respresent a nascent space and with full headroom for growth. Select Biosciences will continue to track this exciting field for research developments as well as development of biomarkers based on glyco-epitopes.

Enal Razvi, Ph.D., conducted his doctoral work on viral immunology and subsequent to receiving his Ph.D. went on to the Rockefeller University in New York to serve as Aaron Diamond Post-doctoral fellow under Professor Ralph Steinman [Nobel Prize Winner in 2011 for his discovery of dendritic cells in the early-70s with Zanvil Cohn]. Subsequently, Dr. Razvi completed his research fellowship at Harvard Medical School. For the last two decades Dr. Razvi has worked with small and large companies and consulted for more than 100 clients worldwide. He currently serves as Biotechnology Analyst and Managing Director of SelectBio U.S. He can be reached at enal@selectbio.us. Gary M. Oosta holds a Ph.D. in Biophysics from Massachusetts Institute of Technology and a B.A. in Chemistry from E. Mich. Univ. He has 25 years of industrial research experience in various technology areas including medical diagnostics, thin-layer coating, bio-effects of electromagnetic radiation, and blood coagulation. Dr. Oosta has authored 20 technical publications and is an inventor on 77 patents worldwide. In addition, he has managed research groups that were responsible for many other patented innovations. Dr. Oosta has a long-standing interest in using patents and publications as strategic technology indicators for future technology selection and new product development. To enjoy more articles like this from GEN, click here to subscribe now!

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3D revolution and tissue repair

Curator: Larry H. Bernstein, MD, FCAP

 

 

Berkeley Lab captures first high-res 3D images of DNA segments

DNA segments are targeted to be building blocks for molecular computer memory and electronic devices, nanoscale drug-delivery systems, and as markers for biological research and imaging disease-relevant proteins

In a Berkeley Lab-led study, flexible double-helix DNA segments (purple, with green DNA models) connected to gold nanoparticles (yellow) are revealed from the 3D density maps reconstructed from individual samples using a Berkeley Lab-developed technique called individual-particle electron tomography (IPET). Projections of the structures are shown in the green background grid. (credit: Berkeley Lab)

An international research team working at the Lawrence Berkeley National Laboratory (Berkeley Lab) has captured the first high-resolution 3D images of double-helix DNA segments attached at either end to gold nanoparticles — which could act as building blocks for molecular computer memory and electronic devices (see World’s smallest electronic diode made from single DNA molecule), nanoscale drug-delivery systems, and as markers for biological research and for imaging disease-relevant proteins.

The researchers connected coiled DNA strands between polygon-shaped gold nanoparticles and then reconstructed 3D images, using a cutting-edge electron microscope technique coupled with a protein-staining process and sophisticated software that provided structural details at the scale of about 2 nanometers.

“We had no idea about what the double-strand DNA would look like between the gold nanoparticles,” said Gang “Gary” Ren, a Berkeley Lab scientist who led the research. “This is the first time for directly visualizing an individual double-strand DNA segment in 3D,” he said.

The results were published in an open-access paper in the March 30 edition of Nature Communications.

The method developed by this team, called individual-particle electron tomography (IPET), had earlier captured the 3-D structure of a single protein that plays a key role in human cholesterol metabolism. By grabbing 2D images of an object from different angles, the technique allows researchers to assemble a 3D image of that object.

The team has also used the technique to uncover the fluctuation of another well-known flexible protein, human immunoglobulin 1, which plays a role in the human immune system.

https://youtu.be/lQrbmg9ry90
Berkeley Lab | 3-D Reconstructions of Double strand DNA and Gold Nanoparticle Structures

For this new study of DNA nanostructures, Ren used an electron-beam study technique called cryo-electron microscopy (cryo-EM) to examine frozen DNA-nanogold samples, and used IPET to reconstruct 3-D images from samples stained with heavy metal salts. The team also used molecular simulation tools to test the natural shape variations (“conformations”) in the samples, and compared these simulated shapes with observations.

First visualization of DNA strand dynamics without distorting x-ray crystallography

Ren explained that the naturally flexible dynamics of samples, like a man waving his arms, cannot be fully detailed by any method that uses an average of many observations.

A popular way to view the nanoscale structural details of delicate biological samples is to form them into crystals and zap them with X-rays, but that destroys their natural shape, especially fir the DNA-nanogold samples in this study, which the scientists say are incredibly challenging to crystallize. Other common research techniques may require a collection of thousands of near-identical objects, viewed with an electron microscope, to compile a single, averaged 3-D structure. But an averaged 3D image may not adequately show the natural shape fluctuations of a given object.

The samples in the latest experiment were formed from individual polygon gold nanostructures, measuring about 5 nanometers across, connected to single DNA-segment strands with 84 base pairs. Base pairs are basic chemical building blocks that give DNA its structure. Each individual DNA segment and gold nanoparticle naturally zipped together with a partner to form the double-stranded DNA segment with a gold particle at either end.

https://youtu.be/RDOpgj62PLU
Berkeley Lab | These views compare the various shape fluctuations obtained from different samples of the same type of double-helix DNA segment (DNA renderings in green, 3D reconstructions in purple) connected to gold nanoparticles (yellow).

The samples were flash-frozen to preserve their structure for study with cryo-EM imaging. The distance between the two gold nanoparticles in individual samples varied from 20 to 30 nanometers, based on different shapes observed in the DNA segments.

Researchers used a cryo-electron microscope at Berkeley Lab’s Molecular Foundry for this study. They collected a series of tilted images of the stained objects, and reconstructed 14 electron-density maps that detailed the structure of individual samples using the IPET technique.

Sub-nanometer images next

Ren said that the next step will be to work to improve the resolution to the sub-nanometer scale.

“Even in this current state we begin to see 3-D structures at 1- to 2-nanometer resolution,” he said. “Through better instrumentation and improved computational algorithms, it would be promising to push the resolution to that visualizing a single DNA helix within an individual protein.”

In future studies, researchers could attempt to improve the imaging resolution for complex structures that incorporate more DNA segments as a sort of “DNA origami,” Ren said. Researchers hope to build and better characterize nanoscale molecular devices using DNA segments that can, for example, store and deliver drugs to targeted areas in the body.

“DNA is easy to program, synthesize and replicate, so it can be used as a special material to quickly self-assemble into nanostructures and to guide the operation of molecular-scale devices,” he said. “Our current study is just a proof of concept for imaging these kinds of molecular devices’ structures.”

The team included researchers at UC Berkeley, the Kavli Energy NanoSciences Institute at Berkeley Lab and UC Berkeley, and Xi’an Jiaotong University in China. This work was supported by the National Science Foundation, DOE Office of Basic Energy Sciences, National Institutes of Health, the National Natural Science Foundation of China, Xi’an Jiaotong University in China, and the Ministry of Science and Technology in China. View more about Gary Ren’s research group here.


Abstract of Three-dimensional structural dynamics and fluctuations of DNA-nanogold conjugates by individual-particle electron tomography

DNA base pairing has been used for many years to direct the arrangement of inorganic nanocrystals into small groupings and arrays with tailored optical and electrical properties. The control of DNA-mediated assembly depends crucially on a better understanding of three-dimensional structure of DNA-nanocrystal-hybridized building blocks. Existing techniques do not allow for structural determination of these flexible and heterogeneous samples. Here we report cryo-electron microscopy and negative-staining electron tomography approaches to image, and three-dimensionally reconstruct a single DNA-nanogold conjugate, an 84-bp double-stranded DNA with two 5-nm nanogold particles for potential substrates in plasmon-coupling experiments. By individual-particle electron tomography reconstruction, we obtain 14 density maps at ~2-nm resolution. Using these maps as constraints, we derive 14 conformations of dsDNA by molecular dynamics simulations. The conformational variation is consistent with that from liquid solution, suggesting that individual-particle electron tomography could be an expected approach to study DNA-assembling and flexible protein structure and dynamics.

 

World’s smallest electronic diode made from single DNA molecule

Electronic components 1,000 times smaller than with silicon may be possible
http://www.kurzweilai.net/worlds-smallest-electronic-diode-made-from-single-dna-molecule
By inserting a small “coralyne” molecule into DNA, scientists were able to create a single-molecule diode (connected here by two gold electrodes), which can be used as an active element in future nanoscale circuits. The diode circuit symbol is shown on the left. (credit: University of Georgia and Ben-Gurion University)

Nanoscale electronic components can be made from single DNA molecules, as researchers at the University of Georgia and at Ben-Gurion University in Israel have demonstrated, using a single molecule of DNA to create the world’s smallest diode.

DNA double helix with base pairs (credit: National Human Genome Research Institute)

A diode is a component vital to electronic devices that allows current to flow in one direction but prevents its flow in the other direction. The development could help stimulate development of DNA components for molecular electronics.

As noted in an open-access Nature Chemistry paper published this week, the researchers designed a 11-base-pair (bp) DNA molecule and inserted a small molecule named coralyne into the DNA.*

They found, surprisingly, that this caused the current flowing through the DNA to be 15 times stronger for negative voltages than for positive voltages, a necessary feature of a diode.

Electronic elements 1,00o times smaller than current components

“Our discovery can lead to progress in the design and construction of nanoscale electronic elements that are at least 1,000 times smaller than current components,” says the study’s lead author, Bingqian Xu an associate professor in the UGA College of Engineering and an adjunct professor in chemistry and physics.

The research team plans to enhance the performance of the molecular diode and construct additional molecular devices, which may include a transistor (similar to a two-layer diode, but with one additional layer).

A theoretical model developed by Yanantan Dubi of Ben-Gurion University indicated the diode-like behavior of DNA originates from the bias voltage-induced breaking of spatial symmetry inside the DNA molecule after the coralyne is inserted.

The research is supported by the National Science Foundation.

*“We prepared the DNA–coralyne complex by specifically intercalating two coralyne molecules into a custom-designed 11-base-pair (bp) DNA molecule (5′-CGCGAAACGCG-3′) containing three mismatched A–A base pairs at the centre,” according to the authors.

UPDATE April 6, 2016 to clarify the coralyne intercalation (insertion) into the DNA molecule.


Abstract of Molecular rectifier composed of DNA with high rectification ratio enabled by intercalation

The predictability, diversity and programmability of DNA make it a leading candidate for the design of functional electronic devices that use single molecules, yet its electron transport properties have not been fully elucidated. This is primarily because of a poor understanding of how the structure of DNA determines its electron transport. Here, we demonstrate a DNA-based molecular rectifier constructed by site-specific intercalation of small molecules (coralyne) into a custom-designed 11-base-pair DNA duplex. Measured current–voltage curves of the DNA–coralyne molecular junction show unexpectedly large rectification with a rectification ratio of about 15 at 1.1 V, a counter-intuitive finding considering the seemingly symmetrical molecular structure of the junction. A non-equilibrium Green’s function-based model—parameterized by density functional theory calculations—revealed that the coralyne-induced spatial asymmetry in the electron state distribution caused the observed rectification. This inherent asymmetry leads to changes in the coupling of the molecular HOMO−1 level to the electrodes when an external voltage is applied, resulting in an asymmetric change in transmission.

 

A stem-cell repair system that can regenerate any kind of human tissue …including disease and aging; human trials next year
http://www.kurzweilai.net/a-stem-cell-repair-system-that-can-regenerate-any-kind-of-human-tissue

http://www.kurzweilai.net/images/spinal_disc_regeneration.jpg

UNSW researchers say the therapy has enormous potential for treating spinal disc injury and joint and muscle degeneration and could also speed up recovery following complex surgeries where bones and joints need to integrate with the body (credit: UNSW TV)

A stem cell therapy system capable of regenerating any human tissue damaged by injury, disease, or aging could be available within a few years, say University of New South Wales (UNSW Australia) researchers.

Their new repair system*, similar to the method used by salamanders to regenerate limbs, could be used to repair everything from spinal discs to bone fractures, and could transform current treatment approaches to regenerative medicine.

The UNSW-led research was published this week in the Proceedings of the National Academy of Sciences journal.

Reprogramming bone and fat cells

The system reprograms bone and fat cells into induced multipotent stem cells (iMS), which can regenerate multiple tissue types and has been successfully demonstrated in mice, according to study lead author, haematologist, and UNSW Associate Professor John Pimanda.

“This technique is a significant advance on many of the current unproven stem cell therapies, which have shown little or no objective evidence they contribute directly to new tissue formation,” Pimanda said. “We have taken bone and fat cells, switched off their memory and converted them into stem cells so they can repair different cell types once they are put back inside the body.”

“We are currently assessing whether adult human fat cells reprogrammed into iMS cells can safely repair damaged tissue in mice, with human trials expected to begin in late 2017.”

http://www.kurzweilai.net/images/UNSW-stem-cell-repair.jpg

Advantages over stem-cell types

There are different types of stem cells including embryonic stem (ES) cells, which during embryonic development generate every type of cell in the human body, and adult stem cells, which are tissue-specific, but don’t regenerate multiple tissue types. Embryonic stem cells cannot be used to treat damaged tissues because of their tumor forming capacity. The other problem when generating stem cells is the requirement to use viruses to transform cells into stem cells, which is clinically unacceptable, the researchers note.

Research shows that up to 20% of spinal implants either don’t heal or there is delayed healing. The rates are higher for smokers, older people and patients with diseases such diabetes or kidney disease.

Human trials are planned next year once the safety and effectiveness of the technique using human cells in mice has been demonstrated.

* The technique involves extracting adult human fat cells and treating them with the compound 5-Azacytidine (AZA), along with platelet-derived growth factor-AB (PDGF-AB) for about two days. The cells are then treated with the growth factor alone for a further two-three weeks.

AZA is known to induce cell plasticity, which is crucial for reprogramming cells. The AZA compound relaxes the hard-wiring of the cell, which is expanded by the growth factor, transforming the bone and fat cells into iMS cells. When the stem cells are inserted into the damaged tissue site, they multiply, promoting growth and healing.

The new technique is similar to salamander limb regeneration, which is also dependent on the plasticity of differentiated cells, which can repair multiple tissue types, depending on which body part needs replacing.

Along with confirming that human adult fat cells reprogrammed into iMS stem cells can safely repair damaged tissue in mice, the researchers said further work is required to establish whether iMS cells remain dormant at the sites of transplantation and retain their capacity to proliferate on demand.

https://youtu.be/zAMCBNujzzw

Abstract of PDGF-AB and 5-Azacytidine induce conversion of somatic cells into tissue-regenerative multipotent stem cells

Current approaches in tissue engineering are geared toward generating tissue-specific stem cells. Given the complexity and heterogeneity of tissues, this approach has its limitations. An alternate approach is to induce terminally differentiated cells to dedifferentiate into multipotent proliferative cells with the capacity to regenerate all components of a damaged tissue, a phenomenon used by salamanders to regenerate limbs. 5-Azacytidine (AZA) is a nucleoside analog that is used to treat preleukemic and leukemic blood disorders. AZA is also known to induce cell plasticity. We hypothesized that AZA-induced cell plasticity occurs via a transient multipotent cell state and that concomitant exposure to a receptive growth factor might result in the expansion of a plastic and proliferative population of cells. To this end, we treated lineage-committed cells with AZA and screened a number of different growth factors with known activity in mesenchyme-derived tissues. Here, we report that transient treatment with AZA in combination with platelet-derived growth factor–AB converts primary somatic cells into tissue-regenerative multipotent stem (iMS) cells. iMS cells possess a distinct transcriptome, are immunosuppressive, and demonstrate long-term self-renewal, serial clonogenicity, and multigerm layer differentiation potential. Importantly, unlike mesenchymal stem cells, iMS cells contribute directly to in vivo tissue regeneration in a context-dependent manner and, unlike embryonic or pluripotent stem cells, do not form teratomas. Taken together, this vector-free method of generating iMS cells from primary terminally differentiated cells has significant scope for application in tissue regeneration.

 

First transistors made entirely of nanocrystal ‘inks’ in simplified process

Transistors and other electronic components to be built into flexible or wearable applications; 3D printing planned
http://www.kurzweilai.net/first-transistors-made-entirely-of-nanocrystal-inks
Because this process works at relatively low temperatures, many transistors can be made on a flexible backing at once. (credit: University of Pennsylvania)

University of Pennsylvania engineers have developed a simplified new approach for making transistors by sequentially depositing their components in the form of liquid nanocrystal “inks.” The new process open the door for transistors and other electronic components to be built into flexible or wearable applications. It also avoids the highly complex current process for creating transistors, which requires high-temperature, high-vacuum equipment. Also, the new lower-temperature process is compatible with a wide array of materials and can be applied to larger areas.

Transistors patterned on plastic backing

The researchers’ nanocrystal-based field effect transistors were patterned onto flexible plastic backings using spin coating, but could eventually be constructed by additive manufacturing systems, like 3D printers.

Published in the journal Science,  the study was lead by Cherie Kagan, the Stephen J. Angello Professor in the School of Engineering and Applied Science, and Ji-Hyuk Choi, then a member of her lab, now a senior researcher at the Korea Institute of Geoscience and Mineral Resources. Researchers at Korea University Korea’s Yonsei University were also involved.

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Kagan’s group developed four nanocrystal inks that comprise the transistor, then deposited them on a flexible backing. (credit: University of Pennsylvania)

The researchers began by dispersing a specific type of nanocrystals in a liquid, creating nanocrystal inks. They developed a library of four of these inks: a conductor (silver), an insulator (aluminum oxide), a semiconductor (cadmium selenide), and a conductor combined with a dopant (a mixture of silver and indium). (“Doping” the semiconductor layer of a transistor with impurities controls whether the device creates a positive or negative charge.)

“These materials are colloids just like the ink in your inkjet printer,” Kagan said, “but you can get all the characteristics that you want and expect from the analogous bulk materials, such as whether they’re conductors, semiconductors or insulators.” Although the electrical properties of several of these nanocrystal inks had been independently verified, they had never been combined into full devices. “Our question was whether you could lay them down on a surface in such a way that they work together to form functional transistors.”

Laying down patterns in layers

Such a process entails layering or mixing them in precise patterns.

First, the conductive silver nanocrystal ink was deposited from liquid on a flexible plastic surface that was treated with a photolithographic mask, then rapidly spun to draw it out in an even layer. The mask was then removed to leave the silver ink in the shape of the transistor’s gate electrode.

The researchers followed that layer by spin-coating a layer of the aluminum oxide nanocrystal-based insulator, then a layer of the cadmium selenide nanocrystal-based semiconductor and finally another masked layer for the indium/silver mixture, which forms the transistor’s source and drain electrodes. Upon heating at relatively low temperatures, the indium dopant diffused from those electrodes into the semiconductor component.

“The trick with working with solution-based materials is making sure that, when you add the second layer, it doesn’t wash off the first, and so on,” Kagan said. “We had to treat the surfaces of the nanocrystals, both when they’re first in solution and after they’re deposited, to make sure they have the right electrical properties and that they stick together in the configuration we want.”

Because this entirely ink-based fabrication process works at lower temperatures than existing vacuum-based methods, the researchers were able to make several transistors on the same flexible plastic backing at the same time.

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The inks’ specialized surface chemistry allowed them to stay in configuration without losing their electrical properties. (credit: University of Pennsylvania)

“Making transistors over larger areas and at lower temperatures have been goals for an emerging class of technologies, when people think of the Internet of things, large area flexible electronics and wearable devices,” Kagan said. “We haven’t developed all of the necessary aspects so they could be printed yet, but because these materials are all solution-based, it demonstrates the promise of this materials class and sets the stage for additive manufacturing.”

Because this entirely ink-based fabrication process works at lower temperatures than existing vacuum-based methods, the researchers were able to make several transistors on the same flexible plastic backing at the same time.

3D-printing transistors for wearables

“This is the first work,” Choi said, “showing that all the components, the metallic, insulating, and semiconducting layers of the transistors, and even the doping of the semiconductor, could be made from nanocrystals.”

“Making transistors over larger areas and at lower temperatures have been goals for an emerging class of technologies, when people think of the Internet of things, large area flexible electronics and wearable devices,” Kagan said. “We haven’t developed all of the necessary aspects so they could be printed yet, but because these materials are all solution-based, it demonstrates the promise of this materials class and sets the stage for additive manufacturing.”

The research was supported by the National Science Foundation, the U.S. Department of Energy, the Office of Naval Research, and the Korea Institute of Geoscience and Mineral Resources funded by the Ministry of Science, ICT, and Future Planning of Korea.


Abstract of Exploiting the colloidal nanocrystal library to construct electronic devices

Synthetic methods produce libraries of colloidal nanocrystals with tunable physical properties by tailoring the nanocrystal size, shape, and composition. Here, we exploit colloidal nanocrystal diversity and design the materials, interfaces, and processes to construct all-nanocrystal electronic devices using solution-based processes. Metallic silver and semiconducting cadmium selenide nanocrystals are deposited to form high-conductivity and high-mobility thin-film electrodes and channel layers of field-effect transistors. Insulating aluminum oxide nanocrystals are assembled layer by layer with polyelectrolytes to form high–dielectric constant gate insulator layers for low-voltage device operation. Metallic indium nanocrystals are codispersed with silver nanocrystals to integrate an indium supply in the deposited electrodes that serves to passivate and dope the cadmium selenide nanocrystal channel layer. We fabricate all-nanocrystal field-effect transistors on flexible plastics with electron mobilities of 21.7 square centimeters per volt-second.

Best textile manufacturing methods for creating human tissues with stem cells
Bioengineers determine three best processes for engineering tissues needed for organ and tissue repair
http://www.kurzweilai.net/best-textile-manufacturing-methods-for-creating-human-tissues-with-stem-cells
All four textile manufacturing processes and corresponding scaffold (structure) types studied exhibited the presence of lipid vacuoles (small red spheres, right column, indicating stem cells undergoing random differentiation), compared to control (left). Electrospun scaffolds (row a) exhibited only a monolayer of lipid vacuoles in a single focal plane, while meltblown, spunbond, and carded scaffolds (rows b, c, d) exhibited vacuoles in multiple planes throughout the fabric thickness. Scale bars: 100 μm (credit: S. A. Tuin et al./Biomedical Materials)

Elizabeth Loboa, dean of the Missouri University College of Engineering, and her team have tested new tissue- engineering methods (based on textile manufacturing) to find ones that are most cost-effective and can be produced in larger quantities.

Tissue engineering is a process that uses novel biomaterials seeded with stem cells to grow and replace missing tissues. When certain types of materials are used, the “scaffolds” that are created to hold stem cells eventually degrade, leaving natural tissue in its place. The new tissues could help patients suffering from wounds caused by diabetes and circulation disorders, patients in need of cartilage or bone repair, and women who have had mastectomies by replacing their breast tissue. The challenge is creating enough of the material on a scale that clinicians need to treat patients.

Comparing textile manufacturing techniques

http://www.kurzweilai.net/images/electrospinning.png

Electrospinning experiment: nanofibers are collected into an ethanol bath and removed at predefined time intervals (credit: J. M. Coburn et al./The Johns Hopkins University/PNAS)

In typical tissue engineering approaches that use fibers as scaffolds, non-woven materials are often bonded together using an electrostatic field. This process, called electrospinning (see Nanoscale scaffolds and stem cells show promise in cartilage repair and Improved artificial blood vessels), creates the scaffolds needed to attach to stem cells.

However, large-scale production with electrospinning is not cost-effective. “Electrospinning produces weak fibers, scaffolds that are not consistent, and pores that are too small,” Loboa said. “The goal of ‘scaling up’ is to produce hundreds of meters of material that look the same, have the same properties, and can be used in clinical settings. So we investigated the processes that create textiles, such as clothing and window furnishings like drapery, to scale up the manufacturing process.”

The group published two papers using three industry-standard, high-throughput manufacturing techniques — meltblowing, spunbonding, and carding — to determine if they would create the materials needed to mimic native tissue.

Meltblowing is a technique during which nonwoven materials are created using a molten polymer to create continuous fibers. Spunbond materials are made much the same way but the fibers are drawn into a web while in a solid state instead of a molten one. Carding involves the separation of fibers through the use of rollers, forming the web needed to hold stem cells in place.

http://www.kurzweilai.net/images/carded-scaffold-fabrication.jpg

Schematic of gilled fiber multifilament spinning and carded scaffold fabrication (credit: Stephen A. Tuin et al./Acta Biomaterialia)

Cost-effective methods

Loboa and her colleagues tested these techniques to create polylactic acid (PLA) scaffolds (a Food and Drug Administration-approved material used as collagen fillers), seeded with human stem cells. They then spent three weeks studying whether the stem cells remained healthy and if they began to differentiate into fat and bone pathways, which is the goal of using stem cells in a clinical setting when new bone and/or new fat tissue is needed at a defect site. Results showed that the three textile manufacturing methods proved as viable if not more so than electrospinning.

“These alternative methods are more cost-effective than electrospinning,” Loboa said. “A small sample of electrospun material could cost between $2 to $5. The cost for the three manufacturing methods is between $.30 to $3.00; these methods proved to be effective and efficient. Next steps include testing how the different scaffolds created in the three methods perform once implanted in animals.”

Researchers at North Carolina State University and the University of North Carolina at Chapel Hill were also involved in the two studies, which were published in Biomedical Materials (open access) and Acta Biomaterialia. The National Science Foundation, the National Institutes of Health, and the Nonwovens Institute provided funding for the studies.


Abstract of Creating tissues from textiles: scalable nonwoven manufacturing techniques for fabrication of tissue engineering scaffolds

Electrospun nonwovens have been used extensively for tissue engineering applications due to their inherent similarities with respect to fibre size and morphology to that of native extracellular matrix (ECM). However, fabrication of large scaffold constructs is time consuming, may require harsh organic solvents, and often results in mechanical properties inferior to the tissue being treated. In order to translate nonwoven based tissue engineering scaffold strategies to clinical use, a high throughput, repeatable, scalable, and economic manufacturing process is needed. We suggest that nonwoven industry standard high throughput manufacturing techniques (meltblowing, spunbond, and carding) can meet this need. In this study, meltblown, spunbond and carded poly(lactic acid) (PLA) nonwovens were evaluated as tissue engineering scaffolds using human adipose derived stem cells (hASC) and compared to electrospun nonwovens. Scaffolds were seeded with hASC and viability, proliferation, and differentiation were evaluated over the course of 3 weeks. We found that nonwovens manufactured via these industry standard, commercially relevant manufacturing techniques were capable of supporting hASC attachment, proliferation, and both adipogenic and osteogenic differentiation of hASC, making them promising candidates for commercialization and translation of nonwoven scaffold based tissue engineering strategies.


Abstract of Fabrication of novel high surface area mushroom gilled fibers and their effects on human adipose derived stem cells under pulsatile fluid flow for tissue engineering applications

The fabrication and characterization of novel high surface area hollow gilled fiber tissue engineering scaffolds via industrially relevant, scalable, repeatable, high speed, and economical nonwoven carding technology is described. Scaffolds were validated as tissue engineering scaffolds using human adipose derived stem cells (hASC) exposed to pulsatile fluid flow (PFF). The effects of fiber morphology on the proliferation and viability of hASC, as well as effects of varied magnitudes of shear stress applied via PFF on the expression of the early osteogenic gene marker runt related transcription factor 2 (RUNX2) were evaluated. Gilled fiber scaffolds led to a significant increase in proliferation of hASC after seven days in static culture, and exhibited fewer dead cells compared to pure PLA round fiber controls. Further, hASC-seeded scaffolds exposed to 3 and 6 dyn/cm2 resulted in significantly increased mRNA expression of RUNX2 after one hour of PFF in the absence of soluble osteogenic induction factors. This is the first study to describe a method for the fabrication of high surface area gilled fibers and scaffolds. The scalable manufacturing process and potential fabrication across multiple nonwoven and woven platforms makes them promising candidates for a variety of applications that require high surface area fibrous materials.

Statement of Significance

We report here for the first time the successful fabrication of novel high surface area gilled fiber scaffolds for tissue engineering applications. Gilled fibers led to a significant increase in proliferation of human adipose derived stem cells after one week in culture, and a greater number of viable cells compared to round fiber controls. Further, in the absence of osteogenic induction factors, gilled fibers led to significantly increased mRNA expression of an early marker for osteogenesis after exposure to pulsatile fluid flow. This is the first study to describe gilled fiber fabrication and their potential for tissue engineering applications. The repeatable, industrially scalable, and versatile fabrication process makes them promising candidates for a variety of scaffold-based tissue engineering applications.

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Microbe meets cancer

Larry H. Bernstein, MD, FCAP, Curator

LPBI

 

Microbes Meet Cancer

Understanding cancer’s relationship with the human microbiome could transform immune-modulating therapies.

By Kate Yandell | April 1, 2016  http://www.the-scientist.com/?articles.view/articleNo/45616/title/Microbes-Meet-Cancer

 © ISTOCK.COM/KATEJA_FN; © ISTOCK.COM/FRANK RAMSPOTT  http://www.the-scientist.com/images/April2016/feature1.jpg

In 2013, two independent teams of scientists, one in Maryland and one in France, made a surprising observation: both germ-free mice and mice treated with a heavy dose of antibiotics responded poorly to a variety of cancer therapies typically effective in rodents. The Maryland team, led by Romina Goldszmidand Giorgio Trinchieri of the National Cancer Institute, showed that both an investigational immunotherapy and an approved platinum chemotherapy shrank a variety of implanted tumor types and improved survival to a far greater extent in mice with intact microbiomes.1 The French group, led by INSERM’s Laurence Zitvogel, got similar results when testing the long-standing chemotherapeutic agent cyclophosphamide in cancer-implanted mice, as well as in mice genetically engineered to develop tumors of the lung.2

The findings incited a flurry of research and speculation about how gut microbes contribute to cancer cell death, even in tumors far from the gastrointestinal tract. The most logical link between the microbiome and cancer is the immune system. Resident microbes can either dial up inflammation or tamp it down, and can modulate immune cells’ vigilance for invaders. Not only does the immune system appear to be at the root of how the microbiome interacts with cancer therapies, it also appears to mediate how our bacteria, fungi, and viruses influence cancer development in the first place.

“We clearly see shifts in the [microbial] community that precede development of tumors,” says microbiologist and immunologist Patrick Schloss, who studies the influence of the microbiome on colon cancer at the University of Michigan.

But the relationship between the microbiome and cancer is complex: while some microbes promote cell proliferation, others appear to protect us against cancerous growth. And in some cases, the conditions that spur one cancer may have the opposite effect in another. “It’s become pretty obvious that the commensal microbiota affect inflammation and, through that or through other mechanisms, affect carcinogenesis,” says Trinchieri. “What we really need is to have a much better understanding of which species, which type of bug, is doing what and try to change the balance.”

Gut feeling

In the late 1970s, pathologist J. Robin Warren of Royal Perth Hospital in Western Australia began to notice that curved bacteria often appeared in stomach tissue biopsies taken from patients with chronic gastritis, an inflammation of the stomach lining that often precedes the development of stomach cancer. He and Barry J. Marshall, a trainee in internal medicine at the hospital, speculated that the bacterium, now called Helicobacter pylori, was somehow causing the gastritis.3 So committed was Marshall to demonstrating the microbe’s causal relationship to the inflammatory condition that he had his own stomach biopsied to show that it contained no H. pylori, then infected himself with the bacterium and documented his subsequent experience of gastritis.4 Scientists now accept that H. pylori, a common gut microbe that is present in about 50 percent of the world’s population, is responsible for many cases of gastritis and most stomach ulcers, and is a strong risk factor for stomach cancer.5 Marshall and Warren earned the 2005 Nobel Prize in Physiology or Medicine for their work.

H. pylori may be the most clear-cut example of a gut bacterium that influences cancer development, but it is likely not the only one. Researchers who study cancer in mice have long had anecdotal evidence that shifts in the microbiome influence the development of diverse tumor types. “You have a mouse model of carcinogenesis. It works beautifully,” says Trinchieri. “You move to another institution. It works completely differently,” likely because the animals’ microbiomes vary with environment.

IMMUNE INFLUENCE: In recent years, research has demonstrated that microbes living in and on the mammalian body can affect cancer risk, as well as responses to cancer treatment. Although the details of this microbe-cancer link remain unclear, investigators suspect that the microbiome’s ability to modulate inflammation and train immune cells to react to tumors is to blame.
See full infographic: WEB | PDF
© AL GRANBERG

Around the turn of the 21st century, cancer researchers began to systematically experiment with the rodent microbiome, and soon had several lines of evidence linking certain gut microbes with a mouse’s risk of colon cancer. In 2001, for example, Shoichi Kado of the Yakult Central Institute for Microbiological Research in Japan and colleagues found that a strain of immunocompromised mice rapidly developed colon tumors, but that germ-free versions of these mice did not.6 That same year, an MIT-based group led by the late David Schauer demonstrated that infecting mice with the bacterium Citrobacter rodentium spurred colon tumor development.7 And in 2003, MIT’s Susan Erdman and her colleagues found that they could induce colon cancer in immunocompromised mice by infecting them with Helicobacter hepaticus, a relative of? H. pylori that commonly exists within the murine gut microbiome.8

More recent work has documented a similar link between colon cancer and the gut microbiome in humans. In 2014, a team led by Schloss sequenced 16S rRNA genes isolated from the stool of 90 people, some with colon cancer, some with precancerous adenomas, and still others with no disease.9 The researchers found that the feces of people with cancer tended to have an altered composition of bacteria, with an excess of the common mouth microbes Fusobacterium or Porphyromonas. A few months later, Peer Bork of the European Molecular Biology Laboratory performed metagenomic sequencing of stool samples from 156 people with or without colorectal cancer. Bork and his colleagues found they could predict the presence or absence of cancer using the relative abundance of 22 bacterial species, including Porphyromonas andFusobacterium.10 They could also use the method to predict colorectal cancer with about the same accuracy as a blood test, correctly identifying about 50 percent of cancers while yielding false positives less than 10 percent of the time. When the two tests were combined, they caught more than 70 percent of cancers.

Whether changes in the microbiota in colon cancer patients are harbingers of the disease or a consequence of tumor development remained unclear. “What comes first, the change in the microbiome or tumor development?” asks Schloss. To investigate this question, he and his colleagues treated mice with microbiome-altering antibiotics before administering a carcinogen and an inflammatory agent, then compared the outcomes in those animals and in mice that had received only the carcinogenic and inflammatory treatments, no antibiotics. The antibiotic-treated animals had significantly fewer and smaller colon tumors than the animals with an undisturbed microbiome, suggesting that resident bacteria were in some way promoting cancer development. And when the researchers transferred microbiota from healthy mice to antibiotic-treated or germ-free mice, the animals developed more tumors following carcinogen exposure. Sterile mice that received microbiota from mice already bearing malignancies developed the most tumors of all.11

Most recently, Schloss and his colleagues showed that treating mice with seven unique combinations of antibiotics prior to exposing them to carcinogens yielded variable but predictable levels of tumor formation. The researchers determined that the number of tumors corresponded to the unique ways that each antibiotic cocktail modulated the microbiome.12

“We’ve kind of proven to ourselves, at least, that the microbiome is involved in colon cancer,” says Schloss, who hypothesizes that gut bacteria–driven inflammation is to blame for creating an environment that is hospitable to tumor development and growth. Gain or loss of certain components of the resident bacterial community could lead to the release of reactive oxygen species, damaging cells and their genetic material. Inflammation also involves increased release of growth factors and blood vessel proliferation, potentially supporting the growth of tumors. (See illustration above.)

Recent research has also yielded evidence that the gut microbiota impact the development of cancer in sites far removed from the intestinal tract, likely through similar immune-modulating mechanisms.

Systemic effects

In the mid-2000s, MIT’s Erdman began infecting a strain of mice predisposed to intestinal tumors withH. hepaticus and observing the subsequent development of colon cancer in some of the animals. To her surprise, one of the mice developed a mammary tumor. Then, more of the mice went on to develop mammary tumors. “This told us that something really interesting was going on,” Erdman recalls. Sure enough, she and her colleagues found that mice infected with H. hepaticus were more likely to develop mammary tumors than mice not exposed to the bacterium.13The researchers showed that systemic immune activation and inflammation could contribute to mammary tumors in other, less cancer-prone mouse models, as well as to the development of prostate cancer.

MICROBIAL STOWAWAYS: Bacteria of the human gut microbiome are intimately involved in cancer development and progression, thanks to their interactions with the immune system. Some microbes, such as Helicobacter pylori, increase the risk of cancer in their immediate vicinity (stomach), while others, such as some Bacteroides species, help protect against tumors by boosting T-cell infiltration.© EYE OF SCIENCE/SCIENCE SOURCE
http://www.the-scientist.com/images/April2016/immune_2.jpg

 

 

© DR. GARY GAUGLER/SCIENCE SOURCE  http://www.the-scientist.com/images/April2016/immune3.jpg

At the University of Chicago, Thomas Gajewski and his colleagues have taken a slightly different approach to studying the role of the microbiome in cancer development. By comparing Black 6 mice coming from different vendors—Taconic Biosciences (formerly Taconic Farms) and the Jackson Laboratory—Gajewski takes advantage of the fact that the animals’ different origins result in different gut microbiomes. “We deliberately stayed away from antibiotics, because we had a desire to model how intersubject heterogeneity [in cancer development] might be impacted by the commensals they happen to be colonized with,” says Gajewski in an email to The Scientist.

Last year, the researchers published the results of a study comparing the progression of melanoma tumors implanted under the mice’s skin, finding that tumors in the Taconic mice grew more aggressively than those in the Jackson mice. When the researchers housed the different types of mice together before their tumors were implanted, however, these differences disappeared. And transferring fecal material from the Jackson mice into the Taconic mice altered the latter’s tumor progression.14

Instead of promoting cancer, in these experiments the gut microbiome appeared to slow tumor growth. Specifically, the reduced tumor growth in the Jackson mice correlated with the presence of Bifidobacterium, which led to the greater buildup of T?cells in the Jackson mice’s tumors. Bifidobacteriaactivate dendritic cells, which present antigens from bacteria or cancer cells to T?cells, training them to hunt down and kill these invaders. Feeding Taconic mice bifidobacteria improved their response to the implanted melanoma cells.

“One hypothesis going into the experiments was that we might identify immune-suppressive bacteria, or commensals that shift the immune response towards a character that was unfavorable for tumor control,” says Gajewski.  “But in fact, we found that even a single type of bacteria could boost the antitumor immune response.”

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Drug interactions

Ideally, the immune system should recognize cancer as invasive and nip tumor growth in the bud. But cancer cells display “self” molecules that can inhibit immune attack. A new type of immunotherapy, dubbed checkpoint inhibition or blockade, spurs the immune system to attack cancer by blocking either the tumor cells’ surface molecules or the receptors on T?cells that bind to them.

CANCER THERAPY AND THE MICROBIOME

In addition to influencing the development and progression of cancer by regulating inflammation and other immune pathways, resident gut bacteria appear to influence the effectiveness of many cancer therapies that are intended to work in concert with host immunity to eliminate tumors.

  • Some cancer drugs, such as oxaliplatin chemotherapy and CpG-oligonucleotide immunotherapy, work by boosting inflammation. If the microbiome is altered in such a way that inflammation is reduced, these therapeutic agents are less effective.
  • Cancer-cell surface proteins bind to receptors on T cells to prevent them from killing cancer cells. Checkpoint inhibitors that block this binding of activated T cells to cancer cells are influenced by members of the microbiota that mediate these same cell interactions.
  • Cyclophosphamide chemotherapy disrupts the gut epithelial barrier, causing the gut to leak certain bacteria. Bacteria gather in lymphoid tissue just outside the gut and spur generation of T helper 1 and T helper 17 cells that migrate to the tumor and kill it.

As part of their comparison of Jackson and Taconic mice, Gajewski and his colleagues decided to test a type of investigational checkpoint inhibitor that targets PD-L1, a ligand found in high quantities on the surface of multiple types of cancer cells. Monoclonal antibodies that bind to PD-L1 block the PD-1 receptors on T?cells from doing so, allowing an immune response to proceed against the tumor cells. While treating Taconic mice with PD-L1–targeting antibodies did improve their tumor responses, they did even better when that treatment was combined with fecal transfers from Jackson mice, indicating that the microbiome and the immunotherapy can work together to take down cancer. And when the researchers combined the anti-PD-L1 therapy with a bifidobacteria-enriched diet, the mice’s tumors virtually disappeared.14

Gajewski’s group is now surveying the gut microbiota in humans undergoing therapy with checkpoint inhibitors to better understand which bacterial species are linked to positive outcomes. The researchers are also devising a clinical trial in which they will give Bifidobacterium supplements to cancer patients being treated with the approved anti-PD-1 therapy pembrolizumab (Keytruda), which targets the immune receptor PD-1 on T?cells, instead of the cancer-cell ligand PD-L1.

Meanwhile, Zitvogel’s group at INSERM is investigating interactions between the microbiome and another class of checkpoint inhibitors called CTLA-4 inhibitors, which includes the breakthrough melanoma treatment ipilimumab (Yervoy). The researchers found that tumors in antibiotic-treated and germ-free mice had poorer responses to a CTLA-4–targeting antibody compared with mice harboring unaltered microbiomes.15 Particular Bacteroides species were associated with T-cell infiltration of tumors, and feedingBacteroides fragilis to antibiotic-treated or germ-free mice improved the animals’ responses to the immunotherapy. As an added bonus, treatment with these “immunogenic” Bacteroides species decreased signs of colitis, an intestinal inflammatory condition that is a dangerous side effect in patients using checkpoint inhibitors. Moreover, Zitvogel and her colleagues showed that human metastatic melanoma patients treated with ipilimumab tended to have elevated levels of B. fragilis in their microbiomes. Mice transplanted with feces from patients who showed particularly strong B. fragilis gains did better on anti-CTLA-4 treatment than did mice transplanted with feces from patients with normal levels of B. fragilis.

“There are bugs that allow the therapy to work, and at the same time, they protect against colitis,” says Trinchieri. “That is very exciting, because not only [can] we do something to improve the therapy, but we can also, at the same time, try to reduce the side effect.”

And these checkpoint inhibitors aren’t the only cancer therapies whose effects are modulated by the microbiome. Trinchieri has also found that an immunotherapy that combines antibodies against interleukin-10 receptors with CpG oligonucleotides is more effective in mice with unaltered microbiomes.1He and his NCI colleague Goldszmid further found that the platinum chemotherapy oxaliplatin (Eloxatin) was more effective in mice with intact microbiomes, and Zitvogel’s group has shown that the chemotherapeutic agent cyclophosphamide is dependent on the microbiota for its proper function.

Although the mechanisms by which the microbiome influences the effectiveness of such therapies remains incompletely understood, researchers once again speculate that the immune system is the key link. Cyclophosphamide, for example, spurs the body to generate two types of T?helper cells, T?helper 1 cells and a subtype of T?helper 17 cells referred to as “pathogenic,” both of which destroy tumor cells. Zitvogel and her colleagues found that, in mice with unaltered microbiomes, treatment with cyclophosphamide works by disrupting the intestinal mucosa, allowing bacteria to escape into the lymphoid tissues just outside the gut. There, the bacteria spur the body to generate T?helper 1 and T?helper 17 cells, which translocate to the tumor. When the researchers transferred the “pathogenic” T?helper 17 cells into antibiotic-treated mice, the mice’s response to chemotherapy was partly restored.

Microbiome modification

As the link between the microbiome and cancer becomes clearer, researchers are thinking about how they can manipulate a patient’s resident microbial communities to improve their prognosis and treatment outcomes. “Once you figure out exactly what is happening at the molecular level, if there is something promising there, I would be shocked if people don’t then go in and try to modulate the microbiome, either by using pharmaceuticals or using probiotics,” says Michael Burns, a postdoc in the lab of University of Minnesota genomicist Ran Blekhman.

Even if researchers succeed in identifying specific, beneficial alterations to the microbiome, however, molding the microbiome is not simple. “It’s a messy, complicated system that we don’t understand,” says Schloss.

So far, studies of the gut microbiome and colon cancer have turned up few consistent differences between cancer patients and healthy controls. And the few bacterial groups that have repeatedly shown up are not present in every cancer patient. “We should move away from saying, ‘This is a causal species of bacteria,’” says Blekhman. “It’s more the function of a community instead of just a single bacterium.”

But the study of the microbiome in cancer is young. If simply adding one type of microbe into a person’s gut is not enough, researchers may learn how to dose people with patient-specific combinations of microbes or antibiotics. In February 2016, a team based in Finland and China showed that a probiotic mixture dubbed Prohep could reduce liver tumor size by 40 percent in mice, likely by promoting an anti-inflammatory environment in the gut.16

“If it is true that, in humans, we can alter the course of the disease by modulating the composition of the microbiota,” says José Conejo-Garcia of the Wistar Institute in Philadelphia, “that’s going to be very impactful.”

Kate Yandell has been a freelance writer living Philadelphia, Pennsylvania. In February she became an associate editor at Cancer Today.

GENETIC CONNECTION

The microbiome doesn’t act in isolation; a patient’s genetic background can also greatly influence response to therapy. Last year, for example, the Wistar Institute’s José Garcia-Conejo and Melanie Rutkowski, now an assistant professor at the University of Virginia, showed that a dominant polymorphism of the gene for the innate immune protein toll-like receptor 5 (TLR5) influences clinical outcomes in cancer patients by changing how the patients’ immune cells interact with their gut microbes (Cancer Cell, 27:27-40, 2015).

More than 7 percent of people carry a specific mutation in TLR5 that prevents them from mounting a full immune response when exposed to bacterial flagellin. Analyzing both genetic and survival data from the Cancer Genome Atlas, Conejo-Garcia, Rutkowski, and their colleagues found that estrogen receptor–positive breast cancer patients who carry the TLR5 mutation, called the R392X polymorphism, have worse outcomes than patients without the mutation. Among patients with ovarian cancer, on the other hand, those with the TLR5 mutation were more likely to live at least six years after diagnosis than patients who don’t carry the mutation.

Investigating the mutation’s contradictory effects, the researchers found that mice with normal TLR5produce higher levels of the cytokine interleukin 6 (IL-6) than those carrying the mutant version, which have higher levels of a different cytokine called interleukin 17 (IL-17). But when the researchers knocked out the animals’ microbiomes, these differences in cytokine production disappeared, as did the differences in cancer progression between mutant and wild-type animals.

“The effectiveness of depleting specific populations or modulating the composition of the microbiome is going to affect very differently people who are TLR5-positive or TLR5-negative,” says Conejo-Garcia. And Rutkowski speculates that many more polymorphisms linked to cancer prognosis may act via microbiome–immune system interactions. “I think that our paper is just the tip of the iceberg.”

References

  1. N. Iida et al., “Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment,” Science, 342:967-70, 2013.
  2. S. Viaud et al., “The intestinal microbiota modulates the anticancer immune effects of cyclophosphamide,” Science, 342:971-76, 2013.
  3. J.R. Warren, B. Marshall, “Unidentified curved bacilli on gastric epithelium in active chronic gastritis,”Lancet, 321:1273-75, 1983.
  4. B.J. Marshall et al., “Attempt to fulfil Koch’s postulates for pyloric Campylobacter,” Med J Aust, 142:436-39, 1985.
  5. J. Parsonnet et al., “Helicobacter pylori infection and the risk of gastric carcinoma,” N Engl J Med, 325:1127-31, 1991.
  6. S. Kado et al., “Intestinal microflora are necessary for development of spontaneous adenocarcinoma of the large intestine in T-cell receptor β chain and p53 double-knockout mice,” Cancer Res, 61:2395-98, 2001.
  7. J.V. Newman et al., “Bacterial infection promotes colon tumorigenesis in ApcMin/+ mice,” J Infect Dis, 184:227-30, 2001.
  8. S.E. Erdman et al., “CD4+ CD25+ regulatory T lymphocytes inhibit microbially induced colon cancer in Rag2-deficient mice,” Am J Pathol, 162:691-702, 2003.
  9. J.P. Zackular et al., “The human gut microbiome as a screening tool for colorectal cancer,” Cancer Prev Res, 7:1112-21, 2014.
  10. G. Zeller et al., “Potential of fecal microbiota for early-stage detection of colorectal cancer,” Mol Syst Biol, 10:766, 2014.
  11. J.P. Zackular et al., “The gut microbiome modulates colon tumorigenesis,” mBio, 4:e00692-13, 2013.
  12. J.P. Zackular et al., “Manipulation of the gut microbiota reveals role in colon tumorigenesis,”mSphere, doi:10.1128/mSphere.00001-15, 2015.
  13. V.P. Rao et al., “Innate immune inflammatory response against enteric bacteria Helicobacter hepaticus induces mammary adenocarcinoma in mice,” Cancer Res, 66:7395, 2006.
  14. A. Sivan et al., “Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy,” Science, 350:1084-89, 2015.
  15. M. Vétizou et al., “Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota,”Science, 350:1079-84, 2015.

……..

 

Microbially Driven TLR5-Dependent Signaling Governs Distal Malignant Progression through Tumor-Promoting Inflammation

Melanie R. Rutkowski, Tom L. Stephen, Nikolaos Svoronos, …., Julia Tchou,  Gabriel A. Rabinovich, Jose R. Conejo-Garcia
Cancer cell    12 Jan 2015; Volume 27, Issue 1, p27–40  http://dx.doi.org/10.1016/j.ccell.2014.11.009
Figure thumbnail fx1
  • TLR5-dependent IL-6 mobilizes MDSCs that drive galectin-1 production by γδ T cells
  • IL-17 drives malignant progression in IL-6-unresponsive tumors
  • TLR5-dependent differences in tumor growth are abrogated upon microbiota depletion
  • A common dominant TLR5 polymorphism influences the outcome of human cancers

The dominant TLR5R392X polymorphism abrogates flagellin responses in >7% of humans. We report that TLR5-dependent commensal bacteria drive malignant progression at extramucosal locations by increasing systemic IL-6, which drives mobilization of myeloid-derived suppressor cells (MDSCs). Mechanistically, expanded granulocytic MDSCs cause γδ lymphocytes in TLR5-responsive tumors to secrete galectin-1, dampening antitumor immunity and accelerating malignant progression. In contrast, IL-17 is consistently upregulated in TLR5-unresponsive tumor-bearing mice but only accelerates malignant progression in IL-6-unresponsive tumors. Importantly, depletion of commensal bacteria abrogates TLR5-dependent differences in tumor growth. Contrasting differences in inflammatory cytokines and malignant evolution are recapitulated in TLR5-responsive/unresponsive ovarian and breast cancer patients. Therefore, inflammation, antitumor immunity, and the clinical outcome of cancer patients are influenced by a common TLR5 polymorphism.

see also… Immune Influence

In recent years, research has demonstrated that microbes living in and on the mammalian body can affect cancer risk, as well as responses to cancer treatment.

By Kate Yandell | April 1, 2016

http://www.the-scientist.com/?articles.view/articleNo/45644/title/Immune-Influence

Although the details of this microbe-cancer link remain unclear, investigators suspect that the microbiome’s ability to modulate inflammation and train immune cells to react to tumors is to blame. Here are some of the hypotheses that have come out of recent research in rodents for how gut bacteria shape immunity and influence cancer.

HOW THE MICROBIOME PROMOTES CANCER

Gut bacteria can dial up inflammation locally in the colon, as well as in other parts of the body, leading to the release of reactive oxygen species, which damage cells and DNA, and of growth factors that spur tumor growth and blood vessel formation.

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Helicobacter pylori can cause inflammation and high cell turnover in the stomach wall, which may lead to cancerous growth.

HOW THE MICROBIOME STEMS CANCER

Gut bacteria can also produce factors that lower inflammation and slow tumor growth. Some gut bacteria (e.g., Bifidobacterium)
appear to activate dendritic cells,
which present cancer-cell antigens to T cells that in turn kill the cancer cells.

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Read the full story.

 

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Blood test uses DNA strands of dying cells

Curators:  Larry H. Bernstein, MD, FCAP and Aviva Lev-Ari, PhD, RN

LPBI

 

Hadassah-Developed Blood Test Detects Multiple Sclerosis, Cancer & Brain Damage

http://www.hadassah.org/news-stories/blood-test-detects-neurodegenerative-disease.html

A new blood test that uses the DNA strands of dying cells to detect diabetes, cancer, traumatic brain injury, and neurodegenerative disease has been developed by researchers at Hadassah Medical Organization (HMO) and The Hebrew University.

In a study involving 320 patients, the researchers were able to infer cell death in specific tissues by looking at the unique chemical modifications (called methylation patterns) of circulating DNA that these dying cells release. Previously, it had not been possible to measure cell death in specific human tissues non-invasively.

The findings are reported in the March 14, 2016 online edition of Proceedings of National Academy of Sciences USA, in an article entitled “Identification of tissue specific cell death using methylation patterns of circulating DNA.”  Prof. Benjamin Glaser, head of Endocrinology at Hadassah, and Dr. Ruth Shemer and Prof. Yuval Dor from The Hebrew University of Jerusalem led an international team in performing the groundbreaking research.

Cell death is a central feature in health and disease. It can signify the early stages of pathology (e.g. a developing tumor or the beginning of an autoimmune or neurodegenerative disease); it can illuminate whether a disease has progressed and whether a particular treatment, such as chemotherapy, is working; and it can alert physicians to unintended toxic effects of treatment or the early rejection of a transplant.

As the researchers relate: “The approach can be adapted to identify cfDNA (cell-free circulating DNA) derived from any cell type in the body, offering a minimally invasive window for diagnosing and monitoring a broad spectrum of human pathologies as well as providing a better understanding of normal tissue dynamics.”

“In the long run,” notes Prof. Glaser, “we envision a new type of blood test aimed at the sensitive detection of tissue damage, even without a-priori suspicion of disease in a specific organ. We believe that such a tool will have broad utility in diagnostic medicine and in the study of human biology.”

The research was performed by Hebrew University students Roni Lehmann-Werman, Daniel Neiman, Hai Zemmour, Joshua Moss and Judith Magenheim, aided by clinicians and scientists from Hadassah Medical Center, Sheba Medical Center, and from institutions in Germany, Sweden, the USA and Canada, who provided precious blood samples from patients.

Scientists have known for decades that dying cells release fragmented DNA into the blood; however, since the DNA sequence of all cells in the body is identical, it had not been possible to determine the tissue of origin of the circulating DNA.  Knowing that the DNA of each cell type carries a unique methylation and that methylation patterns of DNA account for the identity of cells, the researchers were able to use patterns of methylated DNA sequences as biomarkers to detect the origin of the DNA and to identify a specific pathology. For example, they were able to detect evidence of pancreatic beta-cell death in the blood of patients with new-onset type 1 diabetes, oligodendrocyte cell death in patients with relapsing multiple sclerosis, brain cell death in patients after traumatic or ischemic brain damage, and exocrine pancreatic tissue cell death in patients with pancreatic cancer or pancreatitis.

Support for the research came from the Juvenile Diabetes Research Foundation, the Human Islet Research Network of the National Institutes of Health, the Sir Zalman Cowen Universities Fund, the DFG (a Trilateral German-Israel-Palestine program), and the Soyka pancreatic cancer fund.

 Identification of tissue-specific cell death using methylation patterns of circulating DNA.
Minimally invasive detection of cell death could prove an invaluable resource in many physiologic and pathologic situations. Cell-free circulating DNA (cfDNA) released from dying cells is emerging as a diagnostic tool for monitoring cancer dynamics and graft failure. However, existing methods rely on differences in DNA sequences in source tissues, so that cell death cannot be identified in tissues with a normal genome. We developed a method of detecting tissue-specific cell death in humans based on tissue-specific methylation patterns in cfDNA. We interrogated tissue-specific methylome databases to identify cell type-specific DNA methylation signatures and developed a method to detect these signatures in mixed DNA samples. We isolated cfDNA from plasma or serum of donors, treated the cfDNA with bisulfite, PCR-amplified the cfDNA, and sequenced it to quantify cfDNA carrying the methylation markers of the cell type of interest. Pancreatic β-cell DNA was identified in the circulation of patients with recently diagnosed type-1 diabetes and islet-graft recipients; oligodendrocyte DNA was identified in patients with relapsing multiple sclerosis; neuronal/glial DNA was identified in patients after traumatic brain injury or cardiac arrest; and exocrine pancreas DNA was identified in patients with pancreatic cancer or pancreatitis. This proof-of-concept study demonstrates that the tissue origins of cfDNA and thus the rate of death of specific cell types can be determined in humans. The approach can be adapted to identify cfDNA derived from any cell type in the body, offering a minimally invasive window for diagnosing and monitoring a broad spectrum of human pathologies as well as providing a better understanding of normal tissue dynamics.

While impressively organ specific, they did not specifically prove that the DNA was from an actual dying cell. For example, you would need to see if Troponin levels were elevated when assuming the DNA is from injured myocardium. Also, for brain, though impractical , you’d want to see a brain biopsy or imaging for the brain related cases. The experiment of spiking with DNA was clever though. Also, what is the turnaround time for this test in practical use?

Larry HB

Very good comment. I was reluctant to put this up, but it was of interest and published in PNAS.  Perhaps I can find more information.  Troponin levels would be good for 48 hours, longer than CK and comparable to LD.  What about Nat peptides?

Glutamine and cancer: cell biology, physiology, and clinical opportunities

Christopher T. Hensley,1 Ajla T. Wasti,1,2 

J Clin Invest 2013   https://www.jci.org/articles/view/69600

Glutamine is an abundant and versatile nutrient that participates in energy formation, redox homeostasis, macromolecular synthesis, and signaling in cancer cells. These characteristics make glutamine metabolism an appealing target for new clinical strategies to detect, monitor, and treat cancer. Here we review the metabolic functions of glutamine as a super nutrient and the surprising roles of glutamine in supporting the biological hallmarks of malignancy. We also review recent efforts in imaging and therapeutics to exploit tumor cell glutamine dependence, discuss some of the challenges in this arena, and suggest a disease-focused paradigm to deploy these emerging approaches.

It has been nearly a century since the discovery that tumors display metabolic activities that distinguish them from differentiated, non-proliferating tissues and presumably contribute to their supraphysiological survival and growth (1). Interest in cancer metabolism was boosted by discoveries that oncogenes and tumor suppressors could regulate nutrient metabolism, and that mutations in some metabolic enzymes participate in the development of malignancy (2, 3). The persistent appeal of cancer metabolism as a line of investigation lies both in its ability to uncover fundamental aspects of malignancy and in the translational potential of exploiting cancer metabolism to improve the way we diagnose, monitor, and treat cancer. Furthermore, an improved understanding of how altered metabolism contributes to cancer has a high potential for synergy with translational efforts. For example, the demonstration that asparagine is a conditionally essential nutrient in rapidly growing cancer cells paved the way for L-asparaginase therapy in leukemia. Additionally, the avidity of some tumors for glucose uptake led to the development of 18fluoro-2-deoxyglucose imaging by PET; this in turn stimulated hundreds of studies on the biological underpinnings of tumor glucose metabolism.

There continue to be large gaps in understanding which metabolic pathways are altered in cancer, whether these alterations benefit the tumor in a substantive way, and how this information could be used in clinical oncology. In this Review, we consider glutamine, a highly versatile nutrient whose metabolism has implications for tumor cell biology, metabolic imaging, and perhaps novel therapeutics.

Glutamine in intermediary metabolism

Glutamine metabolism has been reviewed extensively and is briefly outlined here (4, 5). The importance of glutamine as a nutrient in cancer derives from its abilities to donate its nitrogen and carbon into an array of growth-promoting pathways (Figure 1). At concentrations of 0.6–0.9 mmol/l, glutamine is the most abundant amino acid in plasma (6). Although most tissues can synthesize glutamine, during periods of rapid growth or other stresses, demand outpaces supply, and glutamine becomes conditionally essential (7). This requirement for glutamine is particularly true in cancer cells, many of which display oncogene-dependent addictions to glutamine in culture (8). Glutamine catabolism begins with its conversion to glutamate in reactions that either donate the amide nitrogen to biosynthetic pathways or release it as ammonia. The latter reactions are catalyzed by the glutaminases (GLSs), of which several isozymes are encoded by human genes GLS and GLS2 (9). Classical studies revealed that GLS isozymes, particularly those encoded by GLS, are expressed in experimental tumors in rats and mice, where their enzyme activity correlates with growth rate and malignancy. Silencing GLS expression or inhibiting GLS activity is sufficient to delay tumor growth in a number of models (1013). The role of GLS2 in cancer appears to be context specific and regulated by factors that are still incompletely characterized. In some tissues, GLS2 is a p53 target gene and seems to function in tumor suppression (14). On the other hand, GLS2 expression is enhanced in some neuroblastomas, where it contributes to cell survival (15). These observations, coupled with the demonstration that c-Myc stimulates GLS expression (12, 16), position at least some of the GLS isozymes as pro-oncogenic.

Glutamine metabolism as a target for diagnostic imaging and therapy in cancFigure 1Glutamine metabolism as a target for diagnostic imaging and therapy in cancer. Glutamine is imported via SLC1A5 and other transporters, then enters a complex metabolic network by which its carbon and nitrogen are supplied to pathways that promote cell survival and growth. Enzymes discussed in the text are shown in green, and inhibitors that target various aspects of glutamine metabolism are shown in red. Green arrows denote reductive carboxylation. 18F-labeled analogs of glutamine are also under development as PET probes for localization of tumor tissue. AcCoA, acetyl-CoA; DON, 6-diazo-5-oxo-L-norleucine; GSH, glutathione; NEAA, nonessential amino acids; ME, malic enzyme; OAA, oxaloacetate; TA, transaminase; 968, compound 968; α-KG, α-ketoglutarate.

Glutamate, the product of the GLS reaction, is a precursor of glutathione, the major cellular antioxidant. It is also the source of amino groups for nonessential amino acids like alanine, aspartate, serine, and glycine, all of which are required for macromolecular synthesis. In glutamine-consuming cells, glutamate is also the major source of α-ketoglutarate, a TCA cycle intermediate and substrate for dioxygenases that modify proteins and DNA. These dioxygenases include prolyl hydroxylases, histone demethylases, and 5-methylcytosine hydroxylases. Their requirement for α-ketoglutarate, although likely accounting for only a small fraction of total α-ketoglutarate utilization, makes this metabolite an essential component of cell signaling and epigenetic networks.

Conversion of glutamate to α-ketoglutarate occurs either through oxidative deamination by glutamate dehydrogenase (GDH) in the mitochondrion or by transamination to produce nonessential amino acids in either the cytosol or the mitochondrion. During avid glucose metabolism, the transamination pathway predominates (17). When glucose is scarce, GDH becomes a major pathway to supply glutamine carbon to the TCA cycle, and is required for cell survival (17, 18). Metabolism of glutamine-derived α-ketoglutarate in the TCA cycle serves several purposes: it generates reducing equivalents for the electron transport chain (ETC) and oxidative phosphorylation, becoming a major source of energy (19); and it is an important anaplerotic nutrient, feeding net production of oxaloacetate to offset export of intermediates from the cycle to supply anabolism (20). Glutamine oxidation also supports redox homeostasis by supplying carbon to malic enzyme, some isoforms of which produce NADPH (Figure 1). In KRAS-driven pancreatic adenocarcinoma cells, a pathway involving glutamine-dependent NADPH production is essential for redox balance and growth (21). In these cells, glutamine is used to produce aspartate in the mitochondria. This aspartate is then trafficked to the cytosol, where it is deaminated to produce oxaloacetate and then malate, the substrate for malic enzyme.

Recent work has uncovered an unexpected role for glutamine in cells with reduced mitochondrial function. Despite glutamine’s conventional role as a respiratory substrate, several studies demonstrated a persistence of glutamine dependence in cells with permanent mitochondrial dysfunction from mutations in the ETC or TCA cycle, or transient impairment secondary to hypoxia (2225). Under these conditions, glutamine-derived α-ketoglutarate is reductively carboxylated by NADPH-dependent isoforms of isocitrate dehydrogenase to produce isocitrate, citrate, and other TCA cycle intermediates (Figure 1). These conditions broaden glutamine’s utility as a carbon source because it becomes not only a major source of oxaloacetate, but also generates acetyl-CoA in what amounts to a striking rewiring of TCA cycle metabolism.

Glutamine promotes hallmarks of malignancy

Deregulated energetics. One hallmark of cancer cells is aberrant bioenergetics (26). Glutamine’s involvement in the pathways outlined above contributes to a phenotype conducive to energy formation, survival, and growth. In addition to its role in mitochondrial metabolism, glutamine also suppresses expression of thioredoxin-interacting protein, a negative regulator of glucose uptake (27). Thus, glutamine contributes to both of the energy-forming pathways in cancer cells: oxidative phosphorylation and glycolysis. Glutamine also modulates hallmarks not traditionally thought to be metabolic, as outlined below. These interactions highlight the complex interplay between glutamine metabolism and many aspects of cell biology.

Sustaining proliferative signaling. Pathological cancer cell growth relies on maintenance of proliferative signaling pathways with increased autonomy relative to non-malignant cells. Several lines of evidence argue that glutamine reinforces activity of these pathways. In some cancer cells, excess glutamine is exported in exchange for leucine and other essential amino acids. This exchange facilitates activation of the serine/threonine kinase mTOR, a major positive regulator of cell growth (28). In addition, glutamine-derived nitrogen is a component of amino sugars, known as hexosamines, that are used to glycosylate growth factor receptors and promote their localization to the cell surface. Disruption of hexosamine synthesis reduces the ability to initiate signaling pathways downstream of growth factors (29).

Enabling replicative immortality. Some aspects of glutamine metabolism oppose senescence and promote replicative immortality in cultured cells. In IMR90 lung fibroblasts, silencing either of two NADPH-generating isoforms of malic enzyme (ME1, ME2) rapidly induced senescence, while malic enzyme overexpression suppressed senescence (30). Both malic enzyme isoforms are repressed at the transcriptional level by p53 and contribute to enhanced levels of glutamine consumption and NADPH production in p53-deficient cells. The ability of p53-replete cells to resist senescence required the expression of ME1 and ME2, and silencing either enzyme reduced the growth of TP53+/+ and, to a lesser degree, TP53–/– tumors (30). These observations position malic enzymes as potential therapeutic targets.

Resisting cell death. Although many cancer cells require glutamine for survival, cells with enhanced expression of Myc oncoproteins are particularly sensitive to glutamine deprivation (8, 12, 16). In these cells, glutamine deprivation induces depletion of TCA cycle intermediates, depression of ATP levels, delayed growth, diminished glutathione pools, and apoptosis. Myc drives glutamine uptake and catabolism by activating the expression of genes involved in glutamine metabolism, including GLSand SLC1A5, which encodes the Na+-dependent amino acid transporter ASCT2 (12, 16). SilencingGLS mimicked some of the effects of glutamine deprivation, including growth suppression in Myc-expressing cells and tumors (10, 12). MYCN amplification occurs in 20%–25% of neuroblastomas and is correlated with poor outcome (31). In cells with high N-Myc levels, glutamine deprivation triggered an ATF4-dependent induction of apoptosis that could be prevented by restoring downstream metabolites oxaloacetate and α-ketoglutarate (15). In this model, pharmacological activation of ATF4, inhibition of glutamine metabolic enzymes, or combinations of these treatments mimicked the effects of glutamine deprivation in cells and suppressed growth of MYCN-amplified subcutaneous and transgenic tumors in mice.

The PKC isoform PKC-ζ also regulates glutamine metabolism. Loss of PKC-ζ enhances glutamine utilization and enables cells to survive glucose deprivation (32). This effect requires flux of carbon and nitrogen from glutamine into serine. PKC-ζ reduces the expression of phosphoglycerate dehydrogenase, an enzyme required for glutamine-dependent serine biosynthesis, and also phosphorylates and inactivates this enzyme. Thus, PKC-ζ loss, which promotes intestinal tumorigenesis in mice, enables cells to alter glutamine metabolism in response to nutrient stress.

Invasion and metastasis. Loss of the epithelial cell-cell adhesion molecule E-cadherin is a component of the epithelial-mesenchymal transition, and is sufficient to induce migration, invasion, and tumor progression (33, 34). Addiction to glutamine may oppose this process because glutamine favors stabilization of tight junctions in some cells (35). Furthermore, the selection of breast cancer cells with the ability to grow without glutamine yielded highly adaptable subpopulations with enhanced mesenchymal marker expression and improved capacity for anchorage-independent growth, therapeutic resistance, and metastasis in vivo (36). It is unknown whether this result reflects a primary role for glutamine in suppressing these markers of aggressiveness in breast cancer, or whether prolonged glutamine deprivation selects for cells with enhanced fitness across a number of phenotypes.

Organ-specific glutamine metabolism in health and disease

As a major player in carbon and nitrogen transport, glutamine metabolism displays complex inter-organ dynamics, with some organs functioning as net producers and others as consumers (Figure 2). Organ-specific glutamine metabolism has frequently been studied in humans and animal models by measuring the arteriovenous difference in plasma glutamine abundance. In healthy subjects, the plasma glutamine pool is largely the result of release from skeletal muscle (3739). In rats, the lungs are comparable to muscle in terms of glutamine production (40, 41), and human lungs also have the capacity for marked glutamine release, although such release is most prominent in times of stress (42, 43). Stress-induced release from the lung is regulated by an induction of glutamine synthase expression as a consequence of glucocorticoid signaling and other mechanisms (44, 45). Although this results in a small arteriovenous difference, the overall release of glutamine is significant because of the large pulmonary perfusion. In rats and humans, adipose tissue is a minor but potentially important source of glutamine (46, 47). The liver has the capacity to synthesize or catabolize glutamine, with these activities subject both to regional heterogeneity among hepatocytes and regulatory effects of systemic acidosis and hyperammonemia. However, the liver does not appear to be a major contributor to the plasma glutamine pool in healthy rats and humans (39, 48, 49).

Model for inter-organ glutamine metabolism in health and cancer.Figure 2Model for inter-organ glutamine metabolism in health and cancer. Organs that release glutamine into the bloodstream are shown in green, and those that consume glutamine are in red; the shade denotes magnitude of consumption/release. For some organs (liver, kidneys), evidence from model systems and/or human studies suggests that there is a change in net glutamine flux during tumorigenesis.

Glutamine consumption occurs largely in the gut and kidney. The organs of the gastrointestinal tract drained by the portal vein, particularly the small intestine, are major consumers of plasma glutamine in both rats and humans (37, 38, 49, 50). Enterocytes oxidize more than half of glutamine carbon to CO2, accounting for a third of the respiration of these cells in fasting animals (51). The kidney consumes net quantities of glutamine to maintain acid-base balance (37, 38, 52, 53). During acidosis, the kidneys substantially increase their uptake of glutamine, cleaving it by GLS to produce ammonia, which is excreted along with organic acids to maintain physiologic pH (52, 54). Glutamine is also a major metabolic substrate in lymphocytes and macrophages, at least during mitogenic stimulation of primary cells in culture (5557).

Importantly, cancer seems to cause major changes in inter-organ glutamine trafficking (Figure 2). Currently, much work in this area is derived from studies in methylcholanthrene-induced fibrosarcoma in the rat, a model of an aggressively growing, glutamine-consuming tumor. In this model, fibrosarcoma induces skeletal muscle expression of glutamine synthetase and greatly increases the release of glutamine into the circulation. As the tumor increases in size, intramuscular glutamine pools are depleted in association with loss of lean muscle mass, mimicking the cachectic phenotype of humans in advanced stages of cancer (52). Simultaneously, both the liver and the kidneys become net glutamine exporters, although the hepatic effect may be diminished as the tumor size becomes very large (48, 49, 52). Glutamine utilization by organs supplied by the portal vein is diminished in cancer (48). In addition to its function as a nutrient for the tumor itself, and possibly for cancer-associated immune cells, glutamine provides additional, indirect metabolic benefits to both the tumor and the host. For example, glutamine was used as a gluconeogenic substrate in cachectic mice with large orthotopic gliomas, providing a significant source of carbon in the plasma glucose pool (58). This glucose was taken up and metabolized by the tumor to produce lactate and to supply the TCA cycle.

It will be valuable to extend work in human inter-organ glutamine trafficking, both in healthy subjects and in cancer patients. Such studies will likely produce a better understanding of the pathophysiology of cancer cachexia, a major source of morbidity and mortality. Research in this area should also aid in the anticipation of organ-specific toxicities of drugs designed to interfere with glutamine metabolism. Alterations of glutamine handling in cancer may induce a different spectrum of toxicities compared with healthy subjects.

Tumors differ according to their need for glutamine

One important consideration is that not all cancer cells need an exogenous supply of glutamine. A panel of lung cancer cell lines displayed significant variability in their response to glutamine deprivation, with some cells possessing almost complete independence (59). Breast cancer cells also demonstrate systematic differences in glutamine dependence, with basal-type cells tending to be glutamine dependent and luminal-type cells tending to be glutamine independent (60). Resistance to glutamine deprivation is associated with the ability to synthesize glutamine de novo and/or to engage alternative pathways of anaplerosis (10, 60).

Tumors also display variable levels of glutamine metabolism in vivo. A study of orthotopic gliomas revealed that genetically diverse, human-derived tumors took up glutamine in the mouse brain but did not catabolize it (58). Rather, the tumors synthesized glutamine de novo and used pyruvate carboxylation for anaplerosis. Cells derived from these tumors did not require glutamine to survive or proliferate when cultured ex vivo. Glutamine synthesis from glucose was also a prominent feature of primary gliomas in human subjects infused with 13C-glucose at the time of surgical resection (61). Furthermore, an analysis of glutamine metabolism in lung and liver tumors revealed that both the tissue of origin and the oncogene influence whether the tumor produces or consumes glutamine (62). MET-induced hepatic tumors produced glutamine, whereas Myc-induced liver tumors catabolized it. In the lung, however, Myc expression was associated with glutamine accumulation.

This variability makes it imperative to develop ways to predict which tumors have the highest likelihood of responding to inhibitors of glutamine metabolism. Methods to image or otherwise quantify glutamine metabolism in vivo would be useful in this regard (63). Infusions of pre-surgical subjects with isotopically labeled glutamine, followed by extraction of metabolites from the tumor and analysis of 13C enrichment, can be used to detect both glutamine uptake and catabolism (58, 62). However, this approach requires a specimen of the tumor to be obtained. Approaches for glutamine-based imaging, which avoid this problem, include a number of glutamine analogs compatible with PET. Although glutamine could in principle be imaged using the radioisotopes 11C, 13N, or 18F, the relatively long half-life of the latter increases its appeal. In mice, 18F-(2S, 4R)4-fluoroglutamine is avidly taken up by tumors derived from highly glutaminolytic cells, and by glutamine-consuming organs including the intestine, kidney, liver, and pancreas (64). Labeled analogs of glutamate are also taken up by some tumors (65, 66). One of these, (4S)-4-(3-[18F] fluoropropyl)-L-glutamate (18F-FSPG, also called BAY 94-9392), was evaluated in small clinical trials involving patients with several types of cancer (65, 67). This analog enters the cell through the cystine/glutamate exchange transporter (xCtransport system), which is linked to glutathione biosynthesis (68). The analog was well tolerated, with high tumor detection rates and good tumor-to-background ratios in hepatocellular carcinoma and lung cancer.

PET approaches detect analog uptake and retention but cannot provide information about downstream metabolism. Analysis of hyperpolarized nuclei can provide a real-time view of enzyme-catalyzed reactions. This technique involves redistribution of the populations of energy levels of a nucleus (e.g., 13C, 15N), resulting in a gain in magnetic resonance signal that can temporarily exceed 10,000-fold (69). This gain in signal enables rapid detection of both the labeled molecule and its downstream metabolites. Glutamine has been hyperpolarized on 15N and 13C (70, 71). In the latter case, the conversion of hyperpolarized glutamine to glutamate could be detected in intact hepatoma cells (70). If these analogs are translated to clinical studies, they might provide a dynamic view of the proximal reactions of glutaminolysis in vivo.

Pharmacological strategies to inhibit glutamine metabolism in cancer

Efforts to inhibit glutamine metabolism using amino acid analogs have an extensive history, including evaluation in clinical trials. Acivicin, 6-diazo-5-oxo-L-norleucine, and azaserine, three of the most widely studied analogs (Figure 1), all demonstrated variable degrees of gastrointestinal toxicity, myelosuppression, and neurotoxicity (72). Because these agents non-selectively target glutamine-consuming processes, recent interest has focused on developing methods directed at specific nodes of glutamine metabolism. First, ASCT2, the Na+-dependent neutral amino acid transporter encoded by SLC1A5, is broadly expressed in lung cancer cell lines and accounts for a majority of glutamine transport in those cells (Figure 1). It has been shown that γ-L-glutamyl-p-nitroanilide (GPNA) inhibits this transporter and limits lung cancer cell growth (73). Additional interest in GPNA lies in its ability to enhance the uptake of drugs imported via the monocarboxylate transporter MCT1. Suppressing glutamine uptake with GPNA enhances MCT1 stability and stimulates uptake of the glycolytic inhibitor 3-bromopyruvate (3-BrPyr) (74, 75). Because enforced MCT1 overexpression is sufficient to sensitize tumor xenografts to 3-BrPyr (76), GPNA may have a place in 3-BrPyr–based therapeutic regimens.

Two inhibitors of GLS isoforms have been characterized in recent years (Figure 1). Compound 968, an inhibitor of the GLS-encoded splice isoform GAC, inhibits the transformation of fibroblasts by oncogenic RhoGTPases and delays the growth of GLS-expressing lymphoma xenografts (13). Bis-2-(5-phenylacetamido-1,2,4-thiadiazol-2-yl)ethyl sulfide (BPTES) also potently inhibits GLS isoforms encoded by GLS (77). BPTES impairs ATP levels and growth rates of P493 lymphoma cells under both normoxic and hypoxic conditions and suppresses the growth of P493-derived xenografts (78).

Evidence also supports a role for targeting the flux from glutamate to α-ketoglutarate, although no potent, specific inhibitors yet exist to inhibit these enzymes in intact cells. Aminooxyacetate (AOA) inhibits aminotransferases non-specifically, but milliomolar doses are typically used to achieve this effect in cultured cells (Figure 1). Nevertheless, AOA has demonstrated efficacy in both breast adenocarcinoma xenografts and autochthonous neuroblastomas in mice (15, 79). Epigallocatechin gallate (EGCG), a green tea polyphenol, has numerous pharmacological effects, one of which is to inhibit GDH (80). The effects of EGCG on GDH have been used to kill glutamine-addicted cancer cells during glucose deprivation or glycolytic inhibition (17, 18) and to suppress growth of neuroblastoma xenografts (15).

A paradigm to exploit glutamine metabolism in cancer

Recent advances in glutamine-based imaging, coupled with the successful application of glutamine metabolic inhibitors in mouse models of cancer, make it possible to conceive of treatment plans that feature consideration of tumor glutamine utilization. A key challenge will be predicting which tumors are most likely to respond to inhibitors of glutamine metabolism. Neuroblastoma is used here as an example of a tumor in which evidence supports the utility of strategies that would involve both glutamine-based imaging and therapy (Figure 3). Neuroblastoma is the second most common extracranial solid malignancy of childhood. High-risk neuroblastoma is defined by age, stage, and biological features of the tumor, including MYCN amplification, which occurs in some 20%–25% of cases (31). Because MYCN-amplified tumor cells require glutamine catabolism for survival and growth (15), glutamine-based PET at the time of standard diagnostic imaging could help predict which tumors would be likely to respond to inhibitors of glutamine metabolism. Infusion of 13C-glutamine coordinated with the diagnostic biopsy could then enable inspection of 13C enrichment in glutamine-derived metabolites from the tumor, confirming the activity of glutamine catabolic pathways. Following on evidence from mouse models of neuroblastoma, treatment could then include agents directed against glutamine catabolism (15). Of note, some tumors were sensitive to the ATF4 agonist fenretinide (FRT), alone or in combination with EGCG. Importantly, FRT has already been the focus of a Phase I clinical trial in children with solid tumors, including neuroblastoma, and was fairly well tolerated (81).

A strategy to integrate glutamine metabolism into the diagnosis, classificaFigure 3A strategy to integrate glutamine metabolism into the diagnosis, classification, treatment, and monitoring of neuroblastoma. Neuroblastoma commonly presents in children as an abdominal mass. A standard evaluation of a child with suspected neuroblastoma includes measurement of urine catecholamines, a bone scan, and full-body imaging with meta-iodobenzylguanidine (MIBG), all of which contribute to diagnosis and disease staging. In animal models, a subset of these tumors requires glutamine metabolism. This finding implies that approaches to image, quantify, or block glutamine metabolism (highlighted in red) in human neuroblastoma could be incorporated into the diagnosis and management of this disease. In particular, glutamine metabolic studies may help predict which tumors would respond to therapies targeting glutamine metabolism. HVA, homovanillic acid; VMA, vanillylmandelic acid.

Conclusions

Glutamine is a versatile nutrient required for the survival and growth of a potentially large subset of tumors. Work over the next several years should produce a more accurate picture of the molecular determinants of glutamine addiction and the identification of death pathways that execute cells when glutamine catabolism is impaired. Advancement of glutamine-based imaging into clinical practice should soon make it possible to differentiate tumors that take up glutamine from those that do not. Finally, the development of safe, high-potency inhibitors of key metabolic nodes should facilitate therapeutic regimens featuring inhibition of glutamine metabolism.

Therapeutic strategies impacting cancer cell glutamine metabolism

The metabolic adaptations that support oncogenic growth can also render cancer cells dependent on certain nutrients. Along with the Warburg effect, increased utilization of glutamine is one of the metabolic hallmarks of the transformed state. Glutamine catabolism is positively regulated by multiple oncogenic signals, including those transmitted by the Rho family of GTPases and by c-Myc. The recent identification of mechanistically distinct inhibitors of glutaminase, which can selectively block cellular transformation, has revived interest in the possibility of targeting glutamine metabolism in cancer therapy. Here, we outline the regulation and roles of glutamine metabolism within cancer cells and discuss possible strategies for, and the consequences of, impacting these processes therapeutically.

Cancer cell metabolism & glutamine addiction

Interest in the metabolic changes characteristic of malignant transformation has undergone a renaissance of sorts in the cancer biology and pharmaceutical communities. However, the recognition that an important connection exists between cellular metabolism and cancer began nearly a century ago with the work of Otto Warburg [13]. Warburg found that rapidly proliferating tumor cells exhibit elevated glucose uptake and glycolytic flux, and furthermore that much of the pyruvate generated by glycolysis is reduced to lactate rather than undergoing mitochondrial oxidation via the tricarboxylic acid (TCA) cycle (Figure 1). This phenomenon persists even under aerobic conditions (‘aerobic glycolysis’), and is known as the Warburg effect [4]. Warburg proposed that aerobic glycolysis was caused by defective mitochondria in cancer cells, but it is now known that mitochondrial dysfunction is relatively rare and that most tumors have an unimpaired capacity for oxidative phosphorylation [5]. In fact, the most important selective advantages provided by the Warburg effect are still debated. Although aerobic glycolysis is an inefficient way to produce ATP (2 ATP/glucose vs ~36 ATP/glucose by complete oxidation), a high glycolytic flux can generate ATP rapidly and furthermore can provide a biosynthetic advantage by supplying precursors and reducing equivalents for the synthesis of macromolecules [4]. The mechanisms underlying the Warburg effect are also not yet fully resolved, although it is increasingly clear that a number of oncogenes and tumor suppressors contribute to the phenomenon. The PI3K/Akt/mTORC1 signaling axis, for example, is a key regulator of aerobic glycolysis and biosynthesis, driving the surface expression of nutrient transporters and the upregulation of glycolytic enzymes [6]. The HIF transcription factor also upregulates expression of glucose transporters and glycolytic enzymes in response to hypoxia and growth factors (or loss of the von Hippel–Landau [VHL] tumor suppressor), and the oncogenic transcription factor c-Myc similarly induces expression of proteins important for glycolysis [6].

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Cell proliferation requires metabolic reprogramming

A second major change in the metabolic program of many cancer cells, and the primary focus of this review, is the alteration of glutamine metabolism. Glutamine is the major carrier of nitrogen between organs, and the most abundant amino acid in plasma [7]. It is also a key nutrient for numerous intracellular processes including oxidative metabolism and ATP generation, biosynthesis of proteins, lipids and nucleic acids, and also redox homeostasis and the regulation of signal transduction pathways [810]. Although most mammalian cells are capable of synthesizing glutamine, the demand for this amino acid can become so great during rapid proliferation that an additional extracellular supply is required; hence glutamine is considered conditionally essential [11]. Indeed, many cancer cells are ‘glutamine addicted’, and cannot survive in the absence of an exogenous glutamine supply [12,13].

An important step in the elevation of glutamine catabolism is the activation of the mitochondrial enzyme glutaminase, which catalyzes the hydrolysis of glutamine to generate glutamate and ammonium. The subsequent deamination of glutamate releases a second ammonium to yield the TCA cycle intermediate α-ketoglutarate (α-KG), a reaction catalyzed by glutamate dehydrogenase (GLUD1). This series of reactions is particularly important in rapidly proliferating cells, in which a considerable proportion of the TCA cycle metabolite citrate is exported from mitochondria in order to generate cytosolic acetyl-CoA for lipid biosynthesis [14]. Replenishment of TCA cycle intermediates (anaplerosis) is therefore required, and glutamine often serves as the key anaplerotic substrate through its conversion via glutamate to α-KG (Figure 1).

Mammals express two genes for glutaminase enzymes [1517]. The GLS gene encodes a protein initially characterized in kidney and thus called kidney-type glutaminase (KGA), although this enzyme and its shorter splice variant glutaminase C (GAC), collectively referred to as GLS, are now known to be widely distributed [1820]. The KGA and GAC isoforms share identical N-terminal and catalytic domains, encoded by exons 1–14 of the GLS gene, but have distinct C-termini derived from exon 15 in the case of GAC and exons 16–19 in the case of KGA [21]. Upregulation of GLS, in particular the GAC iso-form, is common in cancer cells and the degree of GLS overexpression correlates with both the degree of malignancy and the tumor grade in human breast cancer samples [22,23]. The GLS2 gene encodes a protein originally discovered and characterized in liver, which has thus been referred to as liver-type glutaminase and, more recently, as glutaminase 2 (GLS2) [15].

Both KGA and GAC can be activated by inorganic phosphate (Pi), and this activation correlates closely with a dimer-to-tetramer transition for each enzyme [7, 22]. As the concentration of Pi is raised the apparent catalytic constant, kcatapp, increases and simultaneously the apparent Michaelis constant, Kmapp, decreases; consequently the catalytic efficiency rises dramatically, especially in the case of GAC [22]. x-ray crystal structures of GAC and KGA in different states indicate that the positioning of a key loop within each monomer (Glu312 to Pro329), located between the active site and the dimer–dimer interface, is critical for mediating tetramerization-induced activation [22,24]. Given the ability of Pi to promote tetramerization and activation of GAC and KGA, it has been proposed that the elevated mitochondrial Pi levels found under hypoxic conditions, which are commonly encountered in the tumor microenvironment, could be one trigger for GLS activation [22].

Oncogenic alterations affecting glutamine metabolism

At least two classes of cellular signals regulate glutamine metabolism, influencing both the expression level and the enzymatic activity of GLS. The transcription factor c-Myc can suppress the expression of microRNAs miR-23a and miR-23b and, in doing so, upregulates GLS (specifically GAC) expression [13,25]. Independent of changes in GAC expression, oncogenic diffuse B-cell lymphoma protein (Dbl), a GEF for Rho GTPases and oncogenic variants of downstream Rho GTPases are able to signal to activate GAC in a manner that is dependent on NF-κB [23]. Mitochondria isolated from Dbl- or Rho GTPase-transformed NIH-3T3 fibroblasts demonstrate significantly higher basal glutaminase activity than mitochondria isolated from non-transformed cells [23]. Furthermore, the enzymatic activity of GAC immunoprecipitated from Dbl-transformed cells is elevated relative to GAC from non-transformed cells, indicating the presence of activating post-translational modification(s) [23]. Indeed, when GAC isolated from Dbl-transformed cells is treated with alkaline phosphatase, basal enzymatic activity is dramatically reduced [23]. Collectively, these findings point to phosphorylation events underlying the activation of GAC in transformed cells. Similarly, phosphorylation-dependent regulation of KGA activity downstream of the Raf-Mek-Erk signaling axis occurs in response to EGF stimulation [24].

It is becoming clear that, in addition to c-Myc and Dbl, many other oncogenic signals and environmental conditions can impact cellular glutamine metabolism. Loss of the retinoblastoma tumor suppressor, for example, leads to a marked increase in glutamine uptake and catabolism, and renders mouse embryonic fibroblasts dependent on exogenous glutamine [26]. Cells transformed by KRAS also illustrate increased expression of genes associated with glutamine metabolism and a corresponding increased utilization of glutamine for anabolic synthesis [27]. In fact, KRAS signaling appears to induce glutamine dependence, since the deleterious effects of glutamine withdrawal in KRAS-driven cells can be rescued by expression of a dominant-negative GEF for Ras [28]. Downstream of Ras, the Raf-MEK-ERK signaling pathway has been implicated in the upregulation of glutamine uptake and metabolism [24,29]. A recent study using human pancreatic ductal adenocarcinoma cells identified a novel KRAS-regulated metabolic pathway, through which glutamine supports cell growth [30]. Proliferation of KRAS-mutant pancreatic ductal adenocarcinoma cells depends on GLS-catalyzed production of glutamate, but not on downstream deamination of glutamate to α-KG; instead, transaminase-mediated glutamate metabolism is essential for growth. Glutamine-derived aspartate is subsequently transported into the cytoplasm where it is converted by aspartate transaminase into oxaloacetate, which can be used to generate malate and pyruvate. The series of reactions maintains NADPH levels and thus the cellular redox state [30].

Other recent studies have revealed that another pathway for glutamine metabolism can be essential under hypoxic conditions, and also in cancer cells with mitochondrial defects or loss of the VHL tumor suppressor [3135]. In these situations, glutamine-derived α-KG undergoes reductive carboxylation by IDH1 or IDH2 to generate citrate, which can be exported from mitochondria to support lipogenesis (Figure 1). Activation of HIF is both necessary and sufficient for driving the reductive carboxylation phenotype in renal cell carcinoma, and suppression of HIF activity can induce a switch from glutamine-mediated lipogenesis back to glucose-mediated lipogenesis [32,35]. Furthermore, loss of VHL and consequent downstream activation of HIF renders renal cell carcinoma cells sensitive to inhibitors of GLS [35]. Evidently, the metabolic routes through which glutamine supports cancer cell proliferation vary with genetic background and with microenvironmental conditions. Nevertheless, it is increasingly clear that diverse oncogenic signals promote glutamine utilization and furthermore that hypoxia, a common condition within poorly vascularized tumors, increases glutamine dependence.

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Consistent with the critical role of TCA cycle anaplerosis in cancer cell proliferation, a range of glutamine-dependent cancer cell lines are sensitive to silencing or inhibition of GLS [23,93]. Although loss of GLS suppresses proliferation, in some cases the induction of a compensatory anaplerotic mechanism mediated by pyruvate carboxylase (PC) allows the use of glucose- rather than glutamine-derived carbon for anaplerosis [93]. Low glutamine conditions render glioblastoma cells completely dependent on PC for proliferation; reciprocally, glucose deprivation causes them to become dependent on GLUD1, presumably as a mediator of glutamine-dependent anaplerosis [94]. These studies provide insight into the possibility of inhibiting glutamine-dependent TCA cycle anaplerosis (e.g., with 968 or BPTES) and indicate that high expression of PC could represent a means of resistance to GLS inhibitors.

In c-Myc-induced human Burkitt lymphoma P493 cells, entry of glucose-derived carbon into the TCA cycle is attenuated under hypoxia, whereas glutamine oxidation via the TCA cycle persists [95]. Upon complete withdrawal of glucose, the TCA cycle continues to function and is driven by glutamine. The proportions of viable and proliferating cell populations are almost identical in glucose-replete and -deplete conditions so long as glutamine is present. Inhibition of GLS by BPTES causes a decrease in ATP and glutathione levels, with a simultaneous increase in reactive oxygen species production. Strikingly, whereas BPTES treatment under aerobic conditions suppresses proliferation, under hypoxic conditions it results in cell death, an effect ascribed to glutamine’s critical roles in alleviating oxidative stress in addition to supporting bioenergetics.

In addition to deamidation, glutamine-derived carbon can also reach the TCA cycle through transamination [96], and recent studies indicate that inhibition of this process could be a promising strategy for cancer treatment [30,97,98]. The transaminase inhibitor amino-oxyacetate selectively suppresses proliferation of the aggressive breast cancer cell line MDA-MB-231 relative to normal human mammary epithelial cells, and similar effects were observed with siRNA knockdown of aspartate transaminase [97]. Treatment with amino-oxyacetate killed glutamine-dependent glioblastoma cells, in a manner that could be rescued by α-KG and was dependent on c-Myc expression [13]. Transaminase inhibitors have also been found to suppress both anchorage-dependent and anchorage-independent growth of lung carcinoma cells [98].

Reductive carboxylation

The central metabolic precursor for fatty acid biosynthesis is acetyl-CoA, which can be generated from pyruvate in the mitochondria by pyruvate dehydrogenase. Since acetyl-CoA cannot cross the inner mitochondrial membrane, it is exported to the cytosol via the citrate shuttle following its condensation with oxaloacetate in the TCA cycle (Figure 3). In the cytosol, citrate is converted back to acetyl-CoA and oxaloacetate in a reaction catalyzed by ATP citrate lyase. In addition to its synthesis from glycolytic pyruvate, citrate can also be generated by reductive carboxylation of α-KG [99]. Across a range of cancer cell lines, 10–25% of lipogenic acetyl-CoA is generated from glutamine via this reductive pathway; indeed, reductive metabolism is the primary route for incorporation of glutamine, glutamate and α-KG carbon into lipids [32]. Some of the reductive carboxylation of α-KG is catalyzed by cytosolic IDH1, as well as by mitochondrial IDH2 and/or IDH3.

In A549 lung carcinoma cells, glutamine dependence and reductive carboxylation flux increases under hypoxic conditions [32,34], such that glutamine-derived α-KG accounts for approximately 80% of the carbon used for de novo lipogenesis. Similarly, in melanoma cells, the major source of carbon for acetyl-CoA, citrate and fatty acids switches from glucose under normoxia to glutamine (via reductive carboxylation) under hypoxia [31]. The hypoxic switch to reductive glutamine metabolism is dependent on HIF, and constitutive activation of HIF is sufficient to induce the preferential reductive metabolism of α-KG even under normoxic conditions [32]. Tumor cells with mitochondrial defects, such as electron-transport chain mutations/inhibition, also use glutamine-dependent reductive carboxylation as the major pathway for citrate generation, and loss of electron-transport chain activity is sufficient to induce a switch from glucose to glutamine as the primary source of lipogenic carbon [33].

Together these studies indicate that mitochondrial defects/inhibition, and/or hypoxia, might sensitize cancer cells to inhibition of GLS. The fact that P493 cells are more sensitive to BPTES under hypoxic conditions could in part be explained by an increased reliance on glutamine-dependent reductive carboxylation for lipogenesis [95]. Intriguingly, cancer cells harboring neoenzymatic mutations in IDH1, which results in production of the oncometabolite 2-hydroxyglutarate, are also sensitized to GLS inhibition [100]. 2-hydroxyglutarate is generated primarily from glutamine-derived α-KG [100,101], and therefore tumors expressing mutant IDH might be especially susceptible to alterations in α-KG levels.

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As with all therapies, the potential side effects of strategies impacting glutamine metabolism must be seriously considered. The widespread use of l-asparaginase to lower plasma asparagine and glutamine concentrations in ALL patients demonstrates the potential for glutamine metabolism to be safely targeted, and also sheds light on potential toxicological consequences. For example, glutamine is known to be essential for the proliferation of lymphocytes, macrophages and neutrophils, and immunosuppression is a known side effect of l-asparaginase treatment, requiring close monitoring [11,105]. Evidence from early trials using glutamine-mimetic anti-metabolites, such as l-DON, indicates that these unselective molecules can cause excessive gastrointestinal toxicity and neurotoxicity. Within the brain, GLS converts glutamine into the neurotransmitter glutamate in neurons; astrocytes then take up synaptically released glutamate and convert it back to glutamine, which is subsequently transported back to neurons [106,107].

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It has become clear during the past decade that altered metabolism plays a critical, in some cases even causal, role in the development and maintenance of cancers. It is now accepted that virtually all oncogenes and tumor suppressors impact metabolic pathways [5]. Furthermore, mutations in certain metabolic enzymes (e.g., isocitrate dehydrogenase, succinate dehydrogenase and fumarate hydratase) are associated with both familial and sporadic human cancers [113]. With this realization has come a renewed interest in the possibility of selectively targeting the metabolism of cancer cells as a therapeutic strategy. The use of l-asparaginase to treat ALL by depleting plasma asparagine and glutamine levels and the promising outcome of the first use of dichloroacetate (which acts, at least in part, through its inhibition of the metabolic enzyme pyruvate dehydrogenase kinase) in glioblastoma patients [114,115], support the notion that cancer metabolism can be safely and effectively targeted in the clinic. The metabolic adaptations of cancer cells must balance the requirements for modestly increased ATP synthesis, dramatically upregulated macromolecular biosynthesis and maintenance of redox balance. By serving as a carbon source for energy generation, a carbon and nitrogen source for biosynthesis and a precursor of the cellular antioxidant glutathione, glutamine is able to contribute to each of these requirements.

The countless combinations of genetic alterations that are found in human neo-plasias mean that there is not a single rigid metabolic program that is characteristic of all transformed cells. This perhaps explains why some current anti-metabolite chemotherapies (e.g., those targeting nucleotide synthesis) are effective only for certain malignancies. A deeper understanding of the metabolic alterations within specific genetic contexts will allow for better-targeted therapeutic interventions. Furthermore, it seems highly likely that combination therapies based on drug synergisms will be especially important for exploiting therapeutic windows within which cancer cells, but not normal cells, are impacted [37]. Glucose and glutamine metabolic pathways, for example, might be able to compensate for one another under some circumstances. When glucose metabolism is impaired in glioblastoma cells, glutamine catabolism becomes essential for survival [94]; reciprocally, suppression of GLS expression causes cells to become fully dependent on glucose-driven TCA cycle anaplerosis via PC [93]. The implication is that PC inhibition could synergize with GLS inhibition.

A topic warranting further investigation is the role that GLS2 plays in cellular metabolism. GLS, in particular the GAC isoform, is upregulated downstream of oncogenes and downregulated by tumor suppressors, and is essential for growth of many cancer cells. In contrast, GLS2 is activated by the ‘universal’ tumor suppressor p53, and furthermore is significantly downregulated in liver tumors and can block transformed characteristics of some cancer cells when overexpressed [116118]. Emphasizing the importance of genetic context, it was recently reported that GLS2 is significantly upregulated in neuroblastomas overexpressing N-Myc [119]. There are various possible explanations for the apparently different roles of two enzymes that catalyze the same reaction. Because the regulation of GLS and GLS2 is distinct, they will be called up under different conditions. The two enzymes have different kinetic characteristics, and therefore might influence energy metabolism and antioxidant defense in different manners [20]. There is also evidence that GLS2 may act, directly or indirectly, as a transcription factor [118]. Finally, it is possible that the different interactions of GLS and GLS2 with other proteins are responsible for their apparently different roles.

 

Mitochondria as biosynthetic factories for cancer proliferation

Christopher S Ahn and Christian M Metallo

Cancer & Metabolism (2015) 3:1      http://dx.doi.org:/10.1186/s40170-015-0128-2

Unchecked growth and proliferation is a hallmark of cancer, and numerous oncogenic mutations reprogram cellular metabolism to fuel these processes. As a central metabolic organelle, mitochondria execute critical biochemical functions for the synthesis of fundamental cellular components, including fatty acids, amino acids, and nucleotides. Despite the extensive interest in the glycolytic phenotype of many cancer cells, tumors contain fully functional mitochondria that support proliferation and survival. Furthermore, tumor cells commonly increase flux through one or more mitochondrial pathways, and pharmacological inhibition of mitochondrial metabolism is emerging as a potential therapeutic strategy in some cancers. Here, we review the biosynthetic roles of mitochondrial metabolism in tumors and highlight specific cancers where these processes are activated.

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Recent characterizations of metabolic enzymes as tumor suppressors and oncogene-driven metabolic reprogramming have reinvigorated interest in cancer metabolism. Although therapies targeting metabolic processes have long been a staple in cancer treatment (e.g. inhibition of folate metabolism via methotrexate), the focused therapeutic potential surrounding these findings have generated a renewed appreciation for Otto Warburg’s work almost a century ago. Warburg observed that tumor cells ferment much of the glucose taken up during growth to lactate, thus using glycolysis as a major means of adenosine triphosphate (ATP) regeneration [1]. However, the observation of decreased respiration in cancer cells and idea that “the respiration of all cancer cells is damaged” belies the critical role of mitochondria in biosynthesis and cell survival [1]. On the contrary, functional mitochondria are present in all proliferative cells within our body (including all tumors), as they are responsible for converting the diverse nutrients available to cells into the fundamental building blocks required for cell growth. These organelles execute numerous functions in cancer cells to promote tumor growth and survival in response to stress. Here, we outline the critical biosynthetic functions served by mitochondria within tumors (Figure 1). Although many of these functions are similarly important in normal, proliferating cells, we have attempted to highlight potential points where mitochondrial metabolism may be therapeutically targeted to slow cancer growth. This review is organized by specific metabolic pathways or processes (i.e., glucose metabolism and lipogenesis, amino acid metabolism, and nucleotide biosynthesis). Tumors or cancer cell types where enzymes in each pathway have been specifically observed to by dysregulated are described within the text and summarized in Table 1.

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Figure 1

Biosynthetic nodes within mitochondria. Metabolic pathways within mitochondria that contribute to biosynthesis in cancer and other proliferating cells. TCA metabolism and FOCM enable cells to convert carbohydrates and amino acids to lipids, non-essential amino acids, nucleotides (including purines used for cofactor synthesis), glutathione, heme, and other cellular components. Critical biosynthetic routes are indicated by yellow arrows. Enzymatic reactions that are dependent on redox-sensitive cofactors are depicted in red.  https://static-content.springer.com/image/art%3A10.1186%2Fs40170-015-0128-2/MediaObjects/40170_2015_128_Fig1_HTML.gif

Table 1

Overview of mitochondrial biosynthetic enzymes important in cancer

TCA cycle, anaplerosis, and AcCoA metabolism

Cancers in which three or more mitochondrial enzymes have been studied and found to be differentially regulated (or mutated, as indicated) in cancers vs. control groups are included. Dysregulation of each enzyme was demonstrated in clinical tumors samples, animal models, or cell lines at the levels of genes, mRNA, protein, metabolites, and/or flux.

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Figure 2

Coordination of carbon and nitrogen metabolism across amino acids. Glutamate and aKG are key substrates in numerous transamination reactions and can also serve as precursors for glutamine, proline, and the TCA cycle. Mitochondrial enzymes catalyzing these reactions are highlighted in blue, and TCA cycle intermediates are highlighted in orange (pyruvate enters the TCA cycle as acetyl-CoA or oxaloacetate).
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Figure 3

Biosynthetic sources for purine and pyrimidine synthesis. Sources and fates of nitrogen, carbon, and oxygen atoms are colored as indicated. Italicized metabolites can be sourced from the mitochondria or cytosol. The double bond formed by the action of DHODH/ubiquinone is also indicated.      https://static-content.springer.com/image/art%3A10.1186%2Fs40170-015-0128-2/MediaObjects/40170_2015_128_Fig3_HTML.gif

Mitochondria operate as both engine and factory in eukaryotes, coordinating cellular energy production and the availability of fundamental building blocks that are required for cell proliferation. Cancer cells must therefore balance their relative bioenergetic and biosynthetic needs to grow, proliferate, and survive within the physical constraints of energy and mass conservation. In contrast to quiescent cells, which predominantly use oxidative mitochondrial metabolism to produce ATP and uptake glucose at much lower rates than proliferating cells, tumor cells exhibit increased glycolytic rates to provide an elevated flux of substrate for biosynthetic pathways, including those executed within mitochondria. Given these higher rates of nutrient utilization, metabolic flux through mitochondrial pathways and the associated ROS production can often be higher in cancer cells. Not surprisingly, activation of cellular antioxidant response pathways is commonly observed in cancer or subpopulations of cells within tumors [46,78]. Cellular compartmentalization affords a degree of protection from such damaging side products of metabolism, and methods which are able to deconvolute the relative contributions of each cellular compartment (e.g. mitochondria, cytosol, peroxisome, etc.) to cancer metabolism will be crucial to more completely understand the metabolism of cancer cells in the future [74,79]. Ultimately, while mitochondrial dysregulation is widely considered to be a hallmark of cancer, numerous mitochondrial functions remain critical for tumor growth and are emerging as clinical targets.

Following this point, it comes as no surprise that mitochondrial metabolism is highly active in virtually all tumors (i.e., cancer cells, stroma, or both), and investigators have begun targeting these pathways to explore potential efficacy. Indeed, some evidence suggests that biguanides such as metformin or phenformin may limit tumor incidence and burden in humans and animals [80,81]. These effects are presumably due, at least in part, to complex I inhibition of the ETC, which significantly perturbs mitochondrial function [82,83]. However, more insights are needed into the mechanisms of these compounds in patients to determine the therapeutic potential of targeting this and other components of mitochondria. In developing new therapies that target cancer metabolism, researchers will face challenges similar to those that are relevant for many established chemotherapies since deleterious effects on normal proliferating cells that also depend on mitochondrial metabolism (and aerobic glycolysis) are likely to arise.

As we acquire a more detailed picture of how specific genetic modifications in a patient’s tumor correlate with its metabolic profile, opportunities for designing targeted or combinatorial therapies will become increasingly apparent. Cancer therapies that address tumor-specific mitochondrial dysregulation and dysfunction may be particularly effective. For example, some cancer cells harbor mutations in TCA enzymes (e.g., FH, SDH, IDH2) or regulatory proteins that control mitophagy (i.e., LKB1) [84]. Such tumors may be compromised with respect to some aspects of mitochondrial biosynthesis and dependent on alternate pathways for growth and/or survival such that synthetically lethal targets emerge. Ultimately, such strategies will require clinicians and researchers to coordinate metabolic, biochemical, and genetic information in the design of therapeutic strategies.

 

David Terrano, M.D., Ph.D. commented on your update
“Not well versed in Nat peptides so I could not say. I also hesitate with any PNAS paper because those in their academy tend to have a fast track to publication. It has been that way since at least early 2000’s wh n I began research. I don’t doubt their goal and approach (this same group leads the way in methylation-based diagnosis of CNS neoplasms, which is apparently highly accurate). But when I see “dying cells” I know what that means biochemically and look for those hallmarks. Organ specific oligonucleosomes would be a nice cell death surrogate. “

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Schizophrenia, broken-links

Larry H. Bernstein, MD, FCAP, Curator

LPBI

 

Runs in the Family

 New findings about schizophrenia rekindle old questions about genes and identity.
BY Annals of Science MARCH 28, 2016 ISSUE      http://www.newyorker.com/magazine/2016/03/28/the-genetics-of-schizophrenia

http://www.newyorker.com/wp-content/uploads/2016/03/160328_r27877-690.jpg

The author and his father have seen several relatives succumb to mental illness.CREDIT PHOTOGRAPH BY DAYANITA SINGH FOR THE NEW YORKER

In the winter of 2012, I travelled from New Delhi, where I grew up, to Calcutta to visit my cousin Moni. My father accompanied me as a guide and companion, but he was a sullen and brooding presence, lost in a private anguish. He is the youngest of five brothers, and Moni is his firstborn nephew—the eldest brother’s son. Since 2004, Moni, now fifty-two, has been confined to an institution for the mentally ill (a “lunatic home,” as my father calls it), with a diagnosis of schizophrenia. He is kept awash in antipsychotics and sedatives, and an attendant watches, bathes, and feeds him through the day.

My father has never accepted Moni’s diagnosis. Over the years, he has waged a lonely campaign against the psychiatrists charged with his nephew’s care, hoping to convince them that their diagnosis was a colossal error, or that Moni’s broken psyche would somehow mend itself. He has visited the institution in Calcutta twice—once without warning, hoping to see a transformed Moni, living a secretly normal life behind the barred gates. But there was more than just avuncular love at stake for him in these visits. Moni is not the only member of the family with mental illness. Two of my father’s four brothers suffered from various unravellings of the mind. Madness has been among the Mukherjees for generations, and at least part of my father’s reluctance to accept Moni’s diagnosis lies in a grim suspicion that something of the illness may be buried, like toxic waste, in himself.

Rajesh, my father’s third-born brother, had once been the most promising of the Mukherjee boys—the nimblest, the most charismatic, the most admired. But in the summer of 1946, at the age of twenty-two, he began to behave oddly, as if a wire had been tripped in his brain. The most obvious change in his personality was a volatility: good news triggered uncontained outbursts of joy; bad news plunged him into inconsolable desolation. By that winter, the sine curve of Rajesh’s psyche had tightened in its frequency and gained in its amplitude. My father recalls an altered brother: fearful at times, reckless at others, descending and ascending steep slopes of mood, irritable one morning and overjoyed the next. When Rajesh received news of a successful performance on his college exams, he vanished, elated, on a two-night excursion, supposedly “exercising” at a wrestling camp. He was feverish and hallucinating when he returned, and died of pneumonia soon afterward. Only years later, in medical school, did I realize that Rajesh was likely in the throes of an acute manic phase. His mental breakdown was the result of a near-textbook case of bipolar disorder.

Jagu, the fourth-born of my father’s siblings, came to live with us in Delhi in 1975, when I was five years old and he was forty-five. His mind, too, was failing. Tall and rail thin, with a slightly feral look in his eyes and a shock of matted, overgrown hair, he resembled a Bengali Jim Morrison. Unlike Rajesh, whose illness had surfaced in his twenties, Jagu had been troubled from his adolescence. Socially awkward, withdrawn from everyone except my grandmother, he was unable to hold a job or live by himself. By 1975, he had visions, phantasms, and voices in his head that told him what to do. He was still capable of extraordinary bursts of tenderness—when I accidentally smashed a beloved Venetian vase at home, he hid me in his bedclothes and informed my mother that he had “mounds of cash” stashed away, enough to buy “a thousand” replacement vases. But this episode was symptomatic: even his love for me extended the fabric of his psychosis and confabulation.

Unlike Rajesh, Jagu was formally diagnosed. In the late nineteen-seventies, a physician in Delhi examined him and determined that he had schizophrenia. But no medicines were prescribed. Instead, Jagu continued to live at home, half hidden away in my grandmother’s room. (As in many families in India, my grandmother lived with us.) For nearly a decade, she and my father maintained a fragile truce, with Jagu living under her care, eating meals in her room and wearing clothes that she stitched for him. At night, when Jagu was consumed by his fears and fantasies, she put him to bed like a child, with her hand on his forehead. She was his nurse, his housekeeper, his only friend, and, more important, his public defender. When my grandmother died, in 1985, Jagu joined a religious sect in Delhi and disappeared, until his death, a dozen years later.

……

at schizophrenia runs in families was evident even to the person who first defined the illness. In 1911, Eugen Bleuler, a Swiss-German psychiatrist, published a book describing a series of cases of men and women, typically in their teens and early twenties, whose thoughts had begun to tangle and degenerate. “In this malady, the associations lose their continuity,” Bleuler wrote. “The threads between thoughts are torn.” Psychotic visions and paranoid thoughts flashed out of nowhere. Some patients “feel themselves weak, their spirit escapes, they will never survive the day. There is a growth in their heads. Their bones have turned liquid; their hearts have turned into stone. . . . The patient’s wife must not use eggs in cooking, otherwise he will grow feathers.” His patients were often trapped between flickering emotional states, unable to choose between two radically opposed visions, Bleuler noted. “You devil, you angel, you devil, you angel,” one woman said to her lover.

Bleuler tried to find an explanation for the mysterious symptoms, but there was only one seemingly common element: schizophrenic patients tended to have first-degree relatives who were also schizophrenic. He had no tools to understand the mechanism behind the heredity. The word “gene” had been coined just two years before Bleuler published his book. The notion that a mental illness could be carried across generations by unitary, indivisible factors—corpuscles of information threading through families—would have struck most of Bleuler’s contemporaries as mad in its own right. Still, Bleuler was astonishingly prescient about the complex nature of inheritance. “If one is looking for ‘theheredity,’ one can nearly always find it,” he wrote. “We will not be able to do anything about it even later on, unless the single factor of heredity can be broken down into many hereditary factors along specific lines.”

In the nineteen-sixties, Bleuler’s hunch was confirmed by twin studies. Psychiatrists determined that if an identical twin was schizophrenic the other twin had a forty-to-fifty-per-cent chance of developing the disease—fiftyfold higher than the risk in the general population. By the early two-thousands, large population studies had revealed a strong genetic link between schizophrenia and bipolar disorder. Some of the families described in these studies had a crisscrossing history that was achingly similar to my own: one sibling affected with schizophrenia, another with bipolar disorder, and a nephew or niece also schizophrenic.

“The twin studies clarified two important features of schizophrenia and bipolar disorder,” Jeffrey Lieberman, a Columbia University psychiatrist who has studied schizophrenia for thirty years, told me. “First, it was clear that there wasn’t a single gene, but dozens of genes involved in causing schizophrenia—each perhaps exerting a small effect. And, second, even if you inherited the entire set of risk genes, as identical twins do, you still might not develop the disease. Obviously, there were other triggers or instigators involved in releasing the illness.” But while these studies established that schizophrenia had a genetic basis, they revealed nothing about the nature of the genes involved. “For doctors, patients, and families in the schizophrenia community, genetics became the ultimate mystery,” Lieberman said. “If we knew the identity of the genes, we would find the causes, and if we found the causes we could find medicines.”

In 2006, an international consortium of psychiatric geneticists launched a genomic survey of schizophrenia, hoping to advance the search for the implicated genes. With 3,322 patients and 3,587 controls, this was one of the largest and most rigorous such studies in the history of the disease. Researchers scanned through the nearly seven thousand genomes to find variations in gene segments that were correlated with schizophrenia. This strategy, termed an “association study,” does not pinpoint a gene, but it provides a general location where a disease-linked gene may be found, like a treasure map with a large “X” scratched in a corner of the genome.

The results, reported in 2009 (and updated in 2014) in the journal Nature, were a dispiriting validation of Bleuler’s hunch about multiple hereditary factors: more than a hundred independent segments of the genome were associated with schizophrenia. “There are lots of small, common genetic effects, scattered across the genome,” one researcher said. “There are many different biological processes involved.” Some of the putative culprits made biological sense—if dimly. There were genes linked to transmitters that relay messages between neurons, and genes for molecular channels that move electrical signals up and down nerve cells. But by far the most surprising association involved a gene segment on chromosome 6. This region of the genome—termed the MHC region—carries hundreds of genes typically associated with the immune system.

“The MHC-segment finding was so strange and striking that you had to sit up and take notice,” Lieberman told me. “Here was the most definitive evidence that something in the immune system might have something to do with schizophrenia. There had been hints about an immunological association before, but this was impossible to argue with. It raised an endlessly fascinating question: what was the link between immune-response genes and schizophrenia?”

The Rogue Immune Cells That Wreck the Brain

Beth Stevens thinks she has solved a mystery behind brain disorders such as Alzheimer’s and schizophrenia.

by Adam Piore   April 4, 2016            https://www.technologyreview.com/s/601137/the-rogue-immune-cells-that-wreck-the-brain/

In the first years of her career in brain research, Beth Stevens thought of microglia with annoyance if she thought of them at all. When she gazed into a microscope and saw these ubiquitous cells with their spidery tentacles, she did what most neuroscientists had been doing for generations: she looked right past them and focused on the rest of the brain tissue, just as you might look through specks of dirt on a windshield.

“What are they doing there?” she thought. “They’re in the way.’”

Stevens never would have guessed that just a few years later, she would be running a laboratory at Harvard and Boston’s Children’s Hospital devoted to the study of these obscure little clumps. Or that she would be arguing in the world’s top scientific journals that microglia might hold the key to understanding not just normal brain development but also what causes Alzheimer’s, Huntington’s, autism, schizophrenia, and other intractable brain disorders.

Microglia are part of a larger class of cells—known collectively as glia—that carry out an array of functions in the brain, guiding its development and serving as its immune system by gobbling up diseased or damaged cells and carting away debris. Along with her frequent collaborator and mentor, Stanford biologist Ben Barres, and a growing cadre of other scientists, Stevens, 45, is showing that these long-overlooked cells are more than mere support workers for the neurons they surround. Her work has raised a provocative suggestion: that brain disorders could somehow be triggered by our own bodily defenses gone bad.

A type of glial cell known as an oligodendrocyte

In one groundbreaking paper, in January, Stevens and researchers at the Broad Institute of MIT and Harvard showed that aberrant microglia might play a role in schizophrenia—causing or at least contributing to the massive cell loss that can leave people with devastating cognitive defects. Crucially, the researchers pointed to a chemical pathway that might be targeted to slow or stop the disease. Last week, Stevens and other researchers published a similar finding for Alzheimer’s.

This might be just the beginning. Stevens is also exploring the connection between these tiny structures and other neurological diseases—work that earned her a $625,000 MacArthur Foundation “genius” grant last September.

All of this raises intriguing questions. Is it possible that many common brain disorders, despite their wide-ranging symptoms, are caused or at least worsened by the same culprit, a component of the immune system? If so, could many of these disorders be treated in a similar way—by stopping these rogue cells?

Nature. 2016 Feb 11;530(7589):177-83. http://dx.doi.org:/10.1038/nature16549. Epub 2016 Jan 27.   Schizophrenia risk from complex variation of complement component 4.

Schizophrenia is a heritable brain illness with unknown pathogenic mechanisms. Schizophrenia’s strongest genetic association at a population level involves variation in the major histocompatibility complex (MHC) locus, but the genes and molecular mechanisms accounting for this have been challenging to identify. Here we show that this association arises in part from many structurally diverse alleles of the complement component 4 (C4) genes. We found that these alleles generated widely varying levels of C4A and C4B expression in the brain, with each common C4 allele associating with schizophrenia in proportion to its tendency to generate greater expression of C4A. Human C4 protein localized to neuronal synapses, dendrites, axons, and cell bodies. In mice, C4 mediated synapse elimination during postnatal development. These results implicate excessive complement activity in the development of schizophrenia and may help explain the reduced numbers of synapses in the brains of individuals with schizophrenia.

 

Science  31 Mar 2016;        http://dx.doi.org:/10.1126/science.aad8373      Complement and microglia mediate early synapse loss in Alzheimer mouse models.
Soyon Hong1Victoria F. Beja-Glasser1,*Bianca M. Nfonoyim1,*,…., Ben A. Barres6Cynthia A. Lemere,2Dennis J. Selkoe2,7Beth Stevens1,8,

 Synapse loss in Alzheimer’s disease (AD) correlates with cognitive decline. Involvement of microglia and complement in AD has been attributed to neuroinflammation, prominent late in disease. Here we show in mouse models that complement and microglia mediate synaptic loss early in AD. C1q, the initiating protein of the classical complement cascade, is increased and associated with synapses before overt plaque deposition. Inhibition of C1q, C3 or the microglial complement receptor CR3, reduces the number of phagocytic microglia as well as the extent of early synapse loss. C1q is necessary for the toxic effects of soluble β-amyloid (Aβ) oligomers on synapses and hippocampal long-term potentiation (LTP). Finally, microglia in adult brains engulf synaptic material in a CR3-dependent process when exposed to soluble Aβ oligomers. Together, these findings suggest that the complement-dependent pathway and microglia that prune excess synapses in development are inappropriately activated and mediate synapse loss in AD.
Genome-wide association studies (GWAS) implicate microglia and complement-related pathways in AD (1). Previous research has demonstrated both beneficial and detrimental roles of complement and microglia in plaque-related neuropathology (2, 3); however, their roles in synapse loss, a major pathological correlate of cognitive decline in AD (4), remain to be identified. Emerging research implicates microglia and immune-related mechanisms in brain wiring in the healthy brain (1). During development, C1q and C3 localize to synapses and mediate synapse elimination by phagocytic microglia (57). We hypothesized that this normal developmental synaptic pruning pathway is activated early in the AD brain and mediates synapse loss.

 

Complex machinery

It’s not surprising that scientists for years have ignored microglia and other glial cells in favor of neurons. Neurons that fire together allow us to think, breathe, and move. We see, hear, and feel using neurons, and we form memories and associations when the connections between different neurons strengthen at the junctions between them, known as synapses. Many neuroscientists argue that neurons create our very consciousness.

Glia, on the other hand, have always been considered less important and interesting. They have pedestrian duties such as supplying nutrients and oxygen to neurons, as well as mopping up stray chemicals and carting away the garbage.

Scientists have known about glia for some time. In the 1800s, the pathologist Rudolf Virchow noted the presence of small round cells packing the spaces between neurons and named them “nervenkitt” or “neuroglia,” which can be translated as nerve putty or glue. One variety of these cells, known as astrocytes, was defined in 1893. And then in the 1920s, the Spanish scientist Pio del Río Hortega developed novel ways of staining cells taken from the brain. This led him to identify and name two more types of glial cells, including microglia, which are far smaller than the others and are characterized by their spidery shape and multiple branches. It is only when the brain is damaged in adulthood, he suggested, that microglia spring to life—rushing to the injury, where it was thought they helped clean up the area by eating damaged and dead cells. Astrocytes often appeared on the scene as well; it was thought that they created scar tissue.

This emergency convergence of microglia and astrocytes was dubbed “gliosis,” and by the time Ben Barres entered medical school in the late 1970s, it was well established as a hallmark of neurodegenerative diseases, infection, and a wide array of other medical conditions. But no one seemed to understand why it occurred. That intrigued Barres, then a neurologist in training, who saw it every time he looked under a microscope at neural tissue in distress. “It was just really fascinating,” he says. “The great mystery was: what is the point of this gliosis? Is it good? Is it bad? Is it driving the disease process, or is it trying to repair the injured brain?”

 https://youtu.be/6DOYTpXkLOY

Barres began looking for the answer. He learned how to grow glial cells in a dish and apply a new recording technique to them. He could measure their electrical qualities, which determine the biochemical signaling that all brain cells use to communicate and coördinate activity.

“From the second I started recording the glial cells, I thought ‘Oh, my God!’” Barres recalls. The electrical activity was more dynamic and complex than anyone had thought. These strange electrical properties could be explained only if the glial cells were attuned to the conditions around them, and to the signals released from nearby neurons. Barres’s glial cells, in other words, had all the machinery necessary to engage in a complex dialogue with neurons, and presumably to respond to different kinds of conditions in the brain.

Why would they need this machinery, though, if they were simply involved in cleaning up dead cells? What could they possibly be doing? It turns out that in the absence of chemicals released by glia, the neurons committed the biochemical version of suicide. Barres also showed that the astrocytes appeared to play a crucial role in forming synapses, the microscopic connections between neurons that encode memory. In isolation, neurons were capable of forming the spiny appendages necessary to reach the synapses. But without astrocytes, they were incapable of connecting to one another.

Hardly anyone believed him. When he was a young faculty member at Stanford in the 1990s, one of his grant applications to the National Institutes of Health was rejected seven times. “Reviewers kept saying, ‘Nah, there’s no way glia could be doing this,’” Barres recalls. “And even after we published two papers in Science showing that [astrocytes] had profound, almost all-or-nothing effects in controlling synapses’ formation or synapse activity, I still couldn’t get funded! I think it’s still hard to get people to think about glia as doing anything active in the nervous system.”

Marked for elimination

Beth Stevens came to study glia by accident. After graduating from Northeastern University in 1993, she followed her future husband to Washington, D.C., where he had gotten work in the U.S. Senate. Stevens had been pre-med in college and hoped to work in a lab at the National Institutes of Health. But with no previous research experience, she was soundly rebuffed. So she took a job waiting tables at a Chili’s restaurant in nearby Rockville, Maryland, and showed up at NIH with her résumé every week.

After a few months, Stevens received a call from a researcher named Doug Fields, who needed help in his lab. Fields was studying the intricacies of the process in which neurons become insulated in a coating called myelin. That insulation is essential for the transmission of electrical impulses.

As Stevens spent the following years pursuing a PhD at the University of Maryland, she was intrigued by the role that glial cells played in insulating neurons. Along the way, she became familiar with other insights into glial cells that were beginning to emerge, especially from the lab of Ben Barres. Which is why, soon after completing her PhD in 2003, Stevens found herself a postdoc in Barres’s lab at Stanford, about to make a crucial discovery.

Barres’s group had begun to identify the specific compounds astrocytes secreted that seemed to cause neurons to grow synapses. And eventually, they noticed that these compounds also stimulated production of a protein called C1q.

Conventional wisdom held that C1q was activated only in sick cells—the protein marked them to be eaten up by immune cells—and only outside the brain. But Barres had found it in the brain. And it was in healthy neurons that were arguably at their most robust stage: in early development. What was the C1q protein doing there?

https://d267cvn3rvuq91.cloudfront.net/i/images/glia33.jpg?sw=590&cx=0&cy=0&cw=2106&ch=2106

A stained astrocyte.

The answer lies in the fact that marking cells for elimination is not something that happens only in diseased brains; it is also essential for development. As brains develop, their neurons form far more synaptic connections than they will eventually need. Only the ones that are used are allowed to remain. This pruning allows for the most efficient flow of neural transmissions in the brain, removing noise that might muddy the signal.

But it was unknown how exactly the process worked. Was it possible that C1q helped signal the brain to prune unused synapses? Stevens focused her postdoctoral research on finding out. “We could have been completely wrong,” she recalls. “But we went for it.”

It paid off. In a 2007 paper, Barres and Stevens showed that C1q indeed plays a role in eliminating unneeded neurons in the developing brain. And they found that the protein is virtually absent in healthy adult neurons.

Now the scientists faced a new puzzle. Does C1q show up in brain diseases because the same mechanism involved in pruning a developing brain later goes awry? Indeed, evidence was already growing that one of the earliest events in neurodegenerative diseases such as Alzheimer’s, Parkinson’s, and Huntington’s was significant loss of synapses.

When Stevens and Barres examined mice bred to develop glaucoma, a neurodegenerative disease that kills neurons in the optic system, they found that C1q appeared long before any other detectable sign that the disease was taking hold. It cropped up even before the cells started dying.

This suggested the immune cells might in fact cause the disease, or at the very least accelerate it. And that offered an intriguing possibility: that something could be made to halt the process. Barres founded a company, Annexon Biosciences, to develop drugs that could block C1q. Last week’s paper published by Barres, Stevens, and other researchers shows that a compound being tested by Annexon appears to be able to prevent the onset of Alzheimer’s in mice bred to develop the disease. Now the company hopes to test it in humans in the next two years.

Paths to treatments

To better understand the process that C1q helps trigger, Stevens and Barres wanted to figure out what actually plays the role of Pac-Man, eating up the synapses marked for death. It was well known that white blood cells known as macrophages gobbled up diseased cells and foreign invaders in the rest of the body. But macrophages are not usually present in the brain. For their theory to work, there had to be some other mechanism. And further research has shown that the cells doing the eating even in healthy brains are those mysterious clusters of material that Beth Stevens, for years, had been gazing right past in the microscope—the microglia that Río Hortega identified almost 100 years ago.

Now Stevens’s lab at Harvard, which she opened in 2008, devotes half its efforts to figuring out what microglia are doing and what causes them to do it. These cells, it turns out, appear in the mouse embryo at day eight, before any other brain cell, which suggests they might help guide the rest of brain development—and could contribute to any number of neurodevelopmental diseases when they go wrong.

Meanwhile, she is also expanding her study of the way different substances determine what happens in the brain. C1q is actually just the first in a series of proteins that accumulate on synapses marked for elimination. Stevens has begun to uncover evidence that there is a wide array of protective “don’t eat me” molecules too. It’s the balance between all these cues that regulates whether microglia are summoned to destroy synapses. Problems in any one could, conceivably, mess up the system.

Evidence is now growing that microglia are involved in several neurodevelopmental and psychiatric problems. The potential link to schizophrenia that was revealed in January emerged after researchers at the Broad Institute, led by Steven McCarroll and a graduate student named Aswin Sekar, followed a trail of genetic clues that led them directly to Stevens’s work. In 2009, three consortia from around the globe had published papers comparing DNA in people with and without schizophrenia. It was Sekar who identified a possible pattern: the more a specific type of protein was present in synapses, the higher the risk of developing the disease. The protein, C4, was closely related to C1q, the one first identified in the brain by Stevens and Barres.

McCarroll knew that schizophrenia strikes in late adolescence and early adulthood, a time when brain circuits in the prefrontal cortex undergo extensive pruning. Others had found that areas of the prefrontal cortex are among those most ravaged by the disease, which leads to massive synapse loss. Could it be that over-pruning by rogue microglia is part of what causes schizophrenia?

To find out, Sekar and McCarroll got in touch with Stevens, and the two labs began to hold joint weekly meetings. They soon demonstrated that C4 also had a role in pruning synapses in the brains of young mice, suggesting that excessive levels of the protein could indeed lead to over-pruning—and to the thinning out of brain tissue that appears to occur as symptoms such as psychotic episodes grow worse.

If the brain damage seen in Parkinson’s and Alzheimer’s stems from over-pruning that might begin early in life, why don’t symptoms of those diseases show up until later? Barres thinks he knows. He notes that the brain can normally compensate for injury by rewiring itself and generating new synapses. It also contains a lot of redundancy. That would explain why patients with Parkinson’s disease don’t show discernible symptoms until they have lost 90 percent of the neurons that produce dopamine.

It also might mean that subtle symptoms could in fact be detected much earlier. Barres points to a study of nuns published in 2000. When researchers analyzed essays the nuns had written upon entering their convents decades before, they found that women who went on to develop Alzheimer’s had shown less “idea density” even in their 20s. “I think the implication of that is they could be lifelong diseases,” Barres says. “The disease process could be going on for decades and the brain is just compensating, rewiring, making new synapses.” At some point, the microglia are triggered to remove too many cells, Barres argues, and the symptoms of the disease begin to manifest fully.

Turning this insight into a treatment is far from straightforward, because much remains unclear. Perhaps an overly aggressive response from microglia is determined by some combination of genetic variants not shared by everyone. Stevens also notes that diseases like schizophrenia are not caused by one mutation; rather, a wide array of mutations with small effects cause problems when they act in concert. The genes that control the production of C4 and other immune-system proteins may be only part of the story. That may explain why not everyone who has a C4 mutation will go on to develop schizophrenia.

Nonetheless, if Barres and Stevens are right that the immune system is a common mechanism behind devastating brain disorders, that in itself is a fundamental breakthrough. Because we have not known the mechanisms that trigger such diseases, medical researchers have been able only to alleviate the symptoms rather than attack the causes. There are no drugs available to halt or even slow neurodegeneration in diseases like Alzheimer’s. Some drugs elevate neurotransmitters in ways that briefly make it easier for individuals with dementia to form new synaptic connections, but they don’t reduce the rate at which existing synapses are destroyed. Similarly, there are no treatments that tackle the causes of autism or schizophrenia. Even slowing the progress of these disorders would be a major advance. We might finally go after diseases that have run unchecked for generations.

“We’re a ways away from a cure,” Stevens says. “But we definitely have a path forward.”

Adam Piore is a freelance writer who wrote “A Shocking Way to Fix the Brain”  in November/December 2015.

 

Int Immunopharmacol. 2001 Mar;1(3):365-92.

Genetic, structural and functional diversities of human complement components C4A and C4B and their mouse homologues, Slp and C4.

Blanchong CA1Chung EKRupert KLYang YYang ZZhou BMoulds JMYu CY.

Author information

Abstract

The complement protein C4 is a non-enzymatic component of the C3 and C5 convertases and thus essential for the propagation of the classical complement pathway. The covalent binding of C4 to immunoglobulins and immune complexes (IC) also enhances the solubilization of immune aggregates, and the clearance of IC through complement receptor one (CR1) on erythrocytes. Human C4 is the most polymorphic protein of the complement system. In this review, we summarize the current concepts on the 1-2-3 loci model of C4A and C4B genes in the population, factors affecting the expression levels of C4 transcripts and proteins, and the structural, functional and serological diversities of the C4A and C4B proteins. The diversities and polymorphisms of the mouse homologues Slp and C4 proteins are described and contrasted with their human homologues. The human C4 genes are located in the MHC class III region on chromosome 6. Each human C4 gene consists of 41 exons coding for a 5.4-kb transcript. The long gene is 20.6 kb and the short gene is 14.2 kb. In the Caucasian population 55% of the MHC haplotypes have the 2-locus, C4A-C4B configurations and 45% have an unequal number of C4A and C4B genes. Moreover, three-quarters of C4 genes harbor the 6.4 kb endogenous retrovirus HERV-K(C4) in the intron 9 of the long genes. Duplication of a C4 gene always concurs with its adjacent genes RP, CYP21 and TNX, which together form a genetic unit termed an RCCX module. Monomodular, bimodular and trimodular RCCX structures with 1, 2 and 3 complement C4 genes have frequencies of 17%, 69% and 14%, respectively. Partial deficiencies of C4A and C4B, primarily due to the presence of monomodular haplotypes and homo-expression of C4A proteins from bimodular structures, have a combined frequency of 31.6%. Multiple structural isoforms of each C4A and C4B allotype exist in the circulation because of the imperfect and incomplete proteolytic processing of the precursor protein to form the beta-alpha-gamma structures. Immunofixation experiments of C4A and C4B demonstrate > 41 allotypes in the two classes of proteins. A compilation of polymorphic sites from limited C4 sequences revealed the presence of 24 polymophic residues, mostly clustered C-terminal to the thioester bond within the C4d region of the alpha-chain. The covalent binding affinities of the thioester carbonyl group of C4A and C4B appear to be modulated by four isotypic residues at positions 1101, 1102, 1105 and 1106. Site directed mutagenesis experiments revealed that D1106 is responsible for the effective binding of C4A to form amide bonds with immune aggregates or protein antigens, and H1106 of C4B catalyzes the transacylation of the thioester carbonyl group to form ester bonds with carbohydrate antigens. The expression of C4 is inducible or enhanced by gamma-interferon. The liver is the main organ that synthesizes and secretes C4A and C4B to the circulation but there are many extra-hepatic sites producing moderate quantities of C4 for local defense. The plasma protein levels of C4A and C4B are mainly determined by the corresponding gene dosage. However, C4B proteins encoded by monomodular short genes may have relatively higher concentrations than those from long C4A genes. The 5′ regulatory sequence of a C4 gene contains a Spl site, three E-boxes but no TATA box. The sequences beyond–1524 nt may be completely different as the C4 genes at RCCX module I have RPI-specific sequences, while those at Modules II, III and IV have TNXA-specific sequences. The remarkable genetic diversity of human C4A and C4B probably promotes the exchange of genetic information to create and maintain the quantitative and qualitative variations of C4A and C4B proteins in the population, as driven by the selection pressure against a great variety of microbes. An undesirable accompanying byproduct of this phenomenon is the inherent deleterious recombinations among the RCCX constituents leading to autoimmune and genetic disorders.

 

C4A isotype is responsible for effective binding to form amide bonds with immune aggregates or protein antigens, while C4B isotype catalyzes the transacylation of the thioester carbonyl group to form ester bonds with carbohydrate antigens.

Derived from proteolytic degradation of complement C4, C4a anaphylatoxin is a mediator of local inflammatory process.

 

Schizophrenia and the Synapse

Genetic evidence suggests that overactive synaptic pruning drives development of schizophrenia.

By Ruth Williams | January 27, 2016

http://www.the-scientist.com/?articles.view/articleNo/45189/title/Schizophrenia-and-the-Synapse/

Compared to the brains of healthy individuals, those of people with schizophrenia have higher expression of a gene called C4, according to a paper published inNature today (January 27). The gene encodes an immune protein that moonlights in the brain as an eradicator of unwanted neural connections (synapses). The findings, which suggest increased synaptic pruning is a feature of the disease, are a direct extension of genome-wide association studies (GWASs) that pointed to the major histocompatibility (MHC) locus as a key region associated with schizophrenia risk.

“The MHC [locus] is the first and the strongest genetic association for schizophrenia, but many people have said this finding is not useful,” said psychiatric geneticist Patrick Sullivan of the University of North Carolina School of Medicine who was not involved in the study. “The value of [the present study is] to show that not only is it useful, but it opens up new and extremely interesting ideas about the biology and therapeutics of schizophrenia.”

Schizophrenia has a strong genetic component—it runs in families—yet, because of the complex nature of the condition, no specific genes or mutations have been identified. The pathological processes driving the disease remain a mystery.

Researchers have turned to GWASs in the hope of finding specific genetic variations associated with schizophrenia, but even these have not provided clear candidates.

“There are some instances where genome-wide association will literally hit one base [in the DNA],” explained Sullivan. While a 2014 schizophrenia GWAS highlighted the MHC locus on chromosome 6 as a strong risk area, the association spanned hundreds of possible genes and did not reveal specific nucleotide changes. In short, any hope of pinpointing the MHC association was going to be “really challenging,” said geneticist Steve McCarroll of Harvard who led the new study.

Nevertheless, McCarroll and colleagues zeroed in on the particular region of the MHC with the highest GWAS score—the C4 gene—and set about examining how the area’s structural architecture varied in patients and healthy people.

The C4 gene can exist in multiple copies (from one to four) on each copy of chromosome 6, and has four different forms: C4A-short, C4B-short, C4A-long, and C4B-long. The researchers first examined the “structural alleles” of the C4 locus—that is, the combinations and copy numbers of the different C4 forms—in healthy individuals. They then examined how these structural alleles related to expression of both C4Aand C4B messenger RNAs (mRNAs) in postmortem brain tissues.

…………..

Schizophrenia risk from complex variation of complement component 4

Aswin Sekar, Allison R. Bialas, Heather de Rivera, …, Schizophrenia Working Group of the Psychiatric Genomics Consortium, Mark J. Daly, Michael C. Carroll, Beth Stevens & Steven A. McCarroll

Nature (11 Feb 2016); 530: 177–183 http://dx.doi.org:/10.1038/nature16549

Schizophrenia is a heritable brain illness with unknown pathogenic mechanisms. Schizophrenia’s strongest genetic association at a population level involves variation in the major histocompatibility complex (MHC) locus, but the genes and molecular mechanisms accounting for this have been challenging to identify. Here we show that this association arises in part from many structurally diverse alleles of the complement component 4 (C4) genes. We found that these alleles generated widely varying levels of C4A and C4B expression in the brain, with each common C4 allele associating with schizophrenia in proportion to its tendency to generate greater expression of C4A. Human C4 protein localized to neuronal synapses, dendrites, axons, and cell bodies. In mice, C4 mediated synapse elimination during postnatal development. These results implicate excessive complement activity in the development of schizophrenia and may help explain the reduced numbers of synapses in the brains of individuals with schizophrenia.

  1. Cannon, T. D. et al. Cortex mapping reveals regionally specific patterns of genetic and disease-specific gray-matter deficits in twins discordant for schizophrenia. Proc. Natl Acad. Sci. USA 99, 3228–3233 (2002)
  1. Cannon, T. D. et al. Progressive reduction in cortical thickness as psychosis develops: a multisite longitudinal neuroimaging study of youth at elevated clinical risk. Biol. Psychiatry 77,147–157 (2015)
  1. Garey, L. J. et al. Reduced dendritic spine density on cerebral cortical pyramidal neurons in schizophrenia. J. Neurol. Neurosurg. Psychiatry 65, 446–453 (1998)
  1. Glantz, L. A. & Lewis, D. A. Decreased dendritic spine density on prefrontal cortical pyramidal neurons in schizophrenia. Arch. Gen. Psychiatry 57, 65–73 (2000)
  1. Glausier, J. R. & Lewis, D. A. Dendritic spine pathology in schizophrenia. Neuroscience 251,90–107 (2013)
  1. Schizophrenia Working Group of the Psychiatric Genomics Consortium. Biological insights from 108 schizophrenia-associated genetic loci. Nature 511, 421–427 (2014)
  1. Shi, J. et al. Common variants on chromosome 6p22.1 are associated with schizophrenia. Nature 460, 753–757 (2009)
  1. Stefansson, H. et al. Common variants conferring risk of schizophrenia. Nature 460,744–747 (2009)
  1. International Schizophrenia Consortium et al. Common polygenic variation contributes to risk of schizophrenia and bipolar disorder. Nature 460, 748–752 (2009)
  1. Schizophrenia Psychiatric Genome-Wide Association Study Consortium. Genome-wide association study identifies five new schizophrenia loci. Nature Genet . 43, 969–976 (2011)

 

The strongest genetic association found in schizophrenia is its association to genetic markers across the major histocompatibility complex (MHC) locus, first described in three Nature papers in 2009. …

 

Schizophrenia: From genetics to physiology at last

Ryan S. DhindsaDavid B. Goldstein
Nature  (11 Feb 2016); 530:162–163   http://dx.doi.org:/10.1038/nature16874

  1. Schizophrenia Working Group of the Psychiatric Genomics Consortium. Nature511,421–427 (2014).
  2. Stevens, B. et alCell131, 1164–1178 (2007).
  3. Cannon, T. D. et al Psychiatry77, 147–157 (2015).
  4. Glausier, J. R. & Lewis, D. A. Neuroscience251, 90–107 (2013).
  5. Glantz, L. A. & Lewis, D. A.  Gen. Psychiatry57, 65–73 (2000).

 

 Jianxin Shi1, et al.   Common variants on chromosome 6p22.1 are associated with schizophrenia.  Nature 460, 753-757 (6 August 2009) | doi:10.1038/nature08192; Received 29 May 2009; Accepted 10 June 2009; Published online 1 July 2009; Corrected 6 August 2009

Schizophrenia, a devastating psychiatric disorder, has a prevalence of 0.5–1%, with high heritability (80–85%) and complex transmission1. Recent studies implicate rare, large, high-penetrance copy number variants in some cases2, but the genes or biological mechanisms that underlie susceptibility are not known. Here we show that schizophrenia is significantly associated with single nucleotide polymorphisms (SNPs) in the extended major histocompatibility complex region on chromosome 6. We carried out a genome-wide association study of common SNPs in the Molecular Genetics of Schizophrenia (MGS) case-control sample, and then a meta-analysis of data from the MGS, International Schizophrenia Consortium and SGENE data sets. No MGS finding achieved genome-wide statistical significance. In the meta-analysis of European-ancestry subjects (8,008 cases, 19,077 controls), significant association with schizophrenia was observed in a region of linkage disequilibrium on chromosome 6p22.1 (P = 9.54 × 10-9). This region includes a histone gene cluster and several immunity-related genes—possibly implicating aetiological mechanisms involving chromatin modification, transcriptional regulation, autoimmunity and/or infection. These results demonstrate that common schizophrenia susceptibility alleles can be detected. The characterization of these signals will suggest important directions for research on susceptibility mechanisms.

Editor’s Summary   6 August 2009
Schizophrenia risk: link to chromosome 6p22.1

A genome-wide association study using the Molecular Genetics of Schizophrenia case-control data set, followed by a meta-analysis that included over 8,000 cases and 19,000 controls, revealed that while common genetic variation that underlies risk to schizophrenia can be identified, there probably are few or no single common loci with large effects. The common variants identified here lie on chromosome 6p22.1 in a region that includes a histone gene cluster and several genes implicated in immunity.

Letter

Hreinn Stefansson1,48, et al. Common variants conferring risk of schizophrenia.
Nature 460, 744-747 (6 August 2009) | doi:10.1038/nature08186; Received 16 March 2009; Accepted 5 June 2009; Published online 1 July 2009

Schizophrenia is a complex disorder, caused by both genetic and environmental factors and their interactions. Research on pathogenesis has traditionally focused on neurotransmitter systems in the brain, particularly those involving dopamine. Schizophrenia has been considered a separate disease for over a century, but in the absence of clear biological markers, diagnosis has historically been based on signs and symptoms. A fundamental message emerging from genome-wide association studies of copy number variations (CNVs) associated with the disease is that its genetic basis does not necessarily conform to classical nosological disease boundaries. Certain CNVs confer not only high relative risk of schizophrenia but also of other psychiatric disorders1, 2, 3. The structural variations associated with schizophrenia can involve several genes and the phenotypic syndromes, or the ‘genomic disorders’, have not yet been characterized4. Single nucleotide polymorphism (SNP)-based genome-wide association studies with the potential to implicate individual genes in complex diseases may reveal underlying biological pathways. Here we combined SNP data from several large genome-wide scans and followed up the most significant association signals. We found significant association with several markers spanning the major histocompatibility complex (MHC) region on chromosome 6p21.3-22.1, a marker located upstream of the neurogranin gene (NRGN) on 11q24.2 and a marker in intron four of transcription factor 4 (TCF4) on 18q21.2. Our findings implicating the MHC region are consistent with an immune component to schizophrenia risk, whereas the association with NRGN and TCF4 points to perturbation of pathways involved in brain development, memory and cognition.

 

Letter

The International Schizophrenia Consortium. Common polygenic variation contributes to risk of schizophrenia and bipolar disorder.  Nature 460, 748-752 (6 August 2009) | doi:10.1038/nature08185; Received 11 February 2009; Accepted 8 June 2009; Published online 1 July 2009; Corrected 6 August 2009

Schizophrenia is a severe mental disorder with a lifetime risk of about 1%, characterized by hallucinations, delusions and cognitive deficits, with heritability estimated at up to 80%1, 2. We performed a genome-wide association study of 3,322 European individuals with schizophrenia and 3,587 controls. Here we show, using two analytic approaches, the extent to which common genetic variation underlies the risk of schizophrenia. First, we implicate the major histocompatibility complex. Second, we provide molecular genetic evidence for a substantial polygenic component to the risk of schizophrenia involving thousands of common alleles of very small effect. We show that this component also contributes to the risk of bipolar disorder, but not to several non-psychiatric diseases.

 

The Psychiatric GWAS Consortium Steering Committee. A framework for interpreting genome-wide association studies of psychiatric disorders.  Molecular Psychiatry (2009) 14, 10–17; doi:10.1038/mp.2008.126; published online 11 November 2008

Genome-wide association studies (GWAS) have yielded a plethora of new findings in the past 3 years. By early 2009, GWAS on 47 samples of subjects with attention-deficit hyperactivity disorder, autism, bipolar disorder, major depressive disorder and schizophrenia will be completed. Taken together, these GWAS constitute the largest biological experiment ever conducted in psychiatry (59 000 independent cases and controls, 7700 family trios and >40 billion genotypes). We know that GWAS can work, and the question now is whether it will work for psychiatric disorders. In this review, we describe these studies, the Psychiatric GWAS Consortium for meta-analyses of these data, and provide a logical framework for interpretation of some of the conceivable outcomes.

Keywords: genome-wide association, attention-deficit hyperactivity disorder, autism, bipolar disorder, major depressive disorder, schizophrenia

The purpose of this article is to consider the ‘big picture’ and to provide a logical framework for the possible outcomes of these studies. This is not a review of GWAS per se as many excellent reviews of this technically and statistically intricate methodological approach are available.789101112 This is also not a review of the advantages and disadvantages of different study designs and sampling strategies for the dissection of complex psychiatric traits. We would like to consider how the dozens of GWAS papers that will soon be in the literature can be synthesized: what can integrated mega-analyses (meta-analysis is based on summary data (for example, odds ratios) from all available studies whereas ‘mega-analysis’ uses individual-level genotype and phenotype data) of all available GWAS data tell us about the etiology of these psychiatric disorders? This is an exceptional opportunity as positive or negative results will enable us to learn hard facts about these critically important psychiatric disorders. We suggest that it is not a matter of ‘success versus failure’ or ‘optimism versus pessimism’ but rather an opportunity for systematic and logical approaches to empirical data whereby both positive and appropriately qualified negative findings are informative.

The studies that comprise the Psychiatric GWAS Consortium (PGC; http://pgc.unc.edu) are shown in Table 1. GWAS data for ADHD, autism, bipolar disorder, major depressive disorder and schizophrenia from 42 samples of European subjects should be available for mega-analyses by early 2009 (>59 000 independent cases and controls and >7700 family trios). To our knowledge, the PGC will have access to the largest set of GWAS data available.

A major change in human genetics in the past 5 years has been in the growth of controlled-access data repositories, and individual phenotype and genotype data are now available for many of the studies in Table 1. When the PGC mega-analyses are completed, most data will be available to researchers via the NIMH Human Genetics Initiative (http://nimhgenetics.org). Although the ready availability of GWAS data is a benefit to the field by allowing rapid application of a wide range of analytic strategies to GWAS data, there are potential disadvantages. GWAS mega-analysis is complex and requires considerable care and expertise to be done validly. For psychiatric phenotypes, there is the additional challenge of working with disease entities based largely on clinical description, with unknown biological validity and having both substantial clinical variation within diagnostic categories as well as overlaps across categories.13 Given the urgent need to know if there are replicable genotype–phenotype associations, a new type of collaboration was required.

The purpose of the PGC is to conduct rigorous and comprehensive within- and cross-disorder GWAS mega-analyses. The PGC began in early 2007 with the principal investigators of the four GAIN GWAS,14 and within six months had grown to 110 participating scientists from 54 institutions in 11 countries. The PGC has a coordinating committee, five disease-working groups, a cross-disorder group, a statistical analysis and computational group, and a cluster computer for statistical analysis. It is remarkable that almost all investigators approached agreed to participate and that no one has left the PGC. Most effort is donated but we have obtained funding from the NIMH, the Netherlands Scientific Organization, Hersenstichting Nederland and NARSAD.

The PGC has two major specific aims. (1) Within-disorder mega-analyses: conduct separate mega-analyses of all available GWAS data for ADHD, autism, bipolar disorder, major depressive disorder, and schizophrenia to attempt to identify genetic variation convincingly associated with any one of these five disorders. (2) Cross-disorder mega-analyses: the clinically-derived DSM-IV and ICD-10 definitions may not directly reflect the fundamental genetic architecture.15 There are two subaims. (2a) Conduct mega-analysis to identify genetic variation convincingly associated with conventional definitions of two or more disorders. This nosological aim could assist in delineating the boundaries of this set of disorders. (2b) An expert working group will convert epidemiological and genetic epidemiological evidence into explicit hypotheses about overlap among these disorders, and then conduct mega-analyses based on these definitions (for example, to examine the lifetime presence of idiopathic psychotic features without regard to diagnostic context).

The goal of the PGC is to identify convincing genetic variation-disease associations. A convincing association would be extremely unlikely to result from chance, show consistent effect sizes across all or almost all samples and be impervious to vigorous attempts to disprove the finding (for example, by investigating sources of bias, confirmatory genotyping, and so on). Careful attention will be paid to the impact of potential sources of heterogeneity17 with the goal of assessing its impact without minimizing its presence.

Biological plausibility is not an initial requirement for a convincing statistical association, as there are many examples in human genetics of previously unsuspected candidate genes nonetheless showing highly compelling associations. For example, multiple SNPs in intron 1 of the FTO gene were associated with body mass index in 13 cohorts with 38 759 participants18 and yet ‘FTO’ does not appear in an exhaustive 116 page compilation of genetic studies of obesity.19 Some strong associations are in gene deserts: multiple studies have found convincing association between prostate cancer and a region on 8q24 that is ~250 kb from the nearest annotated gene.20 Both of these examples are being intensively investigated and we suspect that a compelling mechanistic ‘story’ will emerge in the near future. The presence of a compelling association without an obvious biological mechanism establishes a priority research area for molecular biology and neuroscience of a psychiatric disorder.

The PGC will use mega-analysis as the main analytic tool as individual-level data will be available from almost all samples. To wield this tool appropriately, a number of preconditions must be met. First, genotype data from different GWAS platforms must be made comparable as the direct overlap between platforms is often modest. This requires meticulous quality control for the inclusion of both SNPs and subjects and attention to the factors that can cause bias (for example, population stratification, cryptic relatedness or genotyping batch effects). Genotype harmonization can be accomplished using imputation (2122, for example) so that the same set of ~2 million2324 directly or imputed SNP genotypes are available for all subjects. Second, phenotypes need to be harmonized across studies. This is one of the most crucial components of the PGC and we are fortunate to have world experts directing the work. Third, the mega-analyses will assess potential heterogeneity of associations across samples.

A decision-tree schematic of the potential outcomes of the PGC mega-analyses is shown in Figure 1. Note that many of the possibilities in Figure 1 are not mutually exclusive and different disorders may take different paths through this framework. It is possible that there eventually will be dozens or hundreds of sequence variants strictly associated with these disorders with frequencies ranging from very rare to common.

………

 

GWAS has the potential to yield considerable insights but it is no panacea and may well perform differently for psychiatric disorders. Even if these psychiatric GWAS efforts are successful, the outcomes will be complex. GWAS may help us learn that clinical syndromes are actually many different things—for example, proportions of individuals with schizophrenia might evidence associations with rare CNVs of major effect,56 with more common genetic variation in dozens (perhaps hundreds) of genomic regions, between genetic variation strongly modified by environmental risk factors, and some proportion may be genetically indistinguishable from the general population. Moreover, as fuel to long-standing ‘lumper versus splitter’ debates in psychiatric nosology, empirical data might show that some clinical disorders or identifiable subsets of subjects might overlap considerably.

The critical advantage of GWAS is the search of a ‘closed’ hypothesis space. If the large amount of GWAS data being generated are analyzed within a strict and coherent framework, it should be possible to establish hard facts about the fundamental genetic architecture of a set of important psychiatric disorders—which might include positive evidence of what these disorders are or exclusionary evidence of what they are not. Whatever the results, these historically large efforts should yield hard facts about ADHD, autism, bipolar disorder, major depressive disorder and schizophrenia that may help guide the next era of psychiatric research.

  1. Pe’er I, Yelensky R, Altshuler D, Daly MJ. Estimation of the multiple testing burden for genomewide association studies of nearly all common variants. Genet Epidemiol 2008; 32: 381–385. | Article | PubMed |
  2. Weiss LA, Shen Y, Korn JM, Arking DE, Miller DT, Fossdal R et al. Association between microdeletion and microduplication at 16p11.2 and autism. N Engl J Med 2008; 358: 667–675. | Article | PubMed | ChemPort |

 

Letter

Hreinn Stefansson1,36, et al. Large recurrent microdeletions associated with schizophrenia. Nature 455, 232-236 (11 September 2008) | doi:10.1038/nature07229; Received 17 April 2008; Accepted 8 July 2008; Corrected 11 September 2008

Reduced fecundity, associated with severe mental disorders1, places negative selection pressure on risk alleles and may explain, in part, why common variants have not been found that confer risk of disorders such as autism2, schizophrenia3 and mental retardation4. Thus, rare variants may account for a larger fraction of the overall genetic risk than previously assumed. In contrast to rare single nucleotide mutations, rare copy number variations (CNVs) can be detected using genome-wide single nucleotide polymorphism arrays. This has led to the identification of CNVs associated with mental retardation4, 5 and autism2. In a genome-wide search for CNVs associating with schizophrenia, we used a population-based sample to identify de novoCNVs by analysing 9,878 transmissions from parents to offspring. The 66 de novo CNVs identified were tested for association in a sample of 1,433 schizophrenia cases and 33,250 controls. Three deletions at 1q21.1, 15q11.2 and 15q13.3 showing nominal association with schizophrenia in the first sample (phase I) were followed up in a second sample of 3,285 cases and 7,951 controls (phase II). All three deletions significantly associate with schizophrenia and related psychoses in the combined sample. The identification of these rare, recurrent risk variants, having occurred independently in multiple founders and being subject to negative selection, is important in itself. CNV analysis may also point the way to the identification of additional and more prevalent risk variants in genes and pathways involved in schizophrenia.

 

The C4 gene can exist in multiple copies (from one to four) on each copy of chromosome 6, and has four different forms: C4A-short, C4B-short, C4A-long, and C4B-long. The researchers first examined the “structural alleles” of the C4 locus—that is, the combinations and copy numbers of the different C4 forms—in healthy individuals. They then examined how these structural alleles related to expression of both C4Aand C4B messenger RNAs (mRNAs) in postmortem brain tissues.

From this the researchers had a clear picture of how the architecture of the C4 locus affected expression ofC4A and C4B. Next, they compared DNA from roughly 30,000 schizophrenia patients with that from 35,000 healthy controls, and a correlation emerged: the alleles most strongly associated with schizophrenia were also those that were associated with the highest C4A expression. Measuring C4A mRNA levels in the brains of 35 schizophrenia patients and 70 controls then revealed that, on average, C4A levels in the patients’ brains were 1.4-fold higher.

C4 is an immune system “complement” factor—a small secreted protein that assists immune cells in the targeting and removal of pathogens. The discovery of C4’s association to schizophrenia, said McCarroll, “would have seemed random and puzzling if it wasn’t for work . . . showing that other complement components regulate brain wiring.” Indeed, complement protein C3 locates at synapses that are going to be eliminated in the brain, explained McCarroll, “and C4 was known to interact with C3 . . . so we thought well, actually, this might make sense.”

McCarroll’s team went on to perform studies in mice that revealed C4 is necessary for C3 to be deposited at synapses. They also showed that the more copies of the C4 gene present in a mouse, the more the animal’s neurons were pruned.

Synaptic pruning is a normal part of development and is thought to reflect the process of learning, where the brain strengthens some connections and eradicates others. Interestingly, the brains of deceased schizophrenia patients exhibit reduced neuron density. The new results, therefore, “make a lot of sense,” said Cardiff University’s Andrew Pocklington who did not participate in the work. They also make sense “in terms of the time period when synaptic pruning is occurring, which sort of overlaps with the period of onset for schizophrenia: around adolescence and early adulthood,” he added.

“[C4] has not been on anybody’s radar for having anything to do with schizophrenia, and now it is and there’s a whole bunch of really neat stuff that could happen,” said Sullivan. For one, he suggested, “this molecule could be something that is amenable to therapeutics.”

 

 

UniProtKB

Derived from proteolytic degradation of complement C4, C4a anaphylatoxin is a mediator of local inflammatory process. It induces the contraction of smooth muscle, increases vascular permeability and causes histamine release from mast cells and basophilic leukocytes.

Non-enzymatic component of C3 and C5 convertases and thus essential for the propagation of the classical complement pathway. Covalently binds to immunoglobulins and immune complexes and enhances the solubilization of immune aggregates and the clearance of IC through CR1 on erythrocytes. C4A isotype is responsible for effective binding to form amide bonds with immune aggregates or protein antigens, while C4B isotype catalyzes the transacylation of the thioester carbonyl group to form ester bonds with carbohydrate antigens.

 

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Testosterone treatment improved primarily sexual function than walking or vitality in older men with low testosterone levels

Reporter and Curator: Dr. Sudipta Saha, Ph.D.

A preliminary study of testosterone therapy in older men with low levels of the hormone and clinical conditions to which low testosterone might contribute, found that restoring levels to those of healthy young men improved sexual function. Treatment had a smaller effect on other aspects of health, such as the ability to walk or the sense of vitality.

 

A high proportion of older men have testosterone levels well below those found in healthy younger men. In most cases, these low levels are not due to diseases known to affect testosterone levels, such as testicular or pituitary conditions. Many of these men also have symptomatic problems that could be related to low testosterone, including diminished sexual function, decreased mobility and fatigue.

 

For a long time, there has been interest in whether testosterone is an appropriate therapy for aging-related conditions in men. This study clarifies questions about some of its potential benefits. The study did not find a pattern of increased cardiovascular disease risk. Clarifying the risks requires further study.

 

Participants included 790 men age 65 and older with serum testosterone levels consistently well below the average for young healthy men. They were randomized to receive testosterone gel applied to the skin or a placebo gel daily. Serum testosterone concentration was measured at one, two, three, six, nine and 12 months. The men were also closely monitored for prostate and cardiovascular problems. In addition to low testosterone, the presence of at least one of three conditions (low sexual function, difficulty in walking or low vitality) was required for eligibility to participate in the T Trials (Testosterone Trials).

 

  • Sexual function — In men with low sexual function, testosterone treatment increased sexual activity, sexual desire and erectile function more than placebo treatment.

 

  • Physical function — In men with difficulty in walking, testosterone treatment did not significantly affect walking ability, as measured by the distance they could walk in six minutes (a common test of walking ability). However, in all men, walking speed and distance did improve among those who received testosterone compared with placebo.

 

  • Vitality — In the group of men with symptoms of low vitality and fatigue, testosterone treatment did not significantly affect fatigue symptoms, but had modest favorable effects on mood.

 

The trials’ results indicate that, for older men with low sexual function, testosterone treatment can contribute to improved function. In contrast, though, the results don’t indicate that testosterone treatment for older men with low walking ability or vitality will improve these conditions to a great extent. Older men should consult their physicians if considering a testosterone treatment.

 

References:

 

http://www.nih.gov/news-events/news-releases/nih-supported-trials-test-hormonal-therapy-older-men-low-testosterone-levels

 

http://www.uptodate.com/contents/overview-of-testosterone-deficiency-in-older-men

 

http://www.mayoclinic.org/healthy-lifestyle/sexual-health/in-depth/testosterone-therapy/art-20045728

 

http://www.webmd.com/men/features/low-testosterone-explained-how-do-you-know-when-levels-are-too-low

 

http://www.healthline.com/health/side-effects-of-low-testosterone

 

http://www.health.harvard.edu/mens-health/hormone-replacement-the-male-version

 

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Myc and Cancer Resistance

Curator: Larry H. Bernstein, MD, FCAP

 

Myc (c-Myc) is a regulator gene that codes for atranscription factor. The protein encoded by this gene is a multifunctional, nuclear phosphoprotein that plays a role in cell cycle progression, apoptosis and cellular transformation.[1]

Myc gene was first discovered in Burkitt lymphoma patients. In Burkitt lymphoma, cancer cells showchromosomal translocations, in which Chromosome 8 is frequently involved. Cloning the break-point of the fusion chromosomes revealed a gene that was similar to myelocytomatosis viral oncogene (v-Myc). Thus, the newfound cellular gene was named c-Myc.

http://www.ncbi.nlm.nih.gov/gene/17869

 

Protein increases signals that protect cancer cells

Researchers have identified a link between the expression of a cancer-related gene and cell-surface molecules that protect tumors from the immune system

http://med.stanford.edu/news/all-news/2016/03/protein-increases-signals-that-protect-cancer-cells.html

Depiction of the Myc protein

http://med.stanford.edu/news/all-news/2016/03/protein-increases-signals-that-protect-cancer-cells/_jcr_content/main/image.img.full.high.jpg

The Myc protein, depicted here, is mutated in more than half of all human cancers.   Petarg/Shutterstock

 

A cancer-associated protein called Myc directly controls the expression of two molecules known to protect tumor cells from the host’s immune system, according to a study by researchers at the Stanford University School of Medicine.

The finding is the first to link two critical steps in the development of a successful tumor: uncontrolled cell growth — when mutated or misregulated, Myc causes an increase in the levels of proteins that promote cell division — and an ability to outwit the immune molecules meant to stop it.

The study was published online March 10 inScience. Dean Felsher, MD, PhD, a professor of oncology and of pathology, is the senior author. The lead author is postdoctoral scholar Stephanie Casey, PhD. The work was conducted in collaboration with researchers at the University of Wurzburg.

“Our findings describe an intimate, causal connection between how oncogenes like Myc cause cancer and how those cancer cells manage to evade the immune system,” Felsher said.

‘Don’t eat me’ and ‘don’t find me’

One of the molecules is the CD47 protein, which researchers in the Stanford laboratory of Irving Weissman, MD, have discovered serves as a “don’t eat me” signal to ward off cancer-gobbling immune cells called macrophages. Weissman is the Virginia and D.K. Ludwig Professor for Clinical Investigation in Cancer Research and the director of Stanford’s Institute for Stem Cell Biology and Regenerative Medicine.

Nearly all human cancers express high levels of CD47 on their surfaces, and an antibody targeting the CD47 protein is currently in phase-1 clinical trials for a variety of human cancers.

The other molecule is a “don’t find me” protein called PD-L1, known to suppress the immune system during cancer and autoimmune diseases but also in normal pregnancy. It’s often overexpressed on human tumor cells. An antibody that binds to PD-L1 has been approved by the U.S. Food and Drug Administration to treat bladder and non-small-cell lung cancer, but it has been shown to be effective in the treatment of many cancers.

Dean Felsher

Programmed death-ligand 1 (PD-L1): an inhibitory immune pathway exploited by cancer

Image of PD-L1 binding to B7.1 and PD-1, deactivating T cell]

http://www.researchcancerimmunotherapy.com/images/pathways/pd-l1-hero.jpg

In cancer, Myc a usual suspect

Researchers in Felsher’s laboratory have been studying the Myc protein for more than a decade. It is encoded by a type of gene known as an oncogene. Oncogenes normally perform vital cellular functions, but when mutated or expressed incorrectly they become powerful cancer promoters. The Myc oncogene is mutated or misregulated in over half of all human cancers.

In particular, Felsher’s lab studies a phenomenon known as oncogene addiction, in which tumor cells are completely dependent on the expression of the oncogene. Blocking the expression of the Myc gene in these cases causes the complete regression of tumors in animals.

In 2010, Felsher and his colleagues showed that this regression could only occur in animals with an intact immune system, but it wasn’t clear why.

“Since then, I’ve had it in the back of my mind that there must be a relationship between Myc and the immune system,” said Felsher.

Turning off Myc expression

Casey and Felsher decided to see if there was a link between Myc expression and the levels of CD47 and PD-L1 proteins on the surface of cancer cells. To do so, they investigated what would happen if they actively turned off Myc expression in tumor cells from mice or humans. They found that a reduction in Myc caused a similar reduction in the levels of CD47 and PD-L1 proteins on the surface of mouse and human acute lymphoblastic leukemia cells, mouse and human liver cancer cells, human skin cancer cells, and human non-small-cell lung cancer cells. In contrast, levels of other immune regulatory molecules found on the surface of the cells were unaffected.

I’ve had it in the back of my mind that there must be a relationship between Myc and the immune system.

In publicly available gene expression data on tumor samples from hundreds of patients, they found that the levels of Myc expression correlated strongly with expression levels of CD47 and PD-L1 genes in liver, kidney and colorectal tumors.

The researchers then looked directly at the regulatory regions in the CD47 and PD-L1 genes. They found high levels of the Myc protein bound directly to the promoter regions of both CD47 and PD-L1 in mouse leukemia cells, as well as in a human bone cancer cell line. They were also able to verify that this binding increased the expression of the CD47 gene in a human blood cell line.

Possible treatment synergy

Finally, Casey and Felsher engineered mouse leukemia cells to constantly express CD47 or PD-L1 genes regardless of Myc expression status. These cells were better able than control cells to evade the detection of immune cells like macrophages and T cells, and, unlike in previous experiments from Felsher’s laboratory, tumors arising from these cells did not regress when Myc expression was deactivated.

“What we’re learning is that if CD47 and PD-L1 are present on the surfaces of cancer cells, even if you shut down a cancer gene, the animal doesn’t mount an adequate immune response, and the tumors don’t regress,” said Felsher.

The work suggests that a combination of therapies targeting the expression of both Myc and CD47 or PD-L1 could possibly have a synergistic effect by slowing or stopping tumor growth, and also waving a red flag at the immune system, Felsher said.

“There is a growing sense of tremendous excitement in the field of cancer immunotherapy,” said Felsher. “In many cases, it’s working. But it’s not been clear why some cancers are more sensitive than others. Our work highlights a direct link between oncogene expression and immune regulation that could be exploited to help patients.”

The research is an example of Stanford Medicine’s focus on precision health, the goal of which is to anticipate and prevent disease in the healthy and precisely diagnose and treat disease in the ill.

Other Stanford co-authors of the paper are oncology instructor Yulin Li, MD, PhD; postdoctoral scholars Ling Tong, PhD, Arvin Gouw, PhD, and Virginie Baylot, PhD; former research assistant Kelly Fitzgerald; and undergraduate student Rachel Do.

The research was supported by the National Institutes of Health (grants RO1CA089305, CA170378, CA184384, CA105102, P50 CA114747, U56CA112973, U01CA188383, 1F32CA177139 and 5T32AI07290).

 

The PD-L1 pathway downregulates cytotoxic T-cell activity to maintain immune homeostasis

Under normal conditions, the inhibitory ligands PD-L1 and PD-L2 play an important role in maintaining immune homeostasis.1 PD-L1 and PD-L2 bind to specific receptors on T cells. When bound to their receptors, cytotoxic T-cell activity is downregulated, thereby protecting normal cells from collateral damage.1,2

Image showing PD-L1 binding to B7.1 and PD-1 to deactivate T cells during immune response]

PD-L1

Broadly expressed in multiple tissue types, including hematopoietic, endothelial, and epithelial cells1,4

B7.1

Receptor expressed on activated T cells and dendritic cells3

PD-1

Receptor expressed primarily on activated T cells3

CONVERSELY, PD-L2 BINDS PRIMARILY TO PD-13

Image showing PD-L1 binding to B7.1 and PD-1 to deactivate T cells during immune response]

PD-L2

Restricted expression on immune cells and in some organs, such as the lung and colon1,4,5

PD-1

Receptor expressed primarily on activated T cells3

 

Many tumors can exploit the PD-L1 pathway to inhibit the antitumor response

In cancer, the PD-L1/B7.1 and PD-L1/PD-1 pathways can protect tumors from cytotoxic T cells, ultimately inhibiting the antitumor immune response in 2 ways.1-3

  • Deactivating cytotoxic T cells in the tumor microenvironment
  • Preventing priming and activation of new T cells in the lymph nodes and subsequent recruitment to the tumor

 

PD-L1 MAY INHIBIT CYTOTOXIC T-CELL ACTIVITY IN THE TUMOR MICROENVIRONMENT

Upregulation of PD-L1 can inhibit the last stages of the cancer immunity cycle by deactivating cytotoxic T cells in the tumor microenvironment.1

Activated T cells in the tumor microenvironment release interferon gamma.2

As a result, tumor cells and tumor-infiltrating immune cells overexpress PD-L1.2

PD-L1 binds to T-cell receptors B7.1 and PD-1, deactivating cytotoxic T cells. Once deactivated, T cells remain inhibited in the tumor microenvironment.1,2

PD-L1 MAY INHIBIT CANCER IMMUNITY CYCLE PROPAGATION IN THE LYMPH NODES

PD-L1 overexpression can also inhibit propagation of the cancer immunity cycle by preventing the priming and activation of T cells in the lymph nodes.1-3

PD-L1 expression is upregulated on dendritic cells within the tumor microenvironment.2,3

PD-L1–expressing dendritic cells travel from the tumor site to the lymph node.4

PD-L1 binds to B7.1 and PD-1 receptors on cytotoxic T cells, leading to their deactivation.3

http://www.researchcancerimmunotherapy.com/pathways/pd-l1-immune-evasion

 

The cancer immunity cycle characterizes the complex interactions between the immune system and cancer

The cancer immunity cycle describes a process of how one’s own immune system can protect the body against cancer. When performing optimally, the cycle is self-sustaining. With subsequent revolutions of the cycle, the breadth and depth of the immune response can be increased.1

 

STEPS 1-3: INITIATING AND PROPAGATING ANTICANCER IMMUNITY1

  • Oncogenesis leads to the expression of neoantigens that can be captured by dendritic cells
  • Dendritic cells can present antigens to T cells, priming and activating cytotoxic T cells to attack the cancer cells

STEPS 4-5: ACCESSING THE TUMOR1

  • Activated T cells travel to the tumor and infiltrate the tumor microenvironment

STEPS 6-7: CANCER-CELL RECOGNITION AND INITIATION OF CYTOTOXICITY1

  • Activated T cells can recognize and kill target cancer cells
  • Dying cancer cells release additional cancer antigens, propagating the cancer immunity cycle

 

 

 

Image of immunity cycle; explore Genentech cancer immunotherapy research on the cancer immunity cycle

http://www.researchcancerimmunotherapy.com/pathways/pd-l1

 

REFERENCES

  1. Chen DS, Mellman I. Oncology meets immunology: the cancer-immunity cycle. Immunity. 2013;39:1-10. PMID: 23890059
  2. Chen DS, Irving BA, Hodi FS. Molecular pathways: next-generation immunotherapy—inhibiting programmed death-ligand 1 and programmed death-1. Clin Cancer Res. 2012;18:6580-6587. PMID: 23087408
  3. Keir ME, Butte MJ, Freeman GJ, Sharpe AH. PD-1 and its ligands in tolerance and immunity. Annu Rev Immunol. 2008;26:677-704. PMID: 18173375
  4. Motz GT, Coukos G. Deciphering and reversing tumor immune suppression. Immunity. 2013;39:61-73. PMID: 23890064

 

 

MYC regulates the antitumor immune response through CD47 and PD-L1

The clinical efficacy of monoclonal antibodies as cancer therapeutics is largely dependent upon their ability to target the tumor and induce a functional antitumor immune response. This two-step process of ADCC utilizes the response of innate immune cells to provide antitumor cytotoxicity triggered by the interaction of the Fc portion of the antibody with the Fc receptor on the immune cell. Immunotherapeutics that target NK cells, γδ T cells, macrophages and dendritic cells can, by augmenting the function of the immune response, enhance the antitumor activity of the antibodies. Advantages of such combination strategies include: the application to multiple existing antibodies (even across multiple diseases), the feasibility (from a regulatory perspective) of combining with previously approved agents and the assurance (to physicians and trial participants) that one of the ingredients – the antitumor antibody – has proven efficacy on its own. Here we discuss current strategies, including biologic rationale and clinical results, which enhance ADCC in the following ways: strategies that increase total target–monoclonal antibody–effector binding, strategies that trigger effector cell ‘activating’ signals and strategies that block effector cell ‘inhibitory’ signals.

Keywords: γδ T cells, ADCC, cancer, cytokines, IMiD, immunocytokines, immunomodulators, interleukins, monoclonal antibodies, NK cells, passive immunotherapy

Monoclonal antibodies (mAbs) can target tumor antigens on the surface of cancer cells and have a favorable toxicity profile in comparison with cytotoxic chemotherapy. Expression of tumor antigens is dynamic and inducible through agents such as Toll-like receptor (TLR) agonists, immunomodulatory drugs (IMiDs) and hypomethylating agents [1]. Following binding of the mAb to the tumor antigen, the Fc portion of the mAb interacts with the Fc receptor (FcR) on the surface of effector cells (i.e., NK cells, γδ T cells and macrophages), leading to antitumor cytotoxicity and/or phagocytosis of the tumor cell. FcR interactions can be stimulatory or inhibitory to the killer cell, depending on which FcR is triggered and on which cell. Stimulatory effects are mediated through FcγRI on macrophages, dendritic cells (DCs) and neutrophils, and FcγRIIIa on NK cells, DCs and macrophages. In murine models, the cytotoxicity resulting from FcR activation on a NK cell, γδ T cell and macrophage is responsible for antitumor activity [2]. The role of DCs should be noted: although not considered to be primary ADCC effector cells, they can respond to mAb-bound tumor cells via their own FcR-mediated activation and probably play a significant role in activating effector cells. Preclinical models have shown that, although not the effector cell, DCs are critical to the efficacy of mAb-mediated tumor elimination [3]. Equally, mAb-activated ADCC effector cells can induce DC activation [4] and the importance of this crosstalk is an increasing focus of study [5].

The antitumor effects of mAbs are caused by multiple mechanisms of action, including cell signaling agonism/antagonism, complement activation and ligand sequestration, although ADCC probably plays a predominant role in the efficacy of some mAbs. In a clinical series, a correlation between the affinity of the receptor FcγRIIIa (determined by inherited FcR polymorphisms) and the clinical response to mAb therapy, supporting the significance of the innate immune response [610]. Several strategies could potentially improve the innate response following FcR activation by a mAb (Figure 1):

Quantitatively increasing the density of the bound target, mAb or the effector cells;

Stimulation of the effector cell by targeting the NK cell, γδ T cell and/or macrophage with small molecules, cytokines or agonistic antibodies;

Blocking an inhibitory interaction between the NK cell or macrophage and the tumor cell.

 

An external file that holds a picture, illustration, etc. Object name is nihms384451f1.jpg

http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3386352/bin/nihms384451f1.jpg

Enhancing ADCC

FcR: Fc receptor; HDACi: Histone deacetylase inhibitor; IMiD: Immunomodulator; KIR: Killer immunoglobulin-like receptor;

The ability of the combination approaches to enhance ADCC is largely determined by the capacity of the mAb to induce ADCC. Since the approval of the first mAb for the treatment of non-Hodgkin’s lymphoma, rituximab (RTX), in 1997, several mAbs have become standard of care for the treatment of both solid tumors and hematologic malignancies, including trastuzumab (TRAST), alemtuzumab, cetuximab, panitumumab and ofatumumab [11]. As noted above, clinical series among lymphoma patients treated with an anti-CD20 mAb (RTX) [6,7], HER2-expressing breast cancer receiving anti-HER2 mAb therapy (TRAST) [8] or colorectal cancer patients treated with an anti-EGFR mAb (cetuximab) [9,10] observed a correlation between clinical benefit and FcγRIIIa genotype, with patients who have higher-affinity polymorphisms demonstrating superior clinical outcomes. By contrast, the anti-EGFR mAb panitumumab does not induce ADCC, owing to a different Fc isotype that does not bind to the FcγRIIIa. Therefore, when considering enhancement of ADCC, such approaches are limited to combinations with mAbs that activate the FcR. Nonetheless, an advantage of this dual therapy strategy is that mAbs yet to be discovered against currently unknown tumor antigens may be combined with the therapeutics discussed herein.

Increasing target–mAb–effector binding

As the central element in the target–mAb–effector cell unit, the mAb seems to be a probable candidate for improvements, either in its antigen-binding or its Fc-binding domains. This approach has been heavily pursued with some degree of success [1215]. Antibody engineering to improve interaction between the target or FcR requires that each new antibody be individually developed and tested as a new entity.

Increasing the antigen target

Tumor cells with a lower density of antigen targets are less responsive to mAbs than higher antigen-expressing diseases [16]. Therefore, it seems logical to try to increase the expression of the target on tumor cells. Antigen expression can be upregulated by cytokines [17], ionizing radiation [18], natural metabolites [19] and hypomethylating agents such as decitabine [20]. In addition, the family of TLR9 agonists known as CpG oligodeoxynucleotides (CpG ODN) can induce CD20 expression on malignant B cells [2123]. Taken together with data showing the activating effect of CpG ODN on effector cells (discussed below), it seems reasonable that the combination of CpG ODN with mAb might have synergistic efficacy. Clinical series, however, have tested CpG ODN administered intravenously or subcutaneously and have observed little efficacy in Phase I and II studies [2426] in low-grade lymphoma. One possible limitation of these studies has been their application to diseases (primarily follicular and mantle cell lymphoma) known to already have high expression of the relevant antigen (CD20). It is plausible that increasing antigen expression on low antigen-expressing diseases such as chronic lymphocytic leukemia could have a greater increase in relative efficacy. To this end, monotherapy studies have recently been undertaken [27,301] and should lead to combination trials.

……

Effector cells: γδ T cells

The role of NK cells and macrophages in mediating ADCC has been well established; however, only recently have γδ T cells been found to play a role as ADCC effectors. Typically, this population is considered as a minor subset (<5% of circulating T cells), although they may infiltrate tumors of epithelial origin preferentially and constitute a large portion of the tumor-infiltrating lymphocytes in cancers such as breast carcinoma. The combination of HLA-unrestricted cytotoxicity against multiple tumor cell lines of various histologies, secretion of cytolytic granules and proinflammatory cytokines such as TNF-α, IL-17 and IFN-γ make γδ T cells potentially potent antitumor effectors [32,33].

……

TLR agonists    

In addition to its aforementioned induction of CD20, CpG ODN also indirectly augments innate immune function. TLRs are specialized to recognize pathogen-associated molecular patterns; they stimulate plasmacytoid DCs and B cells [53], and one of many plasmacytoid DC responses to stimulation by CpG ODNs is activation of local NK cells, thus improving spontaneous cytotoxicity and ADCC [54]. CpG ODN effects on NK cells appeared to be indirect and IFN-γ production by T cells (possibly in response to plasmacytoid DC activation) has been hypothesized as the intermediary of NK cell activation.

…..

Immunomodulatory drugs

IMiDs have shown clinical activity in multiple hematologic malignancies despite their primary mechanism of action being unclear. Among their biologic effects (particularly lenalidomide) there are demonstrable and pleiotropic effects on immune cells and signaling molecules. These include enhancement of in vitro NK cell- and monocyte-mediated ADCC on RTX-coated [68] as well as TRAST- and cetuximab-coated tumor cells [69]. In vivo studies in a human lymphoma severe combined immune deficiency mouse model demonstrated significant increases in NK cell recruitment to tumors mediated via microenvironment cytokine changes and augmented RTX-associated ADCC [70]. Studies suggest that IMiD activation of NK cells occurs indirectly; partly via IL-2 induction by T cells [71]. Clinically, a recent study noted significant increases in peripheral blood NK cells, NK cell cytotoxicity and serum IL-2, IL-15 and GM-CSF [72], the potential ADCC-promoting effects of which are discussed below.

…..

PD-1

PD-1 is a negative regulatory member of the CD28 superfamily expressed on the surface of activated T cells, B cells, NK cells and macrophages, similar to but more broadly regulatory than CTLA-4. Its two known ligands, PD-L1 and PD-L2, are both expressed on a variety of tumor cell lines. The PD-1–PD-L1 axis modulates the NK cell versus multiple myeloma effect, as seen by its blockade enhancing NK cell function against autologous primary myeloma cells, seemingly through effects on NK cell trafficking, immune complex formation with myeloma cells and cytotoxicity specifically toward PD-L1(+) tumor cells [179]. Two anti-PD-1 mAbs (BMS-936558 and CT-011) are currently in clinical trials, the latter in a combination study with RTX for patients with low-grade follicular lymphoma [314].

ConclusionThe recent approval of an anti-CTLA4 mAb has demonstrated that modulating the immune response can improve patient survival [180,181]. As the immune response is a major determinant of mAb efficacy, the opportunity now exists to combine mAb therapy with IMiDs to enhance their antitumor efficacy. Remarkable advances in the basic science of cellular immunology have increased our understanding of the effector mechanisms of mAb antitumor efficacy. Whereas the earliest iterations of such combinations, for example IL-2 and GM-CSF, may have augmented both effector and suppressive cells, newer approaches such as IL-15 and TLR agonists may more efficiently activate effector cells while minimizing the influence of suppressive cells. Despite these encouraging rationale and preliminary data, clinical evidence is still required to demonstrate whether combination therapies will increase the antitumor effects of mAb.

Still, this approach is unique in combining a tumor-targeting therapy, the mAb, with an immune-enhancing therapy. If successful, these therapies may be combined with multiple mAbs in routine practice, as well as novel mAbs yet to be developed. Various approaches including augmenting antigen expression, stimulating the innate response and blocking inhibitory signals are being explored to determine the optimal synergy with mAb therapies. Therapies targeting NK cells, γδ T cells, macrophages and DCs may ultimately be used in combination to further augment ADCC. Encouraging preclinical studies have led to a number of promising therapeutics, and the results of proof-of-concept clinical trials are eagerly awaited.

PD-L1, other targeted therapies await more standardized IHC

February 2016—Immunohistochemistry is heading down a path toward more standardization, and that’s essential as it plays an increasing role in rapidly expanding immunotherapy, says David L. Rimm, MD, PhD, professor of pathology and of medicine (oncology) and director of translational pathology at Yale University School of Medicine. As a co-presenter of a webinar produced by CAP TODAY in collaboration with Horizon Diagnostics, titled “Immunohistochemistry Through the Lens of Companion Diagnostics” (http://j.mp/ihclens_webinar), he analyzes the core challenges of IHC’s adaptation to the needs of precision medicine: binary versus continuous IHC, measuring as opposed to counting or viewing by the pathologist, automation, and assay performance versus protein measurement.

“Immunohistochemistry is 99 percent binary already,” Dr. Rimm points out. “There are only a few assays in our labs—ER, PR, HER2, Ki-67, and maybe a few more—where we really are looking at a continuous curve or a level of expression.”

Two criteria in the 2010 ASCO/CAP guidelines on ER and PR testing in breast cancer patients are key, he says: 1) the percentage of cells staining and 2) any immunoreactivity. “The first is hard to estimate, but the guidelines recommend the use of greater than or equal to one percent of cells that are immunoreactive. That means they could have a tiny bit of signal or they could have a huge amount of signal and they would be considered immunoreactive, which thereby makes this a binary test.”

Having the test be binary can be a problem for companion diagnostic purposes because any immunoreactivity is dependent on the laboratory threshold and counterstain. For example, if two of the same spots, serial sections on a tissue microarray, were shown side by side, one with and one without the hematoxylin counterstain, “you might see the counterstain make this positive test into a negative by eye, which is a potential problem with IHC when you have a binary stain.” (Fig. 1).

Fig1

http://www.captodayonline.com/wordpress/wp-content/uploads/2016/02/Fig1.jpg

Dr. Rimm describes a small study done with three different CLIA-certified labs, each using a different FDA-approved antibody and measuring about 500 breast cancer cases on a tissue microarray. The study showed there can be fairly significant discordance between labs—between 18 and 30 percent discordance—in terms of the cases that were positive. “In fact, if we look at outcome, 18 percent of the cases were called positive in Lab Two but were negative in Lab Three. Lab Three showed outcomes similar to the double positives whereas Lab Two had false-negatives.” This is an important problem that occurs when we try to binarize our immunohistochemistry, he says.

Counting is more variable in a real-world setting due to the variability of the threshold for considering a case positive. “You can easily calculate that if your threshold was five percent, then you’d have 70 percent positive cells. And you would easily call this positive. But if you added more hematoxylin because that’s how your pathologist liked it, then perhaps you’d only have 30 percent positive. So this is the risk of using thresholds.” (Fig. 2).

Fig2

http://www.captodayonline.com/wordpress/wp-content/uploads/2016/02/Fig2.gif

Although this is done in all of immunohistochemistry today, Dr. Rimm thinks it is an important consideration as IHC transitions to more standardized form. “An H score—intensity times area, which has been attempted many times, can’t be done by human beings. Pathologists try but have failed.”

“We can’t do those intensities by eye. We have to measure them with a machine. But we get a very different piece of information content when we measure intensity, as opposed to measuring the percentage of cells above a threshold. In sum, more information is present in a measurement than in counting.”

Pathologists read slides for a living, so it’s uncomfortable to think about giving that up in order to use a machine to measure the slides. “But I think if we want to serve our clients and our patients, we really owe them the accuracy of the 21st century as opposed to the methods of the 20th century.” (Fig. 3).

A shows comparison of a quantitative fluorescence score on the x axis versus an H-score on the y axis. Note the noncontinuous nature of human estimation of intensity times area (H-score). B) The survival curve in a population of lung cancer cases using the H-score. C) The survival curve in the same population using the quantitative score. (Source: David Rimm, MD, PhD)

http://www.captodayonline.com/wordpress/wp-content/uploads/2016/02/Fig3.gif

A shows comparison of a quantitative fluorescence score on the x axis versus an H-score on the y axis. Note the noncontinuous nature of human estimation of intensity times area (H-score). B) The survival curve in a population of lung cancer cases using the H-score. C) The survival curve in the same population using the quantitative score. (Source: David Rimm, MD, PhD)

Among the currently available quantitative measuring devices are the Visiopharm, VIAS (Ventana), Aperio (Leica), InForm (Perkin-Elmer), and Definiens platforms. “We use the platform invented in my lab, called Aqua [Automated Quantitative Analysis], but this is now owned by Genoptix/Novartis. Genoptix intends to provide commercial tests using Aqua internally,” Dr. Rimm says, “as well as enable platform and commercial testing through partnership with additional reference lab providers.

“There are many quantification platforms,” he adds, “and I believe that any of them, used properly, can be effective in measurement.”

(Of the 265 participants in the CAP PM2 Survey, 2015 B mailing, who reported using an imaging system for quantification, 4.6 percent use VIAS, 4.1 percent use ACIS, 0.8 use Applied Imaging, and 10 percent use “other” imaging systems. Of the 1,359 Survey participants who responded to the question about use of an imaging system to analyze hormone receptor slides, 1,094, or 80.5 percent, reported not using any imaging system for quantification.)

Says Dr. Rimm: “The first platform we used to try to quantitate some DAB stain slides was actually the Aperio Nuclear Image Analysis algorithm. But the problem with DAB is that you can’t see through it. And so inherently it’s physically flawed as a method for accurate measurement.” He compares DAB to looking at stacks of pennies from above, where their height and quantity can’t be surmised, as opposed to from the side, where their numbers can be accurately estimated. “This is why I don’t use, in general, DAB-type technologies or any chromogen.”

Fluorescence doesn’t have this problem, and that is the reason Dr. Rimm began using fluorescence as a quantitative method. “We try to be entirely quantitative without any feature extraction. So we define epithelial tumors using a mask of cytokeratin. We define a mask by bleeding and dilating, filling some holes, and then ultimately measure the intensity of each cell, or of each target we’re looking for. In this case, in a molecularly defined compartment.”

Compartments can be defined by any type of molecular interactions. “We defined DAPI-positive pixels as nuclei, and we measure the intensity of the estrogen receptor within the compartment. And that gives us an intensity over an area or the equivalent of a concentration.” Many other fluorescent tools can be used in this same manner, but he cautions against use of fluorescent tools that group and count. “That’s a second approach that can be used, but the result gives you a count instead of a measurement.”

When comparing a pathologist’s reading versus a quantitative immunofluorescence score, he notes, pathologists actually don’t generate a continuous score. Instead, pathologists tend to use groups. “We tend to use a 100 or a 200 or an even number. We never say, ‘Well, it’s 37 percent positive.’ We say, ‘It’s 40 percent positive,’ because we know we can’t reproducibly tell 37 from 38 from 40 percent positive.”

The result of that is a noncontinuous scoring result, which doesn’t give the information content of quantitative measurement. A comparison between the two methods shows that at times, where quantitative measurement shows a significant difference in outcome, nonquantitative measure or an H-score difference may not show a difference in outcome. (Fig. 3 illustrates this concept.)

“Pathologists tend to group things, and we also tend to overestimate. It’s not that pathologists are bad readers. It’s just the tendency of the human eye because of our ability to distinguish different intensities and the subtle difference between intensities. But even if you compare two quantitative methods, you can see that the method where light absorbance occurs—that is the percent positive nuclei by Aperio, which is a chromogen-based method—tends to saturate. This is, in fact, amplified dramatically when you look at something with a wide dynamic range like HER2.” (Fig. 4).

Fig4

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In one study, researchers found less than one percent discordance—essentially no discordance—between two antibodies (Dekker TJ, et al. Breast Cancer Res. 2012;14[3]:R93). But looking at these results graphed quantitatively, you would see a very different result, Dr. Rimm says. “You can see a whole group of cases down below where there’s very low extracellular domain and very high cytoplasmic domain. In fact, some of these cases have essentially no extracellular domain, but high levels of cytoplasmic domain, and other cases have roughly equal levels of each” (Carvajal-Hausdorf DE, et al. J Natl Cancer Inst.2015;107[8]:pii:djv136).

Recent studies by Dr. Rimm’s group have shown this to have clinical implications. He looked at patients treated with trastuzumab in the absence of chemotherapy, in an unusual study called the HeCOG (Hellenic Cooperative Oncology Group) trial.

“We found that patients who had high levels of both extracellular and intracellular domain have much more benefit than patients who are missing the extracellular domain and thereby missing the trastuzumab binding site.” Follow-up studies are being done to validate this finding in larger cohorts.

Preanalytical variables, Dr. Rimm emphasizes, can have significant effects on IHC results, and more than 175 of them have been identified. “These are basically all the things we can’t control, which is the ultimate argument for standardization.”

In a surprising study by Flory Nkoy, et al., he says, it was shown that breast cancer specimens were more likely to be ER negative if the patient’s surgery was on a Friday because there was a higher ER-negative rate on Friday than on Monday. “So how could that be? Well, it was clearly the fact that the tissue was sitting over the weekend. And when it sat over the weekend, the ER positivity rate was going down” (Arch Pathol Lab Med. 2010;134:606–612).

Another study showed that after one hour, four hours, and eight hours of storage at room temperature, you lose significant amounts of staining, Dr. Rimm says. “And perhaps the best nonquantitative study or H-score-based study of this phenomenon was done by Isil Yildiz-Aktas, et al., where a significant decrease in the estrogen receptor score was found after only three hours in delay to fixation” (Mod Pathol. 2012;25:1098–1105).

How long the slide is left to sit after it is cut is another preanalytical variable to be concerned with. “In the clinical lab, that’s not often a problem since we cut them, then stain them right away. But in a research setting, a fresh-cut slide can look very different from a slide that’s two days old, six days old, or 30 days old, where a 2+ spot on a breast cancer patient becomes negative after 30 days sitting on a lab bench. So those are both key variables to be mindful of.”

One solution for those preanalytic variables is trying to prevent delayed time to fixation. “And probably time to fixation is one of the main preanalytic variables, although it’s only one of the many hundreds of variables. The method we use to try to get around this problem is to use core biopsies or allow rapid and complete fixation, and then other things can be done.”

Finally, he warns, don’t cut your tissue until right before you stain it. “If you’re asked to send a tissue out to a collaborator or someone who is going to use it for research purposes later, we recommend coring and re-embedding the core, or sending the whole block. Unstained sections, when not properly stored in a vacuum, will ultimately be damaged by hydration or oxidation, both of which lead to loss of antigenicity.”

The crux of the matter is assay performance versus protein measurement, Dr. Rimm says. “In the last six to nine months, we really are faced with this problem in spades, as PD-L1 has become a very important companion diagnostic.”

There are now four PD-L1 drugs with complementary or companion diagnostic tests (Fig. 5). One of the FDA-approved drugs, nivolumab (Opdivo, Bristol-Myers Squibb), for example, uses a clone called 28-8, which is provided by Dako in an assay, a complementary diagnostic assay, and with the following suggested scoring system: one percent, five percent, or 10 percent. In contrast, pembrolizumab (Keytruda, Merck) is also now FDA-approved but requires a companion diagnostic test that uses a different antibody, although the same Dako Link 48 platform. This diagnostic has a different scoring system of less than one percent, one to 49 percent, and 50 percent and over.

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Two other companies, Roche/Genentech and AstraZeneca, also have drugs in trials that may or may not have companion diagnostic testing, though both have already identified a partner and a unique antibody (neither of those listed above) and companion diagnostic testing scores used in their clinical trials.

“So what’s a pathologist to do?” Dr. Rimm says. “Well, there are a few problems with this. First of all, what we really should be doing is measuring PD-L1. That’s the target and that’s what should ultimately predict response. But instead what we’re stuck with, through the intricacies of the way our field has grown and our legacy, is closed-system assays. While these probably do measure PD-L1, we do not know how these compare to each other.” Two parallel large multi-institutional studies are addressing this issue now, he says.

There are solutions for managing these closed-system assays to be sure the assay is working in your lab and that you can get the right answer, Dr. Rimm says. His laboratory uses a closed-system assay for PD-L1, relying not on the defined system but rather on a test system it has developed in doing a study with different investigators.

Sample runs by these different investigators show the potentially high variability, he says. “In a scan of results, no one would deny which spots are the positive spots and which are the negative.” But the difference in staining prevents accurate measurement of these things and shows the variability inherent even in a closed-box system.

A comparison of two closed-box systems, the SP1 run on the Discovery Ultra on Ventana, and the SP1, same antibody, run on the Dako closed-box system, also shows that, in fact, there’s not 100 percent agreement using same-day, same-FDA-cleared antibody staining and different autostainers. So automation may not solve the problem, Dr. Rimm notes (Fig. 6).

Fig6

“When running these in a quantitative fashion and measuring them quantitatively, there are actually differences in the way these closed-box systems run. And so you, as the pathologist, have to be the one who makes sure your assays are correct, your thresholds are correct, and your measurements are accurate.”

The way to do that, he believes, is to use standardization or index arrays. An index array of HER2 that his laboratory developed has 3+ amplified, 2+ amplified, not amplified, and so on from 80 cases in the lab’s archive, shown stained with immunofluorescence and quantitative and DAB stain. “It was only with this standardization array, run every time we ran our stainer, that we were able to draw the conclusions in the previous study about extracellular versus cytoplasmic domain.”

Companies have realized the importance of this, and specifically companies like NantOmics (formerly OncoPlexDx) have realized they can exactly quantitate the amount of tissue on a slide using a specialized mass spectrometry method, he says. “They can actually give you amol/µg of total protein.”

He and colleagues are working with NantOmics now to try to convert from amols to protein to average quantitative fluorescent scores to help build these standards and make standard arrays more accurate. “This is still a work in progress, but I believe this is ultimately the kind of accuracy that can standardize all of our labs. We have shown that the quantitative fluorescence system is truly linear and quantitative for EGFR measurements when using mass spectrometry as a gold standard.” They are preparing to submit a manuscript with this data.

In the interim, Dr. Rimm’s laboratory has begun working also with Horizon Diagnostics, employing Horizon’s experimental 15-spot positive-control array. “When you use this array and quantitate it with quantitative fluorescence, you get a very interesting profile. If a cut point is set at one point, you would see three clearly positive cells or spots and 12 clearly negative spots with two different antibodies. But is that the threshold?”

“In fact, using a little higher score and a very quantitative test, you might find that the threshold may, in fact, be a little bit lower than that.” It turns out that only three of these 12 spots are true negatives. The others at least have some level of RNA, and some have a lot. “So how do we handle these? And are these behaving the same way with multiple antibodies?” Parallel results, finding nearly the same threshold case, have been found using SP142 from Ventana, E1L3N from Cell Signaling, and SP263 from Ventana.

Studies to address those issues are still in the early stage, he says. He cautions that there is variance in these assays, and more work is being done to reproduce the data. “But I think the important point is that, using these kinds of arrays, you can definitively determine whether your lab has the same cut point as every other lab. And were we to quantitate this with mass spectrometry, we would know exactly the break point for use in the future.”

Dr. Rimm’s laboratory has also built its own PD-L1 index tissue microarray with a number of its own tumor slides ranging from very low to very high expressors, a series of cell lines, and including some placenta-positive controls on normal tumor. He has found that generating an index array has advantages, and he encourages other laboratories to prepare their own index arrays to increase the accuracy and reproducibility of their laboratory-developed tests. “You can produce these in your own lab so that you can be sure you can standardize your tests run in your clinical lab from day to day and week to week as part of an LDT.”

“If we think about it, there really are no clinical antibodies today that are truly quantitative,” Dr. Rimm says. “And when there are, new protocols will be required, but I believe those protocols are now in existence. We just await the clinical trials that require truly quantitative protein measurement or in situ proteomics.”

In that process of moving toward in situ proteomics, suggests web-inar co-presenter Clive Taylor, MD, DPhil, professor of pathology in the Keck School of Medicine at the University of Southern California, FDA approval, per se, will not solve any of the problems discussed in the webinar. (See the January 2016 issue for the full report of Dr. Taylor’s presentation.) “I think what the FDA approval will do is demand that we find solutions to these problems ourselves. The FDA’s attitude is, to a large degree, dependent on the claim. So if we just use immunohistochemistry as a simple stain, then the FDA classes that as sort of class I, level 1. And we can do that [IHC stain] without having to get preapproval by the FDA.

“On the other hand, if we take something like the well-established HercepTest, where based on the result of that test alone, it’s decided whether or not the patient gets treatment, treatment that’s very expensive and treatment that has benefits and…side effects. That claim is, in fact, a very high-level claim. And for that, the FDA is demanding high-level data, which I think is entirely appropriate,” Dr. Taylor says.

Most of these upcoming companion diagnostics, if not all, he says, will be regarded by the FDA as class III, high level or high complexity. They will require a premarket approval study in conjunction with a clinical trial. And the FDA will demand high standards of control and performance, eventually. “There are not many labs that can produce those high standards as in-house or lab-developed tests today. And even the companies currently in trials are not producing the improved performance level for these tests that we are talking about today, as being required for high-quality quantitative and reproducible companion diagnostics. Eventually, I am convinced we will have to do that. It’s just that it will take time to get there.”

The FDA can only approve what is brought to it, Dr. Rimm points out. And so a true, fully quantitative IHC-based assay has presumably never been submitted, or at least never been approved by the FDA. “What we’re seeing instead are the assays that the FDA has approved, which are well defined and rigorously submitted. However, the result is a closed system that we use, which may or may not accurately measure PD-L1 on the slide, depending upon preanalytic variables and individual laboratories’ methods.”

“So questions keep popping up. And I can only say that we, as pathologists, have the final responsibility to our patients. And while it may not be recommended and it may change in the future, right now lab-derived tests or LDTs may be more accurate than FDA-approved platforms.”

“If you think about it, in molecular diagnostics where I’m familiar with EFGR and BRAF and KRAS tests, in that testing setting, less than 25 percent of the labs that do that test actually use the FDA-approved test,” Dr. Rimm says. “The remainder of the labs do their own LDTs, including our labs here at Yale.”

It wouldn’t surprise him if the same thing happens for PD-L1. “I’m aware of at least two labs—and we probably will be the third—that devise our own LDT for PD-L1 testing using the standards I’ve discussed, using array-type controls to be sure that our levels are correct, and then using a scoring system that we derived.”

“We aren’t really in a position to know at the time that we receive a piece of lung cancer tissue whether the oncologist is going to use pembrolizumab, which requires a companion diagnostic, or nivolumab, or the other drugs, which may or may not require a companion diagnostic. So in that sense, we’re almost bound to use an LDT,” Dr. Rimm says, since his lab can’t actually run four different potentially incongruent, though FDA-approved, tests for PD-L1.

Until a truly quantitative approach is developed and submitted to the FDA and approved, Dr. Taylor believes we won’t see things changing. “The algorithms that currently are approved have been approved on the basis that they can produce a similar result to a consensus group of pathologists. So they’re only as good as the pathologists.”

“As Dr. Rimm has discussed, I actually believe we can get a much better result than the pathologists can get with their naked eye. We have to get away from comparing it to what we currently can do and start to try to construct a proper test, just like we did in the clinical lab 30 years ago when we automated the clinical lab,” Dr. Taylor says. “We need to automate anatomic pathology, including the sample preparation, the assay process, and the reading, all three together in a closed system. And we’re nibbling away at the edges of it. We’ll get there, but it’ll take some time.”

Dr. Rimm is skeptical that the diagnostics field has learned any lessons from HercepTest and the companion diagnostics world of almost 20 years ago. “The submissions to the FDA for PD-L1 look very similar to what was submitted in 1998 for the HercepTest, the companion diagnostic test for trastuzumab [Herceptin]. And that’s disappointing. I think that is 20-year-old technology and we can do better. But even if we want to use the 20- or 40-year-old DAB-based technology, we should still be standardizing it and having a mechanism for standardization and having defined thresholds.”

As future FDA submissions come in, Dr. Rimm hopes that “even if they’re not quantitated, they can be standardized as to where the thresholds occur, so that we can be sure we deliver the best possible care to patients. And in the interim, I think we, as pathologists, will have to do that standardization with an LDT to be sure we’re giving our best results.”

Dr. Taylor warns that there is only a limited number of labs in the country and in the world that will be able to produce these LDTs, because of the complexity. “The FDA has already said in a position paper that it believes it may have to regulate LDTs to some extent. And what that will mean is that in the validation process, your own LDT will start to approach what is required for an FDA-approved test. And most labs are in no position to be able to do that.”

“So I think we’re going to come to a blending here, all forced by companion diagnostics. This is in situ proteomics,” Dr. Taylor says. “It’s a new test, essentially. It’s not straightforward immunohistochemistry, but a new test. And I think the fluorescence approach that Dr. Rimm has used has a lot of advantages in relating signal to target in terms of figure out what the best test is and stop comparing it to the pathologists. We should compare it to the best assay we can produce.”

With respect to the PD-L1 problem, Dr. Rimm notes, “I would point out that there is a so-called ‘Blueprint’ for comparison of the different antibodies and the different FDA assays, or potentially FDA-submitted tests anyway, to see how equivalent they are.” Similarly, he adds, the National Comprehensive Cancer Network recently issued a press release describing a multi-institutional study to assess the FDA-approved assay but also including an LDT (the Cell Signaling antibody E1L3N using the Leica Bond staining platform).

He points to a newly published study by his group (McLaughlin J, et al. JAMA Oncol. 2016;2[1]:46–54), finding that objective determination of PD-L1 protein levels in non-small cell lung cancer reveals heterogeneity within tumors and prominent interassay variability or discordance. The authors concluded that future studies measuring PD-L1 quantitatively in patients treated with anti-PD-1 and anti PD-L1 therapies may better address the prognostic or predictive value of these biomarkers. With future rigorous studies, including tissues with known responses to anti-PD-1 and anti-PD-L1 therapies, researchers could determine the optimal assay, PD-L1 antibody, and the best cut point for PD-L1 positivity.

Other work that will probably come out in mid-2016 from Dr. Rimm’s group has shown that expression of PD-L1 is largely bimodal, he says. “That is, there’s a group of patients that express a lot, and then there’s another group of patients that expresses a little or none.”

So time will tell how PD-L1 will be scored. “But if you look at the data from the Merck study and their cut point of greater than 50 percent, or even the cut point from the AstraZeneca studies of greater than 25 percent, you’re really dichotomizing the population into patients who are truly PD-LI positive from patients who are negative or almost negative.”

“Of course, we don’t want to miss patients in that negative to almost-negative group who will respond,” Dr. Rimm says. “On the other hand, we probably will have fairly good specificity and sensitivity with the assay defined by Merck and Dako with 22C3 as was recently published” (Robert C, et al. N Engl J Med. 2015;372[26]:2521–2532).

Many difficulties lie ahead, as researchers try to weigh the merits of different drugs with different approved tests on different platforms, involving different antibodies, Dr. Taylor says. “Does the lab try to set up four different PD-L1s, and if we only have one platform and not another, what do we do about that?” He thinks the tests may often be sent out to larger reference labs or academic centers as a result.

Dr. Rimm confirms that his own lab’s LDT—although literally thousands of PD-L1 tests have been conducted using it—is not yet up and running in the Yale CLIA laboratory, and in the meantime the IHC slides are being sent out to a commercial vendor.

Eventually, Dr. Taylor believes, the pressure of these dilemmas will lead the diagnostics field to develop an immunoassay on tissue sections. “We’ve never been forced to do that before, but once we are, that will produce a huge change in diagnostic capability and research capability.”

Anti–PD-1/PD-L1 therapy of human cancer: past, present, and future

Lieping Chen and  http://www.jci.org/articles/view/80011

The cDNA of programmed cell death 1 (PD-1) was isolated in 1992 from a murine T cell hybridoma and a hematopoietic progenitor cell line undergoing apoptosis (1). Genetic ablation studies showed that deficiencies in PD-1 resulted in different autoimmune phenotypes in various mouse strains (2, 3). PD-1–deficient allogeneic T cells with transgenic T cell receptors exhibited augmented responses to alloantigens, indicating that the PD-1 on T cells plays a negative regulatory role in response to antigen (2).

Several studies contributed to the discovery of the molecules that interact with PD-1. In 1999, the B7 homolog 1 (B7-H1, also called programmed death ligand-1 [PD-L1]) was identified independently from PD-1 using molecular cloning and human expressed-sequence tag database searches based on its homology with B7 family molecules, and it was shown that PD-L1 acts as an inhibitor of human T cell responses in vitro (4). These two independent lines of study merged one year later when Freeman, Wood, and Honjo’s laboratories showed that PD-L1 is a binding and functional partner of PD-1 (5). Next, it was determined that PD-L1–deficient mice (Pdl1 KO mice) were prone to autoimmune diseases, although this strain of mice did not spontaneously develop such diseases (6). It became clear later that the PD-L1/PD-1 interaction plays a dominant role in the suppression of T cell responses in vivo, especially in the tumor microenvironment (7, 8).

In addition to PD-L1, another PD-1 ligand called B7-DC (also known as PD-L2) was also identified by the laboratories of Pardoll (9) and Freeman (10). This PD-1 ligand was found to be selectively expressed on DCs and delivered its suppressive signal by binding PD-1. Mutagenesis studies of PD-L1 and PD-L2 molecules guided by molecular modeling revealed that both PD-L1 and PD-L2 could interact with other molecules in addition to PD-1 and suggested that these interactions had distinct functions (11). The functional predictions from these mutagenesis studies were later confirmed when PD-L1 was found to interact with CD80 on activated T cells to mediate an inhibitory signal (12, 13). This finding came as a surprise because CD80 had been previously identified as a functional ligand for CD28 and cytotoxic T lymphocyte antigen-4 (CTLA-4) (14, 15). PD-L2 was also found to interact with repulsive guidance molecule family member b (RGMb), a molecule that is highly enriched in lung macrophages and may be required for induction of respiratory tolerance (16). With at least five interacting molecules in the PD-1/PD-L1 pathway (referred to as the PD pathway) (Figure 1), further studies will be required to understand the relative contributions of these molecules during activation or suppression of T cells.

The PD pathway. The PD pathway has at least 5 interacting molecules. PD-...

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The PD pathway.

The PD pathway has at least 5 interacting molecules. PD-L1 and PD-L2, with different expression patterns, were identified as ligands of PD-1, and the interaction of PD-L1 or PD-L2 with PD-1 may induce T cell suppression. PD-L1 was found to interact with B7-1 (CD80) on activated T cells and inhibit T cell activity. PD-L2 has a second receptor, RGMb; initially, this interaction activates T cells, but it subsequently induces respiratory tolerance. PD-L1 on tumor cells can also act as a receptor, and the signal delivered from PD-1 on T cells can protect tumor cells from cytotoxic lysis.

The discovery of the PD pathway did not automatically justify its application to cancer therapy, especially after the initial PD-1–deficient mouse studies, which suggested that PD-1 deficiency increases the incidence of autoimmune diseases (2, 3). In our initial work to characterize PD-L1 and its function, PDL1 mRNA was found to be broadly expressed in various tissues (17). However, normal human tissues seldom express PD-L1 protein on their cell surface, with the exception of tonsil (17), placenta (18), and a small fraction of macrophage-like cells in lung and liver (17), suggesting that, under normal physiological conditions, PDL1 mRNA is under tight posttranscriptional regulation. In sharp contrast, PD-L1 protein is abundantly expressed on the cell surface in various human cancers, as indicated by immunohistochemistry in frozen human tumor sections. Additionally, the pattern of PD-L1 expression was found to be focal rather than diffuse in most human cancers (17). In fact, the majority of in vitro–cultured tumor lines of both human and mouse origin are PD-L1–negative on the cell surface, despite overwhelming PD-L1 signal in specimens that are freshly isolated from patients with cancer (17, 19). This discrepancy was explained by the finding that IFN-γ upregulates PD-L1 on the cell surface of normal tissues and in various tumor lines (7, 17, 19). It was widely thought that IFN-γ typically promotes, rather than suppresses, T cell responses by stimulating antigen processing and presentation machinery (20, 21); therefore, the role of IFN-γ in downregulating immune responses in the tumor microenvironment via induction of PD-L1 was not well accepted until more recently. This finding is vital to our current understanding of the unique immunology that takes place in the tumor microenvironment and provided an important clue that led to the “adaptive resistance” hypothesis (see below) that explains this pathway’s mechanism of action to evade tumor immunity.

Due to the lack of cell surface expression of PD-L1 on most cultured tumor lines, it is necessary to reexpress PD-L1 on the surface using transfection to recapitulate the effects of cell surface PD-L1 in human cancers and to create models to study how tumor-associated PD-L1 interacts with immune cells. We now know that cancer cells and other cells in the tumor microenvironment can upregulate the expression of PD-L1 after encountering T cells, mostly via IFN-γ, which may make the transfection-mediated expression of PD-L1 unnecessary in some tumor models. Nevertheless, our results demonstrated that PD-L1+ human tumor cells could eliminate activated effector T cells (Teffs) via apoptosis in coculture systems, and this effect could be blocked by inclusion of an anti-human PD-L1 mAb (clone 2H1). Next, we generated a hamster mAb (clone 10B5) against mouse PD-L1 to block its interaction with T cells and test its role in tumor immunity in vitro and in vivo. We demonstrated that progressive growth of PD-L1+ murine P815 tumors in syngeneic mice could be suppressed using anti–PD-L1 mAb (17). Altogether, these studies represented the initial attempt at using mAb to block the PD pathway as an approach for cancer therapy. These proof-of-concept studies (17) were confirmed by several subsequent studies. A study from Nagahiro Minato’s laboratory showed that the J558L mouse myeloma line constitutively expressed high levels of cell surface PD-L1 and the growth of these cells in syngeneic BALB/c mice could be partially suppressed by administering anti–PD-L1 mAb (22). Our laboratory showed that regression of progressively growing squamous cell carcinomas in syngeneic mice could also be suppressed using a combination of adoptively transferred tumor-draining lymphocytes and anti–PD-L1 mAb (23). Furthermore, the Zou laboratory demonstrated that ovarian cancer–infiltrating human T cells could be activated in vitro using DCs, which showed enhanced activity in the presence of anti–PD-L1 mAb; upon transfer, these cells could eliminate established human ovarian cancers in immune-deficient mice (24). These early studies established the concept that the PD pathway could be used by tumors to escape immune attack in the tumor microenvironment. More importantly, these studies built a solid foundation for the development of anti-PD therapy for the treatment of human cancers.  …..

Anti-PD therapy has taken center stage in immunotherapies for human cancer, especially for solid tumors. This therapy is distinct from the prior immune therapeutic agents, which primarily boost systemic immune responses or generate de novo immunity against cancer; instead, anti-PD therapy modulates immune responses at the tumor site, targets tumor-induced immune defects, and repairs ongoing immune responses. While the clinical success of anti-PD therapy for the treatment of a variety of human cancers has validated this approach, we are still learning from this pathway and the associated immune responses, which will aid in the discovery and design of new clinically applicable approaches in cancer immunotherapy.

 

PD-1 Pathway Inhibitors: Changing the Landscape of Cancer Immunotherapy

Dawn E. Dolan, PharmD, and Shilpa Gupta, MD

Background: Immunotherapeutic approaches to treating cancer have been evaluated during the last few decades with limited success. An understanding of the checkpoint signaling pathway involving the programmed death 1 (PD-1) receptor and its ligands (PD-L1/2) has clarified the role of these approaches in tumor-induced immune suppression and has been a critical advancement in immunotherapeutic drug development. Methods: A comprehensive literature review was performed to identify the available data on checkpoint inhibitors, with a focus on anti–PD-1 and anti–PD-L1 agents being tested in oncology. The search included Medline, PubMed, the ClinicalTrials.gov registry, and abstracts from the American Society of Clinical Oncology meetings through April 2014. The effectiveness and safety of the available anti–PD-1 and anti–PD-L1 drugs are reviewed. Results: Tumors that express PD-L1 can often be aggressive and carry a poor prognosis. The anti–PD-1 and anti–PD-L1 agents have a good safety profile and have resulted in durable responses in a variety of cancers, including melanoma, kidney cancer, and lung cancer, even after stopping treatment. The scope of these agents is being evaluated in various other solid tumors and hematological malignancies, alone or in combination with other therapies, including other checkpoint inhibitors and targeted therapies, as well as cytotoxic chemotherapy. Conclusions: The PD-1/PD-L1 pathway in cancer is implicated in tumors escaping immune destruction and is a promising therapeutic target. The development of anti–PD-1 and anti–PD-L1 agents marks a new era in the treatment of cancer with immunotherapies. Early clinical experience has shown encouraging activity of these agents in a variety of tumors, and further results are eagerly awaited from completed and ongoing studies.

……

Role of PD-1/PD-L1 Pathway PD-1 is an immunoinhibitory receptor that belongs to the CD28 family and is expressed on T cells, B cells, monocytes, natural killer cells, and many tumor-infiltrating lymphocytes (TILs)10; it has 2 ligands that have been described (PD-L1 [B7H1] and PD-L2 [B7-DC]).11 Although PD-L1 is expressed on resting T cells, B cells, dendritic cells, macrophages, vascular endothelial cells, and pancreatic islet cells, PD-L2 expression is seen on macrophages and dendritic cells alone.10 Certain tumors have a higher expression of PD-L1.12 PD-L1 and L2 inhibit T-cell proliferation, cytokine production, and cell adhesion.13 PD-L2 controls immune T-cell activation in lymphoid organs, whereas PD-L1 appears to dampen T-cell function in peripheral tissues.14 PD-1 induction on activated T cells occurs in response to PD-L1 or L2 engagement and limits effector T-cell activity in peripheral organs and tissues during inflammation, thus preventing autoimmunity. This is a crucial step to protect against tissue damage when the immune system is activated in response to infection.15-17 Blocking this pathway in cancer can augment the antitumor immune response.18 Like the CTLA-4, the PD-1 pathway down-modulates Tcell responses by regulating overlapping signaling proteins that are part of the immune checkpoint pathway; however, they function slightly differently.14,16 Although the CTLA-4 focuses on regulating the activation of T cells, PD-1 regulates effector T-cell activity in peripheral tissues in response to infection or tumor progression.16 High levels of CTLA-4 and PD-1 are expressed on regulatory T cells and these regulatory T cells and have been shown to have immune inhibitory activity; thus, they are important for maintaining self-tolerance.16 The role of the PD-1 pathway in the interaction of tumor cells with the host immune response and the PD-L1 tumor cell expression may provide the basis for enhancing immune response through a blockade of this pathway.16 Drugs targeting the PD-1 pathway may provide antitumor immunity, especially in PD-L1 positive tumors. Various cancers, such as melanoma, hepatocellular carcinoma, glioblastoma, lung, kidney, breast, ovarian, pancreatic, and esophageal cancers, as well as hematological malignancies, have positive PD-L1 expression, and this expression has been correlated with poor prognosis.8,19 Melanoma and kidney cancer are prototypes of immunogenic tumors that have historically been known to respond to immunotherapeutic approaches with interferon alfa and interleukin 2. The CTLA-4 antibody ipilimumab is approved by the US Food and Drug Administration for use in melanoma. Clinical activity of drugs blocking the PD-1/PD-L1 pathway has been demonstrated in melanoma and kidney cancer.20-24 In patients with kidney cancer, tumor, TIL-associated PD-L1 expression, or both were associated with a 4.5-fold increased risk of mortality and lower cancer-specific survival rate, even after adjusting for stage, grade, and performance status.18,19,25,26 A correlation between PD-L1 expression and tumor growth has been described in patients with melanoma, providing the rationale for using drugs that block the PD-1/PD-L1 pathway.19,27 Historically, immunotherapy has been ineffective in cases of non–small-cell lung cancer (NSCLC), which has been thought to be a type of nonimmunogenic cancer; nevertheless, lung cancer can evade the immune system through various complex mechanisms.28 In patients with advanced lung cancer, the peripheral and tumor lymphocyte counts are decreased, while levels of regulatory T cells (CD4+), which help suppress tumor immune surveillance, have been found at higher levels.29-32 Immune checkpoint pathways involving the CTLA-4 or the PD-1/PD-L1 are involved in regulating T-cell responses, providing the rationale for blocking this pathway in NSCLC with antibodies against CTLA-4 and the PD-1/PD-L1 pathway.32 Triple negative breast cancer (TNBC) is an aggressive subset of breast cancer with limited treatment options. PD-L1 expression has been reported in patients with TNBC. When PD-L1 expression was evaluated in TILs, it correlated with higher grade and larger-sized tumors.33 Tumor PD-L1 expression also correlates with the infiltration of T-regulatory cells in TNBC, findings that suggest the role of PD-L1–expressing tumors and the PD-1/PD-L1–expressing TILs in regulating immune response in TNBC.34

…….

Preclinical evidence exists for the complementary roles of CTLA-4 and PD-1 in regulating adaptive immunity, and this provides rationale for combining drugs targeting these pathways.44-46 Paradoxically and originally believed to be immunosuppressive, new data allow us to recognize that cytotoxic agents can antagonize immunosuppression in the tumor microenvironment, thus promoting immunity based on the concept that tumor cells die in multiple ways and that some forms of apoptosis may lead to an enhanced immune response.8,15 For example, nivolumab was combined with ipilimumab in a phase 1 trial of patients with advanced melanoma.46 The combination had a manageable safety profile and produced clinical activity in the majority of patients, with rapid and deep tumor regression seen in a large proportion of patients. Based on the results of this study, a phase 3 study is being undertaken to evaluate whether this combination is better than nivolumab alone in melanoma (NCT01844505). Several other early-phase studies are underway to explore combinations of various anti–PD-1/PD-L1 drugs with other therapies across a variety of tumor types (see Tables 1 and 2), possibly paving the way for future combination studies.

 

Development of PD-1/PD-L1 Pathway in Tumor Immune Microenvironment and Treatment for Non-Small Cell Lung Cancer

Jiabei He, Ying Hu, Mingming Hu & Baolan Li

Lung cancer is currently the leading cause of cancer-related death in worldwide, non-small cell lung cancer (NSCLC) accounts for about 85% of all lung cancers. Surgery, platinum-based chemotherapy, molecular targeted agents and radiotherapy are the main treatment of NSCLC. With the strategies of treatment constantly improving, the prognosis of NSCLC patients is not as good as before, new sort of treatments are needed to be exploited. Programmed death 1 (PD-1) and its ligand PD-L1 play a key role in tumor immune escape and the formation of tumor microenvironment, closely related with tumor generation and development. Blockading the PD-1/PD-L1 pathway could reverse the tumor microenvironment and enhance the endogenous antitumor immune responses. Utilizing the PD-1 and/or PD-L1 inhibitors has shown benefits in clinical trials of NSCLC. In this review, we discuss the basic principle of PD-1/PD-L1 pathway and its role in the tumorigenesis and development of NSCLC. The clinical development of PD-1/PD-L1 pathway inhibitors and the main problems in the present studies and the research direction in the future will also be discussed.

Lung cancer is currently the leading cause of cancer-related death in the worldwide. In China, the incidence and mortality of lung cancer is 5.357/10000, 4.557/10000 respectively, with nearly 600,000 new cases every year1. Non-small cell lung cancer (NSCLC) accounts for about 85% of all lung cancers, the early symptoms of patients with NSCLC are not very obvious, especially the peripheral lung cancer. Though the development of clinic diagnostic techniques, the majority of patients with NSCLC have been at advanced stage already as they are diagnosed. Surgery is the standard treatment in the early stages of NSCLC, for the advanced NSCLC, the first-line therapy is platinum-based chemotherapy. In recent years, patients with specific mutations may effectively be treated with molecular targeted agents initially. The prognosis of NSCLC patients is still not optimistic even though the projects of chemotherapy as well as radiotherapy are continuously ameliorating and the launch of new molecular targeted agents is never suspended, the five-year survival rate of NSCLC patients is barely more than 15%2, the new treatment is needed to be opened up.

During the last few decades, significant efforts of the interaction between immune system and immunotherapy to NSCLC have been acquired. Recent data have indicated that the lack of immunologic control is recognized as a hallmark of cancer currently. Programmed death-1 (PD-1) and its ligand PD-L1 play a key role in tumor immune escape and the formation of tumor microenvironment, closely related with tumor generation and development. Blockading the PD-1/PD-L1 pathway could reverse the tumor microenvironment and enhance the endogenous antitumor immune responses.

In this review, we will discuss the PD-1/PD-L1 pathway from the following aspects: the basic principle of PD-1/PD-L1 pathway and its role in the tumorigenesis and development of NSCLC, the clinical development of several anti-PD-1 and anti-PD-L1 drugs, including efficacy, toxicity, and application as single agent, or in combination with other therapies, the main problems in the present studies and the research direction in the future.

 

Cancer as a chronic, polygene and often inflammation-provoking disease, the mechanism of its emergence and progression is very complicated. There are many factors which impacted the development of the disease, such as: environmental factors, living habits, genetic mutations, dysfunction of the immune system and so on. At present, increasing evidence has revealed that the development and progression of tumor are accompanied by the formation of special tumor immune microenvironment. Tumor cells can escape the immune surveillance and disrupt immune checkpoint of host in several methods, therefore, to avoid the elimination from the host immune system. Human cancers contain a number of genetic and epigenetic changes, which can produce neoantigens that are potentially recognizable by the immune system3, thus trigger the body’s T cells immune response. The T cells of immune system recognize cancer cells as abnormal primarily, generate a population of cytotoxic T lymphocytes (CTLs) that can traffic to and infiltrate cancers wherever they reside, and specifically bind to and then kill cancer cells. Effective protective immunity against cancer depends on the coordination of CTLs4. Under normal physiological conditions, there is a balance status in the immune checkpoint molecule which makes the immune response of T cells keep a proper intensity and scope in order to minimize the damage to the surrounding normal tissue and avoid autoimmune reaction. However, numerous pathways are utilized by cancers to up-regulate the negative signals through cell surface molecules, thus inhibit T-cell activation or induce apoptosis and promote the progression and metastasis of cancers5. Increasing experiments and clinical trails show that immunotherapeutic approaches utilizing antagonistic antibodies to block checkpoint pathways, can release cancer inhibition and facilitate antitumor activity, so as to achieve the purpose of treating cancer.

The present research of immune checkpoint molecules are mainly focus on cytotoxic T lymphocyte-associated antigen 4 (CLTA-4), Programmed death-1 (PD-1) and its ligands PD-L1 (B7H1) and PD-L2 (B7-DC). CTLA-4 regulates T cell activity in the early stage predominantly, and PD-1 mainly limits the activity of T-cell in the tumor microenvironment at later stage of tumor growth6. Utilizing the immune checkpoint blockers to block the interactions between PD-1 and its ligands has shown benefits in clinical trials, including the NSCLC patients. PD-1 and its ligands have been rapidly established as the currently most important breakthrough targets in the development of effective immunotherapy.

PD-1/PD-L1 pathway and its expression, regulation

PD-1 is a type 1 trans-membrane protein that encoded by the PDCD1 gene7. It is a member of the extended CD28/CTLA-4 immunoglobulin family and one of the most important inhibitory co-receptors expressed by T cells. The structure of the PD-1 includes an extracellular IgV domain, a hydrophobic trans-membrane region and an intracellular domain. The intracellular tail includes separate potential phosphorylation sites that are located in the immune receptor tyrosine-based inhibitory motif (ITIM) and in the immunoreceptor tyrosine-based switch motif (ITSM). Mutagenetic researches indicated that the activated ITSM is essential for the PD-1 inhibitory effect on T cells8. PD-1 is expressed on T cells, B cells, monocytes, natural killer cells, dendritic cells and many tumor-infiltrating lymphocytes (TILs)9. In addition, the research of Francisoet et al. showed that PD-1 was also expressed on regulatory T cells (Treg) and able to facilitate the proliferation of Treg and restrain immune response10.

PD-1 has two ligands: PD-L1 (also named B7-H1; CD274) and PD-L2 (B7-DC; CD273), that are both coinhibitory. PD-L1 is expressed on resting T cells, B cells, dendritic cells, macrophage, vascular endothelial cells and pancreatic islet cells. PD-L2 expression is seen on macrophages and dendritic cells alone and is far less prevalent than PD-L1 across tumor types. It shows much more restricted expression because of its more restricted tissue distribution. Differences in expression patterns suggest distinct functions in immune regulation across distinct cell types. The restricted expression of PD-L2, largely to antigen-presenting cells, is consistent with a role in regulating T-cell priming or polarization, whereas broad distribution of PD-L1 suggests a more general role in protecting peripheral tissues from excessive inflammation.

PD-L1 is expressed in various types of cancers, especially in NSCLC11,12, melanoma, renal cell carcinoma, gastric cancer, hepatocellular as well as cutaneous and various leukemias, multiple myeloma and so on13,14,15. It is present in the cytoplasm and plasma membrane of cancer cells, but not all cancers or all cells within a cancer express PD-L116,17. The expression of PD-L1 is induced by multiple proinflammatory molecules, including types I and II IFN-γ, TNF-α, LPS, GM-CSF and VEGF, as well as the cytokines IL-10 and IL-4, with IFN-γ being the most potent inducer18,19. IFN-γ and TNF-α are produced by activated type 1 T cells, and GM-CSF and VEGF are produced by a variety of cancer stromal cells, the tumor microenvironment upregulates PD-L1 expression, thereby, promotes immune suppression. This latter effect is called “adaptive immune resistance”, because the tumor protects itself by inducing PD-L1 in response to IFN-γ produced by activated T cells17. PD-L1 is regulated by oncogenes, also known as the inherent immune resistance. PD-L1 expression is suppressed by the tumor suppressor gene: PTEN (phosphatase and tension homolog deleted on chromosome ten) gene. Cancer cells frequently contain mutated PTEN, which can activate the S6K1 gene, thus results in PD-L1 mRNA to polysomes increase greatly20, hence increases the translation of PD-L1 mRNA and plasma membrane expression of PD-L1. Parsa et al.’s research also demonstrated that neuroglioma with PTEN gene deletion regulate PD-L1 expression at the translational level by activating the PI3K/AKT downstream mTOR-S6K1signal pathway and, hence increase the PD-L1 expression21. Micro-RNAs also translationally regulate PD-L1 expression. MiRNA-513 is complementary to the 3′ untranslated region of PD-L1 and prevents PD-L1 mRNA translation22. In addition, a later literature reported that in the model of melanoma, the up-regulation of PD-L1 is closely related to the CD8 T cell, independent of regulation by oncogenes13. Noteworthily, the PD-L1 can bind to T cell expressed CD80, and at this point CD80 is a receptor instead of ligand to transmit negative regulated signals23.

 

PD-1/PD-L1 mediate immune suppression by multiple mechanisms

Like the CTLA-4, the PD-1/PD-L1 pathway down-modulates T-cell response by regulating overlapping signal proteins in the immune checkpoint pathway. However, their functions are slightly different24. The CTLA-4 focuses on regulating the activation of T cells, while PD-1 regulates effector T-cell activity in peripheral tissues in response to infection or tumor progression25. Tregs that high-level expression of PD-1 have been shown to have immune inhibitory activity, thus, they are important for maintaining self-tolerance. In normal human bodies, this is a crucial step to protect against tissue damage when the immune system is activated in response to infection26. However, in response to immune attack, cancer cells overexpress PD-L1 and PD-L2. They bind to PD-1 receptor on T cells, inhibiting the activation of T-cells, thus suppressing T-cell attack and inducing tumor immune escape. Thus tumor cells effectively form a suitable tumor microenvironment and continue to proliferate27. PD-1/PD-L1 pathway regulates immune suppression by multiple mechanisms, specific performance of the following: Induce apoptosis of activated T cells: PD-1 reduces T cell survival by impacting apoptotic genes. During T cell activation, CD28 ligation sustains T cell survival by driving expression of the antiapoptotic gene Bcl-xL. PD-1 prevents Bcl-xL expression by inhibiting PI3K activation, which is essential for upregulation of Bcl-xL. Early studies demonstrated that PD-L1+ murine and human tumor cells induce apoptosis of activated T cells and that antibody blocking of PD-L1 can decrease the apoptosis of T cells and facilitate antitumor immunity28,16. Facilitate T cell anergy and exhaustion: A research shown that the occurrence of tumor is associated with chronic infection29. According to the study of chronic infection, PD-1 overexpressed on the function exhausted T cells, blocking the PD-1/PD-L1 pathway can restore the proliferation, secretion and cytotoxicity30. In addition, later research demonstrated that the exhaustion of TILs in the tumor microenvironment is closely related to the PD-L1 expression of tumor cells, myeloid cells derived from tumor31. Enhance the function of regulatory T cells: PD-L1 can promote the generation of induced Tregs by down-regulating the mTOR, AKT, S6 and the phosphorylation of ERK2 and increasing PTEN, thus restrain the activity of effector T-cell32. Blocking the PD-1/PD-L1 pathway can increase the function of effector CD8 T-cell and inhibt the function of Tregs, bone marrow derived inhibition cells, thus enhance the anti-tumor response. Inhibit the proliferation of T cells: PD-1 ligation also prevents phosphorylation of PKC-theta, which is essential for IL-2 production33, and arrests T cells in the G1 phase, blocking proliferation. PD-1 mediates this effect by activating Smad3, a factor that arrests cycling34. Restrain impaired T cell activation and IL-2 production: PD-1/PD-L1 blocks the downstream signaling events triggered by Ag/MHC engagement of the TCR and co-stimulation through CD28, resulting in impaired T cell activation and IL-2 production. Signaling through the TCR requires phosphorylation of the tyrosine kinase ZAP70. PD-1 engagement reduces the phosphorylation of ZAP70 and, hence, inhibits downstream signaling events. In addition, signaling through PD-1 also prevents the conversion of functional CD8+ T effector memory cells into CD8+ central memory cells35 and, thus, reduces long-term immune memory that might protect against future metastatic disease. PD-L1 also promotes tumor progression by reversing signaling through CD80 into T cells. CD80-PD-L1 interactions restrain self-reactive T cells in an autoimmune setting36, therefore, their inhibition may facilitate antitumor immunity.

Researches on the mechanism of PD-1/PD-L1 pathway mediating immune escape are still ongoing, especially the mechanism of PD-L2 is still unclear. These researches provide the theoretical basis and research direction for the further immunotherapy targets research.

 

Anti-PD-1 antibodies

Nivolumab

Nivolumab (BMS-936558, Brand name: Opdivo) is a human monoclonal IgG4 antibody that essentially lacks detectable antibody-dependent cellular cytotoxicity (ADCC). Inhibition by monoclonal antibody of PD-1 on CD8+ TILs within lung cancers can restore cytokine secretion and T-cell proliferation48. Results of a larger phase I study in 296 patients (236 patients evaluated) reported that the objective response (complete or partial responses) of patients with NSCLC was 18%. A total of 65% of responders had durable responses lasting for more than 1 year. Stable disease lasting 24 weeks was seen in patients with NSCLC. PD-L1expression was tested in 42 patients: 9 of 25(36%) patients whose PD-L1 expression positive were objectively response to PD-1 blockade treatment, while the remaining 17 nonresponsive patients were negative45.

In another early phase I trial of nivolumab49, an objective response was observed in 22 patients (17%; 95% CI, 11%–25%) in a dose-expansion cohort of 129 previously treated patients with advanced NSCLC. Six additional patients who had an unconventional immune-related response were not included. Moreover, the median duration of response was exceptional for 17 months. Although the median PFS in the cohort was 2.3 months and the median overall survival was 9.9 months, it seemed clear that those who responded had sustained benefit. Specifically, the 2-year overall survival rate was 24%, and many remained in remission after completing 96 weeks of continuous therapy.

Single-agent trials of nivolumab are planning or ongoing on NSCLC (NCT01721759, NCT02066636). In addition, there are clinical randomized trials which focus on the comparison of nivolumab and plain-based combination chemotherapy (NCT02041533, NCT01673867). In March 4, 2015, nivolumab was approved by the US Food and Drug Administration for treatment of patients with metastatic NSCLC (squamous cell carcinoma), when progression of their diseases during or after chemotherapy with platinum-based drugs.

Pembrolizumab

Pembrolizumab (MK-3475) is a highly selective, humanized monoclonal antibody with activity against PD-1 that contains a mutation at C228P designed to prevent Fc-mediated ADCC. It is now in the clinical research phases for patients with advanced solid tumors. Its safety and efficacy were evaluated in a phase I clinical trial of KEYNOTE-001. The best response according of 38 cases of patients which initially accepted pembrolizumab 10 mg/kg q3wwas 21% (based on RECIST1.1 evaluation) and the median PFS of responder still has not reached until 62 weeks. The researchers also found that the antitumor activity of pembrolizumab was associated with the PD-L1expression44,50. The critical values of the expression of PD-L1 will be validated in 300 cases of patients which will soon been rolled into the study.

Clinical trial of pembrolizumab monotherapy is ongoing for patients with NSCLC (NCT01840579). Randomized trials comparing pembrolizumab to combination chemotherapy (NCT02142738) or single-agent docetaxel (NCT01905657) are ongoing in PD-L1 positive patients with NSCLC.

Pidilizumab (CT-011)

Pidilizumab is a humanized IgG-1K recombinant anti-PD-1 monoclonal antibody that has demonstrated antitumor activity in mouse cancer models. In a first-in-human phase I dose-escalation study in patients with only advanced hematologic cancers, there is no clinical trials of NSCLC presently51.

 

Anti-PD-L1 antibodies

Another therapeutic method based on the PD-1/PD-L1 pathway is by specific binding between antibody and PD-L1, thus preventing its activity. It was speculated that utilizing PD-L1 as therapeutic target maybe accompanied by less toxicity in part by modulating the immune response selectively in the tumor microenvironment. However, since PD-L2 expressed by tumor cells or some other tumor-associated molecules may play a role in mediating PD-1-expressing lymphocytes, it is conceivable that the magnitude of the anti-tumor immune response could also be blunted.

BMS-936559

BMS-936559/MDX1105 is a fully humanized, high affinity, IgG4 monoclonal antibody that react specifically with PD-L1, thus inhibiting the binding of PD-L1 and PD-1, CD80 (which binds not only PD-L1 but also CTLA-4 and CD28). Initial results from a multicenter and dose-escalation phase I trial of 207 patients(including 75 cases of patients with NSCLC) showed durable tumor regression (objective response rate of 6%–17%) and prolonged stabilization of disease (12%–41% at 24weeks) in patients with advanced cancers, including NSCLC, melanoma and kidney cancer. In patients with NSCLC, there were five objective responses (in 4 patients with the nonsquamous subtype and 1 with the squamous subtype) at doses of 3 mg/kg and 10 mg/kg, with response rates of 8% and 16%, respectively. Six additional patients with NSCLC had stable disease lasting at least 24 weeks52.

MPDL3280A

MPDL3280A is a human IgG1 antibody that targets PD-L1. Its Fc component has been engineered to not activate antibody-dependent cell cytotoxicity. In a recently reported phase I study, a 21% response rate was noted in patients with metastatic melanoma, RCC or NSCLC53, including several patients who demonstrated shrinkage of tumor within a few days of initiating treatment.

Fifty-two patients were enrolled in an expansion cohort of the phase I trial of MPDL3280A, 62% of them were heavily pretreated NSCLC (≥3 lines of systemic therapy) and the ORR was 22%54. Analysis of biomarker data from archival tumor samples demonstrated a correlation between PD-L1 status and response and lack of progressive disease55.

MEDI4736

MEDI4736 is a human IgG1 antibody that binds specifically to PD-L1, thus preventing PD-L1 binding to PD-1 and CD80. Interim results from a phase I trial reported no colitis or pneumonitis of any grade, with several durable remissions, including NSCLC patients56. An ongoing phase I dose-escalation study (NCT01693562) of MEDI-4736 in 26 patients, 4 partial responses (3 in patients with NSCLC and 1 with melanoma) were observed and 5 additional patients exhibited lesser degrees of tumor shrinkage. The disease control rate at 12 weeks was 46%57. Expansion cohorts was opened in Sep 2013, 10 mg/kg q2w dose. 151 patients was enrolled so far in the expansion cohorts, tumor shrinkage was reported as early as the first assessment at 6 weeks and among the 13 patients with NSCLC, responses were sustained at 10 or more to 14.9 or more months58. In the NSCLC expansion cohort, the response rate was 16% in 58 evaluable patients and the disease control rate at 12 weeks was 35% with responses seen in all histologic subtypes as well as in a smaller proportion of PD-L1- tumors.

On the basis of the favorable toxicity profile and promising activity in a heavily pretreated NSCLC population, a global Phase III placebo controlled trial using the 10 mg/kg biweekly dose has been launched in Stage III patients who have not progressed following chemo-radiation (NCT02125461). The primary outcome measures are overall survival and progression-free survival.

AMP-224

AMP-224 was a B7-DC-Fc fusion protein which can block the PD-1 receptor competitively59. Some NSCLC patients were included in a first-in-man phase I trial of this fusion protein drug. A dose-dependent reduction in PD-1-high TILs was observed at 4 hours and 2 weeks after drug administration60.

 

A variety of approaches for combining PD-1/PD-L1 pathway inhibitors with other therapeutic methods have been explored over the past few years in an effort to offer more feasible therapeutic options for clinic to improve treatment outcomes. Approaches have included combinations with other immune checkpoint inhibitors, immunostimulatory cytokines (e.g. IFN-y) cytotoxic chemotherapy, platinum-based chemotherapy, radiotherapy, anti-angiogenic inhibitors, tumor vaccine and small-molecule molecularly targeted therapies many with promising results61,62. Studies indicated that PD-1/PD-L1 pathway inhibitors were most effective when combined with treatments that activating the immune system63.

Preclinical evidence exists for the complementary roles of CTLA-4 and PD-1 in regulating adaptive immunity, and this provides rationale for combining drugs targeting these pathways. In a Phase I study in 46 chemotherapy-naive patients with NSCLC, four cohorts of patients received ipilimumab (3 mg/kg) plus nivolumab for four cycles followed by nivolumab 3 mg/kg intravenously every 2 weeks. The ORR was 22% and did not correlate with PD-L1 status64.

In another Phase I study, 56 patients with advanced NSCLC were assigned based on histology to four cohorts to receive nivolumab (5–10 mg/kg) intravenously every 3 weeks plus one of four concurrent standard “platinum doublet” chemotherapy regimens. No dose de-escalation was required for dose-limiting toxicity. The ORR was 33–50% across arms and the 1-year OS rates were promising at 59–87%65.

…..

The research of cancer immunotherapy provides a new wide space for cancer treatment (including NSCLC), and compared with other therapeutic method, immunotherapy has its unique advantages, such as: relative safety, effectivity, less and low grade side effect and so on. Especially with the discovery and continued in-depth study of PD-1/PD-L1 pathway in the immune regulation mechanism, many significative conclusions were reported. Data from many clinical trails suggest that some patients with NSCLC have been benefited from the drugs of anti-PD-1 and anti-PD-L1 already. However, summarized what have been discussed above, only a small fraction of patients benefit from PD-1 or PD-L1 inhibitors treatment. But with the continuous studies on biomarker and combined treatment in PD-1/PD-L1 pathway, new research progress will be acquired as well. We will make significant progress on treatment and in control of NSCLC.

 

Prospects for Targeting PD-1 and PD-L1 in Various Tumor Types     

Table 1: Selected Anti–PD-1 and Anti–PD-L1 Antibodies
Table 2: Selected Adverse Events
Table 3: Selected Clinical Trials for Metastatic Melanoma
Table: 4 Selected Trials for Metastatic Renal Cell Carcinoma
Table 5: Selected Trials for Non–Small-Cell Lung Cancer (NSCLC )
Table 6: Selected Trials for Other Tumor Types

Immune checkpoints, such as programmed death ligand 1 (PD-L1) or its receptor, programmed death 1 (PD-1), appear to be Achilles’ heels for multiple tumor types. PD-L1 not only provides immune escape for tumor cells but also turns on the apoptosis switch on activated T cells. Therapies that block this interaction have demonstrated promising clinical activity in several tumor types. In this review, we will discuss the current status of several anti–PD-1 and anti–PD-L1 antibodies in clinical development and their direction for the future.

Several PD-1 and PD-L1 antibodies are in clinical development (Table 1). Overall, they are very well tolerated; most did not reach dose-limiting toxicity in their phase I studies. As listed in Table 2, no clinically significant difference in adverse event profiles has been seen between anti–PD-1 and anti–PD-L1 antibodies. Slightly higher rates of infusion reactions (11%) were observed with BMS-936559 (anti–PD-L1) than with BMS-96558 (nivolumab). In an early stage of a nivolumab phase I study, there was concern about fatal pneumonitis.[7] It has been hypothesized that PD-1 interaction with PD-L2 expressed on the normal parenchymal cells of lung and kidney provides unique negative signaling that prevents autoimmunity.[8] Thus, anti–PD-1 antibody blockage of such an interaction may remove this inhibition, allowing autoimmune pneumonitis or nephritis. Anti–PD-L1 antibody, however, would theoretically leave PD-1–PD-L2 interaction intact, preventing the autoimmunity caused by PD-L2 blockade. With implementation of an algorithm to detect early signs of pneumonitis and other immune-related adverse events, many of these side effects have become manageable. However, it does require discerning clinical attention to detect potentially fatal side effects. In terms of antitumor activity, both anti–PD-1 and anti–PD-L1 antibodies have shown responses in overlapping multiple tumor types. Although limited to a fraction of patients, most responses, when observed, were rapid and durable.

– See more at: http://www.cancernetwork.com/oncology-journal/prospects-targeting-pd-1-and-pd-l1-various-tumor-types#sthash.an8uOYLi.dpuf

 

Immune Checkpoint Blockade in Cancer Therapy

Michael A. PostowMargaret K. Callahan and Jedd D. Wolchok
http://jco.ascopubs.org/content/early/2015/01/20/JCO.2014.59.4358.full
 http://dx.doi.org:/10.1200/JCO.2014.59.4358

Immunologic checkpoint blockade with antibodies that target cytotoxic T lymphocyte–associated antigen 4 (CTLA-4) and the programmed cell death protein 1 pathway (PD-1/PD-L1) have demonstrated promise in a variety of malignancies. Ipilimumab (CTLA-4) and pembrolizumab (PD-1) are approved by the US Food and Drug Administration for the treatment of advanced melanoma, and additional regulatory approvals are expected across the oncologic spectrum for a variety of other agents that target these pathways. Treatment with both CTLA-4 and PD-1/PD-L1 blockade is associated with a unique pattern of adverse events called immune-related adverse events, and occasionally, unusual kinetics of tumor response are seen. Combination approaches involving CTLA-4 and PD-1/PD-L1 blockade are being investigated to determine whether they enhance the efficacy of either approach alone. Principles learned during the development of CTLA-4 and PD-1/PD-L1 approaches will likely be used as new immunologic checkpoint blocking antibodies begin clinical investigation.

CTLA-4 was the first immune checkpoint receptor to be clinically targeted (Fig 1) Normally, after T-cell activation, CTLA-4 is upregulated on the plasma membrane where it functions to downregulate T-cell function through a variety of mechanisms, including preventing costimulation by outcompeting CD28 for its ligand, B7, and also by inducing T-cell cycle arrest.15 Through these mechanisms and others, CTLA-4 has an essential role in maintaining normal immunologic homeostasis, as evidenced by the fact that mice deficient in CTLA-4 die from fatal lymphoproliferation.6,7 Recognizing the role of CTLA-4 as a negative regulator of immunity, investigators led studies demonstrating that antibody blockade of CTLA-4 could result in antitumor immunity in preclinical models.8,9

Fig 1.

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http://ascopubs.org/doi/figure/10.1200/JCO.2014.59.4358

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http://jco.ascopubs.org/content/early/2015/01/20/JCO.2014.59.4358/F1.medium.gif

Fig 1.

The cytotoxic T lymphocyte–associated antigen 4 (CTLA-4) immunologic checkpoint. T-cell activation requires antigen presentation in the context of a major histocompatibility complex (MHC) molecule in addition to the costimulatory signal achieved when B7 on an antigen-presenting cell (dendritic cell shown) interacts with CD28 on a T cell. Early after activation, to maintain immunologic homeostasis, CTLA-4 is translocated to the plasma membrane where it downregulates the function of T cells.

On the basis of this preclinical rationale, two antibodies targeting CTLA-4, ipilimumab (Bristol-Myers Squibb, Princeton, NJ) and tremelimumab (formerly Pfizer, currently MedImmune/AstraZeneca, Wilmington, DE), entered clinical development. Early reports of both agents showed durable clinical responses in some patients.1012Unfortunately, despite a proportion of patients experiencing a durable response, tremelimumab did not statistically significantly improve overall survival, which led to a negative phase III study comparing tremelimumab to dacarbazine/temozolomide in patients with advanced melanoma.13 It is possible that the lack of an overall survival benefit was a result of the crossover of patients treated with chemotherapy to an expanded access ipilimumab program or a result of the dosing or scheduling considerations of tremelimumab.

Ipilimumab, however, was successful in improving overall survival in two phase III studies involving patients with advanced melanoma.14,15 Although the median overall survival was only improved by several months in each of these studies, landmark survival after treatment initiation favored ipilimumab; in the first phase III study, 18% of patients were alive after 2 years compared with 5% of patients who received the control treatment of gp100 vaccination.14 More recently reported pooled data from clinical trials of ipilimumab confirm that approximately 20% of patients will have long-term survival of at least 3 years after ipilimumab therapy, with the longest reported survival reaching 10 years.1618

For patients with other malignancies, CTLA-4 antibody therapy has also shown some benefits. Ipilimumab, in combination with carboplatin and paclitaxel in a phased treatment schedule, showed improved progression-free survival compared with carboplatin and paclitaxel alone for patients with non–small-cell lung cancer.19Several patients with pancreatic cancer had declines in CA 19-9 when ipilimumab was given with GVAX (Aduro, Berkeley, CA),20and ipilimumab has also resulted in responses in patients with prostate cancer.21 Unfortunately, a phase III study in patients with castrate-resistant prostate cancer who experienced progression on docetaxel chemotherapy demonstrated that after radiotherapy, ipilimumab did not improve overall survival compared with placebo.22 Although this study is felt to have been a negative study, ipilimumab may have conferred a benefit to patients with favorable prognostic features, such as the absence of visceral metastases, but this requires further study. Another CTLA-4–blocking antibody, tremelimumab, has shown responses in patients with mesothelioma, and ongoing trials are under way.23

CTLA-4 blockade has also been administered together with other immunologic agents, such as the indoleamine 2,3-dioxygenase inhibitor INCB024360,106 the oncolytic virus talimogene laherparepvec,107 and granulocyte-macrophage colony-stimulating factor,108 with encouraging early results. We expect subsequent studies involving engineered T-cell–based therapies and checkpoint blockade.

Other promising data involve CTLA-4 combinations with PD-1 blockade. A phase I study of ipilimumab and nivolumab in patients with melanoma resulted in a high durable response rate and impressive overall survival compared with historical data.109,110Although the most recently reported grade 3 or 4 toxicity rate in patients with melanoma was 64%, which is higher than either ipilimumab or nivolumab individually,111 the vast majority of these irAEs were asymptomatic laboratory abnormalities of unclear clinical consequence. For example, elevations in amylase or lipase were reported in 21% of patients, none of whom met clinical criteria for a diagnosis of pancreatitis. The rate of grade 3 or 4 diarrhea was 7%, which is approximately similar to the rate of grade 3 or 4 diarrhea with ipilimumab monotherapy at 3 mg/kg. Whether ipilimumab and nivolumab improve overall survival compared with either nivolumab or ipilimumab alone remains the subject of an ongoing phase III randomized trial, and investigations of the combination of ipilimumab and nivolumab (and tremelimumab and MEDI4736) are ongoing in many other cancers.

Immunotherapy with checkpoint-blocking antibodies targeting CTLA-4 and PD-1/PD-L1 has improved the outlook for patients with a variety of malignancies. Despite the promise of this approach, many questions remain, such as the optimal management of irAEs and how best to evaluate combination approaches to determine whether they will increase the efficacy of CTLA-4 or PD-1/PD-L1 blockade alone. Themes from the experience with CTLA-4 and PD-1/PD-L1 will likely be relevant for investigations of novel immunologic checkpoints in the future.

This is a very important article, Dr. Larry.

It fits so beautiful with our work on Molecules in Development Table.

Thank you

 

This image depicts the process of metastasis in a mouse tumor, where tumor cells (green) have helped to reorganize the collagen into aligned fibers (blue) that provide the structural support for motility. This helps the tumor cells to enter blood vessels (red), ultimately leading to the formation of metastases in other organs.

http://news.mit.edu/sites/mit.edu.newsoffice/files/styles/news_article_image_top_slideshow/public/images/2016/MIT-Cancer-Migration-1_0.jpg?itok=aEOCRQpn

This image depicts the process of metastasis in a mouse tumor, where tumor cells (green) have helped to reorganize the collagen into aligned fibers (blue) that provide the structural support for motility. This helps the tumor cells to enter blood vessels (red), ultimately leading to the formation of metastases in other organs.  Image: Madeleine Oudin and Jeff Wyckoff

Paving the way for metastasis

Cancer cells remodel their environment to make it easier to reach nearby blood vessels.

Anne Trafton | MIT News Office     March 15, 2016

 

A new study from MIT reveals how cancer cells take some of their first steps away from their original tumor sites. This spread, known as metastasis, is responsible for 90 percent of cancer deaths.

Studying mice, the researchers found that cancer cells with a particular version of the Mena protein, called MenaINV (invasive), are able to remodel their environment to make it easier for them to migrate into blood vessels and spread through the body. They also showed that high levels of this protein are correlated with metastasis and earlier deaths among breast cancer patients.

Finding a way to block this protein could help to prevent metastasis, says Frank Gertler, an MIT professor of biology and a member of the Koch Institute for Integrative Cancer Research.

“That’s something that I think would be very promising, because we know that when we genetically remove MenaINV, the tumors become nonmetastatic,” says Gertler, who is the senior author of a paper describing the findings in the journal Cancer Discovery.

Madeleine Oudin, a postdoc at the Koch Institute, is the paper’s lead author.

On the move

For cancer cells to metastasize, they must first become mobile and then crawl through the surrounding tissue to reach a blood vessel. In the new study, the MIT team found that cancer cells follow the trail of fibronectin, a protein that is part of the “extracellular matrix” that provides support for surrounding cells. Fibronectin is found in particularly high concentrations around the edges of tumors and near blood vessels.

“Cancer cells within a tumor environment are constantly faced with differences in fibronectin concentrations, and they need to be able to move from low to high concentrations to reach the blood vessels,” Oudin says.

MenaINV, an alternative form of the normal Mena protein, is key to this process. MenaINV includes a segment not found in the normal version, and this makes it bind more strongly to a receptor known as alpha-5 integrin, which is found on the surfaces of tumor cells and nearby supporting cells, and recognizes fibronectin.

When MenaINV attaches to this receptor, it promotes the binding of fibronectin to the same receptors. Fibronectin is normally a tangled protein, but when it binds to cell surfaces, it gets stretched out into long bundles. This stimulates the organization of collagen, another extracellular matrix protein, into stiff fibrils that radiate from the edges of the tumor.

This pattern, which is typically seen in tumors that are more aggressive, essentially paves the way for tumor cells to move toward blood vessels.

“If you have curly, coiled collagen, that’s associated with a good outcome, but if it gets realigned into these really straight long fibers, that provides highways for these cells to migrate on,” Oudin says.

In studies of mice, cells with the invasive form of Mena were better able to recognize and crawl toward higher concentrations of fibronectin, moving along the collagen pathways, while cells without MenaINV did not move toward the higher concentrations.

Predicting metastasis

The researchers also looked at data from breast cancer patients and found that high levels of MenaINV and fibronectin are associated with metastasis and earlier death. However, there was no link between the normal version of Mena and earlier death.

Gertler’s lab had previously developed antibodies that can detect the normal and invasive forms of Mena, which are now being developed for testing patient biopsy samples. Such tests could help doctors to determine whether a patient’s tumor is likely to spread or not, and possibly to guide the patient’s treatment. In addition, scientists may be able to develop drugs that inhibit MenaINV, which could be useful for treating cancer or preventing it from metastasizing.

The researchers now hope to study how MenaINV may contribute to other types of cancers. Preliminary studies suggest that it plays a similar role in lung and colon cancers as that seen in breast cancer. They are also investigating how the choice between the two forms of the Mena protein is regulated, and how other proteins found in the extracellular matrix might contribute to cancer cell migration.

Facilitating Tumor Cell Migration

Researchers identify a modified form of a migration-regulating protein in cancer cells that remodels the tumor microenvironment to promote metastasis.
By Catherine Offord | March 16, 2016

Emerging evidence suggests that metastasis—the spread of cancer from one organ or tissue to another—is aided by a significant remodeling of the cancer cells’ surroundings. Now, researchers at MIT have made progress toward understanding the mechanisms involved in this process by highlighting the role of a protein that reorganizes the tumor’s extracellular matrix to facilitate cellular migration into blood vessels. The findings were published yesterday (March 15) in Cancer Discovery.

Using a mouse model, the team showed that a cancer-cell-expressed protein called MenaINV—a mutated, “invasive” form of the cell-migration-modulator Mena—binds more strongly than its normal equivalent to a receptor on tumor and nearby support cells. The binding rearranges fibronectin in the tumor microenvironment, which in turn triggers the reorganization of collagen in the extracellular matrix into linear fibers radiating from the tumor.

This collagen restructuring is key in facilitating the migration of tumor cells to the blood vessels, from where they can disseminate throughout the body.

Tumor cell-driven extracellular matrix remodeling enables haptotaxis during metastatic progression

Madeleine J. Oudin1Oliver Jonas1Tatsiana Kosciuk1Liliane C. Broye1Bruna C. Guido1Jeff Wyckoff1, …., James E. Bear2 and Frank B. Gertler1,*
Cancer Discov CD-15-1183  Jan 25, 2016  http://dx.doi.org:/10.1158/2159-8290.CD-15-1183

Fibronectin (FN) is a major component of the tumor microenvironment, but its role in promoting metastasis is incompletely understood. Here we show that FN gradients elicit directional movement of breast cancer cells, in vitro and in vivo. Haptotaxis on FN gradients requires direct interaction between α5β1 integrin and Mena, an actin regulator, and involves increases in focal complex signaling and tumor-cell-mediated extracellular matrix (ECM) remodeling. Compared to Mena, higher levels of the pro-metastatic MenaINV isoform associate with α5, which enables 3D haptotaxis of tumor cells towards the high FN concentrations typically present in perivascular space and in the periphery of breast tumor tissue. MenaINV and FN levels were correlated in two breast cancer cohorts, and high levels of MenaINV were significantly associated with increased tumor recurrence as well as decreased patient survival. Our results identify a novel tumor-cell-intrinsic mechanism that promotes metastasis through ECM remodeling and ECM guided directional migration.

 

Researchers Find Link Between Death of Tumor-support Cells and Cancer Metastasis       Fri, 02/19/2016
http://www.dddmag.com/news/2016/02/researchers-find-link-between-death-tumor-support-cells-and-cancer-metastasis#.VuatbTol_kI.linkedin

The images show tumors that have metastasized to the lungs (image b) and bones (image d) in mice that had CAFs eliminated after 10 days. (Credit: Biju Parekkadan, Massachusetts General Hospital)

http://www.dddmag.com/sites/dddmag.com/files/20160219-metastasized-cells%20%281%29.jpg

The images show tumors that have metastasized to the lungs (image b) and bones (image d) in mice that had CAFs eliminated after 10 days. (Credit: Biju Parekkadan, Massachusetts General Hospital)

Researchers have discovered that eliminating cells thought to aid tumor growth did not slow or halt the growth of cancer tumors. In fact, when the cancer-associated fibroblasts (CAFs), were eliminated after 10 days, the risk of metastasis of the primary tumor to the lungs and bones of mice increased dramatically. Scientists used bioengineered CAFs equipped with genes that caused those cells to self-destruct at defined moments in tumor progression. The study, published in Scientific Reports on Feb. 19, was conducted by researchers funded by the National Institute of Biomedical Imaging and Bioengineering (NIBIB) at Massachusetts General Hospital (MGH). NIBIB is part of the National Institutes of Health.

What causes cancer to grow and metastasize is not well understood by scientists. CAFs are thought to be fibroblast cells native to the body that cancer cells hijacks and use to sustain their growth. However, because fibroblasts are found throughout the human body, it can be difficult to follow and study cancer effects on these cells.

“This work underscores two important things in solving the puzzle that is cancer,” said Rosemarie Hunziker, Ph.D., program director for Tissue Engineering at NIBIB. “First, we are dealing with a complex disease with so many dimensions that we are really only just beginning to describe it.  Second, this approach shows the power of cell engineering — manipulating a key cell in the cancer environment has led to a significant new understanding of how cancer grows and how it might be controlled in the future.”

Biju Parekkadan, Ph.D., assistant professor of surgery and bioengineering at MGH, and his team designed an experiment with the goal of better understanding the cellular environment in which tumors exist (called tumor microenvironment or TME), and the role of CAFs in tumor growth. In an effort to understand whether targeting CAFs could limit the growth of breast cancer tumors implanted in mice, they bioengineered CAFs with a genetic “kill switch.” The cells were designed to die when exposed to a compound that was not toxic to the surrounding cells.

Parekkadan and his team chose two different stages of tumor growth in which the CAFs were killed off after the tumor was implanted. When the CAFs were eliminated on the third or fourth day, they found no major difference in tumor growth or risk of metastasis compared with the tumors where the CAFs remained. However, there was an increase in tumor-associated macrophages — cells that have been associated with metastasis — in this early stage.

When the team waited to eliminate the CAFs until the 10th or 11th day, they discovered that in addition to the increase in macrophages, the cancer was more likely to spread to the lungs and bones of the mice. The unexpected results from this experiment could spur more research into the role of CAFs in cancer growth and metastasis.

More research may reveal whether or not there is a scientific basis for targeting CAFs for destruction — and if so, the awareness that timing matters when it comes to the response of the tumor. While neither treatment affected the growth of the initial tumor, it is important to understand that most cancer deaths result from metastases to vital organs rather than from the direct effects of the primary tumor.

 

 

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Christopher J. Lynch, MD, PhD, the New Office of Nutrition Research, Director

Curator: Larry H. Bernstein, MD, FCAP

 

Christopher J. Lynch to direct Office of Nutrition Research

National Institute of Diabetes and Digestive and Kidney Diseases (NIDDK)

http://www.nih.gov/news-events/news-releases/christopher-j-lynch-direct-office-nutrition-research

 

Christopher J. Lynch, Ph.D., has been named the new director of the Office of Nutrition Research (ONR) and chief of the Nutrition Research Branch within the National Institute of Diabetes and Digestive and Kidney Diseases (NIDDK). Lynch officially assumed his new roles on Feb. 21, 2016. NIDDK is part of the National Institutes of Health.

Lynch will facilitate nutrition research within NIDDK and — through ONR — across NIH, in part by forming and leading a trans-NIH strategic working group. He will also continue and extend ongoing efforts at NIDDK to collaborate widely to advance nutrition research.

“Dr. Lynch is a leader in the nutrition community and his expertise will be vital to guiding the NIH strategic plan for nutrition research,” said NIH Director Francis S. Collins, M.D., Ph.D.  “As NIH works to expand nutrition knowledge, Dr. Lynch’s understanding of the field will help identify information gaps and create a framework to support future discoveries to ultimately improve human health.”

NIH supports a broad range of nutrition research, including studies on the effects of nutrient and dietary intake on human growth and disease, genetic influences on human nutrition and metabolism and other scientific areas. ONR was established in August 2015 to help NIH develop a strategic plan to expand mission-specific nutrition research.

NARRATIVE:
Our laboratory is dedicated to developing cures for metabolic diseases like Obesity, Diabetes and MSUD. We have several projects:
Project 1: How Antipsychotic Drugs Exert Obesity and Metabolic Disease Side effects
Project 2: Impact of Branched Chain Amino Acid (BCAA) signaling and metabolism in obesity and diabetes.
Project 3: Adipose tissue transplant as a treatment for Maple Syrup Urine Disease.
Project 4: How Gastric Bypass Surgery Provides A Rapid Cure For Diabetes And Other Obesity Co-Morbidities Like Hypertension
Project 5: Novel Mechanism Of Action Of Cannabinoid Receptor 1 Blockers For Improvement Of Diabetes

Timeline

  1. Klingerman CM, Stipanovic ME, Hajnal A, Lynch CJ. Acute Metabolic Effects of Olanzapine Depend on Dose and Injection Site. Dose Response. 2015 Oct-Dec; 13(4):1559325815618915.

View in: PubMed

  1. Lynch CJ, Kimball SR, Xu Y, Salzberg AC, Kawasawa YI. Global deletion of BCATm increases expression of skeletal muscle genes associated with protein turnover. Physiol Genomics. 2015 Nov; 47(11):569-80.

View in: PubMed

  1. Lynch CJ, Xu Y, Hajnal A, Salzberg AC, Kawasawa YI. RNA sequencing reveals a slow to fast muscle fiber type transition after olanzapine infusion in rats. PLoS One. 2015; 10(4):e0123966.

View in: PubMed

  1. Shin AC, Fasshauer M, Filatova N, Grundell LA, Zielinski E, Zhou JY, Scherer T, Lindtner C, White PJ, Lapworth AL, Ilkayeva O, Knippschild U, Wolf AM, Scheja L, Grove KL, Smith RD, Qian WJ, Lynch CJ, Newgard CB, Buettner C. Brain Insulin Lowers Circulating BCAA Levels by Inducing Hepatic BCAA Catabolism. Cell Metab. 2014 Nov 4; 20(5):898-909.

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  1. Lynch CJ, Adams SH. Branched-chain amino acids in metabolic signalling and insulin resistance. Nat Rev Endocrinol. 2014 Dec; 10(12):723-36.

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  1. Olson KC, Chen G, Xu Y, Hajnal A, Lynch CJ. Alloisoleucine differentiates the branched-chain aminoacidemia of Zucker and dietary obese rats. Obesity (Silver Spring). 2014 May; 22(5):1212-5.

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  1. Zimmerman HA, Olson KC, Chen G, Lynch CJ. Adipose transplant for inborn errors of branched chain amino acid metabolism in mice. Mol Genet Metab. 2013 Aug; 109(4):345-53.

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  1. Olson KC, Chen G, Lynch CJ. Quantification of branched-chain keto acids in tissue by ultra fast liquid chromatography-mass spectrometry. Anal Biochem. 2013 Aug 15; 439(2):116-22.

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  1. She P, Olson KC, Kadota Y, Inukai A, Shimomura Y, Hoppel CL, Adams SH, Kawamata Y, Matsumoto H, Sakai R, Lang CH, Lynch CJ. Leucine and protein metabolism in obese Zucker rats. PLoS One. 2013; 8(3):e59443.

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  1. Lackey DE, Lynch CJ, Olson KC, Mostaedi R, Ali M, Smith WH, Karpe F, Humphreys S, Bedinger DH, Dunn TN, Thomas AP, Oort PJ, Kieffer DA, Amin R, Bettaieb A, Haj FG, Permana P, Anthony TG, Adams SH. Regulation of adipose branched-chain amino acid catabolism enzyme expression and cross-adipose amino acid flux in human obesity. Am J Physiol Endocrinol Metab. 2013 Jun 1; 304(11):E1175-87.

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  1. Klingerman CM, Stipanovic ME, Bader M, Lynch CJ. Second-generation antipsychotics cause a rapid switch to fat oxidation that is required for survival in C57BL/6J mice. Schizophr Bull. 2014 Mar; 40(2):327-40.

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  1. Carr TD, DiGiovanni J, Lynch CJ, Shantz LM. Inhibition of mTOR suppresses UVB-induced keratinocyte proliferation and survival. Cancer Prev Res (Phila). 2012 Dec; 5(12):1394-404.

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  1. Lynch CJ, Zhou Q, Shyng SL, Heal DJ, Cheetham SC, Dickinson K, Gregory P, Firnges M, Nordheim U, Goshorn S, Reiche D, Turski L, Antel J. Some cannabinoid receptor ligands and their distomers are direct-acting openers of SUR1 K(ATP) channels. Am J Physiol Endocrinol Metab. 2012 Mar 1; 302(5):E540-51.

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  1. Albaugh VL, Singareddy R, Mauger D, Lynch CJ. A double blind, placebo-controlled, randomized crossover study of the acute metabolic effects of olanzapine in healthy volunteers. PLoS One. 2011; 6(8):e22662.

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  1. She P, Zhang Z, Marchionini D, Diaz WC, Jetton TJ, Kimball SR, Vary TC, Lang CH, Lynch CJ. Molecular characterization of skeletal muscle atrophy in the R6/2 mouse model of Huntington’s disease. Am J Physiol Endocrinol Metab. 2011 Jul; 301(1):E49-61.

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  1. Fogle RL, Hollenbeak CS, Stanley BA, Vary TC, Kimball SR, Lynch CJ. Functional proteomic analysis reveals sex-dependent differences in structural and energy-producing myocardial proteins in rat model of alcoholic cardiomyopathy. Physiol Genomics. 2011 Apr 12; 43(7):346-56.

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  1. Zhou Y, Jetton TL, Goshorn S, Lynch CJ, She P. Transamination is required for {alpha}-ketoisocaproate but not leucine to stimulate insulin secretion. J Biol Chem. 2010 Oct 29; 285(44):33718-26.

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  1. Agostino NM, Chinchilli VM, Lynch CJ, Koszyk-Szewczyk A, Gingrich R, Sivik J, Drabick JJ. Effect of the tyrosine kinase inhibitors (sunitinib, sorafenib, dasatinib, and imatinib) on blood glucose levels in diabetic and nondiabetic patients in general clinical practice. J Oncol Pharm Pract. 2011 Sep; 17(3):197-202.

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  1. Li J, Romestaing C, Han X, Li Y, Hao X, Wu Y, Sun C, Liu X, Jefferson LS, Xiong J, Lanoue KF, Chang Z, Lynch CJ, Wang H, Shi Y. Cardiolipin remodeling by ALCAT1 links oxidative stress and mitochondrial dysfunction to obesity. Cell Metab. 2010 Aug 4; 12(2):154-65.

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  1. Culnan DM, Albaugh V, Sun M, Lynch CJ, Lang CH, Cooney RN. Ileal interposition improves glucose tolerance and insulin sensitivity in the obese Zucker rat. Am J Physiol Gastrointest Liver Physiol. 2010 Sep; 299(3):G751-60.

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  1. Hajnal A, Kovacs P, Ahmed T, Meirelles K, Lynch CJ, Cooney RN. Gastric bypass surgery alters behavioral and neural taste functions for sweet taste in obese rats. Am J Physiol Gastrointest Liver Physiol. 2010 Oct; 299(4):G967-79.

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  1. Lang CH, Lynch CJ, Vary TC. BCATm deficiency ameliorates endotoxin-induced decrease in muscle protein synthesis and improves survival in septic mice. Am J Physiol Regul Integr Comp Physiol. 2010 Sep; 299(3):R935-44.

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  1. Albaugh VL, Vary TC, Ilkayeva O, Wenner BR, Maresca KP, Joyal JL, Breazeale S, Elich TD, Lang CH, Lynch CJ. Atypical antipsychotics rapidly and inappropriately switch peripheral fuel utilization to lipids, impairing metabolic flexibility in rodents. Schizophr Bull. 2012 Jan; 38(1):153-66.

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  1. Fogle RL, Lynch CJ, Palopoli M, Deiter G, Stanley BA, Vary TC. Impact of chronic alcohol ingestion on cardiac muscle protein expression. Alcohol Clin Exp Res. 2010 Jul; 34(7):1226-34.

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  1. Lang CH, Frost RA, Bronson SK, Lynch CJ, Vary TC. Skeletal muscle protein balance in mTOR heterozygous mice in response to inflammation and leucine. Am J Physiol Endocrinol Metab. 2010 Jun; 298(6):E1283-94.

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  1. Albaugh VL, Judson JG, She P, Lang CH, Maresca KP, Joyal JL, Lynch CJ. Olanzapine promotes fat accumulation in male rats by decreasing physical activity, repartitioning energy and increasing adipose tissue lipogenesis while impairing lipolysis. Mol Psychiatry. 2011 May; 16(5):569-81.

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  1. Lang CH, Lynch CJ, Vary TC. Alcohol-induced IGF-I resistance is ameliorated in mice deficient for mitochondrial branched-chain aminotransferase. J Nutr. 2010 May; 140(5):932-8.

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  1. She P, Zhou Y, Zhang Z, Griffin K, Gowda K, Lynch CJ. Disruption of BCAA metabolism in mice impairs exercise metabolism and endurance. J Appl Physiol (1985). 2010 Apr; 108(4):941-9.

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  1. Herman MA, She P, Peroni OD, Lynch CJ, Kahn BB. Adipose tissue branched chain amino acid (BCAA) metabolism modulates circulating BCAA levels. J Biol Chem. 2010 Apr 9; 285(15):11348-56.

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  1. Li P, Knabe DA, Kim SW, Lynch CJ, Hutson SM, Wu G. Lactating porcine mammary tissue catabolizes branched-chain amino acids for glutamine and aspartate synthesis. J Nutr. 2009 Aug; 139(8):1502-9.

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  1. Lu G, Sun H, She P, Youn JY, Warburton S, Ping P, Vondriska TM, Cai H, Lynch CJ, Wang Y. Protein phosphatase 2Cm is a critical regulator of branched-chain amino acid catabolism in mice and cultured cells. J Clin Invest. 2009 Jun; 119(6):1678-87.

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  1. Nairizi A, She P, Vary TC, Lynch CJ. Leucine supplementation of drinking water does not alter susceptibility to diet-induced obesity in mice. J Nutr. 2009 Apr; 139(4):715-9.

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  1. Meirelles K, Ahmed T, Culnan DM, Lynch CJ, Lang CH, Cooney RN. Mechanisms of glucose homeostasis after Roux-en-Y gastric bypass surgery in the obese, insulin-resistant Zucker rat. Ann Surg. 2009 Feb; 249(2):277-85.

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  1. Culnan DM, Cooney RN, Stanley B, Lynch CJ. Apolipoprotein A-IV, a putative satiety/antiatherogenic factor, rises after gastric bypass. Obesity (Silver Spring). 2009 Jan; 17(1):46-52.

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  1. She P, Van Horn C, Reid T, Hutson SM, Cooney RN, Lynch CJ. Obesity-related elevations in plasma leucine are associated with alterations in enzymes involved in branched-chain amino acid metabolism. Am J Physiol Endocrinol Metab. 2007 Dec; 293(6):E1552-63.

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  1. She P, Reid TM, Bronson SK, Vary TC, Hajnal A, Lynch CJ, Hutson SM. Disruption of BCATm in mice leads to increased energy expenditure associated with the activation of a futile protein turnover cycle. Cell Metab. 2007 Sep; 6(3):181-94.

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  1. Vary TC, Lynch CJ. Nutrient signaling components controlling protein synthesis in striated muscle. J Nutr. 2007 Aug; 137(8):1835-43.

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  1. Vary TC, Deiter G, Lynch CJ. Rapamycin limits formation of active eukaryotic initiation factor 4F complex following meal feeding in rat hearts. J Nutr. 2007 Aug; 137(8):1857-62.

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  1. Vary TC, Anthony JC, Jefferson LS, Kimball SR, Lynch CJ. Rapamycin blunts nutrient stimulation of eIF4G, but not PKCepsilon phosphorylation, in skeletal muscle. Am J Physiol Endocrinol Metab. 2007 Jul; 293(1):E188-96.

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  1. Vary TC, Lynch CJ. Meal feeding stimulates phosphorylation of multiple effector proteins regulating protein synthetic processes in rat hearts. J Nutr. 2006 Sep; 136(9):2284-90.

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  1. Lynch CJ, Gern B, Lloyd C, Hutson SM, Eicher R, Vary TC. Leucine in food mediates some of the postprandial rise in plasma leptin concentrations. Am J Physiol Endocrinol Metab. 2006 Sep; 291(3):E621-30.

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  1. Albaugh VL, Henry CR, Bello NT, Hajnal A, Lynch SL, Halle B, Lynch CJ. Hormonal and metabolic effects of olanzapine and clozapine related to body weight in rodents. Obesity (Silver Spring). 2006 Jan; 14(1):36-51.

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  1. Vary TC, Lynch CJ. Meal feeding enhances formation of eIF4F in skeletal muscle: role of increased eIF4E availability and eIF4G phosphorylation. Am J Physiol Endocrinol Metab. 2006 Apr; 290(4):E631-42.

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  1. Vary TC, Goodman S, Kilpatrick LE, Lynch CJ. Nutrient regulation of PKCepsilon is mediated by leucine, not insulin, in skeletal muscle. Am J Physiol Endocrinol Metab. 2005 Oct; 289(4):E684-94.

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  1. Vary TC, Lynch CJ. Biochemical approaches for nutritional support of skeletal muscle protein metabolism during sepsis. Nutr Res Rev. 2004 Jun; 17(1):77-88.

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  1. Lynch CJ, Halle B, Fujii H, Vary TC, Wallin R, Damuni Z, Hutson SM. Potential role of leucine metabolism in the leucine-signaling pathway involving mTOR. Am J Physiol Endocrinol Metab. 2003 Oct; 285(4):E854-63.

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  1. Lynch CJ, Hutson SM, Patson BJ, Vaval A, Vary TC. Tissue-specific effects of chronic dietary leucine and norleucine supplementation on protein synthesis in rats. Am J Physiol Endocrinol Metab. 2002 Oct; 283(4):E824-35.

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  1. Lynch CJ, Patson BJ, Anthony J, Vaval A, Jefferson LS, Vary TC. Leucine is a direct-acting nutrient signal that regulates protein synthesis in adipose tissue. Am J Physiol Endocrinol Metab. 2002 Sep; 283(3):E503-13.

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  1. Vary TC, Lynch CJ, Lang CH. Effects of chronic alcohol consumption on regulation of myocardial protein synthesis. Am J Physiol Heart Circ Physiol. 2001 Sep; 281(3):H1242-51.

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  1. Lynch CJ, Patson BJ, Goodman SA, Trapolsi D, Kimball SR. Zinc stimulates the activity of the insulin- and nutrient-regulated protein kinase mTOR. Am J Physiol Endocrinol Metab. 2001 Jul; 281(1):E25-34.

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Global deletion of BCATm increases expression of skeletal muscle genes associated with protein turnover.

Lynch CJ1Kimball SR2Xu Y2Salzberg AC3Kawasawa YI4.   Author information
Physiol Genomics. 2015 Nov;47(11):569-80.  http://dx.doi.org:/10.1152/physiolgenomics.00055.2015

Consumption of a protein-containing meal by a fasted animal promotes protein accretion in skeletal muscle, in part through leucine stimulation of protein synthesis and indirectly through repression of protein degradation mediated by its metabolite, α-ketoisocaproate. Mice lacking the mitochondrial branched-chain aminotransferase (BCATm/Bcat2), which interconverts leucine and α-ketoisocaproate, exhibit elevated protein turnover. Here, the transcriptomes of gastrocnemius muscle from BCATm knockout (KO) and wild-type mice were compared by next-generation RNA sequencing (RNA-Seq) to identify potential adaptations associated with their persistently altered nutrient signaling. Statistically significant changes in the abundance of 1,486/∼39,010 genes were identified. Bioinformatics analysis of the RNA-Seq data indicated that pathways involved in protein synthesis [eukaryotic initiation factor (eIF)-2, mammalian target of rapamycin, eIF4, and p70S6K pathways including 40S and 60S ribosomal proteins], protein breakdown (e.g., ubiquitin mediated), and muscle degeneration (apoptosis, atrophy, myopathy, and cell death) were upregulated. Also in agreement with our previous observations, the abundance of mRNAs associated with reduced body size, glycemia, plasma insulin, and lipid signaling pathways was altered in BCATm KO mice. Consistently, genes encoding anaerobic and/or oxidative metabolism of carbohydrate, fatty acids, and branched chain amino acids were modestly but systematically reduced. Although there was no indication that muscle fiber type was different between KO and wild-type mice, a difference in the abundance of mRNAs associated with a muscular dystrophy phenotype was observed, consistent with the published exercise intolerance of these mice. The results suggest transcriptional adaptations occur in BCATm KO mice that along with altered nutrient signaling may contribute to their previously reported protein turnover, metabolic and exercise phenotypes.

 

RNA sequencing reveals a slow to fast muscle fiber type transition after olanzapine infusion in rats.

Lynch CJ1Xu Y1Hajnal A2Salzberg AC3Kawasawa YI4. Author information
PLoS One. 2015 Apr 20;10(4):e0123966. http://dx.doi.org:/10.1371/journal.pone.0123966. eCollection 2015.

Second generation antipsychotics (SGAs), like olanzapine, exhibit acute metabolic side effects leading to metabolic inflexibility, hyperglycemia, adiposity and diabetes. Understanding how SGAs affect the skeletal muscle transcriptome could elucidate approaches for mitigating these side effects. Male Sprague-Dawley rats were infused intravenously with vehicle or olanzapine for 24h using a dose leading to a mild hyperglycemia. RNA-Seq was performed on gastrocnemius muscle, followed by alignment of the data with the Rat Genome Assembly 5.0. Olanzapine altered expression of 1347 out of 26407 genes. Genes encoding skeletal muscle fiber-type specific sarcomeric, ion channel, glycolytic, O2- and Ca2+-handling, TCA cycle, vascularization and lipid oxidation proteins and pathways, along with NADH shuttles and LDH isoforms were affected. Bioinformatics analyses indicate that olanzapine decreased the expression of slower and more oxidative fiber type genes (e.g., type 1), while up regulating those for the most glycolytic and least metabolically flexible, fast twitch fiber type, IIb. Protein turnover genes, necessary to bring about transition, were also up regulated. Potential upstream regulators were also identified. Olanzapine appears to be rapidly affecting the muscle transcriptome to bring about a change to a fast-glycolytic fiber type. Such fiber types are more susceptible than slow muscle to atrophy, and such transitions are observed in chronic metabolic diseases. Thus these effects could contribute to the altered body composition and metabolic disease olanzapine causes. A potential interventional strategy is implicated because aerobic exercise, in contrast to resistance exercise, can oppose such slow to fast fiber transitions.

 

Brain insulin lowers circulating BCAA levels by inducing hepatic BCAA catabolism.

Shin AC1Fasshauer M1Filatova N1Grundell LA1Zielinski E1Zhou JY2Scherer T1Lindtner C1White PJ3Lapworth AL3,Ilkayeva O3Knippschild U4Wolf AM4Scheja L5Grove KL6Smith RD2Qian WJ2Lynch CJ7Newgard CB3Buettner C8. Author information
Cell Metab. 2014 Nov 4;20(5):898-909. http://dx.doi.org:/10.1016/j.cmet.2014.09.003   Epub 2014 Oct 9

Circulating branched-chain amino acid (BCAA) levels are elevated in obesity/diabetes and are a sensitive predictor for type 2 diabetes. Here we show in rats that insulin dose-dependently lowers plasma BCAA levels through induction of hepatic protein expression and activity of branched-chain α-keto acid dehydrogenase (BCKDH), the rate-limiting enzyme in the BCAA degradation pathway. Selective induction of hypothalamic insulin signaling in rats and genetic modulation of brain insulin receptors in mice demonstrate that brain insulin signaling is a major regulator of BCAA metabolism by inducing hepatic BCKDH. Short-term overfeeding impairs the ability of brain insulin to lower BCAAs in rats. High-fat feeding in nonhuman primates and obesity and/or diabetes in humans is associated with reduced BCKDH protein in liver. These findings support the concept that decreased hepatic BCKDH is a major cause of increased plasma BCAAs and that hypothalamic insulin resistance may account for impaired BCAA metabolism in obesity and diabetes.

 

Branched-chain amino acids in metabolic signalling and insulin resistance.

Lynch CJ1Adams SH2Author information
Nat Rev Endocrinol. 2014 Dec; 10(12):723-36. http://dx.doi.org:/10.1038/nrendo.2014.171

Branched-chain amino acids (BCAAs) are important nutrient signals that have direct and indirect effects. Frequently, BCAAs have been reported to mediate antiobesity effects, especially in rodent models. However, circulating levels of BCAAs tend to be increased in individuals with obesity and are associated with worse metabolic health and future insulin resistance or type 2 diabetes mellitus (T2DM). A hypothesized mechanism linking increased levels of BCAAs and T2DM involves leucine-mediated activation of the mammalian target of rapamycin complex 1 (mTORC1), which results in uncoupling of insulin signalling at an early stage. A BCAA dysmetabolism model proposes that the accumulation of mitotoxic metabolites (and not BCAAs per se) promotes β-cell mitochondrial dysfunction, stress signalling and apoptosis associated with T2DM. Alternatively, insulin resistance might promote aminoacidaemia by increasing the protein degradation that insulin normally suppresses, and/or by eliciting an impairment of efficient BCAA oxidative metabolism in some tissues. Whether and how impaired BCAA metabolism might occur in obesity is discussed in this Review. Research on the role of individual and model-dependent differences in BCAA metabolism is needed, as several genes (BCKDHA, PPM1K, IVD and KLF15) have been designated as candidate genes for obesity and/or T2DM in humans, and distinct phenotypes of tissue-specific branched chain ketoacid dehydrogenase complex activity have been detected in animal models of obesity and T2DM.

 

Leucine and protein metabolism in obese Zucker rats.

She P1Olson KCKadota YInukai AShimomura YHoppel CLAdams SHKawamata YMatsumoto HSakai RLang CHLynch CJAuthor information
PLoS One. 2013;8(3):e59443. http://dx.doi.org:/10.1371/journal.pone.0059443   Epub 2013 Mar 20.

Branched-chain amino acids (BCAAs) are circulating nutrient signals for protein accretion, however, they increase in obesity and elevations appear to be prognostic of diabetes. To understand the mechanisms whereby obesity affects BCAAs and protein metabolism, we employed metabolomics and measured rates of [1-(14)C]-leucine metabolism, tissue-specific protein synthesis and branched-chain keto-acid (BCKA) dehydrogenase complex (BCKDC) activities. Male obese Zucker rats (11-weeks old) had increased body weight (BW, 53%), liver (107%) and fat (∼300%), but lower plantaris and gastrocnemius masses (-21-24%). Plasma BCAAs and BCKAs were elevated 45-69% and ∼100%, respectively, in obese rats. Processes facilitating these rises appeared to include increased dietary intake (23%), leucine (Leu) turnover and proteolysis [35% per g fat free mass (FFM), urinary markers of proteolysis: 3-methylhistidine (183%) and 4-hydroxyproline (766%)] and decreased BCKDC per g kidney, heart, gastrocnemius and liver (-47-66%). A process disposing of circulating BCAAs, protein synthesis, was increased 23-29% by obesity in whole-body (FFM corrected), gastrocnemius and liver. Despite the observed decreases in BCKDC activities per gm tissue, rates of whole-body Leu oxidation in obese rats were 22% and 59% higher normalized to BW and FFM, respectively. Consistently, urinary concentrations of eight BCAA catabolism-derived acylcarnitines were also elevated. The unexpected increase in BCAA oxidation may be due to a substrate effect in liver. Supporting this idea, BCKAs were elevated more in liver (193-418%) than plasma or muscle, and per g losses of hepatic BCKDC activities were completely offset by increased liver mass, in contrast to other tissues. In summary, our results indicate that plasma BCKAs may represent a more sensitive metabolic signature for obesity than BCAAs. Processes supporting elevated BCAA]BCKAs in the obese Zucker rat include increased dietary intake, Leu and protein turnover along with impaired BCKDC activity. Elevated BCAAs/BCKAs may contribute to observed elevations in protein synthesis and BCAA oxidation.

 

Regulation of adipose branched-chain amino acid catabolism enzyme expression and cross-adipose amino acid flux in human obesity.

Lackey DE1Lynch CJOlson KCMostaedi RAli MSmith WHKarpe FHumphreys SBedinger DHDunn TNThomas APOort PJKieffer DAAmin RBettaieb AHaj FGPermana PAnthony TGAdams SH.
Am J Physiol Endocrinol Metab. 2013 Jun 1; 304(11):E1175-87. http://dx.doi.org:/10.1152/ajpendo.00630.2012

Elevated blood branched-chain amino acids (BCAA) are often associated with insulin resistance and type 2 diabetes, which might result from a reduced cellular utilization and/or incomplete BCAA oxidation. White adipose tissue (WAT) has become appreciated as a potential player in whole body BCAA metabolism. We tested if expression of the mitochondrial BCAA oxidation checkpoint, branched-chain α-ketoacid dehydrogenase (BCKD) complex, is reduced in obese WAT and regulated by metabolic signals. WAT BCKD protein (E1α subunit) was significantly reduced by 35-50% in various obesity models (fa/fa rats, db/db mice, diet-induced obese mice), and BCKD component transcripts significantly lower in subcutaneous (SC) adipocytes from obese vs. lean Pima Indians. Treatment of 3T3-L1 adipocytes or mice with peroxisome proliferator-activated receptor-γ agonists increased WAT BCAA catabolism enzyme mRNAs, whereas the nonmetabolizable glucose analog 2-deoxy-d-glucose had the opposite effect. The results support the hypothesis that suboptimal insulin action and/or perturbed metabolic signals in WAT, as would be seen with insulin resistance/type 2 diabetes, could impair WAT BCAA utilization. However, cross-tissue flux studies comparing lean vs. insulin-sensitive or insulin-resistant obese subjects revealed an unexpected negligible uptake of BCAA from human abdominal SC WAT. This suggests that SC WAT may not be an important contributor to blood BCAA phenotypes associated with insulin resistance in the overnight-fasted state. mRNA abundances for BCAA catabolic enzymes were markedly reduced in omental (but not SC) WAT of obese persons with metabolic syndrome compared with weight-matched healthy obese subjects, raising the possibility that visceral WAT contributes to the BCAA metabolic phenotype of metabolically compromised individuals.

 

Some cannabinoid receptor ligands and their distomers are direct-acting openers of SUR1 K(ATP) channels.

Lynch CJ1Zhou QShyng SLHeal DJCheetham SCDickinson KGregory PFirnges MNordheim UGoshorn SReiche D,Turski LAntel J.   Author information
Am J Physiol Endocrinol Metab. 2012 Mar 1;302(5):E540-51.
http://dx.doi.org:/10.1152/ajpendo.00258.2011

Here, we examined the chronic effects of two cannabinoid receptor-1 (CB1) inverse agonists, rimonabant and ibipinabant, in hyperinsulinemic Zucker rats to determine their chronic effects on insulinemia. Rimonabant and ibipinabant (10 mg·kg⁻¹·day⁻¹) elicited body weight-independent improvements in insulinemia and glycemia during 10 wk of chronic treatment. To elucidate the mechanism of insulin lowering, acute in vivo and in vitro studies were then performed. Surprisingly, chronic treatment was not required for insulin lowering. In acute in vivo and in vitro studies, the CB1 inverse agonists exhibited acute K channel opener (KCO; e.g., diazoxide and NN414)-like effects on glucose tolerance and glucose-stimulated insulin secretion (GSIS) with approximately fivefold better potency than diazoxide. Followup studies implied that these effects were inconsistent with a CB1-mediated mechanism. Thus effects of several CB1 agonists, inverse agonists, and distomers during GTTs or GSIS studies using perifused rat islets were unpredictable from their known CB1 activities. In vivo rimonabant and ibipinabant caused glucose intolerance in CB1 but not SUR1-KO mice. Electrophysiological studies indicated that, compared with diazoxide, 3 μM rimonabant and ibipinabant are partial agonists for K channel opening. Partial agonism was consistent with data from radioligand binding assays designed to detect SUR1 K(ATP) KCOs where rimonabant and ibipinabant allosterically regulated ³H-glibenclamide-specific binding in the presence of MgATP, as did diazoxide and NN414. Our findings indicate that some CB1 ligands may directly bind and allosterically regulate Kir6.2/SUR1 K(ATP) channels like other KCOs. This mechanism appears to be compatible with and may contribute to their acute and chronic effects on GSIS and insulinemia.

 

Transamination is required for {alpha}-ketoisocaproate but not leucine to stimulate insulin secretion.

Zhou Y1Jetton TLGoshorn SLynch CJShe PAuthor information
J Biol Chem. 2010 Oct 29;285(44):33718-26. http://dx.doi.org:/10.1074/jbc.M110.136846

It remains unclear how α-ketoisocaproate (KIC) and leucine are metabolized to stimulate insulin secretion. Mitochondrial BCATm (branched-chain aminotransferase) catalyzes reversible transamination of leucine and α-ketoglutarate to KIC and glutamate, the first step of leucine catabolism. We investigated the biochemical mechanisms of KIC and leucine-stimulated insulin secretion (KICSIS and LSIS, respectively) using BCATm(-/-) mice. In static incubation, BCATm disruption abolished insulin secretion by KIC, D,L-α-keto-β-methylvalerate, and α-ketocaproate without altering stimulation by glucose, leucine, or α-ketoglutarate. Similarly, during pancreas perfusions in BCATm(-/-) mice, glucose and arginine stimulated insulin release, whereas KICSIS was largely abolished. During islet perifusions, KIC and 2 mM glutamine caused robust dose-dependent insulin secretion in BCATm(+/+) not BCATm(-/-) islets, whereas LSIS was unaffected. Consistently, in contrast to BCATm(+/+) islets, the increases of the ATP concentration and NADPH/NADP(+) ratio in response to KIC were largely blunted in BCATm(-/-) islets. Compared with nontreated islets, the combination of KIC/glutamine (10/2 mM) did not influence α-ketoglutarate concentrations but caused 120 and 33% increases in malate in BCATm(+/+) and BCATm(-/-) islets, respectively. Although leucine oxidation and KIC transamination were blocked in BCATm(-/-) islets, KIC oxidation was unaltered. These data indicate that KICSIS requires transamination of KIC and glutamate to leucine and α-ketoglutarate, respectively. LSIS does not require leucine catabolism and may be through leucine activation of glutamate dehydrogenase. Thus, KICSIS and LSIS occur by enhancing the metabolism of glutamine/glutamate to α-ketoglutarate, which, in turn, is metabolized to produce the intracellular signals such as ATP and NADPH for insulin secretion.

 

Effect of the tyrosine kinase inhibitors (sunitinib, sorafenib, dasatinib, and imatinib) on blood glucose levels in diabetic and nondiabetic patients in general clinical practice.

Agostino NM1Chinchilli VMLynch CJKoszyk-Szewczyk AGingrich RSivik JDrabick JJ.
J Oncol Pharm Pract. 2011 Sep; 17(3):197-202. http://dx.doi.org:/10.1177/1078155210378913

Tyrosine kinase is a key enzyme activity utilized in many intracellular messaging pathways. Understanding the role of particular tyrosine kinases in malignancies has allowed for the design of tyrosine kinase inhibitors (TKIs), which can target these enzymes and interfere with downstream signaling. TKIs have proven to be successful in the treatment of chronic myeloid leukemia, renal cell carcinoma and gastrointestinal stromal tumor, and other malignancies. Scattered reports have suggested that these agents appear to affect blood glucose (BG). We retrospectively studied the BG concentrations in diabetic (17) and nondiabetic (61) patients treated with dasatinib (8), imatinib (39), sorafenib (23), and sunitinib (30) in our clinical practice. Mean declines of BG were dasatinib (53 mg/dL), imatinib (9 mg/dL), sorafenib (12 mg/dL), and sunitinib (14 mg/dL). All these declines in BG were statistically significant. Of note, 47% (8/17) of the patients with diabetes were able to discontinue their medications, including insulin in some patients. Only one diabetic patient developed symptomatic hypoglycemia while on sunitinib. The mechanism for the hypoglycemic effect of these drugs is unclear, but of the four agents tested, c-kit and PDGFRβ are the common target kinases. Clinicians should keep the potential hypoglycemic effects of these agents in mind; modification of hypoglycemic agents may be required in diabetic patients. These results also suggest that inhibition of a tyrosine kinase, be it c-kit, PDGFRβ or some other undefined target, may improve diabetes mellitus BG control and it deserves further study as a potential novel therapeutic option.

 

Cardiolipin remodeling by ALCAT1 links oxidative stress and mitochondrial dysfunction to obesity.

Li J1Romestaing CHan XLi YHao XWu YSun CLiu XJefferson LSXiong JLanoue KFChang ZLynch CJWang HShi Y.    Author information
Cell Metab. 2010 Aug 4;12(2):154-65. http://dx.doi.org:/10.1016/j.cmet.2010.07.003

Oxidative stress causes mitochondrial dysfunction and metabolic complications through unknown mechanisms. Cardiolipin (CL) is a key mitochondrial phospholipid required for oxidative phosphorylation. Oxidative damage to CL from pathological remodeling is implicated in the etiology of mitochondrial dysfunction commonly associated with diabetes, obesity, and other metabolic diseases. Here, we show that ALCAT1, a lyso-CL acyltransferase upregulated by oxidative stress and diet-induced obesity (DIO), catalyzes the synthesis of CL species that are highly sensitive to oxidative damage, leading to mitochondrial dysfunction, ROS production, and insulin resistance. These metabolic disorders were reminiscent of those observed in type 2 diabetes and were reversed by rosiglitazone treatment. Consequently, ALCAT1 deficiency prevented the onset of DIO and significantly improved mitochondrial complex I activity, lipid oxidation, and insulin signaling in ALCAT1(-/-) mice. Collectively, these findings identify a key role of ALCAT1 in regulating CL remodeling, mitochondrial dysfunction, and susceptibility to DIO.

 

BCATm deficiency ameliorates endotoxin-induced decrease in muscle protein synthesis and improves survival in septic mice.

Lang CH1Lynch CJVary TC.   Author information
Am J Physiol Regul Integr Comp Physiol. 2010 Sep; 299(3):R935-44.
http://dx.doi.org:/10.1152/ajpregu.00297.2010

Endotoxin (LPS) and sepsis decrease mammalian target of rapamycin (mTOR) activity in skeletal muscle, thereby reducing protein synthesis. Our study tests the hypothesis that inhibition of branched-chain amino acid (BCAA) catabolism, which elevates circulating BCAA and stimulates mTOR, will blunt the LPS-induced decrease in muscle protein synthesis. Wild-type (WT) and mitochondrial branched-chain aminotransferase (BCATm) knockout mice were studied 4 h after Escherichia coli LPS or saline. Basal skeletal muscle protein synthesis was increased in knockout mice compared with WT, and this change was associated with increased eukaryotic initiation factor (eIF)-4E binding protein-1 (4E-BP1) phosphorylation, eIF4E.eIF4G binding, 4E-BP1.raptor binding, and eIF3.raptor binding without a change in the mTOR.raptor complex in muscle. LPS decreased muscle protein synthesis in WT mice, a change associated with decreased 4E-BP1 phosphorylation as well as decreased formation of eIF4E.eIF4G, 4E-BP1.raptor, and eIF3.raptor complexes. In BCATm knockout mice given LPS, muscle protein synthesis only decreased to values found in vehicle-treated WT control mice, and this ameliorated LPS effect was associated with a coordinate increase in 4E-BP1.raptor, eIF3.raptor, and 4E-BP1 phosphorylation. Additionally, the LPS-induced increase in muscle cytokines was blunted in BCATm knockout mice, compared with WT animals. In a separate study, 7-day survival and muscle mass were increased in BCATm knockout vs. WT mice after polymicrobial peritonitis. These data suggest that elevating blood BCAA is sufficient to ameliorate the catabolic effect of LPS on skeletal muscle protein synthesis via alterations in protein-protein interactions within mTOR complex-1, and this may provide a survival advantage in response to bacterial infection.

 

Alcohol-induced IGF-I resistance is ameliorated in mice deficient for mitochondrial branched-chain aminotransferase.

Lang CH1Lynch CJVary TCAuthor information
J Nutr. 2010 May;140(5):932-8. http://dx.doi.org:/10.3945/jn.109.120501

Acute alcohol intoxication decreases skeletal muscle protein synthesis by impairing mammalian target of rapamycin (mTOR). In 2 studies, we determined whether inhibition of branched-chain amino acid (BCAA) catabolism ameliorates the inhibitory effect of alcohol on muscle protein synthesis by raising the plasma BCAA concentrations and/or by improving the anabolic response to insulin-like growth factor (IGF)-I. In the first study, 4 groups of mice were used: wild-type (WT) and mitochondrial branched-chain aminotransferase (BCATm) knockout (KO) mice orally administered saline or alcohol (5 g/kg, 1 h). Protein synthesis was greater in KO mice compared with WT controls and was associated with greater phosphorylation of eukaryotic initiation factor (eIF)-4E binding protein-1 (4EBP1), eIF4E-eIF4G binding, and 4EBP1-regulatory associated protein of mTOR (raptor) binding, but not mTOR-raptor binding. Alcohol decreased protein synthesis in WT mice, a change associated with less 4EBP1 phosphorylation, eIF4E-eIF4G binding, and raptor-4EBP1 binding, but greater mTOR-raptor complex formation. Comparable alcohol effects on protein synthesis and signal transduction were detected in BCATm KO mice. The second study used the same 4 groups, but all mice were injected with IGF-I (25 microg/mouse, 30 min). Alcohol impaired the ability of IGF-I to increase muscle protein synthesis, 4EBP1 and 70-kilodalton ribosomal protein S6 kinase-1 phosphorylation, eIF4E-eIF4G binding, and 4EBP1-raptor binding in WT mice. However, in alcohol-treated BCATm KO mice, this IGF-I resistance was not manifested. These data suggest that whereas the sustained elevation in plasma BCAA is not sufficient to ameliorate the catabolic effect of acute alcohol intoxication on muscle protein synthesis, it does improve the anabolic effect of IGF-I.

 

Impact of chronic alcohol ingestion on cardiac muscle protein expression.

Fogle RL1Lynch CJPalopoli MDeiter GStanley BAVary TCAuthor information
Alcohol Clin Exp Res. 2010 Jul;34(7):1226-34. http://dx.doi.org:/10.1111/j.1530-0277.2010.01200.x

BACKGROUND:

Chronic alcohol abuse contributes not only to an increased risk of health-related complications, but also to a premature mortality in adults. Myocardial dysfunction, including the development of a syndrome referred to as alcoholic cardiomyopathy, appears to be a major contributing factor. One mechanism to account for the pathogenesis of alcoholic cardiomyopathy involves alterations in protein expression secondary to an inhibition of protein synthesis. However, the full extent to which myocardial proteins are affected by chronic alcohol consumption remains unresolved.

METHODS:

The purpose of this study was to examine the effect of chronic alcohol consumption on the expression of cardiac proteins. Male rats were maintained for 16 weeks on a 40% ethanol-containing diet in which alcohol was provided both in drinking water and agar blocks. Control animals were pair-fed to consume the same caloric intake. Heart homogenates from control- and ethanol-fed rats were labeled with the cleavable isotope coded affinity tags (ICAT). Following the reaction with the ICAT reagent, we applied one-dimensional gel electrophoresis with in-gel trypsin digestion of proteins and subsequent MALDI-TOF-TOF mass spectrometric techniques for identification of peptides. Differences in the expression of cardiac proteins from control- and ethanol-fed rats were determined by mass spectrometry approaches.

RESULTS:

Initial proteomic analysis identified and quantified hundreds of cardiac proteins. Major decreases in the expression of specific myocardial proteins were observed. Proteins were grouped depending on their contribution to multiple activities of cardiac function and metabolism, including mitochondrial-, glycolytic-, myofibrillar-, membrane-associated, and plasma proteins. Another group contained identified proteins that could not be properly categorized under the aforementioned classification system.

CONCLUSIONS:

Based on the changes in proteins, we speculate modulation of cardiac muscle protein expression represents a fundamental alteration induced by chronic alcohol consumption, consistent with changes in myocardial wall thickness measured under the same conditions.

 

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