GAPDH mediates nitrosylation of nuclear proteins

Nature Cell Biology

Volumn 12, Issue 11, 2010, Pages 1094-1100

  Kornberg, Michael D ^a   Sen, Nilkantha ^a   Hara, Makoto R ^a,b   Juluri, Krishna R ^a   Nguyen, Judy Van K ^a   Snowman, Adele M ^a   Law, Lindsey ^a   Hester, Lynda D ^a   Snyder, Solomon H ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; DNA DEPENDENT PROTEIN KINASE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HISTONE DEACETYLASE 2; NUCLEAR PROTEIN; PROTEIN SIAH1; SIRTUIN 1; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME BINDING; HUMAN; HUMAN CELL; MOUSE; NITROSYLATION; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

CELLS, CULTURED; DNA-ACTIVATED PROTEIN KINASE; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASES; HISTONE DEACETYLASE 2; HUMANS; NITRIC OXIDE; NITRIC OXIDE DONORS; NUCLEAR PROTEINS; SIGNAL TRANSDUCTION; SIRTUIN 1;

EID: 78149284226     PISSN: 14657392     EISSN: None     Source Type: Journal    
DOI: 10.1038/ncb2114     Document Type: Article

References (42)

1. Hess, D. T., Matsumoto, A., Kim, S. O., Marshall, H. E. & Stamler, J. S. Protein S-nitrosylation: purview and parameters. Nat. Rev. Mol. Cell Biol. 6, 150-166 (2005).
2. Nott, A., Watson, P. M., Robinson, J. D., Crepaldi, L. & Riccio A. S-nitrosylation of histone deacetylase 2 induces chromatin remodelling in neurons. Nature 455, 411-415 (2008).
3. Yu, Z., Kuncewicz, T., Dubinsky, W. P. & Kone, B. C. Nitric oxide-dependent negative feedback of PARP-1 trans-activation of the inducible nitric-oxide synthase gene. J. Biol. Chem. 281, 9101-9109 (2006).
4. Kim, S. F., Huri, D. A. & Snyder, S. H. Inducible nitric oxide synthase binds, S-nitrosylates and activates cyclooxygenase-2. Science 310, 1966-1970 (2005).
5. Lipton, S. A. et al. Cysteine regulation of protein function-as exemplified by NMDA- receptor modulation. Trends Neurosci. 25, 474-480 (2002).
6. Fang, M. et al. Dexras1: a G protein specifically coupled to neuronal nitric oxide synthase via CAPON. Neuron 28, 183-193 (2000).
7. Hara, M. R. et al. S-nitrosylated GAPDH initiates apoptotic cell death by nuclear translocation following Siah1 binding. Nat. Cell Biol. 7, 665-674 (2005).
8. Sen, N. et al. Nitric oxide-induced nuclear GAPDH activates p300/CBP and mediates apoptosis. Nat. Cell Biol. 10, 866-873 (2008).
9. Giot, L. et al. A protein interaction map of Drosophila melanogaster. Science 302, 1727-1736 (2003).
10. Haigis, M. C. & Guarente, L. P. Mammalian sirtuins-emerging roles in physiology, aging and calorie restriction. Genes Dev. 20, 2913-2921 (2006).
11. Jaffrey, S. R., Erdjument-Bromage, H., Ferris, C. D., Tempst, P. & Snyder S. H. Protein S-nitrosylation: a physiological signal for neuronal nitric oxide. Nat. Cell Biol. 3, 193-197 (2001).
12. Chang, K., Shimizu, N., Fukushima, Y., Martyn, J. & Kaneki, M. iNOS inactivates Sirt1, a key regulator of stress resistance and metabolism, by S-Nitrosylation. 2006 Annual Meeting American Society of Anesthesiologists conference abstract, A1067 (2006).
13. Chang, K., Shimizu, N., Fukushima, Y., Martyn, J. & Kaneki, M. Inducible nitric oxide synthase-mediated p53 activation and apoptosis in muscle after burn injury. 2007 Annual Meeting American Society of Anesthesiologists conference abstract, A1856 (2007).
14. 2+ in maintaining structural integrity and suppressing deacetylase activity of SIRT1. J. Inorg. Biochem. 104, 180-185 (2010).
15. Rodgers, J. T. et al. Nutrient control of glucose homeostasis through a complex of PGC-1α and SIRT1. Nature 434, 113-118 (2005).
16. Lerin, C. et al. GCN5 acetyltransferase complex controls glucose metabolism through transcriptional repression of PGC-1α. Cell Metab. 3, 429-438 (2006).
17. Rhee, J. et al. Regulation of hepatic fasting response by PPARγ coactivator-1α (PGC-1): requirement for hepatocyte nuclear factor 4α in gluconeogenesis. Proc. Natl Acad. Sci. USA 100, 4012-4017 (2003).
18. Forrester, M. T. et al. Proteomic analysis of S-nitrosylation and denitrosylation by resinassisted capture. Nat. Biotechnol. 27, 557-559 (2009).
19. Pawloski, J. R., Hess, D. T. & Stamler, J. S. Export by red blood cells of nitric oxide bioactivity. Nature 409, 622-626 (2001).
20. Mitchell, D. A. & Marletta, M. A. Thioredoxin catalyzes the S-nitrosylation of the caspase-3 active site cysteine. Nat. Chem. Biol. 1, 154-158 (2005).
21. Mitchell, D. A., Morton, S. U., Fernhoff, N. B. & Marletta, M. A. Thioredoxin is required for S-nitrosation of procaspase-3 and the inhibition of apoptosis in Jurkat cells. Proc. Natl Acad. Sci. USA 104, 11609-11614 (2007).
22. Benhar, M., Forrester, M. T., Hess, D. T. & Stamler, J. S. Regulated protein denitrosylation by cytosolic and mitochondrial thioredoxins. Science 320, 1050-1054 (2008).
23. Nakamura, T. et al. Transnitrosylation of XIAP regulates caspase-dependent neuronal cell death. Mol. Cell 39, 184-195 (2010).
24. Giordano, A. et al. Evidence for a functional nitric oxide synthase system in brown adipocyte nucleus. FEBS Lett. 514, 135-140 (2002).
25. Gobeil, F. et al. Nitric oxide signaling via nuclearized endothelial nitric-oxide synthase modulates expression of the immediate early genes iNOS and mPGES-1. J. Biol. Chem. 281, 16058-16067 (2006).
26. Grasselli, A. et al. Estrogen receptor-α and endothelial nitric oxide synthase nuclear complex regulates transcription of human telomerase. Circ. Res. 103, 34-42 (2008).
27. Dudzinski, D. M. & Michel, T. Life history of eNOS: partners and pathways. Cardiovasc. Res. 75, 247-260 (2007).
28. Jagnandan, D., Sessa, W. C. & Fulton, D. Intracellular location regulates calcium- calmodulin-dependent activation of organelle-restricted eNOS. Am. J. Physiol. Cell Physiol. 289, C1024-C1033 (2005).
29. Rodgers, J. T., Lerin, C., Gerhart-Hines, Z. & Puigserver, P. Metabolic adaptations through the PGC-1α and SIRT1 pathways. FEBS Lett. 582, 46-53 (2008).
30. Baur, J. A. et al. Resveratrol improves health and survival of mice on a high-calorie diet. Nature 444, 337-342 (2006).
31. Lagouge, M. et al. Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1α. Cell 127, 1109-1122 (2006).
32. Hotamisligil, G. S. Inflammation and metabolic disorders. Nature 444, 860-867 (2006).
33. Schmidt, H. W. & Walter, U. NO at work. Cell 78, 919-925 (1994).
34. Marshall, H. E. & Stamler, J. S. Inhibition of NF-κB by S-nitrosylation. Biochemistry 40, 1688-1693 (2001).
35. Yasinska, I. M. & Sumbayev, V. V. S-nitrosation of Cys 800 of HIF-1a protein activates its interaction with p300 and stimulates its transcriptional activity. FEBS Lett. 549, 105-109 (2003).
36. Zheng, L, Roeder, R. G. & Luo, Y. S phase activation of the histone H2B promoter by OCA-S, a coactivator complex that contains GAPDH as a key component. Cell 114, 255-266 (2003).
37. Meyer-Siegler, K., Rahman-Mansur, N., Wurzer, J. C. & Sirover, M. A. Proliferative dependent regulation of the glyceraldehyde-3-phosphate dehydrogenase/uracil DNA glycosylase gene in human cells. Carcinogenesis 13, 2127-2132 (1992).
38. Singh, R. & Green, M. R. Sequence-specific binding of transfer RNA by glyceraldehydes-3-phosphate dehydrogenase. Science 259, 365-368 (1993).
39. Zhou, Y. et al. The multifunctional protein glyceraldehyde-3-phosphate dehydrogenase is both regulated and controls colony-stimulating factor-1 messenger RNA stability in ovarian cancer. Mol. Cancer Res. 6, 1375-1384 (2008).
40. North, B. J., Schwer B., Ahuja, N., Marshall, B. & Verdin, E. Preparation of enzymatically active recombinant class III protein deacetylases. Methods 36, 338-345 (2005).
41. Jaffrey, S. R. & Snyder, S. H. The biotin switch method for the detection of S-nitrosylated proteins. Science STKE 86, PL1 (2001).
42. Parsons, X. H., Garcia, S. N., Pillus, L. & Kadonaga, J. T. Histone deacetylation by Sir2 generates a transcriptionally repressed nucleoprotein complex. Proc. Natl Acad. Sci. USA 100, 1609-1614 (2003).