STAT3 regulation by S-nitrosylation: Implication for inflammatory disease

Antioxidants and Redox Signaling

Volumn 20, Issue 16, 2014, Pages 2514-2527

  Kim, Jinsu ^a   Won, Je Seong ^a   Singh, Avtar K ^a,b   Sharma, Anand K ^a   Singh, Inderjit ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b RALPH H JOHNSON VA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; CYSTEINE; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 6; JANUS KINASE 2; NITRIC OXIDE; STAT3 PROTEIN; THIOL DERIVATIVE; TYROSINE; STAT3 PROTEIN, MOUSE;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; GENE EXPRESSION; GLUTATHIONYLATION; IMMUNE RESPONSE; INFLAMMATORY DISEASE; MICROGLIA; MOUSE; NITROSYLATION; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TRANSACTIVATION; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL CULTURE; CELL SURVIVAL; DISEASES; DRUG EFFECTS; GENETICS; INFLAMMATION; METABOLISM; PHOSPHORYLATION;

ANIMALS; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; DISEASE; INFLAMMATION; MICE; NITRIC OXIDE; OXIDATION-REDUCTION; PHOSPHORYLATION; STAT3 TRANSCRIPTION FACTOR;

EID: 84900403543     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2013.5223     Document Type: Article

References (60)

1. Anand P and Stamler JS. Enzymatic mechanisms regulating protein S-nitrosylation: implications in health and disease. J Mol Med (Berl) 90: 233-244, 2012.
2. Baker TL, Booden MA, and Buss JE. S-Nitrosocysteine increases palmitate turnover on Ha-Ras in NIH 3T3 cells. J Biol Chem 275: 22037-22047, 2000.
3. Block ML and Hong JS. Microglia and inflammation-mediated neurodegeneration: multiple triggers with a common mechanism. Prog Neurobiol 76: 77-98, 2005.
4. Bromberg JF, Wrzeszczynska MH, Devgan G, Zhao Y, Pes-tell RG, Albanese C, and Darnell JE, Jr. Stat3 as an oncogene. Cell 98: 295-303, 1999.
5. Campbell IL. Cytokine-mediated inflammation, tumori-genesis, and disease-associated JAK/STAT/SOCS signaling circuits in the CNS. Brain Res Brain Res Rev 48: 166-177, 2005.
6. Ceron PI, Cremonez DC, Bendhack LM, and Tedesco AC. The relaxation induced by S-nitroso-glutathione and S-nitroso-N-acetylcysteine in rat aorta is not related to nitric oxide production. J Pharmacol Exp Ther 298: 686-694, 2001.
7. Chen YY, Chu HM, Pan KT, Teng CH, Wang DL, Wang AH, Khoo KH, and Meng TC. Cysteine S-nitrosylation protects protein-tyrosine phosphatase 1B against oxidation-induced permanent inactivation. J Biol Chem 283: 35265-35272, 2008.
8. Chiueh CC and Rauhala P. The redox pathway of S-ni-trosoglutathione, glutathione and nitric oxide in cell to neuron communications. Free Radic Res 31: 641-650, 1999.
9. Chung J, Uchida E, Grammer TC, and Blenis J. STAT3 serine phosphorylation by ERK-dependent and-independent pathways negatively modulates its tyrosine phosphoryla-tion. Mol Cell Biol 17: 6508-6516, 1997.
10. Curcio MF, Batista WL, Linares E, Nascimento FD, Moraes MS, Borges RE, Sap J, Stern A, and Monteiro HP. Regulatory effects of nitric oxide on Src kinase, FAK, p130Cas, and receptor protein tyrosine phosphatase alpha (PTP-alpha): a role for the cellular redox environment. Antioxid Redox Signal 13: 109-125, 2010.
11. Davis KL, Martin E, Turko IV, and Murad F. Novel effects of nitric oxide. Annu Rev Pharmacol Toxicol 41: 203-236, 2001.
12. de Belder AJ, MacAllister R, Radomski MW, Moncada S, and Vallance PJ. Effects of S-nitroso-glutathione in the human forearm circulation: evidence for selective inhibition of platelet activation. Cardiovasc Res 28: 691-694, 1994.
13. Decker T and Kovarik P. Serine phosphorylation of STATs. Oncogene 19: 2628-2637, 2000.
14. Dringen R. Oxidative and antioxidative potential of brain microglial cells. Antioxid Redox Signal 7: 1223-1233, 2005.
15. Foster MW, Hess DT, and Stamler JS. Protein S-nitrosylation in health and disease: a current perspective. Trends Mol Med 15: 391-404, 2009.
16. Foster MW, McMahon TJ, and Stamler JS. S-nitrosylation in health and disease. Trends Mol Med 9: 160-168, 2003.
17. Fukushima A, Loh K, Galic S, Fam B, Shields B, Wiede F, Tremblay ML, Watt MJ, Andrikopoulos S, and Tiganis T. T-cell protein tyrosine phosphatase attenuates STAT3 and insulin signaling in the liver to regulate gluconeogenesis. Diabetes 59: 1906-1914, 2010.
18. Giri S, Nath N, Smith B, Viollet B, Singh AK, and Singh I. 5-aminoimidazole-4-carboxamide-1-beta-4-ribofuranoside inhibits proinflammatory response in glial cells: a possible role of AMP-activated protein kinase. J Neurosci 24: 479-487, 2004.
19. Gow AJ, Buerk DG, and Ischiropoulos H. A novel reaction mechanism for the formation of S-nitrosothiol in vivo. J Biol Chem 272: 2841-2845, 1997.
20. Guan W, Sha J, Chen X, Xing Y, Yan J, and Wang Z. S-Nitrosylation of mitogen activated protein kinase phospha-tase-1 suppresses radiation-induced apoptosis. Cancer Lett 314: 137-146, 2012.
21. Heinrich PC, Behrmann I, Muller-Newen G, Schaper F, and Graeve L. Interleukin-6-type cytokine signalling through the gp130/Jak/STAT pathway. Biochem J 334 (Pt 2): 297-314, 1998.
22. Herrmann JE, Imura T, Song B, Qi J, Ao Y, Nguyen TK, Korsak RA, Takeda K, Akira S, and Sofroniew MV. STAT3 is a critical regulator of astrogliosis and scar formation after spinal cord injury. J Neurosci 28: 7231-7243, 2008.
23. Hess DT, Patterson SI, Smith DS, and Skene JH. Neuronal growth cone collapse and inhibition of protein fatty acyla-tion by nitric oxide. Nature 366: 562-565, 1993.
24. Hess DT and Stamler JS. Regulation by S-nitrosylation of protein post-translational modification. J Biol Chem 287: 4411-4418, 2012.
25. Kacimi R, Giffard RG, and Yenari MA. Endotoxin-activated microglia injure brain derived endothelial cells via NF-kappaB, JAK-STAT and JNK stress kinase pathways. J Inflamm (Lond) 8: 7, 2011.
26. Kawahara K, Gotoh T, Oyadomari S, Kuniyasu A, Kohsaka S, Mori M, and Nakayama H. Nitric oxide inhibits the proliferation of murine microglial MG5 cells by a mechanism involving p21 but independent of p53 and cyclic guanosine monophosphate. Neurosci Lett 310: 89-92, 2001.
27. Khan M, Sekhon B, Giri S, Jatana M, Gilg AG, Ayasolla K, Elango C, Singh AK, and Singh I. S-Nitrosoglutathione reduces inflammation and protects brain against focal cerebral ischemia in a rat model of experimental stroke. J Cereb Blood Flow Metab 25: 177-192, 2005.
28. Kim OS, Park EJ, Joe EH, and Jou I. JAK-STAT signaling mediates gangliosides-induced inflammatory responses in brain microglial cells. J Biol Chem 277: 40594-40601, 2002.
29. Lai SY and Johnson FM. Defining the role of the JAK-STAT pathway in head and neck and thoracic malignancies: implications for future therapeutic approaches. Drug Resist Updat 13: 67-78, 2010.
30. Marshall HE and Stamler JS. Inhibition of NF-kappa B by S-nitrosylation. Biochemistry 40: 1688-1693, 2001.
31. Mohr S, Hallak H, de Boitte A, Lapetina EG, and Brune B. Nitric oxide-induced S-glutathionylation and inactivation of glyceraldehyde-3-phosphate dehydrogenase. J Biol Chem 274: 9427-9430, 1999.
32. Nath N, Morinaga O, and Singh I. S-nitrosoglutathione a physiologic nitric oxide carrier attenuates experimental autoimmune encephalomyelitis. J Neuroimmune Pharmacol 5: 240-251, 2010.
33. Page BD, Ball DP, and Gunning PT. Signal transducer and activator of transcription 3 inhibitors: a patent review. Expert Opin Ther Pat 21: 65-83, 2011.
34. Papapetropoulos A, Rudic RD, and Sessa WC. Molecular control of nitric oxide synthases in the cardiovascular system. Cardiovasc Res 43: 509-520, 1999.
35. Park HS, Yu JW, Cho JH, Kim MS, Huh SH, Ryoo K, and Choi EJ. Inhibition of apoptosis signal-regulating kinase 1 by nitric oxide through a thiol redox mechanism. J Biol Chem 279: 7584-7590, 2004.
36. Pastore A and Piemonte F. S-Glutathionylation signaling in cell biology: progress and prospects. Eur J Pharm Sci 46: 279-292, 2012.
37. Pei DS, Sun YF, and Song YJ. S-nitrosylation of PTEN In-vovled in ischemic brain injury in rat hippocampal CA1 region. Neurochem Res 34: 1507-1512, 2009.
38. Pfitzner E, Kliem S, Baus D, and Litterst CM. The role of STATs in inflammation and inflammatory diseases. Curr Pharm Des 10: 2839-2850, 2004.
39. Prasad R, Giri S, Nath N, Singh I, and Singh AK. GSNO attenuates EAE disease by S-nitrosylation-mediated modulation of endothelial-monocyte interactions. Glia 55: 65-77, 2007.
40. Que LG, Yang Z, Stamler JS, Lugogo NL, and Kraft M. S-nitrosoglutathione reductase: an important regulator in human asthma. Am J Respir Crit Care Med 180: 226-231, 2009.
41. Ray S, Boldogh I, and Brasier AR. STAT3 NH2-terminal acetylation is activated by the hepatic acute-phase response and required for IL-6 induction of angiotensinogen. Gastro-enterology 129: 1616-1632, 2005.
42. Real PJ, Sierra A, De Juan A, Segovia JC, Lopez-Vega JM, and Fernandez-Luna JL. Resistance to chemotherapy via Stat3-dependent overexpression of Bcl-2 in metastatic breast cancer cells. Oncogene 21: 7611-7618, 2002.
43. Sengupta R and Holmgren A. Thioredoxin and thioredoxin reductase in relation to reversible S-nitrosylation. Antioxid Redox Signal 18: 259-269, 2013.
44. Seth D and Stamler JS. The SNO-proteome: causation and classifications. Curr Opin Chem Biol 15: 129-136, 2011.
45. Stamler JS, Lamas S, and Fang FC. Nitrosylation. the prototypic redox-based signaling mechanism. Cell 106: 675-683, 2001.
46. Stamler JS, Simon DI, Osborne JA, Mullins ME, Jaraki O, Michel T, Singel DJ, and Loscalzo J. S-nitrosylation of proteins with nitric oxide: synthesis and characterization of biologically active compounds. Proc Natl Acad Sci U S A 89: 444-448, 1992.
47. Wang H and Xian M. Chemical methods to detect S-ni-trosation. Curr Opin Chem Biol 15: 32-37, 2011.
48. Wang Z. Protein S-nitrosylation and cancer. Cancer Lett 320: 123-129, 2012.
49. Wilms H, Rosenstiel P, Sievers J, Deuschl G, Zecca L, and Lucius R. Activation of microglia by human neuromelanin is NF-kappaB dependent and involves p38 mitogen-activated protein kinase: implications for Parkinson's disease. FASEB J 17: 500-502, 2003.
50. Won JS, Im YB, Key L, Singh I, and Singh AK. The involvement of glucose metabolism in the regulation of in-ducible nitric oxide synthase gene expression in glial cells: possible role of glucose-6-phosphate dehydrogenase and CCAAT/enhancing binding protein. J Neurosci 23: 7470-7478, 2003.
51. Xie Y, Kole S, Precht P, Pazin MJ, and Bernier M. S-glu-tathionylation impairs signal transducer and activator of transcription 3 activation and signaling. Endocrinology 150: 1122-1131, 2009.
52. Yang J, Huang J, Dasgupta M, Sears N, Miyagi M, Wang B, Chance MR, Chen X, Du Y, Wang Y, An L, Wang Q, Lu T, Zhang X, Wang Z, and Stark GR. Reversible methylation of promoter-bound STAT3 by histone-modifying enzymes. Proc Natl Acad Sci U S A 107: 21499-21504, 2010.
53. Yuan ZL, Guan YJ, Chatterjee D, and Chin YE. Stat3 di-merization regulated by reversible acetylation of a single lysine residue. Science 307: 269-273, 2005.
54. Zaman K, Carraro S, Doherty J, Henderson EM, Lendermon E, Liu L, Verghese G, Zigler M, Ross M, Park E, Palmer LA, Doctor A, Stamler JS, and Gaston B. S-nitrosylating agents: a novel class of compounds that increase cystic fibrosis transmembrane conductance regulator expression and maturation in epithelial cells. Mol Pharmacol 70: 1435-1442, 2006.
55. Zaman K, Palmer LA, and CGaston B. S-nitrosothiol signaling and gene regulation in pulmonary pathophysiology. In: Nitric oxide, Cell Signaling, and Gene Expression, edited by Lamas S and Cadenas E. Boca Ranton, FL: CRC Press; 2006, pp. 321-330.
56. Zhang P, Yu PC, Tsang AH, Chen Y, Fu AK, Fu WY, Chung KK, and Ip NY. S-nitrosylation of cyclin-dependent kinase 5 (cdk5) regulates its kinase activity and dendrite growth during neuronal development. J Neurosci 30: 14366-14370, 2010.
57. Zhang T, Kee WH, Seow KT, Fung W, and Cao X. The coiled-coil domain of Stat3 is essential for its SH2 domainmediated receptor binding and subsequent activation induced by epidermal growth factor and interleukin-6. Mol Cell Biol 20: 7132-7139, 2000.
58. Zhang T, Seow KT, Ong CT, and Cao X. Interdomain interaction of Stat3 regulates its Src homology 2 domain-mediated receptor binding activity. J Biol Chem 277: 17556-17563, 2002.
59. Zhang Y and Hogg N. The mechanism of transmembrane S-nitrosothiol transport. Proc Natl Acad Sci U S A 101: 7891-7896, 2004.
60. Zhong Z, Wen Z, and Darnell JE, Jr. Stat3: a STAT family member activated by tyrosine phosphorylation in response to epidermal growth factor and interleukin-6. Science 264: 95-98, 1994.