S-glutathionylation reshapes our understanding of endothelial nitric oxide synthase uncoupling and nitric oxide/reactive oxygen species-mediated signaling

Antioxidants and Redox Signaling

Volumn 14, Issue 10, 2011, Pages 1769-1775

  Zweier, Jay L ^a   Chen, Chun An ^a   Druhan, Lawrence J ^a  

^a THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLUTAREDOXIN; HEME; HYDROGEN PEROXIDE; METHYLARGININE; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; OXYGENASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE; TETRAHYDROBIOPTERIN; THIOREDOXIN; UNCLASSIFIED DRUG; UNCOUPLING PROTEIN;

ATHEROSCLEROSIS; CELL FUNCTION; DIABETES MELLITUS; DISEASE ASSOCIATION; HEART FAILURE; HYPERTENSION; ISCHEMIA; METABOLISM; NEOPLASM; OXIDATION; OXIDATIVE STRESS; PRIORITY JOURNAL; REPERFUSION INJURY; REVIEW; S GLUTATHIONYLATION;

ANIMALS; HUMANS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 79954608953     PISSN: 15230864     EISSN: None     Source Type: Journal    
DOI: 10.1089/ars.2011.3904     Document Type: Review

References (57)

1. Aota M, Matsuda K, Isowa N, Wada H, Yodoi J, and Ban T. Protection against reperfusion-induced arrhythmias by human thioredoxin. J Cardiovasc Pharmacol 27: 727-732, 1996. (Pubitemid 26134250)
2. Beckman JS, Beckman TW, Chen J, Marshall PA, and Freeman BA. Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc Natl Acad Sci USA 87: 1620-1624, 1990.
3. Berry C, Brosnan MJ, Fennell J, Hamilton CA, and Dominiczak AF. Oxidative stress and vascular damage in hypertension. Curr Opin Nephrol Hypertens 10: 247-255, 2001. (Pubitemid 32221768)
4. Biswas S, Chida AS, and Rahman I. Redox modifications of protein-thiols: emerging roles in cell signaling. Biochem Pharmacol 71: 551-564, 2006. (Pubitemid 43121989)
5. Boger RH, Sydow K, Borlak J, Thum T, Lenzen H, Schubert B, Tsikas D, and Bode-Boger SM. LDL cholesterol upregulates synthesis of asymmetrical dimethylarginine in human endothelial cells: involvement of S- adenosylmethioninedependent methyltransferases. Circ Res 87: 99-105, 2000. (Pubitemid 30616904)
6. Bredt DS, Hwang PM, Glatt CE, Lowenstein C, Reed RR, and Snyder SH. Cloned and expressed nitric oxide synthase structurally resembles cytochrome P-450 reductase. Nature 351: 714-718, 1991. (Pubitemid 21896670)
7. Cardounel AJ, Cui H, Samouilov A, Johnson W, Kearns P, Tsai AL, Berka V, and Zweier JL. Evidence for the pathophysiological role of endogenous methylarginines in regulation of endothelial NO production and vascular function. J Biol Chem 282: 879-887, 2007. (Pubitemid 47076535)
8. Chen CA, Wang TY, Varadharaj S, Reyes LA, Hemann C, Talukder MA, Chen YR, Druhan LJ, and Zweier JL. Sglutathionylation uncouples eNOS and regulates its cellular and vascular function. Nature 468: 1115-1118, 2010.
9. Chen CL, Zhang L, Yeh A, Chen CA, Green-Church KB, Zweier JL, and Chen YR. Site-specific S-glutathiolation of mitochondrial NADH ubiquinone reductase. Biochemistry 46: 5754-5765, 2007. (Pubitemid 46764124)
10. Chen W, Druhan LJ, Chen CA, Hemann C, Chen YR, Berka V, Tsai AL, and Zweier JL. Peroxynitrite induces destruction of the tetrahydrobiopterin and heme in endothelial nitric oxide synthase: transition from reversible to irreversible enzyme inhibition. Biochemistry 49: 3129-3137, 2010.
11. Chrestensen CA, Starke DW, and Mieyal JJ. Acute cadmium exposure inactivates thioltransferase (Glutaredoxin), inhibits intracellular reduction of protein-glutathionyl-mixed disulfides, and initiates apoptosis. J Biol Chem 275: 26556-26565, 2000.
12. Costa NJ, Dahm CC, Hurrell F, Taylor ER, and Murphy MP. Interactions of mitochondrial thiols with nitric oxide. Antioxid Redox Signal 5: 291-305, 2003. (Pubitemid 36793013)
13. Crabtree MJ, Tatham AL, Hale AB, Alp NJ, and Channon KM. Critical role for tetrahydrobiopterin recycling by dihydrofolate reductase in regulation of endothelial nitric-oxide synthase coupling: relative importance of the de novo biopterin synthesis versus salvage pathways. J Biol Chem 284: 28128-28136, 2009.
14. Druhan LJ, Forbes SP, Pope AJ, Chen CA, Zweier JL, and Cardounel AJ. Regulation of eNOS-derived superoxide by endogenous methylarginines. Biochemistry 47: 7256-7263, 2008. (Pubitemid 351956374)
15. Dumitrescu C, Biondi R, Xia Y, Cardounel AJ, Druhan LJ, Ambrosio G, and Zweier JL. Myocardial ischemia results in tetrahydrobiopterin (BH4) oxidation with impaired endothelial function ameliorated by BH4. Proc Natl Acad Sci USA 104: 15081-15086, 2007. (Pubitemid 47619596)
16. Forbes SP, Druhan LJ, Guzman JE, Parinandi N, Zhang L, Green-Church KB, and Cardounel AJ. Mechanism of 4-HNE mediated inhibition of hDDAH-1: implications in no regulation. Biochemistry 47: 1819-1826, 2008. (Pubitemid 351231231)
17. Ghezzi P. Regulation of protein function by glutathionylation. Free Radic Res 39: 573-580, 2005. (Pubitemid 40846828)
18. Giles GI and Jacob C. Reactive sulfur species: an emerging concept in oxidative stress. Biol Chem 383: 375-388, 2002. (Pubitemid 34506278)
19. Giustarini D, Rossi R, Milzani A, Colombo R, and Dalle-Donne I. S-glutathionylation: from redox regulation of protein functions to human diseases. J Cell Mol Med 8: 201-212, 2004. (Pubitemid 44145509)
20. Harbrecht BG, Di Silvio M, Chough V, Kim YM, Simmons RL, and Billiar TR. Glutathione regulates nitric oxide synthase in cultured hepatocytes. Ann Surg 225: 76-87, 1997. (Pubitemid 27026806)
21. Hofmann H and Schmidt HH. Thiol dependence of nitric oxide synthase. Biochemistry 34: 13443-13452, 1995.
22. Huang A, Xiao H, Samii JM, Vita JA, and Keaney JF, Jr. Contrasting effects of thiol-modulating agents on endothelial NO bioactivity. Am J Physiol Cell Physiol 281: C719-C725, 2001.
23. Hunley TE, Iwasaki S, Homma T, and Kon V. Nitric oxide and endothelin in pathophysiological settings. Pediatr Nephrol 9: 235-244, 1995.
24. Lin KY, Ito A, Asagami T, Tsao PS, Adimoolam S, Kimoto M, Tsuji H, Reaven GM, and Cooke JP. Impaired nitric oxide synthase pathway in diabetes mellitus: role of asymmetric dimethylarginine and dimethylarginine dimethylaminohydrolase. Circulation 106: 987-992, 2002. (Pubitemid 34925335)
25. List BM, Klosch B, Volker C, Gorren AC, Sessa WC, Werner ER, Kukovetz WR, Schmidt K, and Mayer B. Characterization of bovine endothelial nitric oxide synthase as a homodimer with down-regulated uncoupled NADPH oxidase activity: tetrahydrobiopterin binding kinetics and role of haem in dimerization. Biochem J 323 (Pt 1): 159-165, 1997. (Pubitemid 27153889)
26. Malik G, Nagy N, Ho YS, Maulik N, and Das DK. Role of glutaredoxin-1 in cardioprotection: an insight with Glrx1 transgenic and knockout animals. J Mol Cell Cardiol 44: 261-269, 2008. (Pubitemid 351226190)
27. McCord JM. Oxygen-derived free radicals in postischemic tissue injury. N Engl J Med 312: 159-163, 1985. (Pubitemid 15192863)
28. Okamoto T, Akaike T, Sawa T, Miyamoto Y, van der Vliet A, and Maeda H. Activation of matrix metalloproteinases by peroxynitrite-induced protein S-glutathiolation via disulfide S-oxide formation. J Biol Chem 276: 29596-29602, 2001.
29. Palmer RM, Ashton DS, and Moncada S. Vascular endothelial cells synthesize nitric oxide from L-arginine. Nature 333: 664-666, 1988.
30. Panda K, Ghosh S, and Stuehr DJ. Calmodulin activates intersubunit electron transfer in the neuronal nitric-oxide synthase dimer. J Biol Chem 276: 23349-23356, 2001.
31. Pou S, Pou WS, Bredt DS, Snyder SH, and Rosen GM. Generation of superoxide by purified brain nitric oxide synthase. J Biol Chem 267: 24173-24176, 1992.
32. Rapoport RM, Draznin MB, and Murad F. Endotheliumdependent relaxation in rat aorta may be mediated through cyclic GMP-dependent protein phosphorylation. Nature 306: 174-176, 1983. (Pubitemid 14228339)
33. Reddy S, Jones AD, Cross CE, Wong PS, and Van Der Vliet A. Inactivation of creatine kinase by S-glutathionylation of the active-site cysteine residue. Biochem J 347 Pt 3: 821-827, 2000. (Pubitemid 30260974)
34. Sheehy AM, Burson MA, and Black SM. Nitric oxide exposure inhibits endothelial NOS activity but not gene expression: a role for superoxide. Am J Physiol 274: L833-L841, 1998.
35. Sorescu D and Griendling KK. Reactive oxygen species, mitochondria, and NAD(P)H oxidases in the development and progression of heart failure. Congest Heart Fail 8: 132-140, 2002. (Pubitemid 34669892)
36. Stuehr DJ, Santolini J, Wang ZQ, Wei CC, and Adak S. Update on mechanism and catalytic regulation in the NO synthases. J Biol Chem 279: 36167-36170, 2004. (Pubitemid 39128949)
37. Sun J, Druhan LJ, and Zweier JL. Dose dependent effects of reactive oxygen and nitrogen species on the function of neuronal nitric oxide synthase. Arch Biochem Biophys 471: 126-133, 2008. (Pubitemid 351308077)
38. Sun J, Druhan LJ, and Zweier JL. Reactive oxygen and nitrogen species regulate inducible nitric oxide synthase function shifting the balance of nitric oxide and superoxide production. Arch Biochem Biophys 494: 130-137, 2010.
39. Sydow K, Hornig B, Arakawa N, Bode-Boger SM, Tsikas D, Munzel T, and Boger RH. Endothelial dysfunction in patients with peripheral arterial disease and chronic hyperhomocysteinemia: potential role of ADMA. Vasc Med 9: 93-101, 2004. (Pubitemid 39406423)
40. Sydow K, Schwedhelm E, Arakawa N, Bode-Boger SM, Tsikas D, Hornig B, Frolich JC, and Boger RH. ADMA and oxidative stress are responsible for endothelial dysfunction in hyperhomocyst(e)inemia: effects of L-arginine and B vitamins. Cardiovasc Res 57: 244-252, 2003. (Pubitemid 36009457)
41. Tiefenbacher CP, Chilian WM, Mitchell M, and DeFily DV. Restoration of endothelium-dependent vasodilation after reperfusion injury by tetrahydrobiopterin. Circulation 94: 1423-1429, 1996. (Pubitemid 26307275)
42. Tummala M, Ryzhov V, Ravi K, and Black SM. Identification of the cysteine nitrosylation sites in human endothelial nitric oxide synthase. DNA Cell Biol 27: 25-33, 2008.
43. Vasquez-Vivar J, Kalyanaraman B, Martasek P, Hogg N, Masters BS, Karoui H, Tordo P, and Pritchard KA, Jr. Superoxide generation by endothelial nitric oxide synthase: the influence of cofactors. Proc Natl Acad Sci USA 95: 9220-9225, 1998. (Pubitemid 28506212)
44. Vasquez-Vivar J, Martasek P, Whitsett J, Joseph J, and Kalyanaraman B. The ratio between tetrahydrobiopterin and oxidized tetrahydrobiopterin analogues controls superoxide release from endothelial nitric oxide synthase: an EPR spin trapping study. Biochem J 362: 733-739, 2002. (Pubitemid 34242326)
45. Venardos KM, Perkins A, Headrick J, and Kaye DM. Myocardial ischemia-reperfusion injury, antioxidant enzyme systems, and selenium: a review. Curr Med Chem 14: 1539-1549, 2007. (Pubitemid 46902214)
46. Wang P and Zweier JL. Measurement of nitric oxide and peroxynitrite generation in the postischemic heart. Evidence for peroxynitrite-mediated reperfusion injury. J Biol Chem 271: 29223-29230, 1996. (Pubitemid 26382634)
47. Wei CC, Wang ZQ, Tejero J, Yang YP, Hemann C, Hille R, and Stuehr DJ. Catalytic reduction of a tetrahydrobiopterin radical within nitric-oxide synthase. J Biol Chem 283: 11734-11742, 2008.
48. Wolin MS. Reactive oxygen species and vascular signal transduction mechanisms. Microcirculation 3: 1-17, 1996. (Pubitemid 126445149)
49. Xia Y, Dawson VL, Dawson TM, Snyder SH, and Zweier JL. Nitric oxide synthase generates superoxide and nitric oxide in arginine-depleted cells leading to peroxynitrite-mediated cellular injury. Proc Natl Acad Sci USA 93: 6770-6774, 1996.
50. Xia Y, Tsai AL, Berka V, and Zweier JL. Superoxide generation from endothelial nitric-oxide synthase. A Ca2 + / calmodulin-dependent and tetrahydrobiopterin regulatory process. J Biol Chem 273: 25804-25808, 1998.
51. Xia Y and Zweier JL. Superoxide and peroxynitrite generation from inducible nitric oxide synthase in macrophages. Proc Natl Acad Sci USA 94: 6954-6958, 1997. (Pubitemid 27281972)
52. Zhang J, Li YD, Patel JM, and Block ER. Thioredoxin overexpression prevents NO-induced reduction of NO synthase activity in lung endothelial cells. Am J Physiol 275: L288-L293, 1998.
53. Zou MH, Shi C, and Cohen RA. Oxidation of the zinc-thiolate complex and uncoupling of endothelial nitric oxide synthase by peroxynitrite. J Clin Invest 109: 817-826, 2002. (Pubitemid 34263158)
54. Zou MH and Ullrich V. Peroxynitrite formed by simultaneous generation of nitric oxide and superoxide selectively inhibits bovine aortic prostacyclin synthase. FEBS Lett 382: 101-104, 1996. (Pubitemid 26092944)
55. Zweier JL, Fertmann J, and Wei G. Nitric oxide and peroxynitrite in postischemic myocardium. Antioxid Redox Signal 3: 11-22, 2001. (Pubitemid 32240626)
56. Zweier JL, Flaherty JT, and Weisfeldt ML. Direct measurement of free radical generation following reperfusion of ischemic myocardium. Proc Natl Acad Sci USA 84: 1404-1407, 1987. (Pubitemid 17027362)
57. Zweier JL and Talukder MA. The role of oxidants and free radicals in reperfusion injury. Cardiovasc Res 70: 181-190, 2006.