Role of Nrf2-mediated heme oxygenase-1 upregulation in adaptive survival response to nitrosative stress

Archives of Pharmacal Research

Volumn 32, Issue 8, 2009, Pages 1163-1176

  Surh, Young Joon ^a   Kundu, Joydeb Kumar ^a,c   Li, Mei Hua ^a   Na, Hye Kyung ^a   Cha, Young Nam ^b  

^a Seoul National University   (South Korea)

^b Inha University School of Medicine   (South Korea)

^c UNIVERSITY OF DHAKA   (Bangladesh)

Author keywords

Heme oxygenase 1; Nitric oxide; Nitrosative stress; Nrf2; Peroxynitrite

Indexed keywords

ALPHA TOCOPHEROL; ASCORBIC ACID; CARBON MONOXIDE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLUTATHIONE; HEME OXYGENASE 1; INDUCIBLE NITRIC OXIDE SYNTHASE; KELCH LIKE ECH ASSOCIATED PROTEIN 1; NEURONAL NITRIC OXIDE SYNTHASE; PEROXYNITRITE; RETINOL; THIOREDOXIN; TRANSCRIPTION FACTOR NRF2;

CELL DEATH; CELL SURVIVAL; HYPOXIA; NITROSATIVE STRESS; NONHUMAN; PROTEIN PHOSPHORYLATION; REVIEW;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; CARBON MONOXIDE; CELL DEATH; CELL SURVIVAL; CYTOPROTECTION; GLUTAMATE-CYSTEINE LIGASE; GLUTATHIONE; HEME OXYGENASE-1; HUMANS; MAP KINASE SIGNALING SYSTEM; NF-E2-RELATED FACTOR 2; PHOSPHORYLATION; REACTIVE NITROGEN SPECIES; STRESS, PHYSIOLOGICAL; UP-REGULATION;

EID: 69949086594     PISSN: 02536269     EISSN: 19763786     Source Type: Journal    
DOI: 10.1007/s12272-009-1807-8     Document Type: Review

References (103)

1. N. G. Abraham T. Kushida J. McClung M. Weiss S. Quan R. Lafaro Z. Darzynkiewicz M. Wolin 2003 Heme oxygenase-1 attenuates glucose-mediated cell growth arrest and apoptosis in human microvessel endothelial cells Circ. Res. 93 507 514
2. P. M. Bauer G. M. Buga J. M. Fukuto A. E. Pegg L. J. Ignarro 2001 Nitric oxide inhibits ornithine decarboxylase via S-nitrosylation of cysteine 360 in the active site of the enzyme J. Biol. Chem. 276 34458 34464
3. J. S. Beckman 1996 Oxidative damage and tyrosine nitration from peroxynitrite Chem. Res. Toxicol. 9 836 844
4. A. Bishop J. C. Marquis N. R. Cashman B. Demple 1999 Adaptive resistance to nitric oxide in motor neurons Free Radic. Biol. Med. 26 978 986
5. A. Bishop S. F. Yet M. E. Lee M. A. Perrella B. Demple 2004 A key role for heme oxygenase-1 in nitric oxide resistance in murine motor neurons and glia Biochem. Biophys. Res. Commun. 325 3 9
6. D. Bloom S. Dhakshinamoorthy A. K. Jaiswal 2002 Site-directed mutagenesis of cysteine to serine in the DNA binding region of Nrf2 decreases its capacity to upregulate antioxidant response element-mediated expression and antioxidant induction of NAD(P)H:quinone oxidoreductase1 gene Oncogene 21 2191 2200
7. D. A. Bloom A. K. Jaiswal 2003 Phosphorylation of Nrf2 at Ser40 by protein kinase C in response to antioxidants leads to the release of Nrf2 from INrf2, but is not required for Nrf2 stabilization/accumulation in the nucleus and transcriptional activation of antioxidant response element-mediated NAD(P)H:quinone oxidoreductase-1 gene expression J. Biol. Chem. 278 44675 44682
8. D. Botta C. C. Franklin C. C. White C. M. Krejsa M. J. Dabrowski R. H. Pierce N. Fausto T. J. Kavanagh 2004 Glutamate-cysteine ligase attenuates TNF-induced mitochondrial injury and apoptosis Free Radic. Biol. Med. 37 632 642
9. C. Bouton M. Raveau J. C. Drapier 1996 Modulation of iron regulatory protein functions. Further insights into the role of nitrogen- and oxygen-derived reactive species J. Biol. Chem. 271 2300 2306
10. B. J. Buckley S. Li A. R. Whorton 2008 Keap1 modification and nuclear accumulation in response to S-nitrosocysteine Free Radic. Biol. Med. 44 692 698
11. B. J. Buckley Z. M. Marshall A. R. Whorton 2003 Nitric oxide stimulates Nrf2 nuclear translocation in vascular endothelium Biochem. Biophys. Res. Commun. 307 973 979
12. B. J. Buckley A. R. Whorton 2000 Adaptive responses to peroxynitrite: increased glutathione levels and cystine uptake in vascular cells Am. J. Physiol. Cell Physiol. 279 C1168 1176
13. B. M. Choi H. O. Pae S. I. Jang Y. M. Kim H. T. Chung 2002 Nitric oxide as a pro-apoptotic as well as anti-apoptotic modulator J. Biochem. Mol. Biol. 35 116 126
14. H. T. Chung B. M. Choi Y. G. Kwon Y. M. Kim 2008 Interactive relations between nitric oxide (NO) and carbon monoxide (CO): heme oxygenase-1/CO pathway is a key modulator in NO-mediated antiapoptosis and anti-inflammation Methods Enzymol. 441 329 338
15. C. S. Cobbs T. R. Whisenhunt D. R. Wesemann L. E. Harkins E. G. Van Meir M. Samanta 2003 Inactivation of wild-type p53 protein function by reactive oxygen and nitrogen species in malignant glioma cells Cancer Res. 63 8670 8673
16. M. Colasanti H. Suzuki 2000 The dual personality of NO Trends Pharmacol. Sci. 21 249 252
17. S. Cui J. S. Reichner R. B. Mateo J. E. Albina 1994 Activated murine macrophages induce apoptosis in tumor cells through nitric oxide-dependent or -independent mechanisms Cancer Res. 54 2462 2467
18. O. De Backer E. Elinck B. Blanckaert L. Leybaert R. Motterlini R. A. Lefebvre 2009 Water-soluble CO-releasing molecules reduce the development of postoperative ileus via modulation of MAPK/HO-1 signalling and reduction of oxidative stress Gut 58 347 356
19. S. Dhakshinamoorthy A. G. Porter 2004 Nitric oxide-induced transcriptional up-regulation of protective genes by Nrf2 via the antioxidant response element counteracts apoptosis of neuroblastoma cells J. Biol. Chem. 279 20096 20107
20. A. T. Dinkova-Kostova W. D. Holtzclaw R. N. Cole K. Itoh N. Wakabayashi Y. Katoh M. Yamamoto P. Talalay 2002 Direct evidence that sulfhydryl groups of Keap1 are the sensors regulating induction of phase 2 enzymes that protect against carcinogens and oxidants Proc. Natl. Acad. Sci. USA 99 11908 11913
21. P. J. Downard M. A. Wilson D. A. Spain P. J. Matheson Y. Siow R. N. Garrison 1997 Heme oxygenase-dependent carbon monoxide production is a hepatic adaptive response to sepsis J. Surg. Res. 71 7 12
22. J. C. Drapier J. B. Hibbs Jr. 1986 Murine cytotoxic activated macrophages inhibit aconitase in tumor cells. Inhibition involves the iron-sulfur prosthetic group and is reversible J. Clin. Invest. 78 790 797
23. J. C. Drapier J. Wietzerbin J. B. Hibbs Jr. 1988 Interferon-gamma and tumor necrosis factor induce the L-arginine-dependent cytotoxic effector mechanism in murine macrophages Eur. J. Immunol. 18 1587 1592
24. W. Durante M. H. Kroll N. Christodoulides K. J. Peyton A. I. Schafer 1997 Nitric oxide induces heme oxygenase-1 gene expression and carbon monoxide production in vascular smooth muscle cells Circ. Res. 80 557 564 (Pubitemid 27137293)
25. T. Esch G. B. Stefano G. L. Fricchione H. Benson 2002 Stress-related diseases - a potential role for nitric oxide Med. Sci. Monit. 8 RA103 118
26. F. C. Fang 1997 Perspectives series: host/pathogen interactions. Mechanisms of nitric oxide-related antimicrobial activity J. Clin. Invest. 99 2818 2825
27. K. Fehsel K. D. Kroncke K. L. Meyer H. Huber V. Wahn V. Kolb-Bachofen 1995 Nitric oxide induces apoptosis in mouse thymocytes J. Immunol. 155 2858 2865
28. C. D. Ferris S. R. Jaffrey A. Sawa M. Takahashi S. D. Brady R. K. Barrow S. A. Tysoe H. Wolosker D. E. Baranano S. Dore K. D. Poss S. H. Snyder 1999 Haem oxygenase-1 prevents cell death by regulating cellular iron Nat. Cell Biol. 1 152 157
29. R. Foresti J. E. Clark C. J. Green R. Motterlini 1997 Thiol compounds interact with nitric oxide in regulating heme oxygenase-1 induction in endothelial cells. Involvement of superoxide and peroxynitrite anions J. Biol. Chem. 272 18411 18417
30. H. Fujii T. Takahashi K. Nakahira K. Uehara H. Shimizu M. Matsumi K. Morita M. Hirakawa R. Akagi S. Sassa 2003 Protective role of heme oxygenase-1 in the intestinal tissue injury in an experimental model of sepsis Crit. Care Med. 31 893 902
31. R. F. Furchgott D. Jothianandan 1991 Endothelium-dependent and -independent vasodilation involving cyclic GMP: relaxation induced by nitric oxide, carbon monoxide and light Blood Vessels 28 52 61
32. M. E. Gegg B. Beltran S. Salas-Pino J. P. Bolanos J. B. Clark S. Moncada S. J. Heales 2003 Differential effect of nitric oxide on glutathione metabolism and mitochondrial function in astrocytes and neurones: implications for neuroprotection/neurodegeneration? J. Neurochem. 86 228 237
33. P. Gong A. I. Cederbaum N. Nieto 2004 Heme oxygenase-1 protects HepG2 cells against cytochrome P450 2E1-dependent toxicity Free Radic. Biol. Med. 36 307 318
34. O. W. Griffith R. T. Mulcahy 1999 The enzymes of glutathione synthesis: gamma-glutamylcysteine synthetase Adv. Enzymol. Relat. Areas Mol. Biol. 73 209 267
35. A. Grilli M. A. De Lutiis A. Patruno L. Speranza F. Gizzi A. A. Taccardi P. Di Napoli R. De Caterina P. Conti M. Felaco 2003 Inducible nitric oxide synthase and heme oxygenase-1 in rat heart: direct effect of chronic exposure to hypoxia Ann. Clin. Lab. Sci. 33 208 215 (Pubitemid 36705932)
36. T. J. Guzik R. Korbut T. Adamek-Guzik 2003 Nitric oxide and superoxide in inflammation and immune regulation J. Physiol. Pharmacol. 54 469 487
37. E. Hara K. Takahashi K. Takeda M. Nakayama M. Yoshizawa H. Fujita K. Shirato S. Shibahara 1999 Induction of heme oxygenase-1 as a response in sensing the signals evoked by distinct nitric oxide donors Biochem. Pharmacol. 58 227 236
38. M. T. Heneka P. A. Loschmann M. Gleichmann M. Weller J. B. Schulz U. Wullner T. Klockgether 1998 Induction of nitric oxide synthase and nitric oxide-mediated apoptosis in neuronal PC12 cells after stimulation with tumor necrosis factor-alpha/lipopolysaccharide J. Neurochem. 71 88 94
39. D. T. Hess A. Matsumoto S. O. Kim H. E. Marshall J. S. Stamler 2005 Protein S-nitrosylation: purview and parameters Nat. Rev. Mol. Cell. Biol. 6 150 166
40. M. Husain T. J. Bourret B. D. McCollister J. Jones-Carson J. Laughlin A. Vazquez-Torres 2008 Nitric oxide evokes an adaptive response to oxidative stress by arresting respiration J. Biol. Chem. 283 7682 7689
41. H. Ischiropoulos 2003 Biological selectivity and functional aspects of protein tyrosine nitration Biochem. Biophys. Res. Commun. 305 776 783
42. K. Itoh N. Wakabayashi Y. Katoh T. Ishii K. Igarashi J. D. Engel M. Yamamoto 1999 Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain Genes Dev. 13 76 86
43. R. M. Jackson G. Parish E. S. Helton 1998 Peroxynitrite modulates MnSOD gene expression in lung epithelial cells Free Radic. Biol. Med. 25 463 472
44. A. K. Jain S. Mahajan A. K. Jaiswal 2008 Phosphorylation and dephosphorylation of tyrosine 141 regulate stability and degradation of INrf2: a novel mechanism in Nrf2 activation J. Biol. Chem. 283 17712 17720
45. J. H. Jang O. I. Aruoma L. S. Jen H. Y. Chung Y.-J. Surh 2004 Ergothioneine rescues PC12 cells from beta-amyloid-induced apoptotic death Free Radic. Biol. Med. 36 288 299
46. K. W. Kang S. H. Choi S. G. Kim 2002 Peroxynitrite activates NF-E2-related factor 2/antioxidant response element through the pathway of phosphatidylinositol 3-kinase: the role of nitric oxide synthase in rat glutathione S-transferase A2 induction Nitric Oxide 7 244 253
47. H. P. Kim S. W. Ryter A. M. Choi 2006 CO as a cellular signaling molecule Annu. Rev. Pharmacol. Toxicol. 46 411 449
48. 2-induced apoptosis through Nrf2-mediated upregulation of heme oxygenase-1: potential roles of Akt and ERK1/2 Biochem. Pharmacol. 76 1577 1589
49. J. P. Kolb 2000 Mechanisms involved in the pro- and anti-apoptotic role of NO in human leukemia Leukemia 14 1685 1694
50. R. Kurozumi M. Takahashi S. Kojima 2005 Involvement of mitochondrial peroxynitrite in nitric oxide-induced glutathione synthesis Biol. Pharm. Bull. 28 779 785
51. B. S. Lee J. Heo Y. M. Kim S. M. Shim H. O. Pae H. T. Chung 2006 Carbon monoxide mediates heme oxygenase 1 induction via Nrf2 activation in hepatoma cells Biochem. Biophys. Res. Commun. 343 965 972
52. J. M. Lee J. A. Johnson 2004 An important role of Nrf2-ARE pathway in the cellular defense mechanism J. Biochem. Mol. Biol. 37 139 143
53. L. Leon J. F. Jeannin A. Bettaieb 2008 Post-translational modifications induced by nitric oxide (NO): implication in cancer cells apoptosis Nitric Oxide 19 77 83
54. H. Li Z. M. Marshall A. R. Whorton 1999 Stimulation of cystine uptake by nitric oxide: regulation of endothelial cell glutathione levels Am. J. Physiol. 276 C803 811
55. M. H. Li Y. N. Cha Y.-J. Surh 2006 Carbon monoxide protects PC12 cells from peroxynitrite-induced apoptotic death by preventing the depolarization of mitochondrial transmembrane potential Biochem. Biophys. Res. Commun. 342 984 990
56. M. H. Li Y. N. Cha Y.-J. Surh 2006 Peroxynitrite induces HO-1 expression via PI3K/Akt-dependent activation of NF-E2-related factor 2 in PC12 cells Free Radic. Biol. Med. 41 1079 1091
57. M. H. Li J. H. Jang H. K. Na Y. N. Cha Y. J. Surh 2007 Carbon monoxide produced by heme oxygenase-1 in response to nitrosative stress induces expression of glutamate-cysteine ligase in PC12 cells via activation of phosphatidylinositol 3-kinase and Nrf2 signaling J. Biol. Chem. 282 28577 28586
58. S. Y. Lim J. H. Jang H. K. Na S. C. Lu I. Rahman Y.-J. Surh 2004 15-Deoxy-Delta12,14-prostaglandin J(2) protects against nitrosative PC12 cell death through up-regulation of intracellular glutathione synthesis J. Biol. Chem. 279 46263 46270
59. X. M. Liu K. J. Peyton D. Ensenat H. Wang M. Hannink J. Alam W. Durante 2007 Nitric oxide stimulates heme oxygenase-1 gene transcription via the Nrf2/ARE complex to promote vascular smooth muscle cell survival Cardiovasc. Res. 75 381 389
60. M. D. Maines 1988 Heme oxygenase: function, multiplicity, regulatory mechanisms, and clinical applications FASEB J. 2 2557 2568
61. M. D. Maines 1997 The heme oxygenase system: a regulator of second messenger gases Annu. Rev. Pharmacol. Toxicol. 37 517 554
62. R. J. Mallis J. E. Buss J. A. Thomas 2001 Oxidative modification of H-ras: S-thiolation and S-nitrosylation of reactive cysteines Biochem. J. 355 145 153
63. G. E. Mann D. J. Rowlands F. Y. Li P. de Winter R. C. Siow 2007 Activation of endothelial nitric oxide synthase by dietary isoflavones: role of NO in Nrf2-mediated antioxidant gene expression Cardiovasc. Res. 75 261 274
64. S. K. Manna M. T. Kuo B. B. Aggarwal 1999 Overexpression of gamma-glutamylcysteine synthetase suppresses tumor necrosis factor-induced apoptosis and activation of nuclear transcription factor-kappa B and activator protein-1 Oncogene 18 4371 4382
65. J. B. Mannick A. Hausladen L. Liu D. T. Hess M. Zeng Q. X. Miao L. S. Kane A. J. Gow J. S. Stamler 1999 Fas-induced caspase denitrosylation Science 284 651 654
66. S. Mariotto M. Menegazzi H. Suzuki 2004 Biochemical aspects of nitric oxide Curr. Pharm. Des. 10 1627 1645
67. U. K. Messmer D. M. Reimer J. C. Reed B. Brune 1996 Nitric oxide induced poly(ADP-ribose) polymerase cleavage in RAW 264.7 macrophage apoptosis is blocked by Bcl-2 FEBS Lett. 384 162 166
68. D. Moellering J. McAndrew R. P. Patel T. Cornwell T. Lincoln X. Cao J. L. Messina H. J. Forman H. Jo V. M. Darley-Usmar 1998 Nitric oxide-dependent induction of glutathione synthesis through increased expression of gamma-glutamylcysteine synthetase Arch. Biochem. Biophys. 358 74 82
69. S. Moncada R. M. Palmer E. A. Higgs 1991 Nitric oxide: physiology, pathophysiology, and pharmacology Pharmacol. Rev. 43 109 142
70. R. Moriya T. Uehara Y. Nomura 2000 Mechanism of nitric oxide-induced apoptosis in human neuroblastoma SH-SY5Y cells FEBS Lett. 484 253 260
71. H. Motohashi M. Yamamoto 2004 Nrf2-Keap1 defines a physiologically important stress response mechanism Trends Mol. Med. 10 549 557
72. R. Motterlini A. Hidalgo I. Sammut K. A. Shah S. Mohammed K. Srai C. J. Green 1996 A precursor of the nitric oxide donor SIN-1 modulates the stress protein heme oxygenase-1 in rat liver Biochem. Biophys. Res. Commun. 225 167 172
73. R. T. Mulcahy H. H. Bailey J. J. Gipp 1995 Transfection of complementary DNAs for the heavy and light subunits of human gamma-glutamylcysteine synthetase results in an elevation of intracellular glutathione and resistance to melphalan Cancer Res. 55 4771 4775
74. M. P. Murphy 1999 Nitric oxide and cell death Biochim. Biophys. Acta 1411 401 414
75. P. Naughton M. Hoque C. J. Green R. Foresti R. Motterlini 2002 Interaction of heme with nitroxyl or nitric oxide amplifies heme oxygenase-1 induction: involvement of the transcription factor Nrf2 Cell. Mol. Biol. (Noisy-le-grand) 48 885 894
76. R. R. Nazarewicz W. J. Zenebe A. Parihar S. K. Larson E. Alidema J. Choi P. Ghafourifar 2007 Tamoxifen induces oxidative stress and mitochondrial apoptosis via stimulating mitochondrial nitric oxide synthase Cancer Res. 67 1282 1290
77. T. Nguyen P. J. Sherratt C. B. Pickett 2003 Regulatory mechanisms controlling gene expression mediated by the antioxidant response element Annu. Rev. Pharmacol. Toxicol. 43 233 260
78. I. T. Nizamutdinova J. H. Lee H. G. Seo K. C. Chang H. J. Kim 2009 NS398 protects cells from sodium nitroprusside-mediated cytotoxicity through enhancing HO-1 induction independent of COX-2 inhibition Arch. Pharm. Res. 32 99 107
79. L. Otterbein S. L. Sylvester A. M. Choi 1995 Hemoglobin provides protection against lethal endotoxemia in rats: the role of heme oxygenase-1 Am. J. Respir. Cell Mol. Biol. 13 595 601
80. L. E. Otterbein A. M. Choi 2000 Heme oxygenase: colors of defense against cellular stress Am. J. Physiol. Lung. Cell. Mol. Physiol. 279 L1029 1037
81. P. Pacher J. S. Beckman L. Liaudet 2007 Nitric oxide and peroxynitrite in health and disease Physiol. Rev. 87 315 424
82. M. A. Packer M. P. Murphy 1995 Peroxynitrite formed by simultaneous nitric oxide and superoxide generation causes cyclosporin-A-sensitive mitochondrial calcium efflux and depolarisation Eur. J. Biochem. 234 231 239
83. H. S. Park S. H. Huh M. S. Kim S. H. Lee E. J. Choi 2000 Nitric oxide negatively regulates c-Jun N-terminal kinase/stress-activated protein kinase by means of S-nitrosylation Proc. Natl. Acad. Sci. U S A 97 14382 14387
84. Y. S. Park N. Fujiwara Y. H. Koh Y. Miyamoto K. Suzuki K. Honke N. Taniguchi 2002 Induction of thioredoxin reductase gene expression by peroxynitrite in human umbilical vein endothelial cells Biol. Chem. 383 683 691
85. C. A. Piantadosi 2008 Carbon monoxide, reactive oxygen signaling, and oxidative stress Free Radic. Biol. Med. 45 562 569
86. I. Rahman 2000 Regulation of nuclear factor-kappa B, activator protein-1, and glutathione levels by tumor necrosis factor-alpha and dexamethasone in alveolar epithelial cells Biochem. Pharmacol. 60 1041 1049
87. C. D. Reiter R. J. Teng J. S. Beckman 2000 Superoxide reacts with nitric oxide to nitrate tyrosine at physiological pH via peroxynitrite J. Biol. Chem. 275 32460 32466
88. N. L. Reynaert K. Ckless S. H. Korn N. Vos A. S. Guala E. F. Wouters A. van der Vliet Y. M. Janssen-Heininger 2004 Nitric oxide represses inhibitory kappaB kinase through S-nitrosylation Proc. Natl. Acad. Sci. U S A 101 8945 8950
89. L. A. Ridnour J. E. Sim J. Choi D. A. Dickinson H. J. Forman I. M. Ahmad M. C. Coleman C. R. Hunt P. C. Goswami D. R. Spitz 2005 Nitric oxide-induced resistance to hydrogen peroxide stress is a glutamate cysteine ligase activity-dependent process Free Radic. Biol. Med. 38 1361 1371
90. J. S. Stamler 1994 Redox signaling: nitrosylation and related target interactions of nitric oxide Cell 78 931 936
91. R. Stocker Y. Yamamoto A. F. McDonagh A. N. Glazer B. N. Ames 1987 Bilirubin is an antioxidant of possible physiological importance Science 235 1043 1046
92. D. J. Stuehr 1999 Mammalian nitric oxide synthases Biochim. Biophys. Acta. 1411 217 230
93. Y. J. Surh J. K. Kundu H. K. Na 2008 Nrf2 as a master redox switch in turning on the cellular signaling involved in the induction of cytoprotective genes by some chemopreventive phytochemicals Planta Med. 74 1526 1539
94. C. Szabo H. Ischiropoulos R. Radi 2007 Peroxynitrite: biochemistry, pathophysiology and development of therapeutics Nat. Rev. Drug Discov. 6 662 680
95. D. M. Townsend K. D. Tew H. Tapiero 2003 The importance of glutathione in human disease Biomed. Pharmacother. 57 145 155
96. G. F. Vile S. Basu-Modak C. Waltner R. M. Tyrrell 1994 Heme oxygenase 1 mediates an adaptive response to oxidative stress in human skin fibroblasts Proc. Natl. Acad. Sci. U S A 91 2607 2610
97. R. P. Webster S. Macha D. Brockman L. Myatt 2006 Peroxynitrite treatment in vitro disables catalytic activity of recombinant p38 MAPK Proteomics 6 4838 4844
98. B. Wegiel B. Y. Chin L. E. Otterbein 2008 Inhale to survive, cycle or die? Carbon monoxide and cellular proliferation Cell Cycle 7 1379 1384
99. D. Willis A. R. Moore R. Frederick D. A. Willoughby 1996 Heme oxygenase: a novel target for the modulation of the inflammatory response Nat. Med. 2 87 90
100. D. A. Wink I. Hanbauer M. C. Krishna W. DeGraff J. Gamson J. B. Mitchell 1993 Nitric oxide protects against cellular damage and cytotoxicity from reactive oxygen species Proc. Natl. Acad. Sci. U S A 90 9813 9817
101. G. Wu Y. Z. Fang S. Yang J. R. Lupton N. D. Turner 2004 Glutathione metabolism and its implications for health J. Nutr. 134 489 492
102. H. Zhu K. Itoh M. Yamamoto J. L. Zweier Y. Li 2005 Role of Nrf2 signaling in regulation of antioxidants and phase 2 enzymes in cardiac fibroblasts: protection against reactive oxygen and nitrogen species-induced cell injury FEBS Lett. 579 3029 3036
103. B. Zingarelli M. O'Connor H. Wong A. L. Salzman C. Szabo 1996 Peroxynitrite-mediated DNA strand breakage activates poly-adenosine diphosphate ribosyl synthetase and causes cellular energy depletion in macrophages stimulated with bacterial lipopolysaccharide J. Immunol. 156 350 358