Nitric oxide activates an Nrf2/sulfiredoxin antioxidant pathway in macrophages

Free Radical Biology and Medicine

Volumn 51, Issue 1, 2011, Pages 107-114

  Abbas, Kahina ^a   Breton, Jacques ^a   Planson, Anne Gaelle ^b   Bouton, Cécile ^a   Bignon, Jérome ^a   Seguin, Cendrine ^a   Riquier, Sylvie ^a   Toledano, Michel B ^b   Drapier, Jean Claude ^a  

^a INSTITUT DE CHIMIE DES SUBSTANCES NATURELLES   (France)

^b SERVICE DE CHIMIE BIOORGANIQUE ET DE MARQUAGE   (France)

Author keywords

Free radicals; Macrophage; Nitric oxide; Oxidative stress; Peroxiredoxin; Redox signaling; Sulfiredoxin

Indexed keywords

HYDROGEN PEROXIDE; NITRIC OXIDE; OXIDOREDUCTASE; REACTIVE OXYGEN METABOLITE; SULFIREDOXIN; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; HOMEOSTASIS; INNATE IMMUNITY; MACROPHAGE; MOUSE; NONHUMAN; OXIDATION; OXIDATION REDUCTION POTENTIAL; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; ANTIOXIDANTS; CELLS, CULTURED; HYDROGEN PEROXIDE; IMMUNITY, INNATE; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NF-E2-RELATED FACTOR 2; NITRIC OXIDE; OXIDATION-REDUCTION; OXIDATIVE STRESS; OXIDOREDUCTASES ACTING ON SULFUR GROUP DONORS; POLYMERASE CHAIN REACTION; REACTIVE OXYGEN SPECIES;

EUKARYOTA;

EID: 79957963156     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2011.03.039     Document Type: Article

References (76)

1. L.B. Poole, and K.J. Nelson Discovering mechanisms of signaling-mediated cysteine oxidation Curr. Opin. Chem. Biol. 12 2008 18 24
2. S.G. Rhee, S.W. Kang, W. Jeong, T.S. Chang, K.S. Yang, and H.A. Woo Intracellular messenger function of hydrogen peroxide and its regulation by peroxiredoxins Curr. Opin. Cell Biol. 17 2005 183 189 (Pubitemid 40380942)
3. L. Flohe, and J.R. Harris History of the peroxiredoxins and topical perspectives Subcell. Biochem. 44 2007 1 25
4. V.L. Kinnula, S. Lehtonen, R. Sormunen, R. Kaarteenaho-Wiik, S.W. Kang, S.G. Rhee, and Y. Soini Overexpression of peroxiredoxins I, II, III, V, and VI in malignant mesothelioma J. Pathol. 196 2002 316 323 (Pubitemid 34189421)
5. P. Karihtala, A. Mantyniemi, S.W. Kang, V.L. Kinnula, and Y. Soini Peroxiredoxins in breast carcinoma Clin. Cancer Res. 9 2003 3418 3424 (Pubitemid 37082738)
6. K. Krapfenbauer, E. Engidawork, N. Cairns, M. Fountoulakis, and G. Lubec Aberrant expression of peroxiredoxin subtypes in neurodegenerative disorders Brain Res. 967 2003 152 160 (Pubitemid 36324297)
7. S. Immenschuh, and E. Baumgart-Vogt Peroxiredoxins, oxidative stress, and cell proliferation Antioxid. Redox Signal. 7 2005 768 777 (Pubitemid 40563217)
8. K. Abbas, J. Breton, C.R. Picot, V. Quesniaux, C. Bouton, and J.C. Drapier Signaling events leading to peroxiredoxin 5 up-regulation in immunostimulated macrophages Free Radic. Biol. Med. 47 2009 794 802
9. M. Aran, D.S. Ferrero, E. Pagano, and R.A. Wolosiuk Typical 2-Cys peroxiredoxins-modulation by covalent transformations and noncovalent interactions FEBS J. 276 2009 2478 2493
10. 2, and protein chaperones. Antioxid. Redox Signaling March 2011 [Electronic publication ahead of print].
11. M. Chevallet, E. Wagner, S. Luche, A. van Dorsselaer, E. Leize-Wagner, and T. Rabilloud Regeneration of peroxiredoxins during recovery after oxidative stress: only some overoxidized peroxiredoxins can be reduced during recovery after oxidative stress J. Biol. Chem. 278 2003 37146 37153 (Pubitemid 37175229)
12. H.A. Woo, W. Jeong, T.S. Chang, K.J. Park, S.J. Park, J.S. Yang, and S.G. Rhee Reduction of cysteine sulfinic acid by sulfiredoxin is specific to 2-cys peroxiredoxins J. Biol. Chem. 280 2005 3125 3128 (Pubitemid 40223772)
13. B. Biteau, J. Labarre, and M.B. Toledano ATP-dependent reduction of cysteine-sulphinic acid by S. cerevisiae sulphiredoxin Nature 425 2003 980 984 (Pubitemid 37376931)
14. T.S. Chang, W. Jeong, H.A. Woo, S.M. Lee, S. Park, and S.G. Rhee Characterization of mammalian sulfiredoxin and its reactivation of hyperoxidized peroxiredoxin through reduction of cysteine sulfinic acid in the active site to cysteine J. Biol. Chem. 279 2004 50994 51001 (Pubitemid 40017840)
15. W. Jeong, S.J. Park, T.S. Chang, D.Y. Lee, and S.G. Rhee Molecular mechanism of the reduction of cysteine sulfinic acid of peroxiredoxin to cysteine by mammalian sulfiredoxin J. Biol. Chem. 281 2006 14400 14407 (Pubitemid 43848370)
16. A.V. Budanov, A.A. Sablina, E. Feinstein, E.V. Koonin, and P.M. Chumakov Regeneration of peroxiredoxins by p53-regulated sestrins, homologs of bacterial AhpD Science 304 2004 596 600 (Pubitemid 38541920)
17. H.A. Woo, S.H. Bae, S. Park, and S.G. Rhee Sestrin 2 is not a reductase for cysteine sulfinic acid of peroxiredoxins Antioxid. Redox Signal. 11 2009 739 745
18. S. Essler, N. Dehne, and B. Brune Role of sestrin 2 in peroxide signaling in macrophages FEBS Lett. 583 2009 3531 3535
19. T.J. Jonsson, and W.T. Lowther The peroxiredoxin repair proteins Subcell. Biochem. 44 2007 115 141
20. S.G. Rhee, W. Jeong, T.S. Chang, and H.A. Woo Sulfiredoxin, the cysteine sulfinic acid reductase specific to 2-Cys peroxiredoxin: its discovery, mechanism of action, and biological significance Kidney Int. Suppl. 2007 S3 S8
21. Y.H. Noh, J.Y. Baek, W. Jeong, S.G. Rhee, and T.S. Chang Sulfiredoxin translocation into mitochondria plays a crucial role in reducing hyperoxidized peroxiredoxin III J. Biol. Chem. 284 2009 8470 8477
22. K. Lei, D.M. Townsend, and K.D. Tew Protein cysteine sulfinic acid reductase (sulfiredoxin) as a regulator of cell proliferation and drug response Oncogene 27 2008 4877 4887
23. Q. Wei, H. Jiang, C.P. Matthews, and N.H. Colburn Sulfiredoxin is an AP-1 target gene that is required for transformation and shows elevated expression in human skin malignancies Proc. Natl. Acad. Sci. U. S. A. 105 2008 19738 19743
24. V.J. Findlay, D.M. Townsend, T.E. Morris, J.P. Fraser, L. He, and K.D. Tew A novel role for human sulfiredoxin in the reversal of glutathionylation Cancer Res. 66 2006 6800 6806 (Pubitemid 44085640)
25. J.W. Park, J.J. Mieyal, S.G. Rhee, and P.B. Chock Deglutathionylation of 2-cys peroxiredoxin is specifically catalyzed by sulfiredoxin J. Biol. Chem. 284 2009 23364 23374
26. Mazur, W.; Lindholm, P.; Vuorinen, K.; Myllarniemi, M.; Salmenkivi, K.; Kinnula, V. L. Cell-specific elevation of NRF2 and sulfiredoxin-1 as markers of oxidative stress in the lungs of idiopathic pulmonary fibrosis and non-specific interstitial pneumonia. APMIS 118:703-712; 2010.
27. M.K. Kwak, N. Wakabayashi, K. Itoh, H. Motohashi, M. Yamamoto, and T.W. Kensler Modulation of gene expression by cancer chemopreventive dithiolethiones through the Keap1-Nrf2 pathway: identification of novel gene clusters for cell survival J. Biol. Chem. 278 2003 8135 8145 (Pubitemid 36800555)
28. S.H. Bae, H.A. Woo, S.H. Sung, H.E. Lee, S.K. Lee, I.S. Kil, and S.G. Rhee Induction of sulfiredoxin via an Nrf2-dependent pathway and hyperoxidation of peroxiredoxin III in the lungs of mice exposed to hyperoxia Antioxid. Redox Signal. 11 2009 937 948
29. F.X. Soriano, F. Leveille, S. Papadia, L.G. Higgins, J. Varley, P. Baxter, J.D. Hayes, and G.E. Hardingham Induction of sulfiredoxin expression and reduction of peroxiredoxin hyperoxidation by the neuroprotective Nrf2 activator 3 H-1,2-dithiole-3-thione J. Neurochem. 107 2008 533 543
30. A. Singh, G. Ling, A.N. Suhasini, P. Zhang, M. Yamamoto, A. Navas-Acien, G. Cosgrove, R.M. Tuder, T.W. Kensler, W.H. Watson, and S. Biswal Nrf2-dependent sulfiredoxin-1 expression protects against cigarette smoke-induced oxidative stress in lungs Free Radic. Biol. Med. 46 2009 376 386
31. D.A. Glauser, T. Brun, B.R. Gauthier, and W. Schlegel Transcriptional response of pancreatic beta cells to metabolic stimulation: large scale identification of immediate-early and secondary response genes BMC Mol. Biol. 8 2007 54
32. A. Diet, K. Abbas, C. Bouton, B. Guillon, F. Tomasello, S. Fourquet, M.B. Toledano, and J.C. Drapier Regulation of peroxiredoxins by nitric oxide in immunostimulated macrophages J. Biol. Chem. 282 2007 36199 36205
33. K. Itoh, T. Chiba, S. Takahashi, T. Ishii, K. Igarashi, Y. Katoh, T. Oyake, N. Hayashi, K. Satoh, I. Hatayama, M. Yamamoto, and Y. Nabeshima An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements Biochem. Biophys. Res. Commun. 236 1997 313 322 (Pubitemid 27373291)
34. J.D. MacMicking, R.J. North, R. LaCourse, J.S. Mudgett, S.K. Shah, and C.F. Nathan Identification of nitric oxide synthase as a protective locus against tuberculosis Proc. Natl. Acad. Sci. U. S. A. 94 1997 5243 5248 (Pubitemid 27214768)
35. S. Pervin, R. Singh, E. Hernandez, G. Wu, and G. Chaudhuri Nitric oxide in physiologic concentrations targets the translational machinery to increase the proliferation of human breast cancer cells: involvement of mammalian target of rapamycin/eIF4E pathway Cancer Res. 67 2007 289 299 (Pubitemid 46142787)
36. D.D. Thomas, M.G. Espey, L.A. Ridnour, L.J. Hofseth, D. Mancardi, C.C. Harris, and D.A. Wink Hypoxic inducible factor 1alpha, extracellular signal-regulated kinase, and p53 are regulated by distinct threshold concentrations of nitric oxide Proc. Natl. Acad. Sci. U. S. A. 101 2004 8894 8899 (Pubitemid 38781582)
37. C.N. Hall, R.G. Keynes, and J. Garthwaite Cytochrome P450 oxidoreductase participates in nitric oxide consumption by rat brain Biochem. J. 419 2009 411 418
38. H. Ischiropoulos, L. Zhu, and J.S. Beckman Peroxynitrite formation from macrophage-derived nitric oxide Arch. Biochem. Biophys. 298 1992 446 451
39. C. Amatore, S. Arbault, C. Bouton, J.C. Drapier, H. Ghandour, and A.C. Koh Real-time amperometric analysis of reactive oxygen and nitrogen species released by single immunostimulated macrophages Chembiochem 9 2008 1472 1480
40. S.G. Rhee, H.Z. Chae, and K. Kim Peroxiredoxins: a historical overview and speculative preview of novel mechanisms and emerging concepts in cell signaling Free Radic. Biol. Med. 38 2005 1543 1552 (Pubitemid 40726061)
41. M. Dubuisson, D. Vander Stricht, A. Clippe, F. Etienne, T. Nauser, R. Kissner, W.H. Koppenol, J.F. Rees, and B. Knoops Human peroxiredoxin 5 is a peroxynitrite reductase FEBS Lett. 571 2004 161 165 (Pubitemid 38992941)
42. X. Yu, P.A. Egner, J. Wakabayashi, N. Wakabayashi, M. Yamamoto, and T.W. Kensler Nrf2-mediated induction of cytoprotective enzymes by 15-deoxy-Delta12,14-prostaglandin J2 is attenuated by alkenal/one oxidoreductase J. Biol. Chem. 281 2006 26245 26252 (Pubitemid 44401832)
43. M. Kobayashi, and M. Yamamoto Molecular mechanisms activating the Nrf2-Keap1 pathway of antioxidant gene regulation Antioxid. Redox Signal. 7 2005 385 394 (Pubitemid 40279806)
44. J.D. Hayes, and M. McMahon NRF2 and KEAP1 mutations: permanent activation of an adaptive response in cancer Trends Biochem. Sci. 34 2009 176 188
45. T.W. Kensler, N. Wakabayashi, and S. Biswal Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway Annu. Rev. Pharmacol. Toxicol. 47 2007 89 116
46. B.J. Buckley, Z.M. Marshall, and A.R. Whorton Nitric oxide stimulates Nrf2 nuclear translocation in vascular endothelium Biochem. Biophys. Res. Commun. 307 2003 973 979 (Pubitemid 36871668)
47. C.Q. Li, M.Y. Kim, L.C. Godoy, A. Thiantanawat, L.J. Trudel, and G.N. Wogan Nitric oxide activation of Keap1/Nrf2 signaling in human colon carcinoma cells Proc. Natl. Acad. Sci. U. S. A. 106 2009 14547 14551
48. J. Fang, T. Nakamura, D.H. Cho, Z. Gu, and S.A. Lipton S-nitrosylation of peroxiredoxin 2 promotes oxidative stress-induced neuronal cell death in Parkinson's disease Proc. Natl. Acad. Sci. U. S. A. 104 2007 18742 18747 (Pubitemid 350210767)
49. Fluorescence response of APF, HPF and H2DCFDA to various reactive oxygen species (ROS), Table 18.4. In: Johnson, I., Spence, M.T.Z., eds. Molecular Probes Handbook, A Guide to Fluorescent Probes and Labeling Technologies, 11th Edition, Life Technologies Corporation, Carlsbad, CA, 2010.
50. B.Z. Zhu, B. Kalyanaraman, and G.B. Jiang Molecular mechanism for metal-independent production of hydroxyl radicals by hydrogen peroxide and halogenated quinones Proc. Natl. Acad. Sci. U. S. A. 104 2007 17575 17578 (Pubitemid 350210876)
51. J. MacMicking, Q.W. Xie, and C. Nathan Nitric oxide and macrophage function Annu. Rev. Immunol. 15 1997 323 350 (Pubitemid 27169284)
52. H.J. Forman, and M. Torres Redox signaling in macrophages Mol. Aspects Med. 22 2001 189 216 (Pubitemid 33000522)
53. B.M. Babior Phagocytes and oxidative stress Am. J. Med. 109 2000 33 44 (Pubitemid 30608735)
54. H. Kim, Y. Jung, B.S. Shin, H. Song, S.H. Bae, S.G. Rhee, and W. Jeong Redox regulation of lipopolysaccharide-mediated sulfiredoxin induction which depends on both AP-1 and Nrf2 J. Biol. Chem. 285 2010 34419 34428
55. T. Akaike, Y. Noguchi, S. Ijiri, K. Setoguchi, M. Suga, Y.M. Zheng, B. Dietzschold, and H. Maeda Pathogenesis of influenza virus-induced pneumonia: involvement of both nitric oxide and oxygen radicals Proc. Natl. Acad. Sci. U. S. A. 93 1996 2448 2453 (Pubitemid 26104370)
56. S.G. Rhee, Y.S. Bae, S.R. Lee, and J. Kwon Hydrogen peroxide: a key messenger that modulates protein phosphorylation through cysteine oxidation Sci. STKE 2000 2000 PE1
57. Y. Li, Y. Jia, M. Pichavant, F. Loison, B. Sarraj, A. Kasorn, J. You, B.E. Robson, D.T. Umetsu, J.P. Mizgerd, K. Ye, and H.R. Luo Targeted deletion of tumor suppressor PTEN augments neutrophil function and enhances host defense in neutropenia-associated pneumonia Blood 113 2009 4930 4941
58. K.M. Heinonen, A. Bourdeau, K.M. Doody, and M.L. Tremblay Protein tyrosine phosphatases PTP-1B and TC-PTP play nonredundant roles in macrophage development and IFN-gamma signaling Proc. Natl. Acad. Sci. U. S. A. 106 2009 9368 9372
59. F.X. Soriano, P. Baxter, L.M. Murray, M.B. Sporn, T.H. Gillingwater, and G.E. Hardingham Transcriptional regulation of the AP-1 and Nrf2 target gene sulfiredoxin Mol. Cells 27 2009 279 282
60. S. Papadia, F.X. Soriano, F. Leveille, M.A. Martel, K.A. Dakin, H.H. Hansen, A. Kaindl, M. Sifringer, J. Fowler, V. Stefovska, G. McKenzie, M. Craigon, R. Corriveau, P. Ghazal, K. Horsburgh, B.A. Yankner, D.J. Wyllie, C. Ikonomidou, and G.E. Hardingham Synaptic NMDA receptor activity boosts intrinsic antioxidant defenses Nat. Neurosci. 11 2008 476 487 (Pubitemid 351441886)
61. N. Wakabayashi, A.T. Dinkova-Kostova, W.D. Holtzclaw, M.I. Kang, A. Kobayashi, M. Yamamoto, T.W. Kensler, and P. Talalay Protection against electrophile and oxidant stress by induction of the phase 2 response: fate of cysteines of the Keap1 sensor modified by inducers Proc. Natl. Acad. Sci. U. S. A. 101 2004 2040 2045 (Pubitemid 38229011)
62. D.D. Zhang Mechanistic studies of the Nrf2-Keap1 signaling pathway Drug Metab. Rev. 38 2006 769 789 (Pubitemid 44903268)
63. S. Dhakshinamoorthy, and A.G. Porter 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 2004 20096 20107 (Pubitemid 38623454)
64. 2 involves KEAP1 disulfide formation J. Biol. Chem. 285 2010 8463 8471
65. R.K. Thimmulappa, H. Lee, T. Rangasamy, S.P. Reddy, M. Yamamoto, T.W. Kensler, and S. Biswal Nrf2 is a critical regulator of the innate immune response and survival during experimental sepsis J. Clin. Invest. 116 2006 984 995
66. Nathan, C., Ding, A. Nonresolving inflammation. Cell 140:871-882; 2010.
67. A. Zunino, P. Degan, T. Vigo, and A. Abbondandolo Hydrogen peroxide: effects on DNA, chromosomes, cell cycle and apoptosis induction in Fanconi's anemia cell lines Mutagenesis 16 2001 283 288 (Pubitemid 32447763)
68. K.B. Beckman, and B.N. Ames The free radical theory of aging matures Physiol. Rev. 78 1998 547 581 (Pubitemid 28182903)
69. R.M. Lebovitz, H. Zhang, H. Vogel, J. Cartwright Jr., L. Dionne, N. Lu, S. Huang, and M.M. Matzuk Neurodegeneration, myocardial injury, and perinatal death in mitochondrial superoxide dismutase-deficient mice Proc. Natl. Acad. Sci. U. S. A. 93 1996 9782 9787 (Pubitemid 26296686)
70. Y. Yoshioka, T. Kitao, T. Kishino, A. Yamamuro, and S. Maeda Nitric oxide protects macrophages from hydrogen peroxide-induced apoptosis by inducing the formation of catalase J. Immunol. 176 2006 4675 4681
71. K. Takuma, P. Phuagphong, E. Lee, R. Enomoto, K. Mori, A. Baba, and T. Matsuda The nitric oxide donor NOC12 protects cultured astrocytes against apoptosis via a cGMP-dependent mechanism Jpn. J. Pharmacol. 89 2002 64 71 (Pubitemid 34618610)
72. D.A. Wink, I. Hanbauer, M.C. Krishna, W. DeGraff, J. Gamson, and J.B. Mitchell Nitric oxide protects against cellular damage and cytotoxicity from reactive oxygen species Proc. Natl. Acad. Sci. U. S. A. 90 1993 9813 9817 (Pubitemid 23328200)
73. A.C. Degnim, S.E. Morrow, J. Ku, H.A. Zar, and D.K. Nakayama Nitric oxide inhibits peroxide-mediated endothelial toxicity J. Surg. Res. 75 1998 127 134 (Pubitemid 28304317)
74. K. Hemmrich, C.V. Suschek, G. Lerzynski, and V. Kolb-Bachofen iNOS activity is essential for endothelial stress gene expression protecting against oxidative damage J. Appl. Physiol. 95 2003 1937 1946 (Pubitemid 37310378)
75. D.A. Wink, J.A. Cook, R. Pacelli, J. Liebmann, M.C. Krishna, and J.B. Mitchell Nitric oxide (NO) protects against cellular damage by reactive oxygen species Toxicol. Lett. 82-83 1995 221 226 (Pubitemid 26054708)
76. Planson, A.G., Palais, G., Abbas, K., Gerard, M., Couvelard, L., Delaunay, A., Baulande, S., Drapier, J.C., Toledano, M. Sulfiredoxin protects mice from lipopolysaccharide-induced endotoxic shock. Antioxid. Redox Signaling March 2011 [Electronic publication ahead of print].