Mitochondrial thiols in antioxidant protection and redox signaling: Distinct roles for glutathionylation and other thiol modifications

Antioxidants and Redox Signaling

Volumn 16, Issue 6, 2012, Pages 476-495

  Murphy, Michael P ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

2 OXOGLUTARIC ACID; ALDEHYDE; BACTERIAL ENZYME; CYSTEINE; DEHYDROASCORBIC ACID REDUCTASE; DICARBOXYLIC ACID; DITHIOL DERIVATIVE; ELECTROPHILE; EPOXIDE; GLUTAREDOXIN; GLUTATHIONE; GLUTATHIONE DISULFIDE; GLUTATHIONE PEROXIDASE 1; GLUTATHIONE TRANSFERASE; HYDROGEN PEROXIDE; HYDROPEROXIDE; ISOCITRATE DEHYDROGENASE; MALATE DEHYDROGENASE (DECARBOXYLATING); METHIONINE SULFOXIDE REDUCTASE; PEROXYNITRITE; PHOSPHOLIPID HYDROPEROXIDE GLUTATHIONE PEROXIDASE; QUINONE DERIVATIVE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; SULFENIC ACID DERIVATIVE; THIOCTIC ACID; THIOL; THIOREDOXIN;

ANTIOXIDANT ACTIVITY; BINDING AFFINITY; CAENORHABDITIS ELEGANS; CATALYSIS; CELL CULTURE; CONCENTRATION (PARAMETERS); CYTOSOL; DEGRADATION KINETICS; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ESCHERICHIA COLI; GENE SILENCING; GLUTATHIONE METABOLISM; GLUTATHIONYLATION; HOMOZYGOSITY; INTRACELLULAR SPACE; LYMPHOBLAST; MITOCHONDRIAL MEMBRANE; MOLECULAR WEIGHT; NITROSATION; NONHUMAN; NUCLEOPHILICITY; OLIGOMERIZATION; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PH; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; PROTEIN TARGETING; PROTEIN TRANSPORT; PROTEOMICS; REGENERATION; RESPIRATORY CHAIN; REVIEW; SIGNAL TRANSDUCTION; TRANSLATION REGULATION;

ANIMALS; ANTIOXIDANTS; GLUTATHIONE; HUMANS; MITOCHONDRIA; OXIDATION-REDUCTION; SIGNAL TRANSDUCTION; SULFHYDRYL COMPOUNDS;

EID: 84856729192     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2011.4289     Document Type: Review

References (225)

1. Alvarez B, Carballal S, Turell L, and Radi R. Formation and reactions of sulfenic acid in human serum albumin. Methods Enzymol 473: 117-136, 2010.
2. Arai M, Imai H, Koumura T, Yoshida M, Emoto K, Umeda M, Chiba N, and Nakagawa Y. Mitochondrial phospholipids hydroperoxide glutathione peroxidase plays a major role in preventing oxidative injury to cells. J Biol Chem 274: 4924-4933, 1999.
3. Aran M, Ferrero DS, Pagano E, and Wolosiuk RA. Typical 2-Cys peroxiredoxins-modulation by covalent transformations and noncovalent interactions. FEBS J 276: 2478-2493, 2009.
4. Arner ES and Holmgren A. Physiological functions of thioredoxin and thioredoxin reductase. Eur J Biochem 267: 6102-6109, 2000.
5. Bae SH, Woo HA, Sung SH, Lee HE, Lee SK, Kil IS, and Rhee SG. 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: 937-948, 2009.
6. Balaban RS, Nemoto S, and Finkel T. Mitochondria, oxidants, and aging. Cell 120: 483-495, 2005.
7. Barranco-Medina S, Lazaro JJ, and Dietz KJ. The oligomeric conformation of peroxiredoxins links redox state to function. FEBS Lett 583: 1809-1816, 2009.
8. Beer SM, Taylor ER, Brown SE, Dahm CC, Costa NJ, Runswick MJ, and Murphy MP. Glutaredoxin 2 catalyzes the reversible oxidation and glutathionylation of mitochondrial membrane thiol proteins: Implications for mitochondrial redox regulation and antioxidant defense. J Biol Chem 279: 47939-47951, 2004. (Pubitemid 39540945)
9. Beltran B, Orsi A, Clementi E, and Moncada S. Oxidative stress and S-nitrosylation of proteins in cells. Br J Pharmacol 129: 953-960, 2000. (Pubitemid 30142908)
10. Benhar M, Forrester MT, and Stamler JS. Protein denitrosylation: Enzymatic mechanisms and cellular functions. Nat Rev Mol Cell Biol 10: 721-732, 2009.
11. Berger F, Ramirez-Hernandez MH, and Ziegler M. The new life of a centenarian: Signalling functions of NAD(P). Trends Biochem Sci 29: 111-118, 2004. (Pubitemid 38314856)
12. Bizouarn T, Fjellstrom O, Meuller J, Axelsson M, Bergkvist A, Johansson C, Goran Karlsson B, and Rydstrom J. Proton translocating nicotinamide nucleotide transhydrogenase from E. coli. Mechanism of action deduced from its structural and catalytic properties. Biochim Biophys Acta 1457: 211-228, 2000. (Pubitemid 30201485)
13. Boivin B, Yang M, and Tonks NK. Targeting the reversibly oxidized protein tyrosine phosphatase superfamily. Sci Signal 3: pl2, 2010.
14. Bonini MG and Augusto O. Carbon dioxide stimulates the production of thiyl, sulfinyl, and disulfide radical anion from thiol oxidation by peroxynitrite. J Biol Chem 276: 9749-9754, 2001.
15. Brennan JP, Wait R, Begum S, Bell JR, Dunn MJ, and Eaton P. Detection and mapping of widespread intermolecular protein disulfide formation during cardiac oxidative stress using proteomics with diagonal electrophoresis. J Biol Chem 279: 41352-41360, 2004. (Pubitemid 39313574)
16. Brouwers O, Niessen PM, Ferreira I, Miyata T, Scheffer PG, Teerlink T, Schrauwen P, Brownlee M, Stehouwer CD, and Schalkwijk CG. Overexpression of glyoxalase-I reduces hyperglycemiainduced levels of advanced glycation end products and oxidative stress in diabetic rats. J Biol Chem 286: 1374-1380, 2011.
17. Burwell LS, Nadtochiy SM, Tompkins AJ, Young S, and Brookes PS. Direct evidence for S-nitrosation of mitochondrial complex I. Biochem J 394: 627-634, 2006.
18. Bushweller JH, Aslund F, Wuthrich K, and Holmgren A. Structural and functional characterization of the mutant Escherichia coli glutaredoxin (C14S) and its mixed disulfide with glutathione. Biochemistry 31: 9288-9293, 1992.
19. Cabiscol E and Levine RL. The phosphatase activity of carbonic anhydrase III is reversibly regulated by glutathiolation. Proc Natl Acad Sci U S A 93: 4170-4174, 1996. (Pubitemid 26146729)
20. Cabreiro F, Picot CR, Perichon M, Castel J, Friguet B, and Petropoulos I. Overexpression of mitochondrial methionine sulfoxide reductase B2 protects leukemia cells from oxidative stress-induced cell death and protein damage. J Biol Chem 283: 16673-16681, 2008.
21. Chance B, Sies H, and Boveris A. Hydroperoxide metabolism in mammalian organs. Physiol Rev 59: 527-605, 1979. (Pubitemid 9236599)
22. Chaplen FW, Fahl WE, and Cameron DC. Evidence of high levels of methylglyoxal in cultured Chinese hamster ovary cells. Proc Natl Acad Sci U S A 95: 5533-5538, 1998. (Pubitemid 28224129)
23. Charles RL, Schroder E, May G, Free P, Gaffney PR, Wait R, Begum S, Heads RJ, and Eaton P. Protein sulfenation as a redox sensor: proteomics studies using a novel biotinylated dimedone analogue. Mol Cell Proteomics 6: 1473-1484, 2007. (Pubitemid 47506161)
24. Chen J, Chen CL, Rawale S, Chen CA, Zweier JL, Kaumaya PT, and Chen YR. Peptide-based antibodies against glutathione- binding domains suppress superoxide production mediated by mitochondrial complex I. J Biol Chem 285: 3168-3180, 2010.
25. Chen L, Na R, Gu M, Salmon AB, Liu Y, Liang H, Qi W, Van Remmen H, Richardson A, and Ran Q. Reduction of mitochondrial H2O2 by overexpressing peroxiredoxin 3 improves glucose tolerance in mice. Aging Cell 7: 866-878, 2008. (Pubitemid 352749440)
26. Chen YR, Chen CL, Pfeiffer DR, and Zweier JL. Mitochondrial complex II in the post-ischemic heart: oxidativeinjury and the role of protein S-glutathionylation. J Biol Chem 282: 32640-32654, 2007. (Pubitemid 350159288)
27. Chen Z, Putt DA, and Lash LH. Enrichment and functional reconstitution of glutathione transport activity from rabbit kidney mitochondria: further evidence for the role of the dicarboxylate and 2-oxoglutarate carriers in mitochondrial glutathione transport. Arch Biochem Biophys 373: 193-202, 2000. (Pubitemid 30046504)
28. Cho CS, Lee S, Lee GT, Woo HA, Choi EJ, and Rhee SG. Irreversible inactivation of glutathione peroxidase 1 and reversible inactivation of peroxiredoxin II by H2O2 in red blood cells. Antioxid Redox Signal 12: 1235-1246, 2010.
29. Chouchani ET, Hurd TR, Nadtochiy SM, Brookes PS, Fearnley IM, Lilley KS, Smith RA, and Murphy MP. Identification of S-nitrosated mitochondrial proteins by Snitrosothiol difference in gel electrophoresis (SNO-DIGE): Implications for the regulation of mitochondrial function by reversible S-nitrosation. Biochem J 430: 49-59, 2010.
30. Conrad M. Transgenic mouse models for the vital selenoenzymes cytosolic thioredoxin reductase, mitochondrial thioredoxin reductase and glutathione peroxidase 4. Biochim Biophys Acta 1790: 1575-1585, 2009.
31. Cordell PA, Futers TS, Grant PJ, and Pease RJ. The human hydroxyacylglutathione hydrolase (HAGH) gene encodes both cytosolic and mitochondrial forms of glyoxalase II. J Biol Chem 279: 28653-28661, 2004. (Pubitemid 38900148)
32. 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)
33. Cotgreave IA and Gerdes RG. Recent trends in glutathione biochemistry-glutathione-protein interactions: A molecular link between oxidative stress and cell proliferation? Biochem Biophys Res Commun 242: 1-9, 1998. (Pubitemid 28412367)
34. Cox AG, Peskin AV, Paton LN, Winterbourn CC, and Hampton MB. Redox potential and peroxide reactivity of human peroxiredoxin 3. Biochemistry 48: 6495-6501, 2009.
35. Cox AG, Pullar JM, Hughes G, Ledgerwood EC, and Hampton MB. Oxidation of mitochondrial peroxiredoxin 3 during the initiation of receptor-mediated apoptosis. Free Radic Biol Med 44: 1001-1009, 2008.
36. Cox AG, Winterbourn CC, and Hampton MB. Mitochondrial peroxiredoxin involvement in antioxidant defence and redox signalling. Biochem J 425: 313-325, 2010.
37. Craig CL and Weber RS. Selection costs of amino acid substitutions in ColE1 and ColIa gene clusters harbored by Escherichia coli. Mol Biol Evol 15: 774-776, 1998.
38. D'Autreaux B and Toledano MB. ROS as signalling molecules: Mechanisms that generate specificity in ROS homeostasis. Nat Rev Mol Cell Biol 8: 813-824, 2007. (Pubitemid 47462134)
39. Dahm CC, Moore K, and Murphy MP. Persistent Snitrosation of complex I and other mitochondrial membrane proteins by S-nitrosothiols but not nitric oxide or peroxynitrite: Implications for the interaction of nitric oxide with mitochondria. J Biol Chem 281: 10056-10065, 2006. (Pubitemid 43864540)
40. Dalle-Donne I, Milzani A, Gagliano N, Colombo R, Giustarini D, and Rossi R. Molecular mechanisms and potential clinical significance of S-glutathionylation. Antioxid Redox Signal 10: 445-473, 2008.
41. Dalle-Donne I, Rossi R, Colombo G, Giustarini D, and Milzani A. Protein S-glutathionylation: A regulatory device from bacteria to humans. Trends Biochem Sci 34: 85-96, 2009.
42. Daum G. Lipids of mitochondria. Biochim Biophys Acta 822: 1-42, 1985. (Pubitemid 15042024)
43. de Haan JB, Bladier C, Griffiths P, Kelner M, O'Shea RD, Cheung NS, Bronson RT, Silvestro MJ, Wild S, Zheng SS, Beart PM, Hertzog PJ, and Kola I. Mice with a homozygous null mutation for the most abundant glutathione peroxidase, Gpx1, show increased susceptibility to the oxidative stress-inducing agents paraquat and hydrogen peroxide. J Biol Chem 273: 22528-22536, 1998. (Pubitemid 28399820)
44. De Simoni S, Goemaere J, and Knoops B. Silencing of peroxiredoxin 3 and peroxiredoxin 5 reveals the role of mitochondrial peroxiredoxins in the protection of human neuroblastoma SH-SY5Y cells toward MPP+. Neurosci Lett 433: 219-224, 2008.
45. Delaunay A, Pflieger D, Barrault MB, Vinh J, and Toledano MB. A thiol peroxidase is an H2O2 receptor and redoxtransducer in gene activation. Cell 111: 471-481, 2002. (Pubitemid 35356554)
46. Di Simplicio P, Cacace MG, Lusini L, Giannerini F, Giustarini D, and Rossi R. Role of protein -SH groups in redox homeostasis-the erythrocyte as a model system. Arch Biochem Biophys 355: 145-152, 1998. (Pubitemid 28364362)
47. Doorn JA and Petersen DR. Covalent adduction of nucleophilic amino acids by 4-hydroxynonenal and 4-oxononenal. Chem Biol Interact 143-144: 93-100, 2003. (Pubitemid 36246435)
48. Doulias PT, Greene JL, Greco TM, Tenopoulou M, Seeholzer SH, Dunbrack RL, and Ischiropoulos H. Structural profiling of endogenous S-nitrosocysteine residues reveals unique features that accommodate diverse mechanisms for protein S-nitrosylation. Proc Natl Acad Sci U S A 107: 16958-16963, 2010.
49. Droge W. Free radicals in the physiological control of cell function. Physiol Rev 82: 47-95, 2002. (Pubitemid 34654215)
50. Duchen MR. Mitochondria in health and disease: perspectives on a new mitochondrial biology. Mol Asp Med 25: 365-451, 2004. (Pubitemid 39070333)
51. Eaton P. Protein thiol oxidation in health and disease: Techniques for measuring disulfides and related modifications in complex protein mixtures. Free Radic Biol Med 40: 1889-1899, 2006. (Pubitemid 43744434)
52. Enoksson M, Fernandes AP, Prast S, Lillig CH, Holmgren A, and Orrenius S. Overexpression of glutaredoxin 2 attenuates apoptosis by preventing cytochrome c release. Biochem Biophys Res Commun 327: 774-779, 2005. (Pubitemid 40092816)
53. Esposito LA, Kokoszka JE, Waymire KG, Cottrell B, Mac- Gregor GR, and Wallace DC. Mitochondrial oxidative stress in mice lacking the glutathione peroxidase-1 gene. Free Radic Biol Med 28: 754-766, 2000. (Pubitemid 30171289)
54. Fernandez-Checa JC, Kaplowitz N, Garcia-Ruiz C, and Colell A. Mitochondrial glutathione: Importance and transport. Semin Liver Dis 18: 389-401, 1998. (Pubitemid 29011042)
55. Finkel T. Opinion: Radical medicine: Treating ageing to cure disease. Nat Rev Mol Cell Biol 6: 971-976, 2005. (Pubitemid 41778716)
56. Ford E, Hughes MN, and Wardman P. Kinetics of the reactions of nitrogen dioxide with glutathione, cysteine, and uric acid at physiological pH. Free Radic Biol Med 32: 1314-1323, 2002. (Pubitemid 34607635)
57. Fourquet S, Huang ME, D'Autreaux B, and Toledano MB. The dual functions of thiol-based peroxidases in H2O2 scavenging and signaling. Antioxid Redox Signal 10: 1565-1575, 2008. (Pubitemid 351931930)
58. Fratelli M, Demol H, Puype M, Casagrande S, Eberini I, Salmona M, Bonetto V, Mengozzi M, Duffieux F, Miclet E, Bachi A, Vandekerckhove J, Gianazza E, and Ghezzi P. Identification by redox proteomics of glutathionylated proteins in oxidatively stressed human T lymphocytes. Proc Natl Acad Sci U S A 99: 3505-3510, 2002. (Pubitemid 34252138)
59. Fratelli M, Demol H, Puype M, Casagrande S, Villa P, Eberini I, Vandekerckhove J, Gianazza E, and Ghezzi P. Identification of proteins undergoing glutathionylation in oxidatively stressed hepatocytes and hepatoma cells. Proteomics 3: 1154-1161, 2003. (Pubitemid 36929537)
60. Fratelli M, Gianazza E, and Ghezzi P. Redox proteomics: Identification and functional role of glutathionylated proteins. Expert Rev Proteomics 1: 365-376, 2004.
61. Gallogly MM, Starke DW, Leonberg AK, Ospina SM, and Mieyal JJ. Kinetic and mechanistic characterization and versatile catalytic properties of mammalian glutaredoxin 2: Implications for intracellular roles. Biochemistry 47: 11144-11157, 2008.
62. Gardner JL and Gallagher EP. Development of a peptide antibody specific to human glutathione S-transferase alpha 4-4 (hGSTA4-4) reveals preferential localization in human liver mitochondria. Arch Biochem Biophys 390: 19-27, 2001. (Pubitemid 32496270)
63. Gasdaska PY, Berggren MM, Berry MJ, and Powis G. Cloning, sequencing and functional expression of a novel human thioredoxin reductase. FEBS Lett 442: 105-111, 1999. (Pubitemid 29065388)
64. Gilbert HF. Redox control of enzyme activities by thiol/ disulfide exchange. Methods Enzymol 107: 330-351, 1984. (Pubitemid 14053814)
65. Gilbert HF. Molecular and cellular aspects of thiol-disulfide exchange. Adv Enzymol Relat Areas Mol Biol 63: 69-172, 1990.
66. Gilbert HF. Thiol/disulfide exchange equilibria and disulfide bond stability. Methods Enzymol 251: 8-28, 1995.
67. Gitler C, Zarmi B, and Kalef E. General methods to identify and enrich vicinal thiol proteins present in intact cells in the oxidised disulfide state. Anal Biochem 252: 48-55, 1997. (Pubitemid 27408691)
68. Gladyshev VN, Liu A, Novoselov SV, Krysan K, Sun QA, Kryukov VM, Kryukov GV, and Lou MF. Identification and characterization of a new mammalian glutaredoxin (thioltransferase), Grx2. J Biol Chem 276: 30374-30380, 2001.
69. Go YM and Jones DP. Redox compartmentalization in eukaryotic cells. Biochim Biophys Acta 1780: 1273-1290, 2008.
70. Godeas C, Sandri G, and Panfili E. Distribution of phospholipids hydroperoxide glutathione peroxidase (PHGPx) in rat testis mitochondria. Biochim Biophys Acta 1191: 147-150, 1994. (Pubitemid 24133538)
71. Goto S, Kawakatsu M, Izumi Si, Urata Y, Kageyama K, Ihara Y, Koji T, and Kondo T. Glutathione S-transferase p localizes in mitochondria and protects against oxidative stress. Free Radic Biol Med 46: 1392-1403, 2009.
72. Gravina SA and Mieyal JJ. Thioltransferase is a specific glutathionyl mixed disulfide oxidoreductase. Biochemistry 32: 3368-3376, 1993. (Pubitemid 23126904)
73. Griffith OW and Meister A. Origin and turnover of mitochondrial glutathione. Proc Natl Acad Sci U S A 82: 4668-4672, 1985. (Pubitemid 16239624)
74. Hanschmann EM, Lönn ME, Schü tte LD, Funke M, Godoy JR, Eitner S, Hudemann C, and Lillig CH. Both thioredoxin 2 and glutaredoxin 2 contribute to the reduction of the mitochondrial 2-Cys peroxiredoxin Prx3. J Biol Chem 285: 40699-40705, 2010.
75. Hansen RE, Roth D, and Winther JR. Quantifying the global cellular thiol-disulfide status. Proc Natl Acad Sci U S A 106: 422-427, 2009.
76. Hashemy SI, Johansson C, Berndt C, Lillig CH, and Holmgren A. Oxidation and S-nitrosylation of cysteines in human cytosolic and mitochondrial glutaredoxins: Effects on structure and activity. J Biol Chem 282: 14428-14436, 2007. (Pubitemid 47100442)
77. Hayes JD, Flanagan JU, and Jowsey IR. Glutathione transferases. Annu Rev Pharmacol Toxicol 45: 51-88, 2005. (Pubitemid 40261798)
78. Hayes JD, McMahon M, Chowdhry S, and Dinkova- Kostova AT. Cancer chemoprevention mechanisms mediated through the Keap1-NRF2 pathway. Antioxid Redox Signal 13: 1713-1748, 2010.
79. Herrmann JM and Riemer J. Oxidation and reduction of cysteines in the intermembrane space of mitochondria: Multiple facets of redox control. Antioxid Redox Signal 13: 1323-1326, 2010.
80. Hess DT, Matsumoto A, Nudelman R, and Stamler JS. Snitrosylation: Spectrum and specificity. Nat Cell Biol 3: E46-E49, 2001.
81. Ho YS, Magnenat JL, Bronson RT, Cao J, Gargano M, Sugawara M, and Funk CD. Mice deficient in cellular glutathione peroxidase develop normally and show no increased sensitivity to hyperoxia. J Biol Chem 272: 16644-16651, 1997. (Pubitemid 27276497)
82. Hogg N. The biochemistry and physiology of Snitrosothiols. Annu Rev Pharmacol Toxicol 42: 585-600, 2002.
83. Hogg PJ. Disulfide bonds as switches for protein function. Trends Biochem Sci 28: 210-214, 2003. (Pubitemid 36507160)
84. Holmgren A. Thioredoxin. Annu Rev Biochem 54: 237-271, 1985. (Pubitemid 15073647)
85. Hou Y, Guo Z, Li J, and Wang PG. Seleno compounds and glutathione peroxidase catalyzed decomposition of S-nitrosothiols. Biochem Biophys Res Commun 228: 88-93, 1996. (Pubitemid 26390634)
86. Hurd TR, Costa NJ, Dahm CC, Beer SM, Brown SE, Filipovska A, and Murphy MP. Glutathionylation of mitochondrial proteins. Antioxid Redox Signal 7: 999-1010, 2005. (Pubitemid 40967150)
87. Hurd TR, Filipovska A, Costa NJ, Dahm CC, and Murphy MP. Disulphide formation on mitochondrial protein thiols. Biochem Soc Trans 33: 1390-1393, 2005. (Pubitemid 41779695)
88. Hurd TR, Prime TA, Harbour ME, Lilley KS, and Murphy MP. Detection of reactive oxygen species-sensitive thiol proteins by redox difference gel electrophoresis: Implications for mitochondrial redox signaling. J Biol Chem 282: 22040-22051, 2007. (Pubitemid 47195755)
89. Hurd TR, Requejo R, Filipovska A, Brown S, Prime TA, Robinson AJ, Fearnley IM, and Murphy MP. Complex I within oxidatively stressed bovine heart mitochondria is glutathionylated on Cys-531 and Cys-704 of the 75-kDa subunit: potential role of CYS residues in decreasing oxidative damage. J Biol Chem 283: 24801-24815, 2008.
90. Imai H and Nakagawa Y. Biological significance of phospholipids hydroperoxide glutathione peroxidase (PHGPx, GPx4) in mammalian cells. Free Radic Biol Med 34: 145-169, 2003. (Pubitemid 36084320)
91. Jacob C, Giles GI, Giles NM, and Sies H. Sulfur and selenium: The role of oxidation state in protein structure and function. Angew Chem Int Ed Engl 42: 4742-4758, 2003. (Pubitemid 37314599)
92. Jacob MH, Amir D, Ratner V, Gussakowsky E, and Haas E. Predicting reactivities of protein surface cysteines as part of a strategy for selective multiple labeling. Biochemistry 44: 13664-13672, 2005. (Pubitemid 41507447)
93. Janssen-Heininger YM, Mossman BT, Heintz NH, Forman HJ, Kalyanaraman B, Finkel T, Stamler JS, Rhee SG, and van der Vliet A. Redox-based regulation of signal transduction: principles, pitfalls, and promises. Free Radic Biol Med 45: 1-17, 2008.
94. Jo SH, Son MK, Koh HJ, Lee SM, Song IH, Kim YO, Lee YS, Jeong KS, Kim WB, Park JW, Song BJ, and Huhe TL. Control of mitochondrial redox balance and cellular defense against oxidative damage by mitochondrialNADP+ -dependent isocitrate dehydrogenase. J Biol Chem 276: 16168-16176, 2001.
95. Johansson C, Kavanagh KL, Gileadi O, and Oppermann U. Reversible sequestration of active site cysteines in a 2Fe- 2S-bridged dimer provides a mechanism for glutaredoxin 2 regulation in human mitochondria. J Biol Chem 282: 3077-3082, 2007. (Pubitemid 47084316)
96. Johansson C, Lillig CH, and Holmgren A. Human mitochondrial glutaredoxin reduces S-glutathionylated proteins with high affinity accepting electrons from either glutathione or thioredoxin reductase. J Biol Chem 279: 7537-7543, 2004. (Pubitemid 38294632)
97. Jones DP. Redox sensing: orthogonal control in cell cycle and apoptosis signalling. J Int Med 268: 432-448, 2010.
98. Jones DP and Go YM. Redox compartmentalization and cellular stress. Diabetes Obes Metab 12 Suppl 2: 116-125, 2010.
99. Jowsey IR, Thomson RE, Orton TC, Elcombe CR, and Hayes JD. Biochemical and genetic characterization of a murine class Kappa glutathione S-transferase. Biochem J 373: 559-569, 2003. (Pubitemid 36897858)
100. Jung CH and Thomas JA. S-glutathiolated hepatocyte proteins and insulin disulfides as substrates for reduction by glutaredoxin, thioredoxin, protein disulfide isomerase, and glutathione. Arch Biochem Biophys 335: 61-72, 1996. (Pubitemid 26382679)
101. Kamga CK, Zhang SX, and Wang Y. Dicarboxylate carriermediated glutathione transport is essential for reactive oxygen species homeostasis and normal respiration in rat brain mitochondria. Am J Physiol 299: C497-C505, 2010.
102. Karoui H, Hogg N, Frejaville C, Tordo P, and Kalyanaraman B. Characterisation of sulfur-centred radical intermediates formed during the oxidation of thiols and sulfite by peroxynitrite. J Biol Chem 271: 6000-6009, 1996. (Pubitemid 26095401)
103. Kelner MJ and Montoya MA. Structural organization of the human glutathione reductase gene: Determination of correct cDNA sequence and identification of a mitochondrial leader sequence. Biochem Biophys Res Commun 269: 366-368, 2000. (Pubitemid 30440305)
104. Kim HY and Gladyshev VN. Methionine sulfoxide reduction in mammals: Characterization of methionine-R-sulfoxide reductases.Mol Biol Cell 15: 1055-1064, 2004. (Pubitemid 38316216)
105. Kim HY and Gladyshev VN. Methionine sulfoxide reductases: Selenoprotein forms and roles in antioxidant protein repair in mammals. Biochem J 407: 321-329, 2007. (Pubitemid 350058466)
106. Kissner R, Nauser T, Bugnon P, Lye PG, and Koppenol WH. Formation and properties of peroxynitrite as studied by laser flash photolysis, high-pressure stopped-flow technique, and pulse radiolysis. Chem Res Toxicol 10: 1285-1292, 1997. (Pubitemid 27524836)
107. Klatt P and Lamas S. Regulation of protein function by Sglutathiolation in response to oxidative and nitrosative stress. Eur J Biochem 267: 4928-4944, 2000. (Pubitemid 30641289)
108. Kobayashi M and Yamamoto M. Nrf2-Keap1 regulation of cellular defense mechanisms against electrophiles and reactive oxygen species. Adv Enzyme Regul 46: 113-140, 2006. (Pubitemid 44301353)
109. Kudin AP, Bimpong-Buta NY, Vielhaber S, Elger CE, and Kunz WS. Characterization of superoxide-producing sites in isolated brain mitochondria. J Biol Chem 279: 4127-4135, 2004. (Pubitemid 38198997)
110. Kumar V, Kitaeff N, Hampton MB, Cannell MB, and Winterbourn CC. Reversible oxidation of mitochondrial peroxiredoxin 3 in mouse heart subjected to ischemia and reperfusion. FEBS Lett 583: 997-1000, 2009.
111. Larsen K, Aronsson AC, Marmstal E, and Mannervik B. Immunological comparison of glyoxalase I from yeast and mammals and quantitative determination of the enzyme in human tissues by radioimmunoassay. Compa Biochem Physiol B 82: 625-638, 1985.
112. Lash LH. Mitochondrial GSH transport and intestinal cell injury: A commentary on ''contribution of mitochondrial GSH transport to matrix GSH status and colonic epithelial cell apoptosis.'' Free Radic Biol Med 44: 765-767, 2008.
113. Lee SR, Kim JR, Kwon KS, Yoon HW, Levine RL, Ginsburg A, and Rhee SG. Molecular cloning and characterization of a mitochondrial selenocysteine- containing thioredoxin reductase from rat liver. J Biol Chem 274: 4722-4734, 1999.
114. Leonard SE, Reddie KG, and Carroll KS. Mining the thiol proteome for sulfenic acid modifications reveals new targets for oxidation in cells. Chem Biol 4: 783-799, 2009.
115. Levine RL, Berlett BS, Moskovitz J, Mosoni L, and Stadtman ER. Methionine residues may protect proteins from critical oxidative damage. Mech Ageing Dev 107: 323-332, 1999. (Pubitemid 29210232)
116. Levine RL, Mosoni L, Berlett BS, and Stadtman ER. Methionine residues as endogenous antioxidants in proteins. Proc Natl Acad Sci U S A 93: 15036-15040, 1996. (Pubitemid 27009547)
117. Levonen AL, Landar A, Ramachandran A, Ceaser EK, Dickinson DA, Zanoni G, Morrow JD, and Darley-Usmar VM. Cellular mechanisms of redox cell signalling: Role of cysteine modification in controlling antioxidant defences in response to electrophilic lipid oxidation products. Biochem J 378: 373-382, 2004. (Pubitemid 38367228)
118. Li L, Shoji W, Takano H, Nishimura N, Aoki Y, Takahashi R, Goto S, Kaifu T, Takai T, and Obinata M. Increased susceptibility of MER5 (peroxiredoxin III) knockout mice to LPS-induced oxidative stress. Biochem Biophys Res Commun 355: 715-721, 2007. (Pubitemid 46330210)
119. Li W, James MO, McKenzie SC, Calcutt NA, Liu C, and Stacpoole PW. Mitochondrion as a novel site of dichloroacetate biotransformation by glutathione transferase OEv1. J Pharmacol Exp Ther 336: 87-94, 2011.
120. Li X, Cobb CE, Hill KE, Burk RF, and May JM. Mitochondrial uptake and recycling of ascorbic acid. Arch Biochem Biophys 387: 143-153, 2001. (Pubitemid 32989034)
121. Lillig CH, Berndt C, Vergnolle O, Lönn ME, Hudemann C, Bill E, and Holmgren A. Characterization of human glutaredoxin 2 as iron-sulfur protein: A possible role as redox sensor. Proc Natl Acad Sci U S A 102: 8168-8173, 2005. (Pubitemid 40800061)
122. Lillig CH and Holmgren A. Thioredoxin and related molecules- from biology to health and disease. Antioxid Redox Signal 9: 25-47, 2007. (Pubitemid 44901873)
123. Lillig CH, Lonn ME, Enoksson M, Fernandes AP, and Holmgren A. Short interfering RNA-mediated silencing of glutaredoxin 2 increases the sensitivity of HeLa cells toward doxorubicin and phenylarsine oxide. Proc Natl Acad Sci U S A 101: 13227-13232, 2004. (Pubitemid 39209647)
124. Lundberg M, Johansson C, Chandra J, Enoksson M, Jacobsson G, Ljung J, Johansson M, and Holmgren A. Cloning and expression of a novel human glutaredoxin (Grx2) with mitochondrial and nuclear isoforms. J Biol Chem 276: 26269-26275, 2001.
125. Luo S and Levine RL. Methionine in proteins defends against oxidative stress. FASEB J 23: 464-472, 2009.
126. Luo X, Budihardjo I, Zou H, Slaughter C, and Wang X. Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 94: 481-490, 1998. (Pubitemid 28391864)
127. MacMillan-Crow LA, Crow JP, Kerby JD, Beckman JS, and Thompson JA. Nitration and inactivation of manganese superoxide dismutase in chronic rejection of human renal allografts. Proc Natl Acad Sci U S A 93: 11853-11858, 1996. (Pubitemid 26347213)
128. Madej E, Folkes LK, Wardman P, Czapski G, and Goldstein S. Thiyl radicals react with nitric oxide to form Snitrosothiols with rate constants near the diffusioncontrolled limit. Free Radic Biol Med 44: 2013-2018, 2008.
129. Mallis RJ, Poland BW, Chatterjee TK, Fisher RA, Darmawan S, Honzatko RB, and Thomas JA. Crystal structure of S-glutathiolated carbonic anhydrase III. FEBS Lett 482: 237-241, 2000.
130. Manevich Y, Feinstein SI, and Fisher AB. Activation of the antioxidant enzyme 1-CYS peroxiredoxin requires glutathionylation mediated by heterodimerization with pi GST. Proc Natl Acad Sci U S A 101: 3780-3785, 2004. (Pubitemid 38381055)
131. Marino SM and Gladyshev VN. Cysteine function governs its conservation and degeneration and restricts its utilization on protein surfaces. J Mol Biol 404: 902-916, 2010.
132. Marino SM and Gladyshev VN. Structural analysis of cysteine S-nitrosylation: A modified acid-based motif and the emerging role of trans-nitrosylation. J Mol Biol 395: 844-859, 2010.
133. Marino SM, Li Y, Fomenko DE, Agisheva N, Cerny RL, and Gladyshev VN. Characterization of surface-exposed reactive cysteine residues in Saccharomyces cerevisiae. Biochemistry 49: 7709-7721, 2010.
134. Martensson J, Lai JCK, and Meister A. High-affinity transport of glutathione is part of a multicomponent system essential for mitochondrial function. Proc Natl Acad Sci U S A 87: 7185-7189, 1990.
135. Matsushima S, Ide T, Yamato M, Matsusaka H, Hattori F, Ikeuchi M, Kubota T, Sunagawa K, Hasegawa Y, Kurihara T, Oikawa S, Kinugawa S, and Tsutsui H. Overexpression of mitochondrial peroxiredoxin-3 prevents left ventricular remodeling and failure after myocardial infarction in mice. Circulation 113: 1779-1786, 2006. (Pubitemid 43958471)
136. McKernan TB, Woods EB, and Lash LH. Uptake of glutathione by renal cortical mitochondria. Arch Biochem Biophys 288: 653-663, 1991.
137. Meredith MJ and Reed DJ. Status of the mitochondrial pool of glutathione in the isolated hepatocyte. J Biol Chem 257: 3747-3753, 1982.
138. Mieyal JJ, Gallogly MM, Qanungo S, Sabens EA, and Shelton MD. Molecular mechanisms and clinical implications of reversible protein S-glutathionylation. Antioxid Redox Signal 10: 1941-1988, 2008.
139. Miranda-Vizuete A, Damdimopoulos AE, Pedrajas JR, Gustafsson JA, and Spyrou G. Human mitochondrial thioredoxin reductase cDNA cloning, expression and genomic organization. Eur J Biochem 261: 405-412, 1999. (Pubitemid 29187485)
140. Miseta A and Csutora P. Relationship between the occurrence of cysteine in proteins and the complexity of organisms. Mol Biol Evolution 17: 1232-1239, 2000. (Pubitemid 30617150)
141. Mitra S and Elliott SJ. Oxidative disassembly of the [2Fe-2S] cluster of human Grx2 and redox regulation in the mitochondria. Biochemistry 48: 3813-3815, 2009.
142. Moncada S and Erusalimsky JD. Does nitric oxide modulate mitochondrial energy generation and apoptosis? Nat Rev Mol Cell Biol 3: 214-220, 2002.
143. Morcos M, Du X, Pfisterer F, Hutter H, Sayed AA, Thornalley P, Ahmed N, Baynes J, Thorpe S, Kukudov G, Schlotterer A, Bozorgmehr F, El Baki RA, Stern D, Moehrlen F, Ibrahim Y, Oikonomou D, Hamann A, Becker C, Zeier M, Schwenger V, Miftari N, Humpert P, Hammes HP, Buechler M, Bierhaus A, Brownlee M, and Nawroth PP. Glyoxalase-1 prevents mitochondrial protein modification and enhances lifespan in Caenorhabditis elegans. Aging Cell 7: 260-269, 2008. (Pubitemid 351359658)
144. Moser CC, Farid TA, Chobot SE, and Dutton PL. Electron tunneling chains of mitochondria. Biochim Biophys Acta 1757: 1096-1109, 2006. (Pubitemid 44472548)
145. Murphy MP. How mitochondria produce reactive oxygen species. Biochem J 417: 1-13, 2009.
146. Murray CI, Kane LA, Uhrigshardt H, Wang SB, and Van Eyk JE. Site-mapping of in vitro S-nitrosation in cardiac mitochondria: Implications for cardioprotection. Mol Cell Proteomics 10: M110.004721, 2011.
147. Nadtochiy SM, Burwell LS, and Brookes PS. Cardioprotection and mitochondrial S-nitrosation: Effects of S-nitroso- 2-mercaptopropionyl glycine (SNO-MPG) in cardiac ischemia-reperfusion injury. J Mol Cell Cardiol 42: 812-825, 2007. (Pubitemid 46527599)
148. Nagy N, Malik G, Tosaki A, Ho YS, Maulik N, and Das DK. Overexpression of glutaredoxin-2 reduces myocardial cell death by preventing both apoptosis and necrosis. J Mol Cell Cardiol 44: 252-260, 2008.
149. Nan C, Li Y, Jean-Charles PY, Chen G, Kreymerman A, Prentice H, Weissbach H, and Huang X. Deficiency of methionine sulfoxide reductase A causes cellular dysfunction and mitochondrial damage in cardiac myocytes under physical and oxidative stresses. Biochem Biophys Res Commun 402: 608-613, 2010.
150. Nikiforov A, Dolle C, Niere M, and Ziegler M. Pathways and subcellular compartmentation of NAD biosynthesis in human cells: from entry of extracellular precursors to mitochondrial nad generation. J Biol Chem 286: 21767-21778, 2011.
151. Nikitovic D and Holmgren A. S-nitrosoglutathione is cleaved by the thioredoxin system with liberation of glutathione and redox regulating nitric oxide. J Biol Chem 271: 19180-19185, 1996. (Pubitemid 26271582)
152. Noh YH, Baek JY, Jeong W, Rhee SG, and Chang TS. Sulfiredoxin translocation into mitochondria plays a crucial role in reducing hyperoxidized peroxiredoxin III. J Biol Chem 284: 8470-8477, 2009.
153. Nomura K, Imai H, Koumura T, Arai M, and Nakagawa Y. Mitochondrial phospholipid hydroperoxide glutathione peroxidase suppresses apoptosis mediated by a mitochondrial death pathway. J Biol Chem 274: 29294-29302, 1999.
154. Nomura K, Imai H, Koumura T, Kobayashi T, and Nakagawa Y. Mitochondrial phospholipid hydroperoxide glutathione peroxidase inhibits the release of cytochrome c from mitochondria by suppressing the peroxidation of cardiolipin in hypoglycaemia-induced apoptosis. Biochem J 351: 183-193, 2000.
155. Olafsdottir K and Reed DJ. Retention of oxidized glutathione by isolated rat liver mitochondria during hydroperoxide treatment. Biochim Biophys Acta 964: 377-382, 1988. (Pubitemid 18084986)
156. Outten CE and Culotta VC. A novel NADH kinase is the mitochondrial source of NADPH in Saccharomyces cerevisiae. EMBO J 22: 2015-2024, 2003. (Pubitemid 36565527)
157. Park E-M and Thomas JA. Reduction of protein mixed disulfides (dethiolation) by E. coli thioredoxin: A study with glycogen phosphorylase b and creatine kinase. Arch Biochem Biophys 272: 25-31, 1989. (Pubitemid 19170861)
158. Pascual I, Larrayoz IM, Campos MM, and Rodriguez IR. Methionine sulfoxide reductase B2 is highly expressed in the retina and protects retinal pigmented epithelium cells from oxidative damage. Exp Eye Res 90: 420-428, 2010.
159. Pattison DI and Davies MJ. Absolute rate constants for the reaction of hypochlorous acid with protein side chains and peptide bonds. Chem Res Toxicol 14: 1453-1464, 2001. (Pubitemid 32983270)
160. Pemble SE, Wardle AF, and Taylor JB. Glutathione Stransferase class Kappa: Characterization by the cloning of rat mitochondrial GST and identification of a human homologue. Biochem J 319: 749-754, 1996. (Pubitemid 26386186)
161. Petit E, Michelet X, Rauch C, Bertrand-Michel J, Tercé F, Legouis R, and Morel F. Glutathione transferases kappa 1 and kappa 2 localize in peroxisomes and mitochondria, respectively, and are involved in lipid metabolism and respiration in Caenorhabditis elegans. FEBS J 276: 5030-5040, 2009.
162. Pollak N, Dolle C, and Ziegler M. The power to reduce: pyridine nucleotides-small molecules with a multitude of functions. Biochem J 402: 205-218, 2007. (Pubitemid 46383418)
163. Prime TA, Blaikie FH, Evans C, Nadtochiy SM, James AM, Dahm CC, Vitturi DA, Patel RP, Hiley CR, Abakumova I, Requejo R, Chouchani ET, Hurd TR, Garvey JF, Taylor CT, Brookes PS, Smith RA, and Murphy MP. A mitochondriatargeted S-nitrosothiol modulates respiration, nitrosates thiols, and protects against ischemia-reperfusion injury. Proc Natl Acad Sci U S A 106: 10764-10769, 2009.
164. Rabbani N and Thornalley PJ. Dicarbonyls linked to damage in the powerhouse: glycation of mitochondrial proteins and oxidative stress. Biochem Soc Trans 36: 1045-1050, 2008.
165. Radi R, Beckman JS, Bush KM, and Freeman BA. Peroxynitrite oxidation of sulfhydryls. J Biol Chem 266: 4244-4250, 1991.
166. Ravindrath V and Reed DJ. Glutathione depletion and formation of glutathione-protein mixed disulfide following exposure of brain mitochondria to oxidative stress. Biochem Biophys Res Commun 169: 1075-1079, 1990. (Pubitemid 20220730)
167. Reed D. Glutathione: Toxicological implications. Annu Rev Pharmacol Toxicol 30: 603-631, 1990.
168. Requejo R, Chouchani ET, James AM, Prime TA, Lilley KS, Fearnley IM, and Murphy MP. Quantification and identification of mitochondrial proteins containing vicinal dithiols. Arch Biochem Biophys 504: 228-235, 2010.
169. Requejo R, Hurd TR, Costa NJ, and Murphy MP. Cysteine residues exposed on protein surfaces are the dominant intramitochondrial thiol and may protect against oxidative damage. FEBS J 277: 1465-1480, 2010.
170. Rhee SG. Cell signaling. H2O2, a necessary evil for cell signaling. Science 312: 1882-1883, 2006. (Pubitemid 43993698)
171. Rhee SG, Bae YS, Lee SR, and Kwon J. Hydrogen peroxide: A key messenger that modulates protein phosphorylation through cysteine oxidation. Sci STKE 2000: pe1, 2000.
172. Rhee SG, Kang SW, Chang TS, Jeong W, and Kim K. Peroxiredoxin, a novel family of peroxidases. IUBMB Life 52: 35-41, 2001.
173. Rhee SG, Kang SW, Jeong W, Chang TS, Yang KS, and Woo HA. Intracellular messenger function of hydrogen peroxide and its regulation by peroxiredoxins. Curr Opin Cell Biol 17: 183-189, 2005. (Pubitemid 40380942)
174. Rhee SG, Yang KS, Kang SW, Woo HA, and Chang TS. Controlled elimination of intracellular H2O2: Regulation of peroxiredoxin, catalase, and glutathione peroxidase via post-translational modification. Antioxid Redox Signal 7: 619-626, 2005. (Pubitemid 40563199)
175. Rigobello MP, Folda A, Scutari G, and Bindoli A. The modulation of thiol redox state affects the production and metabolism of hydrogen peroxide by heart mitochondria. Arch Biochem Biophys 441: 112-122, 2005. (Pubitemid 41568203)
176. Salmeen A, Andersen JN, Myers MP, Meng TC, Hinks JA, Tonks NK, and Barford D. Redox regulation of protein tyrosine phosphatase 1B involves a sulphenyl-amide intermediate. Nature 423: 769-773, 2003. (Pubitemid 36735701)
177. Sanchez R, Riddle M, Woo J, and Momand J. Prediction of reversibly oxidized protein cysteine thiols using protein structure properties. Protein Sci 17: 473-481, 2008. (Pubitemid 351281548)
178. Sazanov LA and Jackson JB. Proton-translocating transhydrogenase and NAD- and NADP-linked isocitrate dehydrogenases operate in a substrate cycle which contributes to fine regulation of the tricarboxylic acid cycle activity in mitochondria. FEBS Lett 344: 109-116, 1994.
179. Scarlett JL, Packer MA, Porteous CM, and Murphy MP. Alterations to glutathione and nicotinamide nucleotides during the mitochondrial permeability transition induced by peroxymitrite. Biochem Pharmacol 52: 1047-1055, 1996. (Pubitemid 26338263)
180. Schö neich C. Mechanisms of protein damage induced by cysteine thiyl radical formation. Chem Res Toxicol 21: 1175-1179, 2008. (Pubitemid 351967380)
181. Schafer FQ and Buettner GR. Redox environment of the cell as viewed through the redox state of the glutathione disulfide/ glutathione couple. Free Radic Biol Med 30: 1191-1212, 2001. (Pubitemid 32463931)
182. Schroder E and Eaton P. Hydrogen peroxide as an endogenous mediator and exogenous tool in cardiovascular research: Issues and considerations. Curr Opin Pharmacol 8: 153-159, 2008.
183. Seres T, Ravichandran V, Moriguchi T, Rokutan K, Thomas JA, and Johnston RB, Jr. Protein S-thiolation and dethiolation during the respiratory burst in human monocytes. A reversible post-translational modification with potential for buffering the effects of oxidant stress. J Immunol 156: 1973- 1980, 1996. (Pubitemid 26069333)
184. Shelton MD, Chock PB, and Mieyal JJ. Glutaredoxin: Role in reversible protein s-glutathionylation and regulation of redox signal transduction and protein translocation. Antioxid Redox Signal 7: 348-366, 2005. (Pubitemid 40279804)
185. Sies H. Nicotinamide Nucleotide Compartmentation. London: Academic Press, 1982.
186. Sivaramakrishnan S, Cummings AH, and Gates KS. Protection of a single-cysteine redox switch from oxidative destruction: on the functional role of sulfenyl amide formation in the redox-regulated enzyme PTP1B. Bioorg Medicin Chem Lett 20: 444-447, 2010.
187. Spyrou G, Enmark E, Miranda-Vizuete A, and Gustafsson J. Cloning and expression of a novel mammalian thioredoxin. J Biol Chem 272: 2936-2941, 1997. (Pubitemid 27053344)
188. Stamler JS. Redox signalling: Nitrosylation and related target interactions of nitric oxide. Cell 78: 931-936, 1994. (Pubitemid 24292322)
189. Stamler JS and Hausladen A. Oxidative modifications in nitrosative stress. Nat Struct Biol 5: 247-249, 1998. (Pubitemid 28164870)
190. Stamler JS, Singel DJ, and Loscalzo J. Biochemistry of nitric oxide and its redox activated forms. Science 258: 1898-1902, 1992. (Pubitemid 23026727)
191. Starke DW, Chock PB, and Mieyal JJ. Glutathione-thiyl radical scavenging and transferase properties of human glutaredoxin (thioltransferase). Potential role in redox signal transduction. J Biol Chem 278: 14607-14613, 2003. (Pubitemid 36799782)
192. Sun J, Morgan M, Shen RF, Steenbergen C, and Murphy E. Preconditioning results in S-nitrosylation of proteinsinvolved in regulation of mitochondrial energetics and calcium transport. Circ Res 101: 1155-1163, 2007. (Pubitemid 350146442)
193. Sun J and Murphy E. Protein S-nitrosylation and cardioprotection. Circ Res 106: 285-296, 2010.
194. Tamura T, McMicken HW, Smith CV, and Hansen TN. Gene structure for mouse glutathione reductase, including a putative mitochondrial targeting signal. Biochem Biophys Res Commun 237: 419-422, 1997. (Pubitemid 27406045)
195. Tanaka T, Hosoi F, Yamaguchi-Iwai Y, Nakamura H, Masutani H, Ueda S, Nishiyama A, Takeda S, Wada H, Spyrou G, and Yodoi J. Thioredoxin-2 (TRX-2) is an essential gene regulating mitochondria-dependent apoptosis. EMBO J 21: 1695-1703, 2002. (Pubitemid 34614625)
196. Taylor ER, Hurrell F, Shannon RJ, Lin TK, Hirst J, and Murphy MP. Reversible glutathionylation of complex I increases mitochondrial superoxide formation. J Biol Chem 278: 19603-19610, 2003. (Pubitemid 36799143)
197. Thomas JA, Poland B, and Honzatko R. Protein sulfhydryls and their role in the antioxidant function of protein Sthiolation. Arch Biochem Biophys 319: 1-9, 1995.
198. Todisco S, Agrimi G, Castegna A, and Palmieri F. Identification of the mitochondrial NAD+ transporter in Saccharomyces cerevisiae. J Biol Chem 281: 1524-1531, 2006.
199. Trujillo M, Clippe A, Manta B, Ferrer-Sueta G, Smeets A, Declercq JP, Knoops B, and Radi R. Pre-steady state kinetic characterization of human peroxiredoxin 5: Taking advantage of Trp84 fluorescence increase upon oxidation. Arch Biochem Biophys 467: 95-106, 2007. (Pubitemid 47625297)
200. Turell L, Botti H, Carballal S, Ferrer-Sueta G, Souza JM, Durán R, Freeman BA, Radi R, and Alvarez B. Reactivity of sulfenic acid in human serum albumin. Biochemistry 47: 358-367, 2008.
201. Vougier S, Mary J, and Friguet B. Subcellular localization of methionine sulphoxide reductase A (MsrA): Evidence for mitochondrial and cytosolic isoforms in rat liver cells. Biochem J 373: 531-537, 2003. (Pubitemid 36897855)
202. Wardman P and Von Sonntag C. Kinetic factors that control the fate of thiyl radicals in cells. Methods Enzymol 251: 31-45, 1995.
203. Watabe S, Hiroi T, Yamamoto Y, Fujioka Y, Hasegawa H, Yago N, and Takahashi SY. SP-22 is a thioredoxin-dependent peroxide reductase in mitochondria. Eur J Biochem 249: 52-60, 1997. (Pubitemid 27432595)
204. Weerapana E, Wang C, Simon GM, Richter F, Khare S, Dillon MB, Bachovchin DA, Mowen K, Baker D, and Cravatt BF. Quantitative reactivity profiling predicts functional cysteines in proteomes. Nature 468: 790-795, 2010.
205. Wingert RA, Galloway JL, Barut B, Foott H, Fraenkel P, Axe JL, Weber GJ, Dooley K, Davidson AJ, Schmidt B, Paw BH, Shaw GC, Kingsley P, Palis J, Schubert H, Chen O, Kaplan J, Zon LI, van Bebber F, Busch-Nentwich E, Dahm R, Frohnhü fer HG, Geiger H, Gilmour D, Holley S, Hooge , Jö lich D, Knaut H, Maderspacher F, Neumann C, Nicolson T, Nusslein-Volhard C, Roehl H, Schü nberger U, Seiler C, Sü llner C, Sonawane M, Wehner A, Weiler C, Hagner U, Hennen E, Kaps C, Kirchner A, Koblizek TI, Langheinrich U, Metzger C, Nordin R, Pezzuti M, Schlombs K, deSantana-Stamm J, Trowe T, Vacun G, and Walker A. Deficiency of glutaredoxin 5 reveals Fe-S clusters are required for vertebrate haem synthesis. Nature 436: 1035-1039, 2005. (Pubitemid 41191688)
206. Wink DA, Cook JA, Pacelli R, Liebmann J, Krishna MC, and Mitchell JB. Nitric oxide protects against cellular damaged by reactive oxygen species. Toxicol Lett 82: 221-226, 1995. (Pubitemid 26054708)
207. Winterbourn CC. Superoxide as an intracellular radical sink. Free Radic Biol Med 14: 85-90, 1993. (Pubitemid 23024261)
208. Winterbourn CC. Reconciling the chemistry and biology of reactive oxygen species. Nat Chem Biol 4: 278-287, 2008.
209. Winterbourn CC and Metodiewa D. Reactivity of biologically important thiol compounds with superoxide and hydrogen peroxide. Free Radic Biol Med 27: 322-328, 1999. (Pubitemid 29395424)
210. Woo HA, Chae HZ, Hwang SC, Yang KS, Kang SW, Kim K, and Rhee SG. Reversing the inactivation of peroxiredoxins caused by cysteine sulfinic acid formation. Science 300: 653-656, 2003. (Pubitemid 36520592)
211. Wood ZA, Poole LB, and Karplus PA. Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling. Science 300: 650-653, 2003. (Pubitemid 36520591)
212. Wu H, Xing K, and Lou MF. Glutaredoxin 2 prevents H2O2-induced cell apoptosis by protecting complex I activity in the mitochondria. Biochim Biophys Acta 1797: 1705-1715, 2010.
213. Xiong Y, Uys JD, Tew KD, and Townsend DM. Sglutathionylation: from molecular mechanisms to health outcomes. Antioxid Redox Signal 15: 233-270, 2011.
214. Yant LJ, Ran Q, Rao L, Van Remmen H, Shibatani T, Belter JG, Motta L, Richardson A, and Prolla TA. The selenoprotein GPX4 is essential for mouse development and protects from radiation and oxidative damage insults. Free Radic Biol Med 34: 496-502, 2003. (Pubitemid 36140174)
215. Ye H and Rouault TA. Human iron-sulfur cluster assembly, cellular iron homeostasis, and disease. Biochemistry 49: 4945-4956, 2010.
216. Yermolaieva O, Xu R, Schinstock C, Brot N, Weissbach H, Heinemann SH, and Hoshi T. Methionine sulfoxide reductase A protects neuronal cells against brief hypoxia/ reoxygenation. Proc Natl Acad Sci U S A 101: 1159-1164, 2004. (Pubitemid 38182659)
217. Yim MB, Chae HZ, Rhee SG, Chock PB, and Stadtman ER. On the protective mechanism of the thiol-specific antioxidant enzyme against the oxidative damage of biomacromolecules. J Biol Chem 269: 1621-1626, 1994. (Pubitemid 24035351)
218. Zeng J, Dunlop RA, Rodgers KJ, and Davies MJ. Evidence for inactivation of cysteine proteases by reactive carbonyls via glycation of active site thiols. Biochem J 398: 197-206, 2006. (Pubitemid 44338476)
219. Zhang H, Go YM, and Jones DP. Mitochondrial thioredoxin- 2/peroxiredoxin-3 system functions in parallel with mitochondrial GSH system in protection against oxidative stress. Arch Biochem Biophys 465: 119-126, 2007. (Pubitemid 47283985)
220. Zhang H, Xu Y, Joseph J, and Kalyanaraman B. Intramolecular electron transfer between tyrosyl radical and cysteine residue inhibits tyrosine nitration and induces thiyl radical formation in model peptides treated with myeloperoxidase, H2O2, and NO2-: EPR SPIN trapping studies. J Biol Chem 280: 40684-40698, 2005. (Pubitemid 41780560)
221. Zhang X, Kurnasov OV, Karthikeyan S, Grishin NV, Osterman AL, and Zhang H. Structural characterization of a human cytosolic NMN/NaMN adenylyltransferase and implication in human NAD biosynthesis. J Biol Chem 278: 13503-13511, 2003. (Pubitemid 36800125)
222. Zheng M, Aslund F, and Storz G. Activation of the OxyR transcription factor by reversible disulfide bond formation. Science 279: 1718-1721, 1998 (Pubitemid 28164467)
223. Zhou L, Aon MA, Almas T, Cortassa S, Winslow RL, and O'Rourke B. A reaction-diffusion model of ROS-inducedROS release in a mitochondrial network. PLoS Comp Biol 6: E1000657, 2010.
224. Ziegler DM. Role of reversible oxidation-reduction of enzyme thiols-disulfides in metabolic regulation. Annu Rev Biochem 54: 305-329, 1985. (Pubitemid 15073649)
225. Zorov DB, Juhaszova M, and Sollott SJ. Mitochondrial ROS-induced ROS release: An update and review. Biochim Biophys Acta 1757: 509-517, 2006.