Glutathionylation of mitochondrial proteins

Antioxidants and Redox Signaling

Volumn 7, Issue 7-8, 2005, Pages 999-1010

  Hurd, Thomas R ^a   Costa, Nikola J ^a   Dahm, Christina C ^a   Beer, Samantha M ^a   Brown, Stephanie E ^a   Filipovska, Aleksandra ^a   Murphy, Michael P ^a,b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DISULFIDE; FLAVINE MONONUCLEOTIDE; GLUTAREDOXIN; GLUTATHIONE; GLUTATHIONE TRANSFERASE; MITOCHONDRIAL PROTEIN; NITRIC OXIDE; PEROXYNITRITE; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); THIOL GROUP; THIOREDOXIN;

ANIMAL CELL; ANTIOXIDANT ACTIVITY; APOPTOSIS; CATALYSIS; CONTROLLED STUDY; DISULFIDE BOND; ENZYME ACTIVE SITE; ESCHERICHIA COLI; HELA CELL; HUMAN; HUMAN CELL; MITOCHONDRION; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN MODIFICATION; RAT; REVIEW; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

ANIMALS; ANTIOXIDANTS; GLUTATHIONE; HUMANS; MITOCHONDRIAL PROTEINS; OXIDATION-REDUCTION; SULFHYDRYL COMPOUNDS; THIOREDOXIN;

EID: 22044444687     PISSN: 15230864     EISSN: None     Source Type: Journal    
DOI: 10.1089/ars.2005.7.999     Document Type: Review

References (115)

1. Arai M, Imai H, Koumura T, Yoshida M, Emoto K, Umeda M, Chiba N, and Nakagawa Y. Mitochondrial phospholipid hydroperoxide glutathione peroxidase plays a major role in preventing oxidative injury to cells. J Biol Chem 274: 4924-4933, 1999.
2. Arner ES and Holmgren A. Physiological functions of thioredoxin and thioredoxin reductase. Eur J Biochem 267: 6102-6109, 2000.
3. Axelsson K and Mannervik B. General specificity of cytoplasmic thioltransferase (thiol:disulfide oxidoreductase) from rat liver for thiol and disulfide substrates. Biochim Biophys Acta 613: 324-336, 1980.
4. 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 U S A 87: 1620-1624, 1990.
5. Beckman KB and Ames BN. The free radical theory of aging matures. Physiol Rev 78: 547-581, 1998.
6. 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.
7. Bernardi P, Broekmeier KM, and Pfeiffer DR. Recent progress on regulation of the mitochondrial permeability transition pore; a cyclosporin-sensitive pore in the inner mitochondrial membrane. J Bioenerg Biomembr 26: 509-517, 1994.
8. Bizouarn T, Fjellstrom O, Meuller J, Axelsson M, Bergkvist A, Johansson C, Karlsson BG, 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.
9. Bolanos JP, Almeida A, Stewart V, Peuchan S, Land JM, Clark JB, and Heales SJR. Nitric oxide-mediated mitochondrial damage in the brain: mechanisms and implications for neurodegenerative diseases. J Neurochem 68: 2227-2240, 1997.
10. 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.
11. Brown GC and Cooper CE. Nanomolar concentrations of nitric oxide reversibly inhibit synaptosomal respiration by competing with oxygen at cytochrome oxidase. FEBS Lett 356: 295-298, 1994.
12. Bushweller JH, Aslund F, Wuthrich K, and Holmgren A. Structural and functional characterization of the mutant Escherichia coli glutaredoxin (Cl4-S) and its mixed disulfide with glutathione. Biochemistry 31: 9288-9293, 1992.
13. Bustamante J, Tovar BA, Montero G, and Boveris A. Early redox changes during rat thymocyte apoptosis. Arch Biochem Biophys 337: 121-128, 1997.
14. Cabiscol E and Levine RL. The phosphatase activity of carbonic anhydrase III is reversibly regulated by glutathiolation. Proc Natl Acad Sci USA 93: 4170-4174, 1996.
15. 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.
16. Cleeter MJW, Cooper JM. and Schapira AHV. Irreversible inhibition of mitochondrial complex I by 1-methyl-4-phenylpyridinium: evidence for free radical involvement. J Neurochem 58: 786-789, 1992.
17. Cooper CE. Nitric oxide and cytochrome oxidase: substrate, inhibitor or effector? Trends Biochem Sci 27: 33-39, 2002.
18. Coppola S and Ghibelli L. GSH extrusion and the mitochondrial pathway of apoptotic signalling. Biochem Soc Trans 28: 56-61, 2000.
19. 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.
20. Cotgreave JA 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.
21. Daum G. Lipids of mitochondria. Biochim Biophys Acta 822: 1-42, 1985.
22. Di Monte DA, Chan P, and Sandy MS. Glutathione in Parkinson's disease: a link between oxidative stress and mitochondrial damage? Ann Neurol 32: S111-115, 1992.
23. 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.
24. Eaton P, Byers HL, Leeds N, Ward MA, and Shattock MJ. Detection, quantitation, purification, and identification of cardiac proteins S-thiolated during ischemia and reperfusion. J Biol Chem 277: 9806-9811, 2002.
25. Elfering SL, Sarkela TM, and Giulivi C. Biochemistry of mitochondrial nitric-oxide synthase. J Biol Chem 277: 38079-38086, 2002.
26. Esposito LA, Kokoszka JE, Waymire KG, Cottrell B, MacGregor GR, and Wallace DC. Mitochondrial oxidative stress in mice lacking the glutathione peroxidase-1 gene. Free Radic Biol Med 28: 754-766, 2000.
27. Fagian MM, Pereira-da-Silva L, Martins IS, and Vercesi AE. Membrane protein thiol cross-linking asociated with the permeabilization of the inner mitochondrial membrane by Ca plus prooxidants. J Biol Chem 265: 19955-19960, 1990.
28. Fernandez-Checa JC, Kaplowitz N, Garcia-Ruiz C, and Colell A. Mitochondrial glutathione: importance and transport. Semin Liver Dis 18: 389-401, 1998.
29. Fontaine E, Eriksson O, Ichas F, and Bernardi P. Regulation of the permeability transition pore in skeletal muscle. J Biol Chem 213: 12662-12668, 1998.
30. Foster MW and Stamler JS. New insights into protein S-nitrosylation. Mitochondria as a model system. J Biol Chem 279: 25891-25897, 2004.
31. 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.
32. 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.
33. Garcia-Ruiz C, Colell A, Morales A, Kaplowitz N, and Fernandez-Checa JC. Role of oxidative stress generated from the mitochondrial electron transport chain and mitochondrial glutathione status in loss of mitochondrial function and activation of transcription factor nuclear factor-kappa B: studies with isolated mitochondria and rat hepatocytes. Mol Pharmacol 48: 825-834, 1995.
34. 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.
35. 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.
36. Ghafourifar P and Richter C. Nitric oxide synthase activity in mitochondria. FEBS Lett 418: 291-296, 1997.
37. Ghibelli L, Coppola S, Fanelli C, Rotilio G, Civitareale P, Scovassi AI, and Ciriolo MR. Glutathione depletion causes cytochrome c release even in the absence of cell commitment to apoptosis. FASEB J 13: 2031-2036, 1999.
38. Gilbert HF. Redox control of enzyme activities by thiol/disulfide exchange. Methods Enzymol 107: 330-351, 1984.
39. Gilbert HF. Molecular and cellular aspects of thiol-disulfide exchange. Adv Enzymol 63: 69-172, 1990.
40. Gilbert HF. Thiol/disulfide exchange equilibria and disulfide bond stability. Methods Enzymol 251: 8-28, 1995.
41. 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.
42. 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.
43. 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.
44. Godeas C, Sandri G, and Panfili E. Distribution of phospholipid hydroperoxide glutathione peroxidase (PHGPx) in rat testis mitochondria. Biochim Biophys Acta 1191: 147-150, 1994.
45. Goossens V, Grooten J, De Vos K, and Fiers W. Direct evidence for tumor necrosis factor-induced mitochondrial reactive oxygen intermediates and their involvement in cytotoxicity. Proc Natl Acad Sci U S A 92: 8115-8119, 1995.
46. Gravina SA and Mieyal JJ. Thioltransferase is a specific glutathionyl mixed disulfide oxidoreductase. Biochemistry 32: 3368-3376, 1993.
47. Griffith OW and Meister A. Origin and turnover of mitochondrial glutathione. Proc Natl Acad Sci U S A 82: 4668-4672, 1985.
48. Hirst J, Carroll J, Fearnley IM, Shannon RJ, and Walker JE. The nuclear encoded subunits of complex I from bovine heart mitochondria. Biochim Biophys Acta 1604: 135-150, 2003.
49. Holmgren A. Thioredoxin. Annu Rev Biochem 54: 237-271, 1985.
50. 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.
51. Jenner P. Altered mitochondrial function, iron metabolism and glutathione levels in Parkinson's disease. Acta Neurol Scand Suppl 146: 6-13, 1993.
52. Jha N, Jurma O, Lalli G, Liu Y, Pettus EH, Greenamyre JT, Liu RM, Forman HJ, and Andersen JK. Glutathione depletion in PC12 results in selective inhibition of mitochondrial complex I activity. Implications for Parkinson's disease. J Biol Chem 275: 26096-26101, 2000.
53. +-dependent isocitrate dehydrogenase. J Biol Chem 276: 16168-16176, 2001.
54. Jocelyn PC. Some properties of mitochondrial glutathione. Biochim Biophys Acta 396: 427-436, 1975.
55. 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.
56. 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.
57. Kamphuis IG, Drenth J, and Baker EN. Thiol proteases. Comparative studies based on the high-resolution structures of papain and actinidin, and on amino acid sequence information for cathepsins B and H, and stem bromelain. J Mol Biol 182: 317-329, 1985.
58. Kanai AJ, Pearce LL, Clemens PR, Birder LA, VanBibber MM, Choi SY, de Groat WC, and Peterson J. Identification of a neuronal nitric oxide synthase in isolated cardiac mitochondria using electrochemical detection. Proc Natl Acad Sci U S A 98: 14126-14131, 2001.
59. 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.
60. Klatt P and Lamas S. Regulation of protein function by S-glutathiolation in response to oxidative and nitrosative stress. Eur J Biochem 267: 4928-4944, 2000.
61. Klatt P, Molina EP, De Lacoba MG, Padilla CA, Martinez-Galesteo E, Barcena JA, and Lamas S. Redox regulation of c-Jun DNA binding by reversible S-glutathiolation. FASEB J 13: 1481-1490, 1999.
62. Kurosawa K, Hayashi N, Sato N, Kamada T, and Tagawa K. Transport of glutathione across the mitochondrial membranes. Biochem Biophys Res Commun 167: 367-372, 1990.
63. Lee C-K, Klopp RG, Weindruch R, and Prolla TA. Gene expression profile of aging and its retardation by caloric restriction. Science 285: 1390-1393, 1999.
64. 2+ release from mitochondria by the oxidation-reduction state of pyridine nucleotides. Proc Natl Acad Sci U S A 75: 1690-1694, 1978.
65. 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.
66. Lin T-K. The development of IBTP a novel mitochondrially targeted protein thiol probe. Ph.D. thesis 2002, University of Otago, Dunedin, NZ.
67. 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.
68. 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.
69. Marchetti P, Decaudin D, Macho A, Zamzami N, Hirsch T, Susin SA, and Kroemer G. Redox regulation of apoptosis: impact of thiol oxidation status on mitochondrial function. Eur J Immunol 27: 289-296, 1997.
70. 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.
71. McKernan TB, Woods EB, and Lash LH. Uptake of glutathione by renal cortical mitochondria. Arch Biochem Biophys 288: 653-663, 1991.
72. Meister A. Mitochondrial changes associated with glutathione deficiency. Biochim Biophys Acta 1271: 35-42, 1995.
73. Meredith MJ and Reed DJ. Status of the mitochondrial pool of glutathione in the isolated hepatocyte. J Biol Chem 257: 3747-3753, 1982.
74. 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.
75. Moncada S and Erusalimsky JD. Does nitric oxide modulate mitochondrial energy generation and apoptosis? Nat Rev Mol Cell Biol 3: 214-220, 2002.
76. Murphy MP. Nitric oxide and cell death. Biochim Biophys Acta 1411: 401-414, 1999.
77. Musil D, Zucic D, Turk D, Engh RA, Mayr I, Huber R, Popovic T, Turk V, Towatari T, and Katunuma N. The refined 2.15 A x-ray crystal structure of human liver cathepsin B: the structural basis for its specificity. EMBO J 10: 2321-2330, 1991.
78. Nulton-Persson AC, Starke DW, Mieyal JJ, and Szweda LI. Reversible inactivation of alpha-ketoglutarate dehydrogenase in response to alterations in the mitochondrial glutathione status. Biochemistry 42: 4235-4242, 2003.
79. Odin JA, Huebert RC, Casciola-Rosen L, LaRusso NF, and Rosen A. Bcl-2-dependent oxidation of pyruvate dehydrogenase-E2, a primary biliary cirrhosis autoantigen, during apoptosis. J Clin Invest 108: 223-232, 2001.
80. O'Donovan DJ, Katkin JP, Tamura T, Smith CV, and Welty SE. Attenuation of hyperoxia-induced growth inhibition in H441 cells by gene transfer of mitochondrially targeted glutathione reductase. Am J Respir Cell Mol Biol 22: 732-738, 2000.
81. Olafsdottir K and Reed DJ. Retention of oxidized glutathione by isolated rat liver mitochondria during hydroperoxide treatment. Biochim Biophys Acta 964: 377-382, 1988.
82. Padgett CM and Whorton AR. Regulation of cellular thiol redox status by nitric oxide. Cell Biochem Biophys 27: 157-177, 1995.
83. Padgett CM and Whorton AR. S-Nitrosoglutathione reversibly inhibits GAPDH by S-nitrosylation. Am J Physiol 269: C739-C749, 1995.
84. Panfili E, Sandri G, and Ernster L. Distribution of glutathione peroxidases and glutathione reductase in rat brain mitochondria. FEBS Lett 290: 35-37, 1991.
85. 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.
86. Pemble SE, Wardle AF, and Taylor JB. Glutathione S-transferase class Kappa: characterization by the cloning of rat mitochondrial GST and identification of a human homologue. Biochem J 319 (Pt 3): 749-754, 1996.
87. Petronilli V, Costantini P, Scorrano L, Colonna R, Passamonti S, and Bernardi P. The voltage sensor of the mitochondrial permeability transition is tuned by the oxidation-reduction state of vicinal thiols. J Biol Chem 269: 16638-16642, 1994.
88. Radi R, Beckman JS, Bush KM, and Freeman BA. Peroxynitrite oxidation of sulfhydryls. J Biol Chem 266: 4244-4250, 1991.
89. Reed D. Glutathione: toxicological implications. Annu Rev Pharmacol Toxicol 30: 603-631, 1990.
90. Ricci JE, Munoz-Pinedo C, Fitzgerald P, Bailly-Maitre B, Perkins GA, Yadava N, Scheffler IE, Ellisman MH, and Green DR. Disruption of mitochondrial function during apoptosis is mediated by caspase cleavage of the p75 sub-unit of complex I of the electron transport chain. Cell 117: 773-786, 2004.
91. Ruoppolo M, Lundstrom-Ljung J, Talamo F, Pucci P, and Marino G. Effect of glutaredoxin and protein disulfide isomerase on the glutathione-dependent folding of ribonuclease A. Biochemistry 36: 12259-12267, 1997.
92. Sarkela TM, Berthiaume J, Elfering S, Gybina AA, and Giulivi C. The modulation of oxygen radical production by nitric oxide in mitochondria. J Biol Chem 276: 6945-6949, 2001.
93. Scarlett JL, Packer MA, Porteous CM, and Murphy MP. Alterations to glutathione and nicotinamide nucleotides during the mitochondrial permeability transition induced by peroxynitrite. Biochem Pharmacol 52: 1047-1055, 1996.
94. 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.
95. Schulze-Osthoff K, Bakker AC, Vanhaesebroeck B, Beyaert R, Jacob WA, and Fiers W. Cytotoxic activity of tumor necrosis factor is mediated by early damage of mitochondrial functions. Evidence for the involvement of mitochondrial radical generation. J Biol Chem 267: 5317-5323, 1992.
96. 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.
97. Soderdahl T, Enoksson M, Lundberg M, Holmgren A, Ottersen OP, Orrenius S, Bolcsfoldi G, and Cotgreave IA. Visualization of the compartmentalization of glutathione and protein-glutathione mixed disulfides in cultured cells. FASEB J 17: 124-126, 2003.
98. 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.
99. St-Pierre J, Buckingham JA, Roebuck SJ, and Brand MD. Topology of superoxide production from different sites in the mitochondrial electron transport chain. J Biol Chem 277: 44784-44790, 2002.
100. Stamler JS. Redox signalling: nitrosylation and related target interactions of nitric oxide. Cell 78: 931-936, 1994.
101. Stamler JS and Hausladen A. Oxidative modifications in nitrosative stress. Nat Struct Biol 5: 247-249, 1998.
102. 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.
103. Steffen M, Sarkela TM, Gybina AA, Steele TW, Trasseth NJ, Kuehl D, and Giulivi C. Metabolism of S-nitrosoglutathione in intact mitochondria. Biochem J 356: 395-402, 2001.
104. Tamura T, McMicken HW, Smith CV, and Hansen TN. Mitochondrial targeting of glutathione reductase requires a leader sequence. Biochem Biophys Res Commun 222: 659-663, 1996.
105. 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.
106. 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.
107. Tatoyan A and Giulivi C. Purification and characterization of a nitric-oxide synthase from rat liver mitochondria. J Biol Chem 273: 11044-11048, 1998.
108. 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.
109. Thomas JA, Poland B, and Honzatko R. Protein sulfhydryls and their role in the antioxidant function of protein S-thiolation. Arch Biochem Biophys 319: 1-9, 1995.
110. Valle VGR, Fagian MM, Paretoni LS, Meinecke AR, and Vercesi AE. The participation of reactive oxygen species and protein thiols in the mechanism of mitochondrial inner membrane permeabilisation by calcium plus prooxidants. Arch Biochem Biophys 307: 1-7, 1993.
111. van den Dobbelsteen DJ, Nobel CS, Schlegel J, Cotgreave IA, Orrenius S, and Slater AF. Rapid and specific efflux of reduced glutathione during apoptosis induced by anti-Fas/APO-1 antibody. J Biol Chem 271: 15420-15427, 1996.
112. 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.
113. Winterbourn CC. Superoxide as an intracellular radical sink. Free Radic Biol Med 14: 85-90, 1993.
114. Zheng M, Aslund F, and Storz G. Activation of the OxyR transcription factor by reversible disulfide bond formation. Science 279: 1718-1721, 1998.
115. Ziegler DM. Role of reversible oxidation-reduction of enzyme thiols-disulfides in metabolic regulation. Annu Rev Biochem 54: 305-329, 1985.