Disruption of mitochondrial redox circuitry in oxidative stress

Chemico-Biological Interactions

Volumn 163, Issue 1-2, 2006, Pages 38-53

  Jones, Dean P ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Antioxidants; Glutathione; Oxidative phosphorylation; Respiratory control; Superoxide anion; Thioredoxin

Indexed keywords

ADENOSINE TRIPHOSPHATE; ANTIMYCIN A1; ANTIOXIDANT; CYANIDE; FERRIC ION; FREE RADICAL; GLUTATHIONE; OXIDIZING AGENT; OXYGEN; PARACETAMOL; ROTENONE; SUPEROXIDE; THIOREDOXIN;

ARTICLE; CELL PROTECTION; CYTOPATHOLOGY; CYTOTOXICITY; ELECTRON TRANSPORT; ENERGY METABOLISM; HUMAN; HYPOTHESIS; MITOCHONDRIAL ENERGY TRANSFER; MITOCHONDRIAL RESPIRATION; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; WESTERN BLOTTING;

ANIMALS; DISULFIDES; ENERGY METABOLISM; HUMANS; MITOCHONDRIA; OXIDATION-REDUCTION; OXIDATIVE STRESS; SIGNAL TRANSDUCTION; SULFHYDRYL COMPOUNDS; SUPEROXIDES;

EID: 33749993246     PISSN: 00092797     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbi.2006.07.008     Document Type: Article

References (110)

1. Fishbane S., Durham J.H., Marzo K., and Rudnick M. N-Acetylcysteine in the prevention of radiocontrast-induced nephropathy. J. Am. Soc. Nephrol. 15 2 (2004) 251-260
2. Brion L.P., Bell E.F., and Raghuveer T.S. Vitamin E supplementation for prevention of morbidity and mortality in preterm infants. Cochrane Database Syst. Rev. 3 (2003) CD003665
3. Goodman G.E., Thornquist M.D., Balmes J., Cullen M.R., Meyskens Jr. F.L., Omenn G.S., Valanis B., and Williams Jr. J.H. The beta-carotene and retinol efficacy trial: incidence of lung cancer and cardiovascular disease mortality during 6-year follow-up after stopping beta-carotene and retinol supplements. J. Natl. Cancer Instit. 96 23 (2004) 50
4. Tylicki L., Rutkowski B., and Horl W.H. Antioxidants: a possible role in kidney protection. Kidney Blood Press Res. 26 5/6 (2003) 303-314
5. Scott J.A., and King G.L. Oxidative stress and antioxidant treatment in diabetes. Ann. NY Acad. Sci. 1031 (2004) 204-213
6. Omenn G.S., Goodman G.E., Thornquist M.D., Balmes J., Cullen M.R., Glass A., Keogh J.P., Meyskens Jr. F.L., Valanis B., Williams Jr. J.H., Barnhart S., Cherniack M.G., Brodkin C.A., and Hammar S. Risk factors for lung cancer and for intervention effects in CARET, the beta-carotene and retinol efficacy trial. J. Natl. Cancer Instit. 88 21 (1996) 1550-1559
7. Lonn E., Bosch J., Yusuf S., Sheridan P., Pogue J., Arnold J.M., Ross C., Arnold A., Sleight P., Probstfield J., and Dagenais G.R. Effects of long-term Vitamin E supplementation on cardiovascular events and cancer: a randomized controlled trial. JAMA 293 11 (2005) 1338-1347
8. Madamanchi N.R., Vendrov A., and Runge M.S. Oxidative stress and vascular disease. Arterioscler. Thromb. Vasc. Biol. 25 1 (2005) 29-38
9. Williams K.J., and Fisher E.A. Oxidation, lipoproteins, and atherosclerosis: which is wrong, the antioxidants or the theory?. Curr. Opin. Clin. Nutr. Metab. Care 8 2 (2005) 139-146
10. Sies H. Oxidative stress: introductory remarks. In: Sies H. (Ed). Oxidative Stress (1985), Academic Press, London 1-8
11. Forman H.J., Fukuto J.M., and Torres M. Redox signaling: thiol chemistry defines which reactive oxygen and nitrogen species can act as second messengers. Am. J. Physiol. Cell Physiol. 287 2 (2004) C246-C256
12. D.P. Jones, Redefining oxidative stress, Antioxid. Redox Signal, 2006.
13. H. Sies, D.P. Jones, Oxidative stress, in: Encyclopedia of Stress, Elsevier, in press.
14. Halvey P.J., Watson W.H., Hansen J.M., Go Y.M., Samali A., and Jones D.P. Compartmental oxidation of thiol-disulphide redox couples during epidermal growth factor signalling. Biochem. J. 386 Pt 2 (2005) 215-219
15. Damdimopoulos A.E., Miranda-Vizuete A., Pelto-Huikko M., Gustafsson J.A., and Spyrou G. Human mitochondrial thioredoxin. Involvement in mitochondrial membrane potential and cell death. J. Biol. Chem. 277 36 (2002) 33249-33257
16. Panov A., Dikalov S., Shalbuyeva N., Taylor G., Sherer T., and Greenamyre J.T. Rotenone model of Parkinson disease: multiple brain mitochondria dysfunctions after short term systemic rotenone intoxication. J. Biol. Chem. 280 51 (2005) 42026-42035
17. Keilin D. The History of Cell Respiration and Cytochrome (1966), Cambridge University Press, Cambridge
18. Kappus H., and Sies H. Toxic drug effects associated with oxygen metabolism: redox cycling and lipid peroxidation. Experientia 37 12 (1981) 1233-1241
19. Chance B., Holmes W., Higgins J., and Connelly C.M. Localization of interaction sites in multi-component transfer systems: theorems derived from analogues. Nature 182 4644 (1958) 1190-1193
20. Di Lisa F., Canton M., Menabo R., Dodoni G., and Bernardi P. Mitochondria and reperfusion injury. The role of permeability transition. Basic Res. Cardiol. 98 4 (2003) 235-241
21. Watson W.H., and Jones D.P. Oxidation of nuclear thioredoxin during oxidative stress. FEBS Lett. 543 1-3 (2003) 144-147
22. Hansen J.M., Go Y.M., and Jones D.P. Nuclear and mitochondrial compartmentation of oxidative stress and redox signaling. Annu. Rev. Pharmacol. Toxicol. 46 (2006) 215-234
23. Dalle-Donne I., Scaloni A., Giustarini D., Cavarra E., Tell G., Lungarella G., Colombo R., Rossi R., and Milzani A. Proteins as biomarkers of oxidative/nitrosative stress in diseases: the contribution of redox proteomics. Mass Spectrom. Rev. 24 1 (2005) 55-99
24. Turrens J.F., and Boveris A. Generation of superoxide anion by the NADH dehydrogenase of bovine heart mitochondria. Biochem. J. 191 2 (1980) 421-427
25. Takeshige K., and Minakami S. NADH- and NADPH-dependent formation of superoxide anions by bovine heart submitochondrial particles and NADH-ubiquinone reductase preparation. Biochem. J. 180 1 (1979) 129-135
26. Granger D.N., Rutili G., and McCord J.M. Superoxide radicals in feline intestinal ischemia. Gastroenterology 81 1 (1981) 22-29
27. Tribble D.L., and Jones D.P. Oxygen dependence of oxidative stress. Rate of NADPH supply for maintaining the GSH pool during hypoxia. Biochem. Pharmacol. 39 4 (1990) 729-736
28. Sies H. Nicotinamide nucleotide compartmentation. In: Sies H. (Ed). Metabolic Compartmentation (1982), Academic Press, London 205-231
29. Lambeth J.D. NOX enzymes and the biology of reactive oxygen. Nat. Rev. Immunol. 4 3 (2004) 181-189
30. Zhang R., Al-Lamki R., Bai L., Streb J.W., Miano J.M., Bradley J., and Min W. Thioredoxin-2 inhibits mitochondria-located ASK1-mediated apoptosis in a JNK-independent manner. Circ. Res. 94 11 (2004) 1483-1491
31. Chen Y., Cai J., Murphy T.J., and Jones D.P. Overexpressed human mitochondrial thioredoxin confers resistance to oxidant-induced apoptosis in human osteosarcoma cells. J. Biol. Chem. 277 36 (2002) 33242-33248
32. Burdon R.H. Superoxide and hydrogen peroxide in relation to mammalian cell proliferation. Free Radic. Biol. Med. 18 4 (1995) 775-794
33. 2-dependent activation of GCLC-ARE4 reporter occurs by mitogen-activated protein kinase pathways without oxidation of cellular glutathione or thioredoxin-1. J. Biol. Chem. 279 7 (2004) 5837-5845
34. Jones D.P., Go Y.M., Anderson C.L., Ziegler T.R., Kinkade Jr. J.M., and Kirlin W.G. Cysteine/cystine couple is a newly recognized node in the circuitry for biologic redox signaling and control. FASEB J. 18 11 (2004) 1246-1248
35. Kirlin W.G., Cai J., Thompson S.A., Diaz D., Kavanagh T.J., and Jones D.P. Glutathione redox potential in response to differentiation and enzyme inducers. Free Radic. Biol. Med. 27 11/12 (1999) 1208-1218
36. Hutter D.E., Till B.G., and Greene J.J. Redox state changes in density-dependent regulation of proliferation. Exp. Cell Res. 232 2 (1997) 435-438
37. Jonas C.R., Estivariz C.F., Jones D.P., Gu L.H., Wallace T.M., Diaz E.E., Pascal R.R., Cotsonis G.A., and Ziegler T.R. Keratinocyte growth factor enhances glutathione redox state in rat intestinal mucosa during nutritional repletion. J. Nutr. 129 7 (1999) 1278-1284
38. Samiec P.S., Drews-Botsch C., Flagg E.W., Kurtz J.C., Sternberg Jr. P., Reed R.L., and Jones D.P. Glutathione in human plasma: decline in association with aging, age-related macular degeneration, and diabetes. Free Radic. Biol. Med. 24 5 (1998) 699-704
39. Nkabyo Y.S., Ziegler T.R., Gu L.H., Watson W.H., and Jones D.P. Glutathione and thioredoxin redox during differentiation in human colon epithelial (Caco-2) cells. Am. J. Physiol. Gastrointest. Liver Physiol. 283 6 (2002) G1352-G1359
40. Armstrong J.S., Whiteman M., Yang H., Jones D.P., and Sternberg Jr. P. Cysteine starvation activates the redox-dependent mitochondrial permeability transition in retinal pigment epithelial cells. Invest. Ophthalmol. Vis. Sci. 45 11 (2004) 4183-4189
41. Miller L.T., Watson W.H., Kirlin W.G., Ziegler T.R., and Jones D.P. Oxidation of the glutathione/glutathione disulfide redox state is induced by cysteine deficiency in human colon carcinoma HT29 cells. J. Nutr. 132 8 (2002) 2303-2306
42. Hansen J.M., Watson W.H., and Jones D.P. Compartmentation of Nrf-2 redox control: regulation of cytoplasmic activation by glutathione and DNA binding by thioredoxin-1. Toxicol. Sci. 82 1 (2004) 308-317
43. Jones D.P. Extracellular redox state: refining the definition of oxidative stress in aging. Rejuvenation Res. 9 2 (2006) 169-181
44. Reed D.J., Brodie A.E., and Meredith M.J. Cellular heterogeneity in the status and functions of cysteine and glutathione. In: Larsen A.S.O., Holmgren A., and Mannervik B. (Eds). Functions of Glutathione (1983), Raven Press, New York 39-49
45. Gilbert H.F. Molecular and cellular aspects of thiol-disulfide exchange. Adv. Enzymol. Relat. Areas Mol. Biol. 63 (1990) 69-172
46. Mannervik B., Axelsson K., Sundewall A.C., and Holmgren A. Relative contributions of thioltransferase- and thioredoxin-dependent systems in reduction of low-molecular-mass and protein disulphides. Biochem. J. 213 2 (1983) 519-523
47. Ziegler D.M. Role of reversible oxidation-reduction of enzyme thiols-disulfides in metabolic regulation. Annu. Rev. Biochem. 54 (1985) 305-329
48. Moriarty-Craige S.E., and Jones D.P. Extracellular thiols and thiol/disulfide redox in metabolism. Annu. Rev. Nutr. 24 (2004) 481-509
49. Jones D.P., Carlson J.L., Mody V.C., Cai J., Lynn M.J., and Sternberg P. Redox state of glutathione in human plasma. Free Radic. Biol. Med. 28 4 (2000) 625-635
50. Jones D.P., Mody Jr. V.C., Carlson J.L., Lynn M.J., and Sternberg Jr. P. Redox analysis of human plasma allows separation of pro-oxidant events of aging from decline in antioxidant defenses. Free Radic. Biol. Med. 33 9 (2002) 1290-1300
51. Moriarty-Craige S.E., Adkison J., Lynn M., Gensler G., Bressler S., Jones D.P., and Sternberg Jr. P. Antioxidant supplements prevent oxidation of cysteine/cystine redox in patients with age-related macular degeneration. Am. J. Ophthalmol. 140 6 (2005) 1020-1026
52. Meredith M.J., and Reed D.J. Status of the mitochondrial pool of glutathione in the isolated hepatocyte. J. Biol. Chem. 257 7 (1982) 3747-3753
53. Wahllander A., Soboll S., Sies H., Linke I., and Muller M. Hepatic mitochondrial and cytosolic glutathione content and the subcellular distribution of GSH-S-transferases. FEBS Lett. 97 1 (1979) 138-140
54. Jocelyn P.C., and Kamminga A. The non-protein thiol of rat liver mitochondria. Biochim. Biophys. Acta 343 2 (1974) 356-362
55. Jocelyn P.C. Some properties of mitochondrial glutathione. Biochim. Biophys. Acta 396 3 (1975) 427-436
56. Vignais P.M., and Vignais P.V. Fuscin, an inhibitor of mitochondrial SH-dependent transport-linked functions. Biochim. Biophys. Acta 325 3 (1973) 357-374
57. Garcia-Ruiz C., Morales A., Ballesta A., Rodes J., Kaplowitz N., and Fernandez-Checa J.C. Effect of chronic ethanol feeding on glutathione and functional integrity of mitochondria in periportal and perivenous rat hepatocytes. J. Clin. Invest. 94 1 (1994) 193-201
58. Martensson J., Lai J.C., 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 18 (1990) 7185-7189
59. Lash L.H. Role of glutathione transport processes in kidney function. Toxicol. Appl. Pharmacol. 204 3 (2005) 329-342
60. Lash L.H., Putt D.A., and Matherly L.H. Protection of NRK-52E cells, a rat renal proximal tubular cell line, from chemical-induced apoptosis by overexpression of a mitochondrial glutathione transporter. J. Pharmacol. Exp. Ther. 303 2 (2002) 476-486
61. Chen Z., and Lash L.H. Evidence for mitochondrial uptake of glutathione by dicarboxylate and 2-oxoglutarate carriers. J. Pharmacol. Exp. Ther. 285 2 (1998) 608-618
62. Chen Z., Putt D.A., and Lash L.H. 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 1 (2000) 193-202
63. Shan X., Jones D.P., Hashmi M., and Anders M.W. Selective depletion of mitochondrial glutathione concentrations by (R,S)-3-hydroxy-4-pentenoate potentiates oxidative cell death. Chem. Res. Toxicol. 6 1 (1993) 75-81
64. Fernandez-Checa J.C., Ookhtens M., and Kaplowitz N. Effect of chronic ethanol feeding on rat hepatocytic glutathione. Compartmentation, efflux, and response to incubation with ethanol. J. Clin. Invest. 80 1 (1987) 57-62
65. Fernandez-Checa J.C., Ookhtens M., and Kaplowitz N. Effects of chronic ethanol feeding on rat hepatocytic glutathione. Relationship of cytosolic glutathione to efflux and mitochondrial sequestration. J. Clin. Invest. 83 4 (1989) 1247-1252
66. Fernandez-Checa J.C., Garcia-Ruiz C., Ookhtens M., and Kaplowitz N. Impaired uptake of glutathione by hepatic mitochondria from chronic ethanol-fed rats. Tracer kinetic studies in vitro and in vivo and susceptibility to oxidant stress. J. Clin. Invest. 87 2 (1991) 397-405
67. Vendemiale G., Grattagliano I., Altomare E., Turturro N., and Guerrieri F. Effect of acetaminophen administration on hepatic glutathione compartmentation and mitochondrial energy metabolism in the rat. Biochem. Pharmacol. 52 8 (1996) 1147-1154
68. Rebrin I., and Sohal R.S. Comparison of thiol redox state of mitochondria and homogenates of various tissues between two strains of mice with different longevities. Exp. Gerontol. 39 10 (2004) 1513-1519
69. Cai J., and Jones D.P. Superoxide in apoptosis. Mitochondrial generation triggered by cytochrome c loss. J. Biol. Chem. 273 19 (1998) 11401-11404
70. Sies H., and Moss K.M. A role of mitochondrial glutathione peroxidase in modulating mitochondrial oxidations in liver. Eur. J. Biochem. 84 2 (1978) 377-383
71. Enoksson M., Fernandes A.P., Prast S., Lillig C.H., Holmgren A., and Orrenius S. Overexpression of glutaredoxin 2 attenuates apoptosis by preventing cytochrome c release. Biochem. Biophys. Res. Commun. 327 3 (2005) 774-779
72. Johansson C., Lillig C.H., 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 9 (2004) 7537-7543
73. Beer S.M., Taylor E.R., Brown S.E., Dahm C.C., Costa N.J., Runswick M.J., and Murphy M.P. 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 46 (2004) 47939-47951
74. Nonn L., Berggren M., and Powis G. Increased expression of mitochondrial peroxiredoxin-3 (thioredoxin peroxidase-2) protects cancer cells against hypoxia and drug-induced hydrogen peroxide-dependent apoptosis. Mol. Cancer Res. 1 9 (2003) 682-689
75. Koehler C.M., Beverly K.N., and Leverich E.P. Redox pathways of the mitochondrion. Antioxid. Redox Signal 8 5/6 (2006) 813-822
76. Bailey S.M., Landar A., and Darley-Usmar V. Mitochondrial proteomics in free radical research. Free Radic. Biol. Med. 38 2 (2005) 175-188
77. Bota D.A., and Davies K.J. Lon protease preferentially degrades oxidized mitochondrial aconitase by an ATP-stimulated mechanism. Nat. Cell Biol. 4 9 (2002) 674-680
78. Jones D.P., Shan X., and Park Y. Coordinated multisite regulation of cellular energy metabolism. Annu. Rev. Nutr. 12 (1992) 327-343
79. Boveris A., and Chance B. The mitochondrial generation of hydrogen peroxide. General properties and effect of hyperbaric oxygen. Biochem. J. 134 3 (1973) 707-716
80. Aw T.Y., Andersson B.S., and Jones D.P. Mitochondrial transmembrane ion distribution during anoxia. Am. J. Physiol. 252 4 Pt 1 (1987) C356-C361
81. Andersson B.S., Aw T.Y., and Jones D.P. Mitochondrial transmembrane potential and pH gradient during anoxia. Am. J. Physiol. 252 4 Pt 1 (1987) C349-C355
82. Aw T.Y., Andersson B.S., and Jones D.P. Suppression of mitochondrial respiratory function after short-term anoxia. Am. J. Physiol. 252 4 Pt 1 (1987) C362-C368
83. Park Y., Devlin T.M., and Jones D.P. Protection of hepatocytes against death due to mitochondrial failure: effect of di-Calciphor on antimycin A-induced toxicity. Toxicol. Appl. Pharmacol. 126 1 (1994) 33-38
84. Park Y., Devlin T.M., and Jones D.P. Protective effect of the dimer of 16,16-diMePGB1 against KCN-induced mitochondrial failure in hepatocytes. Am. J. Physiol. 263 2 Pt 1 (1992) C405-C411
85. Armstrong J.S., Whiteman M., Yang H., and Jones D.P. The redox regulation of intermediary metabolism by a superoxide-aconitase rheostat. Bioessays 26 8 (2004) 894-900
86. Talbot D.A., Lambert A.J., and Brand M.D. Production of endogenous matrix superoxide from mitochondrial complex I leads to activation of uncoupling protein 3. FEBS Lett. 556 1-3 (2004) 111-115
87. Echtay K.S., Murphy M.P., Smith R.A., Talbot D.A., and Brand M.D. Superoxide activates mitochondrial uncoupling protein 2 from the matrix side. Studies using targeted antioxidants. J. Biol. Chem. 277 49 (2002) 47129-47135
88. Echtay K.S., Roussel D., St-Pierre J., Jekabsons M.B., Cadenas S., Stuart J.A., Harper J.A., Roebuck S.J., Morrison A., Pickering S., Clapham J.C., and Brand M.D. Superoxide activates mitochondrial uncoupling proteins. Nature 415 6867 (2002) 96-99
89. Guidot D.M., Repine J.E., Kitlowski A.D., Flores S.C., Nelson S.K., Wright R.M., and McCord J.M. Mitochondrial respiration scavenges extramitochondrial superoxide anion via a nonenzymatic mechanism. J. Clin. Invest. 96 2 (1995) 1131-1136
90. J.M. Hansen, H. Zhang, D.P. Jones, Mitochondrial thioredoxin-2 has a key role in determining tumor necrosis factor-{alpha}-induced ROS generation, NF-{kappa}B activation and apoptosis, Toxicol. Sci., in press.
91. Kim J.R., Lee S.M., Cho S.H., Kim J.H., Kim B.H., Kwon J., Choi C.Y., Kim Y.D., and Lee S.R. Oxidation of thioredoxin reductase in HeLa cells stimulated with tumor necrosis factor-alpha. FEBS Lett. 567 2/3 (2004) 189-196
92. Hansen J.M., Zhang H., and Jones D.P. Differential oxidation of thioredoxin-1, thioredoxin-2, and glutathione by metal ions. Free Radic. Biol. Med. 40 1 (2006) 138-145
93. Dooley C.T., Dore T.M., Hanson G.T., Jackson W.C., Remington S.J., and Tsien R.Y. Imaging dynamic redox changes in mammalian cells with green fluorescent protein indicators. J. Biol. Chem. 279 21 (2004) 22284-22293
94. Hanson G.T., Aggeler R., Oglesbee D., Cannon M., Capaldi R.A., Tsien R.Y., and Remington S.J. Investigating mitochondrial redox potential with redox-sensitive green fluorescent protein indicators. J. Biol. Chem. 279 13 (2004) 13044-13053
95. Di Lisa F., and Bernardi P. Mitochondrial function and myocardial aging. A critical analysis of the role of permeability transition. Cardiovasc. Res. 66 2 (2005) 222-232
96. Kagan V.E., Borisenko G.G., Tyurina Y.Y., Tyurin V.A., Jiang J., Potapovich A.I., Kini V., Amoscato A.A., and Fujii Y. Oxidative lipidomics of apoptosis: redox catalytic interactions of cytochrome c with cardiolipin and phosphatidylserine. Free Radic. Biol. Med. 37 12 (2004) 1963-1985
97. Loeb L.A., Wallace D.C., and Martin G.M. The mitochondrial theory of aging and its relationship to reactive oxygen species damage and somatic mtDNA mutations. Proc. Natl. Acad. Sci. U.S.A. 102 52 (2005) 18769-18770
98. 2+. Magn. Reson. Chem. 39 4 (2001) 207-211
99. Baines C.P., Kaiser R.A., Purcell N.H., Blair N.S., Osinska H., Hambleton M.A., Brunskill E.W., Sayen M.R., Gottlieb R.A., Dorn G.W., Robbins J., and Molkentin J.D. Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 434 7033 (2005) 658-662
100. Nakagawa T., Shimizu S., Watanabe T., Yamaguchi O., Otsu K., Yamagata H., Inohara H., Kubo T., and Tsujimoto Y. Cyclophilin D-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death. Nature 434 7033 (2005) 652-658
101. Kokoszka J.E., Waymire K.G., Levy S.E., Sligh J.E., Cai J., Jones D.P., MacGregor G.R., and Wallace D.C. The ADP/ATP translocator is not essential for the mitochondrial permeability transition pore. Nature 427 6973 (2004) 461-465
102. Costantini P., Chernyak B.V., Petronilli V., and Bernardi P. Modulation of the mitochondrial permeability transition pore by pyridine nucleotides and dithiol oxidation at two separate sites. J. Biol. Chem. 271 12 (1996) 6746-6751
103. Costantini P., Belzacq A.S., Vieira H.L., Larochette N., de Pablo M.A., Zamzami N., Susin S.A., Brenner C., and Kroemer G. Oxidation of a critical thiol residue of the adenine nucleotide translocator enforces Bcl-2-independent permeability transition pore opening and apoptosis. Oncogene 19 2 (2000) 307-314
104. Stocker R., and Keaney Jr. J.F. Role of oxidative modifications in atherosclerosis. Physiol. Rev. 84 4 (2004) 1381-1478
105. Cantin A.M. Potential for antioxidant therapy of cystic fibrosis. Curr. Opin. Pulm. Med. 10 6 (2004) 531-536
106. Bonnefont-Rousselot D. The role of antioxidant micronutrients in the prevention of diabetic complications. Treat Endocrinol. 3 1 (2004) 41-52
107. Vina J., Lloret A., Orti R., and Alonso D. Molecular bases of the treatment of Alzheimer's disease with antioxidants: prevention of oxidative stress. Mol. Aspects Med. 25 1/2 (2004) 117-123
108. Berger M.M. Can oxidative damage be treated nutritionally?. Clin. Nutr. 24 2 (2005) 172-183
109. Sun J., Molitor J., and Tower J. Effects of simultaneous over-expression of Cu/ZnSOD and MnSOD on Drosophila melanogaster life span. Mech. Ageing Develop. 125 5 (2004) 341-349
110. Erecinska M., and Wilson D.F. Inhibitors of Mitochondrial Function (1981), Pergamon Press, Oxford