Molecular and Cellular Biochemistry

, Volume 174, Issue 1–2, pp 305–319

Reactive oxygen species, mitochondria, apoptosis and aging

  • S. Papa
  • V.P. Skulachev
Article

Abstract

In this paper, we shall review various antioxygen defense systems of the cell paying particular attention to those that prevent superoxide formation rather than scavenge already formed superoxide and its products. The role of uncoupled, decoupled and non-coupled respiration, mitochondrial pore, mitochondrion-linked apoptosis will be considered. Mitochondrial theory of aging will be regarded in context of reactive oxygen species-induced damage of mitochondrial DNA. (Mol Cell Biochem 174: 305–319, 1997)

mitochondrial metabolism mitochondrial DNA superoxide radicals 

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References

  1. 1.
    Halliwell B: Reactive oxygen species and the central nervous system. In: L Packer, L Prilipko, Y Christen (eds). Free Radicals in the Brain, Springer-Verlag, Berlin, 1992, pp 21–40Google Scholar
  2. 2.
    Shigenaga MK, Hagen TM, Ames BN: Oxidative damage and mitochondrial decay in aging. Proc Nat Acad Sci USA 91: 10771–10778, 1994Google Scholar
  3. 3.
    Luft R: The development of mitochondrial medicine. Proc Nat Acad Sci USA 91: 8731–8738, 1994Google Scholar
  4. 4.
    Trischler H-J, Packer L, Medori R: Oxidative stress and mitochondria dysfunction in neurodegeneration. Biochem Mol Biol Intern 34: 169–180, 1994Google Scholar
  5. 5.
    Wikström M, Krab K, Saraste M: Cytochrome Oxidase – A Synthesis. Acad Press, London, 1981Google Scholar
  6. 6.
    Boveris A, Chance B: The mitochondrial generation of hydrogen peroxide. General properties and effect of hyperbaric oxygen. Biochem J 134: 707–716, 1973Google Scholar
  7. 7.
    Laurindo FRM, da Luz PL, Uint L, Rocha TF, Jaeger RG, Lopes EA: Evidence for superoxide radical-dependent coronary vasospasm after angioplasty in intact dogs. Circulation 83: 1705–1715, 1991Google Scholar
  8. 8.
    Dalton H, Postgate JP: Growth and physiology of Azotobacter ehroococcum in continuous cultures. J Gen Microbiol 56: 307–319, 1969aGoogle Scholar
  9. 9.
    Dalton H, Postgate JP: Effect of oxygen on growth of Azotobacter ehroococcum in batch and continuous cultures. J Gen Microbiol 54: 463–473, 1969bGoogle Scholar
  10. 10.
    Hoffman P, Morgan TV, Der Vartanian DV: Respiratory-chain characteristics of mutants of Azatobacter vinelandii negative to tetramethylp-phenylenediamine oxidase. Eur J Biochem 100: 19–27, 1979Google Scholar
  11. 11.
    Hoffman P, Morgan TV, Der Vartanian DV: Respiratory properties of cytochrome-c-deficient mutants of Azotobacter vinelandii. Eur J Biochem 110: 349–354, 1980Google Scholar
  12. 12.
    Kelly MJS, Poole RK, Yates MG, Kenney C: Cloning and mutagenesis of genes encoding the cytochrome bd terminal oxidase complex in Azotobacter vinelandii: mutants deficient in the cytochrome d complex are unable to fix nitrogen in air. J Bacteriol 172: 6010–6019, 1990Google Scholar
  13. 13.
    Poole RK: Oxygen reactions with bacterial oxidases and globins: binding, reduction and regulation. Antonie van Leeuwenhoek 65: 289–310, 1994Google Scholar
  14. 14.
    Puustinen A, Finel M, Virkki M, Wikström M: Cytochrome o (bo) is a proton pump in Paracoccus denitrificans and Escherichia coli. FEBS Lett 249: 163–167, 1989Google Scholar
  15. 15.
    Puustinen A, Finel M, Haltia T, Gennis RB, Wikström M: Properties of the two terminal oxidases of Escherichia coli. Biochemistry 30: 3936–3942, 1991Google Scholar
  16. 16.
    Verkhovskaya M, Verkhovsky M, Wikström M: pH Dependence of proton translocation by Escherichia coli. J Biol Chem 267: 14559–14562, 1992Google Scholar
  17. 17.
    Dassa J, Fsihi H, Marck C, Dion M, Kieffer-Bontemps M, Boquet PL: A new oxygen-regulated operon in Escherichia coli comprises the genes for a putative third cytochrome oxidase and for pH 2.5 acid phosphatase (appA). Mol Gen Genet 229: 341–352, 1991Google Scholar
  18. 18.
    Douce R, Neuburger M: The uniqueness of plant mitochondria. Annu Rev Plant Physiol Plant Mol Biol 40: 371–414, 1989Google Scholar
  19. 19.
    Skulachev VP: Membrane Bioenergetics, Springer, Berlin, 1988Google Scholar
  20. 20.
    Van den Bergen CWM, Wagner AM, Krab K, Moore AL: The relationship between electron flux and the redox poise of the quinone pool in plant mitochondria. Eur J Biochem 226: 1071–1078, 1994Google Scholar
  21. 21.
    Ribas-Carbo M, Berry JA, Azcon-Bieto J, Siedow JN: The reaction of the plant mitochondrial cyanide-resistant alternative oxidase with oxygen. Biochim Biophys Acta 1188: 205–212, 1994Google Scholar
  22. 22.
    Pietrobon D, Zoratti M, Azzone GF: Molecular slipping in redox and ATPase H+ pumps. Biochim Biophys Acta 723: 317–321, 1983Google Scholar
  23. 23.
    Blair DF, Gelles J, Chan SI: Redox linked proton translocation in cytochrome oxidase: the importance of gating electron flow. Biophys J 50: 713–733, 1986Google Scholar
  24. 24.
    Papa S, Lorusso M, Capitanio N: Mechanistic and phenomenological features of proton pumps in the respiratory chain of mitochondria. J Bioenerg Biomemb 26: 609–618, 1994Google Scholar
  25. 25.
    Luvisetto S, Conti E, Buss M, Az zone GF: Flux ratios and pump stoichiometries at site-II and site-III in liver mitochondria – Effect of slips and leaks. J Biol Chem 266: 1034–1042, 1991Google Scholar
  26. 26.
    Brown GC: The relative proton stoicheiometries of the mitochondrial proton pumps are independent on the proton motive force. J Biol Chem 264: 14704–14709, 1989Google Scholar
  27. 27.
    Papa S, Capitanio N, Capitanio G, De Nitto E, Minuto M: The cytochrome chain exhibits variable H+/e– stoichiometry. FEBS Lett 280: 183–186, 1991Google Scholar
  28. 28.
    Capitanio N, Capitanio G, De Nitto E, Villani G, Papa S: H+/e– stoichiometry of mitochondrial cytochrome complexes reconstituted in liposomes. Rate dependent changes of the stoichiometry in the cytochrome c oxidase vesicles. FEBS Lett 288: 179–182, 1991Google Scholar
  29. 29.
    Babcock GT, Wikström MKF: Oxygen activation and the conservation of energy in cell respiration. Nature 356: 301–309, 1992Google Scholar
  30. 30.
    Cocco T, Lorusso M, Di Paola M, Minuto M, Papa S: Characteristics of energy-linked proton translocation in liposome reconstituted bovine cytochrome bc1 complex. Influence of the protonmotive force on the H+/e– stoichiometry. Eur J Biochem 209: 475–481, 1992Google Scholar
  31. 31.
    Turrens JF, Zeman BA, Levitt JG, Crapo JD: The effect of hyperoxia on superoxide production by lung submitochondrial particles. Arch Biochem Biophys 217: 401–410, 1982Google Scholar
  32. 32.
    Ksenzenko MYu, Konstantinov AA, Tikhonov AN, Ruuge EK: Inhibition of H2O2 and O2·– generation in British anti-Lewisite-treated respiratory chain. Bickhimiya 47: 1577–1579 (Russ.), 1982Google Scholar
  33. 33.
    Ksenzenko MYu, Konstantinov AA, Khomutov GB, Ruuge EK: Studies of superoxide radical generation in the NADH:ubiquinone-reductase segment of the respiratory chain with the aid of a spin probe 2,2,6,6-tetramethyl-4-oxopiperidine-N-oxyl. Biol Membrany 6: 840–849 (Russ.), 1989Google Scholar
  34. 34.
    Konstantinov AA, Peskin AV, Popova EYu, Khomutov GB, Ruuge EK: Superoxide generation by the respiratory chain of tumor mitochondria. Biochim Biophys Acta 894: 1–10, 1987Google Scholar
  35. 35.
    Cross AR, Jones OTG: Enzymatic mechanisms of superoxide production. Biochim Biophys Acta 1057: 281–298, 1991Google Scholar
  36. 36.
    Kashkarov KP, Vasilyeva EV, Ruuge EK: Superoxide radical generation by the mitochondrial respiratory chain of isolated cardiomyocytes. Biochemistry (Moscow) 59: 813–818 (Russ), 1994Google Scholar
  37. 37.
    Massey V: Activation of molecular oxygen by flavins and flavoproteins. J Biol Chem 269: 22459–22462, 1994Google Scholar
  38. 38.
    Turrens JS, Boveris A: Generation of superoxide anion by the NADH debydrogenase of bovine heart mitochondria. Biochem J 191: 421–427, 1980Google Scholar
  39. 39.
    Okuda M, Lee H-C, Kumar C, Chance B: Comparison of the effect of a mitochondrial uncoupler, 2,4-dinitrophenol and adrenaline on oxygen radical production in the isolated perfused rat liver. Acta Physiol Scand 145: 159–168, 1992Google Scholar
  40. 40.
    Kotlyar AB, Sled VD, Burbaev DS, Moroz JA, Vinogradov AD: Coupling site and rotenone-sensitive ubisemiquinone in tightly coupled submitochondrial particles. FEBS Lett 264: 17–20, 1990Google Scholar
  41. 41.
    Vinogradov AD, Sled VD, Burbaev DS, Grivennikova VG, Moroz IA, Ohnishi T: Energy-dependent complex I-associated ubisemiquinones in submitochondrial particles. FEBS Lett 370: 83–87, 1995Google Scholar
  42. 42.
    Liu SS, Huang JP: Co-existence of reactive oxygen cycle with Qcycle in respiratory chain – a hypothesis for generation, partitioning and functioning of O2·– in mitochondria. In: D Moores (ed). Proc. of Intern. Symp. on Natural Antioxidands: Molecular Mechanisms and Health Effects. AOCS Press, Champaign, IL, 1996, (in press)Google Scholar
  43. 43.
    Skulachev VP: Lowering of the intracellular O2·– concentration as a special function of respiratory systems of the cells. Biochemistry (Moscow) 59: 1910–1912 (Russ), 1994Google Scholar
  44. 44.
    Skulachev VP: Non-phosphorylating respiration as a mechanism to minimize formation of reactive oxygen species in the cell. Mol Biologiya 29: 709–715 (Russ), 1995Google Scholar
  45. 45.
    Skulachev VP: The role of nonphosphorylating respiration in minimizing formation of reactive oxygen species. J Mol Med 73: B55, 1995Google Scholar
  46. 46.
    Skulachev VP: Role of uncoupled and non-coupled oxidations in maintenance of safely low levels of oxygen and its one-electron reductants. Quart Rev Biophys 29: 169–202, 1996Google Scholar
  47. 47.
    Rolfe DFS, Brand MD: The contribution of mitochondrial proton leak to basal metabolic rate in the rat. 8th Europ Bioenerg Conf Abstr (Valencia), 1994, p 101Google Scholar
  48. 48.
    Nicholls DG: The influence of respiration and ATP hydrolysis on the proton-electrochemical gradient across the inner membrane of rat-liver mitochondria as determined by ion distribution. Eur J Biochem 50: 305–315, 1974Google Scholar
  49. 49.
    Murphy MP: Slip and leak in mitochondrial oxidative phosphorylation. Biochim Biophys Acta 977: 123–141, 1989Google Scholar
  50. 50.
    Soboll S: Thyroid hormone action on mitochondrial energy transfer. Biochim Biophys Acta 1144: 1–16, 1993Google Scholar
  51. 51.
    Harper M-E, Brand MD: The quantitative contributions of mitochondrial proton leak and ATP turnover reactions to the changed respiration rates of hepatocytes from rats of different thyroid status. J Biol Chem 268: 14850–14860, 1993Google Scholar
  52. 52.
    Harper M-E, Ballantyne JS, Leach M, Brand MD: Effects of thyroid hormones on oxidative phosphorylation. Biochem Soc Trans 21: 785–792, 1993Google Scholar
  53. 53.
    Horst C, Rokos H, Seitz HJ: Rapid stimulation of hepatic oxygen consumption by 3,5-iodo-L-thyronine. Biochem J 261: 945–950, 1989Google Scholar
  54. 54.
    Brand MD: The proton leak across the mitochondrial inner membrane. Biochim Biophys Acta 1018: 128–133, 1990Google Scholar
  55. 55.
    Horrum M A, Tobin RB, Ecklund RE: Effects of 3,3′,5-triiodo-L-thyronine (L-T3) and T3 analogues on mitochondrial function. Biochem Mol Biol Intern 35: 913–920, 1995Google Scholar
  56. 56.
    Lanni A, Moreno M, Cioffi M, Goglia F: Effect of 3,3′-di-iodothyronine and 3,5-di-iodothyronine on rat liver mitochondria. J Endocrynol 136: 59–64, 1993Google Scholar
  57. 57.
    Teare JP, Greenfild SM, Marway JS, Preedy VR, Punchard NA, Peters TJ, Thompson RP: Effect of thyroidectomy and adrenalectomy on changes in liver glutathione and malonaldehyde levels after ethanol injection. Free Radic Biol Med 14: 655–660, 1993Google Scholar
  58. 58.
    Sterling K: Direct thyroid hormone activation of mitochondria: the role of adenine nucleotide translocase. Endocrinology 119: 292–295, 1986Google Scholar
  59. 59.
    Sterling K: Direct thyroid hormone activation of mitochondria: identification of adenine nucleotide translocase (AdNT) as the hormone receptor. Transact Ass Am Physicians 100: 284–293, 1987Google Scholar
  60. 60.
    Sterling K: Thyroid hormone action: identification of the mitochondrial thyroid hormone receptor as adenine nucleotide translocase. Thyroid 1: 167–171, 1991Google Scholar
  61. 61.
    Rasmussen UB, Kohrle J, Rokos H, Hesch R-D: Thyroid hormone effect on rat heart mitochondrial proteins and affinity labelling with N-bromoacetyl-3,3′,5-triiodo-L-thyronine. Lack of direct effect on the adenine nucleotide translocase. FEBS Lett 255: 385–390, 1989Google Scholar
  62. 62.
    Brand MD, Steverding D, Kadenbach B, Stevenson PM, Hafner RP: The mechanism of the increase in mitochondrial proton permeability induced by thyroid hormones. Eur J Biochem 296: 775–781, 1992Google Scholar
  63. 63.
    Terada H: Some biochemical and physicochemical properties of the potent uncoupler SF 6847 (3,5-ditert-butyl-4-hydroxy-benzylidenemalononitrile). Biochim Biophys Acta 387: 519–532, 1975Google Scholar
  64. 64.
    Terada H: The interaction of highly active uncouplers with mitochondria. Biochim Biophys Acta 639: 225–242, 1981Google Scholar
  65. 65.
    Terada H, Fukui Y, Shinohara Y, Ju-chi M: Unique action of a modified weakly acidic uncoupler without an acidic group, methylated SF 6847, as an inhibitor of oxidative phosphorylation with no uncoupling activity: possible identity of uncoupler binding protein. Biochim Biophys Acta 933: 193–199, 1988Google Scholar
  66. 66.
    Luvisetto S, Schmehl I, Intravaia E, Conti E, Azzone GF: Mechanism of loss of thermodynamic control in mitochondria due to hyperthyroidism and temperature. J Biol Chem 267: 15348–15355, 1992Google Scholar
  67. 67.
    Starkov AA, Dedukhova VI, Bloch DA, Severina II, Skulachev VP: Some male sex hormones, progesterone and 6-ketocholestanol counteract uncoupling effects of low concentrations of the most active protonophores. In: F Palmieri et al. (ed). Thirty Years of Progress in Mitochondrial Bioenergetics and Molecular Biology, Elsevier, Amsterdam, 1995, pp 51–55Google Scholar
  68. 68.
    Miyoshi H, Fujita T: Quantitative analyses of uncoupling activity of SF6846 (2,6-di-t-butyl-4-(2,2-dicyanovinyl)phenol) and its analogs with spinach chloroplasts. Biochim Biophys Acta 894: 339–345, 1987Google Scholar
  69. 69.
    Starkov AA, Dedukhova VI, Skulachev VP: 6-Ketocholestanol abolishes the effect of the most potent uncouplers of oxidative phosphorylation in mitochondria. FEBS Lett 355: 305–308, 1994Google Scholar
  70. 70.
    Bernassau JM, Reversat JL, Ferrara P, Caput D, Lefur G: A 3D model of the peripheral benzodiazepine receptor and its implication in intramitochondrial cholesterol transport. J Mol Graphics 11: 236–244, 1993Google Scholar
  71. 71.
    Hall PF: Cellular organization for steroidogenesis. Int Rev Cytology 86: 53–95, 1984Google Scholar
  72. 72.
    Yanagibashi K, Ohno Y, Kazwamura M, Hall PF: The regulation of intracellular transport of cholesterol in bovine adrenal cells: purification of a novel protein. Endocrinology 123: 2075–2082, 1988Google Scholar
  73. 73.
    Krueger KE: Molecular and functional properties of mitochondrial benzodiazepine receptors. Biochim. Biophys. Acta 1241: 453–470, 1995Google Scholar
  74. 74.
    Kragie L, Smiehorowski R: Altered peripheral benzodiazepine receptor binding in cardiac and liver tissues from thyroidectomized rats. Life Sci 55: 1911–1918, 1994Google Scholar
  75. 75.
    Gunter TE, Gunter KK, Sheu S-S, Gavin CE: Mitochondrial calcium transport: physiological and pathological relevance. Am J Physiol 267: C313–C339, 1994Google Scholar
  76. 76.
    Bernardi P, Broekemeier KM, Pfeiffer DR: Recent progress on regulation of the mitochondrial permeability transition pore; a cyclosporinsensitive pore in the inner mitochondrial membrane. J Bioenerg Biomembr 26: 509–517, 1994Google Scholar
  77. 77.
    Zoratti M, Szabo I: The mitochondrial permeability transition. Biochim Biophys Acta 1241: 139–176, 1995Google Scholar
  78. 78.
    Lotscher HR, Winterhalter KH, Carafoli E, Richter C: Hydroperoxides can modulate the redox state of pyridine nucleotides and the calcium balance in rat liver mitochondria. Proc Nat Acad Sci USA 76: 4340–4344, 1979Google Scholar
  79. 79.
    Carbonera D, Azzone GF: Permeability of inner mitochondrial membrane and oxidative stress. Biochim Biophys Acta 943: 245–255, 1988Google Scholar
  80. 80.
    Harris EJ, Booth R, Cooper MB: The effect of superoxide generation on the ability of mitochondria to take up and retain Ca2+. FEBS Lett 146: 267–272, 1982Google Scholar
  81. 81.
    Eriksson O: Effects of the general anaesthetic Propotol on the Ca2+-induced permeabilization of rat liver mitochondria. FEBS Lett 279: 45–48, 1991Google Scholar
  82. 82.
    Chacon E, Acosta D: Mitochondrial regulation of superoxide by Ca2+: an alternative mechanism for the cardiotoxicity of doxorubicin. Toxicol Appl Pharmacol 107: 117–128, 1991Google Scholar
  83. 83.
    Paraidathathu T, DeGroot H, Kehrer JP: Production of reactive oxygen by mitochondria from normoxic and hypoxic rat heart tissue. Free Rad Biol Med 13: 289–297, 1992Google Scholar
  84. 84.
    Bernardi P: Modulation of the mitochondrial cyclosporin A-sensitive permeability transition pore by the proton electrochemical gradient. J Biol Chem 267: 8834–8839, 1992Google Scholar
  85. 85.
    Petronilli V, Costantini P, Scorrano L, Colonna R, Passamonti S, Bernardi P: The voltage sensor of the mitochondrial permeability transition pore is tuned by the oxidation-reduction state of vicinal thiols. Increase of the gating potential by oxidants and its reversal by reducing agents. J Biol Chem 269: 16638–16642, 1994Google Scholar
  86. 86.
    Giron-Calle J, Zwizinski CW, Schmid HHO: Peroxidative damage to cardiac mitochondria. Arch Biochem Biophys 315: 1–7, 1994Google Scholar
  87. 87.
    Gardner PR, Raineri I, Epstein LB, White CW: Superoxide radical and iron modulate aconitase activity in mammalian cells. J Biol Chem 270: 13399–13405, 1995Google Scholar
  88. 88.
    Beinert H, Kennedy MC: Aconitase, a two-faced protein: enzyme and iron regulatory factor. FASEB J 7: 1442–1449, 1993Google Scholar
  89. 89.
    Grigolava IV, Ksenzenko Myu, Konstantinov AA, Tikhonov AN, Kerimov TM, Ruuge EK: Tiron as a spintrap for superoxide radicals produced by the respiratory chain of submitochondrial particles. Biokhimiya 45: 75–82 (Russ.), 1980Google Scholar
  90. 90.
    Yaguzhinsky LS, Smirnova EG, Ratnikova LA, Kolesova GM, Krasinskaya IP: Hydrophobic sites of the mitochondrial electron transfer system. J Bioenerg Biomembr 5: 163–174, 1973Google Scholar
  91. 91.
    Kane DJ, Sarafian TA, Anton R, Hahn H, Gralla EB, Valentine JS, Ord T, Bredesen DE: Bcl-2 inhibition of neural death – decreased generation of reactive oxygen species. Science 262: 1274–1277, 1993Google Scholar
  92. 92.
    Hockenbery DM, Nunez G, Milliman CT, Schreiber RD, Korsmeyer SJ: Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death. Nature 348: 334–336, 1990Google Scholar
  93. 93.
    Hockenbery DM, Oltvai ZN, Yin X-M, Milliman CT, Korsmeyer SJ: Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell 75: 241–251, 1993Google Scholar
  94. 94.
    Monaghan P, Robertson D, Amos TAS, Dyer MJS, Mason DY, Greaves MF: Ultrastructural localization of Bcl-2 protein. J Histochem Cytochem 40: 1819–1825, 1992Google Scholar
  95. 95.
    Jacobson MD, Burne JF, King MP, Miyashita T, Reed JC, Raff MC: Bcl-2 blocks apoptosis in cells lacking mitochondrial DNA. Nature 361: 365–369, 1993Google Scholar
  96. 96.
    Krajewski S, Tanaka S, Takayama S, Schibler MJ, Fenton W, Reed JC: Investigation of the subcellular distribution of the Bcl-2 oncoprotein residence in the nuclear envelope, endoplasmic reticulum, and outer mitochondrial membranes. Cancer Res 53: 4701–4714, 1993Google Scholar
  97. 97.
    Gonzalez-Garcia M, Perez-Ballestero R, Ding L, Duan L, Boise LH: bcl-xL is the major bcl-x mRNA form expressed during murine development and its product localizes to mitochondria. Development 120: 3033–3042, 1994Google Scholar
  98. 98.
    Newmeyer DD, Forschon DM, Reed JC: Cell-free apoptosis in Xenopus egg extracts: inhibition by Bcl-2 and requirement for an organelle fraction enriched in mitochondria. Cell 79: 353–364, 1994Google Scholar
  99. 99.
    Slater AFG, Orrenius S: Oxidative stress and apoptosis. In: RG Cutler, L Packer, J Bertram, A Mori (eds). Oxidative Stress and Aging. Birkhauser Verlag, Basel, 1995, pp 21–25Google Scholar
  100. 100.
    Petit PX, Lecoeur H, Zorn E, Dauguet C, Mignotte B, Gougeon ML: Alterations in mitochondrial structure and function are early events of dexamethasone-induced thymocyte apoptosis. J Cell Biol 130: 157–167, 1995Google Scholar
  101. 101.
    Richter C, Schweizer M, Cossarizza A, Franceschi C: Control of apoptosis by the cellular ATP level. FEBS Lett 378: 107–110, 1996Google Scholar
  102. 102.
    Wolvetang EJ, Johnson KL, Krauer K, Ralph SJ, Linnane AW: Mitochondrial respiratory chain inhibitors induced apoptosis. FEBS Lett 339: 40–44, 1994Google Scholar
  103. 103.
    Yoneda M, Katsumata K, Hayakawa M, Tanaka M, Ozawa T: Oxygen stress induces an apoptotic cell death associated with fragmentation of mitochondrial genome. Biochim Biophys Res Commun 209: 723–729, 1995Google Scholar
  104. 104.
    Zamzami N, Marchetti P, Castedo M, Hirsch T, Susin S, Masse B, Kroemer G: Inhibitors of permeability transition interfere with the disruption of the mitochondrial transmembrane potential during apoptosis. FEBS Lett 384: 53–57, 1996Google Scholar
  105. 105.
    Marchetti P, Susin SA, Decaudin D, Gamen S, Castedo M, Hirsch T, Zamzami N, Naomi Y, Senik A, Kroemer G: Apoptosis-associated derangement of mitochondrial function in cells lacking mitochondrial DNA. Cancer Research 56: 2033–2038, 1996Google Scholar
  106. 106.
    Zamzami N, Susin SA, Marchetti P, Hirsch T, Gomez-Monterrey, Castedo M, Kroemer G: Mitochondrial control of nuclear apoptosis. J Exp Med 183: 1533–1544, 1996Google Scholar
  107. 107.
    Miquel J, Fleming J: Mod Aging Res 8: 51–74, 1986Google Scholar
  108. 108.
    Kitagawa T, Suganuma N, Nawa A, Kikkava F, Tanaka M, Ozawa T, Tomoda Y: Rapid accumulation of deleted mitochondrial deoxyribonucleic acid in postmenopausal ovaries. Biol Reprod 49: 730–736, 1993Google Scholar
  109. 109.
    Luft R: The development of mitochondrial medicine. Biochim Biophys Acta 1271: 1–6, 1995Google Scholar
  110. 110.
    Harman D: J Gerontol 11: 298–306, 1956Google Scholar
  111. 111.
    Stadtman ER: Protein oxidation and Aging. Science, 1220–1224, 1992Google Scholar
  112. 112.
    Ames BA, Shingenaga MK, Park EM: In: KJA Davies (ed). Oxidation Damage and Repair, Chemical, Biological and Medical Aspects. Pergamon, Elmsford, New York, 1991, pp 181–187Google Scholar
  113. 113.
    Toyokuni S, Okamoto K, Yodoi J, Hiai H: Persistent oxidative stress in cancer. FEBS Lett 358: 1–3, 1995Google Scholar
  114. 114.
    Lezza AMS, Boffoli D, Scacco S, Cantatore P, Gadaleta MN: Correlation between mitochondrial DNA 4977-bp deletion and respiratory chain enzyme activities in aging human skeletal muscles. Biochem Biophys Res Commun 205: 772–779, 1994Google Scholar
  115. 115.
    Miquel J: The mitochondrial DNA injury theory of aging: concepts and supporting facts. Abstr of Intern Symp Genetics of Death, Glasgow, 1995Google Scholar
  116. 116.
    Schapira AHV: Mitochondria, free radicals, neurodegeneration and aging. In: RG Cutler, L Packer, J Bertram, A Mori (eds). Oxidative 319 Stress and Aging. Birkhauser Verlag, Basel, 1995, pp 159–169Google Scholar
  117. 117.
    Wong GHW: Protective roles of cytokines against radiation: induction of mitochondrial MnSOD. Biochim Biophys Acta 1271: 205–209, 1995Google Scholar
  118. 118.
    Cortopassi G, Wang E: Modelling the effects of age-related mtDNA mutation accumulation; complex I deficiency, superoxide and cell death. Biochim Biophys Acta 1271: 171–176, 1995Google Scholar
  119. 119.
    Guidot DM, McCord JM, Wright RM, Repine JE: Absence of electron transport (Rho° State) restores growth of a manganese – superoxide dismutase – deficient Saccharomyces cerevisiae in hyperoxia. J Biol Chem 268: 26699–26703, 1993Google Scholar
  120. 120.
    Nagley P, Linnane AW, Zhang C, Liu VWS, Baumer A, Munday AD, Sriratana A, Wolvetang EJ, Lawen A, Hill JS, Kahl SB: Mitochondrial genetic damage and functional decline during ageing and oxidative stress. Abstr of Intern Symp Genetics of Death, Glasgow, 1995Google Scholar
  121. 121.
    Orr WC, Sohal RS: Extension of life-span by overexpression of superoxide dismutase and catalase in Drosophila melanogaster. Science 263: 1128–1130, 1994Google Scholar
  122. 122.
    Johnson TE, Lithgow GL, Murakami S, Tedesco PM, Dubon SA, Shook D, White TM, Melov S: Dissection of the physiology of longlived mutants of C. elegans. Abstr of Intern Symp Genetics of Death, Glasgow, 1995Google Scholar
  123. 123.
    Sohal RS, Agarwal A, Agarwal S, Orr WC: Simultaneous overexpression of copper-and zinc-containing superoxide dismutase and catalase retards age-related oxidative damage and increases metabolic potential in Drosophila melanogaster. J Biol Chem 270: 15671–15674, 1995Google Scholar
  124. 124.
    Laganiere S, Yu BP: Modulation of membrane phospholipid fatty acid composition by age and food restriction. Gerontology 39: 7–18, 1993Google Scholar
  125. 125.
    Robinson NC, Strey F, Talbert L: Investigation of the essential boundary layer phospholipids of cytochrome c oxidase using Triton X-100 delipidation. Biochemistry 19: 3656–3661, 1980Google Scholar
  126. 126.
    Hoch FL: Cardiolipins and biomembrane function. Biochim Biophys Acta 1113, 71–133, 1992Google Scholar
  127. 127.
    Krämer R, Palmieri F: Molecular aspects of isolated and reconstituted carrier proteins from animal mitochondria. Biochim Biophys Acta 974: 1–23, 1989Google Scholar
  128. 128.
    van den Bergh JJm, Op den Kamp JA, Lubin BH, Kuypers FA: Conformational changes in oxidized phospholipids and their preferential hydrolysis by phospholipase A2: a monolayer study. Biochemistry 32: 4962–4967, 1993Google Scholar
  129. 129.
    Hatch GM, Vance DE, Wilton DC: Rat liver mitochondrial phospholipase A2 is an endotoxin-stimulated membrane-associated enzyme of Kupifer cells which is released during liver perfusion. Biochem J 293: 143–150, 1993Google Scholar
  130. 130.
    Guerrieri F, Capozza G, Kalous M, Zanotti F, Drahota Z, Papa S: Age-dependent changes in the mitochondrial F0F1 ATP synthase. Arch Gerontol Geriatr 14: 299–308, 1992Google Scholar
  131. 131.
    Guerrieri F, Capozza G, Kalous M, Papa S: Age-related changes of mitochondrial F0F1 ATP synthase. In: Ion-Motive ATPase: Structure, Function and Regulation. Ann New York Acad Sci 671: 395–402, 1992Google Scholar
  132. 132.
    Guerrieri F, Capozza G, Fratello A, Zanotti F, Papa S, Age-dependent alterations of F0F1 ATP synthase in various tissues. Cardioscience 4, 93–98, 1993Google Scholar
  133. 133.
    Markossian KA, Poghossian AA, Paitian NA, Nalbandyan RM: Superoxide dismutase activity of cytochrome oxidase. Biochem Biophys Res Commun 81: 1336–1343, 1978Google Scholar
  134. 134.
    Papa S: Mitochondrial oxidative phosphorylation changes in the life span. Molecular aspects and physiopathological implications. Biochim Biophys Acta 1276: 87–105, 1996Google Scholar
  135. 135.
    Wilson PD, Franks LM: The effect of age on mitochondrial ultrastructure and enzymes. Adv Exp Med Biol 53: 171–183, 1975Google Scholar
  136. 136.
    Murfitt RR, Sanadi DR: Evidence for increased degeneration of mitochondria in old rats. A brief note. Mech Ageing Dev 8: 197–291, 1978Google Scholar
  137. 137.
    Hansford RG: Bioenergetics of aging. Biochim Biophys Acta 726: 41–80, 1983Google Scholar
  138. 138.
    Zucchini C, Pugnaloni A, Pallotti F, Solmi R, Crimi M, Castaldini C, Biagini G, Lenaz G: Human skeletal muscle mitochondria in aging: lack of detectable morphological and enzymic defects. Biochem Mol Biol Int 37: 607–616, 1995Google Scholar
  139. 139.
    Boffoli D, Scacco SC, Vergari R, Solarino G, Santacroce G, Papa S: Decline with age of the respiratory chain activity in human skeletal muscle. Biochim Biophys Acta 1226: 73–82, 1994Google Scholar
  140. 140.
    Boffoli D, Scacco SC, Vergari R, Persio MT, Solarino G, Laforgia R, Papa S: Ageing is associated in females with a decline in the content and activity of the b-c 1 complex in skeletal muscle mitochondria. Biochim Biophys Acta 1315: 66–72, 1996Google Scholar
  141. 141.
    Wallace DC: Mitochondrial DNA diseases. Ann Rev Biochem 61: 1175–1212, 1992Google Scholar
  142. 142.
    Tzagoloff A, Myers AM: Genetics of mitochondrial biogenesis. Annul Rev Biochem 55: 249–285, 1986Google Scholar
  143. 143.
    Hauska G, Nitschke W, Hermann RG: Amino acid identities in the three redox center-carrying polypeptides of cytochrome bc 1 /b 6 f complexes. J Bioenerg Biomembr 20: 211–228, 1988Google Scholar
  144. 144.
    Schagger H, Link TA, Engel WD, von Jagow G: Isolation of the eleven protein subunits of the bc 1 complex from beef heart. Meth Enzymol 26: 224–237, 1986Google Scholar
  145. 145.
    Anderson S, Bankier AT, Barrell BG, De Bruijn MHL, Coulson AR, Drouin J, Eperon IC, Nierlich DP, Roe BA, Sanger F, Schreirer PH, Smith AJH, Staden R, Young IG: Nature 290: 457–465, 1981Google Scholar
  146. 146.
    Cortopassi GA, Arnheim N: Detection of a specific mitochondrial DNA deletion in tissues of older humans. Nucl Acids Res 18: 6927–6933, 1990Google Scholar
  147. 147.
    Ozawa T: In Biochemistry of Cell Membranes. S Papa, JM Tager (eds). Birkhauser, Basel, 1995, pp 339–361Google Scholar
  148. 148.
    Kadenbach B, Munscher C, Frank V, Müller Hocker J, Napiwotzki J: Human aging with stochastic somatic mutations of mitochondrial DNA. Mutation Res 338: 161–172, 1995Google Scholar
  149. 149.
    Cortopassi GA, Shibata D, Soong NW, Arnheim N: A pattern of accumulation of a somatic deletion of mitochondrial DNA in aging human tissues. Proc Natl Acad Sci USA 89: 7370–7374, 1992Google Scholar
  150. 150.
    Hayashi JI, Ohta S, Kikuchi A, Takemitsu M, Goto YI, Nonaka I: Introduction of disease-related mitochondrial DNA deletions into HeLa cells lacking mitochondrial DNA results in mitochondrial dysfunction. Proc Natl Acad Sci USA 88: 10614–10618, 1991Google Scholar
  151. 151.
    Chomyn AA, Martinuzzi A, Yoneda M, Gada A, Hurko O, Johns D, Lai ST, Nonaka I, Angelini C, Attardi G: MELAS mutation in mtDNA binding site for transcription termination factor causes defects in protein synthesis and in respiration but no change in levels of upstream and downstream mature transcripts. Proc Natl Acad Sci USA 89: 4221–4225, 1992Google Scholar
  152. 152.
    Slater AFG, Nobel CSI, Orrenius S: The role of intracellular oxidants in apoptosis. Biochim Biophys Acta 1271: 59–62, 1995Google Scholar
  153. 153.
    Butthe TM, Sandstrom PA: Oxidative stress as a mediator of apoptosis. Immunol Today 15: 7–10, 1994Google Scholar
  154. 154.
    Lennon SV, Martin SJ, Cotter TG: Dose-dependent induction of apoptosis in human tumour cell lines by widely diverging stimuli. Cell Prolif 24: 203–204, 1991Google Scholar
  155. 155.
    Müller-Hocker J, Seibel P, Schneiderbanger K, Kadenbach B: Different in situ hybridization patterns of mitochondrial DNA in cytocrome c oxidase-deficient extraocular muscle fibers in the elderly. Virchows Archiv A Pathol Anat 422: 7–15, 1993Google Scholar
  156. 156.
    Hayashi JI, Ohta S, Kagawa Kondi H, Kaneda H, Yonekawa H, Takai D, Miyabayashi S: Nuclear but not mitochondrial genome involvement in human age-related mitochondrial dysfunction. Functional integrity of mitochondrial DNA from aged subjects. J Biol Chem 269: 6878–6883, 1994Google Scholar

Copyright information

© Kluwer Academic Publishers 1997

Authors and Affiliations

  • S. Papa
    • 1
  • V.P. Skulachev
    • 2
  1. 1.Institute of Medical Biochemistry and ChemistryUniversity of BariBariItaly
  2. 2.A.N. Belozersky Institute of Physico-Chemical BiologyMoscow State UniversityMoscowRussia

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