Oxidative stress, mitochondrial bioenergetics, and cardiolipin in aging

Free Radical Biology and Medicine

Volumn 48, Issue 10, 2010, Pages 1286-1295

  Paradies, Giuseppe ^a   Petrosillo, Giuseppe ^a   Paradies, Valeria ^a   Ruggiero, Francesca M ^a  

^a UNIVERSITY OF BARI   (Italy)

Author keywords

Aging; Cardiolipin; Free radicals; Mitochondrial bioenergetics; Oxidative stress

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; ANION TRANSPORT PROTEIN; CARDIOLIPIN; CYTOCHROME C; MITOCHONDRIAL PROTEIN; REACTIVE OXYGEN METABOLITE;

AGING; ANION TRANSPORT; APOPTOSIS; BIOENERGY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; HUMAN; LIPID OXIDATION; MITOCHONDRIAL PERMEABILITY; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; NONHUMAN; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN SECRETION; REVIEW;

AGING; ANIMALS; CARDIOLIPINS; ENERGY METABOLISM; HUMANS; MITOCHONDRIA; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES;

EID: 77951937320     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2010.02.020     Document Type: Review

References (166)

1. Harman D. Aging: a theory based on free radical and radiation chemistry. J. Gerontol. 1956, 11:298-300.
2. Harman D. The biologic clock: the mitochondria?. J. Am. Geriatr. Soc. 1972, 20:145-147.
3. Miquel J., Economos A.C., Fleming J., Johnson J.E. Mitochondrial role in cell aging. Exp. Gerontol. 1980, 15:575-591.
4. Pak J.W., Herbst A., Bua E., Gokey N., McKenzie D., Aiken J.M. Mitochondrial DNA mutations as a fundamental mechanism in physiological declines associated with aging. Aging Cell 2003, 2:1-7.
5. Wei Y.H. Mitochondrial DNA alterations as ageing-associated molecular events. Mutat. Res. 1992, 275:145-155.
6. Richter C. Oxidative damage to mitochondrial DNA and its relationship to ageing. Int. J. Biochem. Cell Biol. 1995, 27:647-653.
7. Linnane A.W., Marzuki S., Ozawa T., Tanaka M. Mitochondrial DNA mutations as an important contributor to ageing and degenerative diseases. Lancet 1989, 1:642-645.
8. Judge S., Leeuwenburgh C. Cardiac mitochondrial bioenergetics, oxidative stress, and aging. Am. J. Physiol. Cell Physiol. 2007, 292:C1983-C1992.
9. Sohal R.S., Weindruch R. Oxidative stress, caloric restriction, and aging. Science 1996, 5:59-63.
10. Beckman K.B., Ames B.N. The free radical theory of aging matures. Physiol. Rev. 1998, 78:547-581.
11. Cortopassi G.A., Shibata D., Soong N.W., Arnheim N.A. pattern of accumulation of a somatic deletion of mitochondrial DNA in aging human tissues. Proc. Natl. Acad. Sci. USA 1992, 89:7370-7374.
12. Hayakawa M., Hattori K., Sugiyama S., Ozawa T. Age-associated oxygen damage and mutations in mitochondrial DNA in human hearts. Biochem. Biophys. Res. Commun. 1992, 189:979-985.
13. Paradies G., Ruggiero F.M., Quagliariello E. Age-dependent changes in the activity of anion carriers and in the lipid composition in rat heart mitochondria. Ann. N.Y. Acad. Sci 1992, 26:160-164.
14. Paradies G., Ruggiero F.M., Petrosillo G., Quagliariello E. Age-dependent impairment of mitochondrial function in rat heart tissue: effect of pharmacological agents. Ann. N.Y. Acad. Sci. 1996, 786:252-263.
15. Shigenaga M.K., Hagen T.M., Ames B.N. Oxidative damage and mitochondrial decay in aging. Proc. Natl. Acad. Sci. USA 1994, 91:10771-10778.
16. Lesnefsky E.J., Moghaddas S., Tandler B., Kerner J., Hoppel C.L. Mitochondrial dysfunction in cardiac disease: ischemia-reperfusion, aging, and heart failure. J. Mol. Cell. Cardiol. 2001, 33:1065-1089.
17. Pamplona R. Membrane phospholipids, lipoxidative damage and molecular integrity: a causal role in aging and longevity. Biochim. Biophys. Acta 2008, 1777:1249-1262.
18. Daum G. Lipids of mitochondria. Biochim. Biophys. Acta 1985, 822:1-42.
19. Schlame M., Hostetler K.Y. Mammalian cardiolipin biosynthesis. Methods Enzymol. 1992, 209:330-337.
20. Schlame M., Rua D., Greenberg M.L. The biosynthesis and functional role of cardiolipin. Prog. Lipid Res. 2000, 39:257-288.
21. Hoch F.L. Cardiolipins and biomembrane function. Biochim. Biophys. Acta 1992, 1113:71-133.
22. Robinson N.C. Functional binding of cardiolipin to cytochrome c oxidase. J. Bioenerg. Biomembranes 1993, 25:153-163.
23. Houtkooper R.H., Vaz F.M. Cardiolipin, the heart of mitochondrial metabolism. Cell. Mol. Life Sci. 2008, 65:2493-2506.
24. Paradies G., Ruggiero F.M., Dinoi P., Petrosillo G., Quagliariello E. Decreased cytochrome oxidase activity and changes in phospholipids in heart mitochondria from hypothyroid rats. Arch. Biochem. Biophys. 1993, 307:91-95.
25. Paradies G., Ruggiero F.M., Petrosillo G., Quagliariello E. Enhanced cytochrome oxidase activity and modification of lipids in heart mitochondria from hyperthyroid rats. Biochim. Biophys. Acta 1994, 1225:165-170.
26. Paradies G., Ruggiero F.M., Petrosillo G., Quagliariello E. Age-dependent decline in the cytochrome c oxidase activity in rat heart mitochondria: role of cardiolipin. FEBS Lett. 1997, 406:136-138.
27. Paradies G., Petrosillo G., Pistolese M., Di Venosa N., Serena D., Ruggiero F.M. Lipid peroxidation and alterations to oxidative metabolism in mitochondria isolated from rat heart subjected to ischemia and reperfusion. Free Radic. Biol. Med. 1999, 27:42-50.
28. Chicco A.J., Sparagna G.C. Role of cardiolipin alterations in mitochondrial dysfunction and disease. Am. J. Physiol., Cell Physiol. 2007, 292:C33-C44.
29. Petrosillo G., Portincasa P., Grattagliano I., Casanova G., Matera M., Ruggiero F.M., Ferri D., Paradies G. Mitochondrial dysfunction in rat with nonalcoholic fatty liver: involvement of complex I, reactive oxygen species and cardiolipin. Biochim. Biophys. Acta 2007, 1767:1260-1267.
30. Petrosillo G., Ruggiero F.M., Di Venosa N., Paradies G. Decreased complex III activity in mitochondria isolated from rat heart subjected to ischemia and reperfusion: role of reactive oxygen species and cardiolipin. FASEB J. 2003, 17:714-716.
31. Paradies G., Petrosillo G., Pistolese M., Di Venosa N., Federici A., Ruggiero F.M. Decrease in mitochondrial complex I activity in ischemic/reperfused rat heart: involvement of reactive oxygen species and cardiolipin. Circ. Res. 2004, 94:53-59.
32. Sparagna G.C., Chicco A.J., Murphy R.C., Bristow M.R., Johnson C.A., Rees M.L., Maxey M.L., McCune S.A., Moore R.L. Loss of cardiac tetralinoleoyl cardiolipin in human and experimental heart failure. J. Lipid Res. 2007, 48:1559-15570.
33. Lesnefsky E.J., Hoppel C.L. Cardiolipin as an oxidative target in cardiac mitochondria in the aged rat. Biochim. Biophys. Acta 2008, 1777:1020-1027.
34. Pope S., Land J.M., Heales S.J. Oxidative stress and mitochondrial dysfunction in neurodegeneration: cardiolipin a critical target?. Biochim. Biophys. Acta 2008, 1777:794-799.
35. Kagan V.E., Borisenko G.G., Tyurina Y.Y., Tyurin V.A., Jiang J., Potapovich A.I., Kini V., Amoscato A.A., Fujii Y. Oxidative lipidomics of apoptosis: redox catalytic interactions of cytochrome c with cardiolipin and phosphatidylserine. Free Radic. Biol. Med. 2004, 37:1963-1985.
36. Bayir H., Fadeel B., Palladino M.J., Witasp E., Kurnikov I.V., Tyurina Y.Y., Tyurin V.A., Amoscato A.A., Jiang J., Kochanek P.M., DeKosky S.T., Greenberger J.S., Shvedova A.A., Kagan V.E. Apoptotic interactions of cytochrome c: redox flirting with anionic phospholipids within and outside of mitochondria. Biochim. Biophys. Acta 2006, 1757:648-659.
37. Iverson S.L., Orrenius S. The cardiolipin-cytochrome c interaction and the mitochondrial regulation of apoptosis. Arch. Biochem. Biophys. 2004, 423:37-46.
38. Ott M., Gogvadze V., Orrenius S., Zhivotovsky B. Mitochondria, oxidative stress and cell death. Apoptosis 2007, 12:913-922.
39. Petrosillo G., Ruggiero F.M., Pistolese M., Paradies G. Reactive oxygen species generated from the mitochondrial electron transport chain induce cytochrome c dissociation from beef-heart submitochondrial particles via cardiolipin peroxidation: possible role in the apoptosis. FEBS Lett. 2001, 509:435-438.
40. Petrosillo G., Ruggiero F.M., Paradies G. Role of reactive oxygen species and cardiolipin in the release of cytochrome c from mitochondria. FASEB J. 2003, 15:2202-2208.
41. Paradies G., Petrosillo G., Paradies V., Ruggiero F.M. Role of cardiolipin peroxidation and Ca2+ in mitochondrial dysfunction and disease. Cell Calcium 2009, 45:643-650.
42. Boveris A., Chance B. The mitochondrial generation of hydrogen peroxide: general properties and effect of hyperbaric oxygen. Biochem. J. 1973, 134:707-716.
43. Murphy M.P. How mitochondria produce reactive oxygen species. Biochem. J. 2009, 417:1-13.
44. Turrens J.F., Alexandre A., Lehninger A.L. Ubisemiquinone is the electron donor for superoxide formation by complex III of heart mitochondria. Arch. Biochem. Biophys. 1985, 237:408-414.
45. Barja G. Mitochondrial oxygen radical generation and leak: sites of production in states 4 and 3, organ specificity, and relation to aging and longevity. J. Bioenerg. Biomembr. 1985, 31:347-366.
46. Nohl H., Stolze K. Ubisemiquinones of the mitochondrial respiratory chain do not interact with molecular oxygen. Free Radic. Res. Commun. 1992, 16:409-419.
47. Giulivi C., Poderoso J.J., Boveris A. Production of nitric oxide by mitochondria. J. Biol. Chem. 1998, 273:11038-11043.
48. Ghafourifar P., Richter C. Nitric oxide synthase activity in mitochondria. FEBS Lett. 1997, 418:291-296.
49. Venkatakrishnan P., Nakayasu E.S., Almeida I.C., Miller R.T. Absence of nitric-oxide synthase in sequentially purified rat liver mitochondria. J. Biol. Chem. 2009, 284:19843.
50. Pryor W.A., Squadrito G.L. The chemistry of peroxynitrite: a product from the reaction of nitric oxide with superoxide. Am. J. Physiol. 1995, 268(5 Pt. 1):L699-722.
51. Sarkela T.M., Berthiaume J., Elfering S., Gybina A.A., Giulivi C. The modulation of oxygen radical production by nitric oxide in mitochondria. J. Biol. Chem. 2001, 276:6945-6949.
52. Cleeter M.W., Cooper J.M., Darley-Usmar V.M., Moncada S., Schapira A.H. Reversible inhibition of cytochrome c oxidase, the terminal enzyme of the mitochondrial respiratory chain, by nitric oxide: implications for neurodegenerative diseases. FEBS Lett. 1994, 345:50-54.
53. Gus'kova R.A., Ivanov I.I., Kol'tover V.K., Akhobadze V.V., Rubin A.B. Permeability of bilayer lipid membranes for superoxide (O2•-) radicals. Biochim. Biophys. Acta 1984, 778:579-585.
54. Madesh M., Hajnóczky G. VDAC-dependent permeabilization of the outer mitochondrial membrane by superoxide induces rapid and massive cytochrome c release. J. Cell Biol. 2001, 155:1003-1015.
55. Rhee S.G., Chae H.Z., Kim K. Peroxiredoxins: a historical overview and speculative preview of novel mechanisms and emerging concepts in cell signaling. Free Radic. Biol. Med. 2005, 38:1543-1552.
56. Wood Z.A., Schroder E., Robin Harris J., Poole L.B. Structure, mechanism and regulation of peroxiredoxins. Trends Biochem. Sci. 2003, 28:32-40.
57. Stadtman E.R. Importance of individuality in oxidative stress and aging. Free Radic. Biol. Med. 2002, 33:597-604.
58. Sohal R.S. Role of oxidative stress and protein oxidation in the aging process. Free Radic. Biol. Med. 2002, 33:37-44.
59. Floyd R.A., West M., Hensley K. Oxidative biochemical markers: clues to understanding aging in long-lived species. Exp. Gerontol. 2001, 36:619-640.
60. Van Remmen H., Richardson A. Oxidative damage to mitochondria and aging. Exp. Gerontol. 2001, 36:957-968.
61. Sohal R.S., Agarwal S., Dubey A., Orr W.C. Protein oxidative damage is associated with life expectancy of houseflies. Proc. Natl. Acad. Sci. USA 1993, 90:7255-7259.
62. Yan L.J., Levine R.L., Sohal R. Oxidative damage during aging targets mitochondrial aconitase. Proc. Natl. Acad. Sci. USA 1997, 94:11168-11172.
63. Yan L.J., Sohal R.S. Mitochondrial adenine nucleotide translocase is modified oxidatively during aging. Proc. Natl. Acad. Sci. USA 1998, 95:12896-12901.
64. Wei Y., Lee H. Oxidative stress, mitochondrial DNA mutation, and impairment of antioxidant enzymes. Exp. Biol. Med. 2002, 227:671-682.
65. Barja G. Free radicals and aging. Trends Neurosci. 2004, 27:595-600.
66. Corral-Debrinski M., Horton T., Lott M.T., Shoffner J.M., Beal M.F., Wallace D.C. Mitochondrial DNA deletions in human brain: regional variability and increase with advanced age. Nat. Genet. 1992, 2:324-329.
67. Zhang J., Asin-Cayuela J., Fish J., Michikawa Y., Bonafe M., Olivieri F., Passarino G., De Benedictis G., Franceschi C., Attardi G. Strikingly higher frequency in centenarians and twins of mtDNA mutation causing remodeling of replication origin in leukocytes. Proc. Natl. Acad. Sci. USA 2003, 100:1116-1121.
68. Van Remmen H., Hamilton M.L., Richardson A. Oxidative damage to DNA and aging. Exerc. Sport Sci. Rev. 2003, 31:149-153.
69. Bielski B.H., Arudi R.L., Sutherland M.W. A study of the reactivity of HO2/O2- with unsaturated fatty acids. J. Biol. Chem. 1983, 258:4759-4761.
70. Yu B.P. Membrane alteration as a basis of aging and the protective effects of calorie restriction. Mech. Ageing Dev. 2005, 126:1003-1010.
71. Spiteller G. Lipid peroxidation in aging and age-dependent diseases. Exp. Gerontol. 2001, 36:1425-1457.
72. Ruggiero F.M., Landriscina C., Gnoni G.V., Quagliariello E. Lipid composition of liver mitochondria and microsomes in hyperthyroid rats. Lipids 1984, 19:171-178.
73. Parinandi N.L., Weis B.K., Schmid H.H. Assay of cardiolipin peroxidation by high-performance liquid chromatography. Chem. Phys. Lipids 1988, 49:215-220.
74. Petrosillo G., Matera M., Moro N., Ruggiero F.M., Paradies G. Mitochondrial complex I dysfunction in rat heart with aging: critical role of reactive oxygen species and cardiolipin. Free Radic. Biol. Med. 2009, 46:88-94.
75. Petrosillo G., Matera M., Casanova G., Ruggiero F.M., Paradies G. Mitochondrial dysfunction in rat brain with aging: involvement of complex I, reactive oxygen species and cardiolipin. Neurochem. Int. 2008, 53:126-131.
76. Hagen T.M., Ingersoll R.T., Wehr C.M., Lykkesfeldt J., Vinarsky V., Bartholomew J.C., Song M.H., Ames B.N. Acetyl-l-carnitine fed to old rats partially restores mitochondrial function and ambulatory activity. Proc. Natl. Acad. Sci. USA 1998, 95:9562-9566.
77. Pepe S., Tsuchiya N., Lakatta E.G., Hansford R.G. PUFA and aging modulate cardiac mitochondrial membrane lipid composition and Ca2+ activation of PDH. Am. J. Physiol. 1999, 276:H149-H158.
78. Sen T., Sen N., Jana S., Khan F.H., Chatterjee U., Chakrabarti S. Depolarization and cardiolipin depletion in aged rat brain mitochondria: relationship with oxidative stress and electron transport chain activity. Neurochem. Int. 2007, 50:719-725.
79. Maftah A., Ratinaud M.H., Dumas M., Bonté F., Meybeck A., Julien R. Human epidermal cells progressively lose their cardiolipins during ageing without change in mitochondrial transmembrane potential. Mech. Ageing Dev. 1994, 77:83-96.
80. Skulachev V.P., Anisimov V.N., Antonenko Y.N., Bakeeva L.E., Chernyak B.V., Erichev V.P., Filenko O.F., Kalinina N.I., Kapelko V.I., Kolosova N.G., Kopnin B.P., Korshunova G.A., Lichinitser M.R., Obukhova L.A., Pasyukova E.G., Pisarenko O.I., Roginsky V.A., Ruuge E.K., Senin I.I., Severina I.I., Skulachev M.V., Spivak I.M., Tashlitsky V.N., Tkachuk V.A., Vyssokikh M.Y., Yaguzhinsky L.S., Zorov D.B. An attempt to prevent senescence: a mitochondrial approach. Biochim. Biophys. Acta 2009, 1787:437-461.
81. Moghaddas S., Stoll M.S., Minkler P.E., Salomon R.G., Hoppel C.L., Lesnefsky E.J. Preservation of cardiolipin content during aging in rat heart interfibrillar mitochondria. J. Gerontol. A Biol. Sci. Med. Sci. 2002, 57:B22-28.
82. Dowhan W. Molecular basis for membrane phospholipid diversity: why are there so many lipids?. Annu. Rev. Biochem. 1997, 66:199-232.
83. Fry M., Green M. Cardiolipin requirement for electron transfer in complex I and III of the mitochondrial respiratory chain. J. Biol. Chem. 1981, 256:1874-1880.
84. Dröse S., Zwicker K., Brandt U. Full recovery of the NADH:ubiquinone activity of complex I (NADH:ubiquinone oxidoreductase) from Yarrowia lipolytica by the addition of phospholipids. Biochim. Biophys. Acta 2002, 1556:65-67.
85. Sharpley M.S., Shannon R.J., Draghi F., Hirst J. Interactions between phospholipids and NADH:ubiquinone oxidoreductase (complex I) from bovine mitochondria. Biochemistry 2006, 45:241-248.
86. Lange C., Nett J.H., Trumpower B.L., Hunte C. Specific roles of protein-phospholipid interactions in the yeast cytochrome bc1 complex structure. EMBO J. 2001, 20:6591-6600.
87. Robinson N.C., Zborowski J., Talbert L.H. Cardiolipin-depleted bovine heart cytochrome c oxidase: binding stoichiometry and affinity for cardiolipin derivatives. Biochemistry 1990, 29:8962-8969.
88. Eble K.S., Coleman W.B., Hantgan R.R., Cunningham C.C. Tightly associated cardiolipin in the bovine heart mitochondrial ATP synthase as analyzed by 31P nuclear magnetic resonance spectroscopy. J. Biol. Chem. 1990, 265:19434-19440.
89. Schlame M., Ren M. The role of cardiolipin in the structural organization of mitochondrial membranes. Biochim. Biophys. Acta 2009, 1788:2080-2083.
90. Zhang M., Mileykovskaya E., Dowhan W. Gluing the respiratory chain together: cardiolipin is required for supercomplex formation in the inner mitochondrial membrane. J. Biol. Chem. 2002, 277:43553-43556.
91. Schägger H. Respiratory chain supercomplexes of mitochondria and bacteria. Biochim. Biophys. Acta 2002, 1555:154-159.
92. Schägger H., Pfeiffer K. Supercomplexes in the respiratory chains of yeast and mammalian mitochondria. EMBO J. 2000, 19:1777-1783.
93. Acín-Pérez R., Fernández-Silva P., Peleato M.L., Pérez-Martos A., Enriquez J.A. Respiratory active mitochondrial supercomplexes. Mol. Cell 2008, 32:529-539.
94. Zhang M., Mileykovskaya E., Dowhan W. Cardiolipin is essential for organization of complexes III and IV into a supercomplex in intact yeast mitochondria. J. Biol. Chem. 2005, 280:29403-29408.
95. Claypool S.M., Oktay Y., Boontheung P., Loo J.A., Koehler C.M. Cardiolipin defines the interactome of the major ADP/ATP carrier protein of the mitochondrial inner membrane. J. Cell Biol. 2008, 182:937-950.
96. Claypool S.M. Cardiolipin, a critical determinant of mitochondrial carrier protein assembly and function. Biochim. Biophys. Acta 2009, 1788:2059-2068.
97. Haines T.H., Dencher N.A. Cardiolipin: a proton trap for oxidative phosphorylation. FEBS Lett. 2002, 528:35-39.
98. Klingenberg M. Cardiolipin and mitochondrial carriers. Biochim. Biophys. Acta 2009, 1788:2048-2058.
99. Beyer K., Klingenberg M. ADP/ATP carrier protein from beef heart mitochondria has high amounts of tightly bound cardiolipin, as revealed by 31P nuclear magnetic resonance. Biochemistry 1985, 24:3821-3826.
100. Wenz T., Hielscher R., Hellwig P., Schägger H., Richers S., Hunte C. Role of phospholipids in respiratory cytochrome bc(1) complex catalysis and supercomplex formation. Biochim. Biophys. Acta 2009, 1787:609-616.
101. Epand R.F., Schlattner U., Wallimann T., Lacombe M.L., Epand R.M. Novel lipid transfer property of two mitochondrial proteins that bridge the inner and outer membranes. Biophys. J. 2007, 92:126-137.
102. Lacombe M.L., Tokarska-Schlattner M., Epand R.F., Boissan M., Epand R.M., Schlattner U. Interaction of NDPK-D with cardiolipin-containing membranes: structural basis and implications for mitochondrial physiology. Biochimie 2009, 91:779-783.
103. Schlattner U., Tokarska-Schlattner M., Ramirez S., Brückner A., Kay L., Polge C., Epand R.F., Lee R.M., Lacombe M.L., Epand R.M. Mitochondrial kinases and their molecular interaction with cardiolipin. Biochim. Biophys. Acta 2009, 1788:2032-2047.
104. Barth P.G., Scholte H.R., Berden J.A., Van derKlei-Van Moorsel J.M., Luyt-Houwen I.E., Van(t Veer-Korthof E.T., Van der Harten J.J., Sobotka-Plojhar M.A. An X-linked mitochondrial disease affecting cardiac muscle, skeletal muscle and neutrophil leucocytes. J. Neurol. Sci. 1983, 62:327-355.
105. Hauff K.D., Hatch G.M. Cardiolipin metabolism and Barth syndrome. Prog. Lipid Res. 2006, 45:91-101.
106. Schlame M., Ren M. Barth syndrome, a human disorder of cardiolipin metabolism. FEBS Lett. 2006, 580:5450-5455.
107. Bione S., D'Adamo P., Maestrini E., Gedeon A.K., Bolhuis P.A., Toniolo D.A. novel X-linked gene, G4.5, is responsible for Barth syndrome. Nat. Genet. 1996, 12:385-389.
108. McKenzie M., Lazarou M., Thorburn D.R., Ryan M.T. Mitochondrial respiratory chain supercomplexes are destabilized in Barth syndrome patients. J. Mol. Biol. 2006, 361:462-469.
109. Lenaz G., Bovina C., Castelluccio C., Fato R., Formaggini G., Genova M.L., Marchetti M., Pich M.M., Pallotti F., Parenti Castelli G., Biagini G., Mitochondrial complex I. defects in aging. Mol. Cell. Biochem. 1997, 174:329-333.
110. Navarro A., Boveris A. The mitochondrial energy transduction system and the aging process. Am. J. Physiol., Cell Physiol. 2007, 292:C670-C686.
111. Lesnefsky E.J., Gudz T.I., Moghaddas S., Migita C.T., Ikeda-Saito M., Turkaly P.J., Hoppel C.L. Aging decreases electron transport complex III activity in heart interfibrillar mitochondria by alteration of the cytochrome c binding site. J. Mol. Cell. Cardiol. 2001, 33:37-47.
112. Nakahara H., Kanno T., Inai Y., Utsumi K., Hiramatsu M., Mori A., Packer L. Mitochondrial dysfunction in the senescence accelerated mouse (SAM). Free Radic. Biol. Med. 1998, 24:85-92.
113. Sugiyama S., Takasawa M., Hayakawa M., Ozawa T. Changes in skeletal muscle, heart and liver mitochondrial electron transport activities in rats and dogs of various ages. Biochem. Mol. Biol. Int. 1993, 30:937-944.
114. Kwong L.K., Sohal R.S. Age-related changes in activities of mitochondrial electron transport complexes in various tissues of the mouse. Arch. Biochem. Biophys. 2000, 373:16-22.
115. Miró O., Casademont J., Casals E., Perea M., Urbano-Márquez A., Rustin P., Cardellach F. Aging is associated with increased lipid peroxidation in human hearts, but not with mitochondrial respiratory chain enzyme defects. Cardiovasc. Res. 2000, 47:624-631.
116. Paradies G., Petrosillo G., Pistolese M., Ruggiero F.M. Reactive oxygen species generated by the mitochondrial respiratory chain affect the complex III activity via cardiolipin peroxidation in beef-heart submitochondrial particles. Mitochondrion 2001, 2:151-159.
117. Paradies G., Petrosillo G., Pistolese M., Ruggiero F.M. Reactive oxygen species affect mitochondrial electron transport complex I activity through oxidative cardiolipin damage. Gene 2002, 286:135-141.
118. Cruciat C.M., Brunner S., Baumann F., Neupert W., Stuart R.A. The cytochrome bc1 and cytochrome c oxidase complexes associate to form a single supracomplex in yeast mitochondria. J. Biol. Chem. 2000, 275:18093-18098.
119. Pfeiffer K., Gohil V., Stuart R.A., Hunte C., Brandt U., Greenberg M.L., Schägger H. Cardiolipin stabilizes respiratory chain supercomplexes. J. Biol. Chem. 2003, 278:52873-52880.
120. Jiang F., Ryan M.T., Schlame M., Zhao M., Gu Z., Klingenberg M., Pfanner N., Greenberg M.L. Absence of cardiolipin in the crd1 null mutant results in decreased mitochondrial membrane potential and reduced mitochondrial function. J. Biol. Chem. 2000, 275:22387-22394.
121. Gómez L.A., Monette J.S., Chavez J.D., Maier C.S., Hagen T.M. Supercomplexes of the mitochondrial electron transport chain decline in the aging rat heart. Arch. Biochem. Biophys. 2009, 490:30-35.
122. Palmieri F. The mitochondrial transporter family (SLC25): physiological and pathological implications. Pflugers Arch. 2004, 447:689-709.
123. Palmieri F. Diseases caused by defects of mitochondrial carriers: a review. Biochim. Biophys. Acta 2008, 1777:564-578.
124. Pebay-Peyroula E., Dahout-Gonzalez C., Kahn R., Trézéguet V., Lauquin G.J., Brandolin G. Structure of mitochondrial ADP/ATP carrier in complex with carboxyatractyloside. Nature 2003, 426:39-44.
125. Bisaccia F., Palmieri F. Specific elution from hydroxylapatite of the mitochondrial phosphate carrier by cardiolipin. Biochim. Biophys. Acta 1984, 766:386-394.
126. Noël H., Pande S.V. An essential requirement of cardiolipin for mitochondrial carnitine acylcarnitine translocase activity: lipid requirement of carnitine acylcarnitine translocase. Eur. J. Biochem. 1986, 155:99-102.
127. Nałecz K.A., Kamińska J., Nałecz M.J., Azzi A. The activity of pyruvate carrier in a reconstituted system: substrate specificity and inhibitor sensitivity. Arch. Biochem. Biophys. 1992, 297:162-168.
128. Bisaccia F., De Palma A., Prezioso G., Palmieri F. Kinetic characterization of the reconstituted tricarboxylate carrier from rat liver mitochondria. Biochim. Biophys. Acta 1990, 1019:250-256.
129. Klingenberg M. Cardiolipin and mitochondrial carriers. Biochim. Biophys. Acta 2009, 1788:2048-2058.
130. Crompton M. The mitochondrial permeability transition pore and its role in cell death. Biochem. J. 1999, 341:233-249.
131. Leung A.W., Halestrap A.P. Recent progress in elucidating the molecular mechanism of the mitochondrial permeability transition pore. Biochim. Biophys. Acta 2008, 1777:946-952.
132. Kokoszka J.E., Waymire K.G., Levy S.E., Sligh J.E., Cai J., Jones D.P., MacGregor G.R., Wallace D.C. The ADP/ATP translocator is not essential for the mitochondrial permeability transition pore. Nature 2004, 427:461-465.
133. Halestrap A.P. Mitochondrial permeability: dual role for the ADP/ATP translocator?. Nature 2004, 430:1.
134. Di Lisa; F., Bernardi P. Mitochondrial function and myocardial aging: a critical analysis of the role of permeability transition. Cardiovasc. Res. 2005, 66:222-232.
135. Grimm S., Brdiczka D. The permeability transition pore in cell death. Apoptosis 2007, 12:841-855.
136. Rytömaa M., Mustonen P., Kinnunen P.K. Reversible, nonionic, and pH-dependent association of cytochrome c with cardiolipin-phosphatidylcholine liposomes. J. Biol. Chem. 1992, 267:22243-22248.
137. Cortese J.D., Voglino A.L., Hackenbrock C.R. Persistence of cytochrome c binding to membranes at physiological mitochondrial intermembrane space ionic strength. Biochim. Biophys. Acta 1995, 1228:216-228.
138. Pereverzev M.O., Vygodina T.V., Konstantinov A.A., Skulachev V.P. Cytochrome c, an ideal antioxidant. Biochem. Soc. Trans. 2003, 31:1312-1315.
139. Kagan V.E., Tyurin V.A., Jiang J., Tyurina Y.Y., Ritov V.B., Amoscato A.A., Osipov A.N., Belikova N.A., Kapralov A.A., Kini V., Vlasova I.I., Zhao Q., Zou M., Di P., Svistunenko D.A., Kurnikov I.V., Borisenko G.G. Cytochrome c acts as a cardiolipin oxygenase required for release of proapoptotic factors. Nat. Chem. Biol. 2005, 1:223-232.
140. Petrosillo G., Ruggiero F.M., Pistolese M., Paradies G. Reactive oxygen species generated from the mitochondrial electron transport chain induce cytochrome c dissociation from beef-heart submitochondrial particles via cardiolipin peroxidation: possible role in the apoptosis. FEBS Lett. 2001, 509:435-438.
141. Jiang J., Huang Z., Zhao Q., Feng W., Belikova N.A., Kagan V.E. Interplay between bax, reactive oxygen species production, and cardiolipin oxidation during apoptosis. Biochem. Biophys. Res. Commun. 2008, 368:145-150.
142. Kagan V.E., Borisenko G.G., Tyurina Y.Y., Tyurin V.A., Jiang J., Potapovich A.I., Kini V., Amoscato A.A., Fujii Y. Oxidative lipidomics of apoptosis: redox catalytic interactions of cytochrome c with cardiolipin and phosphatidylserine. Free Radic. Biol. Med. 2004, 37:1963-1985.
143. Schlame M., Hostetler K.Y. Cardiolipin synthase from mammalian mitochondria. Biochim. Biophys. Acta 1997, 1348:207-213.
144. Choi S.Y., Gonzalvez F., Jenkins G.M., Slomianny C., Chretien D., Arnoult D., Petit P.X., Frohman M.A. Cardiolipin deficiency releases cytochrome c from the inner mitochondrial membrane and accelerates stimuli-elicited apoptosis. Cell Death Differ. 2007, 14:597-606.
145. Huang Z., Jiang J., Tyurin V.A., Zhao Q., Mnuskin A., Ren J., Belikova N.A., Feng W., Kurnikov I.V., Kagan V.E. Cardiolipin deficiency leads to decreased cardiolipin peroxidation and increased resistance of cells to apoptosis. Free Radic. Biol. Med. 2008, 44:1935-1944.
146. Petrosillo G., Casanova G., Matera M., Ruggiero F.M., Paradies G. Interaction of peroxidized cardiolipin with rat-heart mitochondrial membranes: induction of permeability transition and cytochrome c release. FEBS Lett. 2006, 580:6311-6316.
147. Petrosillo G., Moro N., Ruggiero F.M., Paradies G. Melatonin inhibits cardiolipin peroxidation in mitochondria and prevents the mitochondrial permeability transition and cytochrome c release. Free Radic. Biol. Med. 2009, 47:969-974.
148. Nury H., Dahout-Gonzalez C., Trézéguet V., Lauquin G., Brandolin G., Pebay-Peyroula E. Structural basis for lipid-mediated interactions between mitochondrial ADP/ATP carrier monomers. FEBS Lett. 2005, 579:6031-6036.
149. Brustovetsky N., Klingenberg M. Mitochondrial ADP/ATP carrier can be reversibly converted into a large channel by Ca2+. Biochemistry 1996, 35:8483-8488.
150. Imai H., Koumura T., Nakajima R., Nomura K., Nakagawa Y. Protection from inactivation of the adenine nucleotide translocator during hypoglycaemia-induced apoptosis by mitochondrial phospholipid hydroperoxide glutathione peroxidase. Biochem. J. 2003, 371:799-809.
151. Halestrap A.P., Clarke S.J., Khaliulin I. The role of mitochondria in protection of the heart by preconditioning. Biochim. Biophys. Acta 2007, 1767:1007-1031.
152. Petrosillo G., Colantuono G., Moro N., Ruggiero F.M., Tiravanti E., Di Venosa N., Fiore T., Paradies G. Melatonin protects against heart ischemia-reperfusion injury by inhibiting mitochondrial permeability transition pore opening. Am. J. Physiol. Heart Circ. Physiol 2009, 297:H1487-H1493.
153. Lesnefsky E.J., Hoppel C.L. Cardiolipin as an oxidative target in cardiac mitochondria in the aged rat. Biochim. Biophys. Acta 2008, 1777:1020-1027.
154. Goodell S., Cortopassi G. Analysis of oxygen consumption and mitochondrial permeability with age in mice. Mech. Ageing Dev. 1998, 101:245-256.
155. Mather M., Rottenberg H. Aging enhances the activation of the permeability transition pore in mitochondria. Biochem. Biophys. Res. Commun. 2000, 273:603-608.
156. Mather M., Rottenberg H. The inhibition of calcium signaling in T lymphocytes from old mice results from enhanced activation of the mitochondrial permeability transition pore. Mech. Ageing Dev. 2002, 123:707-724.
157. Jahangir A., Ozcan C., Holmuhamedov E.L., Terzic A. Increased calcium vulnerability of senescent cardiac mitochondria: protective role for a mitochondrial potassium channel opener. Mech. Ageing Dev. 2001, 122:1073-1086.
158. Hofer T., Servais S., Seo A.Y., Marzetti E., Hiona A., Upadhyay S.J., Wohlgemuth S.E., Leeuwenburgh C. Bioenergetics and permeability transition pore opening in heart subsarcolemmal and interfibrillar mitochondria: effects of aging and lifelong calorie restriction. Mech. Ageing Dev. 2009, 130:297-307.
159. Crompton M. Mitochondria and aging: a role for the permeability transition?. Aging Cell 2004, 3:3-6.
160. Kwak H.B., Song W., Lawler J.M. Exercise training attenuates age-induced elevation in Bax/Bcl-2 ratio, apoptosis, and remodeling in the rat heart. FASEB J. 2006, 20:791-793.
161. Dirks A., Leeuwenburgh C. Apoptosis in skeletal muscle with aging. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2002, 282:R519-R527.
162. Judge S., Jang Y.M., Smith A., Hagen T., Leeuwenburgh C. Age-associated increases in oxidative stress and antioxidant enzyme activities in cardiac interfibrillar mitochondria: implications for the mitochondrial theory of aging. FASEB J. 2005, 19:419-421.
163. Kristal B.S., Park B.K., Yu B.P. 4-Hydroxyhexenal is a potent inducer of the mitochondrial permeability transition. Biol. Chem. 1996, 271:6033-6038.
164. Hoffmann B., Stöckl A., Schlame M., Beyer K., Klingenberg M. The reconstituted ADP/ATP carrier activity has an absolute requirement for cardiolipin as shown in cysteine mutants. J. Biol. Chem. 1994, 269:1940-1944.
165. Kajstura J., Cheng W., Sarangarajan R., Li P., Li B., Nitahara J.A., Chapnick S., Reiss K., Olivetti G., Anversa P. Necrotic and apoptotic myocyte cell death in the aging heart of Fischer 344 rats. Am. J. Physiol. 1996, 271:H1215-H1228.
166. Higami Y., Shimokawa I. Apoptosis in the aging process. Cell Tissue Res. 2000, 301:125-132.