Free radical oxidation of cardiolipin: Chemical mechanisms, detection and implication in apoptosis, mitochondrial dysfunction and human diseases

Free Radical Research

Volumn 46, Issue 8, 2012, Pages 959-974

  Yin, Huiyong ^a,b   Zhu, Mingjiang ^a  

^a INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

4 HNE; Cytochrome c; Intrinsic apoptosis pathway; Lipid peroxidation; Mass spectrometry; Mitochondria; Mitochondrial redox system; ROS

Indexed keywords

CARDIOLIPIN; CYTOCHROME C; FREE RADICAL; HYDROXYL RADICAL; LINOLEIC ACID; PROTEIN BCL 2; PROTEIN BID; REACTIVE OXYGEN METABOLITE; SINGLET OXYGEN;

APOPTOSIS; DISORDERS OF MITOCHONDRIAL FUNCTIONS; LIPID PEROXIDATION; MITOCHONDRIAL MEMBRANE; OXIDATION; REVIEW;

ALDEHYDES; APOPTOSIS; CARDIOLIPINS; CARDIOVASCULAR DISEASES; CYTOCHROMES C; HUMANS; LIPID PEROXIDATION; MITOCHONDRIA; NEURODEGENERATIVE DISEASES; OXIDATION-REDUCTION; OXIDATIVE STRESS; PEROXIDASES; PROTO-ONCOGENE PROTEINS C-BCL-2; REACTIVE OXYGEN SPECIES;

EID: 84863960346     PISSN: 10715762     EISSN: 10292470     Source Type: Journal    
DOI: 10.3109/10715762.2012.676642     Document Type: Review

References (152)

1. Pulfer M, Murphy RC. Electrospray mass spectrometry of phospholipids. Mass Spectrom Rev 2003;22:332-364.
2. Houtkooper RH, Vaz FM. Cardiolipin, the heart of mitochondrial metabolism. Cell Mol Life Sci 2008;65:2493-2506.
3. Esterbauer H. Cytotoxicity and Genotoxicity of Lipid Oxidaation Products. Am J Clin Nutr 1993;57:S779-S786.
4. Porter NA. Mechanisms for the autoxidation of polyunsaturated lipids. Acc. Chem. Res. 1986;19:262-270.
5. Berliner JA, Heinecke JW. The role of oxidized lipoproteins in atherogenesis. Free Radical Biol Med 1996;20: 707-727.
6. Hammad LA, Wu G, Saleh MM, Klouckova I, Dobrolecki LE, Hickey RJ, et al. Elevated levels of hydroxylated phosphocholine lipids in the blood serum of breast cancer patients. Rapid Commun Mass Spectrom 2009;23:863-876.
7. Wu RP, Hayashi T, Cottam HB, Jin G, Yao S, Wu CCN, et al. Nrf2 responses and the therapeutic selectivity of electrophilic compounds in chronic lymphocytic leukemia. Proc Natl Acad Sci USA 2010;107:7479-7484.
8. Silverstein RL, Febbraio M. CD36, a scavenger receptor involved in immunity, metabolism, angiogenesis, and behavior. Sci Signal 2009;2:re3.
9. Yang L, Latchoumycandane C, McMullen MR, Pratt BT, Zhang R, Papouchado BG, Nagy LE, Feldstein AE, McIntyre TM. Chronic alcohol exposure increases circulating bioactive oxidized phospholipids. J Biol Chem 2010;285: 22211-22220.
10. Imai Y, Kuba K, Neely GG, Yaghubian-Malhami R, Perkmann T, van Loo G, et al. Identifi cation of oxidative stress and Toll-like receptor 4 signaling as a key pathway of acute lung injury. Cell 2008;133:235-249.
11. Nonas S, Miller I, Kawkitinarong K, Chatchavalvanich S, Gorshkova I, Bochkov VN, et al. Oxidized phospholipids reduce vascular leak and infl ammation in rat model of acute lung injury. Am J Respir Crit Care Med 2006;173: 1130-1138.
12. Simonian NA, Coyle JT. Oxidative stress in neurodegenerative diseases. Annu Rev Pharmacol Toxicol 1996;36: 83-106.
13. Montine TJ, Montine KS, McMahan W, Markesbery WR, Quinn JF, Morrow JD. F2-Isoprostanes in Alzheimer and Other Neurodegenerative Diseases. Antioxid Redox Signal 2005;7:269-275.
14. Porter FD, Scherrer DE, Lanier MH, Langmade SJ, Molugu V, Gale SE, et al. Cholesterol oxidation products are sensitive and specifi c blood-based biomarkers for Niemann-Pick C1 disease. Sci Trans Med 2010;2:56ra81.
15. Yin H, Xu L, Porter NA. Free radical lipid peroxidation: mechanisms and analysis. Chem Rev 2011;111:5944-5972.
16. Milne GL, Yin H, Hardy KD, Davies SS, Roberts LJ. Isoprostane generation and function. Chem Rev 2011;111: 5973-5996.
17. Yin H, Porter NA. New insights regarding the autoxidation of polyunsaturated fatty acids. Antioxid Redox Signal 2005;7:170-184.
18. Porter NA, Caldwell SE, Mills KA. Mechanisms of free radical oxidation of unsaturated lipids. Lipids 1995;30: 277-290.
19. T yurina YY, Tyurin VA, Kapralova VI, Amoscato AA, Epperly MW, Greenberger JS, Kagan VE. Mass-spectrometric characterization of phospholipids and their hydroperoxide derivatives in vivo: eff ects of total body irradiation. Methods Mol Biol 2009;580:153-183.
20. Yin H, Davis T, Porter NA. Simultaneous analysis of multiple lipid oxidation products in vivo by liquid chromatographicmass spectrometry (LC-MS). Methods Mol Biol 2010;610: 375-386.
21. Yin H, Musiek ES, Morrow JD. Quantifi cation of isoprostanes as an index of oxidative stress: A update. J Biol Sci 2006;6:469-479.
22. Yin H, Porter NA. 2007. Identifi cation of intact lipid peroxides by Agcoordination ionspray mass spectrometry (CIS-MS). In: Brown HA, ed. Methods in enzymology. Lipidomics and bioactive lipids: specialized analytical methods and lipids in disease.San Diego: Academic Press. 193-211.
23. Crimi M, Esposti MD. Apoptosis-induced changes in mitochondrial lipids. Biochim Biophys Acta (BBA) Mol Cell Res 2011;1813:551-557.
24. Cristea IM, Degli Esposti M. Membrane lipids and cell death: an overview. Chem Phys Lipids 2004;129:133-160.
25. Chicco AJ, Sparagna GC. Role of cardiolipin alterations in mitochondrial dysfunction and disease. Am J Physiol Cell Physiol 2007;292:C33-44.
26. Kagan VE, Bayir HA, Belikova NA, Kapralov O, Tyurina YY, Tyurin VA, et al. Cytochrome c/cardiolipin relations in mitochondria: a kiss of death. Free Radic Biol Med 2009;46:1439-1453.
27. Schug ZT, Gottlieb E. Cardiolipin acts as a mitochondrial signalling platform to launch apoptosis. Biochim Biophys Acta 2009;1788:2022-2031.
28. Paradies G, Petrosillo G, Paradies V, Ruggiero FM. Role of cardiolipin peroxidation and Ca2in mitochondrial dysfunction and disease. Cell Calcium 2009;45:643-650.
29. Ott M, Zhivotovsky B, Orrenius S. Role of cardiolipin in cytochrome c release from mitochondria. Cell Death Diff er 2007;14:1243-1247.
30. Halliwell B, Grootveld M. The measurement of free radical reactions in humans: Some thoughts for future experimentation. FEBS Lett 1987;213:9-14.
31. Gonzalvez F, Gottlieb E. Cardiolipin: setting the beat of apoptosis. Apoptosis 2007;12:877-885.
32. Ames BN, Shigenaga MK, Hagen TM. Oxidants, antioxidants, and the degenerative diseases of aging. Proc Natl Acad Sci USA 1993;90:7915-7922.
33. Turrens JF. Mitochondrial formation of reactive oxygen species. J Physiol 2003;552:335-344.
34. Circu ML, Aw TY. Reactive oxygen species, cellular redox systems, and apoptosis. Free Radic Biol Med 2010;48: 749-762.
35. Maillard B, Ingold KU, Scaiano JC. Rate constants for the reactions of free radicals with oxygen in solution. J Am Chem Soc 1983;105:5095-5099.
36. Brash AR. Autoxidation of methyl linoleate: identifi cation of the Bis-allylic 11-Hydroperoxide. Lipids 2000;35:947-952.
37. Kerr JFR. Shrinkage necrosis: A distinct mode of cellular death. The Journal of Pathology 1971;105:13-20.
38. Kischkel FC, Hellbardt S, Behrmann I, Germer M, Pawlita M, Krammer PH, Peter ME. Cytotoxicity-dependent APO-1 (Fas/CD95)-associated proteins form a death-inducing signaling complex (DISC) with the receptor. EMBO J 1995;14: 5579-5588.
39. Liu X, Kim CN, Yang J, Jemmerson R, Wang X. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 1996;86:147-157.
40. Newmeyer DD, Ferguson-Miller S. Mitochondria: releasing power for life and unleashing the machineries of death. Cell 2003;112:481-490.
41. Krebs JJ, Hauser H, Carafoli E. Asymmetric distribution of phospholipids in the inner membrane of beef heart mitochondria. J Biol Chem 1979;254:5308-5316.
42. Ardail D, Privat JP, Egret-Charlier M, Levrat C, Lerme F, Louisot P. Mitochondrial contact sites. Lipid composition and dynamics. J Biol Chem 1990;265:18797-18802.
43. d e Kroon AI, Dolis D, Mayer A, Lill R, de Kruijff B. Phospholipid composition of highly purifi ed mitochondrial outer membranes of rat liver and Neurospora crassa. Is cardiolipin present in the mitochondrial outer membrane? Biochim Biophys Acta 1997;1325:108-116.
44. Eble KS, Coleman WB, Hantgan RR, Cunningham CC. 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.
45. Fry M, Green DE. Cardiolipin requirement for electron transfer in complex I and III of the mitochondrial respiratory chain. J Biol Chem 1981;256:1874-1880.
46. Montero J, Mari M, Colell A, Morales A, Basa ñ ez G, Garcia-Ruiz C, Fern á ndez-Checa JC. Cholesterol and peroxidized cardiolipin in mitochondrial membrane properties, permeabilization and cell death. Biochim Biophys Acta (BBA)-Bioenerg 2010;1797:1217-1224.
47. Rytomaa M, Mustonen P, Kinnunen PK. Reversible, nonionic, and pH-dependent association of cytochrome c with cardiolipin-phosphatidylcholine liposomes. J Biol Chem 1992;267:22243-22248.
48. Kagan VE, Tyurin VA, Jiang J, Tyurina YY, Ritov VB, Amoscato AA, et al. Cytochrome c acts as a cardiolipin oxygenase required for release of proapoptotic factors. Nat Chem Biol 2005;1:223-232.
49. Ott M, Robertson JD, Gogvadze V, Zhivotovsky B, Orrenius S. Cytochrome c release from mitochondria proceeds by a two-step process. Proc Natl Acad Sci USA 2002;99: 1259-1263.
50. Luo X, Budihardjo I, Zou H, Slaughter C, Wang X. Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 1998;94:481-490.
51. Li H, Zhu H, Xu CJ, Yuan J. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 1998;94:491-501.
52. Lutter M, Fang M, Luo X, Nishijima M, Xie X-s, Wang X. Cardiolipin provides specifi city for targeting of tBid to mitochondria. Nat Cell Biol 2000;2:754-761.
53. Esposti MD, Cristea IM, Gaskell SJ, Nakao Y, Dive C. Proapoptotic Bid binds to monolysocardiolipin, a new molecular connection between mitochondrial membranes and cell death. Cell Death Diff er 2003;10:1300-1309.
54. Zha J, Weiler S, Oh KJ, Wei MC, Korsmeyer SJ. Posttranslational N-myristoylation of BID as a molecular switch for targeting mitochondria and apoptosis. Science 2000;290: 1761-1765.
55. Florence TM. The degradation of cytochrome c by hydrogen peroxide. J Inorg Biochem 1985;23:131-141.
56. Radi R, Thomson L, Rubbo H, Prodanov E. Cytochrome c-catalyzed oxidation of organic molecules by hydrogen peroxide. Arch Biochem Biophys 1991;288:112-117.
57. Kagan VE, BayIr HA, Belikova NA, Kapralov O, Tyurina YY, et al. Cytochrome c/cardiolipin relations in mitochondria: a kiss of death. Free Radic Biol Med 2009;46: 1439-1453.
58. Liu J, Dai Q, Chen J, Durrant D, Freeman A, Liu T, Grossman D, Lee RM. Phospholipid scramblase 3 controls mitochondrial structure, function, and apoptotic response. Mol Cancer Res 2003;1:892-902.
59. Liu J, Chen J, Dai Q, Lee RM. Phospholipid scramblase 3 is the mitochondrial target of protein kinase C delta-induced apoptosis. Cancer Res 2003;63:1153-1156.
60. Belikova NA, Tyurina YY, Borisenko G, Tyurin V, Samhan Arias AK, Yanamala N, et al. Heterolytic reduction of fatty acid hydroperoxides by cytochrome c/cardiolipin complexes: antioxidant function in mitochondria. J Am Chem Soc 2009;131:11288-11289.
61. Iwahashi H, Nishizaki K, Takagi I. Cytochrome c catalyses the formation of pentyl radical and octanoic acid radical from linoleic acid hydroperoxide. Biochem J 2002;361:57-66.
62. Barr DP, Martin MV, Guengerich FP, Mason RP. Reaction of cytochrome P450 with cumene hydroperoxide: ESR spintrapping evidence for the homolytic scission of the peroxide O-O bond by ferric cytochrome P450 1A2. Chem Res Toxicol 1996;9:318-325.
63. Schlame M, Haller I, Sammaritano LR, Blanck TJ. Eff ect of cardiolipin oxidation on solid-phase immunoassay for antiphospholipid antibodies. Thromb Haemost 2001;86: 1475-1482.
64. Liu W, Yin H, Akazawa YO, Yoshida Y, Niki E, Porter NA. Ex Vivo Oxidation in Tissue and Plasma Assays of Hydroxyoctadecadienoates: Z,E/E,E Stereoisomer Ratios. Chem Res Toxicol 2010;23:986-995.
65. Cosgrove J, Church D, Pryor W. The kinetics of the autoxidation of polyunsaturated fatty acids. Lipids 1987;22: 299-304.
66. Bowry VW. Arm-to-Arm Autoxidation in a Triglyceride: Remote Group Reaction Kinetics. J Org Chem 1994;59: 2250-2252.
67. Roginsky V. Oxidizability of cardiac cardiolipin in Triton X-100 micelles as determined by using a Clark electrode. Chem Phys Lipids 2010;163:127-130.
68. Liu W, Porter NA, Schneider C, Brash AR, Yin H. Formation of 4-hydroxynonenal from cardiolipin oxidation: Intramolecular peroxyl radical addition and decomposition. Free Radic Biol Med 2011;50:166-178.
69. Uchida K. Role of reactive aldehyde in cardiovascular diseases. Free Radic Biol Med 2000;28:1685-1696.
70. Uchida K, Stadman ER. Covalent attachment of 4-hydroxynonenal to glyceraldehyde-3-phosphate dehydrogenase. A possible involvement of intra-and intermolecular cross-linking reaction. J Biol Chem 1993;268:6388-6393.
71. West JD, Marnett LJ. Endogenous reactive intermediates as modulators of cell signaling and cell death. Chem Res Toxicol 2006;19:173-194.
72. Schneider C, Porter NA, Brash AR. Routes to 4-hydroxynonenal: fundamental issues in the mechanisms of lipid peroxidation. J Biol Chem 2008;283:15539-15543.
73. Schneider C, Boeglin WE, Yin H, Porter NA, Brash AR. Intermolecular peroxyl radical reactions during autoxidation of hydroxy and hydroperoxy arachidonic acids generate a novel series of epoxidized products. Chem Res Toxicol 2008;21:895-903.
74. Benedetti A, Comporti M, Esterbauer H. Identifi cation of 4-hydroxynonenal as a cytotoxic product originating from the peroxidation of liver microsomal lipids. Biochim Biophys Acta 1980;620:281-296.
75. Moon KH, Lee YM, Song BJ. Inhibition of hepatic mitochondrial aldehyde dehydrogenase by carbon tetrachloride through JNK-mediated phosphorylation. Free Radic Biol Med 2010;48:391-398.
76. Ji C, Amarnath V, Pietenpol JA, Marnett LJ. 4-Hydroxynonenal Induces Apoptosis via Caspase-3 Activation and Cytochrome c Release. Chem Res Toxicol 2001;14:1090-1096.
77. Roede JR, Jones DP. Reactive species and mitochondrial dysfunction: Mechanistic signifi cance of 4-hydroxynonenal. Environ Mol Mutagen 2010;51:380-390.
78. Maciel E, Domingues P, Domingues MRM. Liquid chromatography/tandem mass spectrometry analysis of long-chain oxidation products of cardiolipin induced by the hydroxyl radical. Rapid Commun Mass Spectrom 2011;25: 316-326.
79. Domingues MRM, Reis A, Domingues P. Mass spectrometry analysis of oxidized phospholipids. Chem Phys Lipids 2008;156:1-12.
80. Maciel E, Domingues P, Marques D, Simõ e s C, Reis A, Oliveira MM, et al. Cardiolipin and oxidative stress: Identifi cation of new short chain oxidation products of cardiolipin in in vitro analysis and in nephrotoxic drug-induced disturbances in rat kidney tissue. Int J Mass Spectrom 2011; 301:62-73.
81. Dougherty TJ, Gomer CJ, Henderson BW, Jori G, Kessel D, Korbelik M, Moan J, Peng Q. Photodynamic therapy. J Natl Cancer Inst 1998;90:889-905.
82. Oleinick NL, Morris RL, Belichenko I. The role of apoptosis in response to photodynamic therapy: what, where, why, and how. Photochem Photobiol Sci 2002;1:1-21.
83. Cadet J, Ravanat JL, Martinez GR, Medeiros MH, Di Mascio P. Singlet oxygen oxidation of isolated and cellular DNA: product formation and mechanistic insights. Photochem Photobiol 2006;82:1219-1225.
84. Davies MJ. Reactive species formed on proteins exposed to singlet oxygen. Photochem Photobiol Sci 2004;3:17-25.
85. Miyamoto S, Martinez GR, Rettori D, Augusto O, Medeiros MHG, Di Mascio P. Linoleic acid hydroperoxide reacts with hypochlorous acid, generating peroxyl radical intermediates and singlet molecular oxygen. PNAS 2006;103:293-298.
86. Kanofsky JR, Wright J, Miles-Richardson GE, Tauber AI. Biochemical requirements for singlet oxygen production by purifi ed human myeloperoxidase. J Clin Invest 1984;74: 1489-1495.
87. Kanofsky JR. Singlet oxygen production by chloroperoxidasehydrogen peroxide-halide systems. J Biol Chem 1984;259: 5596-5600.
88. Davies MJ. Singlet oxygen-mediated damage to proteins and its consequences. Biochem Biophys Res Commun 2003; 305:761-770.
89. Kim J, Fujioka H, Oleinick NL, Anderson VE. Photosensitization of intact heart mitochondria by the phthalocyanine Pc 4: Correlation of structural and functional defi cits with cytochrome c release. Free Radic Biol Med 2010;49:726-732.
90. Kim J, Rodriguez ME, Oleinick NL, Anderson VE. Photooxidation of cardiolipin and cytochrome c with bilayerembedded Pc 4. Free Radic Biol Med 2010;49:718-725.
91. Orfanopoulos M, Foote CS. The ene reaction of singlet oxygen with olefi ns. Free Radic Res Commun 1987;2:321-326.
92. Thomas M, Pryor W. Singlet oxygen oxidation of methyl linoleate: Isolation and characterization of the NaBH 4-reduced products. Lipids 1980;15:544-548.
93. Tyurina YY, Tyurin VA, Epperly MW, Greenberger JS, Kagan VE. Oxidative lipidomics of [gamma]-irradiationinduced intestinal injury. Free Radic Biol Med 2008;44: 299-314.
94. Yurkova IL, Arnhold J, Fitzl G, Huster D. Fragmentation of mitochondrial cardiolipin by copper ions in the Atp7b/mouse model of Wilson's disease. Chem Phys Lipids 2011;164:393-400.
95. Shadyro OI, Glushonok GK, Glushonok TG, Edimecheva IP, Moroz AG, Sosnovskaya AA, Yurkova IL, Polozov GI. Quinones as free-radical fragmentation inhibitors in biologically important molecules. Free Radic Res 2002;36:859-867.
96. Shadyro OI, Yurkova IL, Kisel MA. Radiation-induced peroxidation and fragmentation of lipids in a model membrane. Int J Radiat Biol 2002;78:211-217.
97. Orrenius S. Reactive Oxygen Species in Mitochondria-Mediated Cell Death. Drug Metab Rev 2007;39:443-455.
98. Orrenius S, Zhivotovsky B. Cardiolipin oxidation sets cytochrome c free. Nat Chem Biol 2005;1:188-189.
99. Green DR, Kroemer G. The pathophysiology of mitochondrial cell death. Science 2004;305:626-629.
100. Nomura K, Imai H, Koumura T, Kobayashi T, Nakagawa Y. Mitochondrial phospholipid hydroperoxide glutathione peroxidase inhibits the release of cytochrome c from mitochondria by suppressing the peroxidation of cardiolipin in hypoglycaemia-induced apoptosis. Biochem J 2000;351: 183-193.
101. Ran Q, Liang H, Gu M, Qi W, Walter CA, Roberts LJ, II, Herman B, Richardson A, Van Remmen H. Transgenic mice overexpressing glutathione peroxidase 4 are protected against oxidative stress-induced apoptosis. J Biol Chem 2004;279: 55137-55146.
102. Enoksson M, Fernandes AP, Prast S, Lillig CH, Holmgren A, Orrenius S. Overexpression of glutaredoxin 2 attenuates apoptosis by preventing cytochrome c release. Biochem Biophys Res Commun 2005;327:774-779.
103. Gonzalvez F, Pariselli F, Dupaigne P, Budihardjo I, Lutter M, Antonsson B, et al. tBid interaction with cardiolipin primarily orchestrates mitochondrial dysfunctions and subsequently activates Bax and Bak. Cell Death Diff er 2005;12:614-626.
104. Gonzalvez F, Pariselli F, Jalmar O, Dupaigne P, Sureau F, Dellinger M, et al. Mechanistic issues of the interaction of the hairpin-forming domain of tBid with mitochondrial cardiolipin. PLoS One 2010;5:e9342.
105. Uren RT, Dewson G, Bonzon C, Lithgow T, Newmeyer DD, Kluck RM. Mitochondrial release of pro-apoptotic proteins: electrostatic interactions can hold cytochrome c but not Smac/DIABLO to mitochondrial membranes. J Biol Chem 2005;280:2266-2274.
106. Kuwana T, Mackey MR, Perkins G, Ellisman MH, Latterich M, Schneiter R, Green DR, Newmeyer DD. Bid, Bax, and lipids cooperate to form supramolecular openings in the outer mitochondrial membrane. Cell 2002;111:331-342.
107. Esposti MD. Lipids, cardiolipin and apoptosis: a greasy licence to kill. Cell Death Diff er 2002;9:234-236.
108. Kim TH, Zhao Y, Ding WX, Shin JN, He X, Seo YW, et a l. Bid-cardiolipin interaction at mitochondrial contact site contributes to mitochondrial cristae reorganization and cytochrome C release. Mol Biol Cell 2004;15:3061-3072.
109. Korytowski W, Basova LV, Pilat A, Kernstock RM, Girotti AW. Permeabilization of the mitochondrial outer membrane by Bax/Truncated Bid (tBid) proteins as sensitized by cardiolipin hydroperoxide translocation. J Biol Chem 2011;286: 26334-26343.
110. Kristal BS, Park BK, Yu BP. 4-Hydroxyhexenal is a potent inducer of the mitochondrial permeability transition. J Biol Chem 1996;271:6033-6038.
111. Jacobs AT, Marnett LJ. Heat shock factor 1 attenuates 4-hydroxynonenal-mediated apoptosis: critical role for heat shock protein 70 induction and stabilization of Bcl-XL. J Biol Chem 2007;282:33412-33420.
112. Jacobs AT, Marnett LJ. HSF1-mediated BAG3 expression attenuates apoptosis in 4-hydroxynonenal-treated colon cancer cells via stabilization of anti-apoptotic Bcl-2 proteins. J Biol Chem 2009;284:9176-9183.
113. Chaudhary P, Sharma R, Sharma A, Vatsyayan R, Yadav S, Singhal SS, et al. Mechanisms of 4-hydroxy-2-nonenal induced pro-and anti-apoptotic signaling. Biochemistry 2010;49:6263-6275.
114. Paradies G, Petrosillo G, Pistolese M, Di Venosa N, Federici A, Ruggiero FM. Decrease in mitochondrial complex I activity in ischemic/reperfused rat heart: involvement of reactive oxygen species and cardiolipin. Circ Res 2004;94:53-59.
115. Paradies G, Petrosillo G, Pistolese M, Ruggiero FM. The eff ect of reactive oxygen species generated from the mitochondrial electron transport chain on the cytochrome c oxidase activity and on the cardiolipin content in bovine heart submitochondrial particles. FEBS Lett 2000;466:323-326.
116. Paradies G, Petrosillo G, Pistolese M, Ruggiero FM. Reactive oxygen species aff ect mitochondrial electron transport complex I activity through oxidative cardiolipin damage. Gene 2002;286:135-141.
117. Paradies G, Ruggiero FM, Petrosillo G, Quagliariello E. Peroxidative damage to cardiac mitochondria: cytochrome oxidase and cardiolipin alterations. FEBS Lett 1998;424:155-158.
118. Paradies G, Petrosillo G, Pistolese M, Ruggiero FM. Reactive oxygen species generated by the mitochondrial respiratory chain aff ect the complex III activity via cardiolipin peroxidation in beef-heart submitochondrial particles. Mitochondrion 2001;1:151-159.
119. Musatov A. Contribution of peroxidized cardiolipin to inactivation of bovine heart cytochrome c oxidase. Free Radic Biol Med 2006;41:238-246.
120. Petersen DR, Doorn JA. Reactions of 4-hydroxynonenal with proteins and cellular targets. Free Radic Biol. Med. 2004; 37:937-945.
121. Chen JJ, Bertrand H, Yu BP. Inhibition of adenine nucleotide translocator by lipid peroxidation products. Free Radic Biol Med 1995;19:583-590.
122. Claypool SM, Koehler CM. The complexity of cardiolipin in health and disease. Trends in Biochemical Sciences 2012; 37:32-41
123. Galluzzi L, Morselli E, Kepp O, Vitale I, Rigoni A, Vacchelli E, et al. Mitochondrial gateways to cancer. Molecular Aspects of Medicine 2010;31:1-20.
124. Colquhoun A. Lipids, Mitochondria and cell death: implications in neuro-oncology. Mol Neurobiol 2010;42:76-88.
125. Pope S, Land JM, Heales SJ. Oxidative stress and mitochondrial dysfunction in neurodegeneration; cardiolipin a critical target? Biochim Biophys Acta 2008;1777:794-799.
126. Barth PG, Scholte HR, Berden JA, Van der Klei-Van Moorsel JM, Luyt-Houwen IE, Van ' t Veer-Korthof ET, Van der Harten JJ, Sobotka-Plojhar MA. An X-linked mitochondrial disease aff ecting cardiac muscle, skeletal muscle and neutrophil leucocytes. J Neurol Sci 1983;62:327-355.
127. Oram JF. Tangier disease and ABCA1. Biochim Biophys Acta 2000;1529:321-330.
128. Petrosillo G, Ruggiero FM, 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.
129. Chen Q, Moghaddas S, Hoppel CL, Lesnefsky EJ. Ischemic defects in the electron transport chain increase the production of reactive oxygen species from isolated rat heart mitochondria. Am J Physiol Cell Physiol 2008;294:C460-466.
130. Paradies G, Ruggiero FM, 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.
131. Paradies G, Ruggiero FM, Petrosillo G, Quagliariello E. Enhanced cytochrome oxidase activity and modifi cation of lipids in heart mitochondria from hyperthyroid rats. Biochim Biophys Acta 1994;1225:165-170.
132. Petrosillo G, Portincasa P, Grattagliano I, Casanova G, Matera M, Ruggiero FM, 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.
133. Han X, Yang J, Cheng H, Yang K, Abendschein DR, Gross RW. Shotgun lipidomics identifi es cardiolipin depletion in diabetic myocardium linking altered substrate utilization with mitochondrial dysfunction. Biochemistry 2005;44:16684-16694.
134. Zhao Z, Zhang X, Zhao C, Choi J, Shi J, Song K, Turk J, Ma ZA. Protection of pancreatic α-cells by group VIA phospholipase A2-mediated repair of mitochondrial membrane peroxidation. Endocrinology 2010;151:3038-3048.
135. Paradies G, Ruggiero FM, Petrosillo G, Quagliariello E. Agedependent decrease in the cytochrome c oxidase activity and changes in phospholipids in rat-heart mitochondria. Arch Gerontol Geriatr 1993;16:263-272.
136. Paradies G, Petrosillo G, Paradies V, Ruggiero FM. Mitochondrial dysfunction in brain aging: Role of oxidative stress and cardiolipin. Neurochem Int 2011;58:447-457.
137. Ostrander DB, Sparagna GC, Amoscato AA, McMillin JB, Dowhan W. Decreased cardiolipin synthesis corresponds with cytochrome c release in palmitate-induced cardiomyocyte apoptosis. J Biol Chem 2001;276:38061-38067.
138. Bione S, D'Adamo P, Maestrini E, Gedeon AK, Bolhuis PA, Toniolo D. A novel X-linked gene, G4.5. is responsible for Barth syndrome. Nat Genet 1996;12:385-389.
139. Valianpour F, Mitsakos V, Schlemmer D, Towbin JA, Taylor JM, Ekert PG, et al. Monolysocardiolipins accumulate in Barth syndrome but do not lead to enhanced apoptosis. J Lipid Res 2005;46:1182-1195.
140. K uijpers TW, Maianski NA, Tool AT, Becker K, Plecko B, Valianpour F, et al. Neutrophils in Barth syndrome (BTHS) avidly bind annexin-V in the absence of apoptosis. Blood 2004;103:3915-3923.
141. Choi SY, Gonzalvez F, Jenkins GM, Slomianny C, Chretien D, Arnoult D, Petit PX, Frohman MA. Cardiolipin defi ciency releases cytochrome c from the inner mitochondrial membrane and accelerates stimuli-elicited apoptosis. Cell Death Diff er 2007;14:597-606.
142. Tyurin VA, Tyurina YY, Feng W, Mnuskin A, Jiang J, Tang M, et al. Mass-spectrometric characterization of phospholipids and their primary peroxidation products in rat cortical neurons during staurosporine-induced apoptosis. J Neurochem 2008;107:1614-1633.
143. Bayir H, Tyurin VA, Tyurina YY, Viner R, Ritov V, Amoscato AA, et al. Selective early cardiolipin peroxidation after traumatic brain injury: an oxidative lipidomics analysis. Ann Neurol 2007;62:154-169.
144. Bayir H, Kapralov AA, Jiang J, Huang Z, Tyurina YY, Tyurin VA, et al. Peroxidase mechanism of lipid-dependent crosslinking of synuclein with cytochrome C: protection against apoptosis versus delayed oxidative stress in Parkinson disease. J Biol Chem 2009;284:15951-15969.
145. Atkinson J, Kapralov AA, Yanamala N, Tyurina YY, Amoscato AA, Pearce L, et al. A mitochondria-targeted inhibitor of cytochrome c peroxidase mitigates radiationinduced death. Nat Commun 2011;2:497.
146. Hoye AT, Davoren JE, Wipf P, Fink MP, Kagan VE. Targeting mitochondria. Acc Chem Res 2008;41:87-97.
147. Kagan VE, Bayir A, Bayir H, Stoyanovsky D, Borisenko GG, Tyurina YY, et al. Mitochondria-targeted disruptors and inhibitors of cytochrome c/cardiolipin peroxidase complexes: A new strategy in anti-apoptotic drug discovery. Mol Nutr Food Res 2009;53:104-114.
148. Wipf P, Xiao J, Jiang J, Belikova NA, Tyurin VA, Fink MP, Kagan VE. Mitochondrial Targeting of Selective Electron Scavengers: Synthesis and Biological Analysis of Hemigramicidin-TEMPO Conjugates. J Am Chem Soc 2005;127:12460-12461.
149. Kagan VE, Wipf P, Stoyanovsky D, Greenberger JS, Borisenko G, Belikova NA, et al. Mitochondrial targeting of electron scavenging antioxidants: Regulation of selective oxidation vs random chain reactions. Adv Drug Deliv Rev 2009;61:1375-1385.
150. Belikova NA, Jiang J, Stoyanovsky DA, Glumac A, Bayir H, Greenberger JS, Kagan VE. Mitochondria-targeted (2-hydroxyamino-vinyl)-triphenyl-phosphonium releases NO(.) and protects mouse embryonic cells against irradiation-induced apoptosis. FEBS Lett 2009;583:1945-1950.
151. Macias C, Chiao J, Xiao J, Arora D, Tyurina Y, Delude R, et al. Treatment with a novel hemigramicidin-TEMPO conjugate prolongs survival in a rat model of lethal hemorrhagic shock. Ann Surg 2007;245:305-314.
152. Arce PM, Khdour OM, Goldschmidt R, Armstrong JS, Hecht SM. A strategy for suppressing redox stress within mitochondria. ACS Med Chem Lett 2011;2:608-613.