Mitochondria in vascular disease

Cardiovascular Research

Volumn 95, Issue 2, 2012, Pages 173-182

  Yu, Emma ^a   Mercer, John ^a   Bennett, Martin ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Atherosclerosis; DNA damage; Mitochondria; Reactive oxygen species

Indexed keywords

CALCIUM; LOSARTAN; REACTIVE OXYGEN METABOLITE; SUPEROXIDE;

APOPTOSIS; ATHEROSCLEROSIS; CELL AGING; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DNA DAMAGE; DRUG MECHANISM; HUMAN; MITOCHONDRION; NONHUMAN; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; VASCULAR DISEASE;

ANIMALS; DNA DAMAGE; DNA, MITOCHONDRIAL; HUMANS; MITOCHONDRIA; MITOCHONDRIAL DISEASES; REACTIVE OXYGEN SPECIES; VASCULAR DISEASES;

EID: 84863712400     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvs111     Document Type: Review

References (132)

1. Levi F, Chatenoud L, Bertuccio P, Lucchini F, Negri E, La Vecchia C. Mortality from cardiovascular and cerebrovascular diseases in Europe and other areas of the world: an update. Eur J Cardiovasc Prev Rehabil 2009;16:333-350.
2. Libby P, Ridker PM, Hansson GK. Progress and challenges in translating the biology of atherosclerosis. Nature 2011;473:317-325.
3. Morel DW, DiCorleto PE, Chisolm GM. Endothelial and smooth muscle cells alter low density lipoprotein in vitro by free radical oxidation. Arteriosclerosis 1984;4: 357-364. (Pubitemid 14092678)
4. Parthasarathy S, Wieland E, Steinberg D. A role for endothelial cell lipoxygenase in the oxidative modification of low density lipoprotein. Proc Natl Acad Sci USA 1989;86: 1046-1050. (Pubitemid 19056287)
5. Clarke MC, Figg N, Maguire JJ, Davenport AP, Goddard M, Littlewood TD et al. Apoptosis of vascular smooth muscle cells induces features of plaque vulnerability in atherosclerosis. Nat Med 2006;12:1075-1080. (Pubitemid 44353389)
6. Thorp E, Li Y, Bao L, Yao PM, Kuriakose G, Rong J et al. Brief report: increased apoptosis in advanced atherosclerotic lesions of Apoe2/2 mice lacking macrophage Bcl-2. Arterioscler Thromb Vasc Biol 2009;29:169-172.
7. Catalano D, Licciulli F, Turi A, Grillo G, Saccone C, D'Elia D. MitoRes: a resource of nuclear-encoded mitochondrial genes and their products in Metazoa. BMC Bioinformatics 2006;7:36.
8. Yamano K, Kuroyanagi-Hasegawa M, Esaki M, Yokota M, Endo T. Step-size analyses of the mitochondrial Hsp70 import motor reveal the Brownian ratchet in operation. J Biol Chem 2008;283:27325-27332.
9. Turrens JF. Mitochondrial formation of reactive oxygen species. J Physiol 2003;552: 335-344. (Pubitemid 37321833)
10. Turrens JF, Boveris A. Generation of superoxide anion by the NADH dehydrogenase of bovine heart mitochondria. Biochem J 1980;191:421-427.
11. Chance B, Sies H, Boveris A. Hydroperoxide metabolism in mammalian organs. Physiol Rev 1979;59:527-605. (Pubitemid 9236599)
12. Chen ZX, Pervaiz S. BCL-2: pro-or anti-oxidant? Front Biosci (Elite Ed) 2009;1: 263-268.
13. Beckman JS, Koppenol WH. Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly. Am J Physiol 1996;271:C1424-C1437.
14. Keisari Y, Braun L, Flescher E. The oxidative burst and related phenomena in mouse macrophages elicited by different sterile inflammatory stimuli. Immunobiology 1983; 165:78-89. (Pubitemid 13075939)
15. Mittal CK, Murad F. Activation of guanylate cyclase by superoxide dismutase and hydroxyl radical: a physiological regulator of guanosine 3′,5′-monophosphate formation. Proc Natl Acad Sci USA 1977;74:4360-4364. (Pubitemid 8225122)
16. Ignarro LJ, Kadowitz PJ. The pharmacological and physiological role of cyclic GMP in vascular smooth muscle relaxation. Annu Rev Pharmacol Toxicol 1985;25:171-191. (Pubitemid 15090979)
17. Baas AS, Berk BC. Differential activation of mitogen-activated protein kinases by H2O2 and O2 2 in vascular smooth muscle cells. Circ Res 1995;77:29-36.
18. Li PF, Dietz R, von Harsdorf R. Differential effect of hydrogen peroxide and superoxide anion on apoptosis and proliferation of vascular smooth muscle cells. Circulation 1997;96:3602-3609. (Pubitemid 27513439)
19. Du XL, Edelstein D, Rossetti L, Fantus IG, Goldberg H, Ziyadeh F et al. Hyperglycemia-induced mitochondrial superoxide overproduction activates the hexosamine pathway and induces plasminogen activator inhibitor-1 expression by increasing Sp1 glycosylation. Proc Natl Acad Sci USA 2000;97:12222-12226.
20. Yamagishi SI, Edelstein D, Du XL, Kaneda Y, Guzman M, Brownlee M. Leptin induces mitochondrial superoxide production and monocyte chemoattractant protein-1 expression in aortic endothelial cells by increasing fatty acid oxidation via protein kinase A. J Biol Chem 2001;276:25096-25100.
21. Turrens JF, Freeman BA, Levitt JG, Crapo JD. The effect of hyperoxia on superoxide production by lung submitochondrial particles. Arch Biochem Biophys 1982;217: 401-410. (Pubitemid 13180648)
22. Kowaltowski AJ, de Souza-Pinto NC, Castilho RF, Vercesi AE. Mitochondria and reactive oxygen species. Free Radic Biol Med 2009;47:333-343.
23. Komary Z, Tretter L, Adam-Vizi V. H2O2 generation is decreased by calcium in isolated brain mitochondria. Biochim Biophys Acta 2008;1777:800-807.
24. Brookes PS, Yoon Y, Robotham JL, Anders MW, Sheu SS. Calcium, ATP, and ROS: a mitochondrial love-hate triangle. Am J Physiol Cell Physiol 2004;287:C817-C833. (Pubitemid 39238305)
25. Alderton WK, Cooper CE, Knowles RG. Nitric oxide synthases: structure, function and inhibition. Biochem J 2001;357:593-615. (Pubitemid 32735142)
26. Cleeter MW, Cooper JM, Darley-Usmar VM, Moncada S, Schapira AH. 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.
27. Lee JH, Paull TT. ATM activation by DNA double-strand breaks through the Mre11-Rad50-Nbs1 complex. Science 2005;308:551-554. (Pubitemid 40570585)
28. Echtay KS, Roussel D, St-Pierre J, Jekabsons MB, Cadenas S, Stuart JA et al. Superoxide activates mitochondrial uncoupling proteins. Nature 2002;415:96-99. (Pubitemid 34062457)
29. De Stefani D, Raffaello A, Teardo E, Szabo I, Rizzuto R. A forty-kilodalton protein of the inner membrane is the mitochondrial calcium uniporter. Nature 2011;476: 336-340.
30. Lawrie AM, Rizzuto R, Pozzan T, Simpson AW. A role for calcium influx in the regulation of mitochondrial calcium in endothelial cells. J Biol Chem 1996;271: 10753-10759. (Pubitemid 26145812)
31. Rizzuto R, Pinton P, Carrington W, Fay FS, Fogarty KE, Lifshitz LM et al. Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca2+ responses. Science 1998;280:1763-1766. (Pubitemid 28283502)
32. Szabadkai G, Duchen MR. Mitochondria: the hub of cellular Ca2+ signaling. Physiology (Bethesda) 2008;23:84-94.
33. Carafoli E. Calcium pump of the plasma membrane. Physiol Rev 1991;71:129-153.
34. MacLennan DH, Rice WJ, Green NM. The mechanism of Ca2+ transport by sarco( endo)plasmic reticulum Ca2+-ATPases. J Biol Chem 1997;272:28815-28818. (Pubitemid 27498155)
35. Krishnan K, Reeve A, Samuels D, Chinnery P, Blackwood J, Taylor R et al. What causes mitochondrial DNA deletions in human cells? Nature Genetics 2008;40: 275-279. (Pubitemid 351311775)
36. Botto N, Berti S, Manfredi S, Al-Jabri A, Federici C, Clerico A et al. Detection of mtDNA with 4977 bp deletion in blood cells and atherosclerotic lesions of patients with coronary artery disease. Mutat Res 2005;570:81-88. (Pubitemid 40179270)
37. Ballinger SW, Patterson C, Yan CN, Doan R, Burow DL, Young CG et al. Hydrogen peroxide-and peroxynitrite-induced mitochondrial DNA damage and dysfunction in vascular endothelial and smooth muscle cells. Circ Res 2000;86:960-966. (Pubitemid 30324308)
38. Ballinger SW, Patterson C, Knight-Lozano CA, Burow DL, Conklin CA, Hu Z et al. Mitochondrial integrity and function in atherogenesis. Circulation 2002;106:544-549. (Pubitemid 34827702)
39. Knight-Lozano CA, Young CG, Burow DL, Hu ZY, Uyeminami D, Pinkerton KE et al. Cigarette smoke exposure and hypercholesterolemia increase mitochondrial damage in cardiovascular tissues. Circulation 2002;105:849-854. (Pubitemid 34174926)
40. Mercer JR, Cheng KK, Figg N, Gorenne I, Mahmoudi M, Griffin J et al. DNA damage links mitochondrial dysfunction to atherosclerosis and the metabolic syndrome. Circ Res 2010;107:1021-1031.
41. Harrison CM, Pompilius M, Pinkerton KE, Ballinger SW. Mitochondrial oxidative stress significantly influences atherogenic risk and cytokine-induced oxidant production. Environ Health Perspect 2010;119:676-681.
42. Nakase H, Moraes CT, Rizzuto R, Lombes A, DiMauro S, Schon EA. Transcription and translation of deleted mitochondrial genomes in Kearns-Sayre syndrome: implications for pathogenesis. Am J Hum Genet 1990;46:418-427.
43. Wallace DC. Mitochondrial diseases in man and mouse. Science 1999;283: 1482-1488.
44. Puddu P, Puddu GM, Cravero E, De Pascalis S, Muscari A. The emerging role of cardiovascular risk factor-induced mitochondrial dysfunction in atherogenesis. J Biomed Sci 2009;16:112.
45. Armani C, Landini L Jr, Leone A. Molecular and biochemical changes of the cardiovascular system due to smoking exposure. Curr Pharm Des 2009;15:1038-1053.
46. Wang PW, Lin TK, Weng SW, Liou CW. Mitochondrial DNA variants in the pathogenesis of type 2 diabetes-relevance of Asian population studies. Rev Diabet Stud 2009;6:237-246.
47. Amaral S, Oliveira PJ, Ramalho-Santos J. Diabetes and the impairment of reproductive function: possible role of mitochondria and reactive oxygen species. Curr Diabetes Rev 2008;4:46-54. (Pubitemid 351210972)
48. Medina-Gomez G, Vidal-Puig A. Gateway to the metabolic syndrome. Nat Med 2005;11:602-603. (Pubitemid 40868299)
49. Gredilla R. DNA damage and base excision repair in mitochondria and their role in aging. J Aging Res 2010;2011:257093.
50. Chan NC, Chan DC. Parkin uses the UPS to ship off dysfunctional mitochondria. Autophagy 2011;7:771-772.
51. Chen H, Detmer SA, Ewald AJ, Griffin EE, Fraser SE, Chan DC. Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. J Cell Biol 2003;160:189-200. (Pubitemid 36254953)
52. Bleazard W, McCaffery JM, King EJ, Bale S, Mozdy A, Tieu Q et al. The dynaminrelated GTPase Dnm1 regulates mitochondrial fission in yeast. Nat Cell Biol 1999; 1:298-304. (Pubitemid 129495781)
53. Ono T, Isobe K, Nakada K, Hayashi JI. Human cells are protected from mitochondrial dysfunction by complementation of DNA products in fused mitochondria. Nat Genet 2001;28:272-275. (Pubitemid 32626031)
54. Parone PA, Da Cruz S, Tondera D, Mattenberger Y, James DI, Maechler P et al. Preventing mitochondrial fission impairs mitochondrial function and leads to loss of mitochondrial DNA. PLoS One 2008;3:e3257.
55. Liu C, Lin JD. PGC-1 coactivators in the control of energy metabolism. Acta Biochim Biophys Sin (Shanghai) 2011;43:248-257.
56. Spiegelman BM. Transcriptional control of energy homeostasis through the PGC1 coactivators. Novartis Found Symp 2007;286:3-6; discussion 6-12, 162-163, 196-203.
57. Jones AW, Yao Z, Vicencio JM, Karkucinska-Wieckowska A, Szabadkai G. PGC-1 family coactivators and cell fate: roles in cancer, neurodegeneration, cardiovascular disease and retrograde mitochondria-nucleus signalling. Mitochondrion 2011;12: 86-99.
58. Wareski P, Vaarmann A, Choubey V, Safiulina D, Liiv J, Kuum M et al. PGC-1a and PGC-1b regulate mitochondrial density in neurons. J Biol Chem 2009;284: 21379-21385.
59. Wadosky KM, Willis MS. The story so far: post-translational regulation of peroxisome proliferator-activated receptors (PPARs) by ubiquitination and SUMOylation. Am J Physiol Heart Circ Physiol 2011;302:H515-H526.
60. Giunta S, Jackson SP. Give me a break, but not in mitosis: the mitotic DNA damage response marks DNA double-strand breaks with early signaling events. Cell Cycle 2011;10:1215-1221.
61. van Attikum H, Gasser SM. Crosstalk between histone modifications during the DNA damage response. Trends Cell Biol 2009;19:207-217.
62. Falck J, Coates J, Jackson SP. Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage. Nature 2005;434:605-611. (Pubitemid 40488547)
63. Shieh SY, Ahn J, Tamai K, Taya Y, Prives C. The human homologs of checkpoint kinases Chk1 and Cds1 (Chk2) phosphorylate p53 at multiple DNA damage-inducible sites. Genes Dev 2000;14:289-300. (Pubitemid 30106484)
64. Pitkanen S, Robinson BH. Mitochondrial complex I deficiency leads to increased production of superoxide radicals and induction of superoxide dismutase. J Clin Invest 1996;98:345-351. (Pubitemid 26255732)
65. Esposito LA, Melov S, Panov A, Cottrell BA, Wallace DC. Mitochondrial disease in mouse results in increased oxidative stress. Proc Natl Acad Sci USA 1999;96: 4820-4825. (Pubitemid 29214495)
66. 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.
67. 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. (Pubitemid 38064098)
68. Yan LJ, Sohal RS. Mitochondrial adenine nucleotide translocase is modified oxidatively during aging. Proc Natl Acad Sci USA 1998;95:12896-12901. (Pubitemid 28509494)
69. Kokoszka JE, Coskun P, Esposito LA,Wallace DC. Increased mitochondrial oxidative stress in the Sod2 ( +2) mouse results in the age-related decline of mitochondrial function culminating in increased apoptosis. Proc Natl Acad Sci USA 2001;98: 2278-2283. (Pubitemid 32209473)
70. Minamino T, Komuro I, Kitakaze M. Endoplasmic reticulum stress as a therapeutic target in cardiovascular disease. Circ Res 2010;107:1071-1082.
71. Saotome M, Katoh H, Satoh H, Nagasaka S, Yoshihara S, Terada H et al. Mitochondrial membrane potential modulates regulation of mitochondrial Ca2+ in rat ventricular myocytes. Am J Physiol Heart Circ Physiol 2005;288:H1820-H1828. (Pubitemid 40418009)
72. McCormack JG, Halestrap AP, Denton RM. Role of calcium ions in regulation of mammalian intramitochondrial metabolism. Physiol Rev 1990;70:391-425. (Pubitemid 20140186)
73. Haworth RA, Hunter DR. The Ca2+-induced membrane transition in mitochondria. II. Nature of the Ca2+ trigger site. Arch Biochem Biophys 1979;195:460-467. (Pubitemid 9235078)
74. Halestrap AP. What is the mitochondrial permeability transition pore? J Mol Cell Cardiol 2009;46:821-831.
75. Varanyuwatana P, Halestrap AP. The roles of phosphate and the phosphate carrier in the mitochondrial permeability transition pore. Mitochondrion 2011;12:120-125.
76. Zoratti M, Szabo I. The mitochondrial permeability transition. Biochim Biophys Acta 1995;1241:139-176.
77. 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. (Pubitemid 26256586)
78. Susin SA, Lorenzo HK, Zamzami N, Marzo I, Snow BE, Brothers GM et al. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 1999;397: 441-446.
79. Du C, Fang M, Li Y, Li L,Wang X. Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell 2000;102: 33-42.
80. Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M, Alnemri ES et al. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 1997;91:479-489. (Pubitemid 27508237)
81. Wallace DC. A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annu Rev Genet 2005;39: 359-407. (Pubitemid 43011120)
82. Quinsay MN, Lee Y, Rikka S, Sayen MR, Molkentin JD, Gottlieb RA et al. Bnip3 mediates permeabilization of mitochondria and release of cytochrome c via a novel mechanism. J Mol Cell Cardiol 2009;48:1146-1156.
83. Hayflick L. The limited in vitro lifetime of human diploid cell strains. Exp Cell Res 1965;37:614-636.
84. ZwerschkeW, Mazurek S, Stockl P, Hutter E, Eigenbrodt E, Jansen-Durr P. Metabolic analysis of senescent human fibroblasts reveals a role for AMP in cellular senescence. Biochem J 2003;376:403-411. (Pubitemid 38010525)
85. Hardie DG, Carling D. The AMP-activated protein kinase-fuel gauge of the mammalian cell? Eur J Biochem 1997;246:259-273. (Pubitemid 27232500)
86. Wang W, Yang X, Lopez de Silanes I, Carling D, Gorospe M. Increased AMP:ATP ratio and AMP-activated protein kinase activity during cellular senescence linked to reduced HuR function. J Biol Chem 2003;278:27016-27023. (Pubitemid 36876855)
87. Wang W, Fan J, Yang X, Furer-Galban S, Lopez de Silanes I, von Kobbe C et al. AMP-activated kinase regulates cytoplasmic HuR. Mol Cell Biol 2002;22:3425-3436. (Pubitemid 34453982)
88. Kukat A, Edgar D, Bratic I, Maiti P, Trifunovic A. Random mtDNA mutations modulate proliferation capacity in mouse embryonic fibroblasts. Biochem Biophys Res Commun 2011;409:394-399.
89. Lutgens E, de Muinck ED, Kitslaar PJ, Tordoir JH, Wellens HJ, Daemen MJ. Biphasic pattern of cell turnover characterizes the progression from fatty streaks to ruptured human atherosclerotic plaques. Cardiovasc Res 1999;41:473-479. (Pubitemid 29087344)
90. Clarke MC, Littlewood TD, Figg N, Maguire JJ, Davenport AP, Goddard M et al. Chronic apoptosis of vascular smooth muscle cells accelerates atherosclerosis and promotes calcification and medial degeneration. Circ Res 2008;102:1529-1538.
91. Ross R. Cell biology of atherosclerosis. Annu Rev Physiol 1995;57:791-804.
92. Chen J, Mehta JL, Haider N, Zhang X, Narula J, Li D. Role of caspases in Ox-LDL-induced apoptotic cascade in human coronary artery endothelial cells. Circ Res 2004;94:370-376. (Pubitemid 38240729)
93. Davidson SM, Duchen MR. Endothelial mitochondria: contributing to vascular function and disease. Circ Res 2007;100:1128-1141. (Pubitemid 46684126)
94. Ross R, Wight TN, Strandness E, Thiele B. Human atherosclerosis. I. Cell constitution and characteristics of advanced lesions of the superficial femoral artery. Am J Pathol 1984;114:79-93. (Pubitemid 14179856)
95. Bennett MR, Macdonald K, Chan SW, Boyle JJ, Weissberg PL. Cooperative interactions between RB and p53 regulate cell proliferation, cell senescence, and apoptosis in human vascular smooth muscle cells from atherosclerotic plaques. Circ Res 1998; 82:704-712. (Pubitemid 28160711)
96. Matthews C, Gorenne I, Scott S, Figg N, Kirkpatrick P, Ritchie A et al. Vascular smooth muscle cells undergo telomere-based senescence in human atherosclerosis: effects of telomerase and oxidative stress. Circ Res 2006;99:156-164. (Pubitemid 44297039)
97. Crass MF 3rd, Borst SE, Scarpace PJ. Beta-adrenergic responsiveness in cultured aorta smooth muscle cells. Effects of subculture and aging. Biochem Pharmacol 1992;43:1811-1815.
98. Robert L, Robert AM, Jacotot B. Elastin-elastase-atherosclerosis revisited. Atherosclerosis 1998;140:281-295. (Pubitemid 28535319)
99. Gorenne I, Kavurma M, Scott S, Bennett M. Vascular smooth muscle cell senescence in atherosclerosis. Cardiovasc Res 2006;72:9-17. (Pubitemid 44310633)
100. Rosca MG, Hoppel CL. Mitochondria in heart failure. Cardiovasc Res 2010;88:40-50.
101. Halestrap AP. Calcium, mitochondria and reperfusion injury: a pore way to die. Biochem Soc Trans 2006;34:232-237.
102. Kearney PM, Whelton M, Reynolds K, Muntner P, Whelton PK, He J. Global burden of hypertension: analysis of worldwide data. Lancet 2005;365:217-223. (Pubitemid 40138015)
103. Zalba G, San Jose G, Moreno MU, Fortuno MA, Fortuno A, Beaumont FJ et al. Oxidative stress in arterial hypertension: role of NAD(P)H oxidase. Hypertension 2001; 38:1395-1399. (Pubitemid 34033422)
104. Abadir PM, Foster DB, Crow M, Cooke CA, Rucker JJ, Jain A et al. Identification and characterization of a functional mitochondrial angiotensin system. Proc Natl Acad Sci USA 2011;108:14849-14854.
105. Cook JL, Re RN. Invited Review: Lessons from in vitro studies and a related intracellular angiotensin II transgenic mouse model. Am J Physiol Regul Integr Comp Physiol 2011;302:R482-R493.
106. Rodrigues SF, Granger DN. Cerebral microvascular inflammation in DOCA saltinduced hypertension: role of angiotensin II and mitochondrial superoxide. J Cereb Blood Flow Metab 2011;32:368-75.
107. Kubo SH, Rector TS, Bank AJ, Williams RE, Heifetz SM. Endothelium-dependent vasodilation is attenuated in patients with heart failure. Circulation 1991;84: 1589-1596.
108. Drexler H, Hayoz D, Munzel T, Hornig B, Just H, Brunner HR et al. Endothelial function in chronic congestive heart failure. Am J Cardiol 1992;69:1596-1601.
109. Irwin MW, Mak S, Mann DL, Qu R, Penninger JM, Yan A et al. Tissue expression and immunolocalization of tumor necrosis factor-alpha in postinfarction dysfunctional myocardium. Circulation 1999;99:1492-1498. (Pubitemid 29140917)
110. Corda S, Laplace C, Vicaut E, Duranteau J. Rapid reactive oxygen species production by mitochondria in endothelial cells exposed to tumor necrosis factor-alpha is mediated by ceramide. Am J Respir Cell Mol Biol 2001;24:762-768. (Pubitemid 32550600)
111. Bauersachs J, Bouloumie A, Fraccarollo D, Hu K, Busse R, Ertl G. Endothelial dysfunction in chronic myocardial infarction despite increased vascular endothelial nitric oxide synthase and soluble guanylate cyclase expression: role of enhanced vascular superoxide production. Circulation 1999;100:292-298. (Pubitemid 29340137)
112. Braunwald E, Kloner RA. Myocardial reperfusion: a double-edged sword? J Clin Invest 1985;76:1713-1719. (Pubitemid 16196036)
113. Carden DL, Granger DN. Pathophysiology of ischaemia-reperfusion injury. J Pathol 2000;190:255-266. (Pubitemid 30141372)
114. Freude B, Masters TN, Robicsek F, Fokin A, Kostin S, Zimmermann R et al. Apoptosis is initiated by myocardial ischemia and executed during reperfusion. J Mol Cell Cardiol 2000;32:197-208. (Pubitemid 30670343)
115. Therade-Matharan S, Laemmel E, Duranteau J, Vicaut E. Reoxygenation after hypoxia and glucose depletion causes reactive oxygen species production by mitochondria in HUVEC. Am J Physiol Regul Integr Comp Physiol 2004;287:R1037-R1043. (Pubitemid 39391047)
116. Brown MS, Goldstein JL. Heart attacks: gone with the century? Science 1996;272:629. (Pubitemid 26152774)
117. Safarova MS, Trukhacheva EP, Ezhov MV, Afanas'eva OI, Afanas'eva MI, Tripoten MI et al. Pleiotropic effects of nicotinic acid therapy in men with coronary heart disease and elevated lipoprotein(a) levels. Kardiologiia 2011;51:9-16.
118. Mahmoudi M, Gorenne I, Mercer J, Figg N, Littlewood T, Bennett M. Statins use a novel Nijmegen breakage syndrome-1-dependent pathway to accelerate DNA repair in vascular smooth muscle cells. Circ Res 2008;103:717-725.
119. Bouitbir J, Charles AL, Echaniz-Laguna A, Kindo M, Daussin F, Auwerx J et al. Opposite effects of statins on mitochondria of cardiac and skeletal muscles: a 'mitohormesis' mechanism involving reactive oxygen species and PGC-1. Eur Heart J 2011; doi:10.1093/eurheartj/ehr1224.
120. James AM, Cocheme HM, Smith RA, Murphy MP. Interactions of mitochondriatargeted and untargeted ubiquinones with the mitochondrial respiratory chain and reactive oxygen species. Implications for the use of exogenous ubiquinones as therapies and experimental tools. J Biol Chem 2005;280:21295-21312. (Pubitemid 40805692)
121. Graham D, Huynh NN, Hamilton CA, Beattie E, Smith RA, Cocheme HM et al. Mitochondria-targeted antioxidant MitoQ10 improves endothelial function and attenuates cardiac hypertrophy. Hypertension 2009;54:322-328.
122. Adlam VJ, Harrison JC, Porteous CM, James AM, Smith RA, Murphy MP et al. Targeting an antioxidant to mitochondria decreases cardiac ischemia-reperfusion injury. FASEB J 2005;19:1088-1095. (Pubitemid 40946434)
123. Mercer JR, Yu E, Figg N, Cheng KK, Prime TA, Griffin JL et al. The mitochondriatargeted antioxidant MitoQ decreases features of the metabolic syndrome in ATM +2/ApoE2/2 mice. Free Radic Biol Med 2011;52:841-849.
124. Taylor EB, Rutter J. Mitochondrial quality control by the ubiquitin-proteasome system. Biochem Soc Trans 2011;39:1509-1513.
125. Taylor RC, Dillin A. Aging as an event of proteostasis collapse. Cold Spring Harb Perspect Biol 2011;3; doi:10.1101/cshperspect.a004440.
126. Ben-Zvi A, Miller EA, Morimoto RI. Collapse of proteostasis represents an early molecular event in Caenorhabditis elegans aging. Proc Natl Acad Sci USA 2009;106: 14914-14919.
127. Trifunovic A, Larsson NG. Mitochondrial dysfunction as a cause of ageing. J Intern Med 2008;263:167-178.
128. Safdar A, Bourgeois JM, Ogborn DI, Little JP, Hettinga BP, Akhtar M et al. Endurance exercise rescues progeroid aging and induces systemic mitochondrial rejuvenation in mtDNA mutator mice. Proc Natl Acad Sci USA 2011;108:4135-4140.
129. Conley KE, Jubrias SA, Amara CE, Marcinek DJ. Mitochondrial dysfunction: impact on exercise performance and cellular aging. Exerc Sport Sci Rev 2007;35:43-49. (Pubitemid 46597375)
130. Schiff M, Benit P, Coulibaly A, Loublier S, El-Khoury R, Rustin P. Mitochondrial response to controlled nutrition in health and disease. Nutr Rev 2011;69:65-75.
131. Cerqueira FM, Laurindo FR, Kowaltowski AJ. Mild mitochondrial uncoupling and calorie restriction increase fasting eNOS, akt and mitochondrial biogenesis. PLoS One 2011;6:e18433.
132. Shimazu T, Hirschey MD, Hua L, Dittenhafer-Reed KE, Schwer B, Lombard DB et al. SIRT3 deacetylates mitochondrial 3-hydroxy-3-methylglutaryl CoA synthase 2 and regulates ketone body production. Cell Metab 2010;12:654-661.