Mitochondrial-nuclear cross-talk in the aging and failing heart

Cardiovascular Drugs and Therapy

Volumn 20, Issue 6, 2006, Pages 477-491

  Marín García, José ^a,b   Pi, YeQing ^a   Goldenthal, Michael J ^a  

^a The Molecular Cardiology and Neuromuscular Institute   (United States)

^b Molecular Cardiology Institute   (United States)

Author keywords

Aging; Gene expression; Heart failure; Mitochondria; Nuclear genes

Indexed keywords

MITOCHONDRIAL DNA; REACTIVE OXYGEN METABOLITE;

AGING; APOPTOSIS; BIOENERGY; BIOGENESIS; CARBOHYDRATE METABOLISM; CATABOLISM; CELL NUCLEUS; DOWN REGULATION; ENERGY; FATTY ACID METABOLISM; GENE EXPRESSION; GENE FUNCTION; GENE MUTATION; GENE OVEREXPRESSION; HEART FAILURE; HUMAN; MICROARRAY ANALYSIS; MITOCHONDRION; NONHUMAN; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEOMICS; RESPIRATORY CHAIN; REVIEW;

AGING; ANIMALS; APOPTOSIS; DNA, MITOCHONDRIAL; ENERGY METABOLISM; GENE EXPRESSION; HEART FAILURE, CONGESTIVE; HUMANS; MITOCHONDRIA, HEART; MUTATION; REACTIVE OXYGEN SPECIES;

EID: 33846405245     PISSN: 09203206     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10557-006-0584-6     Document Type: Review

References (139)

1. Acehan D, Jiang X, Morgan DG, Heuser JE, Wang X, Akey CW. Three-dimensional structure of the apoptosome: implications for assembly, procaspase-9 binding, and activation. Mol Cell 2002;9:423-32.
2. Andreu AL, Arbos MA, Perez-Martos A, Lopez-Perez MJ, Asin J, Lopez N, et al. Reduced mitochondrial DNA transcription in senescent rat heart. Biochem Biophys Res Commun 1998;252:577-81.
3. Arai T, Nakahara K, Matsuoka H, Sawabe M, Chida K, Matsushita S, et al. Age-related mitochondrial DNA deletion in human heart: its relationship with cardiovascular diseases. Aging Clin Exp Res 2003;15:1-5.
4. Attardi G, Schatz G. Biogenesis of mitochondria. Annu Rev Cell Biol 1988;4:289-333.
5. Barazzoni R, Short KR, Nair KS. Effects of aging on mitochondrial DNA copy number and cytochrome c oxidase gene expression in rat skeletal muscle, liver, and heart. J Biol Chem 2000;275:3343-7.
6. Barger PM, Brandt JM, Leone TC, Weinheimer CJ, Kelly DP. Deactivation of peroxisome proliferator-activated receptor-alpha during cardiac hypertrophic growth. J Clin Invest 2000;105:1723-30.
7. Benjamin IJ, Schneider MD. Learning from failure: congestive heart failure in the postgenomic age. J Clin Invest 2005;115:495-9.
8. Bodyak N, Kang PM, Hiromura M, Sulijoadikusumo I, Horikoshi N, Khrapko K, et al. Gene expression profiling of the aging mouse cardiac myocytes. Nucleic Acids Res 2002;30:3788-94.
9. Brookes PS, Darley-Usmar VM. Role of calcium and superoxide dismutase in sensitizing mitochondria to peroxynitrite-induced permeability transition. Am J Physiol Heart Circ Physiol 2004;286:H39-46.
10. Brown GC. Nitric oxide and mitochondrial respiration. Biochim Biophys Acta 1999;1411:351-69.
11. Capetanaki Y. Desmin cytoskeleton: a potential regulator of muscle mitochondrial behavior and function. Trends Cardiovasc Med 2002;12:339-48.
12. Cassina AM, Hodara R, Souza JM, Thomson L, Castro L, Ischiropoulos H, et al. Cytochrome c nitration by peroxynitrite. J Biol Chem 2000;275:21409-15.
13. Castro L, Rodriguez M, Radi R. Aconitase is readily inactivated by peroxynitrite, but not by its precursor, nitric oxide. J Biol Chem 1994;269:29409-15.
14. Choksi KB, Boylston WH, Rabek JP, Widger WR, Papaconstantinou J. Oxidatively damaged proteins of heart mitochondrial electron transport complexes. Biochim Biophys Acta 2004;1688:95-101.
15. Chomyn A, Attardi G. MtDNA mutations in aging and apoptosis. Biochem Biophys Res Commun 2003;304:519-29.
16. Corral-Debrinski M, Stepien G, Shoffner JM, Lott MT, Kanter K, Wallace DC. Hypoxemia is associated with mitochondrial DNA damage and gene induction. Implications for cardiac disease. JAMA 1991;266:1812-6.
17. Cortopassi GA, Arnheim N. Detection of a specific mitochondrial DNA deletion in tissues of older humans. Nucleic Acids Res 1990;18:6927-33.
18. Danial NN, Korsmeyer SJ. Cell death: critical control points. Cell 2004;116:205-19.
19. Davies SM, Poljak A, Duncan MW, Smythe GA, Murphy MP. Measurements of protein carbonyls, ortho- and metatyrosine and oxidative phosphorylation complex activity in mitochondria from young and old rats. Free Radic Biol Med 2001;31:181-90.
20. Di Lisa F, Bernardi P. Mitochondrial function and myocardial aging. A critical analysis of the role of permeability transition. Cardiovasc Res 2005;66:222-32.
21. Dinardo MM, Musicco C, Fracasso F, Milella F, Gadaleta MN, Gadaleta G, et al. Acetylation and level of mitochondrial transcription factor A in several organs of young and old rats. Biochem Biophys Res Commun 2003;301:187-91.
22. Drexler H, Riede U, Munzel T, Konig H, Funke E, Just H. Alterations of skeletal muscle in chronic heart failure. Circulation 1992;85:1751-9.
23. 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;96:4820-5.
24. Fannin SW, Lesnefsky EJ, Slabe TJ, Hassan MO, Hoppel CL. Aging selectively decreases oxidative capacity in rat heart interfibrillar mitochondria. Arch Biochem Biophys 1999;372:399-407.
25. Frahm T, Mohamed SA, Bruse P, Gemund C, Oehmichen M, Meissner C. Lack of age-related increase of mitochondrial DNA amount in brain, skeletal muscle and human heart. Mech Ageing Dev 2005;126:1192-200.
26. Fountoulakis M, Soumaka E, Rapti K, Mavroidis M, Tsangaris G, Maris A, et al. Alterations in the heart mitochondrial proteome in a desmin null heart failure model. J Mol Cell Cardiol 2005;38:461-74.
27. Gadaleta MN, Petruzzella V, Renis M, Fracasso F, Cantatore P. Reduced transcription of mitochondrial DNA in the senescent rat. Tissue dependence and effect of L-carnitine. Eur J Biochem 1990;187:501-6.
28. Gadaleta MN, Rainaldi G, Lezza AM, Milella F, Fracasso F, Cantatore P. Mitochondrial DNA copy number and mitochondrial DNA deletion in adult and senescent rats. Mutat Res 1992;275:181-93.
29. Garnier A, Fortin D, Delomenie C, Momken I, Veksler V, Ventura-Clapier R. Depressed mitochondrial transcription factors and oxidative capacity in rat failing cardiac and skeletal muscle. J Physiol 2003;551:491-501.
30. Genova ML, Castelluccio C, Fato R, Parenti Castelli G, Merlo Pich M, Formiggini G, et al. Major changes in complex I activity in mitochondria from aged rats may not be detected by direct assay of NADH: coenzyme Q reductase. Biochem J 1995;311:105-9.
31. Goyns MH, Charlton MA, Dunford JE, Lavery WL, Merry BJ, Salehi M, et al. Differential display analysis of gene expression indicates that age-related changes are restricted to a small cohort of genes. Mech Ageing Dev 1998;101:73-90.
32. Guerrieri F, Capozza G, Kalous M, Zanotti F, Drahota Z, Papa S. Age-dependent changes in the mitochondrial F0F1 ATP synthase. Arch Gerontol Geriatr 1992;14:299-308.
33. Hansford RG, Castro F. Age-linked changes in the activity of enzymes of the tricarboxylate cycle and lipid oxidation, and of carnitine content, in muscles of the rat. Mech Ageing Dev 1982;19:191-200.
34. Hansford RG, Tsuchiya N, Pepe S. Mitochondria in heart ischaemia and aging. Biochem Soc Symp 1999;66:141-7.
35. Harman D. Aging: a theory based on free radical and radiation chemistry. J Gerontol 1956;11:298-300.
36. Harper ME, Bevilacqua L, Hagopian K, Weindruch R, Ramsey JJ. Ageing, oxidative stress, and mitochondrial uncoupling. Acta Physiol Scand 2004;182:321-31.
37. Hartil K, Charron MJ. Genetic modification of the heart: transgenic modification of cardiac lipid and carbohydrate utilization. J Mol Cell Cardiol 2005;39:581-93.
38. Hattori K, Tanaka M, Sugiyama S, Obayashi T, Ito T, Satake T, et al. Age-dependent increase in deleted mitochondrial DNA in the human heart: possible contributory factor to presbycardia. Am Heart J 1991;121:1735-42.
39. Heddi A, Stepien G, Benke PJ, Wallace DC. Coordinate induction of energy gene expression in tissues of mitochondrial disease patients. J Biol Chem 1999;274:22968-76.
40. Heinke MY, Wheeler CH, Yan JX, Amin V, Chang D, Einstein R, et al. Changes in myocardial protein expression in pacing-induced canine heart failure. Electrophoresis 1999;20:2086-93.
41. Hoppel CL, Moghaddas S, Lesnefsky EJ. Interfibrillar cardiac mitochondrial comples III defects in the aging rat heart. Biogerontology 2002;3:41-4.
42. Hudson EK, Tsuchiya N, Hansford RG. Age-associated changes in mitochondrial mRNA expression and translation in the Wistar rat heart. Mech Ageing Dev 1998;103:179-93.
43. Huss JM, Kelly DP. Nuclear receptor signaling and cardiac energetics. Circ Res 2004;95:568-78.
44. Hwang JJ, Allen PD, Tseng GC, Lam CW, Fananapazir L, Dzau VJ, et al. Microarray gene expression profiles in dilated and hypertrophic cardiomyopathic end-stage heart failure. Physiol Genomics 2002;10:31-44.
45. Ide T, Tsutsui H, Kinugawa S, Utsumi H, Kang D, Hattori N, et al. Mitochondrial electron transport complex I is a potential source of oxygen free radicals in the failing myocardium. Circ Res 1999;85:357-63.
46. Ide T, Tsutsui H, Kinugawa S, Suematsu N, Hayashidani S, Ichikawa K, et al. Direct evidence for increased hydroxyl radicals originating from superoxide in the failing myocardium. Circ Res 2000;86:152-7.
47. Ide T, Tsutsui H, Hayashidani S, Kang D, Suematsu N, Nakamura K, et al. Mitochondrial DNA damage and dysfunction associated with oxidative stress in failing hearts after myocardial infarction. Circ Res 2001;88:529-35.
48. Iemitsu M, Miyauchi T, Maeda S, Tanabe T, Takanashi M, Irukayama-Tomobe Y, et al. Aging-induced decrease in the PPAR-alpha level in hearts is improved by exercise training. Am J Physiol Heart Circ Physiol 2002;283:H1750-60.
49. Ikeuchi M, Matsusaka H, Kang D, Matsushima S, Ide T, Kubota T, et al. Overexpression of mitochondrial transcription factor a ameliorates mitochondrial deficiencies and cardiac failure after myocardial infarction. Circulation 2005;112:683-90.
50. Jahangir A, Ozcan C, Holmuhamedov EL, Terzic A. Increased calcium vulnerability of senescent cardiac mitochondria: protective role for a mitochondrial potassium channel opener. Mech Ageing Dev 2001;122:1073-86.
51. Jarreta D, Orus J, Barrientos A, Miro O, Roig E, Heras M, et al. Mitochondrial function in heart muscle from patients with idiopathic dilated cardiomyopathy. Cardiovasc Res 2000;45:860-5.
52. Joza N, Oudit GY, Brown D, Benit P, Kassiri Z, Vahsen N, et al. Muscle-specific loss of apoptosis-inducing factor leads to mitochondrial dysfunction, skeletal muscle atrophy, and dilated cardiomyopathy. Mol Cell Biol 2005;25:10261-72.
53. Judge S, Jang YM, 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;19:419-21.
54. Kang PM, Yue P, Liu Z, Tarnavski O, Bodyak N, Izumo S. Alterations in apoptosis regulatory factors during hypertrophy and heart failure. Am J Physiol Heart Circ Physiol 2004;287:H72-80.
55. Kates AM, Herrero P, Dence C, Soto P, Srinivasan M, Delano DG, et al. Impact of aging on substrate metabolism by the human heart. J Am Coll Cardiol 2003;41:293-9.
56. Kelly DP, Strauss AW. Inherited cardiomyopathies. N Engl J Med 1994;330:913-9.
57. Kelso GF, Porteous CM, Coulter CV, Hughes G, Porteous WK, Ledgerwood EC, et al. Selective targeting of a redox-active ubiquinone to mitochondria within cells: Antioxidant and antiapoptotic properties. J Biol Chem 2001;276:4588-96.
58. Khrapko K, Bodyak N, Thilly WG, van Orsouw NJ, Zhang X, Coller HA, et al. Cell-by-cell scanning of whole mitochondrial genomes in aged human heart reveals a significant fraction of myocytes with clonally expanded deletions. Nucleic Acids Res 1999;27:2434-41.
59. Kroemer G. Mitochondrial control of apoptosis: an introduction. Biochem Biophys Res Commun 2003;304:433-5.
60. Kujoth GC, Hiona A, Pugh TD, Someya S, Panzer K, Wohlgemuth SE, et al. Mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian aging. Science 2005;309:481-4.
61. Larsson NG, Wang J, Wilhelmsson H, Oldfors A, Rustin P, Lewandoski M, et al. Mitochondrial transcription factor A is necessary for mtDNA maintenance and embryogenesis in mice. Nat Genet 1998;18:231-6.
62. LeDoux SP, Wilson GL. Base excision repair of mitochondrial DNA damage in mammalian cells. Prog Nucleic Acid Res Mol Biol 2001;68:273-84.
63. Lee CK, Allison DB, Brand J, Weindruch R, Prolla TA. Transcriptional profiles associated with aging and middle age-onset caloric restriction in mouse hearts. Proc Natl Acad Sci USA 2002;99:14988-93.
64. Lemoine CM, McClelland GB, Lyons CN, Mathieu-Costello O, Moyes CD. Control of mitochondrial gene expression in the aging rat myocardium. Biochem Cell Biol 2006;84:191-8.
65. Lenaz G, D'Aurelio M, Merlo Pich M, Genova ML, Ventura B, Bovina C, et al. Mitochondrial bioenergetics in aging. Biochim Biophys Acta 2000;1459:397-404.
66. Lesnefsky EJ, Moghaddas S, Tandler B, Kerner J, Hoppel CL. Mitochondrial dysfunction in cardiac disease: ischemia-reperfusion, aging, and heart failure. J Mol Cell Cardiol 2001a;33:1065-89.
67. Lesnefsky EJ, Gudz TI, Moghaddas S, Migita CT, Ikeda-Saito M, Turkaly PJ, et al. Aging decreases electron transport complex III activity in heart interfibrillar mitochondria by alteration of the cytochrome c binding site. J Mol Cell Cardiol 2001b;33:37-47.
68. Li LY, Luo X, Wang X. Endonuclease G is an apoptotic DNase when released from mitochondria. Nature 2001;412:95-9.
69. Linden M, Li Z, Paulin D, Gotow T, Leterrier JF. Effects of desmin gene knockout on mice heart mitochondria. J Bioenerg Biomembranes 2001;33:333-41.
70. Liu Y, Cigola E, Cheng W, Kajstura J, Olivetti G, Hintze TH, et al. Myocyte nuclear mitotic division and programmed myocyte cell death characterize the cardiac myopathy induced by rapid ventricular pacing in dogs. Lab Invest 1995;73:771-87.
71. 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;86:147-57.
72. Maklashina E, Ackrell BA. Is defective electron transport at the hub of aging? Aging Cell 2004;3:21-7.
73. Marin-Garcia J, Goldenthal MJ, Pierpont ME, Ananthakrishnan R. Impaired mitochondrial function in idiopathic dilated cardiomyopathy: biochemical and molecular analysis. J Card Fail 1995;1:285-91.
74. Marin-Garcia J, Goldenthal MJ, Ananthakrishnan R, Pierpont ME, Fricker FJ, Lipshultz SE, et al. Specific mitochondrial DNA deletions in idiopathic dilated cardiomyopathy. Cardiovasc Res 1996;31:306-13.
75. Marin-Garcia J, Ananthakrishnan R, Goldenthal MJ. Mitochondrial gene expression in rat heart and liver during growth and development. Biochem Cell Biol 1997;75:137-42.
76. Marin-Garcia J, Goldenthal MJ, Moe GW. Abnormal cardiac and skeletal muscle mitochondrial function in pacing-induced cardiac failure. Cardiovasc Res 2001;52:103-10.
77. Marin-Garcia J, Goldenthal MJ. Fatty acid metabolism in cardiac failure: biochemical, genetic and cellular analysis. Cardiovasc Res 2002a;54:516-27.
78. Marín-García J, Zoubenko O, Goldenthal MJ. Mutations in the cardiac mtDNA control region associated with cardiomyopathy and aging. J Card Fail 2002b;8:93-100.
79. Marzo I, Brenner C, Zamzami N, Susin SA, Beutner G, Brdiczka D, et al. The permeability transition pore complex: a target for apoptosis regulation by caspases and Bcl-2 related proteins. J Exp Med 1998;187:1261-7.
80. Masuyama M, Iida R, Takatsuka H, Yasuda T, Matsuki T. Quantitative change in mitochondrial DNA content in various mouse tissues during aging. Biochim Biophys Acta 2005;1723:302-8.
81. Meissner C, Bruse P, Oehmichen M. Tissue-specific deletion patterns of the mitochondrial genome with advancing age. Exp Gerontol 2006 Apr 16 (Epub ahead of print).
82. Melov S. Mitochondrial oxidative stress. Physiologic consequences and potential for a role in aging. Ann NY Acad Sci 2000;908:219-25.
83. Miller FJ, Rosenfeldt FL, Zhang C, Linnane AW, Nagley P. Precise determination of mitochondrial DNA copy number in human skeletal and cardiac muscle by a PCR-based assay: lack of change of copy number with age. Nucleic Acids Res 2003;31:e61.
84. Milner DJ, Weitzer G, Tran D, Bradley A, Capetanaki Y. Disruption of muscle architecture and myocardial degeneration in mice lacking desmin. J Cell Biol 1996;134:1255-70.
85. Milner DJ, Mavroidis M, Weisleder N, Capetanaki Y. Desmin cytoskeleton linked to muscle mitochondrial distribution and respiratory function. J Cell Biol 2000;150:1283-98.
86. Miro O, Casademont J, Casals E, Perea M, Urbano-Marquez A, Rustin P, et al. Aging is associated with increased lipid peroxidation in human hearts, but not with mitochondrial respiratory chain enzyme defects. Cardiovasc Res 2000;47:624-31.
87. Moe GW, Marin-Garcia J, Konig A, Goldenthal M, Lu X, Feng Q. In vivo TNF-alpha inhibition ameliorates cardiac mitochondrial dysfunction, oxidative stress, and apoptosis in experimental heart failure. Am J Physiol Heart Circ Physiol 2004;287:H1813-20.
88. Muller-Hocker J. Cytochrome-c-oxidase deficient cardiomyocytes in the human heart - an age-related phenomenon. A histochemical ultracytochemical study. Am J Pathol 1989;134:1167-73.
89. Murray J, Taylor SW, Zhang B, Ghosh SS, Capaldi RA. Oxidative damage to mitochondrial complex I due to peroxynitrite: identification of reactive tyrosines by mass spectrometry. J Biol Chem 2003;278:37223-30.
90. Muscari C, Giaccari A, Stefanelli C, Viticchi C, Giordano E, Guarnieri C, et al. Presence of a DNA-4236 bp deletion and 8-hydroxy-deoxyguanosine in mouse cardiac mitochondrial DNA during aging. Aging (Milano) 1996;8:429-33.
91. Narula J, Haider N, Virmani R, DiSalvo TG, Kolodgie FD, Hajjar RJ, et al. Apoptosis in myocytes in end-stage heart failure. N Engl J Med 1996;35:1182-9.
92. Olivetti G, Abbi R, Quaini F, Kajstura J, Cheng W, Nitahara JA, et al. Apoptosis in the failing heart. N Engl J Med 1997;336:1131-41.
93. Quigley AF, Kapsa RM, Esmore D, Hale G, Byrne E. Mitochondrial respiratory chain activity in idiopathic dilated cardiomyopathy. J Card Fail 2000;6:47-55.
94. Packer MA, Scarlett JL, Martin SW, Murphy MP. Induction of the mitochondrial permeability transition by peroxynitrite. Biochem Soc Trans 1997;25:909-14.
95. Pak JW, Vang F, Johnson C, McKenzie D, Aiken JM. MtDNA point mutations are associated with deletion mutations in aged rat. Exp Gerontol 2005;40:209-18.
96. Papa S. Mitochondrial oxidative phosphorylation changes in the life span. Molecular aspects and physiopathological implications. Biochim Biophys Acta 1996;1276:87-105.
97. Paradies G, Ruggiero FM, Petrosillo G, Gadaleta MN, Quagliariello E. Carnitine-acylcarnitine translocase activity in cardiac mitochondria from aged rats: the effect of acetyl-L-carnitine. Mech Ageing Dev 1995;84:103-12.
98. Paradies G, Ruggiero FM, Petrosillo G, Quagliariello E. Age-dependent decline in the cytochrome c oxidase activity in rat heart mitochondria: role of cardiolipin. FEBS Lett 1997;406:136-8.
99. Phaneuf S, Leeuwenburgh C. Cytochrome c release from mitochondria in the aging heart: a possible mechanism for apoptosis with age. Am J Physiol Integr Comp Physiol 2002;282:R423-30.
100. Pollack M, Phaneuf S, Dirks A, Leeuwenburgh C. The role of apoptosis in the normal aging brain, skeletal muscle, and heart. Ann N Y Acad Sci 2002;959:93-107.
101. Razeghi P, Young ME, Alcorn JL, Moravec CS, Frazier OH, Taegtmeyer H. Metabolic gene expression in fetal and failing human heart. Circulation 2001;104:2923-31.
102. Riobo NA, Clementi E, Melani M, Boveris A, Cadenas E, Moncada S, et al. Nitric oxide inhibits mitochondrial NADH: ubiquinone reductase activity through peroxynitrite formation. Biochem J 2001;359:139-45.
103. Russell LK, Finck BN, Kelly DP. Mouse models of mitochondrial dysfunction and heart failure. J Mol Cell Cardiol 2005;38:81-91.
104. Sam F, Kerstetter DL, Pimental DR, Mulukutla S, Tabaee A, Bristow MR, et al. Increased reactive oxygen species production and functional alterations in antioxidant enzymes in human failing myocardium. J Card Fail 2005;11:473-80.
105. Sayen MR, Gustafsson AB, Sussman MA, Molkentin JD, Gottlieb RA. Calcineurin transgenic mice have mitochondrial dysfunction and elevated superoxide production. Am J Physiol Cell Physiol 2003;284:C562-70.
106. Scheubel RJ, Tostlebe M, Simm A, Rohrbach S, Prondzinsky R, Gellerich FN, et al. Dysfunction of mitochondrial respiratory chain complex I in human failing myocardium is not due to disturbed mitochondrial gene expression. J Am Coll Cardiol 2002;40:2174-81.
107. Schriner SE, Linford NJ, Martin GM, Treuting P, Ogburn CE, Emond M, et al. Extension of murine life span by overexpression of catalase targeted to mitochondria. Science 2005;308:1909-11.
108. Scorrano L, Ashiya M, Buttle K, Weiler S, Oakes S, Mannella CA, et al. A distinct pathway remodels mitochondrial cristae and mobilizes cytochrome c during apoptosis. Dev Cell 2002;2:55-67.
109. Scorrano L, Oakes SA, Opferman JT, Cheng EH, Sorcinelli MD, Pozzan T, et al. BAX and BAK regulation of endoplasmic reticulum Ca2+: a control point for apoptosis. Science 2003;300:135-9.
110. Shen Z, Wu W, Hazen SL. Activated leukocytes oxidatively damage DNA, RNA, and the nucleotide pool through halide-dependent formation of hydroxyl radical. Biochemistry 2000;39:5474-82.
111. Song X, Deng JH, Liu CJ, Bai Y. Specific point mutations may not accumulate with aging in the mouse mitochondrial DNA control region. Gene 2005;350:193-9.
112. Smith RA, Porteous CM, Gane AM, Murphy MP. Delivery of bioactive molecules to mitochondria in vivo. Proc Natl Acad Sci USA 2003;100:5407-12.
113. Stadtman ER, Berlett BS. Reactive oxygen-mediated protein oxidation in aging and disease. Drug Metab Rev 1998;30:225-43.
114. Suh JH, Heath SH, Hagen T. Two subpopulations of mitochondria in the aging rat heart display heterogenous levels of oxidative stress. Free Radic Biol Med 2003;35:1064-72.
115. Susin SA, Lorenzo HK, Zamzami N, Marzo I, Snow BE, Brothers GM, et al. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 1999; 397:441-6.
116. Tanaka Y, Sasaki R, Fukui F, Waki H, Kawabata T, Okazaki M, et al. Acetyl-L-carnitine supplementation restores decreased tissue carnitine levels and impaired lipid metabolism in aged rats. J Lipid Res 2004;45:729-35.
117. Torella D, Rota M, Nurzynska D, Musso E, Monsen A, Shiraishi I, et al. Cardiac stem cell and myocyte aging, heart failure, and insulin-like growth factor-1 overexpression. Circ Res 2004;94:514-24.
118. Torii K, Sugiyama S, Takagi K, Satake T, Ozawa T. Age-related decrease in respiratory muscle mitochondrial function in rats. Am J Respir Cell Mol Biol 1992;6:88-92.
119. Trifunovic A, Wredenberg A, Falkenberg M, Spelbrink JN, Rovio AT, Bruder CE, et al. Premature ageing in mice expressing defective mitochondrial DNA polymerase. Nature 2004;27:417-23.
120. Trifunovic A, Hansson A, Wredenberg A, Rovio AT, Dufour E, Khvorostov I, et al. Somatic mtDNA mutations cause aging phenotypes without affecting reactive oxygen species production. Proc Natl Acad Sci USA 2005;102:17993-8.
121. Tsutsui H, Ide T, Shiomi T, Kang D, Hayashidani S, Suematsu N, et al. 8-oxo-dGTPase, which prevents oxidative stress-induced DNA damage, increases in the mitochondria from failing hearts. Circulation 2001a;104:2883-5.
122. Tsutsui H, Ide T, Hayashidani S, Suematsu N, Shiomi T, Wen J, et al. Enhanced generation of reactive oxygen species in the limb skeletal muscles from a murine infarct model of heart failure. Circulation 2001b;10 104:134-6.
123. Vahsen N, Cande C, Briere JJ, Benit P, Joza N, Larochette N, et al. AIF deficiency compromises oxidative phosphorylation. EMBO J 2004;23:4679-89.
124. van Bilsen M. "Energenetics" of heart failure. Ann N Y Acad Sci 2004;1015:238-49.
125. Vasquez-Vivar J, Kalyanaraman B, Kennedy MC. Mitochondrial aconitase is a source of hydroxyl radical. An electron spin resonance investigation. J Biol Chem 2000;2751:4064-9.
126. Ventura-Clapier R, Garnier A, Veksler V. Energy metabolism in heart failure. J Physiol 2004;555:1-13.
127. Wanagat J, Wolff MR, Aiken JM. Age-associated changes in function, structure and mitochondrial genetic and enzymatic abnormalities in the Fischer 344 x Brown Norway F(1) hybrid rat heart. J Mol Cell Cardiol 2002;34:17-28.
128. Wang J, Wilhelmsson H, Graff C, Li H, Oldfors A, Rustin P, et al. Dilated cardiomyopathy and atrioventricular conduction blocks induced by heart-specific inactivation of mitochondrial DNA gene expression. Nat Genet 1999;21:133-7.
129. Wanrooij S, Luoma P, van Goethem G, van Broeckhoven C, Suomalainen A, Spelbrink JN. Twinkle and POLG defects enhance age-dependent accumulation of mutations in the control region of mtDNA. Nucleic Acids Res 2004;32:3053-64.
130. Wei YH, Lu CY, Lee HC, Pang CY, Ma YS. Oxidative damage and mutation to mitochondrial DNA and age-dependent decline of mitochondrial respiratory function. Ann N Y Acad Sci 1998;854:155-70.
131. Weisleder N, Taffet GE, Capetanaki Y. Bcl-2 overexpression corrects mitochondrial defects and ameliorates inherited desmin null cardiomyopathy. Proc Natl Acad Sci USA 2004;101:769-74.
132. Yakes FM, Van Houten B. Mitochondrial DNA damage is more extensive and persists longer than nuclear DNA damage in human cells following oxidative stress. Proc Natl Acad Sci USA 1997;94:514-9.
133. Yan L, Ge H, Li H, Lieber SC, Natividad F, Resuello RR, et al. Gender-specific proteomic alterations in glycolytic and mitochondrial pathways in aging monkey hearts. J Mol Cell Cardiol 2004;37:921-9.
134. Yang J, Moravec CS, Sussman MA, DiPaola NR, Fu D, Hawthorn L, et al. Decreased SLIM1 expression and increased gelsolin expression in failing human hearts measured by high-density oligonucleotide arrays. Circulation 2000;102:3046-52.
135. Yowe DL, Ames BN. Quantitation of age-related mitochondrial DNA deletions in rat tissues shows that their pattern of accumulation differs from that of humans. Gene 1998;209:23-30.
136. Zhang C, Bills M, Quigley A, Maxwell RJ, Linnane AW, Nagley P. Varied prevalence of age-associated mitochondrial DNA deletions in different species and tissues: a comparison between human and rat. Biochem Biophys Res Commun 1997;230:630-5.
137. Zhang D, Mott JL, Farrar P, Ryerse JS, Chang SW, Stevens M, et al. Mitochondrial DNA mutations activate the mitochondrial apoptotic pathway and cause dilated cardiomyopathy. Cardiovasc Res 2003;57:147-57.
138. Zhang D, Mott JL, Chang SW, Stevens M, Mikolajczak P, Zassenhaus HP. Mitochondrial DNA mutations activate programmed cell survival in the mouse heart. Am J Physiol Heart Circ Physiol 2005;288:H2476-83.
139. Zhao K, Zhao GM, Wu D, Soong Y, Birk AV, Schiller PW, et al. Cell-permeable peptide antioxidants targeted to inner mitochondrial membrane inhibit mitochondrial swelling, oxidative cell death and reperfusion injury. J Biol Chem 2004;279:34682-90.