About this Journal Submit a Manuscript Table of Contents
Journal of Aging Research
Volume 2012 (2012), Article ID 192503, 9 pages
http://dx.doi.org/10.1155/2012/192503
Review Article

Is There a Link between Mitochondrial Reserve Respiratory Capacity and Aging?

1Center for Healthy Aging, Department of Cellular and Molecular Medicine, University of Copenhagen, 2200 Copenhagen, Denmark
2Department of Genetics, School of Medicine, University of Alabama at Birmingham, Birmingham, AL 35294, USA

Received 1 February 2012; Accepted 11 April 2012

Academic Editor: Yousin Suh

Copyright © 2012 Claus Desler et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. B. E. Sansbury, S. P. Jones, D. W. Riggs, V. M. Darley-Usmar, and B. G. Hill, “Bioenergetic function in cardiovascular cells: the importance of the reserve capacity and its biological regulation,” Chemico-Biological Interactions, vol. 191, no. 1-3, pp. 288–295, 2011. View at Publisher · View at Google Scholar · View at Scopus
  2. N. Yadava and D. G. Nicholls, “Spare respiratory capacity rather than oxidative stress regulates glutamate excitotoxicity after partial respiratory inhibition of mitochondrial complex I with rotenone,” Journal of Neuroscience, vol. 27, no. 27, pp. 7310–7317, 2007. View at Publisher · View at Google Scholar · View at Scopus
  3. D. G. Nicholls, “Oxidative stress and energy crises in neuronal dysfunction,” Annals of the New York Academy of Sciences, vol. 1147, pp. 53–60, 2008. View at Publisher · View at Google Scholar · View at Scopus
  4. B. G. Hill, A. N. Higdon, B. P. Dranka, and V. M. Darley-Usmar, “Regulation of vascular smooth muscle cell bioenergetic function by protein glutathiolation,” Biochimica et Biophysica Acta, vol. 1797, no. 2, pp. 285–295, 2010. View at Publisher · View at Google Scholar · View at Scopus
  5. D. Harman, “The biologic clock: the mitochondria?” Journal of the American Geriatrics Society, vol. 20, no. 4, pp. 145–147, 1972. View at Scopus
  6. D. C. Wallace, “Mitochondrial diseases in man and mouse,” Science, vol. 283, no. 5407, pp. 1482–1488, 1999. View at Publisher · View at Google Scholar · View at Scopus
  7. S. DiMauro and E. A. Schon, “Mitochondrial respiratory-chain diseases,” New England Journal of Medicine, vol. 348, no. 26, pp. 2656–2668, 2003. View at Publisher · View at Google Scholar · View at Scopus
  8. S. Melova, J. A. Schneider, P. E. Coskun, D. A. Bennett, and D. C. Wallace, “Mitochondrial DNA rearrangements in aging human brain and in situ PCR of mtDNA,” Neurobiology of Aging, vol. 20, no. 5, pp. 565–571, 1999. View at Publisher · View at Google Scholar · View at Scopus
  9. K. R. Short, M. L. Bigelow, J. Kahl et al., “Decline in skeletal muscle mitochondrial function with aging in humans,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 15, pp. 5618–5623, 2005. View at Publisher · View at Google Scholar · View at Scopus
  10. K. Hattori, M. Tanaka, S. Sugiyama et al., “Age-dependent increase in deleted mitochondrial DNA in the human heart: possible contributory factor to presbycardia,” American Heart Journal, vol. 121, no. 6 I, pp. 1735–1742, 1991. View at Publisher · View at Google Scholar · View at Scopus
  11. C. Desler, M. L. Marcker, K. K. Singh, and L. J. Rasmussen, “The importance of mitochondrial DNA in aging and cancer,” Journal of Aging Research, vol. 2011, Article ID 407536, 2011. View at Publisher · View at Google Scholar
  12. G. Lenaz, “Role of mitochondria in oxidative stress and ageing,” Biochimica et Biophysica Acta, vol. 1366, no. 1-2, pp. 53–67, 1998. View at Publisher · View at Google Scholar · View at Scopus
  13. T. Finkel and N. J. Holbrook, “Oxidants, oxidative stress and the biology of ageing,” Nature, vol. 408, no. 6809, pp. 239–247, 2000. View at Publisher · View at Google Scholar · View at Scopus
  14. T. Finkel, “Radical medicine: treating ageing to cure disease,” Nature Reviews Molecular Cell Biology, vol. 6, no. 12, pp. 971–976, 2005. View at Publisher · View at Google Scholar · View at Scopus
  15. A. Trifunovic, A. Wredenberg, M. Falkenberg et al., “Premature ageing in mice expressing defective mitochondrial DNA polymerase,” Nature, vol. 429, no. 6990, pp. 417–423, 2004. View at Publisher · View at Google Scholar · View at Scopus
  16. C. C. Kujoth, A. Hiona, T. D. Pugh et al., “Medicine: mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian aging,” Science, vol. 309, no. 5733, pp. 481–484, 2005. View at Publisher · View at Google Scholar · View at Scopus
  17. P. Stöckl, C. Zankl, E. Hütter et al., “Partial uncoupling of oxidative phosphorylation induces premature senescence in human fibroblasts and yeast mother cells,” Free Radical Biology and Medicine, vol. 43, no. 6, pp. 947–958, 2007. View at Publisher · View at Google Scholar · View at Scopus
  18. D. Dikov, A. Aulbach, B. Muster, S. Dröse, M. Jendrach, and J. Bereiter-Hahn, “Do UCP2 and mild uncoupling improve longevity?” Experimental Gerontology, vol. 45, no. 7-8, pp. 586–595, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. P. Stöckl, E. Hütter, W. Zwerschke, and P. Jansen-Dürr, “Sustained inhibition of oxidative phosphorylation impairs cell proliferation and induces premature senescence in human fibroblasts,” Experimental Gerontology, vol. 41, no. 7, pp. 674–682, 2006. View at Publisher · View at Google Scholar · View at Scopus
  20. B. Chance and G. R. Williams, “The respiratory chain and oxidative phosphorylation.,” Advances in Enzymology and Related Subjects of Biochemistry, vol. 17, pp. 65–134, 1956. View at Scopus
  21. G. Villani and G. Attardi, “In vivo control of respiration by cytochrome c oxidase in human cells,” Free Radical Biology and Medicine, vol. 29, no. 3-4, pp. 202–210, 2000. View at Publisher · View at Google Scholar · View at Scopus
  22. R. Ramzan, K. Staniek, B. Kadenbach, and S. Vogt, “Mitochondrial respiration and membrane potential are regulated by the allosteric ATP-inhibition of cytochrome c oxidase,” Biochimica et Biophysica Acta, vol. 1797, no. 9, pp. 1672–1680, 2010. View at Publisher · View at Google Scholar · View at Scopus
  23. B. Kadenbach, R. Ramzan, L. Wen, and S. Vogt, “New extension of the Mitchell Theory for oxidative phosphorylation in mitochondria of living organisms,” Biochimica et Biophysica Acta, vol. 1800, no. 3, pp. 205–212, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. C. Piccoli, R. Scrima, D. Boffoli, and N. Capitanio, “Control by cytochrome c oxidase of the cellular oxidative phosphorylation system depends on the mitochondrial energy state,” Biochemical Journal, vol. 396, no. 3, pp. 573–583, 2006. View at Publisher · View at Google Scholar · View at Scopus
  25. M. E. Dalmonte, E. Forte, M. L. Genova, A. Giuffrè, P. Sarti, and G. Lenaz, “Control of respiration by cytochrome c oxidase in intact cells: role of the membrane potential,” Journal of Biological Chemistry, vol. 284, no. 47, pp. 32331–32335, 2009. View at Publisher · View at Google Scholar · View at Scopus
  26. J. J. Poderoso, M. C. Carreras, C. Lisdero, N. Riobó, F. Schöpfer, and A. Boveris, “Nitric oxide inhibits electron transfer and increases superoxide radical production in rat heart mitochondria and submitochondrial particles,” Archives of Biochemistry and Biophysics, vol. 328, no. 1, pp. 85–92, 1996. View at Publisher · View at Google Scholar · View at Scopus
  27. N. A. Riobó, E. Clementi, M. Melani et al., “Nitric oxide inhibits mitochondrial NADH:ubiquinone reductase activity through peroxynitrite formation,” Biochemical Journal, vol. 359, no. 1, pp. 139–145, 2001. View at Publisher · View at Google Scholar · View at Scopus
  28. A. R. Diers, K. A. Broniowska, V. M. Darley-Usmar, and N. Hogg, “Differential regulation of metabolism by nitric oxide and S-nitrosothiols in endothelial cells,” American Journal of Physiology, vol. 301, no. 3, pp. H803–H812, 2011. View at Publisher · View at Google Scholar
  29. T. Persichini, V. Mazzone, F. Polticelli et al., “Mitochondrial type I nitric oxide synthase physically interacts with cytochrome c oxidase,” Neuroscience Letters, vol. 384, no. 3, pp. 254–259, 2005. View at Publisher · View at Google Scholar · View at Scopus
  30. M. C. Franco, V. G. Antico Arciuch, J. G. Peralta et al., “Hypothyroid phenotype is contributed by mitochondrial complex I inactivation due to translocated neuronal nitric-oxide synthase,” Journal of Biological Chemistry, vol. 281, no. 8, pp. 4779–4786, 2006. View at Publisher · View at Google Scholar · View at Scopus
  31. M. W. J. Cleeter, A. M. Cooper, B. M. Darley-Usmar, D. Moncada, and A. H. V. Schapira, “Reversible inhibition of cytochrome c oxidase, the terminal enzyme of the mitochondrial respiratory chain, by nitric oxide,” FEBS Letters, vol. 345, no. 1, pp. 50–54, 1994. View at Publisher · View at Google Scholar · View at Scopus
  32. L. B. Valdez, T. Zaobornyj, and A. Boveris, “Mitochondrial metabolic states and membrane potential modulate mtNOS activity,” Biochimica et Biophysica Acta, vol. 1757, no. 3, pp. 166–172, 2006. View at Publisher · View at Google Scholar · View at Scopus
  33. A. Baracca, S. Barogi, V. Carelli, G. Lenaz, and G. Solaini, “Catalytic activities of mitochondrial ATP synthase in patients with mitochondrial DNA T8993G mutation in the ATPase 6 gene encoding subunit a,” Journal of Biological Chemistry, vol. 275, no. 6, pp. 4177–4182, 2000. View at Publisher · View at Google Scholar · View at Scopus
  34. I. Lee, E. Bender, and B. Kadenbach, “Control of mitochondrial membrane potential and ROS formation by reversible phosphorylation of cytochrome c oxidase,” Molecular and Cellular Biochemistry, vol. 234-235, pp. 63–70, 2002. View at Publisher · View at Google Scholar · View at Scopus
  35. I. Lee, A. R. Salomon, S. Ficarro et al., “cAMP-dependent tyrosine phosphorylation of subunit I inhibits cytochrome c oxidase activity,” Journal of Biological Chemistry, vol. 280, no. 7, pp. 6094–6100, 2005. View at Publisher · View at Google Scholar · View at Scopus
  36. J. K. Fang, S. K. Prabu, N. B. Sepuri et al., “Site specific phosphorylation of cytochrome c oxidase subunits I, IVi1 and Vb in rabbit hearts subjected to ischemia/reperfusion,” FEBS Letters, vol. 581, no. 7, pp. 1302–1310, 2007. View at Publisher · View at Google Scholar · View at Scopus
  37. G. Pocsfalvis, M. Cuccurullo, G. Schlosser, S. Scacco, S. Papa, and A. Malorni, “Phosphorylation of B14.5a subunit from bovine heart complex I identified by titanium dioxide selective enrichment and shotgun proteomics,” Molecular and Cellular Proteomics, vol. 6, no. 2, pp. 231–237, 2007. View at Publisher · View at Google Scholar · View at Scopus
  38. K. Højlund, K. Wrzesinski, P. M. Larsen et al., “Proteome analysis reveals phosphorylation of ATP synthase β-subunit in human skeletal muscle and proteins with potential roles in type 2 diabetes,” Journal of Biological Chemistry, vol. 278, no. 12, pp. 10436–10442, 2003. View at Publisher · View at Google Scholar · View at Scopus
  39. S. L. Elfering, T. M. Sarkela, and C. Giulivi, “Biochemistry of mitochondrial nitric-oxide synthase,” Journal of Biological Chemistry, vol. 277, no. 41, pp. 38079–38086, 2002. View at Publisher · View at Google Scholar · View at Scopus
  40. Y. Burelle and P. W. Hochachka, “Endurance training induces muscle-specific changes in mitochondrial function in skinned muscle fibers,” Journal of Applied Physiology, vol. 92, no. 6, pp. 2429–2438, 2002. View at Scopus
  41. G. López-Lluch, N. Hunt, B. Jones et al., “Calorie restriction induces mitochondrial biogenesis and bioenergetic efficiency,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 6, pp. 1768–1773, 2006. View at Publisher · View at Google Scholar · View at Scopus
  42. F. M. Cerqueira, F. M. Cunha, F. R. M. Laurindo, and A. J. Kowaltowski, “Calorie restriction increases cerebral mitochondrial respiratory capacity in a NO -mediated mechanism: impact on neuronal survival,” Free Radical Biology and Medicine, vol. 52, no. 7, pp. 1236–1241, 2012. View at Publisher · View at Google Scholar
  43. H. Esterbauer, H. Oberkofler, F. Krempler, and W. Patsch, “Human peroxisome proliferator activated receptor gamma coactivator 1 (PPARGC1) gene: cDNA sequence, genomic organization, chromosomal localization, and tissue expression,” Genomics, vol. 62, no. 1, pp. 98–102, 1999. View at Publisher · View at Google Scholar · View at Scopus
  44. C. B. Cairns, J. Walther, A. H. Harken, and A. Banerjee, “Mitochondrial oxidative phosphorylation thermodynamic efficiencies reflect physiological organ roles,” American Journal of Physiology, vol. 274, no. 5, pp. R1376–R1383, 1998. View at Scopus
  45. B. Hennig, “Change of cytochrome c structure during development of the mouse,” European Journal of Biochemistry, vol. 55, no. 1, pp. 167–183, 1975. View at Scopus
  46. M. Hüttemann, I. Lee, J. Liu, and L. I. Grossman, “Transcription of mammalian cytochrome c oxidase subunit IV-2 is controlled by a novel conserved oxygen responsive element,” FEBS Journal, vol. 274, no. 21, pp. 5737–5748, 2007. View at Publisher · View at Google Scholar · View at Scopus
  47. S. Horvat, C. Beyer, and S. Arnold, “Effect of hypoxia on the transcription pattern of subunit isoforms and the kinetics of cytochrome c oxidase in cortical astrocytes and cerebellar neurons,” Journal of Neurochemistry, vol. 99, no. 3, pp. 937–951, 2006. View at Publisher · View at Google Scholar · View at Scopus
  48. A. Navarro, “Mitochondrial enzyme activities as biochemical markers of aging,” Molecular Aspects of Medicine, vol. 25, no. 1-2, pp. 37–48, 2004. View at Publisher · View at Google Scholar · View at Scopus
  49. D. Curti, M. C. Giangare, M. E. Redolfi, I. Fugaccia, and G. Benzi, “Age-related modifications of cytochrome c oxidase activity in discrete brain regions,” Mechanisms of Ageing and Development, vol. 55, no. 2, pp. 171–180, 1990. View at Publisher · View at Google Scholar · View at Scopus
  50. J. Muller-Hocker, “Cytochrome-c-oxidase deficient cardiomyocytes in the human heart: an age-related phenomenon. A histochemical ultracytochemical study,” American Journal of Pathology, vol. 134, no. 5, pp. 1167–1173, 1989. View at Scopus
  51. J. Muller-Hocker, “Cytochrome c oxidase deficient fibres in the limb muscle and diaphragm of man without muscular disease: an age-related alteration,” Journal of the Neurological Sciences, vol. 100, no. 1-2, pp. 14–21, 1990. View at Publisher · View at Google Scholar · View at Scopus
  52. D. Boffoli, S. C. Scacco, R. Vergari, G. Solarino, G. Santacroce, and S. Papa, “Decline with age of the respiratory chain activity in human skeletal muscle,” Biochimica et Biophysica Acta, vol. 1226, no. 1, pp. 73–82, 1994. View at Publisher · View at Google Scholar · View at Scopus
  53. L. A. Gómez, J. S. Monette, J. D. Chavez, C. S. Maier, and T. M. Hagen, “Supercomplexes of the mitochondrial electron transport chain decline in the aging rat heart,” Archives of Biochemistry and Biophysics, vol. 490, no. 1, pp. 30–35, 2009. View at Publisher · View at Google Scholar · View at Scopus
  54. G. Barja and A. Herrero, “Oxidative damage to mitochondrial DNA is inversely related to maximum life span in the heart and brain of mammals,” FASEB Journal, vol. 14, no. 2, pp. 312–318, 2000. View at Scopus
  55. S. Vielhaber, D. Kunz, K. Winkler et al., “Mitochondrial DNA abnormalities in skeletal muscle of patients with sporadic amyotrophic lateral sclerosis,” Brain, vol. 123, no. 7, pp. 1339–1348, 2000. View at Scopus
  56. Z. Ungvari, W. E. Sonntag, and A. Csiszar, “Mitochondria and aging in the vascular system,” Journal of Molecular Medicine, vol. 88, no. 10, pp. 1021–1027, 2010. View at Publisher · View at Google Scholar · View at Scopus
  57. C. Richter, J. W. Park, and B. N. Ames, “Normal oxidative damage to mitochondrial and nuclear DNA is extensive,” Proceedings of the National Academy of Sciences of the United States of America, vol. 85, no. 17, pp. 6465–6467, 1988. View at Scopus
  58. T. Lu, Y. Pan, S. Y. Kao et al., “Gene regulation and DNA damage in the ageing human brain,” Nature, vol. 429, no. 6994, pp. 883–891, 2004. View at Publisher · View at Google Scholar · View at Scopus
  59. T. Kayo, D. B. Allison, R. Weindruch, and T. A. Prolla, “Influences of aging and caloric restriction on the transcriptional profile of skeletal muscle from rhesus monkeys,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 9, pp. 5093–5098, 2001. View at Publisher · View at Google Scholar · View at Scopus
  60. E. Sahin, S. Colla, M. Liesa et al., “Telomere dysfunction induces metabolic and mitochondrial compromise,” Nature, vol. 470, no. 7334, pp. 359–365, 2011. View at Publisher · View at Google Scholar · View at Scopus
  61. D. C. Wallace, J. M. Shoffner, I. Trounce et al., “Mitochondrial DNA mutations in human degenerative diseases and aging,” Biochimica et Biophysica Acta, vol. 1271, no. 1, pp. 141–151, 1995. View at Publisher · View at Google Scholar · View at Scopus
  62. M. F. Beal, “Mitochondria take center stage in aging and neurodegeneration,” Annals of Neurology, vol. 58, no. 4, pp. 495–505, 2005. View at Publisher · View at Google Scholar · View at Scopus
  63. N. A. Bishop, T. Lu, and B. A. Yankner, “Neural mechanisms of ageing and cognitive decline,” Nature, vol. 464, no. 7288, pp. 529–535, 2010. View at Publisher · View at Google Scholar · View at Scopus
  64. A. Novelli, J. A. Reilly, P. G. Lysko, and R. C. Henneberry, “Glutamate becomes neurotoxic via the N-methyl-D-aspartate receptor when intracellular energy levels are reduced,” Brain Research, vol. 451, no. 1-2, pp. 205–212, 1988. View at Scopus
  65. G. Fiskum, A. N. Murphy, and M. F. Beal, “Mitochondria in neurodegeneration: acute ischemia and chronic neurodegenerative diseases,” Journal of Cerebral Blood Flow and Metabolism, vol. 19, no. 4, pp. 351–369, 1999. View at Scopus
  66. L. C. Costantini, L. J. Barr, J. L. Vogel, and S. T. Henderson, “Hypometabolism as a therapeutic target in Alzheimer's disease,” BMC Neuroscience, vol. 9, no. 2, article S16, 2008. View at Publisher · View at Google Scholar · View at Scopus
  67. D. G. Nicholls, “Mitochondrial function and dysfunction in the cell: its relevance to aging and aging-related disease,” International Journal of Biochemistry and Cell Biology, vol. 34, no. 11, pp. 1372–1381, 2002. View at Publisher · View at Google Scholar · View at Scopus
  68. A. C. Bowling, E. M. Mutisya, L. C. Walker, D. L. Price, L. C. Cork, and M. F. Beal, “Age-dependent impairment of mitochondrial function in primate brain,” Journal of Neurochemistry, vol. 60, no. 5, pp. 1964–1967, 1993. View at Scopus
  69. J. Yao, R. W. Irwin, L. Zhao, J. Nilsen, R. T. Hamilton, and R. D. Brinton, “Mitochondrial bioenergetic deficit precedes Alzheimer's pathology in female mouse model of Alzheimer's disease,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 34, pp. 14670–14675, 2009. View at Publisher · View at Google Scholar · View at Scopus
  70. W. M. Brooks, P. J. Lynch, C. C. Ingle et al., “Gene expression profiles of metabolic enzyme transcripts in Alzheimer's disease,” Brain Research, vol. 1127, no. 1, pp. 127–135, 2007. View at Publisher · View at Google Scholar · View at Scopus
  71. D. G. Nicholls and S. L. Budd, “Mitochondria and neuronal survival,” Physiological Reviews, vol. 80, no. 1, pp. 315–360, 2000. View at Scopus
  72. A. Rasola and P. Bernardi, “Mitochondrial permeability transition in Ca2+-dependent apoptosis and necrosis,” Cell Calcium, vol. 50, no. 3, pp. 222–233, 2011. View at Publisher · View at Google Scholar · View at Scopus
  73. M. F. Beal, “Aging, energy, and oxidative stress in neurodegenerative diseases,” Annals of Neurology, vol. 38, no. 3, pp. 357–366, 1995. View at Publisher · View at Google Scholar · View at Scopus
  74. M. Corral-Debrinski, T. Horton, M. T. Lott, J. M. Shoffner, M. F. Beal, and D. C. Wallace, “Mitochondrial DNA deletions in human brain: regional variability and increase with advanced age,” Nature Genetics, vol. 2, no. 4, pp. 324–329, 1992. View at Scopus
  75. N. W. Soong, D. R. Hinton, G. Cortopassi, and N. Arnheim, “Mosaicism for a specific somatic mitochondrial DNA mutation in adult human brain,” Nature Genetics, vol. 2, no. 4, pp. 318–323, 1992. View at Scopus
  76. P. Mecocci, U. MacGarvey, A. E. Kaufman et al., “Oxidative damage to mitochondrial DNA shows marked age-dependent increases in human brain,” Annals of Neurology, vol. 34, no. 4, pp. 609–616, 1993. View at Scopus
  77. J. M. Shoffner, M. D. Brown, A. Torroni et al., “Mitochondrial DNA variants observed in Alzheimer disease and Parkinson disease patients,” Genomics, vol. 17, no. 1, pp. 171–184, 1993. View at Publisher · View at Google Scholar · View at Scopus
  78. A. Bender, K. J. Krishnan, C. M. Morris et al., “High levels of mitochondrial DNA deletions in substantia nigra neurons in aging and Parkinson disease,” Nature Genetics, vol. 38, no. 5, pp. 515–517, 2006. View at Publisher · View at Google Scholar · View at Scopus
  79. M. T. Lin and M. F. Beal, “Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases,” Nature, vol. 443, no. 7113, pp. 787–795, 2006. View at Publisher · View at Google Scholar · View at Scopus
  80. D. G. Nicholls, L. Johnson-Cadwell, S. Vesce, M. Jekabsons, and N. Yadava, “Bioenergetics of mitochondria in cultured neurons and their role in glutamate excitotoxicity,” Journal of Neuroscience Research, vol. 85, no. 15, pp. 3206–3212, 2007. View at Publisher · View at Google Scholar · View at Scopus
  81. G. Gong, J. Liu, P. Liang et al., “Oxidative capacity in failing hearts,” American Journal of Physiology, vol. 285, no. 2, pp. H541–H548, 2003. View at Scopus
  82. A. Garnier, D. Fortin, C. Deloménie, I. Momken, V. Veksler, and R. Ventura-Clapier, “Depressed mitochondrial transcription factors and oxidative capacity in rat failing cardiac and skeletal muscles,” Journal of Physiology, vol. 551, no. 2, pp. 491–501, 2003. View at Publisher · View at Google Scholar · View at Scopus
  83. H. Bugger, C. Guzman, C. Zechner, M. Palmeri, K. S. Russell, and R. R. Russell, “Uncoupling protein downregulation in doxorubicin-induced heart failure improves mitochondrial coupling but increases reactive oxygen species generation,” Cancer Chemotherapy and Pharmacology, vol. 67, no. 6, pp. 1381–1388, 2011. View at Publisher · View at Google Scholar · View at Scopus
  84. G. Faerber, F. Barreto-Perreia, M. Schoepe et al., “Induction of heart failure by minimally invasive aortic constriction in mice: reduced peroxisome proliferator-activated receptor γ coactivator levels and mitochondrial dysfunction,” Journal of Thoracic and Cardiovascular Surgery, vol. 141, no. 2, pp. 492–500, 2011. View at Publisher · View at Google Scholar · View at Scopus
  85. R. J. Scheubel, M. Tostlebe, A. Simm et al., “Dysfunction of mitochondrial respiratory chain complex I in human failing myocardium is not due to disturbed mitochondrial gene expression,” Journal of the American College of Cardiology, vol. 40, no. 12, pp. 2174–2181, 2002. View at Publisher · View at Google Scholar · View at Scopus
  86. C. S. Lin, Y. L. Sun, and C. Y. Liu, “Structural and biochemical evidence of mitochondrial depletion in pigs with hypertrophic cardiomyopathy,” Research in Veterinary Science, vol. 74, no. 3, pp. 219–226, 2003. View at Publisher · View at Google Scholar · View at Scopus
  87. T. Ide, H. Tsutsui, S. Hayashidani et al., “Mitochondrial DNA damage and dysfunction associated with oxidative stress in failing hearts after myocardial infarction,” Circulation Research, vol. 88, no. 5, pp. 529–535, 2001. View at Scopus
  88. J. Marín-García, M. J. Goldenthal, and G. W. Moe, “Abnormal cardiac and skeletal muscle mitochondrial function in pacing-induced cardiac failure,” Cardiovascular Research, vol. 52, no. 1, pp. 103–110, 2001. View at Publisher · View at Google Scholar · View at Scopus
  89. S. Wang, C. Fu, H. Wang et al., “Polymorphisms of the peroxisome proliferator-activated receptor-γ coactivator-1α gene are associated with hypertrophic cardiomyopathy and not with hypertension hypertrophy,” Clinical Chemistry and Laboratory Medicine, vol. 45, no. 8, pp. 962–967, 2007. View at Publisher · View at Google Scholar · View at Scopus
  90. Z. Arany, H. He, J. Lin et al., “Transcriptional coactivator PGC-1α controls the energy state and contractile function of cardiac muscle,” Cell Metabolism, vol. 1, no. 4, pp. 259–271, 2005. View at Publisher · View at Google Scholar · View at Scopus
  91. Y. R. Chen, C. L. Chen, D. R. Pfeiffer, and J. L. Zweier, “Mitochondrial complex II in the post-ischemic heart: Oxidative injury and the role of protein S-glutathionylation,” Journal of Biological Chemistry, vol. 282, no. 45, pp. 32640–32654, 2007. View at Publisher · View at Google Scholar · View at Scopus
  92. W. J. Evans, “What is sarcopenia?” Journals of Gerontology A, vol. 50, pp. 5–8, 1995. View at Scopus
  93. A. Hiona, A. Sanz, G. C. Kujoth et al., “Mitochondrial DNA mutations induce mitochondrial dysfunction, apoptosis and sarcopenia in skeletal muscle of mitochondrial DNA mutator mice,” PLoS ONE, vol. 5, no. 7, Article ID e11468, 2010. View at Publisher · View at Google Scholar · View at Scopus
  94. K. E. Conley, S. A. Jubrias, and P. C. Esselman, “Oxidative capacity and ageing in human muscle,” Journal of Physiology, vol. 526, no. 1, pp. 203–210, 2000. View at Scopus
  95. D. J. Taylor, G. J. Kemp, C. H. Thompson, and G. K. Radda, “Ageing: effects on oxidative function of skeletal muscle in vivo,” Molecular and Cellular Biochemistry, vol. 174, no. 1-2, pp. 321–324, 1997. View at Publisher · View at Google Scholar · View at Scopus
  96. S. Welle, K. Bhatt, and C. A. Thornton, “High-abundance mRNAs in human muscle: comparison between young and old,” Journal of Applied Physiology, vol. 89, no. 1, pp. 297–304, 2000. View at Scopus
  97. I. R. Lanza, D. K. Short, K. R. Short et al., “Endurance exercise as a countermeasure for aging,” Diabetes, vol. 57, no. 11, pp. 2933–2942, 2008. View at Publisher · View at Google Scholar · View at Scopus
  98. I. R. Lanza and K. Sreekumaran Nair, “Regulation of skeletal muscle mitochondrial function: genes to proteins,” Acta Physiologica, vol. 199, no. 4, pp. 529–547, 2010. View at Publisher · View at Google Scholar · View at Scopus
  99. S. Larsen, M. Hey-Mogensen, R. Rabøl, N. Stride, J. W. Helge, and F. Dela, “The influence of age and aerobic fitness: 3 effects on mitochondrial respiration in skeletal muscle,” Acta Physiologica, vol. 205, no. 3, pp. 423–432, 2012.
  100. V. Pesce, A. Cormio, F. Fracasso et al., “Age-related mitochondrial genotypic and phenotypic alterations in human skeletal muscle,” Free Radical Biology and Medicine, vol. 30, no. 11, pp. 1223–1233, 2001. View at Publisher · View at Google Scholar · View at Scopus
  101. E. V. Menshikova, V. B. Ritov, L. Fairfull, R. E. Ferrell, D. E. Kelley, and B. H. Goodpaster, “Effects of exercise on mitochondrial content and function in aging human skeletal muscle,” Journals of Gerontology A, vol. 61, no. 6, pp. 534–540, 2006. View at Scopus
  102. D. L. Waters, W. M. Brooks, C. R. Qualls, and R. N. Baumgartner, “Skeletal muscle mitochondrial function and lean body mass in healthy exercising elderly,” Mechanisms of Ageing and Development, vol. 124, no. 3, pp. 301–309, 2003. View at Publisher · View at Google Scholar · View at Scopus
  103. E. V. Menshikova, V. B. Ritov, F. G. S. Toledo, R. E. Ferrell, B. H. Goodpaster, and D. E. Kelley, “Effects of weight loss and physical activity on skeletal muscle mitochondrial function in obesity,” American Journal of Physiology, vol. 288, no. 4, pp. E818–E825, 2005. View at Publisher · View at Google Scholar · View at Scopus