Alterations in mitochondria and their impact in aging skeletal muscle

Sarcopenia - Age-Related Muscle Wasting and Weakness: Mechanisms and Treatments

Volumn , Issue , 2011, Pages 135-158

  Hepple, Russell T ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

Apoptosis; Denervation; Exercise; Mitochondria; Mitochondrial biogenesis; Mitochondrial dysfunction; Plasticity; Reactive oxygen species

Indexed keywords

EID: 81155136000     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-90-481-9713-2_7     Document Type: Chapter

References (88)

1. Adhihetty, P. J., O'Leary, M. F., Chabi, B., Wicks, K. L., Hood, D. A. (2007). Effect of denervation on mitochondrially mediated apoptosis in skeletal muscle. Journal of Applied Physiology, 102, 1143-1151.
2. Altmann, R. (1890). Die Elementarorganismen und ihre Beziehungen zu den Zellen. Verlag von Veit & Comp Leipzig.
3. Alway, S. E., Degens, H., Krishnamurthy, G., Smith, C. A. (2002). Potential role for Id myogenic repressors in apoptosis and attenuation of hypertrophy in muscles of aged rats. AJP - Cell Physiology, 283, C66-C76.
4. Baar, K., Wende, A. R., Jones, T. E., Marison, M., Nolte, L. A., Chen, M., Kelly, D. P., Holloszy, J. O. (2002). Adaptations of skeletal muscle to exercise: rapid increase in the transcriptional coactivator PGC-1. The FASEB Journal, 16, 1879-1886.
5. Bakeeva, L. E., Chentsov, Y. S., Skulachev, V. P. (1978). Mitochondrial framework (reticulum mitochondriale) in rat diaphragm muscle. Biochim Biophys Acta, 501, 349-369.
6. Baker, D. J. & Hepple, R. T. (2006). Elevated caspase and AIF signaling correlates with the progression of sarcopenia during aging in male F344BN rats. Experimental Gerontology, 41, 1149-1156.
7. Baker, D. J., Betik, A. C., Krause, D. J., Hepple, R. T. (2006). No decline in skeletal muscle oxidative capacity with aging in long-term caloric restricted rats: effects are independent of mtDNA integrity. The Journals of Gerontology. Series A: Biological Sciences and Medical Sciences, 61A, 675-684.
8. Bejma, J. & Ji, L. L. (1999). Aging and acute exercise enhance free radical generation in rat skeletal muscle. Journal of Applied Physiology, 87, 465-470.
9. Betik, A. C., Baker, D. J., Krause, D. J., McConkey, M. J., Hepple, R. T. (2008). Exercise training in late middle-aged male Fischer 344 x Brown Norway F1-hybrid rats improves skeletal muscle aerobic function. Experimental Physiology, 93, 863-871.
10. Betik, A. C., Thomas, M. M., Wright, K. J., Riel, C. D., Hepple, R. T. (2009). Exercise training from late middle age until senescence does not attenuate the declines in skeletal muscle aerobic function. American Journal of Physiology: Regulatory, Integrative and Comparative Physiology, 297, R744-R755.
11. Bhattacharya, A., Muller, F. L., Liu, Y., Sabia, M., Liang, H., Song, W., Jang, Y. C., Ran, Q., Van Remmen, H. (2009). Denervation induces cytosolic phospholipase A2-mediated fatty acid hydroperoxide generation by muscle mitochondria. The Journal of Biological Chemistry, 284, 46-55.
12. Blough, E. R. & Linderman, J. K. (2000). Lack of skeletal muscle hypertrophy in very aged male Fischer 344 X Brown Norway rats. Journal of Applied Physiology, 88, 1265-1270.
13. Boncompagni, S., d'Amelio, L., Fulle, S., Fano, G., Protasi, F. (2006). Progressive disorganization of the excitation-contraction coupling apparatus in aging human skeletal muscle as revealed by electron microscopy: A possible role in the decline of muscle performance. The Journals of Gerontology. Series A: Biological Sciences and Medical Sciences, 61, 995-1008.
14. Booth, F. W. & Holloszy, J. O. (1977). Cytochrome c turnover in rat skeletal muscles. The Journal of Biological Chemistry, 252, 416-419.
15. Bota, D. A., Van Remmen, H., Davies, K. J. (2002). Modulation of Lon protease activity and aconitase turnover during aging and oxidative stress. FEBS Letters, 532, 103-106.
16. Bua, E., Johnson, J., Herbst, A., Delong, B., McKenzie, D., Salamat, S., Aiken, J. M. (2006). Mitochondrial DNA-deletion mutations accumulate intracellularly to detrimental levels in aged human skeletal muscle fibers. American Journal of Human Genetics, 79, 469-480.
17. Bua, E. A., McKiernan, S. H., Wanagat, J., McKenzie, D., Aiken, J. M. (2002). Mitochondrial abnormalities are more frequent in muscles undergoing sarcopenia. Journal of Applied Physiology, 92, 2617-2624.
18. Capel, F., Buffiere, C., Patureau, M. P., Mosoni, L. (2004). Differential variation of mitochondrial H2O2 release during aging in oxidative and glycolytic muscles in rats. Mechanisms of Ageing and Development, 125, 367-373.
19. Capel, F., Rimbert, V., Lioger, D., Diot, A., Rousset, P., Mirand, P. P., Boirie, Y., Morio, B., Mosoni, L. (2005). Due to reverse electron transfer, mitochondrial H2O2 release increases with age in human vastus lateralis muscle although oxidative capacity is preserved. Mechanisms of Ageing and Development, 126, 505-511.
20. Cartee, G. D. & Farrar, R. P. (1987). Muscle respiratory capacity and VO 2max in identically trained young and old rats. Journal of Applied Physiology, 63, 257-261.
21. Chabi, B., Ljubicic, V., Menzies, K. J., Huang, J. H., Saleem, A., Hood, D. A. (2008). Mitochondrial function and apoptotic susceptibility in aging skeletal muscle. Aging Cell, 7, 2-12.
22. Choksi, K. B., Nuss, J. E., Deford, J. H., Papaconstantinou, J. (2008). Age-related alterations in oxidatively damaged proteins of mouse skeletal muscle mitochondrial electron transport chain complexes. Free Radical Biology & Medicine, 45, 826-838.
23. Coggan, A. R., Spina, R. J., King, D. S., Rogers, M. A., Brown, M., Nemeth, P. M., Holloszy, J. O. (1992). Histochemical and enzymatic comparison of the gastrocnemius muscle of young and elderly men and women. Journal of Gerontology, 47, B71-B76.
24. Conley, K. E., Jubrias, S. A., Esselman, P. C. (2000). Oxidative capacity and aging in human muscle. The Journal of Physiology, 526.1, 203-210.
25. Davies, K. J., Packer, L., Brooks, G. A. (1981). Biochemical adaptation of mitochondria, muscle, and whole-animal respiration to endurance training. Archives of Biochemistry and Biophysics, 209, 539-554.
26. Desai, V. G., Weindruch, R., Hart, R. W., Feuers, R. J. (1996). Influences of age and dietary restriction on gastrocnemius electron transport system activities in mice. Archives of Biochemistry and Biophysics, 333, 145-151.
27. Dirks, A. & Leeuwenburgh, C. (2002). Apoptosis in skeletal muscle with aging. AJP - Regulatory, Integrative and Comparative Physiology, 282, R519-R527.
28. Drew, B., Phaneuf, S., Dirks, A., Selman, C., Gredilla, R., Lezza, A., Barja, G., Leeuwenburgh, C. (2003). Effects of aging and caloric restriction on mitochondrial energy production in gastrocnemius muscle and heart. American Journal of Physiology: Regulatory, Integrative and Comparative Physiology, 284, R474-R480.
29. Droge, W. (2002). Free radicals in the physiological control of cell function. Physiological Reviews, 82, 47-95.
30. Dupuis, L., Gonzalez de Aguilar, J. L., Echaniz-Laguna, A., Eschbach, J., Rene, F., Oudart, H., Halter, B., Huze, C., Schaeffer, L., Bouillaud, F., Loeffler, J. P. (2009). Muscle mitochondrial uncoupling dismantles neuromuscular junction and triggers distal degeneration of motor neurons. PLoS ONE, 4, e5390.
31. Essen-Gustavsson, B. & Borges, O. (1986). Histochemical and metabolic characteristics of human skeletal muscle in relation to age. Acta Physiologica Scandinavica, 126, 107-114.
32. Fano, G., Mecocci, P., Vecchiet, J., Belia, S., Fulle, S., Polidori, M. C., Felzani, G., Senin, U., Vecchiet, L., Beal, M. F. (2001). Age and sex influence on oxidative damage and functional status in human skeletal muscle. Journal of Muscle Research and Cell Motility, 22, 345-351.
33. Fugere, N. A., Ferrington, D. A., Thompson, L. V. (2006). Protein nitration with aging in the rat semimembranosus and soleus muscles. The Journals of Gerontology. Series A: Biological Sciences and Medical Sciences, 61, 806-812.
34. Giresi, P. G., Stevenson, E. J., Theilhaber, J., Koncarevic, A., Parkington, J., Fielding, R. A., Kandarian, S. C. (2005). Identification of a molecular signature of sarcopenia. Physiological Genomics, 21, 253-263.
35. Gomez-Cabrera, M. C., Borras, C., Pallardo, F. V., Sastre, J., Ji, L. L., Vina, J. (2005). Decreasing xanthine oxidase-mediated oxidative stress prevents useful cellular adaptations to exercise in rats. The Journal of Physiology Online, 567, 113-120.
36. Hagberg, J. M., Graves, J. E., Limacher, M. C., Woods, D. R., Legget, S. H., Cononie, C. C., Gruber, J. J., Pollock, M. L. (1989). Cardiovascular responses of 70- to 79-yr-old men and women to exercise training. Journal of Applied Physiology, 66, 2589-2594.
37. Hagen, J. L., Krause, D. J., Baker, D. J., Fu, M., Tarnopolsky, M. A., Hepple, R. T. (2004). Skeletal muscle aging in F344BN F1-hybrid rats: I. Mitochondrial dysfunction contributes to the ageassociated reduction in VO2max. The Journals of Gerontology. Series A: Biological Sciences and Medical Sciences, 59A, 1099-1110.
38. Hepple, R. T. (2003). Sarcopenia - A critical perspective. Science of Aging Knowledge Environment 2003, pe31.
39. Hepple, R. T., Hagen, J. L., Krause, D. J., Jackson, C. C. (2003). Aerobic power declines with aging in rat skeletal muscles perfused at matched convective O2 delivery. Journal of Applied Physiology, 94, 744-751.
40. Hepple, R. T., Hagen, J. L., Krause, D. J., Baker, D. J. (2004a). Skeletal muscle aging in F344BN F1-hybrid rats: II. Improved contractile economy in senescence helps compensate for reduced ATP generating capacity. The Journals of Gerontology Series A: Biological Sciences and Medical Sciences, 59A, 1111-1119.
41. Hepple, R. T., Ross, K. D., Rempfer, A. B. (2004b). Fiber Atrophy and Hypertrophy in Skeletal Muscles of Late Middle-Aged Fischer 344 x Brown Norway F1-Hybrid Rats. The Journals of Gerontology Series A: Biological Sciences and Medical Sciences, 59, B108-B117.
42. Hepple, R. T., Baker, D. J., Kaczor, J. J., Krause, D. J. (2005). Long-term caloric restriction abrogates the age-related decline in skeletal muscle aerobic function. The FASEB Journal, 19, 1320-1322.
43. Hepple, R. T., Baker, D. J., McConkey, M., Murynka, T., Norris, R. (2006). Caloric restriction protects mitochondrial function with aging in skeletal and cardiac muscles. Rejuvenation Research, 9, 219-222.
44. Hepple, R. T., Qin, M., Nakamoto, H., Goto, S. (2008). Caloric restriction optimizes the proteasome pathway with aging in rat plantaris muscle: implications for sarcopenia. American Journal of Physiology: Regulatory, Integrative and Comparative Physiology, 295, 1231-1237.
45. Hepple, R. T. & Vogell, J. E. (2004). Anatomic capillarization is maintained in relative excess of fiber oxidative capacity in some skeletal muscles of late middle aged rats. Journal of Applied Physiology, 96, 2257-2264.
46. Hutter, E., Skovbro, M., Lener, B., Prats, C., Rabol, R., Dela, F., Jansen-Durr, P. (2007). Oxidative stress and mitochondrial impairment can be separated from lipofuscin accumulation in aged human skeletal muscle. Aging Cell, 6, 245-256.
47. Jackman, R. W., Kandarian, S. C. (2004). The molecular basis of skeletal muscle atrophy. AJP - Cell Physiology, 287, C834-C843.
48. Jacobs, H. T. (2003). The mitochondrial theory of aging: dead or alive? Aging Cell, 2, 11-17.
49. Kayar, S. R., Hoppeler, H., Mermod, L., Weibel, E. R. (1988). Mitochondrial size and shape in equine skeletal muscle: a three-dimensional reconstruction study. Anatomical Record, 222, 333-339.
50. Lee, C. M., Lopez, M. E., Weindruch, R., Aiken, J. M. (1998). Association of age-related mitochondrial abnormalities with skeletal muscle fiber atrophy. Free Radical Biology and Medicine, 25, 964-972.
51. Lexell, J., Taylor, C. C., Sjostrom, M. (1988). What is the cause of the ageing atrophy? Total number, size and proportion of different fiber types studied in whole vastus lateralis muscle from 15- to 83-year-old men. Journal of the Neurological Sciences, 84, 275-294.
52. Ljubicic, V. & Hood, D. A. (2009). Diminished contraction-induced intracellular signaling towards mitochondrial biogenesis in aged skeletal muscle. Aging Cell, 8, 394-404.
53. Lowe, D. A., Surek, J. T., Thomas, D. D., Thompson, L. V. (2001). Electron paramagnetic resonance reveals age-related myosin structural changes in rat skeletal muscle fibers. American Journal of Physiology - Cell Physiology, 280, C540-C547.
54. Ma, Y. S., Wu, S. B., Lee, W. Y., Cheng, J. S., Wei, Y. H. (2009). Response to the increase of oxidative stress and mutation of mitochondrial DNA in aging. Biochimica et Biophysica Acta, 1790, 1021-1029.
55. Mansouri, A., Muller, F. L., Liu, Y., Ng, R., Faulkner, J., Hamilton, M., Richardson, A., Huang, T. T., Epstein, C. J., Van, R. H. (2006). Alterations in mitochondrial function, hydrogen peroxide release and oxidative damage in mouse hind-limb skeletal muscle during aging. Mechanisms of Ageing and Development, 127, 298-306.
56. Marzetti, E., Wohlgemuth, S. E., Lees, H. A., Chung, H. Y., Giovannini, S., Leeuwenburgh, C. (2008). Age-related activation of mitochondrial caspase-independent apoptotic signaling in rat gastrocnemius muscle. Mechanisms of Ageing and Development, 129, 542-549.
57. Mathieu-Costello, O., Ju, Y., Trejo-Morales, M., Cui, L. (2005). Greater capillary-fiber interface per fiber mitochondrial volume in skeletal muscles of old rats. Journal of Applied Physiology, 99, 281-289.
58. Meredith, C. N., Frontera, W. R., Fisher, E. C., Hughes, V. A., Herland, J. C., Edwards, J., Evans, W. J. (1989). Peripheral effects of endurance training in young and old subjects. Journal of Applied Physiology, 66, 2844-2849.
59. Miwa, S., Lawless, C., von Zglinicki, T. (2008). Mitochondrial turnover in liver is fast in vivo and is accelerated by dietary restriction: application of a simple dynamic model. Aging Cell, 7, 920-923.
60. Muller, F. L., Song, W., Jang, Y. C., Liu, Y., Sabia, M., Richardson, A., Van Remmen, H. (2007). Denervation-induced skeletal muscle atrophy is associated with increased mitochondrial ROS production. American Journal of Physiology: Regulatory, Integrative and Comparative Physiology, 293, 1159-1168.
61. Navarro, A. & Boveris, A. (2007). The mitochondrial energy transduction system and the aging process. AJP - Cell Physiology, 292, C670-C686.
62. Norrbom, J., Sundberg, C. J., Ameln, H., Kraus, W. E., Jansson, E., Gustafsson, T. (2004). PGC- 1{?} mRNA expression is influenced by metabolic perturbation in exercising human skeletal muscle. Journal of Applied Physiology, 96, 189-194.
63. Ogata, T. & Yamasaki, Y. (1997). Ultra-high-resolution scanning electron microscopy of mitochondria and sarcoplasmic reticulum arrangement in human red, white, and intermediate muscle fibers. Anatomical Record, 248, 214-223.
64. Orlander, J. & Aniansson, A. (1980). Effects of physical training on skeletal muscle metabolism and ultrastructure in 70 to 75-year-old men. Acta Physiologica Scandinavica, 109, 149-154.
65. Pollack, M. & Leeuwenburgh, C. (2001). Apoptosis and Aging: Role of the Mitochondria. The Journals of Gerontology. Series A: Biological Sciences and Medical Sciences, 56, B475-B482.
66. Powers, S. K., Kavazis, A. N., DeRuisseau, K. C. (2005). Mechanisms of disuse muscle atrophy: role of oxidative stress. AJP - Regulatory, Integrative and Comparative Physiology, 288, R337-R344.
67. Prochniewicz, E., Thomas, D. D., Thompson, L. V. (2005). Age-related decline in actomyosin function. The Journals of Gerontology. Series A: Biological Sciences and Medical Sciences, 60, 425-431.
68. Raffaello, A., Laveder, P., Romualdi, C., Bean, C., Toniolo, L., Germinario, E., Megighian, A., Danieli-Betto, D., Reggiani, C., Lanfranchi, G. (2006). Denervation in murine fast-twitch muscle: short-term physiological changes and temporal expression profiling. Physiological Genomics, 25, 60-74.
69. Rasmussen, U. F., Krustrup, P., Kjaer, M., Rasmussen, H. N. (2003). Human skeletal muscle mitochondrial metabolism in youth and senescence: no signs of functional changes of ATP formation and mitochondrial capacity. Pflugers Archiv, 446, 270-278.
70. Raue, U., Slivka, D., Minchev, K., Trappe, S. (2009). Improvements in whole muscle and myocellular function are limited with high-intensity resistance training in octogenarian women. Journal of Applied Physiology, 106, 1611-1617.
71. Reznick, R. M., Zong, H., Li, J., Morino, K., Moore, I. K., Yu, H. J., Liu, Z. X., Dong, J., Mustard, K. J., Hawley, S. A., Befroy, D., Pypaert, M., Hardie, D. G., Young, L. H., Shulman, G. I. (2007). Aging-associated reductions in AMP-activated protein kinase activity and mitochondrial biogenesis. Cell Metabolism, 5, 151-156.
72. Rice, K. M. & Blough, E. R. (2006). Sarcopenia-related apoptosis is regulated differently in fastand slow-twitch muscles of the aging F344/NxBN rat model. Mechanisms of Ageing and Development, 127, 670-679.
73. Rooyackers, O. E., Adey, D. B., Ades, P. A., Nair, K. S. (1996). Effect of age on in vivo rates of mitochondrial protein synthesis in human skeletal muscle. Proceedings of the National Academy of Sciences of the United States of America, 93, 15364-15369.
74. Rossiter, H. B., Howlett, R. A., Holcombe, H. H., Entin, P. L., Wagner, H. E., Wagner, P. D. (2005). Age is no barrier to muscle structural, biochemical and angiogenic adaptations to training up to 24 months in female rats. Journal de Physiologie, 565, 993-1005.
75. Sacheck, J. M., Hyatt, J. P., Raffaello, A., Jagoe, R. T., Roy, R. R., Edgerton, V. R., Lecker, S. H., Goldberg, A. L. (2007). Rapid disuse and denervation atrophy involve transcriptional changes similar to those of muscle wasting during systemic diseases. The FASEB Journal, 21, 140-155.
76. Seo, A. Y., Xu, J., Servais, S., Hofer, T., Marzetti, E., Wohlgemuth, S. E., Knutson, M. D., Chung, H. Y., Leeuwenburgh, C. (2008). Mitochondrial iron accumulation with age and functional consequences. Aging Cell, 7, 706-716.
77. Short, K. R., Vittone, J. L., Bigelow, M. L., Proctor, D. N., Rizza, R. A., Coenen-Schimke, J. M., Nair, K. S. (2003). Impact of aerobic exercise training on age-related changes in insulin sensitivity and muscle oxidative capacity. Diabetes, 52, 1888-1896.
78. Short, K. R., Bigelow, M. L., Kahl, J., Singh, R., Coenen-Schimke, J., Raghavakaimal, S., Nair, K. S. (2005). Decline in skeletal muscle mitochondrial function with aging in humans. Proceedings of the National Academy of Sciences of the United States of America, 102, 5618-5623.
79. Slivka, D., Raue, U., Hollon, C., Minchev, K., Trappe, S. (2008). Single muscle fiber adaptations to resistance training in old (>80 yr) men: Evidence for limited skeletal muscle plasticity. American Journal of Physiology: Regulatory, Integrative and Comparative Physiology, 295, R273-R280.
80. Stathokostas, L., Jacob-Johnson, S., Petrella, R. J., Paterson, D. H. (2004). Longitudinal changes in aerobic power in older men and women. Journal of Applied Physiology, 97, 781-789.
81. Sugiyama, S., Takasawa, M., Hayakawa, M., Ozawa, T. (1993). Changes in skeletal muscle, heart and liver mitochondrial electron transport activities in rats and dogs of various ages. Biochemistry and Molecular Biology International, 30, 937-944.
82. Terada, S., Goto, M., Kato, M., Kawanaka, K., Shimokawa, T., Tabata, I. (2002). Effects of lowintensity prolonged exercise on PGC-1 mRNA expression in rat epitrochlearis muscle. Biochemical and Biophysical Research Communications, 296, 350-354.
83. Terman, A. & Brunk, U. T. (2004). Myocyte aging and mitochondrial turnover. Experimental Gerontology, 39, 701-705.
84. Thomas, M. M., Vigna, C., Betik, A. C., Tupling, A. R., Hepple, R. T. (2009). Initiating treadmill exercise training in late middle age offers modest adaptations in Ca2+ handling but enhances protein oxidative damage in senescent rat skeletal muscle. American Journal of Physiology: Regulatory, Integrative and Comparative Physiology, 298, R1269-R1278.
85. Thompson, L. V., Durand, D., Fugere, N. A., Ferrington, D. A. (2006). Myosin and actin expression and oxidation in aging muscle. Journal of Applied Physiology, 101(6), 1581-1587.
86. Tonkonogi, M., Fernstrom, M., Walsh, B., Ji, L. L., Rooyackers, O., Hammarqvist, F., Wernerman, J., Sahlin, K. (2003). Reduced oxidative power but unchanged antioxidative capacity in skeletal muscle from aged humans. Pflugers Archiv, 446, 261-269.
87. Vasilaki, A., Mansouri, A., Remmen, H., der Meulen, J. H., Larkin, L., Richardson, A. G., McArdle, A., Faulkner, J. A., Jackson, M. J. (2006). Free radical generation by skeletal muscle of adult and old mice: effect of contractile activity. Aging Cell, 5, 109-117.
88. Wanagat, J., Cao, Z., Pathare, P., Aiken, J. M. (2001). Mitochondrial DNA deletion mutations colocalize with segmental electron transport system abnormalities, muscle fiber atrophy, fiber splitting, and oxidative damage in sarcopenia. The FASEB Journal, 15, 322-332.