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Journal of Aging Research
Volume 2012, Article ID 172492, 9 pages
http://dx.doi.org/10.1155/2012/172492
Review Article

Role of Exercise Therapy in Prevention of Decline in Aging Muscle Function: Glucocorticoid Myopathy and Unloading

Institute of Exercise Biology and Physiotherapy, University of Tartu, Ravila 14a, 50411 Tartu, Estonia

Received 1 December 2011; Accepted 14 May 2012

Academic Editor: Barbara Tettenborn

Copyright © 2012 Teet Seene and Priit Kaasik. 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. J. M. Haus, J. A. Carrithers, S. W. Trappe, and T. A. Trappe, “Collagen, cross-linking, and advanced glycation end products in aging human skeletal muscle,” Journal of Applied Physiology, vol. 103, no. 6, pp. 2068–2076, 2007. View at Publisher · View at Google Scholar · View at Scopus
  2. T. Trappe, “Influence of aging and long-term unloading on the structure and function of human skeletal muscle,” Applied Physiology, Nutrition and Metabolism, vol. 34, no. 3, pp. 459–464, 2009. View at Publisher · View at Google Scholar · View at Scopus
  3. C. A. D. S. Santos, E. E. M. Dantas, and M. H. R. Moreira, “Correlation of physical aptitude; functional capacity, corporal balance and quality of life (QoL) among elderly women submitted to a post-menopausal physical activities program,” Archives of Gerontology and Geriatrics, vol. 53, pp. 344–349, 2011. View at Publisher · View at Google Scholar · View at Scopus
  4. T. Seene, P. Kaasik, and E. M. Riso, “Review on aging, unloading and reloading: changes in skeletal muscle quantity and quality,” Archives of Gerontology and Geriatrics, vol. 54, no. 2, pp. 374–280, 2011. View at Publisher · View at Google Scholar · View at Scopus
  5. E. Marzetti and C. Leeuwenburgh, “Skeletal muscle apoptosis, sarcopenia and frailty at old age,” Experimental Gerontology, vol. 41, no. 12, pp. 1234–1238, 2006. View at Publisher · View at Google Scholar · View at Scopus
  6. A. Hiona and C. Leeuwenburgh, “The role of mitochondrial DNA mutations in aging and sarcopenia: implications for the mitochondrial vicious cycle theory of aging,” Experimental Gerontology, vol. 43, no. 1, pp. 24–33, 2008. View at Publisher · View at Google Scholar · View at Scopus
  7. P. M. Siu, E. E. Pistilli, and S. E. Alway, “Age-dependent increase in oxidative stress in gastrocnemius muscle with unloading,” Journal of Applied Physiology, vol. 105, no. 6, pp. 1695–1705, 2008. View at Publisher · View at Google Scholar · View at Scopus
  8. S. K. Powers, A. N. Kavazis, and J. M. McClung, “Oxidative stress and disuse muscle atrophy,” Journal of Applied Physiology, vol. 102, no. 6, pp. 2389–2397, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. N. Luden, K. Minchev, E. Hayes, E. Louis, T. Trappe, and S. Trappe, “Human vastus lateralis and soleus muscles display divergent cellular contractile properties,” American Journal of Physiology, vol. 295, no. 5, pp. R1593–R1598, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. C. Leeuwenburgh, C. M. Gurley, B. A. Strotman, and E. E. Dupont-Versteegden, “Age-related differences in apoptosis with disuse atrophy in soleus muscle,” American Journal of Physiology, vol. 288, no. 5, pp. R1288–R1296, 2005. View at Publisher · View at Google Scholar · View at Scopus
  11. A. S. Sreedhar and P. Csermely, “Heat shock proteins in the regulation of apoptosis: new strategies in tumor therapy: a comprehensive review,” Pharmacology and Therapeutics, vol. 101, no. 3, pp. 227–257, 2004. View at Publisher · View at Google Scholar · View at Scopus
  12. T. Ogata, S. Machida, Y. Oishi, M. Higuchi, and I. Muraoka, “Differential cell death regulation between adult-unloaded and aged rat soleus muscle,” Mechanisms of Ageing and Development, vol. 130, no. 5, pp. 328–336, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. J. H. Kim, H. B. Kwak, C. Leeuwenburgh, and J. M. Lawler, “Lifelong exercise and mild (8%) caloric restriction attenuate age-induced alterations in plantaris muscle morphology, oxidative stress and IGF-1 in the fischer-344 rat,” Experimental Gerontology, vol. 43, no. 4, pp. 317–329, 2008. View at Publisher · View at Google Scholar · View at Scopus
  14. T. W. Buford, S. D. Anton, A. R. Judge et al., “Models of accelerated sarcopenia: critical pieces for solving the puzzle of age-related muscle atrophy,” Ageing Research Reviews, vol. 9, no. 4, pp. 369–383, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. R. Roubenoff, “Catabolism of aging: is it an inflammatory process?” Current Opinion in Clinical Nutrition and Metabolic Care, vol. 6, no. 3, pp. 295–299, 2003. View at Publisher · View at Google Scholar · View at Scopus
  16. G. Goldspink and S. D. R. Harridge, “Growth factors and muscle ageing,” Experimental Gerontology, vol. 39, no. 10, pp. 1433–1438, 2004. View at Publisher · View at Google Scholar · View at Scopus
  17. M. J. Toth and A. Tchernof, “Lipid metabolism in the elderly,” European Journal of Clinical Nutrition, vol. 54, supplement 3, pp. S121–S125, 2000. View at Google Scholar · View at Scopus
  18. M. Kjær, P. Magnusson, M. Krogsgaard et al., “Extracellular matrix adaptation of tendon and skeletal muscle to exercise,” Journal of Anatomy, vol. 208, no. 4, pp. 445–450, 2006. View at Publisher · View at Google Scholar · View at Scopus
  19. K. M. Heinemeier, J. L. Olesen, F. Haddad, P. Schjerling, K. M. Baldwin, and M. Kjaer, “Effect of unloading followed by reloading on expression of collagen and related growth factors in rat tendon and muscle,” Journal of Applied Physiology, vol. 106, no. 1, pp. 178–186, 2009. View at Publisher · View at Google Scholar · View at Scopus
  20. A. J. Freemont and J. A. Hoyland, “Morphology, mechanisms and pathology of musculoskeletal ageing,” Journal of Pathology, vol. 211, no. 2, pp. 252–259, 2007. View at Publisher · View at Google Scholar · View at Scopus
  21. D. Pottle and L. E. Gosselin, “Impact of mechanical load on functional recovery after muscle reloading,” Medicine and Science in Sports and Exercise, vol. 32, no. 12, pp. 2012–2017, 2000. View at Google Scholar · View at Scopus
  22. D. Attaix, L. Mosoni, D. Dardevet, L. Combaret, P. P. Mirand, and J. Grizard, “Altered responses in skeletal muscle protein turnover during aging in anabolic and catabolic periods,” International Journal of Biochemistry and Cell Biology, vol. 37, no. 10, pp. 1962–1973, 2005. View at Publisher · View at Google Scholar · View at Scopus
  23. T. Seene, P. Kaasik, A. Pehme, K. Alev, and E. M. Riso, “The effect of glucocorticoids on the myosin heavy chain isoforms' turnover in skeletal muscle,” Journal of Steroid Biochemistry and Molecular Biology, vol. 86, no. 2, pp. 201–206, 2003. View at Publisher · View at Google Scholar · View at Scopus
  24. W. Evans, “Functional and metabolic consequences of sarcopenia,” Journal of Nutrition, vol. 127, no. 5, pp. 9985–10035, 1997. View at Google Scholar · View at Scopus
  25. A. L. Goldberg and H. M. Goodman, “Relationship between cortisone and muscle work in determining muscle size,” Journal of Physiology, vol. 200, no. 3, pp. 667–675, 1969. View at Google Scholar · View at Scopus
  26. T. Seene and A. Viru, “The catabolic effect of glucocorticoids on different types of skeletal muscle fibres and its dependence upon muscle activity and interaction with anabolic steroids,” Journal of Steroid Biochemistry, vol. 16, no. 2, pp. 349–352, 1982. View at Publisher · View at Google Scholar · View at Scopus
  27. R. C. Hickson and J. R. Davis, “Partial prevention of glucocorticoid-induced muscle atrophy by endurance training,” The American Journal of Physiology, vol. 241, no. 3, pp. E226–E232, 1981. View at Google Scholar · View at Scopus
  28. R. C. Hickson, T. M. Galassi, J. A. Capaccio, and R. T. Chatterton, “Limited resistance of hypertrophied skeletal muscle to glucocorticoids,” Journal of Steroid Biochemistry, vol. 24, no. 6, pp. 1179–1183, 1986. View at Google Scholar · View at Scopus
  29. S. M. Czerwinski-Helms and R. C. Hickson, “Specificity of activated glucocorticoid receptor expression in heart and skeletal muscle types,” Biochemical and Biophysical Research Communications, vol. 142, no. 2, pp. 322–328, 1987. View at Google Scholar · View at Scopus
  30. T. Seene, P. Kaasik, and M. Umnova, “Structural rearrangements in contractile apparatus and resulting skeletal muscle remodelling: effect of exercise training,” Journal of Sports Medicine and Physical Fitness, vol. 49, no. 4, pp. 410–423, 2009. View at Google Scholar · View at Scopus
  31. T. Seene, P. Kaasik, and K. Alev, “Muscle protein turnover in endurance training: a review,” International Journal of Sports Medicine, vol. 32, no. 12, pp. 905–911, 2011. View at Publisher · View at Google Scholar · View at Scopus
  32. D. A. Hood, “Mechanisms of exercise-induced mitochondrial biogenesis in skeletal muscle,” Applied Physiology, Nutrition and Metabolism, vol. 34, no. 3, pp. 465–472, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. V. Ljubicic, A. M. Joseph, A. Saleem et al., “Transcriptional and post-transcriptional regulation of mitochondrial biogenesis in skeletal muscle: effects of exercise and aging,” Biochimica et Biophysica Acta, vol. 1800, no. 3, pp. 223–234, 2010. View at Publisher · View at Google Scholar · View at Scopus
  34. T. Seene, “Turnover of skeletal muscle contractile proteins in glucocorticoid myopathy,” Journal of Steroid Biochemistry and Molecular Biology, vol. 50, no. 1-2, pp. 1–4, 1994. View at Publisher · View at Google Scholar · View at Scopus
  35. D. Dardevet, C. Sornet, D. Taillandier, I. Savary, D. Attaix, and J. Grizard, “Sensitivity and protein turnover response to glucocorticoids are different in skeletal muscle from adult and old rats. Lack of regulation of the ubiquitin-proteasome proteolytic pathway in aging,” Journal of Clinical Investigation, vol. 96, no. 5, pp. 2113–2119, 1995. View at Google Scholar · View at Scopus
  36. D. Dardevet, C. Sornet, I. Savary, E. Debras, P. Patureau-Mirand, and J. Grizard, “Glucocorticoid effects on insulin- and IGF-I-regulated muscle protein metabolism during aging,” Journal of Endocrinology, vol. 156, no. 1, pp. 83–89, 1998. View at Publisher · View at Google Scholar · View at Scopus
  37. J. N. Artaza, S. Bhasin, C. Mallidis, W. Taylor, K. Ma, and N. F. Gonzalez-Cadavid, “Endogenous expression and localization of myostatin and its relation to myosin heavy chain distribution in C2C12 skeletal muscle cells,” Journal of Cellular Physiology, vol. 190, no. 2, pp. 170–179, 2002. View at Publisher · View at Google Scholar · View at Scopus
  38. T. Seene, M. Umnova, K. Alev, and A. Pehme, “Effect of glucocorticoids on contractile apparatus of rat skeletal muscle,” Journal of Steroid Biochemistry, vol. 29, no. 3, pp. 313–317, 1988. View at Google Scholar · View at Scopus
  39. P. Kaasik, M. Umnova, A. Pehme et al., “Ageing and dexamethasone associated sarcopenia: peculiarities of regeneration,” Journal of Steroid Biochemistry and Molecular Biology, vol. 105, no. 1–5, pp. 85–90, 2007. View at Publisher · View at Google Scholar · View at Scopus
  40. K. R. Short and K. S. Nair, “The effect of age on protein metabolism,” Current Opinion in Clinical Nutrition and Metabolic Care, vol. 3, no. 1, pp. 39–44, 2000. View at Publisher · View at Google Scholar · View at Scopus
  41. J. Järva, K. Alev, and T. Seene, “Myosin heavy chain composition in regenerating skeletal muscle grafts,” Basic and Applied Myology, vol. 7, no. 2, pp. 137–141, 1997. View at Google Scholar
  42. J. Järva, K. Alev, and T. Seene, “The effect of autografting on the myosin composition in skeletal muscle fibers,” Muscle & Nerve, vol. 20, no. 6, pp. 718–727, 1997. View at Google Scholar
  43. T. Seene, M. Umnova, P. Kaasik, K. Alev, and A. Pehme, “Overtraining injuries in athletic population,” in Skeletal Muscle Damage and Repair, P. Tiidus, Ed., Human Kinetics Books, Champaign, Ill, USA, 2008. View at Google Scholar
  44. A. M. Ahtikoski, E. M. Riso, S. O. A. Koskinen, J. Risteli, and T. E. S. Takala, “Regulation of type IV collagen gene expression and degradation in fast and slow muscles during dexamethasone treatment and exercise,” Pflugers Archiv, vol. 448, no. 1, pp. 123–130, 2004. View at Publisher · View at Google Scholar · View at Scopus
  45. E. M. Riso, A. Ahtikoski, K. Alev, P. Kaasik, A. Pehme, and T. Seene, “Relationship between extracellular matrix, contractile apparatus, muscle mass and strength in case of glucocorticoid myopathy,” Journal of Steroid Biochemistry and Molecular Biology, vol. 108, no. 1-2, pp. 117–120, 2008. View at Publisher · View at Google Scholar · View at Scopus
  46. V. Everts, E. van der Zee, L. Creemers, and W. Beertsen, “Phagocytosis and intracellular digestion of collagen, its role in turnover and remodelling,” Histochemical Journal, vol. 28, no. 4, pp. 229–245, 1996. View at Publisher · View at Google Scholar · View at Scopus
  47. V. Kovanen, H. Suominen, and E. Heikkinen, “Mechanical properties of fast and slow skeletal muscle with special reference to collagen and endurance training,” Journal of Biomechanics, vol. 17, no. 10, pp. 725–735, 1984. View at Google Scholar · View at Scopus
  48. V. Kovanen, H. Suominen, and E. Heikkinen, “Collagen of slow twitch and fast twitch muscle fibres in different types of rat skeletal muscle,” European Journal of Applied Physiology and Occupational Physiology, vol. 52, no. 2, pp. 235–242, 1984. View at Google Scholar · View at Scopus
  49. A. Pehme, K. Alev, P. Kaasik, and T. Seene, “Age-related changes in skeletal-muscle myosin heavy-chain composition: effect of mechanical loading,” Journal of Aging and Physical Activity, vol. 12, no. 1, pp. 29–44, 2004. View at Google Scholar · View at Scopus
  50. A. E. Barani, A. C. Durieux, O. Sabido, and D. Freyssenet, “Age-related changes in the mitotic and metabolic characteristics of muscle-derived cells,” Journal of Applied Physiology, vol. 95, no. 5, pp. 2089–2098, 2003. View at Google Scholar · View at Scopus
  51. S. Machida and F. W. Booth, “Increased nuclear proteins in muscle satellite cells in aged animals as compared to young growing animals,” Experimental Gerontology, vol. 39, no. 10, pp. 1521–1525, 2004. View at Publisher · View at Google Scholar · View at Scopus
  52. B. M. Carlson, “Regeneration of entire skeletal muscles,” Federation Proceedings, vol. 45, no. 5, pp. 1456–1460, 1986. View at Google Scholar · View at Scopus
  53. E. Shultz and K. Darr, “The role of satellite cells in adaptive or induced fiber transformations,” in The Dynamic State of Muscle Fibers, D. Pette, Ed., pp. 667–681, Walter De Gruyter, Berlin, Germany, 1990. View at Google Scholar
  54. T. P. White and S. T. Devor, “Skeletal muscle regeneration and plasticity of grafts,” Exercise and Sport Sciences Reviews, vol. 21, pp. 263–295, 1993. View at Google Scholar · View at Scopus
  55. T. Seene, P. Kaasik, K. Alev, A. Pehme, and E. M. Riso, “Composition and turnover of contractile proteins in volume-overtrained skeletal muscle,” International Journal of Sports Medicine, vol. 25, no. 6, pp. 438–445, 2004. View at Publisher · View at Google Scholar · View at Scopus
  56. P. Balagopal, O. E. Rooyackers, D. B. Adey, P. A. Ades, and K. S. Nair, “Effects of aging on in vivo synthesis of skeletal muscle myosin heavy- chain and sarcoplasmic protein in humans,” American Journal of Physiology, vol. 273, no. 4, pp. E790–E800, 1997. View at Google Scholar · View at Scopus
  57. S. Welle, K. Bhatt, and C. Thornton, “Polyadenylated RNA, actin mRNA, and myosin heavy chain mRNA in young and old human skeletal muscle,” American Journal of Physiology, vol. 270, no. 2, pp. E224–E229, 1996. View at Google Scholar · View at Scopus
  58. B. C. Clark and T. M. Manini, “Sarcopenia dynapenia,” Journals of Gerontology A, vol. 63, no. 8, pp. 829–834, 2008. View at Google Scholar · View at Scopus
  59. T. M. Manini and B. C. Clark, “Dynapenia and aging: an uptate,” Journal of Gerontology, vol. 67A, no. 1, pp. 28–40, 2012. View at Publisher · View at Google Scholar
  60. T. Trappe, “Influence of aging and long-term unloading on the structure and function of human skeletal muscle,” Applied Physiology, Nutrition and Metabolism, vol. 34, no. 3, pp. 459–464, 2009. View at Publisher · View at Google Scholar · View at Scopus
  61. M. B. von Bonsdorff and T. Rantanen, “Progression of functional limitations in relation to physical activity: a life course approach,” European Review of Aging and Physical Activity, vol. 8, no. 1, pp. 23–30, 2011. View at Publisher · View at Google Scholar · View at Scopus
  62. H. Mechling and Y. Netz, “Aging and inactivity-capitalizing on the protective effect of planned physical activity in old age,” European Review of Aging and Physical Activity, vol. 6, no. 2, pp. 89–97, 2009. View at Publisher · View at Google Scholar · View at Scopus
  63. W. J. Rejeski and L. R. Brawley, “Functional health: innovations in research on physical activity with older adults,” Medicine and Science in Sports and Exercise, vol. 38, no. 1, pp. 93–99, 2006. View at Publisher · View at Google Scholar · View at Scopus
  64. C. Ducomps, P. Mauriège, B. Darche, S. Combes, F. Lebas, and J. P. Doutreloux, “Effects of jump training on passive mechanical stress and stiffness in rabbit skeletal muscle: role of collagen,” Acta Physiologica Scandinavica, vol. 178, no. 3, pp. 215–224, 2003. View at Publisher · View at Google Scholar · View at Scopus
  65. G. Goldspink, K. Fernandes, P. E. Williams, and D. J. Wells, “Age-related changes in collagen gene expression in the muscles of mdx dystrophic and normal mice,” Neuromuscular Disorders, vol. 4, no. 3, pp. 183–191, 1994. View at Publisher · View at Google Scholar · View at Scopus
  66. S. L. Mcgee, K. J. Mustard, D. G. Hardie, and K. Baar, “Normal hypertrophy accompanied by phosphoryation and activation of AMP-activated protein kinase α1 following overload in LKB1 knockout mice,” Journal of Physiology, vol. 586, no. 6, pp. 1731–1741, 2008. View at Publisher · View at Google Scholar · View at Scopus
  67. R. C. Hickson, T. T. Kurowski, J. A. Capaccio, and R. T. Chatterton, “Androgen cytosol binding in exercise-induced sparing of muscle atrophy,” American Journal of Physiology, vol. 247, no. 5, part 1, pp. E597–E603, 1984. View at Google Scholar · View at Scopus
  68. S. M. Czerwinski and R. C. Hickson, “Glucocorticoid receptor activation during exercise in muscle,” Journal of Applied Physiology, vol. 68, no. 4, pp. 1615–1620, 1990. View at Google Scholar · View at Scopus
  69. E.-M. Riso, A. M. Ahtikoski, M. Umnova et al., “Partial prevention of muscle atrophy in excessive level of glucocorticoids by exercise: effect on contractile proteins and extracellular matrix,” Baltic Journal of Laboratory Animal Science, vol. 13, no. 1, pp. 5–12, 2003. View at Google Scholar
  70. E. M. Riso, A. M. Ahtikoski, T. E. S. Takala, and T. Seene, “The effect of unloading and reloading on the extracellular matrix in skeletal muscle: changes in muscle strength and motor activity,” Biology of Sport, vol. 27, no. 2, pp. 89–94, 2010. View at Google Scholar · View at Scopus
  71. E. P. Rader and J. A. Faulkner, “Recovery from contraction-induced injury is impaired in weight-bearing muscles of old male mice,” Journal of Applied Physiology, vol. 100, no. 2, pp. 656–661, 2006. View at Publisher · View at Google Scholar · View at Scopus
  72. A. C. Fry, “The role of resistance exercise intensity on muscle fibre adaptations,” Sports Medicine, vol. 34, no. 10, pp. 663–679, 2004. View at Publisher · View at Google Scholar · View at Scopus
  73. K. D. Flack, K. P. Davy, M. W. Hulver et al., “Aging, resistance training, and diabetes prevention,” Journal of Aging Research, vol. 2011, Article ID 127315, 12 pages, 2011. View at Publisher · View at Google Scholar
  74. D. R. Moore, J. E. Tang, N. A. Burd, T. Rerecich, M. A. Tarnopolsky, and S. M. Phillips, “Differential stimulation of myofibrillar and sarcoplasmic protein synthesis with protein ingestion at rest and after resistance exercise,” Journal of Physiology, vol. 587, no. 4, pp. 897–904, 2009. View at Publisher · View at Google Scholar · View at Scopus
  75. D. R. Moore, P. J. Atherton, M. J. Rennie, M. A. Tarnopolsky, and S. M. Phillips, “Resistance exercise enhances mTOR and MAPK signalling in human muscle over that seen at rest after bolus protein ingestion,” Acta Physiologica, vol. 201, no. 3, pp. 365–372, 2011. View at Publisher · View at Google Scholar · View at Scopus
  76. J. R. McLester, P. A. Bishop, J. Smith et al., “A series of studies—a practical protocol for testing muscular endurance recovery,” Journal of Strength and Conditioning Research, vol. 17, no. 2, pp. 259–273, 2003. View at Publisher · View at Google Scholar · View at Scopus
  77. J. Fell and A. D. Williams, “The effect of aging on skeletal-muscle recovery from exercise: possible implications for aging athletes,” Journal of Aging and Physical Activity, vol. 16, no. 1, pp. 97–115, 2008. View at Google Scholar · View at Scopus
  78. T. Seene, A. Pehme, K. Alev, P. Kaasik, M. Umnova, and M. Aru, “Effects of resistance training on fast- and slow-twitch muscles in rats,” Biology of Sport, vol. 27, no. 3, pp. 221–229, 2010. View at Google Scholar · View at Scopus
  79. Y. Itai, Y. Kariya, and Y. Hoshino, “Morphological changes in rat hindlimb muscle fibres during recovery from disuse atrophy,” Acta Physiologica Scandinavica, vol. 181, no. 2, pp. 217–224, 2004. View at Publisher · View at Google Scholar · View at Scopus
  80. H. Suominen, “Ageing and maximal physical performance,” European Review of Aging and Physical Activity, vol. 8, no. 1, pp. 37–42, 2011. View at Publisher · View at Google Scholar · View at Scopus
  81. M. Sagiv, E. Goldhammer, D. Ben-Sira, and R. Amir, “Factors defining oxygen uptake at peak exercise in aged people,” European Review of Aging and Physical Activity, vol. 7, no. 1, pp. 1–2, 2010. View at Publisher · View at Google Scholar · View at Scopus
  82. Y. Netz, “Type of activity and fitness benefits as moderators of the effect of physical activity on affect in advanced age: a review,” European Review of Aging and Physical Activity, vol. 6, no. 1, pp. 19–27, 2009. View at Publisher · View at Google Scholar · View at Scopus
  83. D. Kuh, E. J. Bassey, S. Butterworth, R. Hardy, and M. E. J. Wadsworth, “Grip strength, postural control, and functional leg power in a representative cohort of British men and women: associations with physical activity, health status, and socioeconomic conditions,” Journals of Gerontology A, vol. 60, no. 2, pp. 224–231, 2005. View at Google Scholar · View at Scopus
  84. J. M. Guralnik and L. Ferrucci, “Assessing the building blocks of function: utilizing measures of functional limitation,” American Journal of Preventive Medicine, vol. 25, no. 3, pp. 112–121, 2003. View at Publisher · View at Google Scholar · View at Scopus
  85. R. M. Reznick, H. Zong, J. Li et al., “Aging-associated reductions in AMP-activated protein kinase activity and mitochondrial biogenesis,” Cell Metabolism, vol. 5, no. 2, pp. 151–156, 2007. View at Publisher · View at Google Scholar · View at Scopus
  86. D. M. Thomson, J. D. Brown, N. Fillmore et al., “AMP-activated protein kinase response to contractions and treatment with the AMPK activator AICAR in young adult and old skeletal muscle,” Journal of Physiology, vol. 587, no. 9, pp. 2077–2086, 2009. View at Publisher · View at Google Scholar · View at Scopus
  87. W. W. Winder and D. G. Hardie, “Inactivation of acetyl-CoA carboxylase and activation of AMP-activated protein kinase in muscle during exercise,” American Journal of Physiology, vol. 270, no. 2, pp. E299–E304, 1996. View at Google Scholar · View at Scopus
  88. W. W. Spirduso and D. L. Cronin, “Exercise dose-response effects on quality of life and independent living in older adults,” Medicine and Science in Sports and Exercise, vol. 33, supplement 6, pp. S598–S608, 2001. View at Google Scholar · View at Scopus
  89. A. F. Kramer and K. I. Erickson, “Capitalizing on cortical plasticity: influence of physical activity on cognition and brain function,” Trends in Cognitive Sciences, vol. 11, no. 8, pp. 342–348, 2007. View at Publisher · View at Google Scholar · View at Scopus
  90. R. C. Hickson, “Interference of strength development by simultaneously training for strength and endurance,” European Journal of Applied Physiology and Occupational Physiology, vol. 45, no. 2-3, pp. 255–263, 1980. View at Google Scholar · View at Scopus
  91. K. Inoki, Y. Li, T. Zhu, J. Wu, and K. L. Guan, “TSC2 is phosphorylated and inhibited by Akt and suppresses mTOR signalling,” Nature Cell Biology, vol. 4, no. 9, pp. 648–657, 2002. View at Publisher · View at Google Scholar · View at Scopus
  92. G. A. Nader, “Concurrent strength and endurance training: from molecules to man,” Medicine and Science in Sports and Exercise, vol. 38, no. 11, pp. 1965–1970, 2006. View at Publisher · View at Google Scholar · View at Scopus
  93. E. L. Cadore, R. S. Pinto, F. L. R. Lhullier et al., “Physiological effects of concurrent training in elderly men,” International Journal of Sports Medicine, vol. 31, no. 10, pp. 689–697, 2010. View at Publisher · View at Google Scholar · View at Scopus
  94. R. H. Wood, R. Reyes, M. A. Welsch et al., “Concurrent cardiovascular and resistance training in healthy older adults,” Medicine and Science in Sports and Exercise, vol. 33, no. 10, pp. 1751–1758, 2001. View at Google Scholar · View at Scopus
  95. M. Izquierdo, J. Ibañez, K. Häkkinen, W. J. Kraemer, J. L. Larrión, and E. M. Gorostiaga, “Once weekly combined resistance and cardiovascular training in healthy older men,” Medicine and Science in Sports and Exercise, vol. 36, no. 3, pp. 435–443, 2004. View at Publisher · View at Google Scholar · View at Scopus
  96. L. Karavirta, M. P. Tulppo, D. E. Laaksonen et al., “Heart rate dynamics after combined endurance and strength training in older men,” Medicine and Science in Sports and Exercise, vol. 41, no. 7, pp. 1436–1443, 2009. View at Publisher · View at Google Scholar · View at Scopus