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Journal of Nutrition and Metabolism
Volume 2012, Article ID 268197, 13 pages
http://dx.doi.org/10.1155/2012/268197
Review Article

Resistance Training in Type II Diabetes Mellitus: Impact on Areas of Metabolic Dysfunction in Skeletal Muscle and Potential Impact on Bone

Department of Exercise Science & Sport Studies, Springfield College, 263 Alden St. Athletic Training/Exercise Science Complex, Springfield, MA 01109, USA

Received 8 August 2011; Revised 24 October 2011; Accepted 24 November 2011

Academic Editor: Tai C. Chen

Copyright © 2012 Richard J. Wood and Elizabeth C. O'Neill. 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. S. Wild, G. Roglic, A. Green, R. Sicree, and H. King, “Global Prevalence of Diabetes: estimates for the year 2000 and projections for 2030,” Diabetes Care, vol. 27, no. 5, pp. 1047–1053, 2004. View at Publisher · View at Google Scholar · View at Scopus
  2. Centers for Disease Control. National Diabetes Fact Sheet: national estimates and general information on diabetes and prediabetes in the United States, 2011.
  3. R. A. DeFronzo and D. Tripathy, “Skeletal muscle insulin resistance is the primary defect in type 2 diabetes,” Diabetes Care, vol. 32, pp. S157–S163, 2009. View at Google Scholar · View at Scopus
  4. B. H. Goodpaster, F. L. Thaete, and D. E. Kelley, “Thigh adipose tissue distribution is associated with insulin resistance in obesity and in type 2 diabetes mellitus,” American Journal of Clinical Nutrition, vol. 71, no. 4, pp. 885–892, 2000. View at Google Scholar · View at Scopus
  5. M. G. Cree, B. R. Newcomer, C. S. Katsanos et al., “Intramuscular and liver triglycerides are increased in the elderly,” Journal of Clinical Endocrinology and Metabolism, vol. 89, no. 8, pp. 3864–3871, 2004. View at Publisher · View at Google Scholar · View at Scopus
  6. P. M. Garcia-Roves, “Mitochondrial pathophysiology and type 2 diabetes mellitus,” Archives of Physiology and Biochemistry, vol. 117, no. 3, pp. 177–187, 2011. View at Publisher · View at Google Scholar
  7. A. V. Schwartz, D. E. Sellmeyer, K. E. Ensrud et al., “Older women with diabetes have an increased risk of fracture: a prospective study,” Journal of Clinical Endocrinology and Metabolism, vol. 86, no. 1, pp. 32–38, 2001. View at Publisher · View at Google Scholar · View at Scopus
  8. K. Wongdee and N. Charoenphandhu, “Osteoporosis in diabetes mellitus: possible cellular and molecular mechanisms,” World Journal of Diabetes, vol. 3, pp. 41–48, 2011. View at Google Scholar
  9. W. Wang, X. Zhang, J. Zheng, and J. Yang, “High glucose stimulates adipogenic and inhibits osteogenic differentiation in MG-63 cells through cAMP/protein kinase A/extracellular signal-regulated kinase pathway,” Molecular and Cellular Biochemistry, vol. 338, no. 1-2, pp. 115–122, 2010. View at Publisher · View at Google Scholar · View at Scopus
  10. H. C. Gerstein, M. E. Miller, S. Genuth et al., “Long-term effects of intensive glucose lowering on cardiovascular outcomes,” The New England Journal of Medicine, vol. 364, no. 9, pp. 818–828, 2011. View at Publisher · View at Google Scholar
  11. C. Irvine and N. F. Taylor, “Progressive resistance exercise improves glycaemic control in people with type 2 diabetes mellitus: a systematic review,” The Australian Journal of Physiotherapy, vol. 55, no. 4, pp. 237–246, 2009. View at Google Scholar · View at Scopus
  12. J. Ibañez, M. Izquierdo, I. Argüelles et al., “Twice-weekly progressive resistance training decreases abdominal fat and improves insulin sensitivity in older men with type 2 diabetes,” Diabetes Care, vol. 28, no. 3, pp. 662–667, 2005. View at Publisher · View at Google Scholar
  13. A. Misra, N. K. Alappan, N. K. Vikram et al., “Effect of supervised progressive resistance-exercise training protocol on insulin sensitivity, glycemia, lipids, and Body composition in asian indians with type 2 diabetes,” Diabetes Care, vol. 31, no. 7, pp. 1282–1287, 2008. View at Publisher · View at Google Scholar · View at Scopus
  14. R. J. Sigal, G. P. Kenny, N. G. Boulé et al., “Effects of aerobic training, resistance training, or both on glycemic control in type 2 diabetes: a randomized trial,” Annals of Internal Medicine, vol. 147, no. 6, pp. 357–369, 2007. View at Google Scholar · View at Scopus
  15. S. Zanuso, A. Jimenez, G. Pugliese, G. Corigliano, and S. Balducci, “Exercise for the management of type 2 diabetes: a review of the evidence,” Acta Diabetologica, vol. 47, no. 1, pp. 15–22, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. R. A. DeFronzo, E. Jacot, E. Jequier, E. Maeder, J. Wahren, and J. P. Felber, “The effect of insulin on the disposal of intravenous glucose. Results from indirect calorimetry and hepatic and femoral venous catheterization,” Diabetes, vol. 30, no. 12, pp. 1000–1007, 1981. View at Google Scholar · View at Scopus
  17. J. H. Warram, B. C. Martin, A. S. Krolewski, J. S. Soeldner, and C. R. Kahn, “Slow glucose removal rate and hyperinsulinemia precede the development of type II diabetes in the offspring of diabetic parents,” Annals of Internal Medicine, vol. 113, no. 12, pp. 909–915, 1990. View at Google Scholar · View at Scopus
  18. G. Perseghin, S. Ghosh, K. Gerow, and G. I. Shulman, “Metabolic defects in lean nondiabetic offspring of NIDDM parents: a cross-sectional study,” Diabetes, vol. 46, no. 6, pp. 1001–1009, 1997. View at Google Scholar · View at Scopus
  19. D. Jallut, A. Golay, R. Munger et al., “Impaired glucose tolerance and diabetes in obesity: a 6-year follow-up study of glucose metabolism,” Metabolism, vol. 39, no. 10, pp. 1068–1075, 1990. View at Publisher · View at Google Scholar · View at Scopus
  20. E. Ferrannini, A. Gastaldelli, M. Matsuda et al., “Influence of ethnicity and familial diabetes on glucose tolerance and insulin action: a physiological analysis,” Journal of Clinical Endocrinology and Metabolism, vol. 88, no. 7, pp. 3251–3257, 2003. View at Publisher · View at Google Scholar · View at Scopus
  21. S. R. Kashyap, R. Belfort, R. Berria et al., “Discordant effects of a chronic physiological increase in plasma FFA on insulin signaling in healthy subjects with or without a family history of type 2 diabetes,” American Journal of Physiology, vol. 287, no. 3, pp. E537–E546, 2004. View at Publisher · View at Google Scholar
  22. G. Gulli, E. Ferrannini, M. Stern, S. Haffner, and R. A. DeFronzo, “The metabolic profile of NIDDM is fully established in glucose-tolerant offspring of two Mexican-American NIDDM parents,” Diabetes, vol. 41, no. 12, pp. 1575–1586, 1992. View at Google Scholar · View at Scopus
  23. D. Thiebaud, E. Jacot, and R. A. DeFronzo, “The effect of graded doses of insulin on total glucose uptake, glucose oxidation, and glucose storage in man,” Diabetes, vol. 31, no. 11, pp. 957–963, 1982. View at Google Scholar
  24. R. A. DeFronzo, “Pathogenesis of type 2 diabetes mellitus,” Medical Clinics of North America, vol. 88, no. 4, pp. 787–835, 2004. View at Publisher · View at Google Scholar · View at Scopus
  25. G. I. Shulman, D. L. Rothman, T. Jue, P. Stein, R. A. DeFronzo, and R. G. Shulman, “Quantitation of muscle glycogen synthesis in normal subjects and subjects with non-insulin-dependent diabetes by 13C nuclear magnetic resonance spectroscopy,” The New England Journal of Medicine, vol. 322, no. 4, pp. 223–228, 1990. View at Google Scholar
  26. J. He and D. E. Kelley, “Muscle glycogen content in type 2 diabetes mellitus,” American Journal of Physiology, vol. 287, no. 5, pp. E1002–E1007, 2004. View at Publisher · View at Google Scholar
  27. K. Morino, K. F. Petersen, S. Dufour et al., “Reduced mitochondrial density and increased IRS-1 serine phosphorylation in muscle of insulin-resistant offspring of type 2 diabetic parents,” The Journal of Clinical Investigation, vol. 115, no. 12, pp. 3587–3593, 2005. View at Publisher · View at Google Scholar · View at Scopus
  28. D. E. Kelley, J. He, E. V. Menshikova, and V. B. Ritov, “Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes,” Diabetes, vol. 51, no. 10, pp. 2944–2950, 2002. View at Google Scholar · View at Scopus
  29. F. G. S. Toledo, E. V. Menshikova, V. B. Ritov et al., “Effects of physical activity and weight loss on skeletal muscle mitochondria and relationship with glucose control in type 2 diabetes,” Diabetes, vol. 56, no. 8, pp. 2142–2147, 2007. View at Publisher · View at Google Scholar · View at Scopus
  30. S. Larsen, I. Ara, R. Rabøl et al., “Are substrate use during exercise and mitochondrial respiratory capacity decreased in arm and leg muscle in type 2 diabetes?” Diabetologia, vol. 52, no. 7, pp. 1400–1408, 2009. View at Publisher · View at Google Scholar · View at Scopus
  31. V. B. Ritov, E. V. Menshikova, K. Azuma et al., “Deficiency of electron transport chain in human skeletal muscle mitochondria in type 2 diabetes mellitus and obesity,” American Journal of Physiology, vol. 298, no. 1, pp. E49–E58, 2010. View at Publisher · View at Google Scholar
  32. C. Schmitz-Peiffer, “Protein kinase C and lipid-induced insulin resistance in skeletal muscle,” Annals of the New York Academy of Sciences, vol. 967, pp. 146–157, 2002. View at Google Scholar · View at Scopus
  33. D. E. Kelley and J. A. Simoneau, “Impaired free fatty acid utilization by skeletal muscle in non-insulin- dependent diabetes mellitus,” The Journal of Clinical Investigation, vol. 94, no. 6, pp. 2349–2356, 1994. View at Google Scholar · View at Scopus
  34. G. Perseghin, P. Scifo, F. De Cobelli et al., “Intramyocellular triglyceride content is a determinant of in vivo insulin resistance in humans: a 1H-13C nuclear magnetic resonance spectroscopy assessment in offspring of type 2 diabetic parents,” Diabetes, vol. 48, no. 8, pp. 1600–1606, 1999. View at Publisher · View at Google Scholar
  35. P. Malenfant, D. R. Joanisse, R. Thériault, B. H. Goodpaster, D. E. Kelley, and J.-A. Simoneau, “Fat content in individual muscle fibers of lean and obese subjects,” International Journal of Obesity, vol. 25, no. 9, pp. 1316–1321, 2001. View at Publisher · View at Google Scholar
  36. M. Visser, B. H. Goodpaster, S. B. Kritchevsky et al., “Muscle mass, muscle strength, and muscle fat infiltration as predictors of incident mobility limitations in well-functioning older persons,” The Journals of Gerontology Series A, vol. 60, no. 3, pp. 324–333, 2005. View at Google Scholar · View at Scopus
  37. M. Visser, S. M. F. Pluijm, V. S. Stel, R. J. Bosscher, and D. J. H. Deeg, “Physical activity as a determinant of change in mobility performance: the longitudinal aging study Amsterdam,” Journal of the American Geriatrics Society, vol. 50, no. 11, pp. 1774–1781, 2002. View at Publisher · View at Google Scholar · View at Scopus
  38. A. V. Schwartz, “Diabetes Mellitus: does it affect bone?” Calcified Tissue International, vol. 73, no. 6, pp. 515–519, 2003. View at Publisher · View at Google Scholar · View at Scopus
  39. G. K. Reddy, L. Stehno-Bittel, S. Hamade, and C. S. Enwemeka, “The biomechanical integrity of bone in experimental diabetes,” Diabetes Research and Clinical Practice, vol. 54, no. 1, pp. 1–8, 2001. View at Google Scholar · View at Scopus
  40. H. M. Frost, “Emerging views about “osteoporosis”, bone health, strength, fragility, and their determinants,” Journal of Bone and Mineral Metabolism, vol. 20, no. 6, pp. 319–325, 2002. View at Publisher · View at Google Scholar · View at Scopus
  41. K. K. Nicodemus and A. R. Folsom, “Type 1 and type 2 diabetes and incident hip fractures in postmenopausal women,” Diabetes Care, vol. 24, no. 7, pp. 1192–1197, 2001. View at Google Scholar · View at Scopus
  42. I. I. De Liefde, M. Van Der Klift, C. E. D. H. De Laet, P. L. A. Van Daele, A. Hofman, and H. A. P. Pols, “Bone mineral density and fracture risk in type-2 diabetes mellitus: the Rotterdam Study,” Osteoporosis International, vol. 16, no. 12, pp. 1713–1720, 2005. View at Publisher · View at Google Scholar · View at Scopus
  43. N. A. Sims and J. H. Gooi, “Bone remodeling: multiple cellular interactions required for coupling of bone formation and resorption,” Seminars in Cell and Developmental Biology, vol. 19, no. 5, pp. 444–451, 2008. View at Publisher · View at Google Scholar · View at Scopus
  44. S. L. Teitelbaum, “Bone resorption by osteoclasts,” Science, vol. 289, no. 5484, pp. 1504–1508, 2000. View at Publisher · View at Google Scholar · View at Scopus
  45. T. Akune, N. Ogata, K. Hoshi et al., “Insulin receptor substrate-2 maintains predominance of anabolic function over catabolic function of osteoblasts,” Journal of Cell Biology, vol. 159, no. 1, pp. 147–156, 2002. View at Publisher · View at Google Scholar · View at Scopus
  46. S. Yamagishi, K. Nakamura, and H. Inoue, “Possible participation of advanced glycation end products in the pathogenesis of osteoporosis in diabetic patients,” Medical Hypotheses, vol. 65, no. 6, pp. 1013–1015, 2005. View at Publisher · View at Google Scholar · View at Scopus
  47. M. Zayzafoon, W. E. Gathings, and J. M. McDonald, “Modeled microgravity inhibits osteogenic differentiation of human mesenchymal stem cells and increases adipogenesis,” Endocrinology, vol. 145, no. 5, pp. 2421–2432, 2004. View at Publisher · View at Google Scholar
  48. N. Di Iorgi, M. Rosol, S. D. Mittelman, and V. Gilsanz, “Reciprocal relation between marrow adiposity and the amount of bone in the axial and appendicular skeleton of young adults,” Journal of Clinical Endocrinology and Metabolism, vol. 93, no. 6, pp. 2281–2286, 2008. View at Publisher · View at Google Scholar · View at Scopus
  49. A. Goldin, J. A. Beckman, A. M. Schmidt, and M. A. Creager, “Advanced glycation end products: sparking the development of diabetic vascular injury,” Circulation, vol. 114, no. 6, pp. 597–605, 2006. View at Publisher · View at Google Scholar · View at Scopus
  50. R. Singh, A. Barden, T. Mori, and L. Beilin, “Advanced glycation end-products: a review,” Diabetologia, vol. 44, no. 2, pp. 129–146, 2001. View at Publisher · View at Google Scholar · View at Scopus
  51. M. Alikhani, Z. Alikhani, C. Boyd et al., “Advanced glycation end products stimulate osteoblast apoptosis via the MAP kinase and cytosolic apoptotic pathways,” Bone, vol. 40, no. 2, pp. 345–353, 2007. View at Publisher · View at Google Scholar · View at Scopus
  52. M. Saito, K. Fujii, Y. Mori, and K. Marumo, “Role of collagen enzymatic and glycation induced cross-links as a determinant of bone quality in spontaneously diabetic WBN/Kob rats,” Osteoporosis International, vol. 17, no. 10, pp. 1514–1523, 2006. View at Publisher · View at Google Scholar · View at Scopus
  53. S. Viguet-Carrin, P. Garnero, and P. D. Delmas, “The role of collagen in bone strength,” Osteoporosis International, vol. 17, no. 3, pp. 319–336, 2006. View at Publisher · View at Google Scholar · View at Scopus
  54. N. Brooks, J. E. Layne, P. L. Gordon, R. Roubenoff, M. E. Nelson, and C. Castaneda-Sceppa, “Strength training improves muscle quality and insulin sensitivity in Hispanic older adults with type 2 diabetes,” International Journal of Medical Sciences, vol. 4, no. 1, pp. 19–27, 2007. View at Google Scholar · View at Scopus
  55. E. H. Morrato, J. O. Hill, H. R. Wyatt, V. Ghushchyan, and P. W. Sullivan, “Physical activity in U.S. adults with diabetes and at risk for developing diabetes, 2003,” Diabetes Care, vol. 30, no. 2, pp. 203–209, 2007. View at Publisher · View at Google Scholar · View at Scopus
  56. M. Saito and K. Marumo, “Collagen cross-links as a determinant of bone quality: a possible explanation for bone fragility in aging, osteoporosis, and diabetes mellitus,” Osteoporosis International, vol. 21, no. 2, pp. 195–214, 2010. View at Publisher · View at Google Scholar · View at Scopus
  57. S. Botolin, M. C. Faugere, H. Malluche, M. Orth, R. Meyer, and L. R. McCabe, “Increased bone adiposity and peroxisomal proliferator-activated receptor-γ2 expression in type I diabetic mice,” Endocrinology, vol. 146, no. 8, pp. 3622–3631, 2005. View at Publisher · View at Google Scholar · View at Scopus
  58. Q. Wang and T. Jin, “The role of insulin signaling in the development of β-cell dysfunction and diabetes,” Islets, vol. 1, no. 2, pp. 95–101, 2009. View at Google Scholar
  59. W. L. Haskell, I. M. Lee, R. R. Pate et al., “Physical activity and public health: updated recommendation for adults from the American College of Sports Medicine and the American Heart Association,” Medicine and Science in Sports and Exercise, vol. 39, no. 8, pp. 1423–1434, 2007. View at Publisher · View at Google Scholar · View at Scopus
  60. N. D. Eves and R. C. Plotnikoff, “Resistance training and type 2 diabetes: considerations for implementation at the population level,” Diabetes Care, vol. 29, no. 8, pp. 1933–1941, 2006. View at Publisher · View at Google Scholar · View at Scopus
  61. K. A. Willey and M. A. Fiatarone Singh, “Battling insulin resistance in elderly obese people with type 2 diabetes: bring on the heavy weights,” Diabetes Care, vol. 26, no. 5, pp. 1580–1588, 2003. View at Publisher · View at Google Scholar · View at Scopus
  62. D. J. Cuff, G. S. Meneilly, A. Martin, A. Ignaszewski, H. D. Tildesley, and J. J. Frohlich, “Effective exercise modality to reduce insulin resistance in women with type 2 diabetes,” Diabetes Care, vol. 26, no. 11, pp. 2977–2982, 2003. View at Publisher · View at Google Scholar · View at Scopus
  63. D. W. Dunstan, R. M. Daly, N. Owen et al., “High-intensity resistance training improves glycemic control in older patients with type 2 diabetes,” Diabetes Care, vol. 25, no. 10, pp. 1729–1736, 2002. View at Publisher · View at Google Scholar · View at Scopus
  64. J. C. Baldi and N. Snowling, “Resistance training improves glycaemic control in obese type 2 diabetic men,” International Journal of Sports Medicine, vol. 24, no. 6, pp. 419–423, 2003. View at Publisher · View at Google Scholar · View at Scopus
  65. A. J. Rose and E. A. Richter, “Skeletal muscle glucose uptake during exercise: how is it regulated?” Physiology, no. 4, pp. 260–270, 2005. View at Google Scholar · View at Scopus
  66. C. Castaneda, J. E. Layne, L. Munoz-Orians et al., “A randomized controlled trial of resistance exercise training to improve glycemic control in older adults with type 2 diabetes,” Diabetes Care, vol. 25, no. 12, pp. 2335–2341, 2002. View at Google Scholar · View at Scopus
  67. D. W. Dunstan, I. B. Puddey, L. J. Beilin, V. Burke, A. R. Morton, and K. G. Stanton, “Effects of a short-term circuit weight training program on glycaemic control in NIDDM,” Diabetes Research and Clinical Practice, vol. 40, no. 1, pp. 53–61, 1998. View at Publisher · View at Google Scholar · View at Scopus
  68. N. Musi, N. Fujii, M. F. Hirshman et al., “AMP-activated protein kinase (AMPK) is activated in muscle of subjects with type 2 diabetes during exercise,” Diabetes, vol. 50, no. 5, pp. 921–927, 2001. View at Google Scholar · View at Scopus
  69. T. Ishii, T. Yamakita, T. Sato, S. Tanaka, and S. Fujii, “Resistance training improves insulin sensitivity in NIDDM subjects without altering maximal oxygen uptake,” Diabetes Care, vol. 21, no. 8, pp. 1353–1355, 1998. View at Publisher · View at Google Scholar · View at Scopus
  70. M. K. Holten, M. Zacho, M. Gaster, C. Juel, J. F. P. Wojtaszewski, and F. Dela, “Strength training increases insulin-mediated glucose uptake, GLUT4 content, and insulin signaling in skeletal muscle in patients with type 2 diabetes,” Diabetes, vol. 53, no. 2, pp. 294–305, 2004. View at Publisher · View at Google Scholar · View at Scopus
  71. Y. H. Ku, K. A. Han, H. Ahn et al., “Resistance exercise did not alter intramuscular adipose tissue but reduced retinol-binding protein-4 concentration in individuals with type 2 diabetes mellitus,” Journal of International Medical Research, vol. 38, no. 3, pp. 782–791, 2010. View at Google Scholar · View at Scopus
  72. S. F. E. Praet, R. A. M. Jonkers, G. Schep et al., “Long-standing, insulin-treated type 2 diabetes patients with complications respond well to short-term resistance and interval exercise training,” European Journal of Endocrinology, vol. 158, no. 2, pp. 163–172, 2008. View at Publisher · View at Google Scholar · View at Scopus
  73. L. Coderre, K. V. Kandror, G. Vallega, and P. F. Pilch, “Identification and characterization of an exercise-sensitive pool of glucose transporters in skeletal muscle,” The Journal of Biological Chemistry, vol. 270, no. 46, pp. 27584–27588, 1995. View at Publisher · View at Google Scholar · View at Scopus
  74. K. Lemieux, X. X. Han, L. Dombrowski, A. Bonen, and A. Marette, “The transferrin receptor defines two distinct contraction-responsive GLUT4 vesicle populations in skeletal muscle,” Diabetes, vol. 49, no. 2, pp. 183–189, 2000. View at Google Scholar · View at Scopus
  75. L. J. Goodyear, M. F. Hirshman, P. M. Valyou, and E. S. Horton, “Glucose transporter number, function, and subcellular distribution in rat skeletal muscle after exercise training,” Diabetes, vol. 41, no. 9, pp. 1091–1099, 1992. View at Google Scholar · View at Scopus
  76. E. A. Richter, J. N. Nielsen, S. B. Jørgensen, C. Frøsig, J. B. Birk, and J. O. F. P. Wojtaszewski, “Exercise signalling to glucose transport in skeletal muscle,” Proceedings of the Nutrition Society, vol. 63, no. 2, pp. 211–216, 2004. View at Publisher · View at Google Scholar · View at Scopus
  77. I. K. Martin, A. Katz, and J. Wahren, “Splanchnic and muscle metabolism during exercise in NIDDM patients,” American Journal of Physiology, vol. 269, no. 3, pp. E583–E590, 1995. View at Google Scholar · View at Scopus
  78. R. A. DeFronzo, J. D. Tobin, and R. Andres, “Glucose clamp technique: a method for quantifying insulin secretion and resistance,” American Journal of Physiology Endocrinology Metabolism and Gastrointestinal Physiology, vol. 6, no. 3, pp. E214–E223, 1979. View at Google Scholar · View at Scopus
  79. E. Ferrannini, D. C. Simonson, L. D. Katz et al., “The disposal of an oral glucose load in patients with non-insulin-dependent diabetes,” Metabolism, vol. 37, no. 1, pp. 79–85, 1988. View at Google Scholar · View at Scopus
  80. N. G. Boulé, E. Haddad, G. P. Kenny, G. A. Wells, and R. J. Sigal, “Effects of exercise on glycemic control and body mass in type 2 diabetes mellitus: a meta-analysis of controlled clinical trials,” JAMA, vol. 286, no. 10, pp. 1218–1227, 2001. View at Google Scholar · View at Scopus
  81. V. S. Balakrishnan, M. Rao, V. Menon et al., “Resistance training increases muscle mitochondrial biogenesis in patients with chronic kidney disease,” Clinical Journal of the American Society of Nephrology, vol. 5, no. 6, pp. 996–1002, 2010. View at Publisher · View at Google Scholar · View at Scopus
  82. M. A. Tarnopolsky, “Mitochondrial DNA shifting in older adults following resistance exercise training,” Applied Physiology, Nutrition and Metabolism, vol. 34, no. 3, pp. 348–354, 2009. View at Publisher · View at Google Scholar · View at Scopus
  83. J. M. Luthi, H. Howald, and H. Claassen, “Structural changes in skeletal muscle tissue with heavy-resistance exercise,” International Journal of Sports Medicine, vol. 7, no. 3, pp. 123–127, 1986. View at Google Scholar · View at Scopus
  84. J. D. MacDougall, D. G. Sale, and J. R. Moroz, “Mitochondrial volume density in human skeletal muscle following heavy resistance training,” Medicine and Science in Sports and Exercise, vol. 11, no. 2, pp. 164–166, 1979. View at Google Scholar
  85. G. J. Bell, D. Syrotuik, T. P. Martin, R. Burnham, and H. A. Quinney, “Effect of concurrent strength and endurance training on skeletal muscle properties and hormone concentrations in humans,” European Journal of Applied Physiology, vol. 81, no. 5, pp. 418–427, 2000. View at Google Scholar · View at Scopus
  86. H. J. Green, A. Dahly, K. Shoemaker, C. Goreham, E. Bombardier, and M. Ball-Burnett, “Serial effects of high-resistance and prolonged endurance training on Na+-K+ pump concentration and enzymatic activities in human vastus lateralis,” Acta Physiologica Scandinavica, vol. 165, no. 2, pp. 177–184, 1999. View at Publisher · View at Google Scholar
  87. H. Green, C. Goreham, J. Ouyang, M. Ball-Burnett, and D. Ranney, “Regulation of fiber size, oxidative potential, and capillarization in human muscle by resistance exercise,” American Journal of Physiology, vol. 276, no. 2, pp. R591–R596, 1999. View at Google Scholar · View at Scopus
  88. L. L. Ploutz, P. A. Tesch, R. L. Biro, and G. A. Dudley, “Effect of resistance training on muscle use during exercise,” Journal of Applied Physiology, vol. 76, no. 4, pp. 1675–1681, 1994. View at Google Scholar · View at Scopus
  89. P. A. Tesch, A. Thorsson, and E. B. Colliander, “Effects of eccentric and concentric resistance training on skeletal muscle substrates, enzyme activities and capillary supply,” Acta Physiologica Scandinavica, vol. 140, no. 4, pp. 575–580, 1990. View at Google Scholar · View at Scopus
  90. N. Wang, R. S. Hikida, R. S. Staron, and J. A. Simoneau, “Muscle fiber types of women after resistance training—quantitative ultrastructure and enzyme activity,” Pflügers Archiv European Journal of Physiology, vol. 424, no. 5-6, pp. 494–502, 1993. View at Google Scholar · View at Scopus
  91. J. E. Tang, J. W. Hartman, and S. M. Phillips, “Increased muscle oxidative potential following resistance training induced fibre hypertrophy in young men,” Applied Physiology, Nutrition and Metabolism, vol. 31, no. 5, pp. 495–501, 2006. View at Publisher · View at Google Scholar · View at Scopus
  92. D. L. Costill, E. F. Coyle, and W. F. Fink, “Adaptations in skeletal muscle following strength training,” Journal of Applied Physiology Respiratory Environmental and Exercise Physiology, vol. 46, no. 1, pp. 96–99, 1979. View at Google Scholar
  93. P. V. Komi, J. T. Viitasalo, R. Rauramaa, and V. Vihko, “Effect of isometric strength training on mechanical, electrical, and metabolic aspects of muscle function,” European Journal of Applied Physiology and Occupational Physiology, vol. 40, no. 1, pp. 45–55, 1978. View at Google Scholar · View at Scopus
  94. P. D. Chilibeck, D. G. Syrotuik, and G. J. Bell, “The effect of strength training on estimates of mitochondrial density and distribution throughout muscle fibres,” European Journal of Applied Physiology and Occupational Physiology, vol. 80, no. 6, pp. 604–609, 1999. View at Publisher · View at Google Scholar · View at Scopus
  95. M. Mueller, F. A. Breil, G. Lurman et al., “Different Molecular and Structural Adaptations with Eccentric and Conventional Strength Training in Elderly Men and Women,” Gerontology, vol. 57, no. 6, 2011. View at Publisher · View at Google Scholar · View at Scopus
  96. C. H. Turner and A. G. Robling, “Designing exercise regimens to increase bone strength,” Exercise and Sport Sciences Reviews, vol. 31, no. 1, pp. 45–50, 2003. View at Publisher · View at Google Scholar · View at Scopus
  97. R. L. Duncan and C. H. Turner, “Mechanotransduction and the functional response of bone to mechanical strain,” Calcified Tissue International, vol. 57, no. 5, pp. 344–358, 1995. View at Publisher · View at Google Scholar · View at Scopus
  98. L. E. Lanyon, “Functional strain as a determinant for bone remodeling,” Calcified Tissue International, vol. 36, no. 1, pp. S56–S61, 1984. View at Google Scholar · View at Scopus
  99. S. Srinivasan, B. J. Ausk, S. L. Poliachik, S. E. Warner, T. S. Richardson, and T. S. Gross, “Rest-inserted loading rapidly amplifies the response of bone to small increases in strain and load cycles,” Journal of Applied Physiology, vol. 102, no. 5, pp. 1945–1952, 2007. View at Publisher · View at Google Scholar · View at Scopus
  100. P. J. Ehrlich and L. E. Lanyon, “Mechanical strain and bone cell function: a review,” Osteoporosis International, vol. 13, no. 9, pp. 688–700, 2002. View at Publisher · View at Google Scholar · View at Scopus
  101. L. Vico, P. Collet, A. Guignandon et al., “Effects of long-term microgravity exposure on cancellous and cortical weight-bearing bones of cosmonauts,” The Lancet, vol. 355, no. 9215, pp. 1607–1611, 2000. View at Google Scholar
  102. D. L. Creighton, A. L. Morgan, D. Boardley, and P. Gunnar Brolinson, “Weight-bearing exercise and markers of bone turnover in female athletes,” Journal of Applied Physiology, vol. 90, no. 2, pp. 565–570, 2001. View at Google Scholar · View at Scopus
  103. J. Morel, B. Combe, J. Francisco, and J. Bernard, “Bone mineral density of 704 amateur sportsmen involved in different physical activities,” Osteoporosis International, vol. 12, no. 2, pp. 152–157, 2001. View at Publisher · View at Google Scholar · View at Scopus
  104. R. Fujimura, N. Ashizawa, M. Watanabe et al., “Effect of resistance exercise training on bone formation and resorption in young male subjects assessed by biomarkers of bone metabolism,” Journal of Bone and Mineral Research, vol. 12, no. 4, pp. 656–662, 1997. View at Publisher · View at Google Scholar · View at Scopus
  105. H. C. Almstedt, J. A. Canepa, D. A. Ramirez, and T. C. Shoepe, “Changes in bone mineral density in response to 24 weeks of resistance training in college-age men and women,” Journal of Strength and Conditioning Research, vol. 25, no. 4, pp. 1098–1103, 2011. View at Publisher · View at Google Scholar
  106. D. L. Nichols, C. F. Sanborn, and A. M. Love, “Resistance training and bone mineral density in adolescent females,” Journal of Pediatrics, vol. 139, no. 4, pp. 494–500, 2001. View at Publisher · View at Google Scholar · View at Scopus
  107. L. A. Pruitt, R. D. Jackson, R. L. Bartels, and H. J. Lehnhard, “Weight-training effects on bone mineral density in early postmenopausal women,” Journal of Bone and Mineral Research, vol. 7, no. 2, pp. 179–185, 1992. View at Google Scholar · View at Scopus
  108. J. E. Layne and M. E. Nelson, “The effects of progressive resistance training on bone density: a review,” Medicine and Science in Sports and Exercise, vol. 31, no. 1, pp. 25–30, 1999. View at Publisher · View at Google Scholar · View at Scopus
  109. R. M. Daly, D. W. Dunstan, N. Owen, D. Jolley, J. E. Shaw, and P. Z. Zimmet, “Does high-intensity resistance training maintain bone mass during moderate weight loss in older overweight adults with type 2 diabetes?” Osteoporosis International, vol. 16, no. 12, pp. 1703–1712, 2005. View at Publisher · View at Google Scholar · View at Scopus
  110. K. Menuki, T. Mori, A. Sakai et al., “Climbing exercise enhances osteoblast differentiation and inhibits adipogenic differentiation with high expression of PTH/PTHrP receptor in bone marrow cells,” Bone, vol. 43, no. 3, pp. 613–620, 2008. View at Publisher · View at Google Scholar · View at Scopus
  111. M. Saito, K. Fujii, S. Soshi, and T. Tanaka, “Reductions in degree of mineralization and enzymatic collagen cross-links and increases in glycation-induced pentosidine in the femoral neck cortex in cases of femoral neck fracture,” Osteoporosis International, vol. 17, no. 7, pp. 986–995, 2006. View at Publisher · View at Google Scholar · View at Scopus
  112. P. Boor, P. Celec, M. Behuliak et al., “Regular moderate exercise reduces advanced glycation and ameliorates early diabetic nephropathy in obese Zucker rats,” Metabolism, vol. 58, no. 11, pp. 1669–1677, 2009. View at Publisher · View at Google Scholar · View at Scopus
  113. P. M. Magalhães, H. J. Appell, and J. A. Duarte, “Involvement of advanced glycation end products in the pathogenesis of diabetic complications: the protective role of regular physical activity,” European Review of Aging and Physical Activity, vol. 5, no. 1, pp. 17–29, 2008. View at Publisher · View at Google Scholar · View at Scopus
  114. B. Sen, Z. Xie, N. Case, M. Ma, C. Rubin, and J. Rubin, “Mechanical strain inhibits adipogenesis in mesenchymal stem cells by stimulating a durable β-catenin signal,” Endocrinology, vol. 149, no. 12, pp. 6065–6075, 2008. View at Publisher · View at Google Scholar
  115. D. G. Manuel and S. E. Schultz, “Health-related quality of life and health-adjusted life expectancy of people with diabetes in Ontario, Canada, 1996-1997,” Diabetes Care, vol. 27, no. 2, pp. 407–414, 2004. View at Publisher · View at Google Scholar · View at Scopus
  116. A. Grey, “Thiazolidinedione-induced skeletal fragility—mechanisms and implications,” Diabetes, Obesity and Metabolism, vol. 11, no. 4, pp. 275–284, 2009. View at Publisher · View at Google Scholar · View at Scopus
  117. A. Grey, “Skeletal consequences of thiazolidinedione therapy,” Osteoporosis International, vol. 19, no. 2, pp. 129–137, 2008. View at Publisher · View at Google Scholar · View at Scopus
  118. D. W. Dunstan, R. M. Daly, N. Owen et al., “Home-based resistance training is not sufficient to maintain improved glycemic control following supervised training in older individuals with type 2 diabetes,” Diabetes Care, vol. 28, no. 1, pp. 3–9, 2005. View at Publisher · View at Google Scholar · View at Scopus