Resistance training in type II diabetes mellitus: Impact on areas of metabolic dysfunction in skeletal muscle and potential impact on bone

Journal of Nutrition and Metabolism

Volumn 2012, Issue , 2012, Pages

  Wood, Richard J ^a   O'Neill, Elizabeth C ^a  

^a SPRINGFIELD COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84873848507     PISSN: 20900724     EISSN: 20900732     Source Type: Journal    
DOI: 10.1155/2012/268197     Document Type: Review

References (118)

1. Wild S., Roglic G., Green A., Sicree R., King H., Global Prevalence of Diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care 2004 27 5 1047 1053 2-s2.0-2342466734 10.2337/diacare.27.5.1047 (Pubitemid 38579764)
2. Centers for Disease Control. National Diabetes Fact Sheet: national estimates and general information on diabetes and prediabetes in the United States, 2011
3. DeFronzo R. A., Tripathy D., Skeletal muscle insulin resistance is the primary defect in type 2 diabetes. Diabetes Care 2009 32 S157 S163 2-s2.0-75549085755
4. Goodpaster B. H., Thaete F. L., Kelley D. E., Thigh adipose tissue distribution is associated with insulin resistance in obesity and in type 2 diabetes mellitus. American Journal of Clinical Nutrition 2000 71 4 885 892 2-s2.0-0034107084 (Pubitemid 30176569)
5. Cree M. G., Newcomer B. R., Katsanos C. S., Sheffield-Moore M., Chinkes D., Aarsland A., Urban R., Wolfe R. R., Intramuscular and liver triglycerides are increased in the elderly. Journal of Clinical Endocrinology and Metabolism 2004 89 8 3864 3871 2-s2.0-4043159763 10.1210/jc.2003-031986 (Pubitemid 39071486)
6. Garcia-Roves P. M., pgarciar@clinic.ub.es Mitochondrial pathophysiology and type 2 diabetes mellitus. Archives of Physiology and Biochemistry 2011 117 3 177 187 10.3109/13813455.2011.584538
7. Schwartz A. V., Sellmeyer D. E., Ensrud K. E., Cauley J. A., Tabor H. K., Schreiner P. J., Jamal S. A., Black D. M., Cummings S. R., Older women with diabetes have an increased risk of fracture: a prospective study. Journal of Clinical Endocrinology and Metabolism 2001 86 1 32 38 2-s2.0-0035143770 10.1210/jc.86.1.32 (Pubitemid 32109771)
8. Wongdee K., Charoenphandhu N., Osteoporosis in diabetes mellitus: possible cellular and molecular mechanisms. World Journal of Diabetes 2011 3 41 48
9. Wang W., Zhang X., Zheng J., Yang J., 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 2010 338 1-2 115 122 2-s2.0-77951297831 10.1007/s11010-009-0344-6
10. Gerstein H. C., gerstein@mcmaster.ca Miller M. E., Genuth S., Ismail-Beigi F., Buse J. B., Goff Jr. D. C., Probstfield J. L., Cushman W. C., Ginsberg H. N., Thomas Bigger J., Grimm R. H. Jr., Byington R. P., Rosenberg Y. D., Friedewald W. T., Long-term effects of intensive glucose lowering on cardiovascular outcomes. The New England Journal of Medicine 2011 364 9 818 828 10.1056/NEJMoa1006524
11. Irvine C., Taylor N. F., Progressive resistance exercise improves glycaemic control in people with type 2 diabetes mellitus: a systematic review. The Australian Journal of Physiotherapy 2009 55 4 237 246 2-s2.0-77449137929
12. Ibañez J., jibanezs@cfnavarra.es Izquierdo M., Argüelles I., Forga L., Larrión J. L., García-Unciti M., Idoate F., Gorostiaga E. M., Twice-weekly progressive resistance training decreases abdominal fat and improves insulin sensitivity in older men with type 2 diabetes. Diabetes Care 2005 28 3 662 667 10.2337/diacare.28.3.662 (Pubitemid 40315329)
13. Misra A., Alappan N. K., Vikram N. K., Goel K., Gupta N., Mittal K., Bhatt S., Luthra K., 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 2008 31 7 1282 1287 2-s2.0-49649101838 10.2337/dc07-2316
14. Sigal R. J., Kenny G. P., Boulé N. G., Wells G. A., Prud'homme D., Fortier M., Reid R. D., Tulloch H., Coyle D., Phillips P., Jennings A., Jaffey J., Effects of aerobic training, resistance training, or both on glycemic control in type 2 diabetes: a randomized trial. Annals of Internal Medicine 2007 147 6 357 369 2-s2.0-34548757192 (Pubitemid 351664536)
15. Zanuso S., Jimenez A., Pugliese G., Corigliano G., Balducci S., Exercise for the management of type 2 diabetes: a review of the evidence. Acta Diabetologica 2010 47 1 15 22 2-s2.0-76449089734 10.1007/s00592-009-0126-3
16. DeFronzo R. A., Jacot E., Jequier E., Maeder E., Wahren J., Felber J. P., The effect of insulin on the disposal of intravenous glucose. Results from indirect calorimetry and hepatic and femoral venous catheterization. Diabetes 1981 30 12 1000 1007 2-s2.0-0019762341
17. Warram J. H., Martin B. C., Krolewski A. S., Soeldner J. S., Kahn C. R., Slow glucose removal rate and hyperinsulinemia precede the development of type II diabetes in the offspring of diabetic parents. Annals of Internal Medicine 1990 113 12 909 915 2-s2.0-0025663581
18. Perseghin G., Ghosh S., Gerow K., Shulman G. I., Metabolic defects in lean nondiabetic offspring of NIDDM parents: a cross-sectional study. Diabetes 1997 46 6 1001 1009 2-s2.0-0030941820 (Pubitemid 27221001)
19. Jallut D., Golay A., Munger R., Frascarolo P., Schutz Y., Jequier E., Felber J. P., Impaired glucose tolerance and diabetes in obesity: a 6-year follow-up study of glucose metabolism. Metabolism 1990 39 10 1068 1075 2-s2.0-0025059405 10.1016/0026-0495(90)90168-C (Pubitemid 20351266)
20. Ferrannini E., Gastaldelli A., Matsuda M., Miyazaki Y., Pettiti M., Glass L., DeFronzo R. A., Influence of ethnicity and familial diabetes on glucose tolerance and insulin action: a physiological analysis. Journal of Clinical Endocrinology and Metabolism 2003 88 7 3251 3257 2-s2.0-0037622785 10.1210/jc.2002-021864 (Pubitemid 36877501)
21. Kashyap S. R., Belfort R., Berria R., Suraamornkul S., Pratipranawatr T., Finlayson J., Barrentine A., Bajaj M., Mandarino L., DeFronzo R., Cusi K., cusi@uthscsa.edu 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 2004 287 3 E537 E546 10.1152/ajpendo.00541.2003 (Pubitemid 39095889)
22. Gulli G., Ferrannini E., Stern M., Haffner S., DeFronzo R. A., The metabolic profile of NIDDM is fully established in glucose-tolerant offspring of two Mexican-American NIDDM parents. Diabetes 1992 41 12 1575 1586 2-s2.0-0026539663
23. Thiebaud D., Jacot E., DeFronzo R. A., The effect of graded doses of insulin on total glucose uptake, glucose oxidation, and glucose storage in man. Diabetes 1982 31 11 957 963 (Pubitemid 12005566)
24. DeFronzo R. A., Pathogenesis of type 2 diabetes mellitus. Medical Clinics of North America 2004 88 4 787 835 2-s2.0-4143151942 10.1016/j.mcna.2004.04.013 (Pubitemid 39090340)
25. Shulman G. I., Rothman D. L., Jue T., Stein P., DeFronzo R. A., Shulman R. G., 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 1990 322 4 223 228 (Pubitemid 20034509)
26. He J., Kelley D. E., kelley@msx.dept-med.pitt.edu Muscle glycogen content in type 2 diabetes mellitus. American Journal of Physiology 2004 287 5 E1002 E1007 10.1152/ajpendo.00015.2004 (Pubitemid 39382939)
27. Morino K., Petersen K. F., Dufour S., Befroy D., Frattini J., Shatzkes N., Neschen S., White M. F., Bilz S., Sono S., Pypaert M., Shulman G. I., 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 2005 115 12 3587 3593 2-s2.0-31044433308 10.1172/JCI25151 (Pubitemid 43121847)
28. Kelley D. E., He J., Menshikova E. V., Ritov V. B., Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 2002 51 10 2944 2950 2-s2.0-0036788293
29. Toledo F. G. S., Menshikova E. V., Ritov V. B., Azuma K., Radikova Z., DeLany J., Kelley D. E., Effects of physical activity and weight loss on skeletal muscle mitochondria and relationship with glucose control in type 2 diabetes. Diabetes 2007 56 8 2142 2147 2-s2.0-34547596186 10.2337/db07-0141 (Pubitemid 47195831)
30. Larsen S., Ara I., Rabol R., Andersen J. L., Boushel R., Dela F., Helge J. W., Are substrate use during exercise and mitochondrial respiratory capacity decreased in arm and leg muscle in type 2 diabetes? Diabetologia 2009 52 7 1400 1408 2-s2.0-67349173674 10.1007/s00125-009-1353-4
31. Ritov V. B., ritov@pitt.edu Menshikova E. V., Azuma K., Wood R., Toledo F. G. S., Goodpaster B. H., Ruderman N. B., Kelley D. E., Deficiency of electron transport chain in human skeletal muscle mitochondria in type 2 diabetes mellitus and obesity. American Journal of Physiology 2010 298 1 E49 E58 10.1152/ajpendo.00317.2009
32. Schmitz-Peiffer C., Protein kinase C and lipid-induced insulin resistance in skeletal muscle. Annals of the New York Academy of Sciences 2002 967 146 157 2-s2.0-0036295566 (Pubitemid 34721902)
33. Kelley D. E., Simoneau J. A., Impaired free fatty acid utilization by skeletal muscle in non-insulin- dependent diabetes mellitus. The Journal of Clinical Investigation 1994 94 6 2349 2356 2-s2.0-0027946529
34. Perseghin G., perseghin.gianluca@hsr.it Scifo P., De Cobelli F., Pagliato E., Battezzati A., Arcelloni C., Vanzulli A., Testolin G., Pozza G., Del Maschio A., Luzi L., 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 1999 48 8 1600 1606 10.2337/diabetes.48.8.1600 (Pubitemid 29356869)
35. Malenfant P., Joanisse D. R., Thériault R., Goodpaster B. H., Kelley D. E., Simoneau J.-A., Fat content in individual muscle fibers of lean and obese subjects. International Journal of Obesity 2001 25 9 1316 1321 10.1038/sj.ijo.0801733 (Pubitemid 32835448)
36. Visser M., Goodpaster B. H., Kritchevsky S. B., Newman A. B., Nevitt M., Rubin S. M., Simonsick E. M., Harris T. B., 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 2005 60 3 324 333 2-s2.0-18244399335 (Pubitemid 40628797)
37. Visser M., Pluijm S. M. F., Stel V. S., Bosscher R. J., Deeg D. J. H., Physical activity as a determinant of change in mobility performance: the longitudinal aging study Amsterdam. Journal of the American Geriatrics Society 2002 50 11 1774 1781 2-s2.0-0036843564 10.1046/j.1532-5415.2002.50504.x (Pubitemid 35291719)
38. Schwartz A. V., Diabetes Mellitus: does it affect bone? Calcified Tissue International 2003 73 6 515 519 2-s2.0-0344736959 10.1007/s00223-003-0023-7 (Pubitemid 37517795)
39. Reddy G. K., Stehno-Bittel L., Hamade S., Enwemeka C. S., The biomechanical integrity of bone in experimental diabetes. Diabetes Research and Clinical Practice 2001 54 1 1 8 2-s2.0-0034861630 (Pubitemid 32782639)
40. Frost H. M., Emerging views about osteoporosis bone health, strength, fragility, and their determinants. Journal of Bone and Mineral Metabolism 2002 20 6 319 325 2-s2.0-0345721354 10.1007/s007740200046 (Pubitemid 40645652)
41. Nicodemus K. K., Folsom A. R., Type 1 and type 2 diabetes and incident hip fractures in postmenopausal women. Diabetes Care 2001 24 7 1192 1197 2-s2.0-0035403830 (Pubitemid 33716397)
42. De Liefde I. I., Van Der Klift M., De Laet C. E. D. H., Van Daele P. L. A., Hofman A., Pols H. A. P., Bone mineral density and fracture risk in type-2 diabetes mellitus: the Rotterdam Study. Osteoporosis International 2005 16 12 1713 1720 2-s2.0-29044446311 10.1007/s00198-005-1909-1 (Pubitemid 41790880)
43. Sims N. A., Gooi J. H., Bone remodeling: multiple cellular interactions required for coupling of bone formation and resorption. Seminars in Cell and Developmental Biology 2008 19 5 444 451 2-s2.0-53849106456 10.1016/j.semcdb. 2008.07.016
44. Teitelbaum S. L., Bone resorption by osteoclasts. Science 2000 289 5484 1504 1508 2-s2.0-0034284970 10.1126/science.289.5484.1504
45. Akune T., Ogata N., Hoshi K., Kubota N., Terauchi Y., Tobe K., Takagi H., Azuma Y., Kadowaki T., Nakamura K., Kawaguchi H., Insulin receptor substrate-2 maintains predominance of anabolic function over catabolic function of osteoblasts. Journal of Cell Biology 2002 159 1 147 156 2-s2.0-0037078330 10.1083/jcb.200204046 (Pubitemid 35191526)
46. Yamagishi S., Nakamura K., Inoue H., Possible participation of advanced glycation end products in the pathogenesis of osteoporosis in diabetic patients. Medical Hypotheses 2005 65 6 1013 1015 2-s2.0-26444480186 10.1016/j.mehy.2005. 07.017 (Pubitemid 41425882)
47. Zayzafoon M., Gathings W. E., McDonald J. M., mcdonald@path.uab.edu Modeled microgravity inhibits osteogenic differentiation of human mesenchymal stem cells and increases adipogenesis. Endocrinology 2004 145 5 2421 2432 10.1210/en.2003-1156 (Pubitemid 38535071)
48. Di Iorgi N., Rosol M., Mittelman S. D., Gilsanz V., 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 2008 93 6 2281 2286 2-s2.0-45149131347 10.1210/jc.2007-2691 (Pubitemid 351831548)
49. Goldin A., Beckman J. A., Schmidt A. M., Creager M. A., Advanced glycation end products: sparking the development of diabetic vascular injury. Circulation 2006 114 6 597 605 2-s2.0-33746920337 10.1161/CIRCULATIONAHA.106. 621854 (Pubitemid 44199649)
50. Singh R., Barden A., Mori T., Beilin L., Advanced glycation end-products: a review. Diabetologia 2001 44 2 129 146 2-s2.0-0035135246 10.1007/ s001250051591 (Pubitemid 32156196)
51. Alikhani M., Alikhani Z., Boyd C., MacLellan C. M., Raptis M., Liu R., Pischon N., Trackman P. C., Gerstenfeld L., Graves D. T., Advanced glycation end products stimulate osteoblast apoptosis via the MAP kinase and cytosolic apoptotic pathways. Bone 2007 40 2 345 353 2-s2.0-33846010477 10.1016/j.bone.2006.09.011 (Pubitemid 46054556)
52. Saito M., Fujii K., Mori Y., Marumo K., Role of collagen enzymatic and glycation induced cross-links as a determinant of bone quality in spontaneously diabetic WBN/Kob rats. Osteoporosis International 2006 17 10 1514 1523 2-s2.0-33748645515 10.1007/s00198-006-0155-5 (Pubitemid 44387486)
53. Viguet-Carrin S., Garnero P., Delmas P. D., The role of collagen in bone strength. Osteoporosis International 2006 17 3 319 336 2-s2.0-33645231272 10.1007/s00198-005-2035-9
54. Brooks N., Layne J. E., Gordon P. L., Roubenoff R., Nelson M. E., Castaneda-Sceppa C., Strength training improves muscle quality and insulin sensitivity in Hispanic older adults with type 2 diabetes. International Journal of Medical Sciences 2007 4 1 19 27 2-s2.0-33846037400 (Pubitemid 46066235)
55. Morrato E. H., Hill J. O., Wyatt H. R., Ghushchyan V., Sullivan P. W., Physical activity in U.S. adults with diabetes and at risk for developing diabetes, 2003. Diabetes Care 2007 30 2 203 209 2-s2.0-33846676157 10.2337/dc06-1128 (Pubitemid 46198320)
56. Saito M., Marumo K., Collagen cross-links as a determinant of bone quality: a possible explanation for bone fragility in aging, osteoporosis, and diabetes mellitus. Osteoporosis International 2010 21 2 195 214 2-s2.0-76549123888 10.1007/s00198-009-1066-z
57. Botolin S., Faugere M. C., Malluche H., Orth M., Meyer R., McCabe L. R., Increased bone adiposity and peroxisomal proliferator-activated receptor- γ 2 expression in type I diabetic mice. Endocrinology 2005 146 8 3622 3631 2-s2.0-23044440774 10.1210/en.2004-1677 (Pubitemid 41058134)
58. Wang Q., Jin T., The role of insulin signaling in the development of β -cell dysfunction and diabetes. Islets 2009 1 2 95 101
59. Haskell W. L., Lee I. M., Pate R. R., Powell K. E., Blair S. N., Franklin B. A., MacEra C. A., Heath G. W., Thompson P. D., Bauman A., 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 2007 39 8 1423 1434 2-s2.0-34548239152 10.1249/mss. 0b013e3180616b27 (Pubitemid 47344026)
60. Eves N. D., Plotnikoff R. C., Resistance training and type 2 diabetes: considerations for implementation at the population level. Diabetes Care 2006 29 8 1933 1941 2-s2.0-33746653251 10.2337/dc05-1981 (Pubitemid 44156659)
61. Willey K. A., Fiatarone Singh M. A., Battling insulin resistance in elderly obese people with type 2 diabetes: bring on the heavy weights. Diabetes Care 2003 26 5 1580 1588 2-s2.0-0043170850 10.2337/diacare.26.5.1580 (Pubitemid 36929195)
62. Cuff D. J., Meneilly G. S., Martin A., Ignaszewski A., Tildesley H. D., Frohlich J. J., Effective exercise modality to reduce insulin resistance in women with type 2 diabetes. Diabetes Care 2003 26 11 2977 2982 2-s2.0-0242363749 10.2337/diacare.26.11.2977 (Pubitemid 37339486)
63. Dunstan D. W., Daly R. M., Owen N., Jolley D., De Courten M., Shaw J., Zimmet P., High-intensity resistance training improves glycemic control in older patients with type 2 diabetes. Diabetes Care 2002 25 10 1729 1736 2-s2.0-0036781529 10.2337/diacare.25.10.1729 (Pubitemid 41071078)
64. Baldi J. C., Snowling N., Resistance training improves glycaemic control in obese type 2 diabetic men. International Journal of Sports Medicine 2003 24 6 419 423 2-s2.0-0041928050 10.1055/s-2003-41173 (Pubitemid 37011539)
65. Rose A. J., Richter E. A., Skeletal muscle glucose uptake during exercise: how is it regulated? Physiology 2005 4 260 270 2-s2.0-24044537627 (Pubitemid 41215200)
66. Castaneda C., Layne J. E., Munoz-Orians L., Gordon P. L., Walsmith J., Foldvari M., Roubenoff R., Tucker K. L., Nelson M. E., A randomized controlled trial of resistance exercise training to improve glycemic control in older adults with type 2 diabetes. Diabetes Care 2002 25 12 2335 2341 2-s2.0-0042288034
67. Dunstan D. W., Puddey I. B., Beilin L. J., Burke V., Morton A. R., Stanton K. G., Effects of a short-term circuit weight training program on glycaemic control in NIDDM. Diabetes Research and Clinical Practice 1998 40 1 53 61 2-s2.0-0031818119 10.1016/S0168-8227(98)00027-8 (Pubitemid 28337798)
68. Musi N., Fujii N., Hirshman M. F., Ekberg I., Fröberg S., Ljungqvist O., Thorell A., Goodyear L. J., AMP-activated protein kinase (AMPK) is activated in muscle of subjects with type 2 diabetes during exercise. Diabetes 2001 50 5 921 927 2-s2.0-0035039274 (Pubitemid 32374520)
69. Ishii T., Yamakita T., Sato T., Tanaka S., Fujii S., Resistance training improves insulin sensitivity in NIDDM subjects without altering maximal oxygen uptake. Diabetes Care 1998 21 8 1353 1355 2-s2.0-0031902198 10.2337/diacare.21. 8.1353 (Pubitemid 28365697)
70. Holten M. K., Zacho M., Gaster M., Juel C., Wojtaszewski J. F. P., Dela F., Strength training increases insulin-mediated glucose uptake, GLUT4 content, and insulin signaling in skeletal muscle in patients with type 2 diabetes. Diabetes 2004 53 2 294 305 2-s2.0-0842310044 10.2337/diabetes.53.2.294 (Pubitemid 38174543)
71. Ku Y. H., Han K. A., Ahn H., Kwon H., Koo B. K., Kim H. C., Min K. W., 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 2010 38 3 782 791 2-s2.0-77954808391
72. Praet S. F. E., Jonkers R. A. M., Schep G., Stehouwer C. D. A., Kuipers H., Keizer H. A., van Loon L. J., Long-standing, insulin-treated type 2 diabetes patients with complications respond well to short-term resistance and interval exercise training. European Journal of Endocrinology 2008 158 2 163 172 2-s2.0-38949168972 10.1530/EJE-07-0169 (Pubitemid 351298532)
73. Coderre L., Kandror K. V., Vallega G., Pilch P. F., Identification and characterization of an exercise-sensitive pool of glucose transporters in skeletal muscle. The Journal of Biological Chemistry 1995 270 46 27584 27588 2-s2.0-0028820335 10.1074/jbc.270.46.27584
74. Lemieux K., Han X. X., Dombrowski L., Bonen A., Marette A., The transferrin receptor defines two distinct contraction-responsive GLUT4 vesicle populations in skeletal muscle. Diabetes 2000 49 2 183 189 2-s2.0-0033979604 (Pubitemid 30070995)
75. Goodyear L. J., Hirshman M. F., Valyou P. M., Horton E. S., Glucose transporter number, function, and subcellular distribution in rat skeletal muscle after exercise training. Diabetes 1992 41 9 1091 1099 2-s2.0-0026803256
76. Richter E. A., Nielsen J. N., Jo-rgensen S. B., Frosig C., Birk J. B., Wojtaszewski J. O. F. P., Exercise signalling to glucose transport in skeletal muscle. Proceedings of the Nutrition Society 2004 63 2 211 216 2-s2.0-2942733636 10.1079/PNS2004343 (Pubitemid 38787467)
77. Martin I. K., Katz A., Wahren J., Splanchnic and muscle metabolism during exercise in NIDDM patients. American Journal of Physiology 1995 269 3 E583 E590 2-s2.0-0029089150
78. DeFronzo R. A., Tobin J. D., Andres R., Glucose clamp technique: a method for quantifying insulin secretion and resistance. American Journal of Physiology Endocrinology Metabolism and Gastrointestinal Physiology 1979 6 3 E214 E223 2-s2.0-0018295623 (Pubitemid 9249478)
79. Ferrannini E., Simonson D. C., Katz L. D., Reichard G., Bevilacqua S., Barrett E. J., Olsson M., DeFronzo R. A., The disposal of an oral glucose load in patients with non-insulin-dependent diabetes. Metabolism 1988 37 1 79 85 2-s2.0-0023838435 (Pubitemid 18057200)
80. Boulé N. G., Haddad E., Kenny G. P., Wells G. A., Sigal R. J., Effects of exercise on glycemic control and body mass in type 2 diabetes mellitus: a meta-analysis of controlled clinical trials. JAMA 2001 286 10 1218 1227 2-s2.0-0035850403 (Pubitemid 33015552)
81. Balakrishnan V. S., Rao M., Menon V., Gordon P. L., Pilichowska M., Castaneda F., Castaneda-Sceppa C., Resistance training increases muscle mitochondrial biogenesis in patients with chronic kidney disease. Clinical Journal of the American Society of Nephrology 2010 5 6 996 1002 2-s2.0-77953319258 10.2215/CJN.09141209
82. Tarnopolsky M. A., Mitochondrial DNA shifting in older adults following resistance exercise training. Applied Physiology, Nutrition and Metabolism 2009 34 3 348 354 2-s2.0-67651231036 10.1139/H09-022
83. Luthi J. M., Howald H., Claassen H., Structural changes in skeletal muscle tissue with heavy-resistance exercise. International Journal of Sports Medicine 1986 7 3 123 127 2-s2.0-0022577414 (Pubitemid 16091922)
84. MacDougall J. D., Sale D. G., Moroz J. R., Mitochondrial volume density in human skeletal muscle following heavy resistance training. Medicine and Science in Sports and Exercise 1979 11 2 164 166 (Pubitemid 10221579)
85. Bell G. J., Syrotuik D., Martin T. P., Burnham R., Quinney H. A., Effect of concurrent strength and endurance training on skeletal muscle properties and hormone concentrations in humans. European Journal of Applied Physiology 2000 81 5 418 427 2-s2.0-0034105145 (Pubitemid 30189966)
86. + pump concentration and enzymatic activities in human vastus lateralis. Acta Physiologica Scandinavica 1999 165 2 177 184 10.1046/j.1365-201x.1999.00484.x (Pubitemid 29090266)
87. Green H., Goreham C., Ouyang J., Ball-Burnett M., Ranney D., Regulation of fiber size, oxidative potential, and capillarization in human muscle by resistance exercise. American Journal of Physiology 1999 276 2 R591 R596 2-s2.0-0033057353 (Pubitemid 29098697)
88. Ploutz L. L., Tesch P. A., Biro R. L., Dudley G. A., Effect of resistance training on muscle use during exercise. Journal of Applied Physiology 1994 76 4 1675 1681 2-s2.0-0028197454 (Pubitemid 24125689)
89. Tesch P. A., Thorsson A., Colliander E. B., Effects of eccentric and concentric resistance training on skeletal muscle substrates, enzyme activities and capillary supply. Acta Physiologica Scandinavica 1990 140 4 575 580 2-s2.0-0025600972
90. Wang N., Hikida R. S., Staron R. S., Simoneau J. A., Muscle fiber types of women after resistance training-quantitative ultrastructure and enzyme activity. Pflügers Archiv European Journal of Physiology 1993 424 5-6 494 502 2-s2.0-0027261201 (Pubitemid 23279913)
91. Tang J. E., Hartman J. W., Phillips S. M., Increased muscle oxidative potential following resistance training induced fibre hypertrophy in young men. Applied Physiology, Nutrition and Metabolism 2006 31 5 495 501 2-s2.0-33845994708 10.1139/H06-026
92. Costill D. L., Coyle E. F., Fink W. F., Adaptations in skeletal muscle following strength training. Journal of Applied Physiology Respiratory Environmental and Exercise Physiology 1979 46 1 96 99 (Pubitemid 9115192)
93. Komi P. V., Viitasalo J. T., Rauramaa R., Vihko V., Effect of isometric strength training on mechanical, electrical, and metabolic aspects of muscle function. European Journal of Applied Physiology and Occupational Physiology 1978 40 1 45 55 2-s2.0-0018083616 (Pubitemid 9067154)
94. Chilibeck P. D., Syrotuik D. G., Bell G. J., The effect of strength training on estimates of mitochondrial density and distribution throughout muscle fibres. European Journal of Applied Physiology and Occupational Physiology 1999 80 6 604 609 2-s2.0-0032827883 10.1007/s004210050641 (Pubitemid 29486044)
95. Mueller M., Breil F. A., Lurman G., Klossner S., Flück M., Billeter R., Däpp C., Hoppeler H., Different Molecular and Structural Adaptations with Eccentric and Conventional Strength Training in Elderly Men and Women. Gerontology 2011 57 6 2-s2.0-79751537988 10.1159/000323267
96. Turner C. H., Robling A. G., Designing exercise regimens to increase bone strength. Exercise and Sport Sciences Reviews 2003 31 1 45 50 2-s2.0-0037260879 10.1097/00003677-200301000-00009 (Pubitemid 36158011)
97. Duncan R. L., Turner C. H., Mechanotransduction and the functional response of bone to mechanical strain. Calcified Tissue International 1995 57 5 344 358 2-s2.0-0028807366 10.1007/BF00302070
98. Lanyon L. E., Functional strain as a determinant for bone remodeling. Calcified Tissue International 1984 36 1 S56 S61 2-s2.0-0021131451 (Pubitemid 14043315)
99. Srinivasan S., Ausk B. J., Poliachik S. L., Warner S. E., Richardson T. S., Gross T. S., Rest-inserted loading rapidly amplifies the response of bone to small increases in strain and load cycles. Journal of Applied Physiology 2007 102 5 1945 1952 2-s2.0-34247891505 10.1152/japplphysiol.00507.2006 (Pubitemid 46701966)
100. Ehrlich P. J., Lanyon L. E., Mechanical strain and bone cell function: a review. Osteoporosis International 2002 13 9 688 700 2-s2.0-0036712047 10.1007/s001980200095 (Pubitemid 35000996)
101. Vico L., vico@univ-st-etienne.fr Collet P., Guignandon A., Lafage-Proust M.-H., Thomas T., Rehailia M., Alexandre C., Effects of long-term microgravity exposure on cancellous and cortical weight-bearing bones of cosmonauts. The Lancet 2000 355 9215 1607 1611 (Pubitemid 30240506)
102. Creighton D. L., Morgan A. L., Boardley D., Gunnar Brolinson P., Weight-bearing exercise and markers of bone turnover in female athletes. Journal of Applied Physiology 2001 90 2 565 570 2-s2.0-0035141696 (Pubitemid 32118915)
103. Morel J., Combe B., Francisco J., Bernard J., Bone mineral density of 704 amateur sportsmen involved in different physical activities. Osteoporosis International 2001 12 2 152 157 2-s2.0-0035086122 10.1007/s001980170148 (Pubitemid 32244669)
104. Fujimura R., Ashizawa N., Watanabe M., Mukai N., Amagai H., Fukubayashi T., Hayashi K., Tokuyama K., Suzuki M., 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 1997 12 4 656 662 2-s2.0-0031002946 10.1359/jbmr.1997.12.4.656 (Pubitemid 27155226)
105. Almstedt H. C., halmstedt@lmu.edu Canepa J. A., Ramirez D. A., Shoepe T. C., 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 2011 25 4 1098 1103 10.1519/JSC.0b013e3181d09e9d
106. Nichols D. L., Sanborn C. F., Love A. M., Resistance training and bone mineral density in adolescent females. Journal of Pediatrics 2001 139 4 494 500 2-s2.0-0034771390 10.1067/mpd.2001.116698 (Pubitemid 32977262)
107. Pruitt L. A., Jackson R. D., Bartels R. L., Lehnhard H. J., Weight-training effects on bone mineral density in early postmenopausal women. Journal of Bone and Mineral Research 1992 7 2 179 185 2-s2.0-0026500947
108. Layne J. E., Nelson M. E., The effects of progressive resistance training on bone density: a review. Medicine and Science in Sports and Exercise 1999 31 1 25 30 2-s2.0-0032957460 10.1097/00005768-199901000-00006 (Pubitemid 29036355)
109. Daly R. M., Dunstan D. W., Owen N., Jolley D., Shaw J. E., Zimmet P. Z., Does high-intensity resistance training maintain bone mass during moderate weight loss in older overweight adults with type 2 diabetes? Osteoporosis International 2005 16 12 1703 1712 2-s2.0-29044431648 10.1007/s00198-005-1906-4 (Pubitemid 41790879)
110. Menuki K., Mori T., Sakai A., Sakuma M., Okimoto N., Shimizu Y., Kunugita N., Nakamura T., Climbing exercise enhances osteoblast differentiation and inhibits adipogenic differentiation with high expression of PTH/PTHrP receptor in bone marrow cells. Bone 2008 43 3 613 620 2-s2.0-49149084192 10.1016/j.bone.2008.04.022
111. Saito M., Fujii K., Soshi S., Tanaka T., 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 2006 17 7 986 995 2-s2.0-33744974111 10.1007/s00198-006-0087-0 (Pubitemid 43864852)
112. Boor P., Celec P., Behuliak M., Grančič P., Kebis A., Kukan M., Pronayová N., Liptaj T., Ostendorf T., Šebeková K., Regular moderate exercise reduces advanced glycation and ameliorates early diabetic nephropathy in obese Zucker rats. Metabolism 2009 58 11 1669 1677 2-s2.0-70449704575 10.1016/j.metabol.2009.05.025
113. Magalhães P. M., Appell H. J., Duarte J. A., 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 2008 5 1 17 29 2-s2.0-43449120944 10.1007/s11556-008-0032-7
114. Sen B., Xie Z., Case N., Ma M., Rubin C., Rubin J., jrubin@med.unc.edu Mechanical strain inhibits adipogenesis in mesenchymal stem cells by stimulating a durable β -catenin signal. Endocrinology 2008 149 12 6065 6075 10.1210/en.2008-0687
115. Manuel D. G., Schultz S. E., Health-related quality of life and health-adjusted life expectancy of people with diabetes in Ontario, Canada, 1996-1997. Diabetes Care 2004 27 2 407 414 2-s2.0-0842311559 10.2337/diacare.27.2.407 (Pubitemid 38174065)
116. Grey A., Thiazolidinedione-induced skeletal fragility-mechanisms and implications. Diabetes, Obesity and Metabolism 2009 11 4 275 284 2-s2.0-61549098167 10.1111/j.1463-1326.2008.00931.x
117. Grey A., Skeletal consequences of thiazolidinedione therapy. Osteoporosis International 2008 19 2 129 137 2-s2.0-37749034527 10.1007/s00198-007-0477-y
118. Dunstan D. W., Daly R. M., Owen N., Jolley D., Vulikh E., Shaw J., Zimmet P., Home-based resistance training is not sufficient to maintain improved glycemic control following supervised training in older individuals with type 2 diabetes. Diabetes Care 2005 28 1 3 9 2-s2.0-11844272570 10.2337/diacare.28.1.3 (Pubitemid 40095774)