Exercise interventions to prevent and manage type 2 diabetes: Physiological mechanisms

Medicine and Sport Science

Volumn 60, Issue , 2014, Pages 36-47

  Dela, Flemming ^a   Prats, Clara ^a   Helge, Jørn Wulff ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84929579189     PISSN: 02545020     EISSN: 16622812     Source Type: Book Series    
DOI: 10.1159/000357334     Document Type: Article

References (82)

1. Bacchi E, Negri C, Targher G, Faccioli N, Lanza M, Zoppini G, Zanolin E, Schena F, Bonora E, Moghetti P: Both resistance training and aerobic training reduce hepatic fat content in type 2 diabetic subjects with NAFLD (The RAED2 randomized trial). Hepatology 2013; 58: 1287-1295.
2. Kadoglou NP, Fotiadis G, Athanasiadou Z, Vitta I, Lampropoulos S, Vrabas IS: The effects of resistance training on ApoB/ApoA-I ratio, Lp(a) and inflammatory markers in patients with type 2 diabetes. Endocrine 2012; 42: 561-569.
3. Kahn CR: Insulin resistance, insulin insensitivity, and insulin unresponsiveness: A necessary distinction. Metabolism 1978; 27: 1893-1902.
4. Dela F, Mikines KJ, Tronier B, Galbo H: Diminished arginine-stimulated insulin secretion in trained men. J Appl Physiol 1990; 69: 261-267.
5. King DS, Dalsky GP, Clutter WE, Young DA, Staten MA, Cryer PE, Holloszy JO: Effects of lack of exercise on insulin secretion and action in trained subjects. Am J Physiol 1988; 254:E537-E542.
6. King DS, Dalsky GP, Staten MA, Clutter WE, Van Houten DR, Holloszy JO: Insulin action and secretion in endurancetrained and untrained humans. J Appl Physiol 1987; 63: 2247-2252.
7. King DS, Staten MA, Kohrt WM, Dalsky GP, Elahi D, Holloszy JO: Insulin secretory capacity in endurance-trained and untrained young men. Am J Physiol 1990; 259:E155-E161.
8. Krishnan RK, Hernandez JM, Williamson DL, O'Gorman DJ, Evans WJ, Kirwan JP: Age-related differences in the pancreatic beta-cell response to hyperglycemia after eccentric exercise. Am J Physiol 1998; 275:E463-E470.
9. Mikines KJ, Dela F, Tronier B, Galbo H: Effect of 7 days of bed rest on dose-response relation between glucose and insulin secretion. Am J Physiol 1989; 257:E43-E48.
10. Mikines KJ, Farrell PA, Sonne B, Tronier B, Galbo H: Postexercise dose-response relationship between plasma glucose and insulin secretion. J Appl Physiol 1988; 64: 988-999.
11. Mikines KJ, Sonne B, Tronier B, Galbo H: Effects of training and detraining on dose-response relationship between glucose and insulin secretion. Am J Physiol 1989; 256:E588-E596.
12. Haffner SM, Lehto S, Ronnemaa T, Pyorala K, Laakso M: Mortality from coronary heart disease in subjects with type 1 diabetes and in nondiabetic subjects with and without prior myocardial infarction. N Engl J Med 1998; 339: 229-234.
13. Griffin SJ, Borch-Johnsen K, Davies MJ, Khunti K, Rutten GE, Sandbaek A, Sharp SJ, Simmons RK, van den Donk M, Wareham NJ, Lauritzen T: Effect of early intensive multifactorial therapy on 5-year cardiovascular outcomes in individuals with type 2 diabetes detected by screening (ADDITION-Europe): A cluster-randomised trial. Lancet 2011; 378: 156-167.
14. Simmons RK, Echouffo-Tcheugui JB, Sharp SJ, Sargeant LA, Williams KM, Prevost AT, Kinmonth AL, Wareham NJ, Griffin SJ: Screening for type 2 diabetes and population mortality over 10 years (ADDITION-Cambridge): A cluster-randomised controlled trial. Lancet 2012; 380: 1741-1748.
15. Wei M, Gibbons LW, Kampert JB, Nichaman MZ, Blair SN: Low cardiorespiratory fitness and physical inactivity as predictors of mortality in men with type 2 diabetes. Ann Intern Med 2000; 132: 605-611.
16. Helmrich SP, Ragland DR, Leung RW, Paffenbarger RS: Physical activity and reduced occurrence of non-insulindependent diabetes-mellitus. N Engl J Med 1991; 325: 147-152.
17. Lynch J, Helmrich SP, Lakka TA, Kaplan GA, Cohen RD, Salonen R, Salonen JT: Moderately intense physical activities and high levels of cardiorespiratory fitness reduce the risk of non-insulin-dependent diabetes mellitus in middle-aged men. Arch Intern Med 1996; 156: 1307-1314.
18. Manson JE, Nathan DM, Krolewski AS, Stampfer MJ, Willett WC, Hennekens CH: A prospective study of exercise and incidence of diabetes among United States male physicians. JAMA 1992; 268: 63-67.
19. Manson JE, Rimm EB, Stampfer MJ, Colditz GA, Willett WC, Krolewski AS, Rosner B, Hennekens CH, Speizer FE: Physical activity and incidence of noninsulin-dependent diabetes-mellitus in women. Lancet 1991; 338: 774-778.
20. Wei M, Kampert JB, Barlow CE, Nichaman MZ, Gibbons LW, Paffenbarger RS Jr, Blair SN: Relationship between low cardiorespiratory fitness and mortality in normal-weight, overweight, and obese men. JAMA 1999; 282: 1547-1553.
21. Eriksson K-F, Lindgärde F: Prevention of type 2 (non-insulin-dependent) diabetes mellitus by diet and physical exercise. Diabetologia 1991; 34: 891-898.
22. Pan XR, Li GW, Hu YH, Wang JX, Yang WY, An ZX, Hu ZX, Lin J, Xiao JZ, Cao HB, Liu PA, Jiang XG, Jiang YY, Wang JP, Zheng H, Zhang H, Bennett PH, Howard BV: Effects of diet and exercise in preventing NIDDM in people with impaired glucose tolerance. The Da Qing IGT and Diabetes Study. Diabetes Care 1997; 20: 537-544.
23. Tuomilehto J, Lindström J, Eriksson JG, Valle TT, Hamalainen H, Ilanne-Parikka P, Keinanen-Kiukaanniemi S, Laakso M, Louheranta A, Rastas M, Salminen V, Uusitupa M: Prevention of type 2 diabetes mellitus by changes in lifestyle among subjects with impaired glucose tolerance. N Engl J Med 2001; 344: 1343-1350.
24. Buchanan TA: (How) can we prevent type 2 diabetes? Diabetes 2007; 56: 1502-1507.
25. Knowler WC, Barrett-Connor E, Fowler SE, Hamman RF, Lachin JM, Walker EA, Nathan DM: Reduction in the incidence of type 2 diabetes with lifestyle intervention or metformin. N Engl J Med 2002; 346: 393-403.
26. Ramachandran A, Snehalatha C, Mary S, Mukesh B, Bhaskar AD, Vijay V: The Indian Diabetes Prevention Programme shows that lifestyle modification and metformin prevent type 2 diabetes in Asian Indian subjects with impaired glucose tolerance (IDPP-1). Diabetologia 2006; 49: 289-297.
27. Wojtaszewski JF, Birk JB, Frosig C, Holten M, Pilegaard H, Dela F: 5 ' AMP activated protein kinase expression in human skeletal muscle: effects of strength training and type 2 diabetes. J Physiol 2005; 564: 563-573.
28. Musi N, Hirshman MF, Nygren J, Svanfeldt M, Bavenholm P, Rooyackers O, Zhou G, Williamson JM, Ljunqvist O, Efendic S, Moller DE, Thorell A, Goodyear LJ: Metformin increases AMP-activated protein kinase activity in skeletal muscle of subjects with type 2 diabetes. Diabetes 2002; 51: 2074-2081.
29. Ouyang J, Parakhia RA, Ochs RS: Metformin activates AMP kinase through inhibition of AMP deaminase. J Biol Chem 2011; 286: 1-11.
30. Brunmair B, Staniek K, Gras F, Scharf N, Althaym A, Clara R, Roden M, Gnaiger E, Nohl H, Waldhausl W, Furnsinn C: Thiazolidinediones, like metformin, inhibit respiratory complex I: A common mechanism contributing to their antidiabetic actions? Diabetes 2004; 53: 1052-1059.
31. Larsen S, Rabol R, Hansen CN, Madsbad S, Helge JW, Dela F: Metformin-treated patients with type 2 diabetes have normal mitochondrial complex I respiration. Diabetologia 2012; 55: 443-449.
32. Li G, Zhang P, Wang J, Gregg EW, Yang W, Gong Q, Li H, Li H, Jiang Y, An Y, Shuai Y, Zhang B, Zhang J, Thompson TJ, Gerzoff RB, Roglic G, Hu Y, Bennett PH: The long-term effect of lifestyle interventions to prevent diabetes in the China Da Qing Diabetes Prevention Study: A 20-year follow-up study. Lancet 2008; 371: 1783-1789.
33. Lindström J, Peltonen M, Eriksson JG, Ilanne-Parikka P, Aunola S, Keinanen-Kiukaanniemi S, Uusitupa M, Tuomilehto J: Improved lifestyle and decreased diabetes risk over 13 years: long-term follow-up of the randomised Finnish Diabetes Prevention Study (DPS). Diabetologia 2013; 56: 284-293.
34. Knowler WC, Fowler SE, Hamman RF, Christophi CA, Hoffman HJ, Brenneman AT, Brown-Friday JO, Goldberg R, Venditti E, Nathan DM: 10-year follow-up of diabetes incidence and weight loss in the Diabetes Prevention Program Outcomes Study. Lancet 2009; 374: 1677-1686.
35. Dela F, Mikines KJ, Larsen JJ, Ploug T, Petersen LN, Galbo H: Insulin stimulated muscle glucose clearance in patients with type 2 diabetes mellitus. Effects of one-legged physical training. Diabetes 1995; 44: 1010-1020.
36. Dela F, Ploug T, Handberg A, Petersen LN, Larsen JJ, Mikines KJ, Galbo H: Physical training increases muscle GLUT-4 protein and mRNA in patients with NIDDM. Diabetes 1994; 43: 862-865.
37. Dela F, Stallknecht B: Effect of physical training on insulin secretion and action in skeletal muscle and adipose tissue of first-degree relatives of type 2 diabetic patients. Am J Physiol Endocrinol Metab 2010; 299:E80-E91.
38. Eriksen L, Dahl-Petersen I, Haugaard SB, Dela F: Comparison of the effect of multiple short-duration with single long-duration exercise sessions on glucose homeostasis in type 2 diabetes mellitus. Diabetologia 2007; 50: 2245-2253.
39. Holten MK, Zacho M, Gaster M, Juel C, Wojtaszewski JFP, 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: 294-305.
40. Sonne MP, Scheede-Bergdahl C, Olsen DB, Hojbjerre L, Alibegovic A, Nielsen NB, Stallknecht B, Helge JW, Vaag A, Dela F: Effects of physical training on endothelial function and limb blood flow in type 2 diabetes. Appl Physiol Nutr Metab 2007; 32: 936-941.
41. Wojtaszewski JFP, Pilegaard H, Dela F: Resistance exercise training and the management of diabetes; in Hawley JA, Zierath JR (eds): Physical Activity and Type 2 Diabetes. Therapeutic Effects and Mechanisms of Action. Champaign, Human Kinetics, 2008.
42. Dela F, Larsen JJ, Mikines KJ, Galbo H: Normal effect of insulin to stimulate leg blood flow in NIDDM. Diabetes 1995; 44: 221-226.
43. Laakso M, Edelman SV, Brechtel G, Baron AD: Impaired insulin-mediated skeletal muscle blood flow in patients with NIDDM. Diabetes 1992; 41: 1076-1083.
44. Dela F: The effect of training on insulin binding, content of glucose transporter protein (GLUT4) and glucose uptake in human skeletal muscle; in Barreiros HM (ed): Motricidade Humana. Proceedings at the 4th International Course on Physiological Chemistry of Exercise and Training. Lisboa, Faculdade de Motricidade Humana, 1993, pp 15-22.
45. Baron AD, Tarshoby M, Hook G, Lazaridis EN, Cronin J, Johnson A, Steinberg HO: Interaction between insulin sensitivity and muscle perfusion on glucose uptake in human skeletal muscle: evidence for capillary recruitment. Diabetes 2000; 49: 768-774.
46. Andersen PH, Lund S, Schmitz O, Junker S, Kahn BB, Pedersen O: Increased insulin-stimulated glucose uptake in athletes-The importance of Glut4 Mrna, Glut4 protein and fibre type composition of skeletal muscle. Acta Physiol Scand 1993; 149: 393-404.
47. Christ-Roberts CY, Pratipanawatr T, Pratipanawatr W, Berria R, Belfort R, Kashyap S, Mandarino LJ: Exercise training increases glycogen synthase activity and GLUT4 expression but not insulin signaling in overweight nondiabetic and type 2 diabetic subjects. Metabolism 2004; 53: 1233-1242.
48. Dela F, Larsen JJ, Mikines KJ, Handberg A, Ploug T, Petersen LN, Galbo H: The effect of training on GLUT4 protein and mRNA in patients with type 2 diabetes; in Ninomiya K (ed): IDF Satellite Symposium on Glucose Fluxes, Exercise and Diabetes. London, Smith-Gordon, 1995.
49. Langfort J, Viese M, Ploug T, Dela F: Time course of GLUT4 and AMPK protein expression in human skeletal muscle during one month of physical training. Scand J Med Sci Sports 2003; 13: 169-174.
50. Ren JM, Semenkovich CF, Gulve EA, Gao JP, Holloszy JO: Exercise induces rapid increases in GLUT4 expression, glucose transport capacity, and insulinstimulated glycogen storage in muscle. J Biol Chem 1994; 269: 14396-14401.
51. Lauritzen HP, Ploug T, Prats C, Tavare JM, Galbo H: Imaging of insulin signaling in skeletal muscle of living mice shows major role of T-tubules. Diabetes 2006; 55: 1300-1306.
52. Ludatscher R, Silbermann M, Gershon D, Reznick A: The effects of enforced running on the gastrocnemius muscle in aging mice: an ultrastructural study. Exp Gerontol 1983; 18: 113-123.
53. Mandroukas K, Krotkiewski M, Holm G, Stromblad G, Grimby G, Lithell H, Wroblewski Z, Bjorntrop P: Muscle adaptations and glucose control after physical training in insulin-dependent diabetes mellitus. Clin Physiol 1986; 6: 39-52.
54. Vestergaard H, Lund S, Larsen FS, Bjerrum OJ, Pedersen O: Glycogen synthase and phosphofructokinase protein and messenger RNA levels in skeletal muscle from insulin-resistant patients with non-insulin-dependent diabetes-mellitus. J Clin Invest 1993; 91: 2342-2350.
55. Bogardus C, Lillioja S, Stone K, Mott D: Correlation between muscle glycogen synthase activity and in vivo insulin action in man. J Clin Invest 1984; 73: 1185-1190.
56. Damsbo P, Vaag A, Hother-Nielsen O, Beck-Nielsen H: Reduced glycogen synthase activity in skeletal muscle from obese patients with and without Type 2 (non-insulin-dependent) diabetes mellitus. Diabetologia 1991; 34: 239-245.
57. Roden M, Petersen KF, Shulman GI: Nuclear magnetic resonance studies of hepatic glucose metabolism in humans. Recent Prog Horm Res 2001; 56: 219-237.
58. Shulman GI, Rothman DL, Jue T, Stein P, DeFronzo RA, Shulman RG: Quantitation of muscle glycogen synthesis in normal subjects and subjects with noninsulin-dependent diabetes by 13C nuclear magnetic resonance spectroscopy. N Engl J Med 1990; 322: 223-228.
59. Højlund K, Staehr P, Hansen BF, Green KA, Hardie DG, Richter EA, Beck-Nielsen H, Wojtaszewski JF: Increased phosphorylation of skeletal muscle glycogen synthase at NH2-terminal sites during physiological hyperinsulinemia in type 2 diabetes. Diabetes 2003; 52: 1393-1402.
60. Richter EA, Ruderman NB: AMPK and the biochemistry of exercise: implications for human health and disease. Biochem J 2009; 418: 261-275.
61. Wojtaszewski JF, Richter EA: Effects of acute exercise and training on insulin action and sensitivity: focus on molecular mechanisms in muscle. Essays Biochem 2006; 42: 31-46.
62. Boule NG, Haddad E, Kenny GP, Wells GA, Sigal RJ: Effects of exercise on glycemic control and body mass in type 2 diabetes mellitus-A meta-analysis of controlled clinical trials. JAMA 2001; 286: 1218-1227.
63. Mikines KJ, Sonne B, Farrell PA, Tronier B, Galbo H: Effect of training on the doseresponse relationship for insulin action in men. J Appl Physiol 1989; 66: 695-703.
64. Craig BW, Everhart J, Brown R: The influence of high-resistance training on glucose tolerance in young and elderly subjects. Mech Ageing Develop 1989; 49: 147-157.
65. Eriksson J, Tuominen J, Valle T, Sundberg S, Sovijarvi A, Lindholm H, Tuomilehto J, Koivisto V: Aerobic endurance exercise or circuit-type resistance training for individuals with impaired glucose tolerance? Horm Metab Res 1998; 30: 37-41.
66. Fluckey JD, Hickey MS, Brambrink JK, Hart KK, Alexander K, Craig BW: Effects of resistance exercise on glucose tolerance in normal and glucose-intolerant subjects. J Appl Physiol 1994; 77: 1087-1092.
67. Honkola A, Forsen T, Eriksson J: Resistance training improves the metabolic profile in individuals with type 2 diabetes. Acta Diabetol 1997; 34: 245-248.
68. Hurley BF, Hagberg JM, Goldberg AP, Seals DR, Ehsani AA, Brennan RE, Holloszy JO: Resistive training can reduce coronary risk factors without altering VO 2max or percent body fat. Med Sci Sports Exerc 1988; 20: 150-154.
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: 1353-1355.
70. Miller JP, Pratley RE, Goldberg AP, Gordon P, Rubin M, Treuth MS, Ryan AS, Hurley BF: Strength training increases insulin action in healthy 50-to 65-yearold men. J Appl Physiol 1994; 77: 1122-1127.
71. Rigla M, Sanchez-Quesada JL, Ordonez-Llanos J, Prat T, Caixas A, Jorba O, Serra JR, de Leiva A, Perez A: Effect of physical exercise on lipoprotein(a) and lowdensity lipoprotein modifications in type 1 and type 2 diabetic patients. Metabolism 2000; 49: 640-647.
72. Smutok MA, Reece C, Kokkinos PF, Farmer CM, Dawson PK, DeVane J, Patterson J, Goldberg AP, Hurley BF: Effects of exercise training modality on glucose tolerance in men with abnormal glucose regulation. Int J Sport Med 1994; 15: 283-289.
73. Aarnio P, Lauritsen T, Dela F: Insulin secretion and glucose kinetics during exercise with and without pharmacological alpha(1)-and alpha(2)-receptor blockade. Diabetes 2001; 50: 1834-1843.
74. Larsen JJ, Dela F, Madsbad S, Vibe-Petersen J, Galbo H: Interaction of sulfonylurea and exercise on glucose homeostasis in type 2 diabetic patients. Diabetes Care 1999; 22: 1647-1654.
75. Kitabchi AE, Temprosa M, Knowler WC, Kahn SE, Fowler SE, Haffner SM, Andres R, Saudek C, Edelstein SL, Arakaki R, Murphy MB, Shamoon H: Role of insulin secretion and sensitivity in the evolution of type 2 diabetes in the diabetes prevention program: effects of lifestyle intervention and metformin. Diabetes 2005; 54: 2404-2414.
76. Bloem CJ, Chang AM: Short-term exercise improves beta-cell function and insulin resistance in older people with impaired glucose tolerance. J Clin Endocrinol Metab 2008; 93: 387-392.
77. Dela F, Mikines KJ, von Linstow M, Galbo H: Effect of training on response to a glucose load adjusted for daily carbohydrate intake. Am J Physiol 1991; 260:E14-E20.
78. Kirwan JP, Kohrt WM, Wojta DM, Bourey RE, Holloszy JO: Endurance exercise training reduces glucose-stimulated insulin levels in 60-to 70-year-old men and women. J Gerontol 1993; 48:M84-M90.
79. Burns N, Finucane FM, Hatunic M, Gilman M, Murphy M, Gasparro D, Mari A, Gastaldelli A, Nolan JJ: Early-onset type 2 diabetes in obese white subjects is characterised by a marked defect in beta cell insulin secretion, severe insulin resistance and a lack of response to aerobic exercise training. Diabetologia 2007; 50: 1500-1508.
80. Solomon TP, Haus JM, Kelly KR, Rocco M, Kashyap SR, Kirwan JP: Improved pancreatic beta-cell function in type 2 diabetic patients after lifestyle-induced weight loss is related to glucose-dependent insulinotropic polypeptide. Diabetes Care 2010; 33: 1561-1566.
81. Dela F, Von Linstow ME, Mikines KJ, Galbo H: Physical training may enhance β-cell function in type 2 diabetes. Am J Physiol Endocrinol Metab 2004; 287:E1024-E1031.
82. Carr DB, Utzschneider KM, Boyko EJ, Asberry PJ, Hull RL, Kodama K, Callahan HS, Matthys CC, Leonetti DL, Schwartz RS, Kahn SE, Fujimoto WY: A reduced-fat diet and aerobic exercise in Japanese Americans with impaired glucose tolerance decreases intra-abdominal fat and improves insulin sensitivity but not beta-cell function. Diabetes 2005; 54: 340-347.