Download PDF
Horm Metab Res 2010; 42(13): 950-954
DOI: 10.1055/s-0030-1267174
Animals

© Georg Thieme Verlag KG Stuttgart · New York

Combined Effects of Short-term Calorie Restriction and Exercise on Insulin Action in Normal Rats

H. Y. Jiang1 , 2 , T. Koike1 , 3 , P. Li1 , Z. H. Wang1 , Y. Kawata1 , Y. Oshida1 , 3
  • 1Department of Sports Medicine, Graduate School of Medicine, Nagoya University, Nagoya, Japan
  • 2Department of Physiology and Pathophysiology, Yanbian University Medical College, Yanji, P.R. China
  • 3Research Center of Health, Physical Fitness and Sports, Nagoya University, Nagoya, Japan
Further Information

Publication History

received 10.05.2010

accepted 31.08.2010

Publication Date:
11 October 2010 (online)

Also available at
    Permissions and Reprints

Abstract

The present study examined the effect of combination of short-term calorie restriction (CR) and moderate exercise on insulin action in normal rats. Rats were divided randomly into 4 groups: ad libitum, sedentary (A-Sed); calorie restriction, sedentary (CR-Sed); ad libitum, exercise (A-Ex); and calorie restriction, exercise (CR-Ex). Rats in the exercise groups were run on a rodent treadmill. Rats in the CR groups were fed every alternate day. Oral glucose tolerance test (OGTT) showed improvements in both CR-Sed and A-Ex groups compared with the A-Sed group; no further improvement in glucose tolerance was observed in the CR-Ex group. In contrast, glucose infusion rates (GIRs) determined by the hyperinsulinemic-euglycemic clamp method indicated that the GIR of the CR and exercise combination was significantly better than that of the sole intervention of CR or exercise. There was no difference in the levels of fasting glucose, insulin, or high-molecular weight forms of adiponectin among the 4 groups. Protein expression of GLUT-4 in the skeletal muscle increased by exercise, but not by CR. Our findings indicate that the combination of exercise and CR may be effective in enhancing insulin sensitivity at the skeletal muscle in normal subjects.

Key words

insulin action - euglycemic clamp method - calorie restriction - exercise - glucose transporter

References

  • 1 Bantle JP, Wylie-Rosett J, Albright AL, Apovian CM, Clark NG, Franz MJ, Hoogwerf BJ, Lichtenstein AH, Mayer-Davis E, Mooradian AD, Wheeler ML. Nutrition recommendations and interventions for diabetes: a position statement of the American Diabetes Association.  Diabetes Care. 2008;  31 61-78
    Google Scholar
  • 2 Sigal RJ, Kenny GP, Wasserman DH, Castaneda-Sceppa C. Physical activity/exercise and type 2 diabetes.  Diabetes Care. 2004;  27 2518-2539
    Google Scholar
  • 3 Yazaki Y, Kadowaki T. Combating diabetes and obesity in Japan.  Nat Med. 2006;  12 73-74
    Google Scholar
  • 4 Chan JC, Malik V, Jia W, Kadowaki T, Yajnik CS, Yoon KH, Hu FB. Diabetes in Asia: Epidemiology, Risk Factors, and Pathophysiology.  JAMA. 2009;  301 2129-2140
    Google Scholar
  • 5 Weindruch R, Sohal RS. Seminars in medicine of the Beth Israel Deaconess Medical Center. Caloric intake and aging.  N Engl J Med. 1997;  337 986-994
    Google Scholar
  • 6 Mattison JA, Lane MA, Roth GS, Ingram DK. Calorie restriction in rhesus monkeys.  Exp Gerontol. 2003;  38 35-46
    Google Scholar
  • 7 Colman RJ, Anderson RM, Johnson SC, Kastman EK, Kosmatka KJ, Beasley TM, Allison DB, Cruzen C, Simmons HA, Kemnitz JW, Weindruch R. Caloric restriction delays disease onset and mortality in rhesus monkeys.  Science. 2009;  325 201-204
    Google Scholar
  • 8 Heilbronn LK, de Jonge L, Frisard MI, DeLany JP, Larson-Meyer DE, Rood J, Nguyen T, Martin CK, Volaufova J, Most MM, Greenway FL, Smith SR, Deutsch WA, Williamson DA, Ravussin E. Pennington CALERIE Team. Effect of 6-month calorie restriction on biomarkers of longevity, metabolic adaptation, and oxidative stress in overweight individuals: a randomized controlled trial.  JAMA. 2006;  295 1539-1548
    Google Scholar
  • 9 Varady KA, Hellerstein MK. Do calorie restriction or alternate-day fasting regimens modulate adipose tissue physiology in a way that reduces chronic disease risk?.  Nutrition reviews. 2008;  66 333-342
    Google Scholar
  • 10 Oshida Y, Tachi Y, Morishita Y, Kitakoshi K, Fuku N, Han YQ, Ohsawa I, Sato Y. Nitric oxide decreases insulin resistance induced by high-fructose feeding.  Horm Metab Res. 2000;  32 339-342
    Google Scholar
  • 11 Viana AY, Oshida Y, Han YQ, Koshinaka K, Sato Y. Effects of imidapril, an angiotensin-converting enzyme inhibitor, on insulin sensitivity and responsiveness in streptozotocin-induced diabetic rats.  Horm Metab Res. 2004;  36 34-38
    Google Scholar
  • 12 Li P, Koike T, Qin B, Kubota M, Kawata Y, Jia YJ, Oshida Y. A high-fructose diet impairs Akt and PKCzeta phosphorylation and GLUT4 translocation in rat skeletal muscle.  Horm Metab Res. 2008;  40 528-532
    Google Scholar
  • 13 Qin B, Nagasaki M, Ren M, Bajotto G, Oshida Y, Sato Y. Cinnamon extract prevents the insulin resistance induced by a high-fructose diet.  Horm Metab Res. 2004;  36 119-125
    Google Scholar
  • 14 Kubota M, Koshinaka K, Kawata Y, Koike T, Oshida Y. Effects of continuous low-carbohydrate diet after long-term exercise on GLUT-4 protein content in rat skeletal muscle.  Horm Metab Res. 2008;  40 24-28
    Google Scholar
  • 15 Fontana L, Klein S. Aging, adiposity, and calorie restriction.  JAMA. 2007;  297 986-994
    Google Scholar
  • 16 Larson-Meyer DE, Heilbronn LK, Redman LM, Newcomer BR, Frisard MI, Anton S, Smith SR, Alfonso A, Ravussin E. Effect of calorie restriction with or without exercise on insulin sensitivity, beta-cell function, fat cell size, and ectopic lipid in overweight subjects.  Diabetes Care. 2006;  29 1337-1344
    Google Scholar
  • 17 Ross R, Dagnone D, Jones PJ, Smith H, Paddags A, Hudson R, Janssen I. Reduction in obesity and related comorbid conditions after diet-induced weight loss or exercise-induced weight loss in men: a randomized, controlled trial.  Ann Intern Med. 2000;  133 92-103
    Google Scholar
  • 18 Rice B, Janssen I, Hudson R, Ross R. Effects of exercise and/or diet on insulin, glucose, and abdominal adipose tissue in obese men.  Diabetes Care. 1999;  22 684-691
    Google Scholar
  • 19 Cox KL, Burke V, Morton AR, Beilin LJ, Puddey IB. Independent and additive effects of energy restriction and exercise on glucose and insulin concentrations in sedentary overweight men.  Am J Clin Nutr. 2004;  80 308-316
    Google Scholar
  • 20 Janssen I, Fortier A, Hudson R, Ross R. Effects of an energy-restrictive diet with or without exercise on abdominal fat, intermuscular fat, and metabolic risk factors in obese women.  Diabetes Care. 2002;  25 431-438
    Google Scholar
  • 21 Goodpaster BH, Katsiaras A, Kelley DE. Enhanced fat oxidation through physical activity is associated with improvements in insulin sensitivity in obesity.  Diabetes.. 2003;  52 2191-2197
    Google Scholar
  • 22 DeFronzo RA, Bonadonna RC, Ferrannini E. Pathogenesis of NIDDM. A balanced overview.  Diabetes Care. 1992;  15 318-368
    Google Scholar
  • 23 DeFronzo RA, Jacot E, Jequier E, Maeder E, Wahren J, Felber JP. The effect of insulin on the disposal of intravenous glucose. Results from indirect calorimetry and hepatic and femoral venous catheterization.  Diabetes. 1981;  30 1000-1007
    Google Scholar
  • 24 Kirwan JP, Solomon TP, Wojta DM, Staten MA, Holloszy JO. Effects of 7 days of exercise training on insulin sensitivity and responsiveness in type 2 diabetes mellitus.  Am J Physiol Endocrinol Metab. 2009;  297 151-156
    Google Scholar
  • 25 Redman LM, Heilbronn LK, Martin CK, Alfonso A, Smith SR, Ravussin E. Effect of calorie restriction with or without exercise on body composition and fat distribution.  J Clin Endocrinol Metab. 2007;  92 865-872
    Google Scholar
  • 26 Simpson KA, Singh MA. Effects of exercise on adiponectin: a systematic review.  Obesity. 2008;  16 241-256
    Google Scholar
  • 27 Yamauchi T, Kamon J, Waki H, Terauchi Y, Kubota N, Hara K, Mori Y, Ide T, Murakami K, Tsuboyama-Kasaoka N, Ezaki O, Akanuma Y, Gavrilova O, Vinson C, Reitman ML, Kagechika H, Shudo K, Yoda M, Nakano Y, Tobe K, Nagai R, Kimura S, Tomita M, Froguel P, Kadowaki T. The fat-derived hormone adiponectin reverses insulin resistance associated with both lipoatrophy and obesity.  Nature Medicine. 2001;  7 941-946
    Google Scholar
  • 28 Pajvani UB, Hawkins M, Combs TP, Rajala MW, Doebber T, Berger JP, Wagner JA, Wu M, Knopps A, Xiang AH, Utzschneider KM, Kahn SE, Olefsky JM, Buchanan TA, Scherer PE. Complex distribution, not absolute amount of adiponectin correlates with thiazolinedione-mediated improvement in insulin sensitivity.  J Biol Chem. 2004;  279 12152-12162
    Google Scholar
  • 29 Shinmura K, Tamaki K, Saito K, Nakano Y, Tobe T, Bolli R. Cardioprotective effects of short-term caloric restriction are mediated by adiponectin via activation of AMP-activated protein kinase.  Circulation. 2007;  116 2809-2817
    Google Scholar
  • 30 Whitehead JP, Richards AA, Hickman IJ, Macdonald GA, Prins JB. Adiponectin-a key adipokine in the metabolic syndrome.  Diabetes, Obes Metab. 2006;  8 264-280
    Google Scholar
  • 31 Davidson RT, Arias EB, Cartee GD. Calorie restriction increases muscle insulin action but not IRS-1-, IRS-2-, or phosphotyrosine-PI 3-kinase.  Am J Physiol Endocrinol Metab. 2002;  282 270-276
    Google Scholar
  • 32 Dean DJ, Brozinick Jr JT, Cushman SW, Cartee GD. Calorie restriction increases cell surface GLUT-4 in insulin-stimulated skeletal muscle.  Am J Physiol. 1998;  275 957-964
    Google Scholar
  • 33 Argentino DP, Muñoz MC, Rocha JS, Bartke A, Turyn D, Dominici FP. Short-term calorie restriction does not modify the in vivo insulin signaling pathway leading to Akt activation in skeletal muscle of Ames Dwarf (Prop1df/Prop1df) mice.  Horm Metab Res. 2005;  37 672-679
    Google Scholar
  • 34 Park S, Komatsu T, Hayashi H, Yamaza H, Chiba T, Higami Y, Kuramoto K, Shimokawa I. Calorie restriction initiated at middle age improved glucose tolerance without affecting age-related impairments of insulin signaling in rat skeletal muscle.  Experimental Gerontology. 2006;  41 837-845
    Google Scholar
  • 35 Etgen Jr GJ, Brozinick Jr JT, Kang HY, Ivy JL. Effects of exercise training on skeletal muscle glucose uptake and transport.  Am J Physiol. 1993;  264 727-733
    Google Scholar

Correspondence

Y. OshidaMD, PhD 

Department of Sports Medicine

Graduate School of Medicine

Nagoya University

Nagoya 464-8601

Japan

Phone: +81/52/789 3961

Fax: +81/52/789 3957

Email: oshida@htc.nagoya-u.ac.jp