Effects of Aerobic Training and Caloric Restriction on Intramuscular Lipid, Lipid Profile and Insulin Resistance after 18 Weeks High Fat Diet in Male Rat

Document Type : Research Paper

Authors

Department of Exercise Physiology, Faculty of Physical Education and Sport Sciences, University of Guilan, Rasht, Iran

Abstract

Background&Purpose: Physical inactivity is associated with dysregulation of intramuscular triglyceride (IMTG) metabolism leading to the accumulation of fatty acid metabolites and insulin resistance. The purpose of this study was to evaluate the effects of aerobic training and caloric restriction on intramuscular lipid metabolism, lipid profile and insulin resistance after 18 weeks high fat diet in male rat
Methodology: Study sample were consisted of forty eight Wistar male rats with average weight; 194.5±12.6 g. Blood and muscle samples were collected at, 18th and 28th weeks after an overnight fasting. After weight rats in first week, rats consume high-fat-diet. After 18 weeks High-fat-diet group randomly divided into control (C), calorie restriction (CR) and aerobic training (T) groups. Negative energy balance groups underwent an aerobic training (running) with intensity of 70 to 75% of VO2max, and %25 calorie restriction for 10 weeks. Adipose Triglyceride Lipase, Triacylglycerol (TAG) and diacylglycerol (DAG) Levels in soleus, insulin and glucose levels and lipid profile were measured. HOMA-IR was also calculated.
Results: The results of this study indicated that negative energy balance methods, decreased muscle DAG levels and serum concentrations of insulin, glucose, triacylglycerol and insulin resistance index in obese male rats (P≤0.05). Serum triacylglycerol and cholesterol levels decreased only in T group (P≤0.05).
Conclusion: This study indicated that negative energy balance methods can actually decrease TAG and DAG levels even with simultaneous consumption of high-fat-diet which is largely congruent with improvement in insulin resistance.

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##Broch-Johnsen K. 2007. The metabolic syndrome in a global perspective. The public health impact-secondary publication. Dan Med Bull. 2:165-176.##Muoio DM, Newgard CB. 2008. Mechanisms of disease: molecular and metabolic mechanisms of insulin resistance and beta-cell failure in type 2 diabetes. Nat Rev Mol Cell Biol. 9:193-205.##DeFronzo RA, Jacot E, Jequier E, Maeder E, Wahren J, Felber JP. 1981. The effect of insulin on the disposal of intravenous glucose. Results from indirect calorimetry and hepatic and femoral venous catheterization. Diabetes. 30:1000-1007.##Cartee GD. 2008. Exercise and calorie restriction use different mechanisms to improve insulin sensitivity. In: Hawley JA and Zierath JR, ed. Physical Activity and Type 2 Diabetes. Champaign, IL: Human Kinetics. 119-134.## Jornayvaz FR, Shulman GI. 2012. Diacylglycerol activation of protein kinase Cε and hepatic insulin resistance, Cell Metab. 15:574–584.##Coen PM, Dubé JJ, Amati F, Stefanovic-Racic M, Ferrell RE, Toledo FG, Goodpaster BH. 2010. Insulin resistance is associated with higher intramyocellular triglycerides in type I but not type II myocytes concomitant with higher ceramide content. Diabetes. 59: 80-88.##Skovbro M, Baranowski M, Skov-Jensen C, Flint A, Dela F, Gorski J & Helge JW. 2008. Human skeletal muscle ceramide content is not a major factor in muscle insulin sensitivity. Diabetologia. 51:1253-1260.##Hoeg LD, Sjoberg KA, Jeppesen J, Jensen TE, Frosig C, Birk JB, Bisiani B, Hiscock N, Pilegaard H, Wojtaszewski JF, Richter EA, Kiens B. 2011. Lipid-induced insulin resistance affects women less than men and is not accompanied by inflammation or impaired proximal insulin signaling. Diabetes. 60:64-73.##Frosig C, Rose AJ, Treebak JT, Kiens B, Richter EA & Wojtaszewski JF. 2007. Effects of endurance exercise training on insulin signaling in human skeletal muscle: interactions at the level of phosphatidylinositol 3-kinase, Akt, and AS160. Diabetes. 56:2093-2102.## Griffin ME, Marcucci MJ, Cline GW, Bell K, Barucci N, Lee D, Goodyear LJ, Kraegen EW, White MF, and Shulman GI. 1999. Free fatty acid-induced insulin resistance is associated with activation of protein kinase C theta and alterations in the insulin signaling cascade. Diabetes. 48:1270-1274.##Alsted TJ, Nybo L, Schweiger M, et al. 2009. Adipose triglyceride lipase in human skeletal muscle is upregulated by exercise training.  Am J Physiol Endocrinol Metab. 296:445-453.##Kershaw EE, Hamm JK, Verhagen LA, et al. 2006. Adipose triglyceride lipase: function, regulation by insulin, and comparison with adiponutrin. Diabetes. 55:148-57.## Watt MJ, van Denderen BJ, Castelli LA, et al. 2008. Adipose triglyceride lipase regulation of skeletal muscle lipid metabolism and insulin responsiveness. Mol Endocrinol. 22:1200-12.## Zimmermann R, Strauss JG, Haemmerle G, et al. 2004. Fat mobilization in adipose tissue is promoted by adipose triglyceride lipase. Science. 306:1383-6.##Nicklas BJ, Wang X, You T, Lyles MF, Demons J, et al. 2009. Effect of exercise intensity on abdominal fat loss during calorie restriction in overweight and obese postmenopausal women: a randomized, controlled trial. Am J Clin Nutr. 89:1043-1052.##Argentino DP, Dominici FP, Al-Regaiey K, Bonkowski MS, Bartke A, and Turyn D. 2005. Effects of long-term caloric restriction on early steps of the insulin-signaling system in mouse skeletal muscle. J Gerontol A Biol Sci Med Sci. 60:28-34.##Argentino DP, Munoz MC, Rocha JS, Bartke A, Turyn D, and Dominici FP. 2005. Short-term caloric restriction does not modify the in vivo insulin signaling pathway leading to Akt activation in skeletal muscle of Ames dwarf (Prop1(df)/Prop1(df)) mice. Horm Metab Res. 37:672-9.##Sharma N, Arias EB, Bhat AD, Sequea DA, Ho S, Croff KK, et al. 2011. Mechanisms for increased insulin-stimulated Akt phosphorylation and glucose uptake in fast- and slow-twitch skeletal muscles of calorie-restricted rats. American journal of physiology Endocrinology and metabolism. 300:966-978.##Balage M, Grizard J, Manin M. 1990. Effect of calorie restriction on skeletal muscle and liver insulin binding in growing rat. Horm Metab Res. 22:207-214.##Garekani ET, Mohebbi H, Kraemer RR, and Fathi R. 2011. Exercise training intensity/volume affects plasma and tissue adiponectin concentrations in the male rat. Peptides. 32:1008-12.## Paulino EC, Ferreira JCB, Bechara LR, Tsutsui JM, Mathias W, Lima FB. 2010. Exercise training and caloric restriction prevent reduction in cardiac Ca2+-handling protein profile in obese rats. Hypertension. 56:629-35.##Friedewald WT, Levy RI, and Fredrickson DS. 1972. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clinical chemistry. 18:499-502.##Timmers S, de Vogel-van den Bosch J, Hesselink MK, van Beurden D, Schaart G, Ferraz MJ, Losen M, Martinez-Martinez P, De Baets MH, Aerts JM, Schrauwen P. 2011. Paradoxical increase in TAG and DAG content parallel the insulin sensitizing effect of unilateral DGAT1 overexpression in rat skeletal muscle. PLoS One. 6:14503.##Schwartz DM, Wolins NE.2007. A simple and rapid method to assay triacylglycerol in cells and tissues, J Lipid Res. 48:2514-20.##Murphy JC, McDaniel JL, Mora K, Villareal DT, Fontana L, et al. 2012. Preferential reductions in intermuscular and visceral adipose tissue with exercise-induced weight loss compared with calorie restriction. J Appl Physiol. 112:79-85.##Samjoo IA, Safdar A, Hamadeh MJ, Raha S, Tarnopolsky MA. 2013. The effect of endurance exercise on both skeletal muscle and systemic oxidative stress in previously sedentary obese men. Nutr Diabetes. 3:88.##Johnson NA, Sachinwalla T, Walton DW, Smith K, Armstrong A, et al. 2009. Aerobic exercise training reduces hepatic and visceral lipids in obese individuals without weight loss. Hepatology. 50:1105–1112.##Burneiko RC, Diniz YS, Galhardi CM, Rodrigues HG, Ebaid GM, Faine LA. 2006. Interaction of hypercaloric diet and physical exercise on lipid profile, oxidative stress and antioxidant defenses. Food and chemical toxicology. 44: 1167-72.##Christiansen T, Paulsen SK, Bruun JM, Ploug T, Pedersen SB, and Richelsen B. 2010. Diet-induced weight loss and exercise alone and in combination enhance the expression of adiponectin receptors in adipose tissue and skeletal muscle, but only diet-induced weight loss enhanced circulating adiponectin. J Clinical Endocri Metabo, 95:911-9.##O'Leary V.B, Jorett A.E, Marchetti C.M, Gonzalez F, Phillips S.A, Ciaraldi T.P, et al. 2007. Enhanced adiponectin multimer ratio and skeletal muscle adiponectin receptor expression following exercise training and diet in older insulin-resistant adults. American journal of physiology Endocrinology and metabolism. 293: 421-7.## Sharma N, Arias EB, Bhat AD, Sequea DA, Ho S, Croff KK, Sajan MP, Farese RV, Cartee GD. 2011. Mechanisms for increased insulin-stimulated Akt phosphorylation and glucose uptake in fast- and slow-twitch skeletal muscles of calorie-restricted rats. Am J Physiol Endocrinol Metab. 300:966-978.##Richter EA, Hargreaves M. 2013. Exercise, GLUT4, and skeletal muscle glucose uptake. Physiol Rev. 93:993-1017.##Rogério AL, Paulino EC, Brum PC, Andreotti S, Lima FB, Negrão CE. 2015. Exercise training and caloric restriction reduce adiposity index and hepatic lipids in obese rats, Immunoendocrinology. 2:1053.##Randle PJ, et al. 1963. The glucose fatty-acid cycle. Its role in insulin sensitivity and the metabolic disturbances of diabetes mellitus. Lancet. 1:785-9.## Irrcher I, Adhihetty PJ, Joseph AM, Ljubicic V, Hood DA. 2003. Regulation of mitochondrial bio-genesis in muscle by endurance exercise. Sports Med. 33:783-793.##Bruce, CR, Brolin C, Turner N, Cleasby ME, Van der Leij FR, Cooney GJ, Kraegen EW. 2006. Overex-pression of carnitine palmitoyltransferase I in skeletal muscle in vivo increases fatty acid oxidation and reduces triacyl-glycerol esterification. Am J Physiol Endocrinol Metab. 292:1231-1237.##Goodpaster BH, Wolfe RR, Kelley DE. 2002. Effects of obesity on substrate utilization during exercise. Obes Res. 10:575-584.##Venkatesh G, Navin M, Seigo I, Swee SL, Adonsia YY et al. 2016. Effect of Exercise and Calorie Restriction on Tissue. Acylcarnitines, Tissue Desaturase Indices, and Fat Accumulation in Diet-Induced Obese Rats, Scientific Reports. 6:26445.## Itani SI, Ruderman NB, Schmieder F & Boden G. 2002. Lipid-induced insulin resistance in human muscle is associated with changes in diacylglycerol, protein kinase C, and IkappaB-alpha. Diabetes. 51:2005-2011.##Badin PM, Louche K, Mairal A, Liebisch G, Schmitz G, Rustan AC, Smith SR, Langin D & Moro C. (2011). Altered  skeletal  muscle  lipase  expression  and  activity  contribute  to  insulin  resistance  in humans. Diabetes 60, 1734-1742.##