Caloric Restriction Followed by High Fat Feeding Predisposes to Oxidative Stress in Skeletal Muscle Mitochondria

Abstract

The purpose of the present study was to assess the impact of previous period of caloric restriction on energy balance and skeletal muscle mitochondrial energetics in response to high-fat (HF) diet. To this end, 1 group of rats was subjected to 2 weeks of caloric restriction with nonpurified diet and then fed HF diet (430 kJ metabolizable energy/day) for 1 week, while the second group was fed ad libitum with nonpurified diet for 2 weeks and then fed HF diet (430 kJ metabolizable energy/day) for 1 week. Body composition, energy balance, and glucose homeostasis were measured. Mitochondrial mass, oxidative capacity and efficiency, parameters of oxidative stress, and antioxidant defense were evaluated in subsarcolemmal and intermyofibrillar mitochondria from skeletal muscle. Body energy and lipid content, plasma insulin, and metabolic efficiency were significantly higher, while energy expenditure significantly decreased, in food-restricted rats fed HF diet compared to controls. Mitochondrial efficiency and oxidative damage in skeletal muscle were significantly increased, while antioxidant defence was significantly lower in food-restricted rats fed HF diet, compared with controls. Finally, food-restricted rats fed HF diet exhibited significant reduction in subsarcolemmal mitochondrial mass. In conclusion, caloric restriction elicits higher mitochondrial efficiency and predisposes skeletal muscle to high fat-induced oxidative damage, which in turn could lead to impaired glucose homeostasis in food-restricted rats fed HF diet.

Key words

caloric restriction - mitochondria - high fat diet

• References

• 1 Lionetti L, Mollica MP, Crescenzo R, D’Andrea E, Ferraro M, Bianco F, Liverini G, Iossa S. Skeletal muscle subsarcolemmal mitochondrial dysfunction in high-fat fed rats exhibiting impaired glucose homeostasis. Int J Obes 2007; 31: 1596-1604
• 2 Iossa S, Lionetti L, Mollica MP, Crescenzo R, Botta M, Barletta A, Liverini G. Effect of high-fat feeding on metabolic efficiency and mitochondrial oxidative capacity in adult rats. Br J Nutr 2003; 90: 953-960
• 3 Dulloo AG, Jacquet J, Montani JP. Pathways from weight fluctuations to metabolic diseases: focus on maladaptive thermogenesis during catch-up fat. Int J Obes 2002; 26: S46-S47
• 4 Dulloo AG. Thrifty energy metabolism in catch-up growth trajectories to insulin and leptin resistance. Best Pract Res Clin Endocrinol Metab 2008; 22: 155-171
• 5 Dulloo AG, Girardier L. Influence of dietary composition on energy expenditure during recovery of body weight in the rat: implications for catch-up growth and obesity relapse. Metabolism 1992; 41: 1336-1342
• 6 Crescenzo R, Samec S, Antic V, Rohner-Jeanrenaud F, Seydoux J, Montani JP, Dulloo AG. A role for suppressed thermogenesis favoring catch-up fat in the pathophysiology of catch-up growth. Diabetes 2003; 52: 1090-1097
• 7 Rolfe DFS, Brown GC. Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol Rev 1997; 77: 731-758
• 8 Dulloo AG. A role per suppressed skeletal muscle thermogenesis in pathways from weight fluctuations to the insulin resistance syndrome. Acta Physiol Scand 2005; 184: 295-307
• 9 Crescenzo R, Lionetti L, Mollica MP, Ferraro M, D’Andrea E, Mainieri D, Dulloo AG, Liverini G, Iossa S. Altered skeletal muscle subsarcolemmal mitochondrial compartment during catch-up fat after caloric restriction. Diabetes 2006; 55: 2286-2293
• 10 Cogswell AM, Stevens RJ, Hood DA. Properties of skeletal muscle mitochondria isolated from subsarcolemmal and intermyofibrillar regions. Am J Physiol 1993; 264: C383-C389
• 11 Mollica MP, Lionetti L, Crescenzo R, D’Andrea E, Ferraro M, Liverini G, Iossa S. Heterogeneous bioenergetic behaviour of subsarcolemmal and intermyofibrillar mitochondria in fed and fasted rats. Cell Mol Life Sci 2006; 63: 358-366
• 12 Folch J, Lees M, Stanley GHS. A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 1957; 226: 497-510
• 13 Armsby HP. The Nutrition of Farm animals. New York: The Macmillan Company; 1917
• 14 Iossa S, Mollica MP, Lionetti L, Crescenzo R, Botta M, Liverini G. Skeletal muscle oxidative capacity in rats fed high-fat diet. Int J Obes 2002; 26: 65-72
• 15 Iossa S, Mollica M, Lionetti L, Crescenzo R, Botta M, Samec S, Solinas G, Mainieri D, Dulloo AG, Liverini G. Skeletal muscle mitochondrial efficiency and uncoupling protein 3 in overeating rats with increased thermogenesis. Pflug Arch 2002; 445: 431-436
• 16 Srere PA. Citrate synthase. Meth Enzymol 1969; 13: 3-5
• 17 Fernandes MA, Custodio JBA, Santos MS, Moreno AJ, Vicente JA. Tetrandrine concentrations not affecting oxidative phosphorylation protect rat liver mitochondria from oxidative stress. Mitochondrion 2006; 6: 176-185
• 18 Gardner PR. Aconitase: sensitive target and measure of superoxide. Meth Enzymol 2002; 349: 9-16
• 19 Hausladen A, Fridovich I. Measuring nitric oxide and superoxide: rate constants for aconitase reactivity. Meth Enzymol 1996; 269: 7-41
• 20 Flohè L, Otting F. Superoxide Dismutase Assay. Meth Enzymol 1984; 105: 93-104
• 21 Cacho J, Sevillano J, de Castro J, Herrera E, Ramos MP. Validation of simple indexes to assess insulin sensitivity during pregnancy in Wistar and Sprague-Dawley rats. Am J Physiol 2008; 295: E1269-E1276
• 22 Crescenzo R, Bianco F, Falcone I, Coppola P, Dulloo AG, Liverini G, Iossa S. Mitochondrial energetics in liver and skeletal musce after caloric restriction in young rats. Br J Nutr 2012; 108: 655-665
• 23 Korshunov SS, Skulachev VP, Starkov AA. High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett 1997; 416: 15-18
• 24 Mailloux RJ, Harper ME. Uncoupling proteins and the control of mitochondrial reactive oxygen species production. Free Radic Biol Med 2011; 51: 1106-1115
• 25 Papa S, Skulachev VP. Reactive oxygen species, mitochondria, apoptosis and aging. Mol Cell Biochem 1997; 174: 305-319
• 26 Boden MJ, Brandon AE, Tid-Ang JD, Preston E, Wilks D, Stuart E, Cleasby ME, Turner N, Cooney GJ, Kraegen EW. Overexpression of manganese superoxide dismutase ameliorates high – fat diet-induced insulin resistance in rat skeletal muscle. Am J Physiol Endocrinol Metab 2012; 303: E798-E805
• 27 Gredilla R, Barya G. The role of oxidative stress in relation to caloric restriction and longevity. Endocrinol 2005; 156: 3713-3717
• 28 Mohn A, Catino M, Capanna R, Giannini C, Marcovecchio M, Chiarelli F. Increased oxidative stress in prepubertal severely obese children: effect of a dietary restriction-weight loss program. J Clin Endocrinol Metab 2005; 90: 2653-2658