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Nutrient Physiology, Metabolism, and Nutrient-Nutrient Interactions

Diets High in Sugar, Fat, and Energy Induce Muscle Type–Specific Adaptations in Mitochondrial Functions in Rats^1,2

³ INRA, UMR1019, Clermont-Ferrand, F-63000, France; ⁴ University Clermont 1, UFR Médecine, UMR1019, Clermont-Ferrand, F-63000, France; ⁵ INRA, STIM Unit, Clermont-Ferrand, F-63000, France; ⁶ Inserm, E0221, Grenoble, F-38000, France; Joseph Fourier University, Grenoble, F-38000, France; and ⁷ CHU Clermont-Ferrand, Clermont-Ferrand, F-63000, France

^* To whom correspondence should be addressed. Email: morio{at}clermont.inra.fr.

Obesity is often associated with insulin resistance and mitochondrial dysfunction within skeletal muscles, but the causative factors are not clearly identified. The present study examined the role of nutrition, both qualitatively and quantitatively, in the induction of muscle mitochondrial defects. Two experimental diets [high sucrose (SU) and high fat (F)] were provided for 6 wk to male Wistar rats at 2 levels of energy [standard (N) and high (H)] and compared with a standard energy cornstarch-based diet (C). Insulin sensitivity (intraperitoneal glucose tolerance test, IPGTT) and intramyocellular triglyceride (IMTG) content (¹H MRS) were determined at wk 5. Mitochondrial oxidative phosphorylation and superoxide anion radical (MSR) production were assessed on soleus (oxidative) and tibialis (glycolytic) muscles. Experimental diets induced hyperinsulinemia during IPGTT (P < 0.01 vs. C). Rats in the HSU and HF groups were hyperglycemic relative to the C group, P < 0.05 vs. C. The severity of insulin resistance paralleled IMTG accumulation (P < 0.05). In soleus, mitochondrial respiration and ATP production rates were lower in HSU and HF than in C (P < 0.05). By contrast, respiration was unaffected by the diets in tibialis, whereas ATP production tended to be lower in rats fed the experimental diets compared with C (P = 0.09). Mitochondrial adaptations were associated with more than a 50% reduction in MSR production in HSU and HF compared with C in both soleus (P < 0.05) and tibialis (P < 0.01). Changes in mitochondrial functions in the NSU and NF groups were intermediate and not significantly different from C. Therefore, excess fat or sucrose and more importantly, excess energy intake by rats is associated with muscle type–specific mitochondrial adaptations, which contribute to decrease mitochondrial production of ATP and reactive oxygen species.

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