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Induction of muscle thermogenesis by high-fat diet in mice: association with obesity-resistance

Vladimir Kus,¹ Tomas Prazak,¹ Petr Brauner,¹ Michal Hensler,¹ Ondrej Kuda,¹ Pavel Flachs,¹ Petra Janovska,¹ Dasa Medrikova,¹ Martin Rossmeisl,¹ Zuzana Jilkova,¹ Bohumir Stefl,^4, Eva Pastalkova,³ Zdenek Drahota,² Josef Houstek,² and Jan Kopecky¹

Departments of ¹Adipose Tissue Biology, ²Bioenergetics, and ³Neurophysiology of Memory and Computational Neuroscience, Institute of Physiology, Academy of Sciences of the Czech Republic; and ⁴Department of Physiology and Developmental Biology, Faculty of Science, Charles University, Prague, Czech Republic

Submitted 27 February 2008 ; accepted in final form 20 May 2008

The obesogenic effect of a high-fat (HF) diet is counterbalanced by stimulation of energy expenditure and lipid oxidation in response to a meal. The aim of this study was to reveal whether muscle nonshivering thermogenesis could be stimulated by a HF diet, especially in obesity-resistant A/J compared with obesity-prone C57BL/6J (B/6J) mice. Experiments were performed on male mice born and maintained at 30°C. Four-week-old mice were randomly weaned onto a low-fat (LF) or HF diet for 2 wk. In the A/J LF mice, cold exposure (4°C) resulted in hypothermia, whereas the A/J HF, B/6J LF, and B/6J HF mice were cold tolerant. Cold sensitivity of the A/J LF mice was associated with a relatively low whole body energy expenditure under resting conditions, which was normalized by the HF diet. In both strains, the HF diet induced uncoupling protein-1-mediated thermogenesis, with a stronger induction in A/J mice. Only in A/J mice: 1) the HF diet augmented activation of whole body lipid oxidation by cold; and 2) at 30°C, oxygen consumption, total content, and phosphorylation of AMP-activated protein kinase (AMPK), and AICAR-stimulated palmitate oxidation in soleus muscle was increased by the HF diet in parallel with significantly increased leptinemia. Gene expression data in soleus muscle of the A/J HF mice indicated a shift from carbohydrate to fatty acid oxidation. Our results suggest a role for muscle nonshivering thermogenesis and lipid oxidation in the obesity-resistant phenotype of A/J mice and indicate that a HF diet could induce thermogenesis in oxidative muscle, possibly via the leptin-AMPK axis.

nonshivering thermogenesis; leptin; adenosine monophosphate-activated protein kinase

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