Abstract
BackgroundIn mammals, the hibernating state is characterized by biochemical adjustments, which include metabolic rate depression and a shift in the primary fuel oxidized from carbohydrates to lipids. A number of studies of hibernating species report an upregulation of the levels and/or activity of lipid oxidizing enzymes in muscles during torpor, with a concomitant downregulation for glycolytic enzymes. However, other studies provide contrasting data about the regulation of fuel utilization in skeletal muscles during hibernation. Bears hibernate with only moderate hypothermia but with a drop in metabolic rate down to ~ 25% of basal metabolism. To gain insights into how fuel metabolism is regulated in hibernating bear skeletal muscles, we examined the vastus lateralis proteome and other changes elicited in brown bears during hibernation.ResultsWe show that bear muscle metabolic reorganization is in line with a suppression of ATP turnover. Regulation of muscle enzyme expression and activity, as well as of circulating metabolite profiles, highlighted a preference for lipid substrates during hibernation, although the data suggested that muscular lipid oxidation levels decreased due to metabolic rate depression. Our data also supported maintenance of muscle glycolysis that could be fuelled from liver gluconeogenesis and mobilization of muscle glycogen stores. During hibernation, our data also suggest that carbohydrate metabolism in bear muscle, as well as protein sparing, could be controlled, in part, by actions of n-3 polyunsaturated fatty acids like docosahexaenoic acid.ConclusionsOur work shows that molecular mechanisms in hibernating bear skeletal muscle, which appear consistent with a hypometabolic state, likely contribute to energy and protein savings. Maintenance of glycolysis could help to sustain muscle functionality for situations such as an unexpected exit from hibernation that would require a rapid increase in ATP production for muscle contraction. The molecular data we report here for skeletal muscles of bears hibernating at near normal body temperature represent a signature of muscle preservation despite atrophying conditions.
Highlights
In mammals, the hibernating state is characterized by biochemical adjustments, which include metabolic rate depression and a shift in the primary fuel oxidized from carbohydrates to lipids
Bear muscle proteome is dramatically changed during hibernation From label-free quantitative proteomics data (XIC), statistical analysis highlighted significant seasonal effects in the abundance of 146 muscle proteins, 67 of them being decreased and 79 increased in hibernating versus active bears (Fig. 1a, see Additional file 1: Table S1)
From a merged list of differentially-expressed proteins coming from the two proteomics approaches, functional annotation analysis revealed that differences between hibernating and active bears involved mostly proteins known to play roles in muscle metabolism in a broad sense and in structural remodelling (Fig. 1c)
Summary
The hibernating state is characterized by biochemical adjustments, which include metabolic rate depression and a shift in the primary fuel oxidized from carbohydrates to lipids. To save energy during the prolonged period of winter fasting, hibernators rely essentially on decreased metabolic rates over extended periods of deep torpor characterized by physical inactivity, reductions of heart and breathing rates and decreased body temperature [1]. Within this framework, the hibernation of bears represents an extreme phenotype that can last for up to 6-7 months [4] during which inactive animals do not eat, drink, urinate, defecate, or exhibit arousal episodes [5, 6]. The molecular mechanisms that are involved in organ/tissue metabolic adjustments have not yet been fully elucidated
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