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Front Zool. 2019 May 6;16:12. doi: 10.1186/s12983-019-0312-2. eCollection 2019.

Metabolic reprogramming involving glycolysis in the hibernating brown bear skeletal muscle.

Author information

1
1Université de Strasbourg, CNRS, IPHC UMR 7178, F-67000 Strasbourg, France.
2
10Centre National d'Etudes Spatiales, CNES, F-75001 Paris, France.
3
2Department of Biology, Carleton University, Ottawa, ON K1S 5B6 Canada.
4
3CarMen Laboratory, INSERM 1060, INRA 1397, University of Lyon, F-69600 Oullins, France.
5
4Department of Forestry and Wildlife Management, Inland Norway University of Applied Sciences, Campus Evenstad, NO-2480 Koppang, Norway.
6
5Department of Wildlife, Fish, and Environmental Studies, Swedish University of Agricultural Sciences, SE-901 83 Umeå, Sweden.
7
6Department of Environmental and Health Studies, University College of Southeast Norway, N-3800 Bø, Telemark Norway.
8
7Institute of Wildlife Biology and Game Management, University of Natural Resources and Life Sciences, A-1180 Vienna, Austria.
9
8Faculty of Environmental Sciences and Natural Resource Management, Norwegian University of Life Sciences, NO-1432 Ås, Norway.
10
9Norwegian Institute for Nature Research, NO-7485 Trondheim, Norway.
11
Université d'Auvergne, INRA, UNH UMR1019, F-63122 Saint-Genès Champanelle, France.

Abstract

Background:

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. 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.

Results:

We 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.

Conclusions:

Our 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.

KEYWORDS:

Brown bears; Enzymology; Glycolysis; Hibernation; Lipid oxidation; Metabolism shift; Omics; Skeletal muscle

Conflict of interest statement

The study was approved by the Swedish Ethical Committee on Animal Experiment (applications #C212/9, #C47/9, #C7/12, #C268/12, and #C18/15), the Swedish Environmental Protection Agency (NV-0758-14), and the Swedish Board of Agriculture (31-11,102/12). All procedures complied with Swedish laws and regulations. Additionally, the samples obtained from captive bears had been collected after the animals had been euthanized, and were kindly provided by the Norwegian Veterinary Institute, and the Orsa Predator Park in Sweden (permit N° Dnr5.8.18-06068/2017).The authors declare no competing interests.Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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