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Metabolic reprogramming involving glycolysis in the hibernating brown bear skeletal muscle

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...

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Autores principales: Chazarin, Blandine, Storey, Kenneth B., Ziemianin, Anna, Chanon, Stéphanie, Plumel, Marine, Chery, Isabelle, Durand, Christine, Evans, Alina L., Arnemo, Jon M., Zedrosser, Andreas, Swenson, Jon E., Gauquelin-Koch, Guillemette, Simon, Chantal, Blanc, Stephane, Lefai, Etienne, Bertile, Fabrice
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6503430/
https://www.ncbi.nlm.nih.gov/pubmed/31080489
http://dx.doi.org/10.1186/s12983-019-0312-2
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author Chazarin, Blandine
Storey, Kenneth B.
Ziemianin, Anna
Chanon, Stéphanie
Plumel, Marine
Chery, Isabelle
Durand, Christine
Evans, Alina L.
Arnemo, Jon M.
Zedrosser, Andreas
Swenson, Jon E.
Gauquelin-Koch, Guillemette
Simon, Chantal
Blanc, Stephane
Lefai, Etienne
Bertile, Fabrice
author_facet Chazarin, Blandine
Storey, Kenneth B.
Ziemianin, Anna
Chanon, Stéphanie
Plumel, Marine
Chery, Isabelle
Durand, Christine
Evans, Alina L.
Arnemo, Jon M.
Zedrosser, Andreas
Swenson, Jon E.
Gauquelin-Koch, Guillemette
Simon, Chantal
Blanc, Stephane
Lefai, Etienne
Bertile, Fabrice
author_sort Chazarin, Blandine
collection PubMed
description 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. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12983-019-0312-2) contains supplementary material, which is available to authorized users.
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spelling pubmed-65034302019-05-10 Metabolic reprogramming involving glycolysis in the hibernating brown bear skeletal muscle Chazarin, Blandine Storey, Kenneth B. Ziemianin, Anna Chanon, Stéphanie Plumel, Marine Chery, Isabelle Durand, Christine Evans, Alina L. Arnemo, Jon M. Zedrosser, Andreas Swenson, Jon E. Gauquelin-Koch, Guillemette Simon, Chantal Blanc, Stephane Lefai, Etienne Bertile, Fabrice Front Zool Research 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. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12983-019-0312-2) contains supplementary material, which is available to authorized users. BioMed Central 2019-05-06 /pmc/articles/PMC6503430/ /pubmed/31080489 http://dx.doi.org/10.1186/s12983-019-0312-2 Text en © The Author(s). 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Chazarin, Blandine
Storey, Kenneth B.
Ziemianin, Anna
Chanon, Stéphanie
Plumel, Marine
Chery, Isabelle
Durand, Christine
Evans, Alina L.
Arnemo, Jon M.
Zedrosser, Andreas
Swenson, Jon E.
Gauquelin-Koch, Guillemette
Simon, Chantal
Blanc, Stephane
Lefai, Etienne
Bertile, Fabrice
Metabolic reprogramming involving glycolysis in the hibernating brown bear skeletal muscle
title Metabolic reprogramming involving glycolysis in the hibernating brown bear skeletal muscle
title_full Metabolic reprogramming involving glycolysis in the hibernating brown bear skeletal muscle
title_fullStr Metabolic reprogramming involving glycolysis in the hibernating brown bear skeletal muscle
title_full_unstemmed Metabolic reprogramming involving glycolysis in the hibernating brown bear skeletal muscle
title_short Metabolic reprogramming involving glycolysis in the hibernating brown bear skeletal muscle
title_sort metabolic reprogramming involving glycolysis in the hibernating brown bear skeletal muscle
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6503430/
https://www.ncbi.nlm.nih.gov/pubmed/31080489
http://dx.doi.org/10.1186/s12983-019-0312-2
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