Reduced ATP turnover during hibernation in relaxed skeletal muscle

Abstract Hibernating brown bears, due to a drastic reduction in metabolic rate, show only moderate muscle wasting. Here, we evaluate if ATPase activity of resting skeletal muscle myosin can contribute to this energy sparing. By analyzing single muscle fibers taken from the same bears, either during...

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Main Authors: Cosimo De Napoli, Luisa Schmidt, Mauro Montesel, Laura Cussonneau, Samuele Sanniti, Lorenzo Marcucci, Elena Germinario, Jonas Kindberg, Alina Lynn Evans, Guillemette Gauquelin-Koch, Marco Narici, Fabrice Bertile, Etienne Lefai, Marcus Krüger, Leonardo Nogara, Bert Blaauw
Format: Article
Language:English
Published: Nature Portfolio 2025-01-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-024-55565-4
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author Cosimo De Napoli
Luisa Schmidt
Mauro Montesel
Laura Cussonneau
Samuele Sanniti
Lorenzo Marcucci
Elena Germinario
Jonas Kindberg
Alina Lynn Evans
Guillemette Gauquelin-Koch
Marco Narici
Fabrice Bertile
Etienne Lefai
Marcus Krüger
Leonardo Nogara
Bert Blaauw
author_facet Cosimo De Napoli
Luisa Schmidt
Mauro Montesel
Laura Cussonneau
Samuele Sanniti
Lorenzo Marcucci
Elena Germinario
Jonas Kindberg
Alina Lynn Evans
Guillemette Gauquelin-Koch
Marco Narici
Fabrice Bertile
Etienne Lefai
Marcus Krüger
Leonardo Nogara
Bert Blaauw
author_sort Cosimo De Napoli
collection DOAJ
description Abstract Hibernating brown bears, due to a drastic reduction in metabolic rate, show only moderate muscle wasting. Here, we evaluate if ATPase activity of resting skeletal muscle myosin can contribute to this energy sparing. By analyzing single muscle fibers taken from the same bears, either during hibernation or in summer, we find that fibers from hibernating bears have a mild decline in force production and a significant reduction in ATPase activity. Single fiber proteomics, western blotting, and immunohistochemical analyses reveal major remodeling of the mitochondrial proteome during hibernation. Furthermore, using bioinformatical approaches and western blotting we find that phosphorylated myosin light chain, a known stimulator of basal myosin ATPase activity, is decreased in hibernating and disused muscles. These results suggest that skeletal muscle limits energy loss by reducing myosin ATPase activity, indicating a possible role for myosin ATPase activity modulation in multiple muscle wasting conditions.
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spelling doaj-art-29cd158edce54e0d8a65f14757656ee02025-01-05T12:39:06ZengNature PortfolioNature Communications2041-17232025-01-0116111410.1038/s41467-024-55565-4Reduced ATP turnover during hibernation in relaxed skeletal muscleCosimo De Napoli0Luisa Schmidt1Mauro Montesel2Laura Cussonneau3Samuele Sanniti4Lorenzo Marcucci5Elena Germinario6Jonas Kindberg7Alina Lynn Evans8Guillemette Gauquelin-Koch9Marco Narici10Fabrice Bertile11Etienne Lefai12Marcus Krüger13Leonardo Nogara14Bert Blaauw15Venetian Institute of Molecular Medicine (VIMM)Institute for Genetics, Cologne Excellence Cluster on Cellular Stress Responses in Aging‐Associated Diseases (CECAD), University of CologneVenetian Institute of Molecular Medicine (VIMM)Venetian Institute of Molecular Medicine (VIMM)Venetian Institute of Molecular Medicine (VIMM)Department of Biomedical Sciences, 35131, University of PadovaDepartment of Biomedical Sciences, 35131, University of PadovaNorwegian Institute for Nature ResearchDepartment of Forestry and Wildlife Management, Faculty of Applied Ecology and Biotechnology, Inland Norway University of Applied SciencesFrench Space Agency, Centre National d’Etudes Spatiales (CNES)Department of Biomedical Sciences, 35131, University of PadovaUniversité de Strasbourg, CNRS, IPHC UMR 7178Université Clermont Auvergne, INRAE, UNH UMR 1019, CRNH AuvergneInstitute for Genetics, Cologne Excellence Cluster on Cellular Stress Responses in Aging‐Associated Diseases (CECAD), University of CologneVenetian Institute of Molecular Medicine (VIMM)Venetian Institute of Molecular Medicine (VIMM)Abstract Hibernating brown bears, due to a drastic reduction in metabolic rate, show only moderate muscle wasting. Here, we evaluate if ATPase activity of resting skeletal muscle myosin can contribute to this energy sparing. By analyzing single muscle fibers taken from the same bears, either during hibernation or in summer, we find that fibers from hibernating bears have a mild decline in force production and a significant reduction in ATPase activity. Single fiber proteomics, western blotting, and immunohistochemical analyses reveal major remodeling of the mitochondrial proteome during hibernation. Furthermore, using bioinformatical approaches and western blotting we find that phosphorylated myosin light chain, a known stimulator of basal myosin ATPase activity, is decreased in hibernating and disused muscles. These results suggest that skeletal muscle limits energy loss by reducing myosin ATPase activity, indicating a possible role for myosin ATPase activity modulation in multiple muscle wasting conditions.https://doi.org/10.1038/s41467-024-55565-4
spellingShingle Cosimo De Napoli
Luisa Schmidt
Mauro Montesel
Laura Cussonneau
Samuele Sanniti
Lorenzo Marcucci
Elena Germinario
Jonas Kindberg
Alina Lynn Evans
Guillemette Gauquelin-Koch
Marco Narici
Fabrice Bertile
Etienne Lefai
Marcus Krüger
Leonardo Nogara
Bert Blaauw
Reduced ATP turnover during hibernation in relaxed skeletal muscle
Nature Communications
title Reduced ATP turnover during hibernation in relaxed skeletal muscle
title_full Reduced ATP turnover during hibernation in relaxed skeletal muscle
title_fullStr Reduced ATP turnover during hibernation in relaxed skeletal muscle
title_full_unstemmed Reduced ATP turnover during hibernation in relaxed skeletal muscle
title_short Reduced ATP turnover during hibernation in relaxed skeletal muscle
title_sort reduced atp turnover during hibernation in relaxed skeletal muscle
url https://doi.org/10.1038/s41467-024-55565-4
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