Remodeling of skeletal muscle myosin metabolic states in hibernating mammals

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Remodeling of skeletal muscle myosin metabolic states in hibernating mammals

Lewis, Christopher T. A. (author): Department of Biomedical Sciences, University of Copenhagen, Copenhagen, Denmark

Melhedegaard, Elise G. (author): Department of Biomedical Sciences, University of Copenhagen, Copenhagen, Denmark

Ognjanovic, Marija M. (author): Department of Biomedical Sciences, University of Copenhagen, Copenhagen, Denmark

Olsen, Mathilde S. (author): Department of Biomedical Sciences, University of Copenhagen, Copenhagen, Denmark

Laitila, Jenni (author): Department of Biomedical Sciences, University of Copenhagen, Copenhagen, Denmark

Seaborne, Robert A. E. (author): Department of Biomedical Sciences, University of Copenhagen, Copenhagen, Denmark; Centre for Human and Applied Physiological Sciences, Faculty of Life Sciences & Medicine, King's College London, London, United Kingdom

Gronset, Magnus (author): Department of Cellular and Molecular Medicine, University of Copenhagen, Copenhagen, Denmark

Zhang, Changxin (author): Department of Computational Medicine and Bioinformatics, University of Michigan, Ann Arbor, United States

Iwamoto, Hiroyuki (author): Spring-8, Japan Synchrotron Radiation Research Institute, Hyogo, Japan

Hessel, Anthony L. (author): Institute of Physiology II, University of Muenster, Muenster, Germany; Accelerated Muscle Biotechnologies Consultants, Boston, United States

Kuehn, Michel N. (author): Institute of Physiology II, University of Muenster, Muenster, Germany; Accelerated Muscle Biotechnologies Consultants, Boston, United States

Merino, Carla (author): Biosfer Teslab, Reus, Spain

Amigo, Nuria (author): Biosfer Teslab, Reus, Spain

Fröbert, Ole, 1964- (author): Örebro universitet,Institutionen för medicinska vetenskaper,Department of Clinical Medicine, Faculty of Health, Aarhus University, Aarhus, Denmark; Faculty of Health, Department of Cardiology, Örebro University, Örebro, Sweden

Giroud, Sylvain (author): Energetics Lab, Department of Biology, Northern Michigan University, Marquette, United States; Research Institute of Wildlife Ecology, Department of Interdisciplinary Life Sciences, University of Veterinary Medicine Vienna, Vienna, Austria

Staples, James F. (author): Department of Biology, University of Western Ontario, London, Canada

Goropashnaya, Anna V. (author): Center for Transformative Research in Metabolism, Institute of Arctic Biology, University of Alaska Fairbanks, Fairbanks, United States

Fedorov, Vadim B. (author): Center for Transformative Research in Metabolism, Institute of Arctic Biology, University of Alaska Fairbanks, Fairbanks, United States

Barnes, Brian (author): Center for Transformative Research in Metabolism, Institute of Arctic Biology, University of Alaska Fairbanks, Fairbanks, United States

Toien, Oivind (author): Center for Transformative Research in Metabolism, Institute of Arctic Biology, University of Alaska Fairbanks, Fairbanks, United States

Drew, Kelly (author): Center for Transformative Research in Metabolism, Institute of Arctic Biology, University of Alaska Fairbanks, Fairbanks, United States

Sprenger, Ryan J. (author): Department of Zoology, University of British Columbia, Vancouver, Canada

Ochala, Julien (author): Department of Biomedical Sciences, University of Copenhagen, Copenhagen, Denmark

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eLife Sciences Publications Ltd, 2024
2024
English.
In: eLIFE. - : eLife Sciences Publications Ltd. - 2050-084X. ; 13

Related links:: https://doi.org/10.7...; show more...; https://urn.kb.se/re...; https://doi.org/10.7...; show less...

Journal article (peer-reviewed)

Abstract Subject headings

Hibernation is a period of metabolic suppression utilized by many small and large mammal species to survive during winter periods. As the underlying cellular and molecular mechanisms remain incompletely understood, our study aimed to determine whether skeletal muscle myosin and its metabolic efficiency undergo alterations during hibernation to optimize energy utilization. We isolated muscle fibers from small hibernators, Ictidomys tridecemlineatus and Eliomys quercinus and larger hibernators, Ursus arctos and Ursus americanus. We then conducted loaded Mant-ATP chase experiments alongside X-ray diffraction to measure resting myosin dynamics and its ATP demand. In parallel, we performed multiple proteomics analyses. Our results showed a preservation of myosin structure in U. arctos and U. americanus during hibernation, whilst in I. tridecemlineatus and E. quercinus, changes in myosin metabolic states during torpor unexpectedly led to higher levels in energy expenditure of type II, fast-twitch muscle fibers at ambient lab temperatures (20 °C). Upon repeating loaded Mant-ATP chase experiments at 8 °C (near the body temperature of torpid animals), we found that myosin ATP consumption in type II muscle fibers was reduced by 77-107% during torpor compared to active periods. Additionally, we observed Myh2 hyper-phosphorylation during torpor in I. tridecemilineatus, which was predicted to stabilize the myosin molecule. This may act as a potential molecular mechanism mitigating myosin-associated increases in skeletal muscle energy expenditure during periods of torpor in response to cold exposure. Altogether, we demonstrate that resting myosin is altered in hibernating mammals, contributing to significant changes to the ATP consumption of skeletal muscle. Additionally, we observe that it is further altered in response to cold exposure and highlight myosin as a potentially contributor to skeletal muscle non-shivering thermogenesis.

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NATURAL SCIENCES: NATURAL SCIENCES; and Biological Scien ...; and Biophysics

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By the university: Örebro University

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Remodeling of skeletal muscle myosin metabolic states in hibernating mammals

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