Title
Remodeling of skeletal muscle myosin metabolic states in hibernating mammals
Language
English
Description (en)
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.
Keywords (en)
Animals; Hibernation physiology; Energy Metabolism; Skeletal Muscle Myosinsmetabolism; Ursidaemetabolism physiology; Adenosine Triphosphate metabolism; Muscle, Skeletal metabolism physiology; Muscle Fibers, Skeletal metabolism; Proteomics
DOI
10.7554/eLife.94616
Author of the digital object
Christopher T. A.  Lewis  (University of Copenhagen)
Julien  Ochala  (University of Copenhagen)
Ryan J.  Sprenger  (University of British Columbia)
Kelly  Drew  (University of Alaska Fairbanks)
Oivind  Toien  (University of Alaska Fairbanks)
Brian  Barnes  (University of Alaska Fairbanks)
Vadim B.  Fedorov  (University of Alaska Fairbanks)
Anna V.  Goropashnaya  (University of Alaska Fairbanks)
James F.  Staples  (University of Western Ontario)
Sylvain  Giroud  (University of Veterinary Medicine Vienna / Northern Michigan University)
Ole  Frobert  (Aarhus University / Örebro University)
Nuria  Amigo  (Biosfer Teslab)
Carla  Merino  (Biosfer Teslab)
Michel N.  Kuehn  (University of Muenster / Accelerated Muscle Biotechnologies Consultants)
Anthony L.  Hessel  (University of Muenster / Accelerated Muscle Biotechnologies Consultants)
Hiroyuki  Iwamoto  (Japan Synchrotron Radiation Research Institute)
Changxin  Zhang  (University of Michigan)
Magnus  Gronset  (University of Copenhagen)
Robert A. E.  Seaborne  (University of Copenhagen / King's College London)
Jenni  Laitila  (University of Copenhagen)
Mathilde S.  Olsen  (University of Copenhagen)
Elise G.  Melhedegaard  (University of Copenhagen)
Marija M.  Ognjanovic  (University of Copenhagen)
Format
application/pdf
Size
3.9 MB
Licence Selected
CC BY 4.0 International
Type of publication
Article
Name of Publication (en)
eLife
Pages or Volume
26
Volume
13
Publisher
eLife Sciences Publications Ltd
Publication Date
2024
Content
Details
Object type
PDFDocument
Format
application/pdf
Created
08.07.2024 02:20:54
This object is in collection
Metadata
Veterinärmedizinische Universität Wien (Vetmeduni) | Veterinärplatz 1 | 1210 Wien - Österreich | T +43 1 25077-0 | Web: vetmeduni.ac.at