Remodeling of skeletal muscle myosin metabolic states in hibernating mammals
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 efficie...
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eLife Sciences Publications, Ltd
2024
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Online Access: | http://dx.doi.org/10.7554/elife.94616.3 https://cdn.elifesciences.org/articles/94616/elife-94616-v1.pdf https://cdn.elifesciences.org/articles/94616/elife-94616-v1.xml https://elifesciences.org/articles/94616 |
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crelifesciences:10.7554/elife.94616.3 2024-09-30T14:45:38+00:00 Remodeling of skeletal muscle myosin metabolic states in hibernating mammals Lewis, Christopher TA Melhedegaard, Elise G Ognjanovic, Marija M Olsen, Mathilde S Laitila, Jenni Seaborne, Robert AE Gronset, Magnus Zhang, Changxin Iwamoto, Hiroyuki Hessel, Anthony L Kuehn, Michel N Merino, Carla Amigo, Nuria Frobert, Ole Giroud, Sylvain Staples, James F Goropashnaya, Anna V Fedorov, Vadim B Barnes, Brian Toien, Oivind Drew, Kelly Sprenger, Ryan J Ochala, Julien Carlsbergfondet Novo Nordisk Foundation Norwegian Environment Agency and the Swedish Environmental Protection Agency Natural Sciences and Engineering Research Council 2024 http://dx.doi.org/10.7554/elife.94616.3 https://cdn.elifesciences.org/articles/94616/elife-94616-v1.pdf https://cdn.elifesciences.org/articles/94616/elife-94616-v1.xml https://elifesciences.org/articles/94616 en eng eLife Sciences Publications, Ltd http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/ eLife volume 13 ISSN 2050-084X journal-article 2024 crelifesciences https://doi.org/10.7554/elife.94616.3 2024-09-09T06:25:05Z 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. Article in Journal/Newspaper Ursus arctos eLife eLife 13 |
institution |
Open Polar |
collection |
eLife |
op_collection_id |
crelifesciences |
language |
English |
description |
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. |
author2 |
Carlsbergfondet Novo Nordisk Foundation Norwegian Environment Agency and the Swedish Environmental Protection Agency Natural Sciences and Engineering Research Council |
format |
Article in Journal/Newspaper |
author |
Lewis, Christopher TA Melhedegaard, Elise G Ognjanovic, Marija M Olsen, Mathilde S Laitila, Jenni Seaborne, Robert AE Gronset, Magnus Zhang, Changxin Iwamoto, Hiroyuki Hessel, Anthony L Kuehn, Michel N Merino, Carla Amigo, Nuria Frobert, Ole Giroud, Sylvain Staples, James F Goropashnaya, Anna V Fedorov, Vadim B Barnes, Brian Toien, Oivind Drew, Kelly Sprenger, Ryan J Ochala, Julien |
spellingShingle |
Lewis, Christopher TA Melhedegaard, Elise G Ognjanovic, Marija M Olsen, Mathilde S Laitila, Jenni Seaborne, Robert AE Gronset, Magnus Zhang, Changxin Iwamoto, Hiroyuki Hessel, Anthony L Kuehn, Michel N Merino, Carla Amigo, Nuria Frobert, Ole Giroud, Sylvain Staples, James F Goropashnaya, Anna V Fedorov, Vadim B Barnes, Brian Toien, Oivind Drew, Kelly Sprenger, Ryan J Ochala, Julien Remodeling of skeletal muscle myosin metabolic states in hibernating mammals |
author_facet |
Lewis, Christopher TA Melhedegaard, Elise G Ognjanovic, Marija M Olsen, Mathilde S Laitila, Jenni Seaborne, Robert AE Gronset, Magnus Zhang, Changxin Iwamoto, Hiroyuki Hessel, Anthony L Kuehn, Michel N Merino, Carla Amigo, Nuria Frobert, Ole Giroud, Sylvain Staples, James F Goropashnaya, Anna V Fedorov, Vadim B Barnes, Brian Toien, Oivind Drew, Kelly Sprenger, Ryan J Ochala, Julien |
author_sort |
Lewis, Christopher TA |
title |
Remodeling of skeletal muscle myosin metabolic states in hibernating mammals |
title_short |
Remodeling of skeletal muscle myosin metabolic states in hibernating mammals |
title_full |
Remodeling of skeletal muscle myosin metabolic states in hibernating mammals |
title_fullStr |
Remodeling of skeletal muscle myosin metabolic states in hibernating mammals |
title_full_unstemmed |
Remodeling of skeletal muscle myosin metabolic states in hibernating mammals |
title_sort |
remodeling of skeletal muscle myosin metabolic states in hibernating mammals |
publisher |
eLife Sciences Publications, Ltd |
publishDate |
2024 |
url |
http://dx.doi.org/10.7554/elife.94616.3 https://cdn.elifesciences.org/articles/94616/elife-94616-v1.pdf https://cdn.elifesciences.org/articles/94616/elife-94616-v1.xml https://elifesciences.org/articles/94616 |
genre |
Ursus arctos |
genre_facet |
Ursus arctos |
op_source |
eLife volume 13 ISSN 2050-084X |
op_rights |
http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/ |
op_doi |
https://doi.org/10.7554/elife.94616.3 |
container_title |
eLife |
container_volume |
13 |
_version_ |
1811646167111434240 |