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Functional divergence of the sarcomeric myosin, MYH7b, supports species-specific biological roles

Myosin heavy chain 7b (MYH7b) is an evolutionarily ancient member of the sarcomeric myosin family, which typically supports striated muscle function. However, in mammals, alternative splicing prevents MYH7b protein production in cardiac and most skeletal muscles and limits expression to a subset of...

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Autores principales: Lee, Lindsey A., Barrick, Samantha K., Meller, Artur, Walklate, Jonathan, Lotthammer, Jeffrey M., Tay, Jian Wei, Stump, W. Tom, Bowman, Gregory, Geeves, Michael A., Greenberg, Michael J., Leinwand, Leslie A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Biochemistry and Molecular Biology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9800208/
https://www.ncbi.nlm.nih.gov/pubmed/36334627
http://dx.doi.org/10.1016/j.jbc.2022.102657
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author Lee, Lindsey A.
Barrick, Samantha K.
Meller, Artur
Walklate, Jonathan
Lotthammer, Jeffrey M.
Tay, Jian Wei
Stump, W. Tom
Bowman, Gregory
Geeves, Michael A.
Greenberg, Michael J.
Leinwand, Leslie A.
author_facet Lee, Lindsey A.
Barrick, Samantha K.
Meller, Artur
Walklate, Jonathan
Lotthammer, Jeffrey M.
Tay, Jian Wei
Stump, W. Tom
Bowman, Gregory
Geeves, Michael A.
Greenberg, Michael J.
Leinwand, Leslie A.
author_sort Lee, Lindsey A.
collection PubMed
description Myosin heavy chain 7b (MYH7b) is an evolutionarily ancient member of the sarcomeric myosin family, which typically supports striated muscle function. However, in mammals, alternative splicing prevents MYH7b protein production in cardiac and most skeletal muscles and limits expression to a subset of specialized muscles and certain nonmuscle environments. In contrast, MYH7b protein is abundant in python cardiac and skeletal muscles. Although the MYH7b expression pattern diverges in mammals versus reptiles, MYH7b shares high sequence identity across species. So, it remains unclear how mammalian MYH7b function may differ from that of other sarcomeric myosins and whether human and python MYH7b motor functions diverge as their expression patterns suggest. Thus, we generated recombinant human and python MYH7b protein and measured their motor properties to investigate any species-specific differences in activity. Our results reveal that despite having similar working strokes, the MYH7b isoforms have slower actin-activated ATPase cycles and actin sliding velocities than human cardiac β-MyHC. Furthermore, python MYH7b is tuned to have slower motor activity than human MYH7b because of slower kinetics of the chemomechanical cycle. We found that the MYH7b isoforms adopt a higher proportion of myosin heads in the ultraslow, super-relaxed state compared with human cardiac β-MyHC. These findings are supported by molecular dynamics simulations that predict MYH7b preferentially occupies myosin active site conformations similar to those observed in the structurally inactive state. Together, these results suggest that MYH7b is specialized for slow and energy-conserving motor activity and that differential tuning of MYH7b orthologs contributes to species-specific biological roles.
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spelling pubmed-98002082023-01-03 Functional divergence of the sarcomeric myosin, MYH7b, supports species-specific biological roles Lee, Lindsey A. Barrick, Samantha K. Meller, Artur Walklate, Jonathan Lotthammer, Jeffrey M. Tay, Jian Wei Stump, W. Tom Bowman, Gregory Geeves, Michael A. Greenberg, Michael J. Leinwand, Leslie A. J Biol Chem Research Article Myosin heavy chain 7b (MYH7b) is an evolutionarily ancient member of the sarcomeric myosin family, which typically supports striated muscle function. However, in mammals, alternative splicing prevents MYH7b protein production in cardiac and most skeletal muscles and limits expression to a subset of specialized muscles and certain nonmuscle environments. In contrast, MYH7b protein is abundant in python cardiac and skeletal muscles. Although the MYH7b expression pattern diverges in mammals versus reptiles, MYH7b shares high sequence identity across species. So, it remains unclear how mammalian MYH7b function may differ from that of other sarcomeric myosins and whether human and python MYH7b motor functions diverge as their expression patterns suggest. Thus, we generated recombinant human and python MYH7b protein and measured their motor properties to investigate any species-specific differences in activity. Our results reveal that despite having similar working strokes, the MYH7b isoforms have slower actin-activated ATPase cycles and actin sliding velocities than human cardiac β-MyHC. Furthermore, python MYH7b is tuned to have slower motor activity than human MYH7b because of slower kinetics of the chemomechanical cycle. We found that the MYH7b isoforms adopt a higher proportion of myosin heads in the ultraslow, super-relaxed state compared with human cardiac β-MyHC. These findings are supported by molecular dynamics simulations that predict MYH7b preferentially occupies myosin active site conformations similar to those observed in the structurally inactive state. Together, these results suggest that MYH7b is specialized for slow and energy-conserving motor activity and that differential tuning of MYH7b orthologs contributes to species-specific biological roles. American Society for Biochemistry and Molecular Biology 2022-11-09 /pmc/articles/PMC9800208/ /pubmed/36334627 http://dx.doi.org/10.1016/j.jbc.2022.102657 Text en © 2022 The Authors https://creativecommons.org/licenses/by/4.0/This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Research Article
Lee, Lindsey A.
Barrick, Samantha K.
Meller, Artur
Walklate, Jonathan
Lotthammer, Jeffrey M.
Tay, Jian Wei
Stump, W. Tom
Bowman, Gregory
Geeves, Michael A.
Greenberg, Michael J.
Leinwand, Leslie A.
Functional divergence of the sarcomeric myosin, MYH7b, supports species-specific biological roles
title Functional divergence of the sarcomeric myosin, MYH7b, supports species-specific biological roles
title_full Functional divergence of the sarcomeric myosin, MYH7b, supports species-specific biological roles
title_fullStr Functional divergence of the sarcomeric myosin, MYH7b, supports species-specific biological roles
title_full_unstemmed Functional divergence of the sarcomeric myosin, MYH7b, supports species-specific biological roles
title_short Functional divergence of the sarcomeric myosin, MYH7b, supports species-specific biological roles
title_sort functional divergence of the sarcomeric myosin, myh7b, supports species-specific biological roles
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9800208/
https://www.ncbi.nlm.nih.gov/pubmed/36334627
http://dx.doi.org/10.1016/j.jbc.2022.102657
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