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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creator | 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. |
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. |
doi_str_mv | 10.1016/j.jbc.2022.102657 |
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Tom ; Bowman, Gregory ; Geeves, Michael A. ; Greenberg, Michael J. ; Leinwand, Leslie A.</creator><creatorcontrib>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.</creatorcontrib><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.</description><identifier>ISSN: 0021-9258</identifier><identifier>EISSN: 1083-351X</identifier><identifier>DOI: 10.1016/j.jbc.2022.102657</identifier><identifier>PMID: 36334627</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>actin ; Animals ; cardiac muscle ; Cardiac Myosins - genetics ; Cardiac Myosins - metabolism ; Humans ; interacting heads motif ; kinetics ; Mammals - metabolism ; molecular motor ; Muscle, Skeletal - metabolism ; myosin ; Myosin Heavy Chains - genetics ; Myosin Heavy Chains - metabolism ; Protein Isoforms - genetics ; Protein Isoforms - metabolism ; skeletal muscle ; structure–function ; super-relaxed state</subject><ispartof>The Journal of biological chemistry, 2023-01, Vol.299 (1), p.102657-102657, Article 102657</ispartof><rights>2022 The Authors</rights><rights>Copyright © 2022 The Authors. Published by Elsevier Inc. All rights reserved.</rights><rights>2022 The Authors 2022</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c451t-aeaba6dd71b964140392092a734486c9513bb318a2f0f92d16d47456dd3ac5b03</citedby><cites>FETCH-LOGICAL-c451t-aeaba6dd71b964140392092a734486c9513bb318a2f0f92d16d47456dd3ac5b03</cites><orcidid>0000-0002-5022-7006 ; 0000-0003-1320-3547 ; 0000-0002-0203-7769 ; 0000-0002-8634-5039 ; 0000-0002-5504-2684</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9800208/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9800208/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36334627$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Lee, Lindsey A.</creatorcontrib><creatorcontrib>Barrick, Samantha K.</creatorcontrib><creatorcontrib>Meller, Artur</creatorcontrib><creatorcontrib>Walklate, Jonathan</creatorcontrib><creatorcontrib>Lotthammer, Jeffrey M.</creatorcontrib><creatorcontrib>Tay, Jian Wei</creatorcontrib><creatorcontrib>Stump, W. Tom</creatorcontrib><creatorcontrib>Bowman, Gregory</creatorcontrib><creatorcontrib>Geeves, Michael A.</creatorcontrib><creatorcontrib>Greenberg, Michael J.</creatorcontrib><creatorcontrib>Leinwand, Leslie A.</creatorcontrib><title>Functional divergence of the sarcomeric myosin, MYH7b, supports species-specific biological roles</title><title>The Journal of biological chemistry</title><addtitle>J Biol Chem</addtitle><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.</description><subject>actin</subject><subject>Animals</subject><subject>cardiac muscle</subject><subject>Cardiac Myosins - genetics</subject><subject>Cardiac Myosins - metabolism</subject><subject>Humans</subject><subject>interacting heads motif</subject><subject>kinetics</subject><subject>Mammals - metabolism</subject><subject>molecular motor</subject><subject>Muscle, Skeletal - metabolism</subject><subject>myosin</subject><subject>Myosin Heavy Chains - genetics</subject><subject>Myosin Heavy Chains - metabolism</subject><subject>Protein Isoforms - genetics</subject><subject>Protein Isoforms - metabolism</subject><subject>skeletal muscle</subject><subject>structure–function</subject><subject>super-relaxed state</subject><issn>0021-9258</issn><issn>1083-351X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kUtLxDAUhYMoOo7-ADfSpQs75tkHgiDiCxQ3CroKSXo7ZmibmrQD_nszjopuzOYScs7J5XwIHRA8I5hkJ4vZQpsZxZTGO81EvoEmBBcsZYI8b6IJxpSkJRXFDtoNYYHj4SXZRjssY4xnNJ8gdTV2ZrCuU01S2SX4OXQGElcnwyskQXnjWvDWJO27C7Y7Tu5fbnJ9nISx750fQhJ6MBZC-jnrKNTWNW5uTQz0roGwh7Zq1QTY_5pT9HR1-Xhxk949XN9enN-lhgsypAqUVllV5USXGSccs5LikqqccV5kphSEac1IoWiN65JWJKt4zkV0MGWExmyKzta5_ahbqAx0g1eN7L1tlX-XTln596Wzr3LulrIsYk-xtSk6-grw7m2EMMjWBgNNozpwY5A0Z1TEbcRKStZS410IHuqfbwiWKzRyISMauUIj12ii5_D3fj-ObxZRcLoWQGxpacHLEJuNNCrrwQyycvaf-A_th6BL</recordid><startdate>20230101</startdate><enddate>20230101</enddate><creator>Lee, Lindsey A.</creator><creator>Barrick, Samantha K.</creator><creator>Meller, Artur</creator><creator>Walklate, Jonathan</creator><creator>Lotthammer, Jeffrey M.</creator><creator>Tay, Jian Wei</creator><creator>Stump, W. Tom</creator><creator>Bowman, Gregory</creator><creator>Geeves, Michael A.</creator><creator>Greenberg, Michael J.</creator><creator>Leinwand, Leslie A.</creator><general>Elsevier Inc</general><general>American Society for Biochemistry and Molecular Biology</general><scope>6I.</scope><scope>AAFTH</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-5022-7006</orcidid><orcidid>https://orcid.org/0000-0003-1320-3547</orcidid><orcidid>https://orcid.org/0000-0002-0203-7769</orcidid><orcidid>https://orcid.org/0000-0002-8634-5039</orcidid><orcidid>https://orcid.org/0000-0002-5504-2684</orcidid></search><sort><creationdate>20230101</creationdate><title>Functional divergence of the sarcomeric myosin, MYH7b, supports species-specific biological roles</title><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></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c451t-aeaba6dd71b964140392092a734486c9513bb318a2f0f92d16d47456dd3ac5b03</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>actin</topic><topic>Animals</topic><topic>cardiac muscle</topic><topic>Cardiac Myosins - genetics</topic><topic>Cardiac Myosins - metabolism</topic><topic>Humans</topic><topic>interacting heads motif</topic><topic>kinetics</topic><topic>Mammals - metabolism</topic><topic>molecular motor</topic><topic>Muscle, Skeletal - metabolism</topic><topic>myosin</topic><topic>Myosin Heavy Chains - genetics</topic><topic>Myosin Heavy Chains - metabolism</topic><topic>Protein Isoforms - genetics</topic><topic>Protein Isoforms - metabolism</topic><topic>skeletal muscle</topic><topic>structure–function</topic><topic>super-relaxed state</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Lee, Lindsey A.</creatorcontrib><creatorcontrib>Barrick, Samantha K.</creatorcontrib><creatorcontrib>Meller, Artur</creatorcontrib><creatorcontrib>Walklate, Jonathan</creatorcontrib><creatorcontrib>Lotthammer, Jeffrey M.</creatorcontrib><creatorcontrib>Tay, Jian Wei</creatorcontrib><creatorcontrib>Stump, W. Tom</creatorcontrib><creatorcontrib>Bowman, Gregory</creatorcontrib><creatorcontrib>Geeves, Michael A.</creatorcontrib><creatorcontrib>Greenberg, Michael J.</creatorcontrib><creatorcontrib>Leinwand, Leslie A.</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of biological chemistry</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Lee, Lindsey A.</au><au>Barrick, Samantha K.</au><au>Meller, Artur</au><au>Walklate, Jonathan</au><au>Lotthammer, Jeffrey M.</au><au>Tay, Jian Wei</au><au>Stump, W. Tom</au><au>Bowman, Gregory</au><au>Geeves, Michael A.</au><au>Greenberg, Michael J.</au><au>Leinwand, Leslie A.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Functional divergence of the sarcomeric myosin, MYH7b, supports species-specific biological roles</atitle><jtitle>The Journal of biological chemistry</jtitle><addtitle>J Biol Chem</addtitle><date>2023-01-01</date><risdate>2023</risdate><volume>299</volume><issue>1</issue><spage>102657</spage><epage>102657</epage><pages>102657-102657</pages><artnum>102657</artnum><issn>0021-9258</issn><eissn>1083-351X</eissn><abstract>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.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>36334627</pmid><doi>10.1016/j.jbc.2022.102657</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0002-5022-7006</orcidid><orcidid>https://orcid.org/0000-0003-1320-3547</orcidid><orcidid>https://orcid.org/0000-0002-0203-7769</orcidid><orcidid>https://orcid.org/0000-0002-8634-5039</orcidid><orcidid>https://orcid.org/0000-0002-5504-2684</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | actin Animals cardiac muscle Cardiac Myosins - genetics Cardiac Myosins - metabolism Humans interacting heads motif kinetics Mammals - metabolism molecular motor Muscle, Skeletal - metabolism myosin Myosin Heavy Chains - genetics Myosin Heavy Chains - metabolism Protein Isoforms - genetics Protein Isoforms - metabolism skeletal muscle structure–function super-relaxed state |
title | Functional divergence of the sarcomeric myosin, MYH7b, supports species-specific biological roles |
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