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Making waves: A proposed new role for myosin-binding protein C in regulating oscillatory contractions in vertebrate striated muscle

Myosin-binding protein C (MyBP-C) is a critical regulator of muscle performance that was first identified through its strong binding interactions with myosin, the force-generating protein of muscle. Almost simultaneously with its discovery, MyBP-C was soon found to bind to actin, the physiological c...

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Published in:	The Journal of general physiology 2021-03, Vol.153 (3), p.1
Main Author:	Harris, Samantha P
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Language:	English
Subjects:	Actin Biophysics Catalysts Contraction and cell motility Filaments Molecular modelling Muscle contraction Myofilament Special Issue, 2020 Myosin Myosin-binding protein C Protein C Proteins Skeletal muscle Viewpoint
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description	Myosin-binding protein C (MyBP-C) is a critical regulator of muscle performance that was first identified through its strong binding interactions with myosin, the force-generating protein of muscle. Almost simultaneously with its discovery, MyBP-C was soon found to bind to actin, the physiological catalyst for myosin's activity. However, the two observations posed an apparent paradox, in part because interactions of MyBP-C with myosin were on the thick filament, whereas MyBP-C interactions with actin were on the thin filament. Despite the intervening decades since these initial discoveries, it is only recently that the dual binding modes of MyBP-C are becoming reconciled in models that place MyBP-C at a central position between actin and myosin, where MyBP-C alternately stabilizes a newly discovered super-relaxed state (SRX) of myosin on thick filaments in resting muscle and then prolongs the "on" state of actin on thin filaments in active muscle. Recognition of these dual, alternating functions of MyBP-C reveals how it is central to the regulation of both muscle contraction and relaxation. The purpose of this Viewpoint is to briefly summarize the roles of MyBP-C in binding to myosin and actin and then to highlight a possible new role for MyBP-C in inducing and damping oscillatory waves of contraction and relaxation. Because the contractile waves bear similarity to cycles of contraction and relaxation in insect flight muscles, which evolved for fast, energetically efficient contraction, the ability of MyBP-C to damp so-called spontaneous oscillatory contractions (SPOCs) has broad implications for previously unrecognized regulatory mechanisms in vertebrate striated muscle. While the molecular mechanisms by which MyBP-C can function as a wave maker or a wave breaker are just beginning to be explored, it is likely that MyBP-C dual interactions with both myosin and actin will continue to be important for understanding the new functions of this enigmatic protein.
doi_str_mv	10.1085/jgp.202012729
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The purpose of this Viewpoint is to briefly summarize the roles of MyBP-C in binding to myosin and actin and then to highlight a possible new role for MyBP-C in inducing and damping oscillatory waves of contraction and relaxation. Because the contractile waves bear similarity to cycles of contraction and relaxation in insect flight muscles, which evolved for fast, energetically efficient contraction, the ability of MyBP-C to damp so-called spontaneous oscillatory contractions (SPOCs) has broad implications for previously unrecognized regulatory mechanisms in vertebrate striated muscle. While the molecular mechanisms by which MyBP-C can function as a wave maker or a wave breaker are just beginning to be explored, it is likely that MyBP-C dual interactions with both myosin and actin will continue to be important for understanding the new functions of this enigmatic protein.</description><identifier>ISSN: 0022-1295</identifier><identifier>EISSN: 1540-7748</identifier><identifier>DOI: 10.1085/jgp.202012729</identifier><identifier>PMID: 33275758</identifier><language>eng</language><publisher>United States: Rockefeller University Press</publisher><subject>Actin ; Biophysics ; Catalysts ; Contraction and cell motility ; Filaments ; Molecular modelling ; Muscle contraction ; Myofilament Special Issue, 2020 ; Myosin ; Myosin-binding protein C ; Protein C ; Proteins ; Skeletal muscle ; Viewpoint</subject><ispartof>The Journal of general physiology, 2021-03, Vol.153 (3), p.1</ispartof><rights>2020 Harris.</rights><rights>Copyright Rockefeller University Press Mar 2021</rights><rights>2020 Harris 2020</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c481t-bbc5db19f1afb63f31ecce1345d86d8ee5032644fe568bee83be67c87286e9e43</citedby><cites>FETCH-LOGICAL-c481t-bbc5db19f1afb63f31ecce1345d86d8ee5032644fe568bee83be67c87286e9e43</cites><orcidid>0000-0003-0822-0238</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/PMC7721898/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7721898/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,315,733,786,790,891,27957,27958,53827,53829</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33275758$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Harris, Samantha P</creatorcontrib><title>Making waves: A proposed new role for myosin-binding protein C in regulating oscillatory contractions in vertebrate striated muscle</title><title>The Journal of general physiology</title><addtitle>J Gen Physiol</addtitle><description>Myosin-binding protein C (MyBP-C) is a critical regulator of muscle performance that was first identified through its strong binding interactions with myosin, the force-generating protein of muscle. Almost simultaneously with its discovery, MyBP-C was soon found to bind to actin, the physiological catalyst for myosin's activity. However, the two observations posed an apparent paradox, in part because interactions of MyBP-C with myosin were on the thick filament, whereas MyBP-C interactions with actin were on the thin filament. Despite the intervening decades since these initial discoveries, it is only recently that the dual binding modes of MyBP-C are becoming reconciled in models that place MyBP-C at a central position between actin and myosin, where MyBP-C alternately stabilizes a newly discovered super-relaxed state (SRX) of myosin on thick filaments in resting muscle and then prolongs the "on" state of actin on thin filaments in active muscle. Recognition of these dual, alternating functions of MyBP-C reveals how it is central to the regulation of both muscle contraction and relaxation. The purpose of this Viewpoint is to briefly summarize the roles of MyBP-C in binding to myosin and actin and then to highlight a possible new role for MyBP-C in inducing and damping oscillatory waves of contraction and relaxation. Because the contractile waves bear similarity to cycles of contraction and relaxation in insect flight muscles, which evolved for fast, energetically efficient contraction, the ability of MyBP-C to damp so-called spontaneous oscillatory contractions (SPOCs) has broad implications for previously unrecognized regulatory mechanisms in vertebrate striated muscle. While the molecular mechanisms by which MyBP-C can function as a wave maker or a wave breaker are just beginning to be explored, it is likely that MyBP-C dual interactions with both myosin and actin will continue to be important for understanding the new functions of this enigmatic protein.</description><subject>Actin</subject><subject>Biophysics</subject><subject>Catalysts</subject><subject>Contraction and cell motility</subject><subject>Filaments</subject><subject>Molecular modelling</subject><subject>Muscle contraction</subject><subject>Myofilament Special Issue, 2020</subject><subject>Myosin</subject><subject>Myosin-binding protein C</subject><subject>Protein C</subject><subject>Proteins</subject><subject>Skeletal muscle</subject><subject>Viewpoint</subject><issn>0022-1295</issn><issn>1540-7748</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><recordid>eNpdkc1v1DAQxS1ERZfCkSuyxIVLWn_EscMBqVrxJbXqBc6W40wWL4kdbGerPfOP46hlBfgwMxr_9DRPD6FXlFxSosTVfjdfMsIIZZK1T9CGippUUtbqKdoQwlhFWSvO0fOU9qQ8wcgzdM45k0IKtUG_bs0P53f43hwgvcPXeI5hDgl67OEexzACHkLE0zEk56vO-X6lC5TBebzFpUTYLaPJ6z4k68Yyh3jENvgcjc0u-LRiB4gZumgy4JSjK73H05LsCC_Q2WDGBC8f-wX69vHD1-3n6ubu05ft9U1la0Vz1XVW9B1tB2qGruEDp2AtUF6LXjW9AhCEs6auBxCN6gAU76CRVkmmGmih5hfo_YPuvHQT9BbWA0c9RzeZeNTBOP3vj3ff9S4ctJSMqlYVgbePAjH8XCBlPblkoTj2EJakWd3IppCkLeib_9B9WKIv9jQTRFJZE74KVg-UjSGlCMPpGEr0Gq8u8epTvIV__beDE_0nT_4b4Dukrg</recordid><startdate>20210301</startdate><enddate>20210301</enddate><creator>Harris, Samantha P</creator><general>Rockefeller University Press</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>7TS</scope><scope>8FD</scope><scope>FR3</scope><scope>K9.</scope><scope>P64</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-0822-0238</orcidid></search><sort><creationdate>20210301</creationdate><title>Making waves: A proposed new role for myosin-binding protein C in regulating oscillatory contractions in vertebrate striated muscle</title><author>Harris, Samantha P</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c481t-bbc5db19f1afb63f31ecce1345d86d8ee5032644fe568bee83be67c87286e9e43</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Actin</topic><topic>Biophysics</topic><topic>Catalysts</topic><topic>Contraction and cell motility</topic><topic>Filaments</topic><topic>Molecular modelling</topic><topic>Muscle contraction</topic><topic>Myofilament Special Issue, 2020</topic><topic>Myosin</topic><topic>Myosin-binding protein C</topic><topic>Protein C</topic><topic>Proteins</topic><topic>Skeletal muscle</topic><topic>Viewpoint</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Harris, Samantha P</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Physical Education Index</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of general physiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Harris, Samantha P</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Making waves: A proposed new role for myosin-binding protein C in regulating oscillatory contractions in vertebrate striated muscle</atitle><jtitle>The Journal of general physiology</jtitle><addtitle>J Gen Physiol</addtitle><date>2021-03-01</date><risdate>2021</risdate><volume>153</volume><issue>3</issue><spage>1</spage><pages>1-</pages><issn>0022-1295</issn><eissn>1540-7748</eissn><notes>ObjectType-Article-1</notes><notes>SourceType-Scholarly Journals-1</notes><notes>ObjectType-Feature-2</notes><notes>content type line 23</notes><notes>This work is part of a special collection on myofilament function and disease.</notes><abstract>Myosin-binding protein C (MyBP-C) is a critical regulator of muscle performance that was first identified through its strong binding interactions with myosin, the force-generating protein of muscle. Almost simultaneously with its discovery, MyBP-C was soon found to bind to actin, the physiological catalyst for myosin's activity. However, the two observations posed an apparent paradox, in part because interactions of MyBP-C with myosin were on the thick filament, whereas MyBP-C interactions with actin were on the thin filament. Despite the intervening decades since these initial discoveries, it is only recently that the dual binding modes of MyBP-C are becoming reconciled in models that place MyBP-C at a central position between actin and myosin, where MyBP-C alternately stabilizes a newly discovered super-relaxed state (SRX) of myosin on thick filaments in resting muscle and then prolongs the "on" state of actin on thin filaments in active muscle. Recognition of these dual, alternating functions of MyBP-C reveals how it is central to the regulation of both muscle contraction and relaxation. The purpose of this Viewpoint is to briefly summarize the roles of MyBP-C in binding to myosin and actin and then to highlight a possible new role for MyBP-C in inducing and damping oscillatory waves of contraction and relaxation. Because the contractile waves bear similarity to cycles of contraction and relaxation in insect flight muscles, which evolved for fast, energetically efficient contraction, the ability of MyBP-C to damp so-called spontaneous oscillatory contractions (SPOCs) has broad implications for previously unrecognized regulatory mechanisms in vertebrate striated muscle. 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subjects	Actin Biophysics Catalysts Contraction and cell motility Filaments Molecular modelling Muscle contraction Myofilament Special Issue, 2020 Myosin Myosin-binding protein C Protein C Proteins Skeletal muscle Viewpoint
title	Making waves: A proposed new role for myosin-binding protein C in regulating oscillatory contractions in vertebrate striated muscle
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