Andrew F Mead, Neil B Wood, Shane R Nelson, Bradley M Palmer, Lin Yang, Samantha Beck Previs, Angela Ploysangngam, Guy G Kennedy, Jennifer F McAdow, Sarah M Tremble, Marcus A Zimmermann, Marilyn J Cipolla, Alicia M Ebert, Aaron N Johnson, Christina A Gurnett, Michael J Previs, David M Warshaw
{"title":"肌球蛋白结合蛋白 H 在发育中脊椎动物快节奏骨骼肌粗丝中的功能作用","authors":"Andrew F Mead, Neil B Wood, Shane R Nelson, Bradley M Palmer, Lin Yang, Samantha Beck Previs, Angela Ploysangngam, Guy G Kennedy, Jennifer F McAdow, Sarah M Tremble, Marcus A Zimmermann, Marilyn J Cipolla, Alicia M Ebert, Aaron N Johnson, Christina A Gurnett, Michael J Previs, David M Warshaw","doi":"10.1085/jgp.202413604","DOIUrl":null,"url":null,"abstract":"<p><p>Myosin-binding protein H (MyBP-H) is a component of the vertebrate skeletal muscle sarcomere with sequence and domain homology to myosin-binding protein C (MyBP-C). Whereas skeletal muscle isoforms of MyBP-C (fMyBP-C, sMyBP-C) modulate muscle contractility via interactions with actin thin filaments and myosin motors within the muscle sarcomere \"C-zone,\" MyBP-H has no known function. This is in part due to MyBP-H having limited expression in adult fast-twitch muscle and no known involvement in muscle disease. Quantitative proteomics reported here reveal that MyBP-H is highly expressed in prenatal rat fast-twitch muscles and larval zebrafish, suggesting a conserved role in muscle development and prompting studies to define its function. We take advantage of the genetic control of the zebrafish model and a combination of structural, functional, and biophysical techniques to interrogate the role of MyBP-H. Transgenic, FLAG-tagged MyBP-H or fMyBP-C both localize to the C-zones in larval myofibers, whereas genetic depletion of endogenous MyBP-H or fMyBP-C leads to increased accumulation of the other, suggesting competition for C-zone binding sites. Does MyBP-H modulate contractility in the C-zone? Globular domains critical to MyBP-C's modulatory functions are absent from MyBP-H, suggesting that MyBP-H may be functionally silent. However, our results suggest an active role. In vitro motility experiments indicate MyBP-H shares MyBP-C's capacity as a molecular \"brake.\" These results provide new insights and raise questions about the role of the C-zone during muscle development.</p>","PeriodicalId":54828,"journal":{"name":"Journal of General Physiology","volume":"156 12","pages":""},"PeriodicalIF":3.3000,"publicationDate":"2024-12-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11461142/pdf/","citationCount":"0","resultStr":"{\"title\":\"Functional role of myosin-binding protein H in thick filaments of developing vertebrate fast-twitch skeletal muscle.\",\"authors\":\"Andrew F Mead, Neil B Wood, Shane R Nelson, Bradley M Palmer, Lin Yang, Samantha Beck Previs, Angela Ploysangngam, Guy G Kennedy, Jennifer F McAdow, Sarah M Tremble, Marcus A Zimmermann, Marilyn J Cipolla, Alicia M Ebert, Aaron N Johnson, Christina A Gurnett, Michael J Previs, David M Warshaw\",\"doi\":\"10.1085/jgp.202413604\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>Myosin-binding protein H (MyBP-H) is a component of the vertebrate skeletal muscle sarcomere with sequence and domain homology to myosin-binding protein C (MyBP-C). Whereas skeletal muscle isoforms of MyBP-C (fMyBP-C, sMyBP-C) modulate muscle contractility via interactions with actin thin filaments and myosin motors within the muscle sarcomere \\\"C-zone,\\\" MyBP-H has no known function. This is in part due to MyBP-H having limited expression in adult fast-twitch muscle and no known involvement in muscle disease. Quantitative proteomics reported here reveal that MyBP-H is highly expressed in prenatal rat fast-twitch muscles and larval zebrafish, suggesting a conserved role in muscle development and prompting studies to define its function. We take advantage of the genetic control of the zebrafish model and a combination of structural, functional, and biophysical techniques to interrogate the role of MyBP-H. Transgenic, FLAG-tagged MyBP-H or fMyBP-C both localize to the C-zones in larval myofibers, whereas genetic depletion of endogenous MyBP-H or fMyBP-C leads to increased accumulation of the other, suggesting competition for C-zone binding sites. Does MyBP-H modulate contractility in the C-zone? Globular domains critical to MyBP-C's modulatory functions are absent from MyBP-H, suggesting that MyBP-H may be functionally silent. However, our results suggest an active role. In vitro motility experiments indicate MyBP-H shares MyBP-C's capacity as a molecular \\\"brake.\\\" These results provide new insights and raise questions about the role of the C-zone during muscle development.</p>\",\"PeriodicalId\":54828,\"journal\":{\"name\":\"Journal of General Physiology\",\"volume\":\"156 12\",\"pages\":\"\"},\"PeriodicalIF\":3.3000,\"publicationDate\":\"2024-12-02\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11461142/pdf/\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Journal of General Physiology\",\"FirstCategoryId\":\"3\",\"ListUrlMain\":\"https://doi.org/10.1085/jgp.202413604\",\"RegionNum\":2,\"RegionCategory\":\"医学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"2024/10/7 0:00:00\",\"PubModel\":\"Epub\",\"JCR\":\"Q1\",\"JCRName\":\"PHYSIOLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of General Physiology","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1085/jgp.202413604","RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2024/10/7 0:00:00","PubModel":"Epub","JCR":"Q1","JCRName":"PHYSIOLOGY","Score":null,"Total":0}
Functional role of myosin-binding protein H in thick filaments of developing vertebrate fast-twitch skeletal muscle.
Myosin-binding protein H (MyBP-H) is a component of the vertebrate skeletal muscle sarcomere with sequence and domain homology to myosin-binding protein C (MyBP-C). Whereas skeletal muscle isoforms of MyBP-C (fMyBP-C, sMyBP-C) modulate muscle contractility via interactions with actin thin filaments and myosin motors within the muscle sarcomere "C-zone," MyBP-H has no known function. This is in part due to MyBP-H having limited expression in adult fast-twitch muscle and no known involvement in muscle disease. Quantitative proteomics reported here reveal that MyBP-H is highly expressed in prenatal rat fast-twitch muscles and larval zebrafish, suggesting a conserved role in muscle development and prompting studies to define its function. We take advantage of the genetic control of the zebrafish model and a combination of structural, functional, and biophysical techniques to interrogate the role of MyBP-H. Transgenic, FLAG-tagged MyBP-H or fMyBP-C both localize to the C-zones in larval myofibers, whereas genetic depletion of endogenous MyBP-H or fMyBP-C leads to increased accumulation of the other, suggesting competition for C-zone binding sites. Does MyBP-H modulate contractility in the C-zone? Globular domains critical to MyBP-C's modulatory functions are absent from MyBP-H, suggesting that MyBP-H may be functionally silent. However, our results suggest an active role. In vitro motility experiments indicate MyBP-H shares MyBP-C's capacity as a molecular "brake." These results provide new insights and raise questions about the role of the C-zone during muscle development.
期刊介绍:
General physiology is the study of biological mechanisms through analytical investigations, which decipher the molecular and cellular mechanisms underlying biological function at all levels of organization.
The mission of Journal of General Physiology (JGP) is to publish mechanistic and quantitative molecular and cellular physiology of the highest quality, to provide a best-in-class author experience, and to nurture future generations of independent researchers. The major emphasis is on physiological problems at the cellular and molecular level.