Functional role of myosin-binding protein H in thick filaments of developing vertebrate fast-twitch skeletal muscle

Mead, Andrew F.; Wood, Neil B.; Nelson, Shane R.; Palmer, Bradley M.; Yang, Lin; Previs, Samantha Beck; Ploysangngam, Angela; Kennedy, Guy G.; McAdow, Jennifer F.; Tremble, Sarah M.; Zimmermann, Marcus A.; Cipolla, Marilyn J.; Ebert, Alicia M.; Johnson, Aaron N.; Gurnett, Christina A.; Previs, Michael J.; Warshaw, David M.

doi:10.1085/jgp.202413604

Functional role of myosin-binding protein H in thick filaments of developing vertebrate fast-twitch skeletal muscle

Journal Article · Mon Oct 07 00:00:00 EDT 2024 · Journal of General Physiology

DOI:https://doi.org/10.1085/jgp.202413604· OSTI ID:2459389

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Univ. of Vermont, Burlington, VT (United States)
Brookhaven National Laboratory (BNL), Upton, NY (United States). National Synchrotron Light Source II (NSLS-II)
Univ. of Vermont, Burlington, VT (United States); Washington Univ., St. Louis, MO (United States). School of Medicine
Washington Univ., St. Louis, MO (United States). School of Medicine

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. Here, 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.

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Research Organization:: Brookhaven National Laboratory (BNL), Upton, NY (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF); USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: SC0012704

OSTI ID:: 2459389

Alternate ID(s):: OSTI ID: 2475957

Report Number(s):: BNL--226307-2024-JAAM

Journal Information:: Journal of General Physiology, Journal Name: Journal of General Physiology Journal Issue: 12 Vol. 156; ISSN 0022-1295

Publisher:: Rockefeller University PressCopyright Statement

Country of Publication:: United States

Language:: English

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