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

J Gen Physiol. 2024 Dec 2;156(12):e202413604. doi: 10.1085/jgp.202413604. Epub 2024 Oct 7.

Abstract

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.

MeSH terms

  • Actin Cytoskeleton / metabolism
  • Animals
  • Carrier Proteins* / genetics
  • Carrier Proteins* / metabolism
  • Muscle Contraction / physiology
  • Muscle Development / physiology
  • Muscle Fibers, Fast-Twitch* / metabolism
  • Muscle Fibers, Fast-Twitch* / physiology
  • Rats
  • Sarcomeres / metabolism
  • Zebrafish Proteins / genetics
  • Zebrafish Proteins / metabolism
  • Zebrafish*

Substances

  • Carrier Proteins
  • myosin-binding protein C
  • Zebrafish Proteins