Cavin4 interacts with Bin1 to promote T-tubule formation and stability in developing skeletal muscle

J Cell Biol. 2021 Dec 6;220(12):e201905065. doi: 10.1083/jcb.201905065. Epub 2021 Oct 11.

Abstract

The cavin proteins are essential for caveola biogenesis and function. Here, we identify a role for the muscle-specific component, Cavin4, in skeletal muscle T-tubule development by analyzing two vertebrate systems, mouse and zebrafish. In both models, Cavin4 localized to T-tubules, and loss of Cavin4 resulted in aberrant T-tubule maturation. In zebrafish, which possess duplicated cavin4 paralogs, Cavin4b was shown to directly interact with the T-tubule-associated BAR domain protein Bin1. Loss of both Cavin4a and Cavin4b caused aberrant accumulation of interconnected caveolae within the T-tubules, a fragmented T-tubule network enriched in Caveolin-3, and an impaired Ca2+ response upon mechanical stimulation. We propose a role for Cavin4 in remodeling the T-tubule membrane early in development by recycling caveolar components from the T-tubule to the sarcolemma. This generates a stable T-tubule domain lacking caveolae that is essential for T-tubule function.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing / metabolism*
  • Animals
  • Caveolae / metabolism
  • Cell Line
  • Embryo, Nonmammalian / metabolism
  • Imaging, Three-Dimensional
  • Membrane Proteins / metabolism*
  • Mice
  • Mice, Inbred C57BL
  • Muscle Fibers, Skeletal / metabolism
  • Muscle Fibers, Skeletal / ultrastructure
  • Muscle Proteins / metabolism*
  • Muscle, Skeletal / metabolism*
  • Muscle, Skeletal / ultrastructure
  • Nerve Tissue Proteins / metabolism*
  • Protein Binding
  • Sarcolemma / metabolism*
  • Sarcolemma / ultrastructure
  • Tumor Suppressor Proteins / metabolism*
  • Zebrafish / embryology
  • Zebrafish / metabolism*
  • Zebrafish Proteins / metabolism*

Substances

  • Adaptor Proteins, Signal Transducing
  • Bin1 protein, mouse
  • Cavin4 protein, mouse
  • Membrane Proteins
  • Muscle Proteins
  • Nerve Tissue Proteins
  • Tumor Suppressor Proteins
  • Zebrafish Proteins
  • bin1b protein, zebrafish
  • cavin4b protein, zebrafish