Spectrin is a mechanoresponsive protein shaping fusogenic synapse architecture during myoblast fusion

Nat Cell Biol. 2018 Jun;20(6):688-698. doi: 10.1038/s41556-018-0106-3. Epub 2018 May 25.

Abstract

Spectrin is a membrane skeletal protein best known for its structural role in maintaining cell shape and protecting cells from mechanical damage. Here, we report that α/βH-spectrin (βH is also called karst) dynamically accumulates and dissolves at the fusogenic synapse between fusing Drosophila muscle cells, where an attacking fusion partner invades its receiving partner with actin-propelled protrusions to promote cell fusion. Using genetics, cell biology, biophysics and mathematical modelling, we demonstrate that spectrin exhibits a mechanosensitive accumulation in response to shear deformation, which is highly elevated at the fusogenic synapse. The transiently accumulated spectrin network functions as a cellular fence to restrict the diffusion of cell-adhesion molecules and a cellular sieve to constrict the invasive protrusions, thereby increasing the mechanical tension of the fusogenic synapse to promote cell membrane fusion. Our study reveals a function of spectrin as a mechanoresponsive protein and has general implications for understanding spectrin function in dynamic cellular processes.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.
  • Video-Audio Media

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Cell Fusion*
  • Cell Line
  • Cell Membrane / metabolism*
  • Cell Membrane / ultrastructure
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism*
  • Drosophila melanogaster / genetics
  • Drosophila melanogaster / metabolism*
  • Drosophila melanogaster / ultrastructure
  • Mechanotransduction, Cellular*
  • Membrane Fusion*
  • Mice
  • Microscopy, Fluorescence
  • Models, Biological
  • Myoblasts / metabolism*
  • Myoblasts / ultrastructure
  • Myoblasts, Skeletal / metabolism
  • Spectrin / genetics
  • Spectrin / metabolism*
  • Stress, Mechanical
  • Time Factors

Substances

  • Drosophila Proteins
  • kst protein, Drosophila
  • Spectrin