Myofiber necroptosis promotes muscle stem cell proliferation via releasing Tenascin-C during regeneration

Cell Res. 2020 Dec;30(12):1063-1077. doi: 10.1038/s41422-020-00393-6. Epub 2020 Aug 24.

Abstract

Necroptosis, a form of programmed cell death, is characterized by the loss of membrane integrity and release of intracellular contents, the execution of which depends on the membrane-disrupting activity of the Mixed Lineage Kinase Domain-Like protein (MLKL) upon its phosphorylation. Here we found myofibers committed MLKL-dependent necroptosis after muscle injury. Either pharmacological inhibition of the necroptosis upstream kinase Receptor Interacting Protein Kinases 1 (RIPK1) or genetic ablation of MLKL expression in myofibers led to significant muscle regeneration defects. By releasing factors into the muscle stem cell (MuSC) microenvironment, necroptotic myofibers facilitated muscle regeneration. Tenascin-C (TNC), released by necroptotic myofibers, was found to be critical for MuSC proliferation. The temporary expression of TNC in myofibers is tightly controlled by necroptosis; the extracellular release of TNC depends on necroptotic membrane rupture. TNC directly activated EGF receptor (EGFR) signaling pathway in MuSCs through its N-terminus assembly domain together with the EGF-like domain. These findings indicate that necroptosis plays a key role in promoting MuSC proliferation to facilitate muscle regeneration.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Line
  • Cell Proliferation / drug effects
  • ErbB Receptors / metabolism
  • Humans
  • Mice
  • Models, Biological
  • Muscle Fibers, Skeletal / drug effects
  • Muscle Fibers, Skeletal / metabolism
  • Muscle Fibers, Skeletal / pathology*
  • Necroptosis* / drug effects
  • Recombinant Proteins / pharmacology
  • Regeneration* / drug effects
  • Stem Cells / drug effects
  • Stem Cells / pathology*
  • Tenascin / metabolism*

Substances

  • Recombinant Proteins
  • Tenascin
  • ErbB Receptors