Rab5a activates IRS1 to coordinate IGF-AKT-mTOR signaling and myoblast differentiation during muscle regeneration

Cell Death Differ. 2020 Aug;27(8):2344-2362. doi: 10.1038/s41418-020-0508-1. Epub 2020 Feb 12.

Abstract

Rab5 is a master regulator for endosome biogenesis and transport while its in vivo physiological function remains elusive. Here, we find that Rab5a is upregulated in several in vivo and in vitro myogenesis models. By generating myogenic Rab5a-deficient mice, we uncover the essential roles of Rab5a in regulating skeletal muscle regeneration. We further reveal that Rab5a promotes myoblast differentiation and directly interacts with insulin receptor substrate 1 (IRS1), an essential scaffold protein for propagating IGF signaling. Rab5a interacts with IRS1 in a GTP-dependent manner and this interaction is enhanced upon IGF-1 activation and myogenic differentiation. We subsequently identify that the arginine 207 and 222 of IRS1 and tyrosine 82, 89, and 90 of Rab5a are the critical amino acid residues for mediating the association. Mechanistically, Rab5a modulates IRS1 activation by coordinating the association between IRS1 and the IGF receptor (IGFR) and regulating the intracellular membrane targeting of IRS1. Both myogenesis-induced and IGF-evoked AKT-mTOR signaling are dependent on Rab5a. Myogenic deletion of Rab5a also reduces the activation of AKT-mTOR signaling during skeletal muscle regeneration. Taken together, our study uncovers the physiological function of Rab5a in regulating muscle regeneration and delineates the novel role of Rab5a as a critical switch controlling AKT-mTOR signaling by activating IRS1.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Differentiation*
  • Cell Line
  • HEK293 Cells
  • Hindlimb / metabolism
  • Humans
  • Insulin Receptor Substrate Proteins / metabolism*
  • Insulin-Like Growth Factor I / metabolism*
  • Intracellular Membranes / metabolism
  • Mice, Inbred C57BL
  • Muscle Development / genetics
  • Muscle, Skeletal / physiology*
  • Myoblasts / cytology*
  • Myoblasts / metabolism
  • Protein Binding
  • Proto-Oncogene Proteins c-akt / metabolism*
  • RNA, Small Interfering / metabolism
  • Receptor, IGF Type 1 / metabolism
  • Regeneration / physiology*
  • Signal Transduction
  • TOR Serine-Threonine Kinases / metabolism
  • Up-Regulation / genetics
  • rab5 GTP-Binding Proteins / genetics
  • rab5 GTP-Binding Proteins / metabolism*

Substances

  • Insulin Receptor Substrate Proteins
  • RNA, Small Interfering
  • Insulin-Like Growth Factor I
  • Receptor, IGF Type 1
  • Proto-Oncogene Proteins c-akt
  • TOR Serine-Threonine Kinases
  • rab5 GTP-Binding Proteins