The transcriptional co-repressor TLE3 regulates myogenic differentiation by repressing the activity of the MyoD transcription factor

J Biol Chem. 2017 Aug 4;292(31):12885-12894. doi: 10.1074/jbc.M116.774570. Epub 2017 Jun 12.

Abstract

Satellite cells are skeletal muscle stem cells that provide myonuclei for postnatal muscle growth, maintenance, and repair/regeneration in adults. Normally, satellite cells are mitotically quiescent, but they are activated in response to muscle injury, in which case they proliferate extensively and exhibit up-regulated expression of the transcription factor MyoD, a master regulator of myogenesis. MyoD forms a heterodimer with E proteins through their basic helix-loop-helix domain, binds to E boxes in the genome and thereby activates transcription at muscle-specific promoters. The central role of MyoD in muscle differentiation has increased interest in finding potential MyoD regulators. Here we identified transducin-like enhancer of split (TLE3), one of the Groucho/TLE family members, as a regulator of MyoD function during myogenesis. TLE3 was expressed in activated and proliferative satellite cells in which increased TLE3 levels suppressed myogenic differentiation, and, conversely, reduced TLE3 levels promoted myogenesis with a concomitant increase in proliferation. We found that, via its glutamine- and serine/proline-rich domains, TLE3 interferes with MyoD function by disrupting the association between the basic helix-loop-helix domain of MyoD and E proteins. Our findings indicate that TLE3 participates in skeletal muscle homeostasis by dampening satellite cell differentiation via repression of MyoD transcriptional activity.

Keywords: MyoD; TLE; basic helix-loop-helix (bHLH) transcription factor; mesenchymal stem cells (MSCs); myogenesis; skeletal muscle.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Activating Transcription Factor 3 / chemistry
  • Activating Transcription Factor 3 / genetics
  • Activating Transcription Factor 3 / metabolism
  • Animals
  • Cell Proliferation
  • Cells, Cultured
  • Co-Repressor Proteins / antagonists & inhibitors
  • Co-Repressor Proteins / chemistry
  • Co-Repressor Proteins / genetics
  • Co-Repressor Proteins / metabolism*
  • Gene Deletion
  • Gene Expression Regulation, Developmental*
  • Helix-Loop-Helix Motifs
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Muscle Development*
  • Muscle Fibers, Skeletal / cytology
  • Muscle Fibers, Skeletal / metabolism*
  • MyoD Protein / antagonists & inhibitors*
  • MyoD Protein / chemistry
  • MyoD Protein / genetics
  • MyoD Protein / metabolism
  • Myoblasts / cytology
  • Myoblasts / metabolism*
  • Peptide Fragments / antagonists & inhibitors
  • Peptide Fragments / chemistry
  • Peptide Fragments / genetics
  • Peptide Fragments / metabolism
  • Protein Interaction Domains and Motifs
  • Protein Multimerization
  • RNA Interference
  • Recombinant Fusion Proteins / chemistry
  • Recombinant Fusion Proteins / metabolism
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / metabolism
  • Satellite Cells, Skeletal Muscle / cytology
  • Satellite Cells, Skeletal Muscle / metabolism*

Substances

  • Activating Transcription Factor 3
  • Atf3 protein, mouse
  • Co-Repressor Proteins
  • MyoD Protein
  • MyoD1 myogenic differentiation protein
  • Peptide Fragments
  • Recombinant Fusion Proteins
  • Recombinant Proteins
  • Tle3 protein, mouse