The SWI/SNF subunit/tumor suppressor BAF47/INI1 is essential in cell cycle arrest upon skeletal muscle terminal differentiation

PLoS One. 2014 Oct 1;9(10):e108858. doi: 10.1371/journal.pone.0108858. eCollection 2014.

Abstract

Myogenic terminal differentiation is a well-orchestrated process starting with permanent cell cycle exit followed by muscle-specific genetic program activation. Individual SWI/SNF components have been involved in muscle differentiation. Here, we show that the master myogenic differentiation factor MyoD interacts with more than one SWI/SNF subunit, including the catalytic subunit BRG1, BAF53a and the tumor suppressor BAF47/INI1. Downregulation of each of these SWI/SNF subunits inhibits skeletal muscle terminal differentiation but, interestingly, at different differentiation steps and extents. BAF53a downregulation inhibits myotube formation but not the expression of early muscle-specific genes. BRG1 or BAF47 downregulation disrupt both proliferation and differentiation genetic programs expression. Interestingly, BRG1 and BAF47 are part of the SWI/SNF remodeling complex as well as the N-CoR-1 repressor complex in proliferating myoblasts. However, our data show that, upon myogenic differentiation, BAF47 shifts in favor of N-CoR-1 complex. Finally, BRG1 and BAF47 are well-known tumor suppressors but, strikingly, only BAF47 seems essential in the myoblasts irreversible cell cycle exit. Together, our data unravel differential roles for SWI/SNF subunits in muscle differentiation, with BAF47 playing a dual role both in the permanent cell cycle exit and in the regulation of muscle-specific genes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Cycle Checkpoints / genetics*
  • Cell Differentiation / genetics*
  • Chromosomal Proteins, Non-Histone / genetics*
  • Chromosomal Proteins, Non-Histone / metabolism
  • DNA-Binding Proteins / genetics*
  • DNA-Binding Proteins / metabolism
  • HeLa Cells
  • Humans
  • Muscle Development / genetics*
  • Muscle, Skeletal / cytology
  • Muscle, Skeletal / metabolism*
  • MyoD Protein / genetics
  • MyoD Protein / metabolism
  • SMARCB1 Protein
  • Transcription Factors / genetics*
  • Transcription Factors / metabolism

Substances

  • Chromosomal Proteins, Non-Histone
  • DNA-Binding Proteins
  • MyoD Protein
  • SMARCB1 Protein
  • SMARCB1 protein, human
  • Transcription Factors

Grants and funding

This work was supported by the: Association Française contre les Myopathies Téléthon (Grant N° 16557, http://www.afm-telethon.fr/association); Agence Nationale de la Recherche (http://www.agence-nationale-recherche.fr/), Fondation Bettencourt- Schueller (Grant 2006; http://www.fondationbs.org/); Fondation Association pour la Recherche sur le Cancer (Fondation ARC, Grant N° SFI20121205835; http://www.fondation-arc.org/); Groupement des Entreprises Françaises pour la Lutte contre le Cancer (GEFLUC, Grant 2011; http://www.gefluc.org/); Institut National du Cancer (INCa; grant N° INCa_5879); CNRS; Université Paris Diderot (Appel d'Offre Projets Puridisciplinaires Paris Diderot 2011–2012) and the "Who Am I?" Laboratory of Excellence #ANR-11- LABX-0071 funded by the French Government through its "Investments for the Future" program operated by the ANR under grant #ANR-11-IDEX-0005-01. OA was recipient of a Univ Paris Diderot and DIM Stem-Pôle fellowships, VB was recipient of the Ministère de la Recherche PhD fellowship, Fondation ARC and FRM fellowships and JP was recipient of the Ministère de la Recherche PhD fellowship and Fondation ARC fellowship. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. The authors do not have any conflict of interest regarding the manuscript.