NoRC Recruitment by H2A.X Deposition at rRNA Gene Promoter Limits Embryonic Stem Cell Proliferation

Cell Rep. 2018 May 8;23(6):1853-1866. doi: 10.1016/j.celrep.2018.04.023.

Abstract

Embryonic stem cells (ESCs) display an abbreviated cell cycle, resulting in a short doubling time and rapid proliferation. The histone variant H2A.X is critical for proliferation of stem cells, although mechanistic insights have remained obscure. Here, we show that H2A.X defines the rate of mouse ESC proliferation independently of the DNA damage response pathway, and it associates with three major chromatin-modifying complexes. Our functional and biochemical analyses demonstrate that H2A.X-associated factors mediate the H2A.X-dependent effect on ESC proliferation and involve the nucleolar remodeling complex (NoRC). A specific H2A.X deposition at rDNA promoters determines the chromatin recruitment of the NoRC, histone modifications, the rRNA transcription, and the rate of proliferation. Collectively, our results suggest that NoRC assembly by H2A.X deposition at rRNA promoters silences transcription, and this represents an important regulatory component for ESC proliferation.

Keywords: BRG1; G1; H2A.X; SNF2H; SPT16; TIP5; cell cycle; cell cycle arrest; proliferation; rDNA; rRNA; ribosomal biogenesis; stem cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Nucleolus / metabolism*
  • Cell Proliferation
  • Chromatin Assembly and Disassembly
  • Gene Silencing
  • Heterochromatin / metabolism
  • Histones / metabolism*
  • Mice
  • Mouse Embryonic Stem Cells / cytology*
  • Mouse Embryonic Stem Cells / metabolism*
  • Multiprotein Complexes / metabolism*
  • Phosphorylation
  • Promoter Regions, Genetic / genetics*
  • Protein Binding
  • Protein Interaction Mapping

Substances

  • H2AX protein, mouse
  • Heterochromatin
  • Histones
  • Multiprotein Complexes