PR-DUB maintains the expression of critical genes through FOXK1/2- and ASXL1/2/3-dependent recruitment to chromatin and H2AK119ub1 deubiquitination

Genome Res. 2020 Aug;30(8):1119-1130. doi: 10.1101/gr.261016.120. Epub 2020 Aug 3.

Abstract

Polycomb group proteins are important for maintaining gene expression patterns and cell identity in metazoans. The mammalian Polycomb repressive deubiquitinase (PR-DUB) complexes catalyze removal of monoubiquitination on lysine 119 of histone H2A (H2AK119ub1) through a multiprotein core comprised of BAP1, HCFC1, FOXK1/2, and OGT in combination with either of ASXL1, 2, or 3. Mutations in PR-DUB components are frequent in cancer. However, mechanistic understanding of PR-DUB function in gene regulation is limited. Here, we show that BAP1 is dependent on the ASXL proteins and FOXK1/2 in facilitating gene activation across the genome. Although PR-DUB was previously shown to cooperate with PRC2, we observed minimal overlap and functional interaction between BAP1 and PRC2 in embryonic stem cells. Collectively, these results demonstrate that PR-DUB, by counteracting accumulation of H2AK119ub1, maintains chromatin in an optimal configuration ensuring expression of genes important for general functions such as cell metabolism and homeostasis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Proliferation / genetics
  • Cells, Cultured
  • Chromatin / genetics
  • Chromatin / metabolism*
  • Deubiquitinating Enzymes / genetics
  • Deubiquitinating Enzymes / metabolism*
  • Forkhead Transcription Factors / metabolism
  • Gene Expression Regulation / genetics*
  • Gene Knockout Techniques
  • Histones / metabolism*
  • Mice
  • Mice, Inbred BALB C
  • Mice, Knockout
  • Mouse Embryonic Stem Cells
  • Polycomb-Group Proteins / genetics
  • Polycomb-Group Proteins / metabolism*
  • Repressor Proteins / metabolism
  • Tumor Suppressor Proteins / metabolism
  • Ubiquitin Thiolesterase / metabolism

Substances

  • ASXL2 protein, mouse
  • Asxl1 protein, mouse
  • BAP1 protein, mouse
  • Chromatin
  • Forkhead Transcription Factors
  • FoxK2 protein, mouse
  • Foxk1 protein, mouse
  • Histones
  • Polycomb-Group Proteins
  • Repressor Proteins
  • Tumor Suppressor Proteins
  • Deubiquitinating Enzymes
  • Ubiquitin Thiolesterase