PML is recruited to heterochromatin during S phase and represses DAXX-mediated histone H3.3 chromatin assembly

J Cell Sci. 2019 Mar 26;132(6):jcs220970. doi: 10.1242/jcs.220970.

Abstract

The incorporation of the histone H3 variant, H3.3, into chromatin by the H3.3-specific chaperone DAXX and the ATP-dependent chromatin remodeling factor ATRX is a critical mechanism for silencing repetitive DNA. DAXX and ATRX are also components of promyelocytic nuclear bodies (PML-NBs), which have been identified as sites of H3.3 chromatin assembly. Here, we use a transgene array that can be visualized in single living cells to investigate the mechanisms that recruit PML-NB proteins (i.e. PML, DAXX, ATRX, and SUMO-1, SUMO-2 and SUMO-3) to heterochromatin and their functions in H3.3 chromatin assembly. We show that DAXX and PML are recruited to the array through distinct SUMOylation-dependent mechanisms. Additionally, PML is recruited during S phase and its depletion increases H3.3 deposition. Since this effect is abrogated when PML and DAXX are co-depleted, it is likely that PML represses DAXX-mediated H3.3 chromatin assembly. Taken together, these results suggest that, at heterochromatin, PML-NBs coordinate H3.3 chromatin assembly with DNA replication, which has important implications for understanding how transcriptional silencing is established and maintained.

Keywords: ATRX; DAXX; Histone H3.3; PML; PML nuclear body; SUMOylation.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Cell Cycle Proteins / metabolism
  • Cell Line
  • Co-Repressor Proteins / metabolism*
  • DNA Replication / physiology
  • Gene Silencing / physiology
  • HeLa Cells
  • Heterochromatin / metabolism
  • Histone Chaperones / metabolism
  • Histones / metabolism*
  • Humans
  • Molecular Chaperones / metabolism*
  • Nucleosomes / metabolism
  • Promyelocytic Leukemia Protein / metabolism*
  • S Phase / physiology*

Substances

  • Cell Cycle Proteins
  • Co-Repressor Proteins
  • DAXX protein, human
  • H3-3A protein, human
  • Heterochromatin
  • Histone Chaperones
  • Histones
  • Molecular Chaperones
  • Nucleosomes
  • Promyelocytic Leukemia Protein
  • PML protein, human