Recycling of modified H2A-H2B provides short-term memory of chromatin states

Cell. 2023 Mar 2;186(5):1050-1065.e19. doi: 10.1016/j.cell.2023.01.007. Epub 2023 Feb 6.

Abstract

Chromatin landscapes are disrupted during DNA replication and must be restored faithfully to maintain genome regulation and cell identity. The histone H3-H4 modification landscape is restored by parental histone recycling and modification of new histones. How DNA replication impacts on histone H2A-H2B is currently unknown. Here, we measure H2A-H2B modifications and H2A.Z during DNA replication and across the cell cycle using quantitative genomics. We show that H2AK119ub1, H2BK120ub1, and H2A.Z are recycled accurately during DNA replication. Modified H2A-H2B are segregated symmetrically to daughter strands via POLA1 on the lagging strand, but independent of H3-H4 recycling. Post-replication, H2A-H2B modification and variant landscapes are quickly restored, and H2AK119ub1 guides accurate restoration of H3K27me3. This work reveals epigenetic transmission of parental H2A-H2B during DNA replication and identifies cross talk between H3-H4 and H2A-H2B modifications in epigenome propagation. We propose that rapid short-term memory of recycled H2A-H2B modifications facilitates restoration of stable H3-H4 chromatin states.

Keywords: DNA replication; H2A; H2A.Z; H2B; chromatin; histone PTM cross talk; histone recycling; polycomb; post-translational modifications; ubiquitination.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Cycle
  • Chromatin*
  • DNA Replication
  • Histones / metabolism
  • Memory, Short-Term*
  • Mice
  • Nucleosomes
  • Rabbits

Substances

  • Chromatin
  • Histones
  • Nucleosomes