Accurate Recycling of Parental Histones Reproduces the Histone Modification Landscape during DNA Replication

Nazaret Reverón-Gómez, Cristina González-Aguilera, Kathleen R. Stewart-Morgan, Nataliya Petryk, Valentin Flury, Simona Graziano, Jens Vilstrup Johansen, Janus Schou Jakobsen, Constance Alabert, Anja Groth

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Abstract

Chromatin organization is disrupted genome-wide during DNA replication. On newly synthesized DNA, nucleosomes are assembled from new naive histones and old modified histones. It remains unknown whether the landscape of histone post-translational modifications (PTMs) is faithfully copied during DNA replication or the epigenome is perturbed. Here we develop chromatin occupancy after replication (ChOR-seq) to determine histone PTM occupancy immediately after DNA replication and across the cell cycle. We show that H3K4me3, H3K36me3, H3K79me3, and H3K27me3 positional information is reproduced with high accuracy on newly synthesized DNA through histone recycling. Quantitative ChOR-seq reveals that de novo methylation to restore H3K4me3 and H3K27me3 levels occurs across the cell cycle with mark- and locus-specific kinetics. Collectively, this demonstrates that accurate parental histone recycling preserves positional information and allows PTM transmission to daughter cells while modification of new histones gives rise to complex epigenome fluctuations across the cell cycle that could underlie cell-to-cell heterogeneity. Histone modifications are a core component of the epigenome. Reverón-Gómez et al. develop ChOR-seq to profile histone modifications after DNA replication and find that the genomic localization of modified parental histones is preserved on daughter strands while new histone modification to restore pre-replication levels follows mark- and locus-specific kinetics.

Original languageEnglish
Pages (from-to)239-249.e5
Number of pages16
JournalMolecular Cell
Volume72
Issue number2
Early online date23 Aug 2018
DOIs
Publication statusPublished - 18 Oct 2018

Keywords

  • cell cycle
  • ChOR-seq
  • chromatin replication
  • epigenetics
  • epigenome maintenance
  • H3K27me3
  • H3K4me3
  • histone modification
  • histone recycling
  • quantitative ChIP-seq

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    Reverón-Gómez, N., González-Aguilera, C., Stewart-Morgan, K. R., Petryk, N., Flury, V., Graziano, S., Johansen, J. V., Jakobsen, J. S., Alabert, C., & Groth, A. (2018). Accurate Recycling of Parental Histones Reproduces the Histone Modification Landscape during DNA Replication. Molecular Cell, 72(2), 239-249.e5. https://doi.org/10.1016/j.molcel.2018.08.010