Histone H3 serine-57 is a CHK1 substrate whose phosphorylation affects DNA repair

Nikolaos Parisis, Pablo D. Dans, Muhammad Jbara, Balveer Singh, Diane Schausi-Tiffoche, Diego Molina-Serrano, Isabelle Brun-Heath, Denisa Hendrychová, Suman Kumar Maity, Diana Buitrago, Rafael Lema, Thiziri Nait Achour, Simona Giunta, Michael Girardot, Nicolas Talarek, Valérie Rofidal, Katerina Danezi, Damien Coudreuse, Marie-Noëlle Prioleau, Robert Feil, Modesto Orozco, Ashraf Brik, Pei-Yun Jenny Wu, Liliana Krasinska () and Daniel Fisher ()
Additional contact information
Nikolaos Parisis: IGMM, CNRS, INSERM, University of Montpellier
Pablo D. Dans: IRB Barcelona, BIST
Muhammad Jbara: Schulich Faculty of Chemistry, Technion Israel Institute of Technology
Balveer Singh: IGDR, CNRS, University of Rennes
Diane Schausi-Tiffoche: IGDR, CNRS, University of Rennes
Diego Molina-Serrano: IGDR, CNRS, University of Rennes
Isabelle Brun-Heath: IRB Barcelona, BIST
Denisa Hendrychová: IGMM, CNRS, INSERM, University of Montpellier
Suman Kumar Maity: Schulich Faculty of Chemistry, Technion Israel Institute of Technology
Diana Buitrago: IRB Barcelona, BIST
Rafael Lema: IRB Barcelona, BIST
Thiziri Nait Achour: IGMM, CNRS, INSERM, University of Montpellier
Simona Giunta: The Rockefeller University
Michael Girardot: IGMM, CNRS, INSERM, University of Montpellier
Nicolas Talarek: IGMM, CNRS, INSERM, University of Montpellier
Valérie Rofidal: University of Montpellier
Katerina Danezi: IGMM, CNRS, INSERM, University of Montpellier
Damien Coudreuse: IGDR, CNRS, University of Rennes
Marie-Noëlle Prioleau: University Paris Diderot
Robert Feil: IGMM, CNRS, INSERM, University of Montpellier
Modesto Orozco: IRB Barcelona, BIST
Ashraf Brik: Schulich Faculty of Chemistry, Technion Israel Institute of Technology
Pei-Yun Jenny Wu: IGDR, CNRS, University of Rennes
Liliana Krasinska: IGMM, CNRS, INSERM, University of Montpellier
Daniel Fisher: IGMM, CNRS, INSERM, University of Montpellier

Nature Communications, 2023, vol. 14, issue 1, 1-20

Abstract: Abstract Histone post-translational modifications promote a chromatin environment that controls transcription, DNA replication and repair, but surprisingly few phosphorylations have been documented. We report the discovery of histone H3 serine-57 phosphorylation (H3S57ph) and show that it is implicated in different DNA repair pathways from fungi to vertebrates. We identified CHK1 as a major human H3S57 kinase, and disrupting or constitutively mimicking H3S57ph had opposing effects on rate of recovery from replication stress, 53BP1 chromatin binding, and dependency on RAD52. In fission yeast, mutation of all H3 alleles to S57A abrogated DNA repair by both non-homologous end-joining and homologous recombination, while cells with phospho-mimicking S57D alleles were partly compromised for both repair pathways, presented aberrant Rad52 foci and were strongly sensitised to replication stress. Mechanistically, H3S57ph loosens DNA-histone contacts, increasing nucleosome mobility, and interacts with H3K56. Our results suggest that dynamic phosphorylation of H3S57 is required for DNA repair and recovery from replication stress, opening avenues for investigating the role of this modification in other DNA-related processes.

Date: 2023
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DOI: 10.1038/s41467-023-40843-4

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