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Histone H1 facilitates restoration of H3K27me3 during DNA replication by chromatin compaction

Author

Listed:
  • Cuifang Liu

    (CAS Center for Excellence in Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences)

  • Juan Yu

    (CAS Center for Excellence in Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences)

  • Aoqun Song

    (CAS Center for Excellence in Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Min Wang

    (CAS Center for Excellence in Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences)

  • Jiansen Hu

    (Institute of Biophysics, Chinese Academy of Science)

  • Ping Chen

    (CAS Center for Excellence in Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences
    Capital Medical University)

  • Jicheng Zhao

    (CAS Center for Excellence in Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences)

  • Guohong Li

    (CAS Center for Excellence in Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences
    University of Chinese Academy of Sciences
    Wuhan University)

Abstract

During cell renewal, epigenetic information needs to be precisely restored to maintain cell identity and genome integrity following DNA replication. The histone mark H3K27me3 is essential for the formation of facultative heterochromatin and the repression of developmental genes in embryonic stem cells. However, how the restoration of H3K27me3 is precisely achieved following DNA replication is still poorly understood. Here we employ ChOR-seq (Chromatin Occupancy after Replication) to monitor the dynamic re-establishment of H3K27me3 on nascent DNA during DNA replication. We find that the restoration rate of H3K27me3 is highly correlated with dense chromatin states. In addition, we reveal that the linker histone H1 facilitates the rapid post-replication restoration of H3K27me3 on repressed genes and the restoration rate of H3K27me3 on nascent DNA is greatly compromised after partial depletion of H1. Finally, our in vitro biochemical experiments demonstrate that H1 facilitates the propagation of H3K27me3 by PRC2 through compacting chromatin. Collectively, our results indicate that H1-mediated chromatin compaction facilitates the propagation and restoration of H3K27me3 after DNA replication.

Suggested Citation

  • Cuifang Liu & Juan Yu & Aoqun Song & Min Wang & Jiansen Hu & Ping Chen & Jicheng Zhao & Guohong Li, 2023. "Histone H1 facilitates restoration of H3K27me3 during DNA replication by chromatin compaction," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39846-y
    DOI: 10.1038/s41467-023-39846-y
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    1. Benjamin D. Pope & Tyrone Ryba & Vishnu Dileep & Feng Yue & Weisheng Wu & Olgert Denas & Daniel L. Vera & Yanli Wang & R. Scott Hansen & Theresa K. Canfield & Robert E. Thurman & Yong Cheng & Günhan G, 2014. "Topologically associating domains are stable units of replication-timing regulation," Nature, Nature, vol. 515(7527), pages 402-405, November.
    2. Michael A. Willcockson & Sean E. Healton & Cary N. Weiss & Boris A. Bartholdy & Yair Botbol & Laxmi N. Mishra & Dhruv S. Sidhwani & Tommy J. Wilson & Hugo B. Pinto & Maxim I. Maron & Karin A. Skalina , 2021. "H1 histones control the epigenetic landscape by local chromatin compaction," Nature, Nature, vol. 589(7841), pages 293-298, January.
    3. Nevin Yusufova & Andreas Kloetgen & Matt Teater & Adewola Osunsade & Jeannie M. Camarillo & Christopher R. Chin & Ashley S. Doane & Bryan J. Venters & Stephanie Portillo-Ledesma & Joseph Conway & Jude, 2021. "Histone H1 loss drives lymphoma by disrupting 3D chromatin architecture," Nature, Nature, vol. 589(7841), pages 299-305, January.
    4. Raphael Margueron & Neil Justin & Katsuhito Ohno & Miriam L. Sharpe & Jinsook Son & William J. Drury III & Philipp Voigt & Stephen R. Martin & William R. Taylor & Valeria De Marco & Vincenzo Pirrotta , 2009. "Role of the polycomb protein EED in the propagation of repressive histone marks," Nature, Nature, vol. 461(7265), pages 762-767, October.
    5. Yingyao Zhou & Bin Zhou & Lars Pache & Max Chang & Alireza Hadj Khodabakhshi & Olga Tanaseichuk & Christopher Benner & Sumit K. Chanda, 2019. "Metascape provides a biologist-oriented resource for the analysis of systems-level datasets," Nature Communications, Nature, vol. 10(1), pages 1-10, December.
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