IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-39846-y.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-39846-y
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-39846-y?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. 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.
    2. 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.
    3. 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.
    4. 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.
    5. 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.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Fei Sun & Nourhan Nashat Ali & Daniela Londoño-Vásquez & Constantine A. Simintiras & Huanyu Qiao & M. Sofia Ortega & Yuksel Agca & Masashi Takahashi & Rocío M. Rivera & Andrew M. Kelleher & Peter Suto, 2024. "Increased DNA damage in full-grown oocytes is correlated with diminished autophagy activation," Nature Communications, Nature, vol. 15(1), pages 1-20, December.

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Laura A. Murray-Nerger & Clarisel Lozano & Eric M. Burton & Yifei Liao & Nathan A. Ungerleider & Rui Guo & Benjamin E. Gewurz, 2024. "The nucleic acid binding protein SFPQ represses EBV lytic reactivation by promoting histone H1 expression," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    2. Sora Yoon & Aditi Chandra & Golnaz Vahedi, 2022. "Stripenn detects architectural stripes from chromatin conformation data using computer vision," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    3. Yangmian Yuan & Yu Fan & Yihao Zhou & Rong Qiu & Wei Kang & Yu Liu & Yuchen Chen & Chenyu Wang & Jiajian Shi & Chengyu Liu & Yangkai Li & Min Wu & Kun Huang & Yong Liu & Ling Zheng, 2023. "Linker histone variant H1.2 is a brake on white adipose tissue browning," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    4. Rina Hirano & Haruhiko Ehara & Tomoya Kujirai & Tamami Uejima & Yoshimasa Takizawa & Shun-ichi Sekine & Hitoshi Kurumizaka, 2022. "Structural basis of RNA polymerase II transcription on the chromatosome containing linker histone H1," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    5. Ko Sato & Amarjeet Kumar & Keisuke Hamada & Chikako Okada & Asako Oguni & Ayumi Machiyama & Shun Sakuraba & Tomohiro Nishizawa & Osamu Nureki & Hidetoshi Kono & Kazuhiro Ogata & Toru Sengoku, 2021. "Structural basis of the regulation of the normal and oncogenic methylation of nucleosomal histone H3 Lys36 by NSD2," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    6. Hikaru Hayashi & Sayaka Seki & Takeshi Tomita & Masayoshi Kato & Norihiro Ashihara & Tokuhiro Chano & Hideki Sanjo & Miwa Kawade & Chenhui Yan & Hiroki Sakai & Hidenori Tomida & Miyuki Tanaka & Mai Iw, 2025. "Synthetic short mRNA prevents metastasis via innate-adaptive immunity," Nature Communications, Nature, vol. 16(1), pages 1-16, December.
    7. Michelle Dietzen & Haoran Zhai & Olivia Lucas & Oriol Pich & Christopher Barrington & Wei-Ting Lu & Sophia Ward & Yanping Guo & Robert E. Hynds & Simone Zaccaria & Charles Swanton & Nicholas McGranaha, 2024. "Replication timing alterations are associated with mutation acquisition during breast and lung cancer evolution," Nature Communications, Nature, vol. 15(1), pages 1-23, December.
    8. Xiangwei Li & Thomas Delerue & Ben Schöttker & Bernd Holleczek & Eva Grill & Annette Peters & Melanie Waldenberger & Barbara Thorand & Hermann Brenner, 2022. "Derivation and validation of an epigenetic frailty risk score in population-based cohorts of older adults," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    9. Andreas Herchenröther & Stefanie Gossen & Tobias Friedrich & Alexander Reim & Nadine Daus & Felix Diegmüller & Jörg Leers & Hakimeh Moghaddas Sani & Sarah Gerstner & Leah Schwarz & Inga Stellmacher & , 2023. "The H2A.Z and NuRD associated protein HMG20A controls early head and heart developmental transcription programs," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    10. Hao A. Duong & Kenkichi Baba & Jason P. DeBruyne & Alec J. Davidson & Christopher Ehlen & Michael Powell & Gianluca Tosini, 2024. "Environmental circadian disruption re-writes liver circadian proteomes," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    11. Ramachandran Prakasam & Angela Bonadiman & Roberta Andreotti & Emanuela Zuccaro & Davide Dalfovo & Caterina Marchioretti & Debasmita Tripathy & Gianluca Petris & Eric N. Anderson & Alice Migazzi & Lau, 2023. "LSD1/PRMT6-targeting gene therapy to attenuate androgen receptor toxic gain-of-function ameliorates spinobulbar muscular atrophy phenotypes in flies and mice," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    12. Li Guo & Cheng Hu & Yang Liu & Xiaoyu Chen & Deli Song & Runling Shen & Zhanzhen Liu & Xudong Jia & Qinfen Zhang & Yuanzhu Gao & Zhezhi Deng & Tao Zuo & Jun Hu & Wenbo Zhu & Jing Cai & Guangmei Yan & , 2023. "Directed natural evolution generates a next-generation oncolytic virus with a high potency and safety profile," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    13. Alon Diament & Tamir Tuller, 2015. "Improving 3D Genome Reconstructions Using Orthologous and Functional Constraints," PLOS Computational Biology, Public Library of Science, vol. 11(5), pages 1-22, May.
    14. Cecilia Pessoa Rodrigues & Aindrila Chatterjee & Meike Wiese & Thomas Stehle & Witold Szymanski & Maria Shvedunova & Asifa Akhtar, 2021. "Histone H4 lysine 16 acetylation controls central carbon metabolism and diet-induced obesity in mice," Nature Communications, Nature, vol. 12(1), pages 1-21, December.
    15. Tianshi Feng & Xuemei Zhao & Ping Gu & Wah Yang & Cunchuan Wang & Qingyu Guo & Qiaoyun Long & Qing Liu & Ying Cheng & Jin Li & Cynthia Kwan Yui Cheung & Donghai Wu & Xinyu Kong & Yong Xu & Dewei Ye & , 2022. "Adipocyte-derived lactate is a signalling metabolite that potentiates adipose macrophage inflammation via targeting PHD2," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    16. Elisa Bellucci & Andrea Benazzo & Chunming Xu & Elena Bitocchi & Monica Rodriguez & Saleh Alseekh & Valerio Di Vittori & Tania Gioia & Kerstin Neumann & Gaia Cortinovis & Giulia Frascarelli & Ester Mu, 2023. "Selection and adaptive introgression guided the complex evolutionary history of the European common bean," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    17. Jiayin Peng & Lili Han & Biao Liu & Jiawen Song & Yuang Wang & Kunpeng Wang & Qian Guo & XinYan Liu & Yu Li & Jujin Zhang & Wenqing Wu & Sheng Li & Xin Fu & Cheng-le Zhuang & Weikang Zhang & Shengbao , 2023. "Gli1 marks a sentinel muscle stem cell population for muscle regeneration," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    18. Brent S. Perlman & Noah Burget & Yeqiao Zhou & Gregory W. Schwartz & Jelena Petrovic & Zora Modrusan & Robert B. Faryabi, 2024. "Enhancer-promoter hubs organize transcriptional networks promoting oncogenesis and drug resistance," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    19. Elisa Setten & Alessandra Castagna & Josué Manik Nava-Sedeño & Jonathan Weber & Roberta Carriero & Andreas Reppas & Valery Volk & Jessica Schmitz & Wilfried Gwinner & Haralampos Hatzikirou & Friedrich, 2022. "Understanding fibrosis pathogenesis via modeling macrophage-fibroblast interplay in immune-metabolic context," Nature Communications, Nature, vol. 13(1), pages 1-22, December.
    20. Andrea Zanetti & Gwendal Dujardin & Lucas Fares-Taie & Jeanne Amiel & Jérôme E. Roger & Isabelle Audo & Matthieu P. Robert & Pierre David & Vincent Jung & Nicolas Goudin & Ida Chiara Guerrera & Stépha, 2024. "GPATCH11 variants cause mis-splicing and early-onset retinal dystrophy with neurological impairment," Nature Communications, Nature, vol. 15(1), pages 1-20, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39846-y. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.