IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-36467-3.html
   My bibliography  Save this article

H2B ubiquitination recruits FACT to maintain a stable altered nucleosome state for transcriptional activation

Author

Listed:
  • Anfeng Luo

    (Capital Medical University)

  • Jingwei Kong

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Jun Chen

    (Capital Medical University)

  • Xue Xiao

    (Chinese Academy of Sciences)

  • Jie Lan

    (Institute of Biophysics, Chinese Academy of Sciences)

  • Xiaorong Li

    (Institute of Biophysics, Chinese Academy of Sciences)

  • Cuifang Liu

    (Institute of Biophysics, Chinese Academy of Sciences)

  • Peng-Ye Wang

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences
    Songshan Lake Materials Laboratory)

  • Guohong Li

    (University of Chinese Academy of Sciences
    Institute of Biophysics, Chinese Academy of Sciences)

  • Wei Li

    (Chinese Academy of Sciences
    Institute of Biophysics, Chinese Academy of Sciences
    Songshan Lake Materials Laboratory)

  • Ping Chen

    (Capital Medical University
    Institute of Biophysics, Chinese Academy of Sciences)

Abstract

Histone H2B mono-ubiquitination at lysine 120 (ubH2B) has been found to regulate transcriptional elongation by collaborating with the histone chaperone FACT (Facilitates Chromatin Transcription) and plays essential roles in chromatin-based transcriptional processes. However, the mechanism of how ubH2B directly collaborates with FACT at the nucleosome level still remains elusive. In this study, we demonstrate that ubH2B impairs the mechanical stability of the nucleosome and helps to recruit FACT by enhancing the binding of FACT on the nucleosome. FACT prefers to bind and deposit H2A-ubH2B dimers to form an intact nucleosome. Strikingly, the preferable binding of FACT on ubH2B-nucleosome greatly enhances nucleosome stability and maintains its integrity. The stable altered nucleosome state obtained by ubH2B and FACT provides a key platform for gene transcription, as revealed by genome-wide and time-course ChIP-qPCR analyses. Our findings provide mechanistic insights of how ubH2B directly collaborates with FACT to regulate nucleosome dynamics for gene transcription.

Suggested Citation

  • Anfeng Luo & Jingwei Kong & Jun Chen & Xue Xiao & Jie Lan & Xiaorong Li & Cuifang Liu & Peng-Ye Wang & Guohong Li & Wei Li & Ping Chen, 2023. "H2B ubiquitination recruits FACT to maintain a stable altered nucleosome state for transcriptional activation," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36467-3
    DOI: 10.1038/s41467-023-36467-3
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-36467-3
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-36467-3?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. Robert K. McGinty & Jaehoon Kim & Champak Chatterjee & Robert G. Roeder & Tom W. Muir, 2008. "Chemically ubiquitylated histone H2B stimulates hDot1L-mediated intranucleosomal methylation," Nature, Nature, vol. 453(7196), pages 812-816, June.
    2. Karolin Luger & Armin W. Mäder & Robin K. Richmond & David F. Sargent & Timothy J. Richmond, 1997. "Crystal structure of the nucleosome core particle at 2.8 Å resolution," Nature, Nature, vol. 389(6648), pages 251-260, September.
    3. George Orphanides & Wei-Hua Wu & William S. Lane & Michael Hampsey & Danny Reinberg, 1999. "The chromatin-specific transcription elongation factor FACT comprises human SPT16 and SSRP1 proteins," Nature, Nature, vol. 400(6741), pages 284-288, July.
    4. Yang Liu & Keda Zhou & Naifu Zhang & Hui Wei & Yong Zi Tan & Zhening Zhang & Bridget Carragher & Clinton S. Potter & Sheena D’Arcy & Karolin Luger, 2020. "FACT caught in the act of manipulating the nucleosome," Nature, Nature, vol. 577(7790), pages 426-431, January.
    Full references (including those not matched with items on IDEAS)

    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. Un Seng Chio & Eugene Palovcak & Anton A. A. Smith & Henriette Autzen & Elise N. Muñoz & Zanlin Yu & Feng Wang & David A. Agard & Jean-Paul Armache & Geeta J. Narlikar & Yifan Cheng, 2024. "Functionalized graphene-oxide grids enable high-resolution cryo-EM structures of the SNF2h-nucleosome complex without crosslinking," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    2. Namrata Kumar & Arjan F. Theil & Vera Roginskaya & Yasmin Ali & Michael Calderon & Simon C. Watkins & Ryan P. Barnes & Patricia L. Opresko & Alex Pines & Hannes Lans & Wim Vermeulen & Bennett Houten, 2022. "Global and transcription-coupled repair of 8-oxoG is initiated by nucleotide excision repair proteins," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    3. Wilfried Engl & Aliz Kunstar-Thomas & Siyi Chen & Woei Shyuan Ng & Hendrik Sielaff & Ziqing Winston Zhao, 2024. "Single-molecule imaging of SWI/SNF chromatin remodelers reveals bromodomain-mediated and cancer-mutants-specific landscape of multi-modal DNA-binding dynamics," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    4. Masaki Kikuchi & Satoshi Morita & Masatoshi Wakamori & Shin Sato & Tomomi Uchikubo-Kamo & Takehiro Suzuki & Naoshi Dohmae & Mikako Shirouzu & Takashi Umehara, 2023. "Epigenetic mechanisms to propagate histone acetylation by p300/CBP," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    5. Fritz Nagae & Yasuto Murayama & Tsuyoshi Terakawa, 2024. "Molecular mechanism of parental H3/H4 recycling at a replication fork," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    6. Zhen Hou & Frank Nightingale & Yanan Zhu & Craig MacGregor-Chatwin & Peijun Zhang, 2023. "Structure of native chromatin fibres revealed by Cryo-ET in situ," Nature Communications, Nature, vol. 14(1), pages 1-7, December.
    7. Marko Dunjić & Felix Jonas & Gilad Yaakov & Roye More & Yoav Mayshar & Yoach Rais & Ayelet-Hashahar Orenbuch & Saifeng Cheng & Naama Barkai & Yonatan Stelzer, 2023. "Histone exchange sensors reveal variant specific dynamics in mouse embryonic stem cells," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    8. Xiao Chen & Yinglu Li & Fang Zhu & Xinjing Xu & Brian Estrella & Manuel A. Pazos & John T. McGuire & Dimitris Karagiannis & Varun Sahu & Mustafo Mustafokulov & Claudio Scuoppo & Francisco J. Sánchez-R, 2023. "Context-defined cancer co-dependency mapping identifies a functional interplay between PRC2 and MLL-MEN1 complex in lymphoma," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    9. 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.
    10. Timothy A. Daugird & Yu Shi & Katie L. Holland & Hosein Rostamian & Zhe Liu & Luke D. Lavis & Joseph Rodriguez & Brian D. Strahl & Wesley R. Legant, 2024. "Correlative single molecule lattice light sheet imaging reveals the dynamic relationship between nucleosomes and the local chromatin environment," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    11. Jaeyoon Lee & Meiling Wu & James T. Inman & Gundeep Singh & Seong ha Park & Joyce H. Lee & Robert M. Fulbright & Yifeng Hong & Joshua Jeong & James M. Berger & Michelle D. Wang, 2023. "Chromatinization modulates topoisomerase II processivity," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    12. Nithya Ramakrishnan & Sibi Raj B Pillai & Ranjith Padinhateeri, 2022. "High fidelity epigenetic inheritance: Information theoretic model predicts threshold filling of histone modifications post replication," PLOS Computational Biology, Public Library of Science, vol. 18(2), pages 1-22, February.
    13. Jiayi Fan & Andrew T. Moreno & Alexander S. Baier & Joseph J. Loparo & Craig L. Peterson, 2022. "H2A.Z deposition by SWR1C involves multiple ATP-dependent steps," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    14. Shuhei Onishi & Kotone Uchiyama & Ko Sato & Chikako Okada & Shunsuke Kobayashi & Keisuke Hamada & Tomohiro Nishizawa & Osamu Nureki & Kazuhiro Ogata & Toru Sengoku, 2024. "Structure of the human Bre1 complex bound to the nucleosome," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    15. Dian Spakman & Tinka V. M. Clement & Andreas S. Biebricher & Graeme A. King & Manika I. Singh & Ian D. Hickson & Erwin J. G. Peterman & Gijs J. L. Wuite, 2022. "PICH acts as a force-dependent nucleosome remodeler," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    16. Xiaowei Xu & Shoufu Duan & Xu Hua & Zhiming Li & Richard He & Zhiguo Zhang, 2022. "Stable inheritance of H3.3-containing nucleosomes during mitotic cell divisions," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    17. Victoria S. Frisbie & Hideharu Hashimoto & Yixuan Xie & Francisca N. De Luna Vitorino & Josue Baeza & Tam Nguyen & Zhangerjiao Yuan & Janna Kiselar & Benjamin A. Garcia & Erik W. Debler, 2024. "Two DOT1 enzymes cooperatively mediate efficient ubiquitin-independent histone H3 lysine 76 tri-methylation in kinetoplastids," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    18. Shuxiang Li & Tiejun Wei & Anna R. Panchenko, 2023. "Histone variant H2A.Z modulates nucleosome dynamics to promote DNA accessibility," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    19. Samuel Schwab & Yimin Hu & Bert Erp & Marc K. M. Cajili & Marcus D. Hartmann & Birte Hernandez Alvarez & Vikram Alva & Aimee L. Boyle & Remus T. Dame, 2024. "Histones and histone variant families in prokaryotes," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    20. Joana Segura & Ofelia Díaz-Ingelmo & Belén Martínez-García & Alba Ayats-Fraile & Christoforos Nikolaou & Joaquim Roca, 2024. "Nucleosomal DNA has topological memory," Nature Communications, Nature, vol. 15(1), pages 1-10, 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_s41467-023-36467-3. 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.