IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-35003-z.html
   My bibliography  Save this article

Structural basis of RNA polymerase II transcription on the chromatosome containing linker histone H1

Author

Listed:
  • Rina Hirano

    (The University of Tokyo)

  • Haruhiko Ehara

    (RIKEN Center for Biosystems Dynamics Research)

  • Tomoya Kujirai

    (The University of Tokyo
    RIKEN Center for Biosystems Dynamics Research)

  • Tamami Uejima

    (RIKEN Center for Biosystems Dynamics Research)

  • Yoshimasa Takizawa

    (The University of Tokyo)

  • Shun-ichi Sekine

    (RIKEN Center for Biosystems Dynamics Research)

  • Hitoshi Kurumizaka

    (The University of Tokyo
    RIKEN Center for Biosystems Dynamics Research)

Abstract

In chromatin, linker histone H1 binds to nucleosomes, forming chromatosomes, and changes the transcription status. However, the mechanism by which RNA polymerase II (RNAPII) transcribes the DNA in the chromatosome has remained enigmatic. Here we report the cryo-electron microscopy (cryo-EM) structures of transcribing RNAPII-chromatosome complexes (forms I and II), in which RNAPII is paused at the entry linker DNA region of the chromatosome due to H1 binding. In the form I complex, the H1 bound to the nucleosome restricts the linker DNA orientation, and the exit linker DNA is captured by the RNAPII DNA binding cleft. In the form II complex, the RNAPII progresses a few bases ahead by releasing the exit linker DNA from the RNAPII cleft, and directly clashes with the H1 bound to the nucleosome. The transcription elongation factor Spt4/5 masks the RNAPII DNA binding region, and drastically reduces the H1-mediated RNAPII pausing.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-35003-z
    DOI: 10.1038/s41467-022-35003-z
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-35003-z
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-022-35003-z?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. Anton Valouev & Steven M. Johnson & Scott D. Boyd & Cheryl L. Smith & Andrew Z. Fire & Arend Sidow, 2011. "Determinants of nucleosome organization in primary human cells," Nature, Nature, vol. 474(7352), pages 516-520, June.
    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. Seychelle M. Vos & Lucas Farnung & Henning Urlaub & Patrick Cramer, 2018. "Structure of paused transcription complex Pol II–DSIF–NELF," Nature, Nature, vol. 560(7720), pages 601-606, August.
    5. C. Plaschka & M. Hantsche & C. Dienemann & C. Burzinski & J. Plitzko & P. Cramer, 2016. "Transcription initiation complex structures elucidate DNA opening," Nature, Nature, vol. 533(7603), pages 353-358, May.
    6. Thomas Schalch & Sylwia Duda & David F. Sargent & Timothy J. Richmond, 2005. "X-ray structure of a tetranucleosome and its implications for the chromatin fibre," Nature, Nature, vol. 436(7047), pages 138-141, July.
    7. 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.
    8. Matthew J. Rossi & Prashant K. Kuntala & William K. M. Lai & Naomi Yamada & Nitika Badjatia & Chitvan Mittal & Guray Kuzu & Kylie Bocklund & Nina P. Farrell & Thomas R. Blanda & Joshua D. Mairose & An, 2021. "A high-resolution protein architecture of the budding yeast genome," Nature, Nature, vol. 592(7853), pages 309-314, April.
    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. 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.
    2. 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.
    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. 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.
    5. 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.
    6. 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.
    7. 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.
    8. 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.
    9. Ji-Ping Wang & Yvonne Fondufe-Mittendorf & Liqun Xi & Guei-Feng Tsai & Eran Segal & Jonathan Widom, 2008. "Preferentially Quantized Linker DNA Lengths in Saccharomyces cerevisiae," PLOS Computational Biology, Public Library of Science, vol. 4(9), pages 1-10, September.
    10. Heeyoun Bunch & Deukyeong Kim & Masahiro Naganuma & Reiko Nakagawa & Anh Cong & Jaehyeon Jeong & Haruhiko Ehara & Hongha Vu & Jeong Ho Chang & Matthew J. Schellenberg & Shun-ichi Sekine, 2023. "ERK2-topoisomerase II regulatory axis is important for gene activation in immediate early genes," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    11. Yi Li & James Lee & Lu Bai, 2024. "DNA methylation-based high-resolution mapping of long-distance chromosomal interactions in nucleosome-depleted regions," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    12. Yan Li & Qianmin Wang & Yanhui Xu & Ze Li, 2024. "Structures of co-transcriptional RNA capping enzymes on paused transcription complex," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    13. Monica Naughtin & Zofia Haftek-Terreau & Johan Xavier & Sam Meyer & Maud Silvain & Yan Jaszczyszyn & Nicolas Levy & Vincent Miele & Mohamed Salah Benleulmi & Marc Ruff & Vincent Parissi & Cédric Vaill, 2015. "DNA Physical Properties and Nucleosome Positions Are Major Determinants of HIV-1 Integrase Selectivity," PLOS ONE, Public Library of Science, vol. 10(6), pages 1-28, June.
    14. Seina Ohe & Yuji Kubota & Kiyoshi Yamaguchi & Yusuke Takagi & Junichiro Nashimoto & Hiroko Kozuka-Hata & Masaaki Oyama & Yoichi Furukawa & Mutsuhiro Takekawa, 2022. "ERK-mediated NELF-A phosphorylation promotes transcription elongation of immediate-early genes by releasing promoter-proximal pausing of RNA polymerase II," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    15. 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.
    16. Roberto Bandiera & Rebecca E. Wagner & Thiago Britto-Borges & Christoph Dieterich & Sabine Dietmann & Susanne Bornelöv & Michaela Frye, 2021. "RN7SK small nuclear RNA controls bidirectional transcription of highly expressed gene pairs in skin," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    17. Tianbao Li & Qi Liu & Zhong Chen & Kun Fang & Furong Huang & Xueqi Fu & Qianben Wang & Victor X. Jin, 2022. "Dynamic nucleosome landscape elicits a noncanonical GATA2 pioneer model," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    18. Francesca Maggioni & Marida Bertocchi & Ettore Mosca & Rolland Reinbold & Ileana Zucchi, 2013. "Modeling chromatin fibre folding for human embryonic stem cells," Working Papers (2013-) 1301_qum, University of Bergamo, Department of Management, Economics and Quantitative Methods.
    19. 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.
    20. Jieqiong Zhang & Zhenhua Hu & Hwa Hwa Chung & Yun Tian & Kah Weng Lau & Zheng Ser & Yan Ting Lim & Radoslaw M. Sobota & Hwei Fen Leong & Benjamin Jieming Chen & Clarisse Jingyi Yeo & Shawn Ying Xuan T, 2023. "Dependency of NELF-E-SLUG-KAT2B epigenetic axis in breast cancer carcinogenesis," Nature Communications, Nature, vol. 14(1), pages 1-21, 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:13:y:2022:i:1:d:10.1038_s41467-022-35003-z. 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.