IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-35040-8.html
   My bibliography  Save this article

PICH acts as a force-dependent nucleosome remodeler

Author

Listed:
  • Dian Spakman

    (Vrije Universiteit Amsterdam)

  • Tinka V. M. Clement

    (Vrije Universiteit Amsterdam)

  • Andreas S. Biebricher

    (Vrije Universiteit Amsterdam)

  • Graeme A. King

    (Vrije Universiteit Amsterdam
    University College London)

  • Manika I. Singh

    (University of Copenhagen)

  • Ian D. Hickson

    (University of Copenhagen)

  • Erwin J. G. Peterman

    (Vrije Universiteit Amsterdam)

  • Gijs J. L. Wuite

    (Vrije Universiteit Amsterdam)

Abstract

In anaphase, any unresolved DNA entanglements between the segregating sister chromatids can give rise to chromatin bridges. To prevent genome instability, chromatin bridges must be resolved prior to cytokinesis. The SNF2 protein PICH has been proposed to play a direct role in this process through the remodeling of nucleosomes. However, direct evidence of nucleosome remodeling by PICH has remained elusive. Here, we present an in vitro single-molecule assay that mimics chromatin under tension, as is found in anaphase chromatin bridges. Applying a combination of dual-trap optical tweezers and fluorescence imaging of PICH and histones bound to a nucleosome-array construct, we show that PICH is a tension- and ATP-dependent nucleosome remodeler that facilitates nucleosome unwrapping and then subsequently slides remaining histones along the DNA. This work elucidates the role of PICH in chromatin-bridge dissolution, and might provide molecular insights into the mechanisms of related SNF2 proteins.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-35040-8
    DOI: 10.1038/s41467-022-35040-8
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-35040-8
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-35040-8?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. 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.
    2. Christian F. Nielsen & Diana Huttner & Anna H. Bizard & Seiki Hirano & Tian-Neng Li & Timea Palmai-Pallag & Victoria A. Bjerregaard & Ying Liu & Erich A. Nigg & Lily Hui-Ching Wang & Ian D. Hickson, 2015. "PICH promotes sister chromatid disjunction and co-operates with topoisomerase II in mitosis," Nature Communications, Nature, vol. 6(1), pages 1-15, December.
    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. 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.
    2. 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.
    3. 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.
    4. 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.
    5. 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.
    6. 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.
    7. 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.
    8. 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.
    9. 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.
    10. 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.
    11. 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.
    12. 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.
    13. 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.
    14. 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.
    15. 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.
    16. 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.
    17. 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.
    18. Ke Chen & Li Wang & Zishuo Yu & Jiali Yu & Yulei Ren & Qianmin Wang & Yanhui Xu, 2024. "Structure of the human TIP60 complex," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    19. Tyler M. Weaver & Nicole M. Hoitsma & Jonah J. Spencer & Lokesh Gakhar & Nicholas J. Schnicker & Bret D. Freudenthal, 2022. "Structural basis for APE1 processing DNA damage in the nucleosome," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    20. Yu Zhang & Min Ma & Meng Liu & Aiqing Sun & Xiaoyun Zheng & Kunpeng Liu & Chunmei Yin & Chuanshun Li & Cizhong Jiang & Xiaoyu Tu & Yuda Fang, 2023. "Histone H2A monoubiquitination marks are targeted to specific sites by cohesin subunits in Arabidopsis," Nature Communications, Nature, vol. 14(1), pages 1-12, 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_s41467-022-35040-8. 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.