IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-35444-6.html
   My bibliography  Save this article

Functional crosstalk between the cohesin loader and chromatin remodelers

Author

Listed:
  • Sofía Muñoz

    (The Francis Crick Institute
    University of Salamanca)

  • Andrew Jones

    (The Francis Crick Institute)

  • Céline Bouchoux

    (The Francis Crick Institute)

  • Tegan Gilmore

    (The Francis Crick Institute)

  • Harshil Patel

    (The Francis Crick Institute)

  • Frank Uhlmann

    (The Francis Crick Institute)

Abstract

The cohesin complex participates in many structural and functional aspects of genome organization. Cohesin recruitment onto chromosomes requires nucleosome-free DNA and the Scc2-Scc4 cohesin loader complex that catalyzes topological cohesin loading. Additionally, the cohesin loader facilitates promoter nucleosome clearance in a yet unknown way, and it recognizes chromatin receptors such as the RSC chromatin remodeler. Here, we explore the cohesin loader-RSC interaction. Amongst multi-pronged contacts by Scc2 and Scc4, we find that Scc4 contacts a conserved patch on the RSC ATPase motor module. The cohesin loader directly stimulates in vitro nucleosome sliding by RSC, providing an explanation how it facilitates promoter nucleosome clearance. Furthermore, we observe cohesin loader interactions with a wide range of chromatin remodelers. Our results provide mechanistic insight into how the cohesin loader recognizes, as well as influences, the chromatin landscape, with implications for our understanding of human developmental disorders including Cornelia de Lange and Coffin-Siris syndromes.

Suggested Citation

  • Sofía Muñoz & Andrew Jones & Céline Bouchoux & Tegan Gilmore & Harshil Patel & Frank Uhlmann, 2022. "Functional crosstalk between the cohesin loader and chromatin remodelers," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-35444-6
    DOI: 10.1038/s41467-022-35444-6
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-35444-6
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-35444-6?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. Felix R. Wagner & Christian Dienemann & Haibo Wang & Alexandra Stützer & Dimitry Tegunov & Henning Urlaub & Patrick Cramer, 2020. "Structure of SWI/SNF chromatin remodeller RSC bound to a nucleosome," Nature, Nature, vol. 579(7799), pages 448-451, March.
    2. Sebastian Eustermann & Kevin Schall & Dirk Kostrewa & Kristina Lakomek & Mike Strauss & Manuela Moldt & Karl-Peter Hopfner, 2018. "Structural basis for ATP-dependent chromatin remodelling by the INO80 complex," Nature, Nature, vol. 556(7701), pages 386-390, April.
    3. Lucas Farnung & Seychelle M. Vos & Christoph Wigge & Patrick Cramer, 2017. "Nucleosome–Chd1 structure and implications for chromatin remodelling," Nature, Nature, vol. 550(7677), pages 539-542, October.
    4. Yan Han & Alexis A Reyes & Sara Malik & Yuan He, 2020. "Cryo-EM structure of SWI/SNF complex bound to a nucleosome," Nature, Nature, vol. 579(7799), pages 452-455, March.
    5. Yasuto Murayama & Frank Uhlmann, 2014. "Biochemical reconstitution of topological DNA binding by the cohesin ring," Nature, Nature, vol. 505(7483), pages 367-371, January.
    6. Cedric R. Clapier & Bradley R. Cairns, 2012. "Regulation of ISWI involves inhibitory modules antagonized by nucleosomal epitopes," Nature, Nature, vol. 492(7428), pages 280-284, December.
    7. Mohamed-Ali Hakimi & Daniel A. Bochar & John A. Schmiesing & Yuanshu Dong & Orr G. Barak & David W. Speicher & Kyoko Yokomori & Ramin Shiekhattar, 2002. "A chromatin remodelling complex that loads cohesin onto human chromosomes," Nature, Nature, vol. 418(6901), pages 994-998, August.
    8. Michael H. Kagey & Jamie J. Newman & Steve Bilodeau & Ye Zhan & David A. Orlando & Nynke L. van Berkum & Christopher C. Ebmeier & Jesse Goossens & Peter B. Rahl & Stuart S. Levine & Dylan J. Taatjes &, 2010. "Mediator and cohesin connect gene expression and chromatin architecture," Nature, Nature, vol. 467(7314), pages 430-435, September.
    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. Li Wang & Jiali Yu & Zishuo Yu & Qianmin Wang & Wanjun Li & Yulei Ren & Zhenguo Chen & Shuang He & Yanhui Xu, 2022. "Structure of nucleosome-bound human PBAF complex," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    2. Luka Bacic & Guillaume Gaullier & Jugal Mohapatra & Guanzhong Mao & Klaus Brackmann & Mikhail Panfilov & Glen Liszczak & Anton Sabantsev & Sebastian Deindl, 2024. "Asymmetric nucleosome PARylation at DNA breaks mediates directional nucleosome sliding by ALC1," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
    3. Dhurjhoti Saha & Solomon Hailu & Arjan Hada & Junwoo Lee & Jie Luo & Jeff A. Ranish & Yuan-chi Lin & Kyle Feola & Jim Persinger & Abhinav Jain & Bin Liu & Yue Lu & Payel Sen & Blaine Bartholomew, 2023. "The AT-hook is an evolutionarily conserved auto-regulatory domain of SWI/SNF required for cell lineage priming," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    4. 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.
    5. Melissa S Gildenberg & M Todd Washington, 2019. "Conformational flexibility of fork-remodeling helicase Rad5 shown by full-ensemble hybrid methods," PLOS ONE, Public Library of Science, vol. 14(10), pages 1-16, October.
    6. Yichen Zhong & Hakimeh Moghaddas Sani & Bishnu P. Paudel & Jason K. K. Low & Ana P. G. Silva & Stefan Mueller & Chandrika Deshpande & Santosh Panjikar & Xavier J. Reid & Max J. Bedward & Antoine M. Oi, 2022. "The role of auxiliary domains in modulating CHD4 activity suggests mechanistic commonality between enzyme families," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    7. Alexandra D’Oto & Jie Fang & Hongjian Jin & Beisi Xu & Shivendra Singh & Anoushka Mullasseril & Victoria Jones & Ahmed Abu-Zaid & Xinyu Buttlar & Bailey Cooke & Dongli Hu & Jason Shohet & Andrew J. Mu, 2021. "KDM6B promotes activation of the oncogenic CDK4/6-pRB-E2F pathway by maintaining enhancer activity in MYCN-amplified neuroblastoma," Nature Communications, Nature, vol. 12(1), pages 1-19, December.
    8. Ryuichiro Nakato & Toyonori Sakata & Jiankang Wang & Luis Augusto Eijy Nagai & Yuya Nagaoka & Gina Miku Oba & Masashige Bando & Katsuhiko Shirahige, 2023. "Context-dependent perturbations in chromatin folding and the transcriptome by cohesin and related factors," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    9. Mingyue Guo & Fengjun Yang & Lijuan Zhu & Leilei Wang & Zhichao Li & Zhenyu Qi & Vasileios Fotopoulos & Jingquan Yu & Jie Zhou, 2024. "Loss of cold tolerance is conferred by absence of the WRKY34 promoter fragment during tomato evolution," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    10. Benjamin M. Spector & Mrutyunjaya Parida & Ming Li & Christopher B. Ball & Jeffery L. Meier & Donal S. Luse & David H. Price, 2022. "Differences in RNA polymerase II complexes and their interactions with surrounding chromatin on human and cytomegalovirus genomes," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    11. Daniel Bsteh & Hagar F. Moussa & Georg Michlits & Ramesh Yelagandula & Jingkui Wang & Ulrich Elling & Oliver Bell, 2023. "Loss of cohesin regulator PDS5A reveals repressive role of Polycomb loops," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    12. Kadir Buyukcelebi & Xintong Chen & Fatih Abdula & Hoda Elkafas & Alexander James Duval & Harun Ozturk & Fidan Seker-Polat & Qiushi Jin & Ping Yin & Yue Feng & Serdar E. Bulun & Jian Jun Wei & Feng Yue, 2023. "Engineered MED12 mutations drive leiomyoma-like transcriptional and metabolic programs by altering the 3D genome compartmentalization," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    13. Dácil Alonso-Gil & Ana Cuadrado & Daniel Giménez-Llorente & Miriam Rodríguez-Corsino & Ana Losada, 2023. "Different NIPBL requirements of cohesin-STAG1 and cohesin-STAG2," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    14. Gang Ren & Wai Lim Ku & Guangzhe Ge & Jackson A. Hoffman & Jee Youn Kang & Qingsong Tang & Kairong Cui & Yong He & Yukun Guan & Bin Gao & Chengyu Liu & Trevor K. Archer & Keji Zhao, 2024. "Acute depletion of BRG1 reveals its primary function as an activator of transcription," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    15. David Flores-Solis & Irina P. Lushpinskaia & Anton A. Polyansky & Arya Changiarath & Marc Boehning & Milana Mirkovic & James Walshe & Lisa M. Pietrek & Patrick Cramer & Lukas S. Stelzl & Bojan Zagrovi, 2023. "Driving forces behind phase separation of the carboxy-terminal domain of RNA polymerase II," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    16. Ashish Kumar Singh & Tamás Schauer & Lena Pfaller & Tobias Straub & Felix Mueller-Planitz, 2021. "The biogenesis and function of nucleosome arrays," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    17. Ignacio Prusén Mota & Marta Galova & Alexander Schleiffer & Tan-Trung Nguyen & Ines Kovacikova & Carolina Farias Saad & Gabriele Litos & Tomoko Nishiyama & Juraj Gregan & Jan-Michael Peters & Peter Sc, 2024. "Sororin is an evolutionary conserved antagonist of WAPL," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    18. 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.
    19. Aditi Kaushik & Thane Than & Naomi J. Petela & Menelaos Voulgaris & Charlotte Percival & Peter Daniels & John B. Rafferty & Kim A. Nasmyth & Bin Hu, 2023. "Conformational dynamics of cohesin/Scc2 loading complex are regulated by Smc3 acetylation and ATP binding," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    20. Kwangbeom Hyun & Jihye Ahn & Hyoungmin Kim & Jihyun Kim & Yong-In Kim & Hee-Sung Park & Robert G. Roeder & J. Eugene Lee & Jaehoon Kim, 2024. "The BAF complex enhances transcription through interaction with H3K56ac in the histone globular domain," Nature Communications, Nature, vol. 15(1), pages 1-13, 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_s41467-022-35444-6. 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.