IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-41316-4.html
   My bibliography  Save this article

Context-dependent perturbations in chromatin folding and the transcriptome by cohesin and related factors

Author

Listed:
  • Ryuichiro Nakato

    (The University of Tokyo)

  • Toyonori Sakata

    (The University of Tokyo
    Karolinska Institutet, Department of Biosciences and Nutrition, Biomedicum
    Karolinska Institutet, Department of Cell and Molecular Biology, Biomedicum)

  • Jiankang Wang

    (Hunan University)

  • Luis Augusto Eijy Nagai

    (The University of Tokyo)

  • Yuya Nagaoka

    (The University of Tokyo)

  • Gina Miku Oba

    (The University of Tokyo)

  • Masashige Bando

    (The University of Tokyo)

  • Katsuhiko Shirahige

    (The University of Tokyo
    Karolinska Institutet, Department of Biosciences and Nutrition, Biomedicum
    Karolinska Institutet, Department of Cell and Molecular Biology, Biomedicum)

Abstract

Cohesin regulates gene expression through context-specific chromatin folding mechanisms such as enhancer–promoter looping and topologically associating domain (TAD) formation by cooperating with factors such as cohesin loaders and the insulation factor CTCF. We developed a computational workflow to explore how three-dimensional (3D) structure and gene expression are regulated collectively or individually by cohesin and related factors. The main component is CustardPy, by which multi-omics datasets are compared systematically. To validate our methodology, we generated 3D genome, transcriptome, and epigenome data before and after depletion of cohesin and related factors and compared the effects of depletion. We observed diverse effects on the 3D genome and transcriptome, and gene expression changes were correlated with the splitting of TADs caused by cohesin loss. We also observed variations in long-range interactions across TADs, which correlated with their epigenomic states. These computational tools and datasets will be valuable for 3D genome and epigenome studies.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41316-4
    DOI: 10.1038/s41467-023-41316-4
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-41316-4
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-41316-4?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. Antonio Tedeschi & Gordana Wutz & Sébastien Huet & Markus Jaritz & Annelie Wuensche & Erika Schirghuber & Iain Finley Davidson & Wen Tang & David A. Cisneros & Venugopal Bhaskara & Tomoko Nishiyama & , 2013. "Wapl is an essential regulator of chromatin structure and chromosome segregation," Nature, Nature, vol. 501(7468), pages 564-568, September.
    2. Jesse R. Dixon & Siddarth Selvaraj & Feng Yue & Audrey Kim & Yan Li & Yin Shen & Ming Hu & Jun S. Liu & Bing Ren, 2012. "Topological domains in mammalian genomes identified by analysis of chromatin interactions," Nature, Nature, vol. 485(7398), pages 376-380, May.
    3. Georg A. Busslinger & Roman R. Stocsits & Petra van der Lelij & Elin Axelsson & Antonio Tedeschi & Niels Galjart & Jan-Michael Peters, 2017. "Cohesin is positioned in mammalian genomes by transcription, CTCF and Wapl," Nature, Nature, vol. 544(7651), pages 503-507, April.
    4. Patricia Garcia & Rita Fernandez-Hernandez & Ana Cuadrado & Ignacio Coca & Antonio Gomez & Maria Maqueda & Ana Latorre-Pellicer & Beatriz Puisac & Feliciano J. Ramos & Juan Sandoval & Manel Esteller &, 2021. "Disruption of NIPBL/Scc2 in Cornelia de Lange Syndrome provokes cohesin genome-wide redistribution with an impact in the transcriptome," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    5. Kerstin S. Wendt & Keisuke Yoshida & Takehiko Itoh & Masashige Bando & Birgit Koch & Erika Schirghuber & Shuichi Tsutsumi & Genta Nagae & Ko Ishihara & Tsuyoshi Mishiro & Kazuhide Yahata & Fumio Imamo, 2008. "Cohesin mediates transcriptional insulation by CCCTC-binding factor," Nature, Nature, vol. 451(7180), pages 796-801, February.
    6. Jesse R. Dixon & Inkyung Jung & Siddarth Selvaraj & Yin Shen & Jessica E. Antosiewicz-Bourget & Ah Young Lee & Zhen Ye & Audrey Kim & Nisha Rajagopal & Wei Xie & Yarui Diao & Jing Liang & Huimin Zhao , 2015. "Chromatin architecture reorganization during stem cell differentiation," Nature, Nature, vol. 518(7539), pages 331-336, February.
    7. Elphège P. Nora & Laura Caccianini & Geoffrey Fudenberg & Kevin So & Vasumathi Kameswaran & Abigail Nagle & Alec Uebersohn & Bassam Hajj & Agnès Le Saux & Antoine Coulon & Leonid A. Mirny & Katherine , 2020. "Molecular basis of CTCF binding polarity in genome folding," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
    8. Yuanlong Liu & Luca Nanni & Stephanie Sungalee & Marie Zufferey & Daniele Tavernari & Marco Mina & Stefano Ceri & Elisa Oricchio & Giovanni Ciriello, 2021. "Systematic inference and comparison of multi-scale chromatin sub-compartments connects spatial organization to cell phenotypes," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
    9. Wibke Schwarzer & Nezar Abdennur & Anton Goloborodko & Aleksandra Pekowska & Geoffrey Fudenberg & Yann Loe-Mie & Nuno A Fonseca & Wolfgang Huber & Christian H. Haering & Leonid Mirny & Francois Spitz, 2017. "Two independent modes of chromatin organization revealed by cohesin removal," Nature, Nature, vol. 551(7678), pages 51-56, November.
    10. Nicholas T. Crump & Erica Ballabio & Laura Godfrey & Ross Thorne & Emmanouela Repapi & Jon Kerry & Marta Tapia & Peng Hua & Christoffer Lagerholm & Panagis Filippakopoulos & James O. J. Davies & Thoma, 2021. "BET inhibition disrupts transcription but retains enhancer-promoter contact," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    11. Matthew A. Deardorff & Masashige Bando & Ryuichiro Nakato & Erwan Watrin & Takehiko Itoh & Masashi Minamino & Katsuya Saitoh & Makiko Komata & Yuki Katou & Dinah Clark & Kathryn E. Cole & Elfride De B, 2012. "HDAC8 mutations in Cornelia de Lange syndrome affect the cohesin acetylation cycle," Nature, Nature, vol. 489(7415), pages 313-317, September.
    12. Emily Crane & Qian Bian & Rachel Patton McCord & Bryan R. Lajoie & Bayly S. Wheeler & Edward J. Ralston & Satoru Uzawa & Job Dekker & Barbara J. Meyer, 2015. "Condensin-driven remodelling of X chromosome topology during dosage compensation," Nature, Nature, vol. 523(7559), pages 240-244, July.
    13. Timothy J. Stasevich & Yoko Hayashi-Takanaka & Yuko Sato & Kazumitsu Maehara & Yasuyuki Ohkawa & Kumiko Sakata-Sogawa & Makio Tokunaga & Takahiro Nagase & Naohito Nozaki & James G. McNally & Hiroshi K, 2014. "Regulation of RNA polymerase II activation by histone acetylation in single living cells," Nature, Nature, vol. 516(7530), pages 272-275, December.
    14. 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)

    Citations

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


    Cited by:

    1. Jiakai Hou & Yanjun Wei & Jing Zou & Roshni Jaffery & Long Sun & Shaoheng Liang & Ningbo Zheng & Ashley M. Guerrero & Nicholas A. Egan & Ritu Bohat & Si Chen & Caishang Zheng & Xiaobo Mao & S. Stephen, 2024. "Integrated multi-omics analyses identify anti-viral host factors and pathways controlling SARS-CoV-2 infection," Nature Communications, Nature, vol. 15(1), pages 1-14, 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. Julia Minderjahn & Alexander Fischer & Konstantin Maier & Karina Mendes & Margit Nuetzel & Johanna Raithel & Hanna Stanewsky & Ute Ackermann & Robert Månsson & Claudia Gebhard & Michael Rehli, 2022. "Postmitotic differentiation of human monocytes requires cohesin-structured chromatin," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    2. 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.
    3. Louisa Hill & Gordana Wutz & Markus Jaritz & Hiromi Tagoh & Lesly Calderón & Jan-Michael Peters & Anton Goloborodko & Meinrad Busslinger, 2023. "Igh and Igk loci use different folding principles for V gene recombination due to distinct chromosomal architectures of pro-B and pre-B cells," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    4. Jiankang Wang & Masashige Bando & Katsuhiko Shirahige & Ryuichiro Nakato, 2022. "Large-scale multi-omics analysis suggests specific roles for intragenic cohesin in transcriptional regulation," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    5. Hossein Salari & Geneviève Fourel & Daniel Jost, 2024. "Transcription regulates the spatio-temporal dynamics of genes through micro-compartmentalization," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    6. 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.
    7. Li-Hsin Chang & Sourav Ghosh & Andrea Papale & Jennifer M. Luppino & Mélanie Miranda & Vincent Piras & Jéril Degrouard & Joanne Edouard & Mallory Poncelet & Nathan Lecouvreur & Sébastien Bloyer & Amél, 2023. "Multi-feature clustering of CTCF binding creates robustness for loop extrusion blocking and Topologically Associating Domain boundaries," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    8. Jia-Yong Zhong & Longjian Niu & Zhuo-Bin Lin & Xin Bai & Ying Chen & Feng Luo & Chunhui Hou & Chuan-Le Xiao, 2023. "High-throughput Pore-C reveals the single-allele topology and cell type-specificity of 3D genome folding," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    9. Yufan Zhou & Tian Li & Lavanya Choppavarapu & Kun Fang & Shili Lin & Victor X. Jin, 2024. "Integration of scHi-C and scRNA-seq data defines distinct 3D-regulated and biological-context dependent cell subpopulations," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    10. Jingxuan Xu & Xiang Xu & Dandan Huang & Yawen Luo & Lin Lin & Xuemei Bai & Yang Zheng & Qian Yang & Yu Cheng & An Huang & Jingyi Shi & Xiaochen Bo & Jin Gu & Hebing Chen, 2024. "A comprehensive benchmarking with interpretation and operational guidance for the hierarchy of topologically associating domains," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    11. Yi Liao & Juntao Wang & Zhangsheng Zhu & Yuanlong Liu & Jinfeng Chen & Yongfeng Zhou & Feng Liu & Jianjun Lei & Brandon S. Gaut & Bihao Cao & J. J. Emerson & Changming Chen, 2022. "The 3D architecture of the pepper genome and its relationship to function and evolution," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    12. Anna-Maria Göbel & Sida Zhou & Zhidan Wang & Sofia Tzourtzou & Axel Himmelbach & Shiwei Zheng & Mónica Pradillo & Chang Liu & Hua Jiang, 2024. "Mutations of PDS5 genes enhance TAD-like domain formation in Arabidopsis thaliana," Nature Communications, Nature, vol. 15(1), pages 1-8, 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. Jacques Serizay & Cyril Matthey-Doret & Amaury Bignaud & Lyam Baudry & Romain Koszul, 2024. "Orchestrating chromosome conformation capture analysis with Bioconductor," Nature Communications, Nature, vol. 15(1), pages 1-9, December.
    15. Tomas Zelenka & Antonios Klonizakis & Despina Tsoukatou & Dionysios-Alexandros Papamatheakis & Sören Franzenburg & Petros Tzerpos & Ioannis-Rafail Tzonevrakis & George Papadogkonas & Manouela Kapsetak, 2022. "The 3D enhancer network of the developing T cell genome is shaped by SATB1," Nature Communications, Nature, vol. 13(1), pages 1-22, December.
    16. Shuai Liu & Yaqiang Cao & Kairong Cui & Qingsong Tang & Keji Zhao, 2022. "Hi-TrAC reveals division of labor of transcription factors in organizing chromatin loops," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    17. Thais Ealo & Victor Sanchez-Gaya & Patricia Respuela & María Muñoz-San Martín & Elva Martin-Batista & Endika Haro & Alvaro Rada-Iglesias, 2024. "Cooperative insulation of regulatory domains by CTCF-dependent physical insulation and promoter competition," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    18. Markus Götz & Olivier Messina & Sergio Espinola & Jean-Bernard Fiche & Marcelo Nollmann, 2022. "Multiple parameters shape the 3D chromatin structure of single nuclei at the doc locus in Drosophila," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    19. Judith H. I. Haarhuis & Robin H. Weide & Vincent A. Blomen & Koen D. Flach & Hans Teunissen & Laureen Willems & Thijn R. Brummelkamp & Benjamin D. Rowland & Elzo Wit, 2022. "A Mediator-cohesin axis controls heterochromatin domain formation," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    20. Zhen-Hui Wang & Xin-Feng Wang & Tianyuan Lu & Ming-Rui Li & Peng Jiang & Jing Zhao & Si-Tong Liu & Xue-Qi Fu & Jonathan F. Wendel & Yves Peer & Bao Liu & Lin-Feng Li, 2022. "Reshuffling of the ancestral core-eudicot genome shaped chromatin topology and epigenetic modification in Panax," Nature Communications, Nature, vol. 13(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:14:y:2023:i:1:d:10.1038_s41467-023-41316-4. 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.