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Cohesin mediates transcriptional insulation by CCCTC-binding factor

Author

Listed:
  • Kerstin S. Wendt

    (Research Institute of Molecular Pathology (I.M.P.), Dr. Bohr Gasse 7, 1030 Vienna, Austria)

  • Keisuke Yoshida

    (Graduate School of Bioscience and Biotechnology, Tokyo Institute of Technology, B2C 4259, Nagatsuta, Midori-ku, Yokohama City, Kanagawa 226-8501, Japan)

  • Takehiko Itoh

    (Research Center for Advanced Science and Technology, Mitsubishi Research Institute Inc., Chiyoda-ku, Tokyo 100-8141, Japan)

  • Masashige Bando

    (Graduate School of Bioscience and Biotechnology, Tokyo Institute of Technology, B2C 4259, Nagatsuta, Midori-ku, Yokohama City, Kanagawa 226-8501, Japan)

  • Birgit Koch

    (Research Institute of Molecular Pathology (I.M.P.), Dr. Bohr Gasse 7, 1030 Vienna, Austria)

  • Erika Schirghuber

    (Research Institute of Molecular Pathology (I.M.P.), Dr. Bohr Gasse 7, 1030 Vienna, Austria)

  • Shuichi Tsutsumi

    (Research Center for Advanced Science and Technology (RCAST), the University of Tokyo)

  • Genta Nagae

    (Research Center for Advanced Science and Technology (RCAST), the University of Tokyo)

  • Ko Ishihara

    (Institute of Molecular Embryology and Genetics Kumamoto University, 2-2-1 Honjo, Kumamoto 860-0811, Japan)

  • Tsuyoshi Mishiro

    (Institute of Molecular Embryology and Genetics Kumamoto University, 2-2-1 Honjo, Kumamoto 860-0811, Japan)

  • Kazuhide Yahata

    (Research Institute for Microbial Diseases, Osaka University, Suita, Osaka 565-0871, Japan)

  • Fumio Imamoto

    (Research Institute for Microbial Diseases, Osaka University, Suita, Osaka 565-0871, Japan)

  • Hiroyuki Aburatani

    (Research Center for Advanced Science and Technology (RCAST), the University of Tokyo)

  • Mitsuyoshi Nakao

    (Institute of Molecular Embryology and Genetics Kumamoto University, 2-2-1 Honjo, Kumamoto 860-0811, Japan)

  • Naoko Imamoto

    (Cellular Dynamics Laboratory, RIKEN, Wako, Saitama 351-0198, Japan)

  • Kazuhiro Maeshima

    (Cellular Dynamics Laboratory, RIKEN, Wako, Saitama 351-0198, Japan)

  • Katsuhiko Shirahige

    (Graduate School of Bioscience and Biotechnology, Tokyo Institute of Technology, B2C 4259, Nagatsuta, Midori-ku, Yokohama City, Kanagawa 226-8501, Japan)

  • Jan-Michael Peters

    (Research Institute of Molecular Pathology (I.M.P.), Dr. Bohr Gasse 7, 1030 Vienna, Austria)

Abstract

Cohesin complexes mediate sister-chromatid cohesion in dividing cells but may also contribute to gene regulation in postmitotic cells. How cohesin regulates gene expression is not known. Here we describe cohesin-binding sites in the human genome and show that most of these are associated with the CCCTC-binding factor (CTCF), a zinc-finger protein required for transcriptional insulation. CTCF is dispensable for cohesin loading onto DNA, but is needed to enrich cohesin at specific binding sites. Cohesin enables CTCF to insulate promoters from distant enhancers and controls transcription at the H19/IGF2 (insulin-like growth factor 2) locus. This role of cohesin seems to be independent of its role in cohesion. We propose that cohesin functions as a transcriptional insulator, and speculate that subtle deficiencies in this function contribute to ‘cohesinopathies’ such as Cornelia de Lange syndrome.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:nature:v:451:y:2008:i:7180:d:10.1038_nature06634
    DOI: 10.1038/nature06634
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    Cited by:

    1. 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.
    2. Silvia Peripolli & Leticia Meneguello & Chiara Perrod & Tanya Singh & Harshil Patel & Sazia T. Rahman & Koshiro Kiso & Peter Thorpe & Vincenzo Calvanese & Cosetta Bertoli & Robertus A. M. de Bruin, 2024. "Oncogenic c-Myc induces replication stress by increasing cohesins chromatin occupancy in a CTCF-dependent manner," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    3. Ning Qing Liu & Irene Paassen & Lars Custers & Peter Zeller & Hans Teunissen & Dilara Ayyildiz & Jiayou He & Juliane Laura Buhl & Eelco Wieger Hoving & Alexander Oudenaarden & Elzo Wit & Jarno Drost, 2023. "SMARCB1 loss activates patient-specific distal oncogenic enhancers in malignant rhabdoid tumors," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    4. Gabrielle A. Dotson & Can Chen & Stephen Lindsly & Anthony Cicalo & Sam Dilworth & Charles Ryan & Sivakumar Jeyarajan & Walter Meixner & Cooper Stansbury & Joshua Pickard & Nicholas Beckloff & Amit Su, 2022. "Deciphering multi-way interactions in the human genome," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    5. 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.
    6. Xiaofeng Dai & Wenwen Guo & Chunjun Zhan & Xiuxia Liu & Zhonghu Bai & Yankun Yang, 2015. "WDR5 Expression Is Prognostic of Breast Cancer Outcome," PLOS ONE, Public Library of Science, vol. 10(9), pages 1-15, September.
    7. Georgii Pobegalov & Lee-Ya Chu & Jan-Michael Peters & Maxim I. Molodtsov, 2023. "Single cohesin molecules generate force by two distinct mechanisms," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    8. 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.
    9. 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.
    10. 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.
    11. 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.

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