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ESCO1 and CTCF enable formation of long chromatin loops by protecting cohesinSTAG1 from WAPL

View ORCID ProfileGordana Wutz, View ORCID ProfileRene Ladurner, Brian St. Hilaire, Roman Stocsits, View ORCID ProfileKota Nagasaka, Benoit Pignard, Adrian Sanborn, Wen Tang, View ORCID ProfileCsilla Várnai, View ORCID ProfileMiroslav Ivanov, View ORCID ProfileStefan Schoenfelder, Petra van der Lelij, Xingfan Huang, Gerhard Dürnberger, View ORCID ProfileElisabeth Roitinger, View ORCID ProfileKarl Mechtler, Iain F. Davidson, Peter Fraser, View ORCID ProfileErez Lieberman Aiden, View ORCID ProfileJan-Michael Peters
doi: https://doi.org/10.1101/779058
Gordana Wutz
1Research Institute of Molecular Pathology (IMP), Vienna Biocentre (VBC), Campus-Vienna-Biocentre 1, 1030 Vienna, Austria
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  • ORCID record for Gordana Wutz
Rene Ladurner
1Research Institute of Molecular Pathology (IMP), Vienna Biocentre (VBC), Campus-Vienna-Biocentre 1, 1030 Vienna, Austria
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Brian St. Hilaire
2The Center for Genome Architecture, Baylor College of Medicine, Houston, TX 77030, USA
3Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA
4Center for Theoretical Biological Physics, Rice University, Houston, TX 77030, USA
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Roman Stocsits
1Research Institute of Molecular Pathology (IMP), Vienna Biocentre (VBC), Campus-Vienna-Biocentre 1, 1030 Vienna, Austria
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Kota Nagasaka
1Research Institute of Molecular Pathology (IMP), Vienna Biocentre (VBC), Campus-Vienna-Biocentre 1, 1030 Vienna, Austria
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Benoit Pignard
1Research Institute of Molecular Pathology (IMP), Vienna Biocentre (VBC), Campus-Vienna-Biocentre 1, 1030 Vienna, Austria
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Adrian Sanborn
2The Center for Genome Architecture, Baylor College of Medicine, Houston, TX 77030, USA
6Department of Computer Science, Stanford University, Stanford, CA 94305, USA
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Wen Tang
1Research Institute of Molecular Pathology (IMP), Vienna Biocentre (VBC), Campus-Vienna-Biocentre 1, 1030 Vienna, Austria
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Csilla Várnai
5Nuclear Dynamics Programme, The Babraham Institute, Babraham Research Campus, Cambridge CB22 3AT, United Kingdom
12Centre for Computational Biology, University of Birmingham, B15 2TT Birmingham, UK
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Miroslav Ivanov
1Research Institute of Molecular Pathology (IMP), Vienna Biocentre (VBC), Campus-Vienna-Biocentre 1, 1030 Vienna, Austria
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Stefan Schoenfelder
5Nuclear Dynamics Programme, The Babraham Institute, Babraham Research Campus, Cambridge CB22 3AT, United Kingdom
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Petra van der Lelij
1Research Institute of Molecular Pathology (IMP), Vienna Biocentre (VBC), Campus-Vienna-Biocentre 1, 1030 Vienna, Austria
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Xingfan Huang
2The Center for Genome Architecture, Baylor College of Medicine, Houston, TX 77030, USA
8Departments of Computer Science and Computational and Applied Mathematics, Rice University, Houston, TX 77030, USA
9Departments of Computer Science and Genome Sciences, University of Washington, Seattle, WA 98195, USA
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Gerhard Dürnberger
7Institute of Molecular Biotechnology, Vienna Biocentre (VBC), Vienna, Austria
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Elisabeth Roitinger
7Institute of Molecular Biotechnology, Vienna Biocentre (VBC), Vienna, Austria
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  • ORCID record for Elisabeth Roitinger
Karl Mechtler
1Research Institute of Molecular Pathology (IMP), Vienna Biocentre (VBC), Campus-Vienna-Biocentre 1, 1030 Vienna, Austria
7Institute of Molecular Biotechnology, Vienna Biocentre (VBC), Vienna, Austria
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Iain F. Davidson
1Research Institute of Molecular Pathology (IMP), Vienna Biocentre (VBC), Campus-Vienna-Biocentre 1, 1030 Vienna, Austria
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Peter Fraser
5Nuclear Dynamics Programme, The Babraham Institute, Babraham Research Campus, Cambridge CB22 3AT, United Kingdom
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Erez Lieberman Aiden
2The Center for Genome Architecture, Baylor College of Medicine, Houston, TX 77030, USA
3Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA
4Center for Theoretical Biological Physics, Rice University, Houston, TX 77030, USA
8Departments of Computer Science and Computational and Applied Mathematics, Rice University, Houston, TX 77030, USA
10Broad Institute of MIT and Harvard, Cambridge, MA 02139, USA
11Shanghai Institute for Advanced Immunochemical Studies, Shanghai Tech University, Shanghai, China
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  • For correspondence: peters@imp.ac.at erez@erez.com
Jan-Michael Peters
1Research Institute of Molecular Pathology (IMP), Vienna Biocentre (VBC), Campus-Vienna-Biocentre 1, 1030 Vienna, Austria
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  • For correspondence: peters@imp.ac.at erez@erez.com
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Abstract

Eukaryotic genomes are folded into loops. It is thought that these are formed by cohesin complexes via extrusion, either until loop expansion is arrested by CTCF or until cohesin is removed from DNA by WAPL. Although WAPL limits cohesin’s chromatin residence time to minutes, it has been reported that some loops exist for hours. How these loops can persist is unknown. We show that during G1-phase, mammalian cells contain acetylated cohesinSTAG1 which binds chromatin for hours, whereas cohesinSTAG2 binds chromatin for minutes. Our results indicate that CTCF and the acetyltransferase ESCO1 protect a subset of cohesinSTAG1 complexes from WAPL, thereby enable formation of long and presumably long-lived loops, and that ESCO1, like CTCF, contributes to boundary formation in chromatin looping. Our data are consistent with a model of nested loop extrusion, in which acetylated cohesinSTAG1 forms stable loops between CTCF sites, demarcating the boundaries of more transient cohesinSTAG2 extrusion activity.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted September 23, 2019.
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ESCO1 and CTCF enable formation of long chromatin loops by protecting cohesinSTAG1 from WAPL
Gordana Wutz, Rene Ladurner, Brian St. Hilaire, Roman Stocsits, Kota Nagasaka, Benoit Pignard, Adrian Sanborn, Wen Tang, Csilla Várnai, Miroslav Ivanov, Stefan Schoenfelder, Petra van der Lelij, Xingfan Huang, Gerhard Dürnberger, Elisabeth Roitinger, Karl Mechtler, Iain F. Davidson, Peter Fraser, Erez Lieberman Aiden, Jan-Michael Peters
bioRxiv 779058; doi: https://doi.org/10.1101/779058
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ESCO1 and CTCF enable formation of long chromatin loops by protecting cohesinSTAG1 from WAPL
Gordana Wutz, Rene Ladurner, Brian St. Hilaire, Roman Stocsits, Kota Nagasaka, Benoit Pignard, Adrian Sanborn, Wen Tang, Csilla Várnai, Miroslav Ivanov, Stefan Schoenfelder, Petra van der Lelij, Xingfan Huang, Gerhard Dürnberger, Elisabeth Roitinger, Karl Mechtler, Iain F. Davidson, Peter Fraser, Erez Lieberman Aiden, Jan-Michael Peters
bioRxiv 779058; doi: https://doi.org/10.1101/779058

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