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Cohesin depleted cells rebuild functional nuclear compartments after endomitosis

View ORCID ProfileMarion Cremer, View ORCID ProfileKatharina Brandstetter, View ORCID ProfileAndreas Maiser, Suhas S P Rao, Volker Schmid, Miguel Guirao-Ortiz, Namita Mitra, Stefania Mamberti, Kyle N Klein, View ORCID ProfileDavid M Gilbert, Heinrich Leonhardt, Maria Cristina Cardoso, Erez Lieberman Aiden, Hartmann Harz, View ORCID ProfileThomas Cremer
doi: https://doi.org/10.1101/816611
Marion Cremer
1Anthropology and Human Genomics, Department Biology II, Ludwig-Maximilians-Universität München, Germany
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  • ORCID record for Marion Cremer
  • For correspondence: thomas.cremer@lrz.uni-muenchen.de
Katharina Brandstetter
2Human Biology & BioImaging, Center for Molecular Biosystems, Department Biology II, Ludwig-Maximilians-Universität München, Germany
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  • ORCID record for Katharina Brandstetter
Andreas Maiser
2Human Biology & BioImaging, Center for Molecular Biosystems, Department Biology II, Ludwig-Maximilians-Universität München, Germany
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Suhas S P Rao
3Center for Genome Architecture, Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, Texas, United States of America
4Department of Structural Biology, Stanford University School of Medicine, California, United States of America
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Volker Schmid
5BioImaging Group, Department of Statistics, Ludwig-Maximilians-Universität München, Germany
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Miguel Guirao-Ortiz
2Human Biology & BioImaging, Center for Molecular Biosystems, Department Biology II, Ludwig-Maximilians-Universität München, Germany
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Namita Mitra
3Center for Genome Architecture, Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, Texas, United States of America
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Stefania Mamberti
6Cell Biology and Epigenetics, Department of Biology, Technische Universität Darmstadt, Germany
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Kyle N Klein
7Department of Biological Science, Florida State University, Tallahassee, Florida, United States of America
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David M Gilbert
7Department of Biological Science, Florida State University, Tallahassee, Florida, United States of America
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  • ORCID record for David M Gilbert
Heinrich Leonhardt
2Human Biology & BioImaging, Center for Molecular Biosystems, Department Biology II, Ludwig-Maximilians-Universität München, Germany
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Maria Cristina Cardoso
6Cell Biology and Epigenetics, Department of Biology, Technische Universität Darmstadt, Germany
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Erez Lieberman Aiden
3Center for Genome Architecture, Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, Texas, United States of America
8Center for Theoretical Biological Physics, Rice University, Houston, Texas, United States of America
9Broad Institute of the Massachusetts Institute of Technology and Harvard University, Cambridge, Massachusetts, United States of America
10Departments of Computer Science and Computational and Applied Mathematics, Rice University, Houston, Texas, United States of America
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Hartmann Harz
2Human Biology & BioImaging, Center for Molecular Biosystems, Department Biology II, Ludwig-Maximilians-Universität München, Germany
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  • For correspondence: thomas.cremer@lrz.uni-muenchen.de
Thomas Cremer
1Anthropology and Human Genomics, Department Biology II, Ludwig-Maximilians-Universität München, Germany
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  • ORCID record for Thomas Cremer
  • For correspondence: thomas.cremer@lrz.uni-muenchen.de
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Abstract

Cohesin plays an essential role in chromatin loop extrusion, but its impact on a compartmentalized nuclear architecture, linked to nuclear functions, is debatable. Using live-cell and super-resolved 3D microscopy, we demonstrate that cohesin depleted cells pass through an endomitosis and rebuild a single multilobulated nucleus (MLN) with chromosome territories (CTs) pervaded by interchromatin channels. CTs contain chromatin domain clusters with a zonal organization of repressed chromatin domains in the interior and transcriptionally competent domains located at the periphery. Splicing speckles are located nearby within the lining channel system. These clusters form microscopically defined, active and inactive compartments, which correspond to A/B compartments, detected with ensemble Hi-C. Functionality of MLN despite continuous absence of cohesin was demonstrated by their ability to pass through S-phase with typical spatio-temporal patterns of replication domains. Evidence for structural changes of these domains compared to controls suggests that cohesin is required for their full integrity.

Competing Interest Statement

The authors have declared no competing interest.

  • Abbreviations

    3D FISH
    3D fluorescence in situ hybridization
    3D SIM
    3D structured illumination microscopy
    AID
    auxin inducible degron
    ANC / INC
    active / inactive nuclear compartment
    CT
    chromosome territory
    CD(C)
    chromatin domain (cluster)
    CTCF
    CCCTC binding factor
    DAPI
    4’,6-diamidino-2-phenylindole
    EdU
    5-Ethynyl-2’-deoxyuridine
    Hi-C
    chromosome conformation capturing combined with deep sequencing
    IC
    interchromatin compartment
    MLN
    multilobulated nucleus
    NC
    nucleosome cluster
    PBS
    phosphate buffered saline
    PBST
    phosphate buffered saline with 0.02% Tween
    PR
    perichromatin region
    RD
    replication domain
    RL
    replication labeling
    TAD
    topologically associating domain
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    Posted September 14, 2020.
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    Cohesin depleted cells rebuild functional nuclear compartments after endomitosis
    Marion Cremer, Katharina Brandstetter, Andreas Maiser, Suhas S P Rao, Volker Schmid, Miguel Guirao-Ortiz, Namita Mitra, Stefania Mamberti, Kyle N Klein, David M Gilbert, Heinrich Leonhardt, Maria Cristina Cardoso, Erez Lieberman Aiden, Hartmann Harz, Thomas Cremer
    bioRxiv 816611; doi: https://doi.org/10.1101/816611
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    Cohesin depleted cells rebuild functional nuclear compartments after endomitosis
    Marion Cremer, Katharina Brandstetter, Andreas Maiser, Suhas S P Rao, Volker Schmid, Miguel Guirao-Ortiz, Namita Mitra, Stefania Mamberti, Kyle N Klein, David M Gilbert, Heinrich Leonhardt, Maria Cristina Cardoso, Erez Lieberman Aiden, Hartmann Harz, Thomas Cremer
    bioRxiv 816611; doi: https://doi.org/10.1101/816611

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