1. Cell Biology
  2. Chromosomes and Gene Expression

Cohesin and condensin extrude DNA loops in a cell-cycle dependent manner

  1. Stefan Golfier
  2. Thomas Quail
  3. Hiroshi Kimura
  4. Jan Brugués  Is a corresponding author
  1. Max Planck Institute of Molecular Cell Biology and Genetics, Germany
  2. Tokyo Institute of Technology, Japan
https://doi.org/10.7554/eLife.53885
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  1. Stefan Golfier
  2. Thomas Quail
  3. Hiroshi Kimura
  4. Jan Brugués
(2020)
Cohesin and condensin extrude DNA loops in a cell-cycle dependent manner
eLife 9:e53885.
https://doi.org/10.7554/eLife.53885
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Abstract

Loop extrusion by structural maintenance of chromosomes complexes (SMCs) has been proposed as a mechanism to organize chromatin in interphase and metaphase. However, the requirements for chromatin organization in these cell cycle phases are different, and it is unknown whether loop extrusion dynamics and the complexes that extrude DNA also differ. Here, we used Xenopus egg extracts to reconstitute and image loop extrusion of single DNA molecules during the cell cycle. We show that loops form in both metaphase and interphase, but with distinct dynamic properties. Condensin extrudes DNA loops non-symmetrically in metaphase, whereas cohesin extrudes loops symmetrically in interphase. Our data show that loop extrusion is a general mechanism underlying DNA organization, with dynamic and structural properties that are biochemically regulated during the cell cycle.

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All data generated or analysed during this study are included in the manuscript.

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Author details

  1. Stefan Golfier

    Molecular Cell Biology and Genetics, Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.

  2. Thomas Quail

    Molecular Cell Biology and Genetics, Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.

  3. Hiroshi Kimura

    Graduate School of Bioscience and Biotechnology, Tokyo Institute of Technology, Yokohama, Japan
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0854-083X

  4. Jan Brugués

    Molecular Cell Biology and Genetics, Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
    For correspondence
    brugues@mpi-cbg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6731-4130

Funding

Human Frontier Science Program (CDA00074/2014)

  • Jan Brugués

European Molecular Biology Organization (ALTF 1456-2015)

  • Thomas Quail

ELBE fellowship

  • Stefan Golfier

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: Animal experimentation: All animals were handled according to the directive 2010/63/EU on the protection of animals used for scientific purposes, and the german animal welfare law under the license document number DD24-5131/367/9 from the Landesdirektion Sachsen (Dresden) - Section 24D.

Copyright

© 2020, Golfier et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Stefan Golfier
  2. Thomas Quail
  3. Hiroshi Kimura
  4. Jan Brugués
(2020)
Cohesin and condensin extrude DNA loops in a cell-cycle dependent manner
eLife 9:e53885.
https://doi.org/10.7554/eLife.53885

Share this article

https://doi.org/10.7554/eLife.53885

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Further reading

    1. Chromosomes and Gene Expression
    2. Physics of Living Systems

    The interplay between asymmetric and symmetric DNA loop extrusion

    Edward J Banigan, Leonid A Mirny
    Research Advance Updated

    Chromosome compaction is essential for reliable transmission of genetic information. Experiments suggest that ∼1000-fold compaction is driven by condensin complexes that extrude chromatin loops, by progressively collecting chromatin fiber from one or both sides of the complex to form a growing loop. Theory indicates that symmetric two-sided loop extrusion can achieve such compaction, but recent single-molecule studies (Golfier et al., 2020) observed diverse dynamics of condensins that perform one-sided, symmetric two-sided, and asymmetric two-sided extrusion. We use simulations and theory to determine how these molecular properties lead to chromosome compaction. High compaction can be achieved if even a small fraction of condensins have two essential properties: a long residence time and the ability to perform two-sided (not necessarily symmetric) extrusion. In mixtures of condensins I and II, coupling two-sided extrusion and stable chromatin binding by condensin II promotes compaction. These results provide missing connections between single-molecule observations and chromosome-scale organization.