Contractile acto-myosin network on nuclear envelope remnants positions human chromosomes for mitosis

  1. Alexander JR Booth
  2. Zuojun Yue
  3. John K Eykelenboom
  4. Tom Stiff
  5. GW Gant Luxton
  6. Helfrid Hochegger
  7. Tomoyuki U Tanaka  Is a corresponding author
  1. University of Dundee, United Kingdom
  2. University of Sussex, United Kingdom
  3. University of Minnesota, United States

Abstract

To ensure proper segregation during mitosis, chromosomes must be efficiently captured by spindle microtubules and subsequently aligned on the mitotic spindle. The efficacy of chromosome interaction with the spindle can be influenced by how widely chromosomes are scattered in space. Here, we quantify chromosome-scattering volume (CSV) and find that it is reduced soon after nuclear envelope breakdown (NEBD) in human cells. The CSV reduction occurs primarily independently of microtubules and is therefore not an outcome of interactions between chromosomes and the spindle. We find that, prior to NEBD, an acto-myosin network is assembled in a LINC complex-dependent manner on the cytoplasmic surface of the nuclear envelope. This acto-myosin network remains on nuclear envelope remnants soon after NEBD, and its myosin-II-mediated contraction reduces CSV and facilitates timely chromosome congression and correct segregation. Thus we find a novel mechanism that positions chromosomes in early mitosis to ensure efficient and correct chromosome-spindle interactions.

Data availability

A source data file has been provided for each figure, and it contains the source data at individual time points in individual cells where relevant.

Article and author information

Author details

  1. Alexander JR Booth

    School of Life Sciences, University of Dundee, Dundee, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3320-7919
  2. Zuojun Yue

    School of Life Sciences, University of Dundee, Dundee, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. John K Eykelenboom

    School of Life Sciences, University of Dundee, Dundee, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Tom Stiff

    Genome Damage and Stability Centre, University of Sussex, Brighton, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. GW Gant Luxton

    College of Biological Sciences, University of Minnesota, Minneapolis, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6180-8906
  6. Helfrid Hochegger

    Genome Damage and Stability Centre, University of Sussex, Brighton, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  7. Tomoyuki U Tanaka

    School of Life Sciences, University of Dundee, Dundee, United Kingdom
    For correspondence
    t.tanaka@dundee.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9886-5947

Funding

Wellcome (096535/Z/11/Z)

  • Tomoyuki U Tanaka

Wellcome (097945/Z/11/Z)

  • Tomoyuki U Tanaka

Wellcome (208401/Z/17/Z)

  • Tomoyuki U Tanaka

Cancer Research UK (C28206/A114499)

  • Helfrid Hochegger

Medical Research Council (MR/K015869/1)

  • Tomoyuki U Tanaka

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

Reviewing Editor

  1. Silke Hauf, Virginia Tech, United States

Version history

  1. Received: March 15, 2019
  2. Accepted: July 1, 2019
  3. Accepted Manuscript published: July 2, 2019 (version 1)
  4. Accepted Manuscript updated: July 3, 2019 (version 2)
  5. Version of Record published: July 16, 2019 (version 3)

Copyright

© 2019, Booth 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. Alexander JR Booth
  2. Zuojun Yue
  3. John K Eykelenboom
  4. Tom Stiff
  5. GW Gant Luxton
  6. Helfrid Hochegger
  7. Tomoyuki U Tanaka
(2019)
Contractile acto-myosin network on nuclear envelope remnants positions human chromosomes for mitosis
eLife 8:e46902.
https://doi.org/10.7554/eLife.46902

Share this article

https://doi.org/10.7554/eLife.46902

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