Microtubule rescue at midzone edges promotes overlap stability and prevents spindle collapse during anaphase B

  1. Manuel Lera-Ramirez  Is a corresponding author
  2. François J Nédélec  Is a corresponding author
  3. Phong T Tran  Is a corresponding author
  1. Institut Curie, France
  2. Cambridge University, United Kingdom

Abstract

During anaphase B, molecular motors slide interpolar microtubules to elongate the mitotic spindle, contributing to the separation of chromosomes. However, sliding of antiparallel microtubules reduces their overlap, which may lead to spindle breakage, unless microtubules grow to compensate sliding. How sliding and growth are coordinated is still poorly understood. In this study, we have used the fission yeast S. pombe to measure microtubule dynamics during anaphase B. We report that the coordination of microtubule growth and sliding relies on promoting rescues at the midzone edges. This makes microtubules stable from pole to midzone, while their distal parts including the plus ends alternate between assembly and disassembly. Consequently, the midzone keeps a constant length throughout anaphase, enabling sustained sliding without the need for a precise regulation of microtubule growth speed. Additionally, we found that in S. pombe, which undergoes closed mitosis, microtubule growth speed decreases when the nuclear membrane wraps around the spindle midzone.

Data availability

Source code to reproduce and analyse the simulations is deposited in github at https://github.com/manulera/simulationsLeraRamirez2021Source code to annotate and analyse kymographs is deposited in github athttps://github.com/manulera/KymoAnalyzerSource code to find spindles in microscopy images is deposited in github at https://github.com/manulera/ImageAnalysisFunctions/tree/master/detection_functions/spindleWe have uploaded the source data for all figures as comma separated values files.

The following data sets were generated

Article and author information

Author details

  1. Manuel Lera-Ramirez

    CNRS, UMR 144, Institut Curie, Paris, France
    For correspondence
    manuel.lera-ramirez@curie.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8666-9746
  2. François J Nédélec

    Sainsbury Laboratory, Cambridge University, Cambridge, United Kingdom
    For correspondence
    francois.nedelec@slcu.cam.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
  3. Phong T Tran

    CNRS, UMR 144, Institut Curie, Paris, France
    For correspondence
    phong.tran@curie.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2410-2277

Funding

H2020 Marie Skłodowska-Curie Actions (675737)

  • Manuel Lera-Ramirez

Gatsby Charitable Foundation

  • François J Nédélec

Institut National Du Cancer

  • Phong T Tran

Fondation ARC pour la Recherche sur le Cancer

  • Phong T Tran

Ligue Contre le Cancer

  • Phong T Tran

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: July 29, 2021
  2. Preprint posted: August 6, 2021 (view preprint)
  3. Accepted: March 15, 2022
  4. Accepted Manuscript published: March 16, 2022 (version 1)
  5. Version of Record published: April 19, 2022 (version 2)

Copyright

© 2022, Lera-Ramirez 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. Manuel Lera-Ramirez
  2. François J Nédélec
  3. Phong T Tran
(2022)
Microtubule rescue at midzone edges promotes overlap stability and prevents spindle collapse during anaphase B
eLife 11:e72630.
https://doi.org/10.7554/eLife.72630

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https://doi.org/10.7554/eLife.72630

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