BUB-1 promotes amphitelic chromosome biorientation via multiple activities at the kinetochore

  1. Frances Edwards
  2. Gilliane Maton
  3. Nelly Gareil
  4. Julie C Canman
  5. Julien Dumont  Is a corresponding author
  1. Institut Jacques Monod-CNRS, France
  2. Columbia University, United States

Abstract

Accurate chromosome segregation relies on bioriented amphitelic attachments of chromosomes to microtubules of the mitotic spindle, in which sister chromatids are connected to opposite spindle poles. BUB-1 is a protein of the Spindle Assembly Checkpoint (SAC) that coordinates chromosome attachment with anaphase onset. BUB-1 is also required for accurate sister chromatid segregation independently of its SAC function, but the underlying mechanism remains unclear. Here we show that, in Caenorhabditis elegans embryos, BUB-1 accelerates the establishment of non-merotelic end-on kinetochore-microtubule attachments by recruiting the RZZ complex and its downstream partner dynein-dynactin at the kinetochore. In parallel, BUB-1 limits attachment maturation by the SKA complex. This activity opposes kinetochore-microtubule attachment stabilisation promoted by CLS-2CLASP-dependent kinetochore-microtubule assembly. BUB-1 is therefore a SAC component that coordinates the function of multiple downstream kinetochore-associated proteins to ensure accurate chromosome segregation.

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

Article and author information

Author details

  1. Frances Edwards

    Cell Biology, Institut Jacques Monod-CNRS, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  2. Gilliane Maton

    Cell Biology, Institut Jacques Monod-CNRS, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Nelly Gareil

    Cell Biology, Institut Jacques Monod-CNRS, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Julie C Canman

    Department of Pathology and Cell Biology, Columbia University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8135-2072
  5. Julien Dumont

    Cell Biology, Institut Jacques Monod-CNRS, Paris, France
    For correspondence
    julien.dumont@ijm.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5312-9770

Funding

Fondation ARC pour la Recherche sur le Cancer (Doctorant en 4e année de thèse)

  • Frances Edwards

Fondation pour la Recherche Médicale (DEQ20160334869)

  • Julien Dumont

National Institutes of Health (R01GM117407)

  • Julie C Canman

Mairie de Paris (Emergence)

  • Julien Dumont

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

Copyright

© 2018, Edwards 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. Frances Edwards
  2. Gilliane Maton
  3. Nelly Gareil
  4. Julie C Canman
  5. Julien Dumont
(2018)
BUB-1 promotes amphitelic chromosome biorientation via multiple activities at the kinetochore
eLife 7:e40690.
https://doi.org/10.7554/eLife.40690

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https://doi.org/10.7554/eLife.40690