BUB-1 targets PP2A:B56 to regulate chromosome congression during meiosis I in C. elegans oocytes

  1. Laura Bel Borja
  2. Flavie Soubigou
  3. Samuel JP Taylor
  4. Conchita Fraguas Bringas
  5. Jacqueline Budrewicz
  6. Pablo Lara-Gonzalez
  7. Christopher G Sorensen Turpin
  8. Joshua N Bembenek
  9. Dhanya K Cheerambathur
  10. Federico Pelisch  Is a corresponding author
  1. University of Dundee, United Kingdom
  2. Ludwig Institute for Cancer Research, United States
  3. University of Tennessee, United States
  4. University of Michigan, United States
  5. University of Edinburgh, United Kingdom

Abstract

Protein Phosphatase 2A (PP2A) is a heterotrimer composed of scaffolding (A), catalytic (C), and regulatory (B) subunits. PP2A complexes with B56 subunits are targeted by Shugoshin and BUBR1 to protect centromeric cohesion and stabilise kinetochore-microtubule attachments in yeast and mouse meiosis. In C. elegans the closest BUBR1 ortholog lacks the B56-interaction domain and Shugoshin is not required for meiotic segregation. Therefore, the role of PP2A in C. elegans female meiosis is unknown. We report that PP2A is essential for meiotic spindle assembly and chromosome dynamics during C. elegans female meiosis. BUB-1 is the main chromosome-targeting factor for B56 subunits during prometaphase I. BUB-1 recruits PP2A:B56 to the chromosomes via a newly identified LxxIxE motif in a phosphorylation-dependent manner and this recruitment is important for proper chromosome congression. Our results highlight a novel mechanism for B56 recruitment, essential for recruiting a pool of PP2A involved in chromosome congression during meiosis I.

Data availability

While some time points are shown in the figures, representative movies showing all time points are provided as Supplementary Movies. The mass spectrometry proteomics data have been deposited to the ProteomeXchange Consortium via the PRIDE (Perez-Riverol et al., 2019) partner repository with the dataset identifier PXD023258.

Article and author information

Author details

  1. Laura Bel Borja

    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:" 0000-0002-8381-934X
  2. Flavie Soubigou

    School of Life Sciences, University of Dundee, Dundee, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Samuel JP Taylor

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

    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:" 0000-0001-9594-5856
  5. Jacqueline Budrewicz

    Ludwig Institute for Cancer Research, San Diego, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Pablo Lara-Gonzalez

    Ludwig Institute for Cancer Research, San Diego, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Christopher G Sorensen Turpin

    Department of Biochemistry, Cellular and Molecular Biology, University of Tennessee, Knoxville, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Joshua N Bembenek

    Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Dhanya K Cheerambathur

    Wellcome Centre for Cell Biology & Institute of Cell Biology, School of Biological Sciences, University of Edinburgh, Edinburgh, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  10. Federico Pelisch

    School of Life Sciences, University of Dundee, Dundee, United Kingdom
    For correspondence
    f.pelisch@dundee.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4575-1492

Funding

Medical Research Council (MR/R008574/1)

  • Laura Bel Borja
  • Flavie Soubigou
  • Federico Pelisch

The Wellcome (208833)

  • Dhanya K Cheerambathur

NIH Office of the Director (R01 GM074215)

  • Jacqueline Budrewicz
  • Pablo Lara-Gonzalez

NIH Office of the Director (R01 GM114471)

  • Christopher G Sorensen Turpin
  • Joshua N Bembenek

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

Reviewing Editor

  1. Jon Pines, Institute of Cancer Research Research, United Kingdom

Publication history

  1. Received: November 30, 2020
  2. Accepted: December 17, 2020
  3. Accepted Manuscript published: December 23, 2020 (version 1)
  4. Accepted Manuscript updated: December 24, 2020 (version 2)
  5. Version of Record published: January 6, 2021 (version 3)

Copyright

© 2020, Bel Borja 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. Laura Bel Borja
  2. Flavie Soubigou
  3. Samuel JP Taylor
  4. Conchita Fraguas Bringas
  5. Jacqueline Budrewicz
  6. Pablo Lara-Gonzalez
  7. Christopher G Sorensen Turpin
  8. Joshua N Bembenek
  9. Dhanya K Cheerambathur
  10. Federico Pelisch
(2020)
BUB-1 targets PP2A:B56 to regulate chromosome congression during meiosis I in C. elegans oocytes
eLife 9:e65307.
https://doi.org/10.7554/eLife.65307

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