BUB-1 and CENP-C recruit PLK-1 to control chromosome alignment and segregation during meiosis I in C. elegans oocytes
- University of Dundee, United Kingdom
- Ludwig Institute for Cancer Research, United States
- University of Edinburgh, United Kingdom
Abstract
Phosphorylation is a key post-translational modification that is utilised in many biological processes for the rapid and reversible regulation of protein localisation and activity. Polo-like kinase 1 (PLK-1) is essential for both mitotic and meiotic cell divisions, with key functions being conserved in eukaryotes. The roles and regulation of PLK-1 during mitosis have been well characterised. However, the discrete roles and regulation of PLK-1 during meiosis have remained obscure. Here, we used Caenorhabditis elegans (C. elegans) oocytes to show that PLK-1 plays distinct roles in meiotic spindle assembly and/or stability, chromosome alignment and segregation, and polar body extrusion during meiosis I. Furthermore, by a combination of live imaging and biochemical analysis we identified the chromosomal recruitment mechanisms of PLK-1 during C. elegans oocyte meiosis. The spindle assembly checkpoint kinase BUB-1 directly recruits PLK-1 to the kinetochore and midbivalent while the chromosome arm population of PLK-1 depends on a direct interaction with the centromeric-associated protein CENP-CHCP-4. We found that perturbing both BUB-1 and CENP-CHCP-4 recruitment of PLK-1 leads to severe meiotic defects, resulting in highly aneuploid oocytes. Overall, our results shed light on the roles played by PLK-1 during oocyte meiosis and provide a mechanistic understanding of PLK-1 targeting to meiotic chromosomes.
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A supporting file containing all the information for the graphs presented in the manuscript has been added.
Article and author information
Author details
Funding
Medical Research Council (MR/R008574/1)
- Laura Bel Borja
- Flavie Soubigou
- Federico Pelisch
Wellcome Trust (208833)
- Dhanya K Cheerambathur
National Science Foundation (1650112)
- Jack Houston
National Institutes of Health (GM074215)
- Jack Houston
Wellcome Trust (105606/Z/14/Z)
- Federico Pelisch
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Jon Pines, Institute of Cancer Research Research, United Kingdom
Version history
- Preprint posted: October 7, 2022 (view preprint)
- Received: October 9, 2022
- Accepted: April 14, 2023
- Accepted Manuscript published: April 17, 2023 (version 1)
- Version of Record published: May 3, 2023 (version 2)
Copyright
© 2023, Taylor 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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BUB-1 and CENP-C recruit PLK-1 to control chromosome alignment and segregation during meiosis I in C. elegans oocytes
eLife 12:e84057.
https://doi.org/10.7554/eLife.84057
