BUB-1 and CENP-C recruit PLK-1 to control chromosome alignment and segregation during meiosis I in C. elegans oocytes
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...
| Main Authors: | , , , , , |
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| Format: | Article |
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eLife Sciences Publications Ltd
2023-04-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/84057 |
| _version_ | 1797834081972518912 |
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| author | Samuel JP Taylor Laura Bel Borja Flavie Soubigou Jack Houston Dhanya K Cheerambathur Federico Pelisch |
| author_facet | Samuel JP Taylor Laura Bel Borja Flavie Soubigou Jack Houston Dhanya K Cheerambathur Federico Pelisch |
| author_sort | Samuel JP Taylor |
| collection | DOAJ |
| description | 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 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. |
| first_indexed | 2024-04-09T14:32:57Z |
| format | Article |
| id | doaj.art-ba866f58063d402a8e2da7c7ec514fc4 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-09T14:32:57Z |
| publishDate | 2023-04-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-ba866f58063d402a8e2da7c7ec514fc42023-05-03T14:33:29ZengeLife Sciences Publications LtdeLife2050-084X2023-04-011210.7554/eLife.84057BUB-1 and CENP-C recruit PLK-1 to control chromosome alignment and segregation during meiosis I in C. elegans oocytesSamuel JP Taylor0https://orcid.org/0000-0002-0654-619XLaura Bel Borja1https://orcid.org/0000-0002-8381-934XFlavie Soubigou2Jack Houston3Dhanya K Cheerambathur4Federico Pelisch5https://orcid.org/0000-0003-4575-1492Centre for Gene Regulation and Expression, Sir James Black Centre, School of Life Sciences, University of Dundee, Dundee, United KingdomCentre for Gene Regulation and Expression, Sir James Black Centre, School of Life Sciences, University of Dundee, Dundee, United KingdomCentre for Gene Regulation and Expression, Sir James Black Centre, School of Life Sciences, University of Dundee, Dundee, United KingdomLudwig Institute for Cancer Research, San Diego Branch, La Jolla, United StatesWellcome Centre for Cell Biology & Institute of Cell Biology, School of Biological Sciences, University of Edinburgh, Edinburgh, United KingdomCentre for Gene Regulation and Expression, Sir James Black Centre, School of Life Sciences, University of Dundee, Dundee, United KingdomPhosphorylation 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 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.https://elifesciences.org/articles/84057meiosisC. elegansoocytePLK1centromerekinetochore |
| spellingShingle | Samuel JP Taylor Laura Bel Borja Flavie Soubigou Jack Houston Dhanya K Cheerambathur Federico Pelisch BUB-1 and CENP-C recruit PLK-1 to control chromosome alignment and segregation during meiosis I in C. elegans oocytes eLife meiosis C. elegans oocyte PLK1 centromere kinetochore |
| title | BUB-1 and CENP-C recruit PLK-1 to control chromosome alignment and segregation during meiosis I in C. elegans oocytes |
| title_full | BUB-1 and CENP-C recruit PLK-1 to control chromosome alignment and segregation during meiosis I in C. elegans oocytes |
| title_fullStr | BUB-1 and CENP-C recruit PLK-1 to control chromosome alignment and segregation during meiosis I in C. elegans oocytes |
| title_full_unstemmed | BUB-1 and CENP-C recruit PLK-1 to control chromosome alignment and segregation during meiosis I in C. elegans oocytes |
| title_short | BUB-1 and CENP-C recruit PLK-1 to control chromosome alignment and segregation during meiosis I in C. elegans oocytes |
| title_sort | bub 1 and cenp c recruit plk 1 to control chromosome alignment and segregation during meiosis i in c elegans oocytes |
| topic | meiosis C. elegans oocyte PLK1 centromere kinetochore |
| url | https://elifesciences.org/articles/84057 |
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