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

View ORCID ProfileLaura Bel Borja, Flavie Soubigou, Samuel J.P. Taylor, Conchita Fraguas Bringas, Jacqueline Budrewicz, View ORCID ProfilePablo Lara-Gonzalez, View ORCID ProfileChristopher G. Sorensen Turpin, View ORCID ProfileJoshua N. Bembenek, View ORCID ProfileDhanya K. Cheerambathur, View ORCID ProfileFederico Pelisch
doi: https://doi.org/10.1101/2020.06.12.148254
Laura Bel Borja
1Centre for Gene Regulation and Expression, Sir James Black Centre, School of Life Sciences, University of Dundee. Dundee, DD1 5EH, UK
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  • ORCID record for Laura Bel Borja
Flavie Soubigou
1Centre for Gene Regulation and Expression, Sir James Black Centre, School of Life Sciences, University of Dundee. Dundee, DD1 5EH, UK
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Samuel J.P. Taylor
1Centre for Gene Regulation and Expression, Sir James Black Centre, School of Life Sciences, University of Dundee. Dundee, DD1 5EH, UK
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Conchita Fraguas Bringas
1Centre for Gene Regulation and Expression, Sir James Black Centre, School of Life Sciences, University of Dundee. Dundee, DD1 5EH, UK
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Jacqueline Budrewicz
2Ludwig Institute for Cancer Research, San Diego, California, 92093, USA
3Department of Cellular and Molecular Medicine, University of California at San Diego, La Jolla, California, 92093, USA
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Pablo Lara-Gonzalez
2Ludwig Institute for Cancer Research, San Diego, California, 92093, USA
3Department of Cellular and Molecular Medicine, University of California at San Diego, La Jolla, California, 92093, USA
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Christopher G. Sorensen Turpin
4Department of Biochemistry, Cellular and Molecular Biology, University of Tennessee, C211 Walters Life Sciences Building, 1414 Cumberland Avenue, Knoxville, TN 37996, USA
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Joshua N. Bembenek
5Department of Molecular, Cellular, and Developmental Biology, University of Michigan. 1105 North University Ave., Ann Arbor, MI 48109-1085, USA
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Dhanya K. Cheerambathur
6Wellcome Centre for Cell Biology & Institute of Cell Biology, School of Biological Sciences, The University of Edinburgh, Edinburgh, EH9 3BF, UK
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Federico Pelisch
1Centre for Gene Regulation and Expression, Sir James Black Centre, School of Life Sciences, University of Dundee. Dundee, DD1 5EH, UK
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  • For correspondence: f.pelisch@dundee.ac.uk
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ABSTRACT

Protein Phosphatase 2A (PP2A) is an heterotrimer composed of scaffolding (A), catalytic (C), and regulatory (B) subunits with various key roles during cell division. While A and C subunits form the core enzyme, the diversity generated by interchangeable B subunits dictates substrate specificity. Within the B subunits, B56-type subunits play important roles during meiosis in yeast and mice by protecting centromeric cohesion and stabilising the kinetochore-microtubule attachments. These functions are achieved through targeting of B56 subunits to centromere and kinetochore by Shugoshin and BUBR1. In the nematode Caenorhabditis elegans (C. elegans) the closest BUBR1 ortholog lacks the B56 interaction domain and the Shugoshin orthologue is not required for normal segregation during oocyte meiosis. Therefore, the role of PP2A in C. elegans female meiosis is not known. Here, we report that PP2A is essential for meiotic spindle assembly and chromosome dynamics during C. elegans female meiosis. Specifically, B56 subunits PPTR-1 and PPTR-2 associate with chromosomes during prometaphase I and regulate chromosome congression. The chromosome localization of B56 subunits does not require shugoshin orthologue SGO-1. Instead we have identified the kinase BUB-1 as the key B56 targeting factor to the chromosomes during meiosis. PP2A BUB-1 recruits PP2A:B56 to the chromosomes via dual mechanism: 1) PPTR-1/2 interacts with the newly identified LxxIxE short linear motif (SLiM) within a disordered region in BUB-1 in a phosphorylation-dependent manner; and 2) PPTR-2 can also be recruited to chromosomes in a BUB-1 kinase domain-dependent manner. Our results highlight a novel, BUB-1-dependent mechanism for B56 recruitment, essential for recruiting a pool of PP2A required for proper chromosome congression during meiosis I.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • This version of the manuscript has been updated after revision in eLife. the new manuscript has improved dramatically, with two major achievements: 1) we have now addressed the role of phosphorylation of the BUB-1 LxxIxE motif in vivo and in vitro and 2) we have characterised the chromosome congression/alignment defect in the absence of both B56 subunits as well as in BUB-1 mutants.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC 4.0 International license.
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Posted November 30, 2020.
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BUB-1 targets PP2A:B56 to regulate chromosome congression during meiosis I in C. elegans oocytes
Laura Bel Borja, Flavie Soubigou, Samuel J.P. Taylor, Conchita Fraguas Bringas, Jacqueline Budrewicz, Pablo Lara-Gonzalez, Christopher G. Sorensen Turpin, Joshua N. Bembenek, Dhanya K. Cheerambathur, Federico Pelisch
bioRxiv 2020.06.12.148254; doi: https://doi.org/10.1101/2020.06.12.148254
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BUB-1 targets PP2A:B56 to regulate chromosome congression during meiosis I in C. elegans oocytes
Laura Bel Borja, Flavie Soubigou, Samuel J.P. Taylor, Conchita Fraguas Bringas, Jacqueline Budrewicz, Pablo Lara-Gonzalez, Christopher G. Sorensen Turpin, Joshua N. Bembenek, Dhanya K. Cheerambathur, Federico Pelisch
bioRxiv 2020.06.12.148254; doi: https://doi.org/10.1101/2020.06.12.148254

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