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

doi:10.7554/eLife.65307

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 (Lead / Corresponding author)

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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 Caenorhabditis elegans, the closest BUBR1 orthologue 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.

Original language	English
Article number	e65307
Number of pages	27
Journal	eLife
Volume	9
Early online date	23 Dec 2020
DOIs	https://doi.org/10.7554/eLife.65307
Publication status	Published - 6 Jan 2021

ASJC Scopus subject areas

General Neuroscience
General Immunology and Microbiology
General Biochemistry,Genetics and Molecular Biology

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10.7554/eLife.65307Licence: CC BY

Final Published VersionFinal published version, 4.73 MBLicence: CC BY

Regulation of Meiotic Chromosome Segregation by Post-Translational Modifications
Pelisch, F. (Investigator)
Medical Research Council
14/05/18 → 13/11/23
Project: Research

Investigating PLK-1 and PP2A:B56 recruitment mechanisms in C. elegans oocyte meiosis
Taylor, S. J. P. (Author), Pelisch, F. (Supervisor) & Hay, R. (Supervisor), 2024
Student thesis: Doctoral Thesis › Doctor of Philosophy

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Pelisch, Fede
- Molecular Cell and Developmental Biology - Principal Investigator/Senior Lecturer (Teaching and Research)
Person: Academic

Cite this

@article{9d0d2e4efd164c66b59503344d4c11bf,

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

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 Caenorhabditis elegans, the closest BUBR1 orthologue 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.",

author = "{Bel Borja}, Laura and Flavie Soubigou and Taylor, {Samuel J. P.} and {Fraguas Bringas}, Conchita and Jacqueline Budrewicz and Pablo Lara-Gonzalez and {Sorensen Turpin}, {Christopher G.} and Bembenek, {Joshua N.} and Cheerambathur, {Dhanya K.} and Federico Pelisch",

note = "Funding Information: This work was supported by a Career Development Award from the Medical Research Council (grant MR/R008574/1) and an ISSF grant funded by the Wellcome Trust (105606/Z/14/Z). ST is funded by a Medical Research Council Doctoral Training Programme. DKC is supported by a Sir Henry Dale Fellowship from the Wellcome Trust (208833). PL-G and JB were supported by NIH grant R01 GM074215, awarded to Arshad Desai. Work in the JNB lab is supported by NIH grant R01 GM114471. We acknowledge the FingerPrints Proteomics Facility and the Dundee Imaging Facility, which are supported by a 'Wellcome Trust Technology Platform' award (097945/B/11/Z) and the Tissue Imaging Facility, funded by a Wellcome Trust award (101468/Z/13/Z). Some nematode strains were provided by the CGC, which is funded by NIH Office of Research Infrastructure Programs (P40 OD010440). Copyright: {\textcopyright} Bel Borja et al.",

year = "2021",

month = jan,

day = "6",

doi = "10.7554/eLife.65307",

language = "English",

volume = "9",

journal = "eLife",

issn = "2050-084X",

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T1 - BUB-1 targets PP2A

T2 - B56 to regulate chromosome congression during meiosis I in C. elegans oocytes

AU - Bel Borja, Laura

AU - Soubigou, Flavie

AU - Taylor, Samuel J. P.

AU - Fraguas Bringas, Conchita

AU - Budrewicz, Jacqueline

AU - Lara-Gonzalez, Pablo

AU - Sorensen Turpin, Christopher G.

AU - Bembenek, Joshua N.

AU - Cheerambathur, Dhanya K.

AU - Pelisch, Federico

N1 - Funding Information: This work was supported by a Career Development Award from the Medical Research Council (grant MR/R008574/1) and an ISSF grant funded by the Wellcome Trust (105606/Z/14/Z). ST is funded by a Medical Research Council Doctoral Training Programme. DKC is supported by a Sir Henry Dale Fellowship from the Wellcome Trust (208833). PL-G and JB were supported by NIH grant R01 GM074215, awarded to Arshad Desai. Work in the JNB lab is supported by NIH grant R01 GM114471. We acknowledge the FingerPrints Proteomics Facility and the Dundee Imaging Facility, which are supported by a 'Wellcome Trust Technology Platform' award (097945/B/11/Z) and the Tissue Imaging Facility, funded by a Wellcome Trust award (101468/Z/13/Z). Some nematode strains were provided by the CGC, which is funded by NIH Office of Research Infrastructure Programs (P40 OD010440). Copyright: © Bel Borja et al.

PY - 2021/1/6

Y1 - 2021/1/6

N2 - 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 Caenorhabditis elegans, the closest BUBR1 orthologue 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.

AB - 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 Caenorhabditis elegans, the closest BUBR1 orthologue 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.

U2 - 10.7554/eLife.65307

DO - 10.7554/eLife.65307

M3 - Article

C2 - 33355089

SN - 2050-084X

VL - 9

JO - eLife

JF - eLife

M1 - e65307

ER -

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

Abstract

ASJC Scopus subject areas

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Regulation of Meiotic Chromosome Segregation by Post-Translational Modifications

Investigating PLK-1 and PP2A:B56 recruitment mechanisms in C. elegans oocyte meiosis

Pelisch, Fede

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

Abstract

ASJC Scopus subject areas

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Projects

Regulation of Meiotic Chromosome Segregation by Post-Translational Modifications

Student theses

Investigating PLK-1 and PP2A:B56 recruitment mechanisms in C. elegans oocyte meiosis

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Pelisch, Fede

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