Spatiotemporal regulation of Aurora B recruitment ensures release of cohesion during C. Elegans oocyte meiosis

Nuria Ferrandiz; Consuelo Barroso; Oana Telecan; Nan Shao; Hyun Min Kim; Sarah Testori; Peter Faull; Pedro Cutillas; Ambrosious P. Snijders; Monica P. Colaiácovo; Enrique Martinez-Perez

doi:10.1038/s41467-018-03229-5

Spatiotemporal regulation of Aurora B recruitment ensures release of cohesion during C. Elegans oocyte meiosis

Nuria Ferrandiz, Consuelo Barroso, Oana Telecan, Nan Shao, Hyun Min Kim, Sarah Testori, Peter Faull, Pedro Cutillas, Ambrosious P. Snijders, Monica P. Colaiácovo, Enrique Martinez-Perez^*

^*Corresponding author for this work

PCE - Proteomics Center of Excellence

Research output: Contribution to journal › Article › peer-review

45 Scopus citations

Abstract

The formation of haploid gametes from diploid germ cells requires the regulated two-step release of sister chromatid cohesion (SCC) during the meiotic divisions. Here, we show that phosphorylation of cohesin subunit REC-8 by Aurora B promotes SCC release at anaphase I onset in C. Elegans oocytes. Aurora B loading to chromatin displaying Haspin-mediated H3 T3 phosphorylation induces spatially restricted REC-8 phosphorylation, preventing full SCC release during anaphase I. H3 T3 phosphorylation is locally antagonized by protein phosphatase 1, which is recruited to chromosomes by HTP-1/2 and LAB-1. Mutating the N terminus of HTP-1 causes ectopic H3 T3 phosphorylation, triggering precocious SCC release without impairing earlier HTP-1 roles in homolog pairing and recombination. CDK-1 exerts temporal regulation of Aurora B recruitment, coupling REC-8 phosphorylation to oocyte maturation. Our findings elucidate a complex regulatory network that uses chromosome axis components, H3 T3 phosphorylation, and cell cycle regulators to ensure accurate chromosome segregation during oogenesis.

Original language	English (US)
Article number	834
Journal	Nature communications
Volume	9
Issue number	1
DOIs	https://doi.org/10.1038/s41467-018-03229-5
State	Published - Dec 1 2018

Funding

We thank the Caenorhabditis Genetics Center (CGC) for providing C. Elegans strains and Dirk Dormann for help with live imaging. This work was supported by an MRC corefunded grant and by a David Phillips Fellowship to E.M.-P, and by National Institutes of Health grants R01GM072551 and R01GM105853 to M.P.C. We thank the Caenorhabditis Genetics Center (CGC) for providing C. elegans strains and Dirk Dormann for help with live imaging. This work was supported by an MRC core-funded grant and by a David Phillips Fellowship to E.M.-P, and by National Institutes of Health grants R01GM072551 and R01GM105853 to M.P.C.

ASJC Scopus subject areas

General Chemistry
General Biochemistry, Genetics and Molecular Biology
General Physics and Astronomy

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title = "Spatiotemporal regulation of Aurora B recruitment ensures release of cohesion during C. Elegans oocyte meiosis",

abstract = "The formation of haploid gametes from diploid germ cells requires the regulated two-step release of sister chromatid cohesion (SCC) during the meiotic divisions. Here, we show that phosphorylation of cohesin subunit REC-8 by Aurora B promotes SCC release at anaphase I onset in C. Elegans oocytes. Aurora B loading to chromatin displaying Haspin-mediated H3 T3 phosphorylation induces spatially restricted REC-8 phosphorylation, preventing full SCC release during anaphase I. H3 T3 phosphorylation is locally antagonized by protein phosphatase 1, which is recruited to chromosomes by HTP-1/2 and LAB-1. Mutating the N terminus of HTP-1 causes ectopic H3 T3 phosphorylation, triggering precocious SCC release without impairing earlier HTP-1 roles in homolog pairing and recombination. CDK-1 exerts temporal regulation of Aurora B recruitment, coupling REC-8 phosphorylation to oocyte maturation. Our findings elucidate a complex regulatory network that uses chromosome axis components, H3 T3 phosphorylation, and cell cycle regulators to ensure accurate chromosome segregation during oogenesis.",

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AU - Ferrandiz, Nuria

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AU - Shao, Nan

AU - Kim, Hyun Min

AU - Testori, Sarah

AU - Faull, Peter

AU - Cutillas, Pedro

AU - Snijders, Ambrosious P.

AU - Colaiácovo, Monica P.

AU - Martinez-Perez, Enrique

PY - 2018/12/1

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N2 - The formation of haploid gametes from diploid germ cells requires the regulated two-step release of sister chromatid cohesion (SCC) during the meiotic divisions. Here, we show that phosphorylation of cohesin subunit REC-8 by Aurora B promotes SCC release at anaphase I onset in C. Elegans oocytes. Aurora B loading to chromatin displaying Haspin-mediated H3 T3 phosphorylation induces spatially restricted REC-8 phosphorylation, preventing full SCC release during anaphase I. H3 T3 phosphorylation is locally antagonized by protein phosphatase 1, which is recruited to chromosomes by HTP-1/2 and LAB-1. Mutating the N terminus of HTP-1 causes ectopic H3 T3 phosphorylation, triggering precocious SCC release without impairing earlier HTP-1 roles in homolog pairing and recombination. CDK-1 exerts temporal regulation of Aurora B recruitment, coupling REC-8 phosphorylation to oocyte maturation. Our findings elucidate a complex regulatory network that uses chromosome axis components, H3 T3 phosphorylation, and cell cycle regulators to ensure accurate chromosome segregation during oogenesis.

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Spatiotemporal regulation of Aurora B recruitment ensures release of cohesion during C. Elegans oocyte meiosis

Abstract

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