Cohesin-interacting protein WAPL-1 regulates meiotic chromosome structure and cohesion by antagonizing specific cohesin complexes
Wapl induces cohesin dissociation from DNA throughout the mitotic cell cycle, modulating sister chromatid cohesion and higher-order chromatin structure. Cohesin complexes containing meiosis-specific kleisin subunits govern most aspects of meiotic chromosome function, but whether Wapl regulates these...
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doaj-4b4e7c5ddc494e91840a5f486dd224052021-05-05T00:15:10ZengeLife Sciences Publications LtdeLife2050-084X2016-02-01510.7554/eLife.10851Cohesin-interacting protein WAPL-1 regulates meiotic chromosome structure and cohesion by antagonizing specific cohesin complexesOliver Crawley0https://orcid.org/0000-0002-5054-0051Consuelo Barroso1Sarah Testori2Nuria Ferrandiz3Nicola Silva4Maikel Castellano-Pozo5Angel Luis Jaso-Tamame6Enrique Martinez-Perez7Meiosis group, MRC Clinical Sciences Centre, Faculty of Medicine, Imperial College London, London, United KingdomMeiosis group, MRC Clinical Sciences Centre, Faculty of Medicine, Imperial College London, London, United KingdomMeiosis group, MRC Clinical Sciences Centre, Faculty of Medicine, Imperial College London, London, United KingdomMeiosis group, MRC Clinical Sciences Centre, Faculty of Medicine, Imperial College London, London, United KingdomMeiosis group, MRC Clinical Sciences Centre, Faculty of Medicine, Imperial College London, London, United KingdomMeiosis group, MRC Clinical Sciences Centre, Faculty of Medicine, Imperial College London, London, United KingdomMeiosis group, MRC Clinical Sciences Centre, Faculty of Medicine, Imperial College London, London, United KingdomMeiosis group, MRC Clinical Sciences Centre, Faculty of Medicine, Imperial College London, London, United KingdomWapl induces cohesin dissociation from DNA throughout the mitotic cell cycle, modulating sister chromatid cohesion and higher-order chromatin structure. Cohesin complexes containing meiosis-specific kleisin subunits govern most aspects of meiotic chromosome function, but whether Wapl regulates these complexes remains unknown. We show that during C. elegans oogenesis WAPL-1 antagonizes binding of cohesin containing COH-3/4 kleisins, but not REC-8, demonstrating that sensitivity to WAPL-1 is dictated by kleisin identity. By restricting the amount of chromosome-associated COH-3/4 cohesin, WAPL-1 controls chromosome structure throughout meiotic prophase. In the absence of REC-8, WAPL-1 inhibits COH-3/4-mediated cohesion, which requires crossover-fated events formed during meiotic recombination. Thus, WAPL-1 promotes functional specialization of meiotic cohesin: WAPL-1-sensitive COH-3/4 complexes modulate higher-order chromosome structure, while WAPL-1-refractory REC-8 complexes provide stable cohesion. Surprisingly, a WAPL-1-independent mechanism removes cohesin before metaphase I. Our studies provide insight into how meiosis-specific cohesin complexes are regulated to ensure formation of euploid gametes.https://elifesciences.org/articles/10851MeiosisCohesinSister chromatid cohesionChromosome structure |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Oliver Crawley Consuelo Barroso Sarah Testori Nuria Ferrandiz Nicola Silva Maikel Castellano-Pozo Angel Luis Jaso-Tamame Enrique Martinez-Perez |
spellingShingle |
Oliver Crawley Consuelo Barroso Sarah Testori Nuria Ferrandiz Nicola Silva Maikel Castellano-Pozo Angel Luis Jaso-Tamame Enrique Martinez-Perez Cohesin-interacting protein WAPL-1 regulates meiotic chromosome structure and cohesion by antagonizing specific cohesin complexes eLife Meiosis Cohesin Sister chromatid cohesion Chromosome structure |
author_facet |
Oliver Crawley Consuelo Barroso Sarah Testori Nuria Ferrandiz Nicola Silva Maikel Castellano-Pozo Angel Luis Jaso-Tamame Enrique Martinez-Perez |
author_sort |
Oliver Crawley |
title |
Cohesin-interacting protein WAPL-1 regulates meiotic chromosome structure and cohesion by antagonizing specific cohesin complexes |
title_short |
Cohesin-interacting protein WAPL-1 regulates meiotic chromosome structure and cohesion by antagonizing specific cohesin complexes |
title_full |
Cohesin-interacting protein WAPL-1 regulates meiotic chromosome structure and cohesion by antagonizing specific cohesin complexes |
title_fullStr |
Cohesin-interacting protein WAPL-1 regulates meiotic chromosome structure and cohesion by antagonizing specific cohesin complexes |
title_full_unstemmed |
Cohesin-interacting protein WAPL-1 regulates meiotic chromosome structure and cohesion by antagonizing specific cohesin complexes |
title_sort |
cohesin-interacting protein wapl-1 regulates meiotic chromosome structure and cohesion by antagonizing specific cohesin complexes |
publisher |
eLife Sciences Publications Ltd |
series |
eLife |
issn |
2050-084X |
publishDate |
2016-02-01 |
description |
Wapl induces cohesin dissociation from DNA throughout the mitotic cell cycle, modulating sister chromatid cohesion and higher-order chromatin structure. Cohesin complexes containing meiosis-specific kleisin subunits govern most aspects of meiotic chromosome function, but whether Wapl regulates these complexes remains unknown. We show that during C. elegans oogenesis WAPL-1 antagonizes binding of cohesin containing COH-3/4 kleisins, but not REC-8, demonstrating that sensitivity to WAPL-1 is dictated by kleisin identity. By restricting the amount of chromosome-associated COH-3/4 cohesin, WAPL-1 controls chromosome structure throughout meiotic prophase. In the absence of REC-8, WAPL-1 inhibits COH-3/4-mediated cohesion, which requires crossover-fated events formed during meiotic recombination. Thus, WAPL-1 promotes functional specialization of meiotic cohesin: WAPL-1-sensitive COH-3/4 complexes modulate higher-order chromosome structure, while WAPL-1-refractory REC-8 complexes provide stable cohesion. Surprisingly, a WAPL-1-independent mechanism removes cohesin before metaphase I. Our studies provide insight into how meiosis-specific cohesin complexes are regulated to ensure formation of euploid gametes. |
topic |
Meiosis Cohesin Sister chromatid cohesion Chromosome structure |
url |
https://elifesciences.org/articles/10851 |
work_keys_str_mv |
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