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...

Full description

Bibliographic Details
Main Authors: Oliver Crawley, Consuelo Barroso, Sarah Testori, Nuria Ferrandiz, Nicola Silva, Maikel Castellano-Pozo, Angel Luis Jaso-Tamame, Enrique Martinez-Perez
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2016-02-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/10851
id doaj-4b4e7c5ddc494e91840a5f486dd22405
record_format Article
spelling 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 AT olivercrawley cohesininteractingproteinwapl1regulatesmeioticchromosomestructureandcohesionbyantagonizingspecificcohesincomplexes
AT consuelobarroso cohesininteractingproteinwapl1regulatesmeioticchromosomestructureandcohesionbyantagonizingspecificcohesincomplexes
AT sarahtestori cohesininteractingproteinwapl1regulatesmeioticchromosomestructureandcohesionbyantagonizingspecificcohesincomplexes
AT nuriaferrandiz cohesininteractingproteinwapl1regulatesmeioticchromosomestructureandcohesionbyantagonizingspecificcohesincomplexes
AT nicolasilva cohesininteractingproteinwapl1regulatesmeioticchromosomestructureandcohesionbyantagonizingspecificcohesincomplexes
AT maikelcastellanopozo cohesininteractingproteinwapl1regulatesmeioticchromosomestructureandcohesionbyantagonizingspecificcohesincomplexes
AT angelluisjasotamame cohesininteractingproteinwapl1regulatesmeioticchromosomestructureandcohesionbyantagonizingspecificcohesincomplexes
AT enriquemartinezperez cohesininteractingproteinwapl1regulatesmeioticchromosomestructureandcohesionbyantagonizingspecificcohesincomplexes
_version_ 1721476492051873792