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Meiosis-specific prophase-like pathway controls cleavage-independent release of cohesin by Wapl phosphorylation

Sister chromatid cohesion on chromosome arms is essential for the segregation of homologous chromosomes during meiosis I while it is dispensable for sister chromatid separation during mitosis. It was assumed that, unlike the situation in mitosis, chromosome arms retain cohesion prior to onset of ana...

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Autores principales: Challa, Kiran, Fajish V, Ghanim, Shinohara, Miki, Klein, Franz, Gasser, Susan M., Shinohara, Akira
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6317811/
https://www.ncbi.nlm.nih.gov/pubmed/30605471
http://dx.doi.org/10.1371/journal.pgen.1007851
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author Challa, Kiran
Fajish V, Ghanim
Shinohara, Miki
Klein, Franz
Gasser, Susan M.
Shinohara, Akira
author_facet Challa, Kiran
Fajish V, Ghanim
Shinohara, Miki
Klein, Franz
Gasser, Susan M.
Shinohara, Akira
author_sort Challa, Kiran
collection PubMed
description Sister chromatid cohesion on chromosome arms is essential for the segregation of homologous chromosomes during meiosis I while it is dispensable for sister chromatid separation during mitosis. It was assumed that, unlike the situation in mitosis, chromosome arms retain cohesion prior to onset of anaphase-I. Paradoxically, reduced immunostaining signals of meiosis-specific cohesin, including the kleisin Rec8, were observed on chromosomes during late prophase-I of budding yeast. This decrease is seen in the absence of Rec8 cleavage and depends on condensin-mediated recruitment of Polo-like kinase (PLK/Cdc5). In this study, we confirmed that this release indeed accompanies the dissociation of acetylated Smc3 as well as Rec8 from meiotic chromosomes during late prophase-I. This release requires, in addition to PLK, the cohesin regulator, Wapl (Rad61/Wpl1 in yeast), and Dbf4-dependent Cdc7 kinase (DDK). Meiosis-specific phosphorylation of Rad61/Wpl1 and Rec8 by PLK and DDK collaboratively promote this release. This process is similar to the vertebrate “prophase” pathway for cohesin release during G2 phase and pro-metaphase. In yeast, meiotic cohesin release coincides with PLK-dependent compaction of chromosomes in late meiotic prophase-I. We suggest that yeast uses this highly regulated cleavage-independent pathway to remove cohesin during late prophase-I to facilitate morphogenesis of condensed metaphase-I chromosomes.
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spelling pubmed-63178112019-01-19 Meiosis-specific prophase-like pathway controls cleavage-independent release of cohesin by Wapl phosphorylation Challa, Kiran Fajish V, Ghanim Shinohara, Miki Klein, Franz Gasser, Susan M. Shinohara, Akira PLoS Genet Research Article Sister chromatid cohesion on chromosome arms is essential for the segregation of homologous chromosomes during meiosis I while it is dispensable for sister chromatid separation during mitosis. It was assumed that, unlike the situation in mitosis, chromosome arms retain cohesion prior to onset of anaphase-I. Paradoxically, reduced immunostaining signals of meiosis-specific cohesin, including the kleisin Rec8, were observed on chromosomes during late prophase-I of budding yeast. This decrease is seen in the absence of Rec8 cleavage and depends on condensin-mediated recruitment of Polo-like kinase (PLK/Cdc5). In this study, we confirmed that this release indeed accompanies the dissociation of acetylated Smc3 as well as Rec8 from meiotic chromosomes during late prophase-I. This release requires, in addition to PLK, the cohesin regulator, Wapl (Rad61/Wpl1 in yeast), and Dbf4-dependent Cdc7 kinase (DDK). Meiosis-specific phosphorylation of Rad61/Wpl1 and Rec8 by PLK and DDK collaboratively promote this release. This process is similar to the vertebrate “prophase” pathway for cohesin release during G2 phase and pro-metaphase. In yeast, meiotic cohesin release coincides with PLK-dependent compaction of chromosomes in late meiotic prophase-I. We suggest that yeast uses this highly regulated cleavage-independent pathway to remove cohesin during late prophase-I to facilitate morphogenesis of condensed metaphase-I chromosomes. Public Library of Science 2019-01-03 /pmc/articles/PMC6317811/ /pubmed/30605471 http://dx.doi.org/10.1371/journal.pgen.1007851 Text en © 2019 Challa et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Challa, Kiran
Fajish V, Ghanim
Shinohara, Miki
Klein, Franz
Gasser, Susan M.
Shinohara, Akira
Meiosis-specific prophase-like pathway controls cleavage-independent release of cohesin by Wapl phosphorylation
title Meiosis-specific prophase-like pathway controls cleavage-independent release of cohesin by Wapl phosphorylation
title_full Meiosis-specific prophase-like pathway controls cleavage-independent release of cohesin by Wapl phosphorylation
title_fullStr Meiosis-specific prophase-like pathway controls cleavage-independent release of cohesin by Wapl phosphorylation
title_full_unstemmed Meiosis-specific prophase-like pathway controls cleavage-independent release of cohesin by Wapl phosphorylation
title_short Meiosis-specific prophase-like pathway controls cleavage-independent release of cohesin by Wapl phosphorylation
title_sort meiosis-specific prophase-like pathway controls cleavage-independent release of cohesin by wapl phosphorylation
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6317811/
https://www.ncbi.nlm.nih.gov/pubmed/30605471
http://dx.doi.org/10.1371/journal.pgen.1007851
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