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Surveillance of cohesin-supported chromosome structure controls meiotic progression
Chromosome movements and programmed DNA double-strand breaks (DSBs) promote homologue pairing and initiate recombination at meiosis onset. Meiotic progression involves checkpoint-controlled termination of these events when all homologue pairs achieve synapsis and form crossover precursors. Exploitin...
Autores principales: | , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Nature Publishing Group UK
2020
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7455720/ https://www.ncbi.nlm.nih.gov/pubmed/32859945 http://dx.doi.org/10.1038/s41467-020-18219-9 |
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author | Castellano-Pozo, Maikel Pacheco, Sarai Sioutas, Georgios Jaso-Tamame, Angel Luis Dore, Marian H. Karimi, Mohammad M. Martinez-Perez, Enrique |
author_facet | Castellano-Pozo, Maikel Pacheco, Sarai Sioutas, Georgios Jaso-Tamame, Angel Luis Dore, Marian H. Karimi, Mohammad M. Martinez-Perez, Enrique |
author_sort | Castellano-Pozo, Maikel |
collection | PubMed |
description | Chromosome movements and programmed DNA double-strand breaks (DSBs) promote homologue pairing and initiate recombination at meiosis onset. Meiotic progression involves checkpoint-controlled termination of these events when all homologue pairs achieve synapsis and form crossover precursors. Exploiting the temporo-spatial organisation of the C. elegans germline and time-resolved methods of protein removal, we show that surveillance of the synaptonemal complex (SC) controls meiotic progression. In nuclei with fully synapsed homologues and crossover precursors, removing different meiosis-specific cohesin complexes, which are individually required for SC stability, or a SC central region component causes functional redeployment of the chromosome movement and DSB machinery, triggering whole-nucleus reorganisation. This apparent reversal of the meiotic programme requires CHK-2 kinase reactivation via signalling from chromosome axes containing HORMA proteins, but occurs in the absence of transcriptional changes. Our results uncover an unexpected plasticity of the meiotic programme and show how chromosome signalling orchestrates nuclear organisation and meiotic progression. |
format | Online Article Text |
id | pubmed-7455720 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2020 |
publisher | Nature Publishing Group UK |
record_format | MEDLINE/PubMed |
spelling | pubmed-74557202020-09-04 Surveillance of cohesin-supported chromosome structure controls meiotic progression Castellano-Pozo, Maikel Pacheco, Sarai Sioutas, Georgios Jaso-Tamame, Angel Luis Dore, Marian H. Karimi, Mohammad M. Martinez-Perez, Enrique Nat Commun Article Chromosome movements and programmed DNA double-strand breaks (DSBs) promote homologue pairing and initiate recombination at meiosis onset. Meiotic progression involves checkpoint-controlled termination of these events when all homologue pairs achieve synapsis and form crossover precursors. Exploiting the temporo-spatial organisation of the C. elegans germline and time-resolved methods of protein removal, we show that surveillance of the synaptonemal complex (SC) controls meiotic progression. In nuclei with fully synapsed homologues and crossover precursors, removing different meiosis-specific cohesin complexes, which are individually required for SC stability, or a SC central region component causes functional redeployment of the chromosome movement and DSB machinery, triggering whole-nucleus reorganisation. This apparent reversal of the meiotic programme requires CHK-2 kinase reactivation via signalling from chromosome axes containing HORMA proteins, but occurs in the absence of transcriptional changes. Our results uncover an unexpected plasticity of the meiotic programme and show how chromosome signalling orchestrates nuclear organisation and meiotic progression. Nature Publishing Group UK 2020-08-28 /pmc/articles/PMC7455720/ /pubmed/32859945 http://dx.doi.org/10.1038/s41467-020-18219-9 Text en © The Author(s) 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. |
spellingShingle | Article Castellano-Pozo, Maikel Pacheco, Sarai Sioutas, Georgios Jaso-Tamame, Angel Luis Dore, Marian H. Karimi, Mohammad M. Martinez-Perez, Enrique Surveillance of cohesin-supported chromosome structure controls meiotic progression |
title | Surveillance of cohesin-supported chromosome structure controls meiotic progression |
title_full | Surveillance of cohesin-supported chromosome structure controls meiotic progression |
title_fullStr | Surveillance of cohesin-supported chromosome structure controls meiotic progression |
title_full_unstemmed | Surveillance of cohesin-supported chromosome structure controls meiotic progression |
title_short | Surveillance of cohesin-supported chromosome structure controls meiotic progression |
title_sort | surveillance of cohesin-supported chromosome structure controls meiotic progression |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7455720/ https://www.ncbi.nlm.nih.gov/pubmed/32859945 http://dx.doi.org/10.1038/s41467-020-18219-9 |
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