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Polo-like kinase-dependent phosphorylation of the synaptonemal complex protein SYP-4 regulates double-strand break formation through a negative feedback loop.

The synaptonemal complex (SC) is an ultrastructurally conserved proteinaceous structure that holds homologous chromosomes together and is required for the stabilization of pairing interactions and the completion of crossover (CO) formation between homologs during meiosis I. Here, we identify a novel...

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Autores principales: Nadarajan, Saravanapriah, Lambert, Talley J, Altendorfer, Elisabeth, Gao, Jinmin, Blower, Michael D, Waters, Jennifer C, Colaiácovo, Monica P
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5423773/
https://www.ncbi.nlm.nih.gov/pubmed/28346135
http://dx.doi.org/10.7554/eLife.23437
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author Nadarajan, Saravanapriah
Lambert, Talley J
Altendorfer, Elisabeth
Gao, Jinmin
Blower, Michael D
Waters, Jennifer C
Colaiácovo, Monica P
author_facet Nadarajan, Saravanapriah
Lambert, Talley J
Altendorfer, Elisabeth
Gao, Jinmin
Blower, Michael D
Waters, Jennifer C
Colaiácovo, Monica P
author_sort Nadarajan, Saravanapriah
collection PubMed
description The synaptonemal complex (SC) is an ultrastructurally conserved proteinaceous structure that holds homologous chromosomes together and is required for the stabilization of pairing interactions and the completion of crossover (CO) formation between homologs during meiosis I. Here, we identify a novel role for a central region component of the SC, SYP-4, in negatively regulating formation of recombination-initiating double-strand breaks (DSBs) via a feedback loop triggered by crossover designation in C. elegans. We found that SYP-4 is phosphorylated dependent on Polo-like kinases PLK-1/2. SYP-4 phosphorylation depends on DSB formation and crossover designation, is required for stabilizing the SC in pachytene by switching the central region of the SC from a more dynamic to a less dynamic state, and negatively regulates DSB formation. We propose a model in which Polo-like kinases recognize crossover designation and phosphorylate SYP-4 thereby stabilizing the SC and making chromosomes less permissive for further DSB formation. DOI: http://dx.doi.org/10.7554/eLife.23437.001
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spelling pubmed-54237732017-05-10 Polo-like kinase-dependent phosphorylation of the synaptonemal complex protein SYP-4 regulates double-strand break formation through a negative feedback loop. Nadarajan, Saravanapriah Lambert, Talley J Altendorfer, Elisabeth Gao, Jinmin Blower, Michael D Waters, Jennifer C Colaiácovo, Monica P eLife Cell Biology The synaptonemal complex (SC) is an ultrastructurally conserved proteinaceous structure that holds homologous chromosomes together and is required for the stabilization of pairing interactions and the completion of crossover (CO) formation between homologs during meiosis I. Here, we identify a novel role for a central region component of the SC, SYP-4, in negatively regulating formation of recombination-initiating double-strand breaks (DSBs) via a feedback loop triggered by crossover designation in C. elegans. We found that SYP-4 is phosphorylated dependent on Polo-like kinases PLK-1/2. SYP-4 phosphorylation depends on DSB formation and crossover designation, is required for stabilizing the SC in pachytene by switching the central region of the SC from a more dynamic to a less dynamic state, and negatively regulates DSB formation. We propose a model in which Polo-like kinases recognize crossover designation and phosphorylate SYP-4 thereby stabilizing the SC and making chromosomes less permissive for further DSB formation. DOI: http://dx.doi.org/10.7554/eLife.23437.001 eLife Sciences Publications, Ltd 2017-03-27 /pmc/articles/PMC5423773/ /pubmed/28346135 http://dx.doi.org/10.7554/eLife.23437 Text en © 2017, Nadarajan et al http://creativecommons.org/licenses/by/4.0/ This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Cell Biology
Nadarajan, Saravanapriah
Lambert, Talley J
Altendorfer, Elisabeth
Gao, Jinmin
Blower, Michael D
Waters, Jennifer C
Colaiácovo, Monica P
Polo-like kinase-dependent phosphorylation of the synaptonemal complex protein SYP-4 regulates double-strand break formation through a negative feedback loop.
title Polo-like kinase-dependent phosphorylation of the synaptonemal complex protein SYP-4 regulates double-strand break formation through a negative feedback loop.
title_full Polo-like kinase-dependent phosphorylation of the synaptonemal complex protein SYP-4 regulates double-strand break formation through a negative feedback loop.
title_fullStr Polo-like kinase-dependent phosphorylation of the synaptonemal complex protein SYP-4 regulates double-strand break formation through a negative feedback loop.
title_full_unstemmed Polo-like kinase-dependent phosphorylation of the synaptonemal complex protein SYP-4 regulates double-strand break formation through a negative feedback loop.
title_short Polo-like kinase-dependent phosphorylation of the synaptonemal complex protein SYP-4 regulates double-strand break formation through a negative feedback loop.
title_sort polo-like kinase-dependent phosphorylation of the synaptonemal complex protein syp-4 regulates double-strand break formation through a negative feedback loop.
topic Cell Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5423773/
https://www.ncbi.nlm.nih.gov/pubmed/28346135
http://dx.doi.org/10.7554/eLife.23437
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