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Centriole foci persist in starfish oocytes despite Polo-like kinase 1 inactivation or loss of microtubule nucleation activity

Centrioles must be eliminated or inactivated from the oocyte to ensure that only the two functional centrioles contributed by the sperm are present in the zygote. Such removal can occur during oogenesis, as in Drosophila, where departure of Polo kinase from centrosomes leads to loss of microtubule n...

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Autores principales: Pierron, Marie, Kalbfuss, Nils, Borrego-Pinto, Joana, Lénárt, Péter, Gönczy, Pierre
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The American Society for Cell Biology 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7185973/
https://www.ncbi.nlm.nih.gov/pubmed/32073992
http://dx.doi.org/10.1091/mbc.E19-06-0346
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author Pierron, Marie
Kalbfuss, Nils
Borrego-Pinto, Joana
Lénárt, Péter
Gönczy, Pierre
author_facet Pierron, Marie
Kalbfuss, Nils
Borrego-Pinto, Joana
Lénárt, Péter
Gönczy, Pierre
author_sort Pierron, Marie
collection PubMed
description Centrioles must be eliminated or inactivated from the oocyte to ensure that only the two functional centrioles contributed by the sperm are present in the zygote. Such removal can occur during oogenesis, as in Drosophila, where departure of Polo kinase from centrosomes leads to loss of microtubule nucleating activity and centriole removal. In other species, oocyte-derived centrioles are removed around the time of fertilization through incompletely understood mechanisms. Here, we use confocal imaging of live starfish oocytes and zygotes expressing markers of microtubule nucleating activity and centrioles to investigate this question. We first assay the role of Polo-like kinase 1 (Plk1) in centriole elimination. We find that although Plk1 localizes around oocyte-derived centrioles, kinase impairment with BI-2536 does not protect centrioles from removal in the bat star Patiria miniata. Moreover, we uncover that all four oocyte-derived centrioles lose microtubule nucleating activity when retained experimentally in the zygote of the radiate star Asterias forbesi. Interestingly, two such centrioles nevertheless retain the centriolar markers mEGFP::PACT and pmPoc1::mEGFP. Together, these findings indicate that centrioles can persist when Plk1 activity is impaired, as well as when microtubule nucleating activity is lacking, uncovering further diversity in the mechanisms governing centriole removal.
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spelling pubmed-71859732020-06-30 Centriole foci persist in starfish oocytes despite Polo-like kinase 1 inactivation or loss of microtubule nucleation activity Pierron, Marie Kalbfuss, Nils Borrego-Pinto, Joana Lénárt, Péter Gönczy, Pierre Mol Biol Cell Brief Reports Centrioles must be eliminated or inactivated from the oocyte to ensure that only the two functional centrioles contributed by the sperm are present in the zygote. Such removal can occur during oogenesis, as in Drosophila, where departure of Polo kinase from centrosomes leads to loss of microtubule nucleating activity and centriole removal. In other species, oocyte-derived centrioles are removed around the time of fertilization through incompletely understood mechanisms. Here, we use confocal imaging of live starfish oocytes and zygotes expressing markers of microtubule nucleating activity and centrioles to investigate this question. We first assay the role of Polo-like kinase 1 (Plk1) in centriole elimination. We find that although Plk1 localizes around oocyte-derived centrioles, kinase impairment with BI-2536 does not protect centrioles from removal in the bat star Patiria miniata. Moreover, we uncover that all four oocyte-derived centrioles lose microtubule nucleating activity when retained experimentally in the zygote of the radiate star Asterias forbesi. Interestingly, two such centrioles nevertheless retain the centriolar markers mEGFP::PACT and pmPoc1::mEGFP. Together, these findings indicate that centrioles can persist when Plk1 activity is impaired, as well as when microtubule nucleating activity is lacking, uncovering further diversity in the mechanisms governing centriole removal. The American Society for Cell Biology 2020-04-15 /pmc/articles/PMC7185973/ /pubmed/32073992 http://dx.doi.org/10.1091/mbc.E19-06-0346 Text en © 2020 Pierron, Kalbfuss, Borrego-Pinto, et al. “ASCB®,” “The American Society for Cell Biology®,” and “Molecular Biology of the Cell®” are registered trademarks of The American Society for Cell Biology. http://creativecommons.org/licenses/by-nc-sa/3.0 This article is distributed by The American Society for Cell Biology under license from the author(s). Two months after publication it is available to the public under an Attribution–Noncommercial–Share Alike 3.0 Unported Creative Commons License.
spellingShingle Brief Reports
Pierron, Marie
Kalbfuss, Nils
Borrego-Pinto, Joana
Lénárt, Péter
Gönczy, Pierre
Centriole foci persist in starfish oocytes despite Polo-like kinase 1 inactivation or loss of microtubule nucleation activity
title Centriole foci persist in starfish oocytes despite Polo-like kinase 1 inactivation or loss of microtubule nucleation activity
title_full Centriole foci persist in starfish oocytes despite Polo-like kinase 1 inactivation or loss of microtubule nucleation activity
title_fullStr Centriole foci persist in starfish oocytes despite Polo-like kinase 1 inactivation or loss of microtubule nucleation activity
title_full_unstemmed Centriole foci persist in starfish oocytes despite Polo-like kinase 1 inactivation or loss of microtubule nucleation activity
title_short Centriole foci persist in starfish oocytes despite Polo-like kinase 1 inactivation or loss of microtubule nucleation activity
title_sort centriole foci persist in starfish oocytes despite polo-like kinase 1 inactivation or loss of microtubule nucleation activity
topic Brief Reports
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7185973/
https://www.ncbi.nlm.nih.gov/pubmed/32073992
http://dx.doi.org/10.1091/mbc.E19-06-0346
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