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Distinct mechanisms eliminate mother and daughter centrioles in meiosis of starfish oocytes

Centriole elimination is an essential process that occurs in female meiosis of metazoa to reset centriole number in the zygote at fertilization. How centrioles are eliminated remains poorly understood. Here we visualize the entire elimination process live in starfish oocytes. Using specific fluoresc...

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Autores principales: Borrego-Pinto, Joana, Somogyi, Kálmán, Karreman, Matthia A., König, Julia, Müller-Reichert, Thomas, Bettencourt-Dias, Mónica, Gönczy, Pierre, Schwab, Yannick, Lénárt, Péter
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Rockefeller University Press 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4810307/
https://www.ncbi.nlm.nih.gov/pubmed/27002173
http://dx.doi.org/10.1083/jcb.201510083
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author Borrego-Pinto, Joana
Somogyi, Kálmán
Karreman, Matthia A.
König, Julia
Müller-Reichert, Thomas
Bettencourt-Dias, Mónica
Gönczy, Pierre
Schwab, Yannick
Lénárt, Péter
author_facet Borrego-Pinto, Joana
Somogyi, Kálmán
Karreman, Matthia A.
König, Julia
Müller-Reichert, Thomas
Bettencourt-Dias, Mónica
Gönczy, Pierre
Schwab, Yannick
Lénárt, Péter
author_sort Borrego-Pinto, Joana
collection PubMed
description Centriole elimination is an essential process that occurs in female meiosis of metazoa to reset centriole number in the zygote at fertilization. How centrioles are eliminated remains poorly understood. Here we visualize the entire elimination process live in starfish oocytes. Using specific fluorescent markers, we demonstrate that the two older, mother centrioles are selectively removed from the oocyte by extrusion into polar bodies. We show that this requires specific positioning of the second meiotic spindle, achieved by dynein-driven transport, and anchorage of the mother centriole to the plasma membrane via mother-specific appendages. In contrast, the single daughter centriole remaining in the egg is eliminated before the first embryonic cleavage. We demonstrate that these distinct elimination mechanisms are necessary because if mother centrioles are artificially retained, they cannot be inactivated, resulting in multipolar zygotic spindles. Thus, our findings reveal a dual mechanism to eliminate centrioles: mothers are physically removed, whereas daughters are eliminated in the cytoplasm, preparing the egg for fertilization.
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spelling pubmed-48103072016-09-28 Distinct mechanisms eliminate mother and daughter centrioles in meiosis of starfish oocytes Borrego-Pinto, Joana Somogyi, Kálmán Karreman, Matthia A. König, Julia Müller-Reichert, Thomas Bettencourt-Dias, Mónica Gönczy, Pierre Schwab, Yannick Lénárt, Péter J Cell Biol Research Articles Centriole elimination is an essential process that occurs in female meiosis of metazoa to reset centriole number in the zygote at fertilization. How centrioles are eliminated remains poorly understood. Here we visualize the entire elimination process live in starfish oocytes. Using specific fluorescent markers, we demonstrate that the two older, mother centrioles are selectively removed from the oocyte by extrusion into polar bodies. We show that this requires specific positioning of the second meiotic spindle, achieved by dynein-driven transport, and anchorage of the mother centriole to the plasma membrane via mother-specific appendages. In contrast, the single daughter centriole remaining in the egg is eliminated before the first embryonic cleavage. We demonstrate that these distinct elimination mechanisms are necessary because if mother centrioles are artificially retained, they cannot be inactivated, resulting in multipolar zygotic spindles. Thus, our findings reveal a dual mechanism to eliminate centrioles: mothers are physically removed, whereas daughters are eliminated in the cytoplasm, preparing the egg for fertilization. The Rockefeller University Press 2016-03-28 /pmc/articles/PMC4810307/ /pubmed/27002173 http://dx.doi.org/10.1083/jcb.201510083 Text en © 2016 Borrego-Pinto et al. This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 3.0 Unported license, as described at http://creativecommons.org/licenses/by-nc-sa/3.0/).
spellingShingle Research Articles
Borrego-Pinto, Joana
Somogyi, Kálmán
Karreman, Matthia A.
König, Julia
Müller-Reichert, Thomas
Bettencourt-Dias, Mónica
Gönczy, Pierre
Schwab, Yannick
Lénárt, Péter
Distinct mechanisms eliminate mother and daughter centrioles in meiosis of starfish oocytes
title Distinct mechanisms eliminate mother and daughter centrioles in meiosis of starfish oocytes
title_full Distinct mechanisms eliminate mother and daughter centrioles in meiosis of starfish oocytes
title_fullStr Distinct mechanisms eliminate mother and daughter centrioles in meiosis of starfish oocytes
title_full_unstemmed Distinct mechanisms eliminate mother and daughter centrioles in meiosis of starfish oocytes
title_short Distinct mechanisms eliminate mother and daughter centrioles in meiosis of starfish oocytes
title_sort distinct mechanisms eliminate mother and daughter centrioles in meiosis of starfish oocytes
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4810307/
https://www.ncbi.nlm.nih.gov/pubmed/27002173
http://dx.doi.org/10.1083/jcb.201510083
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