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The careful control of Polo kinase by APC/C-Ube2C ensures the intercellular transport of germline centrosomes during Drosophila oogenesis

A feature of metazoan reproduction is the elimination of maternal centrosomes from the oocyte. In animals that form syncytial cysts during oogenesis, including Drosophila and human, all centrosomes within the cyst migrate to the oocyte where they are subsequently degenerated. The importance and the...

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Autores principales: Braun, Alexis Leah, Meghini, Francesco, Villa-Fombuena, Gema, Guermont, Morgane, Fernandez-Martinez, Elisa, Qian, Zhang, Dolores Martín-Bermudo, Maria, González-Reyes, Acaimo, Glover, David Moore, Kimata, Yuu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Royal Society 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8241486/
https://www.ncbi.nlm.nih.gov/pubmed/34186008
http://dx.doi.org/10.1098/rsob.200371
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author Braun, Alexis Leah
Meghini, Francesco
Villa-Fombuena, Gema
Guermont, Morgane
Fernandez-Martinez, Elisa
Qian, Zhang
Dolores Martín-Bermudo, Maria
González-Reyes, Acaimo
Glover, David Moore
Kimata, Yuu
author_facet Braun, Alexis Leah
Meghini, Francesco
Villa-Fombuena, Gema
Guermont, Morgane
Fernandez-Martinez, Elisa
Qian, Zhang
Dolores Martín-Bermudo, Maria
González-Reyes, Acaimo
Glover, David Moore
Kimata, Yuu
author_sort Braun, Alexis Leah
collection PubMed
description A feature of metazoan reproduction is the elimination of maternal centrosomes from the oocyte. In animals that form syncytial cysts during oogenesis, including Drosophila and human, all centrosomes within the cyst migrate to the oocyte where they are subsequently degenerated. The importance and the underlying mechanism of this event remain unclear. Here, we show that, during early Drosophila oogenesis, control of the Anaphase Promoting Complex/Cyclosome (APC/C), the ubiquitin ligase complex essential for cell cycle control, ensures proper transport of centrosomes into the oocyte through the regulation of Polo/Plk1 kinase, a critical regulator of the integrity and activity of the centrosome. We show that novel mutations in the APC/C-specific E2, Vihar/Ube2c, that affect its inhibitory regulation on APC/C cause precocious Polo degradation and impedes centrosome transport, through destabilization of centrosomes. The failure of centrosome migration correlates with weakened microtubule polarization in the cyst and allows ectopic microtubule nucleation in nurse cells, leading to the loss of oocyte identity. These results suggest a role for centrosome migration in oocyte fate maintenance through the concentration and confinement of microtubule nucleation activity into the oocyte. Considering the conserved roles of APC/C and Polo throughout the animal kingdom, our findings may be translated into other animals.
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spelling pubmed-82414862021-06-30 The careful control of Polo kinase by APC/C-Ube2C ensures the intercellular transport of germline centrosomes during Drosophila oogenesis Braun, Alexis Leah Meghini, Francesco Villa-Fombuena, Gema Guermont, Morgane Fernandez-Martinez, Elisa Qian, Zhang Dolores Martín-Bermudo, Maria González-Reyes, Acaimo Glover, David Moore Kimata, Yuu Open Biol Research A feature of metazoan reproduction is the elimination of maternal centrosomes from the oocyte. In animals that form syncytial cysts during oogenesis, including Drosophila and human, all centrosomes within the cyst migrate to the oocyte where they are subsequently degenerated. The importance and the underlying mechanism of this event remain unclear. Here, we show that, during early Drosophila oogenesis, control of the Anaphase Promoting Complex/Cyclosome (APC/C), the ubiquitin ligase complex essential for cell cycle control, ensures proper transport of centrosomes into the oocyte through the regulation of Polo/Plk1 kinase, a critical regulator of the integrity and activity of the centrosome. We show that novel mutations in the APC/C-specific E2, Vihar/Ube2c, that affect its inhibitory regulation on APC/C cause precocious Polo degradation and impedes centrosome transport, through destabilization of centrosomes. The failure of centrosome migration correlates with weakened microtubule polarization in the cyst and allows ectopic microtubule nucleation in nurse cells, leading to the loss of oocyte identity. These results suggest a role for centrosome migration in oocyte fate maintenance through the concentration and confinement of microtubule nucleation activity into the oocyte. Considering the conserved roles of APC/C and Polo throughout the animal kingdom, our findings may be translated into other animals. The Royal Society 2021-06-30 /pmc/articles/PMC8241486/ /pubmed/34186008 http://dx.doi.org/10.1098/rsob.200371 Text en © 2021 The Authors. https://creativecommons.org/licenses/by/4.0/Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, provided the original author and source are credited.
spellingShingle Research
Braun, Alexis Leah
Meghini, Francesco
Villa-Fombuena, Gema
Guermont, Morgane
Fernandez-Martinez, Elisa
Qian, Zhang
Dolores Martín-Bermudo, Maria
González-Reyes, Acaimo
Glover, David Moore
Kimata, Yuu
The careful control of Polo kinase by APC/C-Ube2C ensures the intercellular transport of germline centrosomes during Drosophila oogenesis
title The careful control of Polo kinase by APC/C-Ube2C ensures the intercellular transport of germline centrosomes during Drosophila oogenesis
title_full The careful control of Polo kinase by APC/C-Ube2C ensures the intercellular transport of germline centrosomes during Drosophila oogenesis
title_fullStr The careful control of Polo kinase by APC/C-Ube2C ensures the intercellular transport of germline centrosomes during Drosophila oogenesis
title_full_unstemmed The careful control of Polo kinase by APC/C-Ube2C ensures the intercellular transport of germline centrosomes during Drosophila oogenesis
title_short The careful control of Polo kinase by APC/C-Ube2C ensures the intercellular transport of germline centrosomes during Drosophila oogenesis
title_sort careful control of polo kinase by apc/c-ube2c ensures the intercellular transport of germline centrosomes during drosophila oogenesis
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8241486/
https://www.ncbi.nlm.nih.gov/pubmed/34186008
http://dx.doi.org/10.1098/rsob.200371
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