The careful control of Polo kinase by APC/C-Ube2C ensures the intercellular transport of germline centrosomes during <italic toggle="yes">Drosophila</italic> 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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Main Authors: Alexis Leah Braun, Francesco Meghini, Gema Villa-Fombuena, Morgane Guermont, Elisa Fernandez-Martinez, Zhang Qian, Maria Dolores Martín-Bermudo, Acaimo González-Reyes, David Moore Glover, Yuu Kimata
Format: Article
Language:English
Published: The Royal Society 2021-06-01
Series:Open Biology
Subjects:
Online Access:https://royalsocietypublishing.org/doi/10.1098/rsob.200371
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spelling doaj-5e10494a01c84c0887c8e75732aaa2e02021-06-29T23:05:24ZengThe Royal SocietyOpen Biology2046-24412021-06-0111610.1098/rsob.200371The careful control of Polo kinase by APC/C-Ube2C ensures the intercellular transport of germline centrosomes during <italic toggle="yes">Drosophila</italic> oogenesisAlexis Leah Braun0Francesco Meghini1Gema Villa-Fombuena2Morgane Guermont3Elisa Fernandez-Martinez4Zhang Qian5Maria Dolores Martín-Bermudo6Acaimo González-Reyes7David Moore Glover8Yuu Kimata9Department of Genetics, University of Cambridge, Cambridge CB2 3EH, UKDepartment of Genetics, University of Cambridge, Cambridge CB2 3EH, UKCentro Andaluz de Biología del Desarrollo, CSIC/Universidad Pablo de Olavide/JA, Carretera de Utrera km 1, 41013 Sevilla, SpainDepartment of Genetics, University of Cambridge, Cambridge CB2 3EH, UKDepartment of Genetics, University of Cambridge, Cambridge CB2 3EH, UKSchool of Life Science and Technology, ShanghaiTech University, 393 Middle Huaxia Road, Shanghai 201210, People's Republic of ChinaCentro Andaluz de Biología del Desarrollo, CSIC/Universidad Pablo de Olavide/JA, Carretera de Utrera km 1, 41013 Sevilla, SpainCentro Andaluz de Biología del Desarrollo, CSIC/Universidad Pablo de Olavide/JA, Carretera de Utrera km 1, 41013 Sevilla, SpainDepartment of Genetics, University of Cambridge, Cambridge CB2 3EH, UKDepartment of Genetics, University of Cambridge, Cambridge CB2 3EH, UKA 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.https://royalsocietypublishing.org/doi/10.1098/rsob.200371DrosophilagermlinecentrosomesPolo kinaseAPC/Cfertility
collection DOAJ
language English
format Article
sources DOAJ
author Alexis Leah Braun
Francesco Meghini
Gema Villa-Fombuena
Morgane Guermont
Elisa Fernandez-Martinez
Zhang Qian
Maria Dolores Martín-Bermudo
Acaimo González-Reyes
David Moore Glover
Yuu Kimata
spellingShingle Alexis Leah Braun
Francesco Meghini
Gema Villa-Fombuena
Morgane Guermont
Elisa Fernandez-Martinez
Zhang Qian
Maria Dolores Martín-Bermudo
Acaimo González-Reyes
David Moore Glover
Yuu Kimata
The careful control of Polo kinase by APC/C-Ube2C ensures the intercellular transport of germline centrosomes during <italic toggle="yes">Drosophila</italic> oogenesis
Open Biology
Drosophila
germline
centrosomes
Polo kinase
APC/C
fertility
author_facet Alexis Leah Braun
Francesco Meghini
Gema Villa-Fombuena
Morgane Guermont
Elisa Fernandez-Martinez
Zhang Qian
Maria Dolores Martín-Bermudo
Acaimo González-Reyes
David Moore Glover
Yuu Kimata
author_sort Alexis Leah Braun
title The careful control of Polo kinase by APC/C-Ube2C ensures the intercellular transport of germline centrosomes during <italic toggle="yes">Drosophila</italic> oogenesis
title_short The careful control of Polo kinase by APC/C-Ube2C ensures the intercellular transport of germline centrosomes during <italic toggle="yes">Drosophila</italic> oogenesis
title_full The careful control of Polo kinase by APC/C-Ube2C ensures the intercellular transport of germline centrosomes during <italic toggle="yes">Drosophila</italic> oogenesis
title_fullStr The careful control of Polo kinase by APC/C-Ube2C ensures the intercellular transport of germline centrosomes during <italic toggle="yes">Drosophila</italic> oogenesis
title_full_unstemmed The careful control of Polo kinase by APC/C-Ube2C ensures the intercellular transport of germline centrosomes during <italic toggle="yes">Drosophila</italic> oogenesis
title_sort careful control of polo kinase by apc/c-ube2c ensures the intercellular transport of germline centrosomes during <italic toggle="yes">drosophila</italic> oogenesis
publisher The Royal Society
series Open Biology
issn 2046-2441
publishDate 2021-06-01
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.
topic Drosophila
germline
centrosomes
Polo kinase
APC/C
fertility
url https://royalsocietypublishing.org/doi/10.1098/rsob.200371
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