Dynamics of centriole amplification in centrosome-depleted brain multiciliated progenitors

Abstract Reproductive and respiratory organs, along with brain ventricles, are lined by multiciliated epithelial cells (MCC) that generate cilia-powered fluid flows. MCC hijack the centrosome duplication pathway to form hundreds of centrioles and nucleate motile cilia. In these cells, the large majo...

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Autores principales:	Olivier Mercey, Adel Al Jord, Philippe Rostaing, Alexia Mahuzier, Aurélien Fortoul, Amélie-Rose Boudjema, Marion Faucourt, Nathalie Spassky, Alice Meunier
Formato:	article
Lenguaje:	EN
Publicado:	Nature Portfolio 2019
Materias:	Medicine R Science Q
Acceso en línea:	https://doaj.org/article/567fd48fc7314b0484c43d9031f21fd7
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spelling	oai:doaj.org-article:567fd48fc7314b0484c43d9031f21fd72021-12-02T15:08:47ZDynamics of centriole amplification in centrosome-depleted brain multiciliated progenitors10.1038/s41598-019-49416-22045-2322https://doaj.org/article/567fd48fc7314b0484c43d9031f21fd72019-09-01T00:00:00Zhttps://doi.org/10.1038/s41598-019-49416-2https://doaj.org/toc/2045-2322Abstract Reproductive and respiratory organs, along with brain ventricles, are lined by multiciliated epithelial cells (MCC) that generate cilia-powered fluid flows. MCC hijack the centrosome duplication pathway to form hundreds of centrioles and nucleate motile cilia. In these cells, the large majority of procentrioles are formed associated with partially characterized organelles called deuterosomes. We recently challenged the paradigm that deuterosomes and procentrioles are formed de novo by providing data, in brain MCC, suggesting that they are nucleated from the pre-existing centrosomal younger centriole. However, the origin of deuterosomes and procentrioles is still under debate. Here, we further question centrosome importance for deuterosome and centriole amplification. First, we provide additional data confirming that centriole amplification occurs sequentially from the centrosomal region, and that the first procentriole-loaded deuterosomes are associated with the daughter centriole or in the centrosomal centriole vicinity. Then, to further test the requirement of the centrosome in deuterosome and centriole formation, we depleted centrosomal centrioles using a Plk4 inhibitor. We reveal unexpected limited consequences in deuterosome/centriole number in absence of centrosomal centrioles. Notably, in absence of the daughter centriole only, deuterosomes are not seen associated with the mother centriole. In absence of both centrosomal centrioles, procentrioles are still amplified sequentially and with no apparent structural defects. They seem to arise from a focal region, characterized by microtubule convergence and pericentriolar material (PCM) assembly. The relevance of deuterosome association with the daughter centriole as well as the role of the PCM in the focal and sequential genesis of centrioles in absence of centrosomal centrioles are discussed.Olivier MerceyAdel Al JordPhilippe RostaingAlexia MahuzierAurélien FortoulAmélie-Rose BoudjemaMarion FaucourtNathalie SpasskyAlice MeunierNature PortfolioarticleMedicineRScienceQENScientific Reports, Vol 9, Iss 1, Pp 1-11 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	Medicine R Science Q
spellingShingle	Medicine R Science Q Olivier Mercey Adel Al Jord Philippe Rostaing Alexia Mahuzier Aurélien Fortoul Amélie-Rose Boudjema Marion Faucourt Nathalie Spassky Alice Meunier Dynamics of centriole amplification in centrosome-depleted brain multiciliated progenitors
description	Abstract Reproductive and respiratory organs, along with brain ventricles, are lined by multiciliated epithelial cells (MCC) that generate cilia-powered fluid flows. MCC hijack the centrosome duplication pathway to form hundreds of centrioles and nucleate motile cilia. In these cells, the large majority of procentrioles are formed associated with partially characterized organelles called deuterosomes. We recently challenged the paradigm that deuterosomes and procentrioles are formed de novo by providing data, in brain MCC, suggesting that they are nucleated from the pre-existing centrosomal younger centriole. However, the origin of deuterosomes and procentrioles is still under debate. Here, we further question centrosome importance for deuterosome and centriole amplification. First, we provide additional data confirming that centriole amplification occurs sequentially from the centrosomal region, and that the first procentriole-loaded deuterosomes are associated with the daughter centriole or in the centrosomal centriole vicinity. Then, to further test the requirement of the centrosome in deuterosome and centriole formation, we depleted centrosomal centrioles using a Plk4 inhibitor. We reveal unexpected limited consequences in deuterosome/centriole number in absence of centrosomal centrioles. Notably, in absence of the daughter centriole only, deuterosomes are not seen associated with the mother centriole. In absence of both centrosomal centrioles, procentrioles are still amplified sequentially and with no apparent structural defects. They seem to arise from a focal region, characterized by microtubule convergence and pericentriolar material (PCM) assembly. The relevance of deuterosome association with the daughter centriole as well as the role of the PCM in the focal and sequential genesis of centrioles in absence of centrosomal centrioles are discussed.
format	article
author	Olivier Mercey Adel Al Jord Philippe Rostaing Alexia Mahuzier Aurélien Fortoul Amélie-Rose Boudjema Marion Faucourt Nathalie Spassky Alice Meunier
author_facet	Olivier Mercey Adel Al Jord Philippe Rostaing Alexia Mahuzier Aurélien Fortoul Amélie-Rose Boudjema Marion Faucourt Nathalie Spassky Alice Meunier
author_sort	Olivier Mercey
title	Dynamics of centriole amplification in centrosome-depleted brain multiciliated progenitors
title_short	Dynamics of centriole amplification in centrosome-depleted brain multiciliated progenitors
title_full	Dynamics of centriole amplification in centrosome-depleted brain multiciliated progenitors
title_fullStr	Dynamics of centriole amplification in centrosome-depleted brain multiciliated progenitors
title_full_unstemmed	Dynamics of centriole amplification in centrosome-depleted brain multiciliated progenitors
title_sort	dynamics of centriole amplification in centrosome-depleted brain multiciliated progenitors
publisher	Nature Portfolio
publishDate	2019
url	https://doaj.org/article/567fd48fc7314b0484c43d9031f21fd7
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Dynamics of centriole amplification in centrosome-depleted brain multiciliated progenitors

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