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Fibrogranular materials function as organizers to ensure the fidelity of multiciliary assembly

Multicilia are delicate motile machineries, and how they are accurately assembled is poorly understood. Here, we show that fibrogranular materials (FGMs), large arrays of electron-dense granules specific to multiciliated cells, are essential for their ultrastructural fidelity. Pcm1 forms the granula...

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Autores principales: Zhao, Huijie, Chen, Qingxia, Li, Fan, Cui, Lihong, Xie, Lele, Huang, Qiongping, Liang, Xin, Zhou, Jun, Yan, Xiumin, Zhu, Xueliang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7904937/
https://www.ncbi.nlm.nih.gov/pubmed/33627667
http://dx.doi.org/10.1038/s41467-021-21506-8
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author Zhao, Huijie
Chen, Qingxia
Li, Fan
Cui, Lihong
Xie, Lele
Huang, Qiongping
Liang, Xin
Zhou, Jun
Yan, Xiumin
Zhu, Xueliang
author_facet Zhao, Huijie
Chen, Qingxia
Li, Fan
Cui, Lihong
Xie, Lele
Huang, Qiongping
Liang, Xin
Zhou, Jun
Yan, Xiumin
Zhu, Xueliang
author_sort Zhao, Huijie
collection PubMed
description Multicilia are delicate motile machineries, and how they are accurately assembled is poorly understood. Here, we show that fibrogranular materials (FGMs), large arrays of electron-dense granules specific to multiciliated cells, are essential for their ultrastructural fidelity. Pcm1 forms the granular units that further network into widespread FGMs, which are abundant in spherical FGM cores. FGM cores selectively concentrate multiple important centriole-related proteins as clients, including Cep131 that specifically decorates a foot region of ciliary central pair (CP) microtubules. FGMs also tightly contact deuterosome-procentriole complexes. Disruption of FGMs in mouse cells undergoing multiciliogenesis by Pcm1 RNAi markedly deregulates centriolar targeting of FGM clients, elongates CP-foot, and alters deuterosome size, number, and distribution. Although the multicilia are produced in correct numbers, they display abnormal ultrastructure and motility. Our results suggest that FGMs organize deuterosomes and centriole-related proteins to facilitate the faithful assembly of basal bodies and multiciliary axonemes.
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spelling pubmed-79049372021-03-11 Fibrogranular materials function as organizers to ensure the fidelity of multiciliary assembly Zhao, Huijie Chen, Qingxia Li, Fan Cui, Lihong Xie, Lele Huang, Qiongping Liang, Xin Zhou, Jun Yan, Xiumin Zhu, Xueliang Nat Commun Article Multicilia are delicate motile machineries, and how they are accurately assembled is poorly understood. Here, we show that fibrogranular materials (FGMs), large arrays of electron-dense granules specific to multiciliated cells, are essential for their ultrastructural fidelity. Pcm1 forms the granular units that further network into widespread FGMs, which are abundant in spherical FGM cores. FGM cores selectively concentrate multiple important centriole-related proteins as clients, including Cep131 that specifically decorates a foot region of ciliary central pair (CP) microtubules. FGMs also tightly contact deuterosome-procentriole complexes. Disruption of FGMs in mouse cells undergoing multiciliogenesis by Pcm1 RNAi markedly deregulates centriolar targeting of FGM clients, elongates CP-foot, and alters deuterosome size, number, and distribution. Although the multicilia are produced in correct numbers, they display abnormal ultrastructure and motility. Our results suggest that FGMs organize deuterosomes and centriole-related proteins to facilitate the faithful assembly of basal bodies and multiciliary axonemes. Nature Publishing Group UK 2021-02-24 /pmc/articles/PMC7904937/ /pubmed/33627667 http://dx.doi.org/10.1038/s41467-021-21506-8 Text en © The Author(s) 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Zhao, Huijie
Chen, Qingxia
Li, Fan
Cui, Lihong
Xie, Lele
Huang, Qiongping
Liang, Xin
Zhou, Jun
Yan, Xiumin
Zhu, Xueliang
Fibrogranular materials function as organizers to ensure the fidelity of multiciliary assembly
title Fibrogranular materials function as organizers to ensure the fidelity of multiciliary assembly
title_full Fibrogranular materials function as organizers to ensure the fidelity of multiciliary assembly
title_fullStr Fibrogranular materials function as organizers to ensure the fidelity of multiciliary assembly
title_full_unstemmed Fibrogranular materials function as organizers to ensure the fidelity of multiciliary assembly
title_short Fibrogranular materials function as organizers to ensure the fidelity of multiciliary assembly
title_sort fibrogranular materials function as organizers to ensure the fidelity of multiciliary assembly
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7904937/
https://www.ncbi.nlm.nih.gov/pubmed/33627667
http://dx.doi.org/10.1038/s41467-021-21506-8
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