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Multiciliated cell basal bodies align in stereotypical patterns coordinated by the apical cytoskeleton

Multiciliated cells (MCCs) promote fluid flow through coordinated ciliary beating, which requires properly organized basal bodies (BBs). Airway MCCs have large numbers of BBs, which are uniformly oriented and, as we show here, align linearly. The mechanism for BB alignment is unexplored. To study th...

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Detalles Bibliográficos
Autores principales: Herawati, Elisa, Taniguchi, Daisuke, Kanoh, Hatsuho, Tateishi, Kazuhiro, Ishihara, Shuji, Tsukita, Sachiko
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Rockefeller University Press 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5004441/
https://www.ncbi.nlm.nih.gov/pubmed/27573463
http://dx.doi.org/10.1083/jcb.201601023
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author Herawati, Elisa
Taniguchi, Daisuke
Kanoh, Hatsuho
Tateishi, Kazuhiro
Ishihara, Shuji
Tsukita, Sachiko
author_facet Herawati, Elisa
Taniguchi, Daisuke
Kanoh, Hatsuho
Tateishi, Kazuhiro
Ishihara, Shuji
Tsukita, Sachiko
author_sort Herawati, Elisa
collection PubMed
description Multiciliated cells (MCCs) promote fluid flow through coordinated ciliary beating, which requires properly organized basal bodies (BBs). Airway MCCs have large numbers of BBs, which are uniformly oriented and, as we show here, align linearly. The mechanism for BB alignment is unexplored. To study this mechanism, we developed a long-term and high-resolution live-imaging system and used it to observe green fluorescent protein–centrin2–labeled BBs in cultured mouse tracheal MCCs. During MCC differentiation, the BB array adopted four stereotypical patterns, from a clustering “floret” pattern to the linear “alignment.” This alignment process was correlated with BB orientations, revealed by double immunostaining for BBs and their asymmetrically associated basal feet (BF). The BB alignment was disrupted by disturbing apical microtubules with nocodazole and by a BF-depleting Odf2 mutation. We constructed a theoretical model, which indicated that the apical cytoskeleton, acting like a viscoelastic fluid, provides a self-organizing mechanism in tracheal MCCs to align BBs linearly for mucociliary transport.
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spelling pubmed-50044412017-02-28 Multiciliated cell basal bodies align in stereotypical patterns coordinated by the apical cytoskeleton Herawati, Elisa Taniguchi, Daisuke Kanoh, Hatsuho Tateishi, Kazuhiro Ishihara, Shuji Tsukita, Sachiko J Cell Biol Research Articles Multiciliated cells (MCCs) promote fluid flow through coordinated ciliary beating, which requires properly organized basal bodies (BBs). Airway MCCs have large numbers of BBs, which are uniformly oriented and, as we show here, align linearly. The mechanism for BB alignment is unexplored. To study this mechanism, we developed a long-term and high-resolution live-imaging system and used it to observe green fluorescent protein–centrin2–labeled BBs in cultured mouse tracheal MCCs. During MCC differentiation, the BB array adopted four stereotypical patterns, from a clustering “floret” pattern to the linear “alignment.” This alignment process was correlated with BB orientations, revealed by double immunostaining for BBs and their asymmetrically associated basal feet (BF). The BB alignment was disrupted by disturbing apical microtubules with nocodazole and by a BF-depleting Odf2 mutation. We constructed a theoretical model, which indicated that the apical cytoskeleton, acting like a viscoelastic fluid, provides a self-organizing mechanism in tracheal MCCs to align BBs linearly for mucociliary transport. The Rockefeller University Press 2016-08-29 /pmc/articles/PMC5004441/ /pubmed/27573463 http://dx.doi.org/10.1083/jcb.201601023 Text en © 2016 Herawati 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
Herawati, Elisa
Taniguchi, Daisuke
Kanoh, Hatsuho
Tateishi, Kazuhiro
Ishihara, Shuji
Tsukita, Sachiko
Multiciliated cell basal bodies align in stereotypical patterns coordinated by the apical cytoskeleton
title Multiciliated cell basal bodies align in stereotypical patterns coordinated by the apical cytoskeleton
title_full Multiciliated cell basal bodies align in stereotypical patterns coordinated by the apical cytoskeleton
title_fullStr Multiciliated cell basal bodies align in stereotypical patterns coordinated by the apical cytoskeleton
title_full_unstemmed Multiciliated cell basal bodies align in stereotypical patterns coordinated by the apical cytoskeleton
title_short Multiciliated cell basal bodies align in stereotypical patterns coordinated by the apical cytoskeleton
title_sort multiciliated cell basal bodies align in stereotypical patterns coordinated by the apical cytoskeleton
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5004441/
https://www.ncbi.nlm.nih.gov/pubmed/27573463
http://dx.doi.org/10.1083/jcb.201601023
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