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Tracheal motile cilia in mice require CAMSAP3 for the formation of central microtubule pair and coordinated beating

Motile cilia of multiciliated epithelial cells undergo synchronized beating to produce fluid flow along the luminal surface of various organs. Each motile cilium consists of an axoneme and a basal body (BB), which are linked by a “transition zone” (TZ). The axoneme exhibits a characteristic 9+2 micr...

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Autores principales: Saito, Hiroko, Matsukawa-Usami, Fumiko, Fujimori, Toshihiko, Kimura, Toshiya, Ide, Takahiro, Yamamoto, Takaki, Shibata, Tatsuo, Onoue, Kenta, Okayama, Satoko, Yonemura, Shigenobu, Misaki, Kazuyo, Soba, Yurina, Kakui, Yasutaka, Sato, Masamitsu, Toya, Mika, Takeichi, Masatoshi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The American Society for Cell Biology 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8684751/
https://www.ncbi.nlm.nih.gov/pubmed/34319756
http://dx.doi.org/10.1091/mbc.E21-06-0303
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author Saito, Hiroko
Matsukawa-Usami, Fumiko
Fujimori, Toshihiko
Kimura, Toshiya
Ide, Takahiro
Yamamoto, Takaki
Shibata, Tatsuo
Onoue, Kenta
Okayama, Satoko
Yonemura, Shigenobu
Misaki, Kazuyo
Soba, Yurina
Kakui, Yasutaka
Sato, Masamitsu
Toya, Mika
Takeichi, Masatoshi
author_facet Saito, Hiroko
Matsukawa-Usami, Fumiko
Fujimori, Toshihiko
Kimura, Toshiya
Ide, Takahiro
Yamamoto, Takaki
Shibata, Tatsuo
Onoue, Kenta
Okayama, Satoko
Yonemura, Shigenobu
Misaki, Kazuyo
Soba, Yurina
Kakui, Yasutaka
Sato, Masamitsu
Toya, Mika
Takeichi, Masatoshi
author_sort Saito, Hiroko
collection PubMed
description Motile cilia of multiciliated epithelial cells undergo synchronized beating to produce fluid flow along the luminal surface of various organs. Each motile cilium consists of an axoneme and a basal body (BB), which are linked by a “transition zone” (TZ). The axoneme exhibits a characteristic 9+2 microtubule arrangement important for ciliary motion, but how this microtubule system is generated is not yet fully understood. Here we show that calmodulin-regulated spectrin-associated protein 3 (CAMSAP3), a protein that can stabilize the minus-end of a microtubule, concentrates at multiple sites of the cilium–BB complex, including the upper region of the TZ or the axonemal basal plate (BP) where the central pair of microtubules (CP) initiates. CAMSAP3 dysfunction resulted in loss of the CP and partial distortion of the BP, as well as the failure of multicilia to undergo synchronized beating. These findings suggest that CAMSAP3 plays pivotal roles in the formation or stabilization of the CP by localizing at the basal region of the axoneme and thereby supports the coordinated motion of multicilia in airway epithelial cells.
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spelling pubmed-86847512022-01-14 Tracheal motile cilia in mice require CAMSAP3 for the formation of central microtubule pair and coordinated beating Saito, Hiroko Matsukawa-Usami, Fumiko Fujimori, Toshihiko Kimura, Toshiya Ide, Takahiro Yamamoto, Takaki Shibata, Tatsuo Onoue, Kenta Okayama, Satoko Yonemura, Shigenobu Misaki, Kazuyo Soba, Yurina Kakui, Yasutaka Sato, Masamitsu Toya, Mika Takeichi, Masatoshi Mol Biol Cell Articles Motile cilia of multiciliated epithelial cells undergo synchronized beating to produce fluid flow along the luminal surface of various organs. Each motile cilium consists of an axoneme and a basal body (BB), which are linked by a “transition zone” (TZ). The axoneme exhibits a characteristic 9+2 microtubule arrangement important for ciliary motion, but how this microtubule system is generated is not yet fully understood. Here we show that calmodulin-regulated spectrin-associated protein 3 (CAMSAP3), a protein that can stabilize the minus-end of a microtubule, concentrates at multiple sites of the cilium–BB complex, including the upper region of the TZ or the axonemal basal plate (BP) where the central pair of microtubules (CP) initiates. CAMSAP3 dysfunction resulted in loss of the CP and partial distortion of the BP, as well as the failure of multicilia to undergo synchronized beating. These findings suggest that CAMSAP3 plays pivotal roles in the formation or stabilization of the CP by localizing at the basal region of the axoneme and thereby supports the coordinated motion of multicilia in airway epithelial cells. The American Society for Cell Biology 2021-10-01 /pmc/articles/PMC8684751/ /pubmed/34319756 http://dx.doi.org/10.1091/mbc.E21-06-0303 Text en © 2021 Saito et al. “ASCB®,” “The American Society for Cell Biology®,” and “Molecular Biology of the Cell®” are registered trademarks of The American Society for Cell Biology. https://creativecommons.org/licenses/by-nc-sa/3.0/This article is distributed by The American Society for Cell Biology under license from the author(s). Two months after publication it is available to the public under an Attribution–Noncommercial–Share Alike 3.0 Unported Creative Commons License.
spellingShingle Articles
Saito, Hiroko
Matsukawa-Usami, Fumiko
Fujimori, Toshihiko
Kimura, Toshiya
Ide, Takahiro
Yamamoto, Takaki
Shibata, Tatsuo
Onoue, Kenta
Okayama, Satoko
Yonemura, Shigenobu
Misaki, Kazuyo
Soba, Yurina
Kakui, Yasutaka
Sato, Masamitsu
Toya, Mika
Takeichi, Masatoshi
Tracheal motile cilia in mice require CAMSAP3 for the formation of central microtubule pair and coordinated beating
title Tracheal motile cilia in mice require CAMSAP3 for the formation of central microtubule pair and coordinated beating
title_full Tracheal motile cilia in mice require CAMSAP3 for the formation of central microtubule pair and coordinated beating
title_fullStr Tracheal motile cilia in mice require CAMSAP3 for the formation of central microtubule pair and coordinated beating
title_full_unstemmed Tracheal motile cilia in mice require CAMSAP3 for the formation of central microtubule pair and coordinated beating
title_short Tracheal motile cilia in mice require CAMSAP3 for the formation of central microtubule pair and coordinated beating
title_sort tracheal motile cilia in mice require camsap3 for the formation of central microtubule pair and coordinated beating
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8684751/
https://www.ncbi.nlm.nih.gov/pubmed/34319756
http://dx.doi.org/10.1091/mbc.E21-06-0303
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