Cargando…
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...
Autores principales: | , , , , , , , , , , , , , , , |
---|---|
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 |
_version_ | 1784617684260880384 |
---|---|
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. |
format | Online Article Text |
id | pubmed-8684751 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | The American Society for Cell Biology |
record_format | MEDLINE/PubMed |
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 |
work_keys_str_mv | AT saitohiroko trachealmotileciliainmicerequirecamsap3fortheformationofcentralmicrotubulepairandcoordinatedbeating AT matsukawausamifumiko trachealmotileciliainmicerequirecamsap3fortheformationofcentralmicrotubulepairandcoordinatedbeating AT fujimoritoshihiko trachealmotileciliainmicerequirecamsap3fortheformationofcentralmicrotubulepairandcoordinatedbeating AT kimuratoshiya trachealmotileciliainmicerequirecamsap3fortheformationofcentralmicrotubulepairandcoordinatedbeating AT idetakahiro trachealmotileciliainmicerequirecamsap3fortheformationofcentralmicrotubulepairandcoordinatedbeating AT yamamototakaki trachealmotileciliainmicerequirecamsap3fortheformationofcentralmicrotubulepairandcoordinatedbeating AT shibatatatsuo trachealmotileciliainmicerequirecamsap3fortheformationofcentralmicrotubulepairandcoordinatedbeating AT onouekenta trachealmotileciliainmicerequirecamsap3fortheformationofcentralmicrotubulepairandcoordinatedbeating AT okayamasatoko trachealmotileciliainmicerequirecamsap3fortheformationofcentralmicrotubulepairandcoordinatedbeating AT yonemurashigenobu trachealmotileciliainmicerequirecamsap3fortheformationofcentralmicrotubulepairandcoordinatedbeating AT misakikazuyo trachealmotileciliainmicerequirecamsap3fortheformationofcentralmicrotubulepairandcoordinatedbeating AT sobayurina trachealmotileciliainmicerequirecamsap3fortheformationofcentralmicrotubulepairandcoordinatedbeating AT kakuiyasutaka trachealmotileciliainmicerequirecamsap3fortheformationofcentralmicrotubulepairandcoordinatedbeating AT satomasamitsu trachealmotileciliainmicerequirecamsap3fortheformationofcentralmicrotubulepairandcoordinatedbeating AT toyamika trachealmotileciliainmicerequirecamsap3fortheformationofcentralmicrotubulepairandcoordinatedbeating AT takeichimasatoshi trachealmotileciliainmicerequirecamsap3fortheformationofcentralmicrotubulepairandcoordinatedbeating |