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Directional ciliary beats across epithelia require Ccdc57-mediated coupling between axonemal orientation and basal body polarity

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  • Xinwen Pan

    (Chinese Academy of Sciences
    ShanghaiTech University)

  • Chuyu Fang

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Chuan Shen

    (Chinese Academy of Sciences
    ShanghaiTech University)

  • Xixia Li

    (Chinese Academy of Sciences)

  • Lele Xie

    (Chinese Academy of Sciences)

  • Luan Li

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Shan Huang

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Xiumin Yan

    (Shanghai Jiao Tong University School of Medicine)

  • Xueliang Zhu

    (Chinese Academy of Sciences
    ShanghaiTech University
    University of Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

Abstract

Motile cilia unify their axonemal orientations (AOs), or beat directions, across epithelia to drive liquid flows. This planar polarity results from cytoskeleton-driven swiveling of basal foot (BF), a basal body (BB) appendage coincident with the AO, in response to regulatory cues. How and when the BF-AO relationship is established, however, are unaddressed. Here, we show that the BF-AO coupling occurs during rotational polarizations of BBs and requires Ccdc57. Ccdc57 localizes on BBs as a rotationally-asymmetric punctum, which polarizes away from the BF in BBs having achieved the rotational polarity to probably fix the BF-AO relationship. Consistently, Ccdc57-deficient ependymal multicilia lack the BF-AO coupling and display directional beats at only single cell level. Ccdc57 −/− tracheal multicilia also fail to fully align their BFs. Furthermore, Ccdc57 −/− mice manifest severe hydrocephalus, due to impaired cerebrospinal fluid flow, and high mortality. These findings unravel mechanisms governing the planar polarity of epithelial motile cilia.

Suggested Citation

  • Xinwen Pan & Chuyu Fang & Chuan Shen & Xixia Li & Lele Xie & Luan Li & Shan Huang & Xiumin Yan & Xueliang Zhu, 2024. "Directional ciliary beats across epithelia require Ccdc57-mediated coupling between axonemal orientation and basal body polarity," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-54766-1
    DOI: 10.1038/s41467-024-54766-1
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    References listed on IDEAS

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    1. Hao Liu & Jianqun Zheng & Lei Zhu & Lele Xie & Yawen Chen & Yirong Zhang & Wei Zhang & Yue Yin & Chao Peng & Jun Zhou & Xueliang Zhu & Xiumin Yan, 2021. "Wdr47, Camsaps, and Katanin cooperate to generate ciliary central microtubules," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    2. Daniel K. Clare & Jérémy Magescas & Tristan Piolot & Maud Dumoux & Christine Vesque & Evelyne Pichard & Tien Dang & Boris Duvauchelle & Françoise Poirier & Delphine Delacour, 2014. "Basal foot MTOC organizes pillar MTs required for coordination of beating cilia," Nature Communications, Nature, vol. 5(1), pages 1-9, December.
    3. Huijie Zhao & Qingxia Chen & Fan Li & Lihong Cui & Lele Xie & Qiongping Huang & Xin Liang & Jun Zhou & Xiumin Yan & Xueliang Zhu, 2021. "Fibrogranular materials function as organizers to ensure the fidelity of multiciliary assembly," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
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