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

Xinwen Pan, Chuyu Fang, Chuan Shen, Xixia Li, Lele Xie, Luan Li, Shan Huang, Xiumin Yan () and Xueliang Zhu ()
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Xinwen Pan: Chinese Academy of Sciences
Chuyu Fang: Chinese Academy of Sciences
Chuan Shen: Chinese Academy of Sciences
Xixia Li: Chinese Academy of Sciences
Lele Xie: Chinese Academy of Sciences
Luan Li: Chinese Academy of Sciences
Shan Huang: Chinese Academy of Sciences
Xiumin Yan: Shanghai Jiao Tong University School of Medicine
Xueliang Zhu: Chinese Academy of Sciences

Nature Communications, 2024, vol. 15, issue 1, 1-16

Abstract: 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.

Date: 2024
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DOI: 10.1038/s41467-024-54766-1

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