Multi-scale structures of the mammalian radial spoke and divergence of axonemal complexes in ependymal cilia

Xueming Meng, Cong Xu, Jiawei Li, Benhua Qiu, Jiajun Luo, Qin Hong, Yujie Tong, Chuyu Fang, Yanyan Feng, Rui Ma, Xiangyi Shi, Cheng Lin, Chen Pan, Xueliang Zhu (), Xiumin Yan () and Yao Cong ()
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Xueming Meng: Chinese Academy of Sciences, University of Chinese Academy of Sciences
Cong Xu: Chinese Academy of Sciences, University of Chinese Academy of Sciences
Jiawei Li: Chinese Academy of Sciences, University of Chinese Academy of Sciences
Benhua Qiu: Chinese Academy of Sciences, University of Chinese Academy of Sciences
Jiajun Luo: Chinese Academy of Sciences, University of Chinese Academy of Sciences
Qin Hong: Chinese Academy of Sciences, University of Chinese Academy of Sciences
Yujie Tong: Chinese Academy of Sciences, University of Chinese Academy of Sciences
Chuyu Fang: Chinese Academy of Sciences, University of Chinese Academy of Sciences
Yanyan Feng: Shanghai Jiao Tong University School of Medicine
Rui Ma: Shanghai Nanoport, Thermofisher Scientific
Xiangyi Shi: Shanghai Nanoport, Thermofisher Scientific
Cheng Lin: Chinese Academy of Sciences, University of Chinese Academy of Sciences
Chen Pan: Chinese Academy of Sciences
Xueliang Zhu: Chinese Academy of Sciences, University of Chinese Academy of Sciences
Xiumin Yan: Shanghai Jiao Tong University School of Medicine
Yao Cong: Chinese Academy of Sciences, University of Chinese Academy of Sciences

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

Abstract: Abstract Radial spokes (RS) transmit mechanochemical signals between the central pair (CP) and axonemal dynein arms to coordinate ciliary motility. Atomic-resolution structures of metazoan RS and structures of axonemal complexes in ependymal cilia, whose rhythmic beating drives the circulation of cerebrospinal fluid, however, remain obscure. Here, we present near-atomic resolution cryo-EM structures of mouse RS head-neck complex in both monomer and dimer forms and reveal the intrinsic flexibility of the dimer. We also map the genetic mutations related to primary ciliary dyskinesia and asthenospermia on the head-neck complex. Moreover, we present the cryo-ET and sub-tomogram averaging map of mouse ependymal cilia and build the models for RS1-3, IDAs, and N-DRC. Contrary to the conserved RS structure, our cryo-ET map reveals the lack of IDA-b/c/e and the absence of Tektin filaments within the A-tubule of doublet microtubules in ependymal cilia compared with mammalian respiratory cilia and sperm flagella, further exemplifying the structural diversity of mammalian motile cilia. Our findings shed light on the stepwise mammalian RS assembly mechanism, the coordinated rigid and elastic RS-CP interaction modes beneficial for the regulation of asymmetric ciliary beating, and also facilitate understanding on the etiology of ciliary dyskinesia-related ciliopathies and on the ependymal cilia in the development of hydrocephalus.

Date: 2024
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DOI: 10.1038/s41467-023-44577-1

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