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Fibrogranular materials function as organizers to ensure the fidelity of multiciliary assembly

Author

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  • Huijie Zhao

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

  • Qingxia Chen

    (Chinese Academy of Sciences
    ShanghaiTech University)

  • Fan Li

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

  • Lihong Cui

    (Tsinghua University)

  • Lele Xie

    (Chinese Academy of Sciences)

  • Qiongping Huang

    (Chinese Academy of Sciences)

  • Xin Liang

    (Tsinghua University)

  • Jun Zhou

    (Shandong Normal University)

  • Xiumin Yan

    (Chinese Academy of Sciences)

  • Xueliang Zhu

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

Abstract

Multicilia are delicate motile machineries, and how they are accurately assembled is poorly understood. Here, we show that fibrogranular materials (FGMs), large arrays of electron-dense granules specific to multiciliated cells, are essential for their ultrastructural fidelity. Pcm1 forms the granular units that further network into widespread FGMs, which are abundant in spherical FGM cores. FGM cores selectively concentrate multiple important centriole-related proteins as clients, including Cep131 that specifically decorates a foot region of ciliary central pair (CP) microtubules. FGMs also tightly contact deuterosome-procentriole complexes. Disruption of FGMs in mouse cells undergoing multiciliogenesis by Pcm1 RNAi markedly deregulates centriolar targeting of FGM clients, elongates CP-foot, and alters deuterosome size, number, and distribution. Although the multicilia are produced in correct numbers, they display abnormal ultrastructure and motility. Our results suggest that FGMs organize deuterosomes and centriole-related proteins to facilitate the faithful assembly of basal bodies and multiciliary axonemes.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-21506-8
    DOI: 10.1038/s41467-021-21506-8
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    Cited by:

    1. Muqing Cao & Xiaoxiao Zou & Chaoyi Li & Zaisheng Lin & Ni Wang & Zhongju Zou & Youqiong Ye & Joachim Seemann & Beth Levine & Zaiming Tang & Qing Zhong, 2023. "An actin filament branching surveillance system regulates cell cycle progression, cytokinesis and primary ciliogenesis," Nature Communications, Nature, vol. 14(1), pages 1-18, December.

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