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Cilia locally synthesize proteins to sustain their ultrastructure and functions

Author

Listed:
  • Kai Hao

    (State Key Laboratory of Cell Biology, Shanghai Institute of Biochemistry and Cell Biology, Center for Excellence in Molecular Cell Science, Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Yawen Chen

    (State Key Laboratory of Cell Biology, Shanghai Institute of Biochemistry and Cell Biology, Center for Excellence in Molecular Cell Science, Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Xiumin Yan

    (Ministry of Education-Shanghai Key Laboratory of Children’s Environmental Health, Institute of Early Life Health, Xinhua Hospital, Shanghai Jiao Tong University School of Medicine)

  • Xueliang Zhu

    (State Key Laboratory of Cell Biology, Shanghai Institute of Biochemistry and Cell Biology, Center for Excellence in Molecular Cell Science, Chinese Academy of Sciences
    University of Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

Abstract

Cilia are microtubule-based hair-like organelles propelling locomotion and extracellular liquid flow or sensing environmental stimuli. As cilia are diffusion barrier-gated subcellular compartments, their protein components are thought to come from the cell body through intraflagellar transport or diffusion. Here we show that cilia locally synthesize proteins to maintain their structure and functions. Multicilia of mouse ependymal cells are abundant in ribosomal proteins, translation initiation factors, and RNA, including 18 S rRNA and tubulin mRNA. The cilia actively generate nascent peptides, including those of tubulin. mRNA-binding protein Fmrp localizes in ciliary central lumen and appears to function in mRNA delivery into the cilia. Its depletion by RNAi impairs ciliary local translation and induces multicilia degeneration. Expression of exogenous Fmrp, but not an isoform tethered to mitochondria, rescues the degeneration defects. Therefore, local translation defects in cilia might contribute to the pathology of ciliopathies and other diseases such as Fragile X syndrome.

Suggested Citation

  • Kai Hao & Yawen Chen & Xiumin Yan & Xueliang Zhu, 2021. "Cilia locally synthesize proteins to sustain their ultrastructure and functions," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-27298-1
    DOI: 10.1038/s41467-021-27298-1
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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. Manuel Ascano & Neelanjan Mukherjee & Pradeep Bandaru & Jason B. Miller & Jeffrey D. Nusbaum & David L. Corcoran & Christine Langlois & Mathias Munschauer & Scott Dewell & Markus Hafner & Zev Williams, 2012. "FMRP targets distinct mRNA sequence elements to regulate protein expression," Nature, Nature, vol. 492(7429), pages 382-386, December.
    3. Andreas M. Anger & Jean-Paul Armache & Otto Berninghausen & Michael Habeck & Marion Subklewe & Daniel N. Wilson & Roland Beckmann, 2013. "Structures of the human and Drosophila 80S ribosome," Nature, Nature, vol. 497(7447), pages 80-85, May.
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