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Native doublet microtubules from Tetrahymena thermophila reveal the importance of outer junction proteins

Author

Listed:
  • Shintaroh Kubo

    (McGill University
    McGill University)

  • Corbin S. Black

    (McGill University
    McGill University)

  • Ewa Joachimiak

    (Nencki Institute of Experimental Biology of Polish Academy of Sciences)

  • Shun Kai Yang

    (McGill University
    McGill University)

  • Thibault Legal

    (McGill University
    McGill University)

  • Katya Peri

    (McGill University
    McGill University)

  • Ahmad Abdelzaher Zaki Khalifa

    (McGill University
    McGill University)

  • Avrin Ghanaeian

    (McGill University
    McGill University)

  • Caitlyn L. McCafferty

    (University of Texas)

  • Melissa Valente-Paterno

    (McGill University
    McGill University)

  • Chelsea Bellis

    (McGill University)

  • Phuong M. Huynh

    (McGill University)

  • Zhe Fan

    (McGill University)

  • Edward M. Marcotte

    (University of Texas)

  • Dorota Wloga

    (Nencki Institute of Experimental Biology of Polish Academy of Sciences)

  • Khanh Huy Bui

    (McGill University
    McGill University)

Abstract

Cilia are ubiquitous eukaryotic organelles responsible for cellular motility and sensory functions. The ciliary axoneme is a microtubule-based cytoskeleton consisting of two central singlets and nine outer doublet microtubules. Cryo-electron microscopy-based studies have revealed a complex network inside the lumen of both tubules composed of microtubule-inner proteins (MIPs). However, the functions of most MIPs remain unknown. Here, we present single-particle cryo-EM-based analyses of the Tetrahymena thermophila native doublet microtubule and identify 42 MIPs. These data shed light on the evolutionarily conserved and diversified roles of MIPs. In addition, we identified MIPs potentially responsible for the assembly and stability of the doublet outer junction. Knockout of the evolutionarily conserved outer junction component CFAP77 moderately diminishes Tetrahymena swimming speed and beat frequency, indicating the important role of CFAP77 and outer junction stability in cilia beating generation and/or regulation.

Suggested Citation

  • Shintaroh Kubo & Corbin S. Black & Ewa Joachimiak & Shun Kai Yang & Thibault Legal & Katya Peri & Ahmad Abdelzaher Zaki Khalifa & Avrin Ghanaeian & Caitlyn L. McCafferty & Melissa Valente-Paterno & Ch, 2023. "Native doublet microtubules from Tetrahymena thermophila reveal the importance of outer junction proteins," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37868-0
    DOI: 10.1038/s41467-023-37868-0
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    References listed on IDEAS

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    1. Kathryn Tunyasuvunakool & Jonas Adler & Zachary Wu & Tim Green & Michal Zielinski & Augustin Žídek & Alex Bridgland & Andrew Cowie & Clemens Meyer & Agata Laydon & Sameer Velankar & Gerard J. Kleywegt, 2021. "Highly accurate protein structure prediction for the human proteome," Nature, Nature, vol. 596(7873), pages 590-596, August.
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    Cited by:

    1. Avrin Ghanaeian & Sumita Majhi & Caitlyn L. McCafferty & Babak Nami & Corbin S. Black & Shun Kai Yang & Thibault Legal & Ophelia Papoulas & Martyna Janowska & Melissa Valente-Paterno & Edward M. Marco, 2023. "Integrated modeling of the Nexin-dynein regulatory complex reveals its regulatory mechanism," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    2. Michelle M. Shimogawa & Angeline S. Wijono & Hui Wang & Jiayan Zhang & Jihui Sha & Natasha Szombathy & Sabeeca Vadakkan & Paula Pelayo & Keya Jonnalagadda & James Wohlschlegel & Z. Hong Zhou & Kent L., 2023. "FAP106 is an interaction hub for assembling microtubule inner proteins at the cilium inner junction," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    3. Jens S. Andersen & Aaran Vijayakumaran & Christopher Godbehere & Esben Lorentzen & Vito Mennella & Kenneth Bødtker Schou, 2024. "Uncovering structural themes across cilia microtubule inner proteins with implications for human cilia function," Nature Communications, Nature, vol. 15(1), pages 1-17, December.

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