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Inner lumen proteins stabilize doublet microtubules in cilia and flagella

Author

Listed:
  • Mikito Owa

    (The University of Tokyo)

  • Takayuki Uchihashi

    (Nagoya University)

  • Haru-aki Yanagisawa

    (The University of Tokyo)

  • Takashi Yamano

    (Kyoto University)

  • Hiro Iguchi

    (Kyoto University)

  • Hideya Fukuzawa

    (Kyoto University)

  • Ken-ichi Wakabayashi

    (Tokyo Institute of Technology)

  • Toshio Ando

    (Kanazawa University)

  • Masahide Kikkawa

    (The University of Tokyo)

Abstract

Motile cilia are microtubule-based organelles that play important roles in most eukaryotes. Although axonemal microtubules are sufficiently stable to withstand their beating motion, it remains unknown how they are stabilized while serving as tracks for axonemal dyneins. To address this question, we have identified two uncharacterized proteins, FAP45 and FAP52, as microtubule inner proteins (MIPs) in Chlamydomonas. These proteins are conserved among eukaryotes with motile cilia. Using cryo-electron tomography (cryo-ET) and high-speed atomic force microscopy (HS-AFM), we show that lack of these proteins leads to a loss of inner protrusions in B-tubules and less stable microtubules. These protrusions are located near the inner junctions of doublet microtubules and lack of both FAP52 and a known inner junction protein FAP20 results in detachment of the B-tubule from the A-tubule, as well as flagellar shortening. These results demonstrate that FAP45 and FAP52 bind to the inside of microtubules and stabilize ciliary axonemes.

Suggested Citation

  • Mikito Owa & Takayuki Uchihashi & Haru-aki Yanagisawa & Takashi Yamano & Hiro Iguchi & Hideya Fukuzawa & Ken-ichi Wakabayashi & Toshio Ando & Masahide Kikkawa, 2019. "Inner lumen proteins stabilize doublet microtubules in cilia and flagella," Nature Communications, Nature, vol. 10(1), pages 1-10, December.
    • Handle: RePEc:nat:natcom:v:10:y:2019:i:1:d:10.1038_s41467-019-09051-x
    DOI: 10.1038/s41467-019-09051-x
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    Cited by:

    1. Paul W. Chrystal & Nils J. Lambacher & Lance P. Doucette & James Bellingham & Elena R. Schiff & Nicole C. L. Noel & Chunmei Li & Sofia Tsiropoulou & Geoffrey A. Casey & Yi Zhai & Nathan J. Nadolski & , 2022. "The inner junction protein CFAP20 functions in motile and non-motile cilia and is critical for vision," Nature Communications, Nature, vol. 13(1), pages 1-22, December.
    2. 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 & Yao Cong, 2024. "Multi-scale structures of the mammalian radial spoke and divergence of axonemal complexes in ependymal cilia," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    3. 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.
    4. 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.

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