1. Structural Biology and Molecular Biophysics

The inner junction complex of the cilia is an interaction hub that involves tubulin post-translational modifications

  1. Ahmad Abdelzaher Zaki Khalifa
  2. Muneyoshi Ichikawa
  3. Daniel Dai
  4. Shintaroh Kubo
  5. Corbin Black
  6. Katya Peri
  7. Thomas S McAlear
  8. Simon Veyron
  9. Shun Kai Yang
  10. Javier Vargas
  11. Susanne Bechstedt
  12. Jean-François Trempe
  13. Khanh Huy Bui  Is a corresponding author
  1. McGill University, Canada
  2. Kyoto University, Japan
https://doi.org/10.7554/eLife.52760
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  1. Ahmad Abdelzaher Zaki Khalifa
  2. Muneyoshi Ichikawa
  3. Daniel Dai
  4. Shintaroh Kubo
  5. Corbin Black
  6. Katya Peri
  7. Thomas S McAlear
  8. Simon Veyron
  9. Shun Kai Yang
  10. Javier Vargas
  11. Susanne Bechstedt
  12. Jean-François Trempe
  13. Khanh Huy Bui
(2020)
The inner junction complex of the cilia is an interaction hub that involves tubulin post-translational modifications
eLife 9:e52760.
https://doi.org/10.7554/eLife.52760
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Abstract

Microtubules are cytoskeletal structures involved in stability, transport and organization in the cell. The building blocks, the α- and β-tubulin heterodimers, form protofilaments that associate laterally into the hollow microtubule. Microtubule also exists as highly stable doublet microtubules in the cilia where stability is needed for ciliary beating and function. The doublet microtubule maintains its stability through interactions at its inner and outer junctions where its A- and B-tubules meet. Here, using cryo-electron microscopy, bioinformatics and mass spectrometry of the doublets of Chlamydomonas reinhardtii and Tetrahymena thermophila, we identified two new inner junction proteins, FAP276 and FAP106, and an inner junction-associated protein, FAP126, thus presenting the complete answer to the inner junction identity and localization. Our structural study of the doublets shows that the inner junction serves as an interaction hub involved tubulin post-translational modification. These interactions contribute to the stability of the doublet and hence, normal ciliary motility.

Data availability

Cryo-EM maps have been deposited in EM data bank (EMDB) with accession numbers of EMD-20855 (48-nm averaged Chlamydomonas doublet), EMD-20858 (16-nm averaged Chlamydomonas IJ region) and EMD-20856 (16-nm averaged Tetrahymena IJ region). The model of IJ of Chlamydomonas is available in Protein Data Bank (PDB) with an accession number of PDB: 6VE7.The mass spectrometry is deposited in DataDryad (doi:10.5061/dryad.d51c59zxt). Available at:https://datadryad.org/stash/share/bkrXp5Ww0iQUis6ocuEya2ivHWQ_YiTFO-VLeIjkQcM

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Author details

  1. Ahmad Abdelzaher Zaki Khalifa

    Department of Anatomy and Cell Biology, McGill University, Montréal, Canada
    Competing interests
    The authors declare that no competing interests exist.

  2. Muneyoshi Ichikawa

    Department of Anatomy and Cell Biology, McGill University, Montréal, Canada
    Competing interests
    The authors declare that no competing interests exist.

  3. Daniel Dai

    Department of Anatomy and Cell Biology, McGill University, Montréal, Canada
    Competing interests
    The authors declare that no competing interests exist.

  4. Shintaroh Kubo

    Department of Biophysics, Graduate School of Science, Kyoto University, Kyoto, Japan
    Competing interests
    The authors declare that no competing interests exist.

  5. Corbin Black

    Department of Anatomy and Cell Biology, McGill University, Montréal, Canada
    Competing interests
    The authors declare that no competing interests exist.

  6. Katya Peri

    Department of Anatomy and Cell Biology, McGill University, Montréal, Canada
    Competing interests
    The authors declare that no competing interests exist.

  7. Thomas S McAlear

    Department of Anatomy and Cell Biology, McGill University, Montréal, Canada
    Competing interests
    The authors declare that no competing interests exist.

  8. Simon Veyron

    Department of Pharmacology, McGill University, Montréal, Canada
    Competing interests
    The authors declare that no competing interests exist.

  9. Shun Kai Yang

    Department of Anatomy and Cell Biology, McGill University, Montréal, Canada
    Competing interests
    The authors declare that no competing interests exist.

  10. Javier Vargas

    Department of Anatomy and Cell Biology, McGill University, Montréal, Canada
    Competing interests
    The authors declare that no competing interests exist.

  11. Susanne Bechstedt

    Department of Anatomy and Cell Biology, McGill University, Montréal, Canada
    Competing interests
    The authors declare that no competing interests exist.

  12. Jean-François Trempe

    Department of Pharmacology, McGill University, Montréal, Canada
    Competing interests
    The authors declare that no competing interests exist.

  13. Khanh Huy Bui

    Department of Anatomy and Cell Biology, McGill University, Montréal, Canada
    For correspondence
    huy.bui@mcgill.ca
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2814-9889

Funding

Canadian Institutes of Health Research (PJT-156354)

  • Khanh Huy Bui

Natural Sciences and Engineering Research Council of Canada (RGPIN-2016-04954)

  • Khanh Huy Bui

Natural Sciences and Engineering Research Council of Canada (RGPIN-2018-04813)

  • Javier Vargas

Canada Institute For Advanced Research (Arzieli Global Scholar Program)

  • Khanh Huy Bui

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Andrew P Carter, MRC Laboratory of Molecular Biology, United Kingdom

Publication history

  1. Received: October 15, 2019
  2. Accepted: January 16, 2020
  3. Accepted Manuscript published: January 17, 2020 (version 1)
  4. Version of Record published: January 31, 2020 (version 2)

Copyright

© 2020, Khalifa et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Ahmad Abdelzaher Zaki Khalifa
  2. Muneyoshi Ichikawa
  3. Daniel Dai
  4. Shintaroh Kubo
  5. Corbin Black
  6. Katya Peri
  7. Thomas S McAlear
  8. Simon Veyron
  9. Shun Kai Yang
  10. Javier Vargas
  11. Susanne Bechstedt
  12. Jean-François Trempe
  13. Khanh Huy Bui
(2020)
The inner junction complex of the cilia is an interaction hub that involves tubulin post-translational modifications
eLife 9:e52760.
https://doi.org/10.7554/eLife.52760

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