Super-resolution microscopy reveals coupling between mammalian centriole subdistal appendages and distal appendages

  1. Weng Man Chong
  2. Won-Jing Wang
  3. Chien-Hui Lo
  4. Tzu-Yuan Chiu
  5. Ting-Jui Chang
  6. You-Pi Liu
  7. Barbara Tanos
  8. Gregory Mazo
  9. Meng-Fu Bryan Tsou
  10. Wann-Neng Jane
  11. T Tony Yang  Is a corresponding author
  12. Jung-Chi Liao  Is a corresponding author
  1. Academia Sinica, Taiwan, Republic of China
  2. National Yang-Ming University, Taiwan, Republic of China
  3. Institute of Cancer Research, United Kingdom
  4. Memorial Sloan Kettering Cancer Center, United States
  5. National Taiwan University, Taiwan, Republic of China

Abstract

Subdistal appendages (sDAPs) are centriolar elements observed proximal to the distal appendages (DAPs) in vertebrates. Despite their obvious presence, structural and functional understanding of sDAPs remains elusive. Here, by combining super-resolved localization analysis and CRISPR-Cas9 genetic perturbation, we find that, although DAPs and sDAPs are primarily responsible for distinct functions in ciliogenesis and microtubule anchoring respectively, the presence of one element actually affects the positioning of the other. Specifically, we find dual layers of both ODF2 and CEP89, where their localizations are differentially regulated by DAP and sDAP integrity. DAP depletion relaxes longitudinal occupancy of sDAP protein ninein to cover the DAP region, implying a role of DAPs in sDAP positioning. Removing sDAPs alter the distal border of centrosomal γ-tubulins, illustrating a new role of sDAPs. Together, our results provide an architectural framework of sDAPs to shed light on functional understanding, surprisingly revealing the coupling between DAPs and sDAPs.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files.

Article and author information

Author details

  1. Weng Man Chong

    Institute of Atomic and Molecular Sciences, Academia Sinica, Taipei, Taiwan, Republic of China
    Competing interests
    The authors declare that no competing interests exist.
  2. Won-Jing Wang

    Institute of Biochemistry and Molecular Biology, College of Life Sciences, National Yang-Ming University, Taipei, Taiwan, Republic of China
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9733-0839
  3. Chien-Hui Lo

    Institute of Biochemistry and Molecular Biology, College of Life Sciences, National Yang-Ming University, Taipei, Taiwan, Republic of China
    Competing interests
    The authors declare that no competing interests exist.
  4. Tzu-Yuan Chiu

    Institute of Atomic and Molecular Sciences, Academia Sinica, Taipei, Taiwan, Republic of China
    Competing interests
    The authors declare that no competing interests exist.
  5. Ting-Jui Chang

    Institute of Atomic and Molecular Sciences, Academia Sinica, Taipei, Taiwan, Republic of China
    Competing interests
    The authors declare that no competing interests exist.
  6. You-Pi Liu

    Institute of Atomic and Molecular Sciences, Academia Sinica, Taipei, Taiwan, Republic of China
    Competing interests
    The authors declare that no competing interests exist.
  7. Barbara Tanos

    Cancer Therapeutics, Institute of Cancer Research, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  8. Gregory Mazo

    Dermatology Service, Department of Medicine, Memorial Sloan Kettering Cancer Center, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Meng-Fu Bryan Tsou

    Cell Biology Program, Memorial Sloan Kettering Cancer Center, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2159-8836
  10. Wann-Neng Jane

    Institute of Plant and Microbial Biology, Academia Sinica, Taipei, Taiwan, Republic of China
    Competing interests
    The authors declare that no competing interests exist.
  11. T Tony Yang

    Department of Electrical Engineering, National Taiwan University, Taipei, Taiwan, Republic of China
    For correspondence
    tonyyang@ntu.edu.tw
    Competing interests
    The authors declare that no competing interests exist.
  12. Jung-Chi Liao

    Institute of Atomic and Molecular Sciences, Academia Sinica, Taipei, Taiwan, Republic of China
    For correspondence
    jcliao@iams.sinica.edu.tw
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4323-6318

Funding

Ministry of Science and Technology, Taiwan (107-2112-M-001-037)

  • Weng Man Chong
  • Tzu-Yuan Chiu
  • Ting-Jui Chang
  • You-Pi Liu
  • T Tony Yang
  • Jung-Chi Liao

Ministry of Science and Technology, Taiwan (107-2313-B-001-009)

  • Weng Man Chong
  • Tzu-Yuan Chiu
  • Ting-Jui Chang
  • You-Pi Liu
  • T Tony Yang
  • Jung-Chi Liao

Academia Sinica (2317-1040300)

  • Weng Man Chong
  • Tzu-Yuan Chiu
  • Ting-Jui Chang
  • You-Pi Liu
  • T Tony Yang
  • Jung-Chi Liao

Ministry of Science and Technology, Taiwan (108-2313-B-010-001)

  • Won-Jing Wang

Ministry of Science and Technology, Taiwan (108-2628-B-010-007)

  • Won-Jing Wang

Ministry of Science and Technology, Taiwan (108-2638-B-010-001 -MY2)

  • Won-Jing Wang

National Institutes of Health (GM088253)

  • Meng-Fu Bryan Tsou

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

Reviewing Editor

  1. Anna Akhmanova, Utrecht University, Netherlands

Version history

  1. Received: November 13, 2019
  2. Accepted: April 2, 2020
  3. Accepted Manuscript published: April 3, 2020 (version 1)
  4. Version of Record published: April 21, 2020 (version 2)

Copyright

© 2020, Chong 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. Weng Man Chong
  2. Won-Jing Wang
  3. Chien-Hui Lo
  4. Tzu-Yuan Chiu
  5. Ting-Jui Chang
  6. You-Pi Liu
  7. Barbara Tanos
  8. Gregory Mazo
  9. Meng-Fu Bryan Tsou
  10. Wann-Neng Jane
  11. T Tony Yang
  12. Jung-Chi Liao
(2020)
Super-resolution microscopy reveals coupling between mammalian centriole subdistal appendages and distal appendages
eLife 9:e53580.
https://doi.org/10.7554/eLife.53580

Share this article

https://doi.org/10.7554/eLife.53580

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