Insights into centriole geometry revealed by cryoTomography of doublet and triplet centrioles

  1. Garrett A Greenan
  2. Bettina Keszthelyi
  3. Ronald D Vale
  4. David A Agard  Is a corresponding author
  1. University of California, San Francisco, United States

Abstract

Centrioles are cylindrical assemblies comprised of 9 singlet, doublet, or triplet microtubules, essential for the formation of motile and sensory cilia. While the structure of the cilium is being defined at increasing resolution, centriolar structure remains poorly understood. Here, we used electron cryo-tomography to determine the structure of mammalian (triplet) and Drosophila (doublet) centrioles. Mammalian centrioles have two distinct domains: a 200 nm proximal core region connected by A-C linkers, and a distal domain where the C-tubule is incomplete and a pair of novel linkages stabilize the assembly producing a geometry more closely resembling the ciliary axoneme. Drosophila centrioles resemble the mammalian core, but with their doublet microtubules linked through the A tubules. The commonality of core-region length, and the abrupt transition in mammalian centrioles, suggests a conserved length-setting mechanism. The unexpected linker diversity suggests how unique centriolar architectures arise in different tissues and organisms.

Data availability

Average maps have been submitted to the Electron Microscopy Database (EMDB)

The following data sets were generated

Article and author information

Author details

  1. Garrett A Greenan

    Department of Biochemistry and Biophysics, University of California, San Francisco, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Bettina Keszthelyi

    Department of Biochemistry and Biophysics, University of California, San Francisco, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Ronald D Vale

    Department of Cellular and Molecular Pharmacology, University of California, San Francisco, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3460-2758
  4. David A Agard

    Department of Biochemistry and Biophysics, University of California, San Francisco, San Francisco, United States
    For correspondence
    agard@msg.ucsf.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3512-695X

Funding

Howard Hughes Medical Institute

  • Ronald D Vale
  • David A Agard

National Institute of General Medical Sciences (GM031627)

  • David A Agard

National Institute of General Medical Sciences (GM118099)

  • David A Agard

National Institute of General Medical Sciences (GM118106)

  • Ronald D Vale

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

Reviewing Editor

  1. Jordan W Raff, University of Oxford, United Kingdom

Publication history

  1. Received: March 21, 2018
  2. Accepted: August 3, 2018
  3. Accepted Manuscript published: August 6, 2018 (version 1)
  4. Version of Record published: August 27, 2018 (version 2)

Copyright

© 2018, Greenan 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. Garrett A Greenan
  2. Bettina Keszthelyi
  3. Ronald D Vale
  4. David A Agard
(2018)
Insights into centriole geometry revealed by cryoTomography of doublet and triplet centrioles
eLife 7:e36851.
https://doi.org/10.7554/eLife.36851

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