Long-range migration of centrioles to the apical surface of the olfactory epithelium

  1. Kaitlin Ching
  2. Jennifer T Wang
  3. Tim Stearns  Is a corresponding author
  1. Stanford University, United States

Abstract

Olfactory sensory neurons (OSNs) in vertebrates detect odorants using multiple cilia, which protrude from the end of the dendrite and require centrioles for their formation. In mouse olfactory epithelium, the centrioles originate in progenitor cells near the basal lamina, often 50 to 100 μm from the apical surface. It is unknown how centrioles traverse this distance or mature to form cilia. Using high-resolution expansion microscopy, we found that centrioles migrate together, with multiple centrioles per group and multiple groups per OSN, during dendrite outgrowth. Centrioles were found by live imaging to migrate slowly, with a maximum rate of 0.18 µm/min. Centrioles in migrating groups were associated with microtubule nucleation factors, but acquired rootletin and appendages only in mature OSNs. The parental centriole had preexisting appendages, formed a single cilium before other centrioles, and retained its unique appendage configuration in the mature OSN. We developed an air-liquid interface explant culture system for OSNs and used it to show that centriole migration can be perturbed ex vivo by stabilizing microtubules. We consider these results in the context of a comprehensive model for centriole formation, migration, and maturation in this important sensory cell type.

Data availability

Figure 2 - Source Data 1, Figure 5 - Source Data 1, Figure 5 - Figure supplement 1 - Source Data 1, and Figure 5 - Figure supplement 1 - Source Data 2 contain the numerical data used to generate the figures

Article and author information

Author details

  1. Kaitlin Ching

    Department of Biology, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0517-2421
  2. Jennifer T Wang

    Department of Biology, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8506-5182
  3. Tim Stearns

    Department of Biology, Stanford University, Stanford, United States
    For correspondence
    stearns@stanford.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0671-6582

Funding

National Institutes of Health (R35GM130286)

  • Tim Stearns

National Institutes of Health (R01NS082208)

  • Tim Stearns

National Institutes of Health (K99GM131024)

  • Jennifer T Wang

National Institutes of Health (T32GM007276)

  • Kaitlin Ching

National Science Foundation (D-G16E5 6518)

  • Kaitlin Ching

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

Ethics

Animal experimentation: All animal procedures in this study were approved by the Stanford University Administrative Panel for Laboratory Animal Care (SUAPLAC protocol 11659) and carried out according to SUAPLAC guidelines.

Reviewing Editor

  1. Danelle Devenport, Princeton University, United States

Publication history

  1. Received: October 2, 2021
  2. Preprint posted: October 13, 2021 (view preprint)
  3. Accepted: April 13, 2022
  4. Accepted Manuscript published: April 14, 2022 (version 1)
  5. Version of Record published: May 3, 2022 (version 2)

Copyright

© 2022, Ching 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. Kaitlin Ching
  2. Jennifer T Wang
  3. Tim Stearns
(2022)
Long-range migration of centrioles to the apical surface of the olfactory epithelium
eLife 11:e74399.
https://doi.org/10.7554/eLife.74399
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