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

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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.

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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

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Kaitlin Ching

Department of Biology, Stanford University, Stanford, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-0517-2421
Jennifer T Wang

Department of Biology, Stanford University, Stanford, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-8506-5182
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.

"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.

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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.