Long-range migration of centrioles to the apical surface of the olfactory epithelium
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 50–100 μm from the ap...
| Main Authors: | , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2022-04-01
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| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/74399 |
| _version_ | 1818018403800055808 |
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| author | Kaitlin Ching Jennifer T Wang Tim Stearns |
| author_facet | Kaitlin Ching Jennifer T Wang Tim Stearns |
| author_sort | Kaitlin Ching |
| collection | DOAJ |
| description | 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 50–100 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/minute. 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. |
| first_indexed | 2024-04-14T07:38:44Z |
| format | Article |
| id | doaj.art-b83da0c517994c289eb611d3091e9c5c |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-14T07:38:44Z |
| publishDate | 2022-04-01 |
| publisher | eLife Sciences Publications Ltd |
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| spelling | doaj.art-b83da0c517994c289eb611d3091e9c5c2022-12-22T02:05:35ZengeLife Sciences Publications LtdeLife2050-084X2022-04-011110.7554/eLife.74399Long-range migration of centrioles to the apical surface of the olfactory epitheliumKaitlin Ching0https://orcid.org/0000-0002-0517-2421Jennifer T Wang1https://orcid.org/0000-0002-8506-5182Tim Stearns2https://orcid.org/0000-0002-0671-6582Department of Biology, Stanford University, Stanford, United StatesDepartment of Biology, Stanford University, Stanford, United StatesDepartment of Biology, Stanford University, Stanford, United States; Department of Genetics, Stanford University School of Medicine, Stanford, United StatesOlfactory 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 50–100 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/minute. 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.https://elifesciences.org/articles/74399olfactionsensory neuroncentrioleciliaexpansion microscopymigration |
| spellingShingle | Kaitlin Ching Jennifer T Wang Tim Stearns Long-range migration of centrioles to the apical surface of the olfactory epithelium eLife olfaction sensory neuron centriole cilia expansion microscopy migration |
| title | Long-range migration of centrioles to the apical surface of the olfactory epithelium |
| title_full | Long-range migration of centrioles to the apical surface of the olfactory epithelium |
| title_fullStr | Long-range migration of centrioles to the apical surface of the olfactory epithelium |
| title_full_unstemmed | Long-range migration of centrioles to the apical surface of the olfactory epithelium |
| title_short | Long-range migration of centrioles to the apical surface of the olfactory epithelium |
| title_sort | long range migration of centrioles to the apical surface of the olfactory epithelium |
| topic | olfaction sensory neuron centriole cilia expansion microscopy migration |
| url | https://elifesciences.org/articles/74399 |
| work_keys_str_mv | AT kaitlinching longrangemigrationofcentriolestotheapicalsurfaceoftheolfactoryepithelium AT jennifertwang longrangemigrationofcentriolestotheapicalsurfaceoftheolfactoryepithelium AT timstearns longrangemigrationofcentriolestotheapicalsurfaceoftheolfactoryepithelium |