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

cell biology centriole cilia expansion microscopy migration mouse neuroscience olfaction sensory neuron

Journal

eLife
ISSN: 2050-084X
Titre abrégé: Elife
Pays: England
ID NLM: 101579614

Informations de publication

Date de publication:
14 04 2022
Historique:
received: 02 10 2021
accepted: 13 04 2022
pubmed: 15 4 2022
medline: 6 5 2022
entrez: 14 4 2022
Statut: epublish

Résumé

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

Identifiants

pubmed: 35420544
doi: 10.7554/eLife.74399
pii: 74399
pmc: PMC9064291
doi:
pii:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : NIGMS NIH HHS
ID : K99 GM131024
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS082208
Pays : United States
Organisme : NIGMS NIH HHS
ID : R35 GM130286
Pays : United States

Informations de copyright

© 2022, Ching et al.

Déclaration de conflit d'intérêts

KC, JW, TS No competing interests declared

Références

J Anat. 1975 Jul;119(Pt 3):471-98
pubmed: 1141050
J Cell Biol. 1971 Jul;50(1):10-34
pubmed: 4998200
Curr Top Dev Biol. 2008;85:333-70
pubmed: 19147011
Nat Methods. 2012 Jun 28;9(7):676-82
pubmed: 22743772
Nat Genet. 2004 Sep;36(9):994-8
pubmed: 15322545
Cells. 2020 May 29;9(6):
pubmed: 32485978
J Cell Sci. 1968 Jun;3(2):207-30
pubmed: 5661997
Chem Senses. 1997 Jun;22(3):295-311
pubmed: 9218142
Nat Commun. 2015 Aug 21;6:8077
pubmed: 26293378
Curr Biol. 2014 Feb 17;24(4):351-60
pubmed: 24485834
Chem Senses. 2009 Jun;34(5):451-64
pubmed: 19406873
Anat Rec. 1977 Oct;189(2):187-99
pubmed: 911043
Proc Natl Acad Sci U S A. 2018 Mar 6;115(10):E2246-E2253
pubmed: 29463719
Cell Tissue Res. 1978 Oct 30;193(3):503-24
pubmed: 728957
J Cell Biol. 2010 Nov 15;191(4):721-9
pubmed: 21059850
Nat Commun. 2016 Jul 13;7:12187
pubmed: 27405868
J Cell Sci. 2022 Mar 1;135(5):
pubmed: 33771931
Nat Cell Biol. 2000 Jan;2(1):20-4
pubmed: 10620802
J Cell Biol. 1970 May;45(2):306-20
pubmed: 4327572
J Neurosci Res. 2010 Nov 15;88(15):3243-56
pubmed: 20882566
Nat Commun. 2014 Dec 15;5:5813
pubmed: 25504142
J Cell Biol. 2004 Aug 30;166(5):637-43
pubmed: 15337773
Physiol Rev. 1967 Jan;47(1):1-52
pubmed: 5343221
Nat Methods. 2019 Jan;16(1):71-74
pubmed: 30559430
J Anat. 2018 Apr;232(4):674-685
pubmed: 29313978
Front Cell Neurosci. 2020 Nov 19;14:594199
pubmed: 33328893
Curr Biol. 2012 Dec 4;22(23):2203-12
pubmed: 23122850
J Biol Chem. 2017 Dec 15;292(50):20592-20598
pubmed: 28974579
J Cell Biol. 2014 Sep 29;206(7):855-65
pubmed: 25246616
Cell Rep. 2014 Aug 21;8(4):957-65
pubmed: 25131205
Dev Cell. 2020 Oct 26;55(2):224-236.e6
pubmed: 33038333
Science. 2017 Nov 10;358(6364):803-806
pubmed: 28982797
J Cell Biol. 2011 May 16;193(4):727-39
pubmed: 21576395
J Ultrastruct Res. 1968 Jul;24(1):86-101
pubmed: 5693260
Acta Histochem Cytochem. 2015 Oct 29;48(5):145-52
pubmed: 26633906
Development. 2001 May;128(10):1889-97
pubmed: 11311168
J Neurosci. 2014 Apr 30;34(18):6377-88
pubmed: 24790208
J Cell Sci. 1988 Jan;89 ( Pt 1):67-80
pubmed: 2901423
Histochem Cell Biol. 2005 Jun;123(4-5):419-28
pubmed: 15868179
Sci Rep. 2018 Feb 27;8(1):3692
pubmed: 29487380
Proc Natl Acad Sci U S A. 2015 May 5;112(18):5821-6
pubmed: 25902488
J Microsc. 2019 Dec;276(3):145-159
pubmed: 31691972
J Cell Biol. 2010 Dec 13;191(6):1089-95
pubmed: 21135143
Nat Commun. 2021 Feb 24;12(1):1273
pubmed: 33627667
Curr Biol. 2015 Oct 5;25(19):2503-12
pubmed: 26365258
Physiol Genomics. 2008 Jan 17;32(2):198-206
pubmed: 17971504
J Cell Sci. 1989 Jan;92 ( Pt 1):9-20
pubmed: 2570783
J Cell Sci. 2007 Jan 1;120(Pt 1):7-15
pubmed: 17182899
J Vis Exp. 2014 Dec 27;(94):
pubmed: 25590569
Elife. 2020 Jul 13;9:
pubmed: 32657271
Science. 2010 Feb 5;327(5966):704-7
pubmed: 20056854
Genes Dev. 2013 Jan 15;27(2):163-8
pubmed: 23348840
Curr Opin Neurobiol. 2020 Aug;63:87-94
pubmed: 32361600
Mol Biol Cell. 2014 Oct 1;25(19):2919-33
pubmed: 25103236
EMBO J. 2017 Sep 1;36(17):2553-2566
pubmed: 28743734
Methods Cell Biol. 2020;160:281-293
pubmed: 32896322
Annu Rev Biochem. 2019 Jun 20;88:691-724
pubmed: 30601682
Mol Biol Cell. 2008 Jan;19(1):115-25
pubmed: 17959831
Am J Respir Cell Mol Biol. 2010 Dec;43(6):731-9
pubmed: 20118219
J Ultrastruct Res. 1971 May;35(3):274-81
pubmed: 4934086
J Cell Sci. 2019 Feb 15;132(5):
pubmed: 30665891
Dev Cell. 2007 Aug;13(2):203-13
pubmed: 17681132
Biol Cell. 1988;63(2):195-208
pubmed: 2904829
J Cell Biol. 2010 Jan 25;188(2):181-90
pubmed: 19951897
Neurosci Lett. 1997 Jun 20;229(1):17-20
pubmed: 9224791
J Comp Neurol. 1985 Dec 8;242(2):147-60
pubmed: 3878850
Proc Natl Acad Sci U S A. 2007 Oct 2;104(40):15917-22
pubmed: 17898177
Nat Cell Biol. 2011 Oct 03;13(10):1154-60
pubmed: 21968988
J Cell Biol. 2002 Nov 11;159(3):431-40
pubmed: 12427867
Nat Cell Biol. 2015 Feb;17(2):113-22
pubmed: 25599390
J Neurobiol. 2004 Jan;58(1):3-17
pubmed: 14598366
Chem Senses. 2020 Dec 5;45(9):805-822
pubmed: 33075817
Proc Natl Acad Sci U S A. 2014 Jul 15;111(28):E2841-50
pubmed: 24982133
PLoS Biol. 2020 Sep 15;18(9):e3000852
pubmed: 32931487
Nature. 1997 Sep 4;389(6646):81-5
pubmed: 9288971
Cytoskeleton (Hoboken). 2016 Sep;73(9):442-60
pubmed: 26887570

Auteurs

Kaitlin Ching (K)

Department of Biology, Stanford University, Stanford, United States.

Jennifer T Wang (JT)

Department of Biology, Stanford University, Stanford, United States.

Tim Stearns (T)

Department of Biology, Stanford University, Stanford, United States.
Department of Genetics, Stanford University School of Medicine, Stanford, United States.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH