» Articles » PMID: 32931487

Centrioles Are Amplified in Cycling Progenitors of Olfactory Sensory Neurons

Overview
Journal PLoS Biol
Specialty Biology
Date 2020 Sep 15
PMID 32931487
Citations 12
Authors
Affiliations
Soon will be listed here.
Abstract

Olfaction in most animals is mediated by neurons bearing cilia that are accessible to the environment. Olfactory sensory neurons (OSNs) in chordates usually have multiple cilia, each with a centriole at its base. OSNs differentiate from stem cells in the olfactory epithelium, and how the epithelium generates cells with many centrioles is not yet understood. We show that centrioles are amplified via centriole rosette formation in both embryonic development and turnover of the olfactory epithelium in adult mice, and rosette-bearing cells often have free centrioles in addition. Cells with amplified centrioles can go on to divide, with centrioles clustered at each pole. Additionally, we found that centrioles are amplified in immediate neuronal precursors (INPs) concomitant with elevation of mRNA for polo-like kinase 4 (Plk4) and SCL/Tal1-interrupting locus gene (Stil), key regulators of centriole duplication. These results support a model in which centriole amplification occurs during a transient state characterized by elevated Plk4 and Stil in early INP cells. These cells then go on to divide at least once to become OSNs, demonstrating that cell division with amplified centrioles, known to be tolerated in disease states, can occur as part of a normal developmental program.

Citing Articles

Centrioles are frequently amplified in early B cell development but dispensable for humoral immunity.

Schapfl M, LoMastro G, Braun V, Hirai M, Levine M, Kiermaier E Nat Commun. 2024; 15(1):8890.

PMID: 39406735 PMC: 11480410. DOI: 10.1038/s41467-024-53222-4.


Amplified centrosomes-more than just a threat.

Kiermaier E, Stotzel I, Schapfl M, Villunger A EMBO Rep. 2024; 25(10):4153-4167.

PMID: 39285247 PMC: 11467336. DOI: 10.1038/s44319-024-00260-0.


Prolonged overexpression of PLK4 leads to formation of centriole rosette clusters that are connected via canonical centrosome linker proteins.

Ozcan S, Kalkan B, Cicek E, Canbaz A, Acilan C Sci Rep. 2024; 14(1):4370.

PMID: 38388511 PMC: 10883960. DOI: 10.1038/s41598-024-53985-2.


The forkhead transcription factor Foxj1 controls vertebrate olfactory cilia biogenesis and sensory neuron differentiation.

Rayamajhi D, Ege M, Ukhanov K, Ringers C, Zhang Y, Jung I PLoS Biol. 2024; 22(1):e3002468.

PMID: 38271330 PMC: 10810531. DOI: 10.1371/journal.pbio.3002468.


GPRC5C regulates the composition of cilia in the olfactory system.

Bhat S, Dietz A, Senf K, Nietzsche S, Hirabayashi Y, Westermann M BMC Biol. 2023; 21(1):292.

PMID: 38110903 PMC: 10729543. DOI: 10.1186/s12915-023-01790-0.


References
1.
Cuschieri A, Bannister L . The development of the olfactory mucosa in the mouse: electron microscopy. J Anat. 1975; 119(Pt 3):471-98. PMC: 1231637. View

2.
Thelander L, Berg P . Isolation and characterization of expressible cDNA clones encoding the M1 and M2 subunits of mouse ribonucleotide reductase. Mol Cell Biol. 1986; 6(10):3433-42. PMC: 367091. DOI: 10.1128/mcb.6.10.3433-3442.1986. View

3.
Meunier A, Azimzadeh J . Multiciliated Cells in Animals. Cold Spring Harb Perspect Biol. 2016; 8(12. PMC: 5131768. DOI: 10.1101/cshperspect.a028233. View

4.
Li D, Yang Q, Chen J, Zhou H, Liu R, Huang X . Dynamic distribution of Ser-10 phosphorylated histone H3 in cytoplasm of MCF-7 and CHO cells during mitosis. Cell Res. 2005; 15(2):120-6. DOI: 10.1038/sj.cr.7290276. View

5.
Packard A, Giel-Moloney M, Leiter A, Schwob J . Progenitor cell capacity of NeuroD1-expressing globose basal cells in the mouse olfactory epithelium. J Comp Neurol. 2011; 519(17):3580-96. PMC: 4005605. DOI: 10.1002/cne.22726. View