Massive centriole production can occur in the absence of deuterosomes in multiciliated cells

Olivier Mercey, Michelle S. Levine, Gina M. LoMastro, Philippe Rostaing, Eva Brotslaw, Valerie Gomez, Abhijay Kumar, Nathalie Spassky, Brian J. Mitchell, Alice Meunier, Andrew J. Holland

Research output: Contribution to journalArticle

Abstract

Multiciliated cells (MCCs) amplify large numbers of centrioles that convert into basal bodies, which are required for producing multiple motile cilia. Most centrioles amplified by MCCs grow on the surface of organelles called deuterosomes, whereas a smaller number grow through the centriolar pathway in association with the two parent centrioles. Here, we show that MCCs lacking deuterosomes amplify the correct number of centrioles with normal step-wise kinetics. This is achieved through a massive production of centrioles on the surface and in the vicinity of parent centrioles. Therefore, deuterosomes may have evolved to relieve, rather than supplement, the centriolar pathway during multiciliogenesis. Remarkably, MCCs lacking parent centrioles and deuterosomes also amplify the appropriate number of centrioles inside a cloud of pericentriolar and fibrogranular material. These data show that the centriole number is set independently of their nucleation platforms and suggest that massive centriole production in MCCs is a robust process that can self-organize.

Original languageEnglish (US)
Pages (from-to)1544-1552
Number of pages9
JournalNature cell biology
Volume21
Issue number12
DOIs
StatePublished - Dec 1 2019

Fingerprint

Centrioles
Basal Bodies
Cilia
Organelles

ASJC Scopus subject areas

  • Cell Biology

Cite this

Massive centriole production can occur in the absence of deuterosomes in multiciliated cells. / Mercey, Olivier; Levine, Michelle S.; LoMastro, Gina M.; Rostaing, Philippe; Brotslaw, Eva; Gomez, Valerie; Kumar, Abhijay; Spassky, Nathalie; Mitchell, Brian J.; Meunier, Alice; Holland, Andrew J.

In: Nature cell biology, Vol. 21, No. 12, 01.12.2019, p. 1544-1552.

Research output: Contribution to journalArticle

Mercey, O, Levine, MS, LoMastro, GM, Rostaing, P, Brotslaw, E, Gomez, V, Kumar, A, Spassky, N, Mitchell, BJ, Meunier, A & Holland, AJ 2019, 'Massive centriole production can occur in the absence of deuterosomes in multiciliated cells', Nature cell biology, vol. 21, no. 12, pp. 1544-1552. https://doi.org/10.1038/s41556-019-0427-x
Mercey O, Levine MS, LoMastro GM, Rostaing P, Brotslaw E, Gomez V et al. Massive centriole production can occur in the absence of deuterosomes in multiciliated cells. Nature cell biology. 2019 Dec 1;21(12):1544-1552. https://doi.org/10.1038/s41556-019-0427-x
Mercey, Olivier ; Levine, Michelle S. ; LoMastro, Gina M. ; Rostaing, Philippe ; Brotslaw, Eva ; Gomez, Valerie ; Kumar, Abhijay ; Spassky, Nathalie ; Mitchell, Brian J. ; Meunier, Alice ; Holland, Andrew J. / Massive centriole production can occur in the absence of deuterosomes in multiciliated cells. In: Nature cell biology. 2019 ; Vol. 21, No. 12. pp. 1544-1552.
@article{864596d1b39c4ae2b24088fd069abcfd,
title = "Massive centriole production can occur in the absence of deuterosomes in multiciliated cells",
abstract = "Multiciliated cells (MCCs) amplify large numbers of centrioles that convert into basal bodies, which are required for producing multiple motile cilia. Most centrioles amplified by MCCs grow on the surface of organelles called deuterosomes, whereas a smaller number grow through the centriolar pathway in association with the two parent centrioles. Here, we show that MCCs lacking deuterosomes amplify the correct number of centrioles with normal step-wise kinetics. This is achieved through a massive production of centrioles on the surface and in the vicinity of parent centrioles. Therefore, deuterosomes may have evolved to relieve, rather than supplement, the centriolar pathway during multiciliogenesis. Remarkably, MCCs lacking parent centrioles and deuterosomes also amplify the appropriate number of centrioles inside a cloud of pericentriolar and fibrogranular material. These data show that the centriole number is set independently of their nucleation platforms and suggest that massive centriole production in MCCs is a robust process that can self-organize.",
author = "Olivier Mercey and Levine, {Michelle S.} and LoMastro, {Gina M.} and Philippe Rostaing and Eva Brotslaw and Valerie Gomez and Abhijay Kumar and Nathalie Spassky and Mitchell, {Brian J.} and Alice Meunier and Holland, {Andrew J.}",
year = "2019",
month = "12",
day = "1",
doi = "10.1038/s41556-019-0427-x",
language = "English (US)",
volume = "21",
pages = "1544--1552",
journal = "Nature Cell Biology",
issn = "1465-7392",
publisher = "Nature Publishing Group",
number = "12",

}

TY - JOUR

T1 - Massive centriole production can occur in the absence of deuterosomes in multiciliated cells

AU - Mercey, Olivier

AU - Levine, Michelle S.

AU - LoMastro, Gina M.

AU - Rostaing, Philippe

AU - Brotslaw, Eva

AU - Gomez, Valerie

AU - Kumar, Abhijay

AU - Spassky, Nathalie

AU - Mitchell, Brian J.

AU - Meunier, Alice

AU - Holland, Andrew J.

PY - 2019/12/1

Y1 - 2019/12/1

N2 - Multiciliated cells (MCCs) amplify large numbers of centrioles that convert into basal bodies, which are required for producing multiple motile cilia. Most centrioles amplified by MCCs grow on the surface of organelles called deuterosomes, whereas a smaller number grow through the centriolar pathway in association with the two parent centrioles. Here, we show that MCCs lacking deuterosomes amplify the correct number of centrioles with normal step-wise kinetics. This is achieved through a massive production of centrioles on the surface and in the vicinity of parent centrioles. Therefore, deuterosomes may have evolved to relieve, rather than supplement, the centriolar pathway during multiciliogenesis. Remarkably, MCCs lacking parent centrioles and deuterosomes also amplify the appropriate number of centrioles inside a cloud of pericentriolar and fibrogranular material. These data show that the centriole number is set independently of their nucleation platforms and suggest that massive centriole production in MCCs is a robust process that can self-organize.

AB - Multiciliated cells (MCCs) amplify large numbers of centrioles that convert into basal bodies, which are required for producing multiple motile cilia. Most centrioles amplified by MCCs grow on the surface of organelles called deuterosomes, whereas a smaller number grow through the centriolar pathway in association with the two parent centrioles. Here, we show that MCCs lacking deuterosomes amplify the correct number of centrioles with normal step-wise kinetics. This is achieved through a massive production of centrioles on the surface and in the vicinity of parent centrioles. Therefore, deuterosomes may have evolved to relieve, rather than supplement, the centriolar pathway during multiciliogenesis. Remarkably, MCCs lacking parent centrioles and deuterosomes also amplify the appropriate number of centrioles inside a cloud of pericentriolar and fibrogranular material. These data show that the centriole number is set independently of their nucleation platforms and suggest that massive centriole production in MCCs is a robust process that can self-organize.

UR - http://www.scopus.com/inward/record.url?scp=85076196733&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85076196733&partnerID=8YFLogxK

U2 - 10.1038/s41556-019-0427-x

DO - 10.1038/s41556-019-0427-x

M3 - Article

C2 - 31792378

AN - SCOPUS:85076196733

VL - 21

SP - 1544

EP - 1552

JO - Nature Cell Biology

JF - Nature Cell Biology

SN - 1465-7392

IS - 12

ER -