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

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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

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ASJC Scopus subject areas

  • Cell Biology

Cite this

Mercey, O., Levine, M. S., LoMastro, G. M., Rostaing, P., Brotslaw, E., Gomez, V., Kumar, A., Spassky, N., Mitchell, B. J., Meunier, A., & Holland, A. J. (2019). Massive centriole production can occur in the absence of deuterosomes in multiciliated cells. Nature cell biology, 21(12), 1544-1552. https://doi.org/10.1038/s41556-019-0427-x