Cargando…

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

Multiciliated cells (MCCs) amplify large numbers of centrioles, which convert into basal bodies that are required for producing multiple motile cilia. Most centrioles amplified by MCCs grow on the surface of organelles called deuterosomes, while a smaller number grow through the centriolar pathway i...

Descripción completa

Detalles Bibliográficos
Autores principales: 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.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6913274/
https://www.ncbi.nlm.nih.gov/pubmed/31792378
http://dx.doi.org/10.1038/s41556-019-0427-x
_version_ 1783479632524214272
author 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.
author_facet 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.
author_sort Mercey, Olivier
collection PubMed
description Multiciliated cells (MCCs) amplify large numbers of centrioles, which convert into basal bodies that are required for producing multiple motile cilia. Most centrioles amplified by MCCs grow on the surface of organelles called deuterosomes, while 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 centriole number is set independently of their nucleation platforms and that massive centriole production in MCCs is a robust process that can self-organize.
format Online
Article
Text
id pubmed-6913274
institution National Center for Biotechnology Information
language English
publishDate 2019
record_format MEDLINE/PubMed
spelling pubmed-69132742020-06-02 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. Nat Cell Biol Article Multiciliated cells (MCCs) amplify large numbers of centrioles, which convert into basal bodies that are required for producing multiple motile cilia. Most centrioles amplified by MCCs grow on the surface of organelles called deuterosomes, while 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 centriole number is set independently of their nucleation platforms and that massive centriole production in MCCs is a robust process that can self-organize. 2019-12-02 2019-12 /pmc/articles/PMC6913274/ /pubmed/31792378 http://dx.doi.org/10.1038/s41556-019-0427-x Text en Users may view, print, copy, and download text and data-mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use:http://www.nature.com/authors/editorial_policies/license.html#terms
spellingShingle Article
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
title Massive centriole production can occur in the absence of deuterosomes in multiciliated cells
title_full Massive centriole production can occur in the absence of deuterosomes in multiciliated cells
title_fullStr Massive centriole production can occur in the absence of deuterosomes in multiciliated cells
title_full_unstemmed Massive centriole production can occur in the absence of deuterosomes in multiciliated cells
title_short Massive centriole production can occur in the absence of deuterosomes in multiciliated cells
title_sort massive centriole production can occur in the absence of deuterosomes in multiciliated cells
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6913274/
https://www.ncbi.nlm.nih.gov/pubmed/31792378
http://dx.doi.org/10.1038/s41556-019-0427-x
work_keys_str_mv AT merceyolivier massivecentrioleproductioncanoccurintheabsenceofdeuterosomesinmulticiliatedcells
AT levinemichelles massivecentrioleproductioncanoccurintheabsenceofdeuterosomesinmulticiliatedcells
AT lomastroginam massivecentrioleproductioncanoccurintheabsenceofdeuterosomesinmulticiliatedcells
AT rostaingphilippe massivecentrioleproductioncanoccurintheabsenceofdeuterosomesinmulticiliatedcells
AT brotslaweva massivecentrioleproductioncanoccurintheabsenceofdeuterosomesinmulticiliatedcells
AT gomezvalerie massivecentrioleproductioncanoccurintheabsenceofdeuterosomesinmulticiliatedcells
AT kumarabhijay massivecentrioleproductioncanoccurintheabsenceofdeuterosomesinmulticiliatedcells
AT spasskynathalie massivecentrioleproductioncanoccurintheabsenceofdeuterosomesinmulticiliatedcells
AT mitchellbrianj massivecentrioleproductioncanoccurintheabsenceofdeuterosomesinmulticiliatedcells
AT meunieralice massivecentrioleproductioncanoccurintheabsenceofdeuterosomesinmulticiliatedcells
AT hollandandrewj massivecentrioleproductioncanoccurintheabsenceofdeuterosomesinmulticiliatedcells