Cargando…

PLK4 drives centriole amplification and apical surface area expansion in multiciliated cells

Multiciliated cells (MCCs) are terminally differentiated epithelia that assemble multiple motile cilia used to promote fluid flow. To template these cilia, MCCs dramatically expand their centriole content during a process known as centriole amplification. In cycling cells, the master regulator of ce...

Descripción completa

Detalles Bibliográficos
Autores principales: LoMastro, Gina M, Drown, Chelsea G, Maryniak, Aubrey L, Jewett, Cayla E, Strong, Margaret A, Holland, Andrew Jon
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9507127/
https://www.ncbi.nlm.nih.gov/pubmed/35969030
http://dx.doi.org/10.7554/eLife.80643
_version_ 1784796845007962112
author LoMastro, Gina M
Drown, Chelsea G
Maryniak, Aubrey L
Jewett, Cayla E
Strong, Margaret A
Holland, Andrew Jon
author_facet LoMastro, Gina M
Drown, Chelsea G
Maryniak, Aubrey L
Jewett, Cayla E
Strong, Margaret A
Holland, Andrew Jon
author_sort LoMastro, Gina M
collection PubMed
description Multiciliated cells (MCCs) are terminally differentiated epithelia that assemble multiple motile cilia used to promote fluid flow. To template these cilia, MCCs dramatically expand their centriole content during a process known as centriole amplification. In cycling cells, the master regulator of centriole assembly Polo-like kinase 4 (PLK4) is essential for centriole duplication; however recent work has questioned the role of PLK4 in centriole assembly in MCCs. To address this discrepancy, we created genetically engineered mouse models and demonstrated that both PLK4 protein and kinase activity are critical for centriole amplification in MCCs. Tracheal epithelial cells that fail centriole amplification accumulate large assemblies of centriole proteins and do not undergo apical surface area expansion. These results show that the initial stages of centriole assembly are conserved between cycling cells and MCCs and suggest that centriole amplification and surface area expansion are coordinated events.
format Online
Article
Text
id pubmed-9507127
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher eLife Sciences Publications, Ltd
record_format MEDLINE/PubMed
spelling pubmed-95071272022-09-24 PLK4 drives centriole amplification and apical surface area expansion in multiciliated cells LoMastro, Gina M Drown, Chelsea G Maryniak, Aubrey L Jewett, Cayla E Strong, Margaret A Holland, Andrew Jon eLife Cell Biology Multiciliated cells (MCCs) are terminally differentiated epithelia that assemble multiple motile cilia used to promote fluid flow. To template these cilia, MCCs dramatically expand their centriole content during a process known as centriole amplification. In cycling cells, the master regulator of centriole assembly Polo-like kinase 4 (PLK4) is essential for centriole duplication; however recent work has questioned the role of PLK4 in centriole assembly in MCCs. To address this discrepancy, we created genetically engineered mouse models and demonstrated that both PLK4 protein and kinase activity are critical for centriole amplification in MCCs. Tracheal epithelial cells that fail centriole amplification accumulate large assemblies of centriole proteins and do not undergo apical surface area expansion. These results show that the initial stages of centriole assembly are conserved between cycling cells and MCCs and suggest that centriole amplification and surface area expansion are coordinated events. eLife Sciences Publications, Ltd 2022-08-15 /pmc/articles/PMC9507127/ /pubmed/35969030 http://dx.doi.org/10.7554/eLife.80643 Text en © 2022, LoMastro et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Cell Biology
LoMastro, Gina M
Drown, Chelsea G
Maryniak, Aubrey L
Jewett, Cayla E
Strong, Margaret A
Holland, Andrew Jon
PLK4 drives centriole amplification and apical surface area expansion in multiciliated cells
title PLK4 drives centriole amplification and apical surface area expansion in multiciliated cells
title_full PLK4 drives centriole amplification and apical surface area expansion in multiciliated cells
title_fullStr PLK4 drives centriole amplification and apical surface area expansion in multiciliated cells
title_full_unstemmed PLK4 drives centriole amplification and apical surface area expansion in multiciliated cells
title_short PLK4 drives centriole amplification and apical surface area expansion in multiciliated cells
title_sort plk4 drives centriole amplification and apical surface area expansion in multiciliated cells
topic Cell Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9507127/
https://www.ncbi.nlm.nih.gov/pubmed/35969030
http://dx.doi.org/10.7554/eLife.80643
work_keys_str_mv AT lomastroginam plk4drivescentrioleamplificationandapicalsurfaceareaexpansioninmulticiliatedcells
AT drownchelseag plk4drivescentrioleamplificationandapicalsurfaceareaexpansioninmulticiliatedcells
AT maryniakaubreyl plk4drivescentrioleamplificationandapicalsurfaceareaexpansioninmulticiliatedcells
AT jewettcaylae plk4drivescentrioleamplificationandapicalsurfaceareaexpansioninmulticiliatedcells
AT strongmargareta plk4drivescentrioleamplificationandapicalsurfaceareaexpansioninmulticiliatedcells
AT hollandandrewjon plk4drivescentrioleamplificationandapicalsurfaceareaexpansioninmulticiliatedcells