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Regulation of cilia abundance in multiciliated cells

Multiciliated cells (MCC) contain hundreds of motile cilia used to propel fluid over their surface. To template these cilia, each MCC produces between 100-600 centrioles by a process termed centriole amplification. Yet, how MCC regulate the precise number of centrioles and cilia remains unknown. Air...

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Autores principales: Nanjundappa, Rashmi, Kong, Dong, Shim, Kyuhwan, Stearns, Tim, Brody, Steven L, Loncarek, Jadranka, Mahjoub, Moe R
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6504233/
https://www.ncbi.nlm.nih.gov/pubmed/31025935
http://dx.doi.org/10.7554/eLife.44039
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author Nanjundappa, Rashmi
Kong, Dong
Shim, Kyuhwan
Stearns, Tim
Brody, Steven L
Loncarek, Jadranka
Mahjoub, Moe R
author_facet Nanjundappa, Rashmi
Kong, Dong
Shim, Kyuhwan
Stearns, Tim
Brody, Steven L
Loncarek, Jadranka
Mahjoub, Moe R
author_sort Nanjundappa, Rashmi
collection PubMed
description Multiciliated cells (MCC) contain hundreds of motile cilia used to propel fluid over their surface. To template these cilia, each MCC produces between 100-600 centrioles by a process termed centriole amplification. Yet, how MCC regulate the precise number of centrioles and cilia remains unknown. Airway progenitor cells contain two parental centrioles (PC) and form structures called deuterosomes that nucleate centrioles during amplification. Using an ex vivo airway culture model, we show that ablation of PC does not perturb deuterosome formation and centriole amplification. In contrast, loss of PC caused an increase in deuterosome and centriole abundance, highlighting the presence of a compensatory mechanism. Quantification of centriole abundance in vitro and in vivo identified a linear relationship between surface area and centriole number. By manipulating cell size, we discovered that centriole number scales with surface area. Our results demonstrate that a cell-intrinsic surface area-dependent mechanism controls centriole and cilia abundance in multiciliated cells.
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spelling pubmed-65042332019-05-09 Regulation of cilia abundance in multiciliated cells Nanjundappa, Rashmi Kong, Dong Shim, Kyuhwan Stearns, Tim Brody, Steven L Loncarek, Jadranka Mahjoub, Moe R eLife Cell Biology Multiciliated cells (MCC) contain hundreds of motile cilia used to propel fluid over their surface. To template these cilia, each MCC produces between 100-600 centrioles by a process termed centriole amplification. Yet, how MCC regulate the precise number of centrioles and cilia remains unknown. Airway progenitor cells contain two parental centrioles (PC) and form structures called deuterosomes that nucleate centrioles during amplification. Using an ex vivo airway culture model, we show that ablation of PC does not perturb deuterosome formation and centriole amplification. In contrast, loss of PC caused an increase in deuterosome and centriole abundance, highlighting the presence of a compensatory mechanism. Quantification of centriole abundance in vitro and in vivo identified a linear relationship between surface area and centriole number. By manipulating cell size, we discovered that centriole number scales with surface area. Our results demonstrate that a cell-intrinsic surface area-dependent mechanism controls centriole and cilia abundance in multiciliated cells. eLife Sciences Publications, Ltd 2019-04-26 /pmc/articles/PMC6504233/ /pubmed/31025935 http://dx.doi.org/10.7554/eLife.44039 Text en © 2019, Nanjundappa et al http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Cell Biology
Nanjundappa, Rashmi
Kong, Dong
Shim, Kyuhwan
Stearns, Tim
Brody, Steven L
Loncarek, Jadranka
Mahjoub, Moe R
Regulation of cilia abundance in multiciliated cells
title Regulation of cilia abundance in multiciliated cells
title_full Regulation of cilia abundance in multiciliated cells
title_fullStr Regulation of cilia abundance in multiciliated cells
title_full_unstemmed Regulation of cilia abundance in multiciliated cells
title_short Regulation of cilia abundance in multiciliated cells
title_sort regulation of cilia abundance in multiciliated cells
topic Cell Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6504233/
https://www.ncbi.nlm.nih.gov/pubmed/31025935
http://dx.doi.org/10.7554/eLife.44039
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