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Cytoskeleton polarity is essential in determining orientational order in basal bodies of multi-ciliated cells
In multi-ciliated cells, directed and synchronous ciliary beating in the apical membrane occurs through appropriate configuration of basal bodies (BBs, roots of cilia). Although it has been experimentally shown that the position and orientation of BBs are coordinated by apical cytoskeletons (CSKs),...
Autores principales: | , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2020
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7055923/ https://www.ncbi.nlm.nih.gov/pubmed/32084125 http://dx.doi.org/10.1371/journal.pcbi.1007649 |
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author | Namba, Toshinori Ishihara, Shuji |
author_facet | Namba, Toshinori Ishihara, Shuji |
author_sort | Namba, Toshinori |
collection | PubMed |
description | In multi-ciliated cells, directed and synchronous ciliary beating in the apical membrane occurs through appropriate configuration of basal bodies (BBs, roots of cilia). Although it has been experimentally shown that the position and orientation of BBs are coordinated by apical cytoskeletons (CSKs), such as microtubules (MTs), and planar cell polarity (PCP), the underlying mechanism for achieving the patterning of BBs is not yet understood. In this study, we propose that polarity in bundles of apical MTs play a crucial role in the patterning of BBs. First, the necessity of the polarity was discussed by theoretical consideration on the symmetry of the system. The existence of the polarity was investigated by measuring relative angles between the MTs and BBs using published experimental data. Next, a mathematical model for BB patterning was derived by combining the polarity and self-organizational ability of CSKs. In the model, BBs were treated as finite-size particles in the medium of CSKs and excluded volume effects between BBs and CSKs were taken into account. The model reproduces the various experimental observations, including normal and drug-treated phenotypes. Our model with polarity provides a coherent and testable mechanism for apical BB pattern formation. We have also discussed the implication of our study on cell chirality. |
format | Online Article Text |
id | pubmed-7055923 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2020 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-70559232020-03-13 Cytoskeleton polarity is essential in determining orientational order in basal bodies of multi-ciliated cells Namba, Toshinori Ishihara, Shuji PLoS Comput Biol Research Article In multi-ciliated cells, directed and synchronous ciliary beating in the apical membrane occurs through appropriate configuration of basal bodies (BBs, roots of cilia). Although it has been experimentally shown that the position and orientation of BBs are coordinated by apical cytoskeletons (CSKs), such as microtubules (MTs), and planar cell polarity (PCP), the underlying mechanism for achieving the patterning of BBs is not yet understood. In this study, we propose that polarity in bundles of apical MTs play a crucial role in the patterning of BBs. First, the necessity of the polarity was discussed by theoretical consideration on the symmetry of the system. The existence of the polarity was investigated by measuring relative angles between the MTs and BBs using published experimental data. Next, a mathematical model for BB patterning was derived by combining the polarity and self-organizational ability of CSKs. In the model, BBs were treated as finite-size particles in the medium of CSKs and excluded volume effects between BBs and CSKs were taken into account. The model reproduces the various experimental observations, including normal and drug-treated phenotypes. Our model with polarity provides a coherent and testable mechanism for apical BB pattern formation. We have also discussed the implication of our study on cell chirality. Public Library of Science 2020-02-21 /pmc/articles/PMC7055923/ /pubmed/32084125 http://dx.doi.org/10.1371/journal.pcbi.1007649 Text en © 2020 Namba, Ishihara http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. |
spellingShingle | Research Article Namba, Toshinori Ishihara, Shuji Cytoskeleton polarity is essential in determining orientational order in basal bodies of multi-ciliated cells |
title | Cytoskeleton polarity is essential in determining orientational order in basal bodies of multi-ciliated cells |
title_full | Cytoskeleton polarity is essential in determining orientational order in basal bodies of multi-ciliated cells |
title_fullStr | Cytoskeleton polarity is essential in determining orientational order in basal bodies of multi-ciliated cells |
title_full_unstemmed | Cytoskeleton polarity is essential in determining orientational order in basal bodies of multi-ciliated cells |
title_short | Cytoskeleton polarity is essential in determining orientational order in basal bodies of multi-ciliated cells |
title_sort | cytoskeleton polarity is essential in determining orientational order in basal bodies of multi-ciliated cells |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7055923/ https://www.ncbi.nlm.nih.gov/pubmed/32084125 http://dx.doi.org/10.1371/journal.pcbi.1007649 |
work_keys_str_mv | AT nambatoshinori cytoskeletonpolarityisessentialindeterminingorientationalorderinbasalbodiesofmulticiliatedcells AT ishiharashuji cytoskeletonpolarityisessentialindeterminingorientationalorderinbasalbodiesofmulticiliatedcells |