Cargando…

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),...

Descripción completa

Detalles Bibliográficos
Autores principales: Namba, Toshinori, Ishihara, Shuji
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2020
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
_version_ 1783503451098972160
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