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Coordinating cell polarization and morphogenesis through mechanical feedback

Many cellular processes require cell polarization to be maintained as the cell changes shape, grows or moves. Without feedback mechanisms relaying information about cell shape to the polarity molecular machinery, the coordination between cell polarization and morphogenesis, movement or growth would...

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Detalles Bibliográficos
Autores principales: Banavar, Samhita P., Trogdon, Michael, Drawert, Brian, Yi, Tau-Mu, Petzold, Linda R., Campàs, Otger
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7872284/
https://www.ncbi.nlm.nih.gov/pubmed/33507956
http://dx.doi.org/10.1371/journal.pcbi.1007971
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author Banavar, Samhita P.
Trogdon, Michael
Drawert, Brian
Yi, Tau-Mu
Petzold, Linda R.
Campàs, Otger
author_facet Banavar, Samhita P.
Trogdon, Michael
Drawert, Brian
Yi, Tau-Mu
Petzold, Linda R.
Campàs, Otger
author_sort Banavar, Samhita P.
collection PubMed
description Many cellular processes require cell polarization to be maintained as the cell changes shape, grows or moves. Without feedback mechanisms relaying information about cell shape to the polarity molecular machinery, the coordination between cell polarization and morphogenesis, movement or growth would not be possible. Here we theoretically and computationally study the role of a genetically-encoded mechanical feedback (in the Cell Wall Integrity pathway) as a potential coordination mechanism between cell morphogenesis and polarity during budding yeast mating projection growth. We developed a coarse-grained continuum description of the coupled dynamics of cell polarization and morphogenesis as well as 3D stochastic simulations of the molecular polarization machinery in the evolving cell shape. Both theoretical approaches show that in the absence of mechanical feedback (or in the presence of weak feedback), cell polarity cannot be maintained at the projection tip during growth, with the polarization cap wandering off the projection tip, arresting morphogenesis. In contrast, for mechanical feedback strengths above a threshold, cells can robustly maintain cell polarization at the tip and simultaneously sustain mating projection growth. These results indicate that the mechanical feedback encoded in the Cell Wall Integrity pathway can provide important positional information to the molecular machinery in the cell, thereby enabling the coordination of cell polarization and morphogenesis.
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spelling pubmed-78722842021-02-19 Coordinating cell polarization and morphogenesis through mechanical feedback Banavar, Samhita P. Trogdon, Michael Drawert, Brian Yi, Tau-Mu Petzold, Linda R. Campàs, Otger PLoS Comput Biol Research Article Many cellular processes require cell polarization to be maintained as the cell changes shape, grows or moves. Without feedback mechanisms relaying information about cell shape to the polarity molecular machinery, the coordination between cell polarization and morphogenesis, movement or growth would not be possible. Here we theoretically and computationally study the role of a genetically-encoded mechanical feedback (in the Cell Wall Integrity pathway) as a potential coordination mechanism between cell morphogenesis and polarity during budding yeast mating projection growth. We developed a coarse-grained continuum description of the coupled dynamics of cell polarization and morphogenesis as well as 3D stochastic simulations of the molecular polarization machinery in the evolving cell shape. Both theoretical approaches show that in the absence of mechanical feedback (or in the presence of weak feedback), cell polarity cannot be maintained at the projection tip during growth, with the polarization cap wandering off the projection tip, arresting morphogenesis. In contrast, for mechanical feedback strengths above a threshold, cells can robustly maintain cell polarization at the tip and simultaneously sustain mating projection growth. These results indicate that the mechanical feedback encoded in the Cell Wall Integrity pathway can provide important positional information to the molecular machinery in the cell, thereby enabling the coordination of cell polarization and morphogenesis. Public Library of Science 2021-01-28 /pmc/articles/PMC7872284/ /pubmed/33507956 http://dx.doi.org/10.1371/journal.pcbi.1007971 Text en © 2021 Banavar et al 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
Banavar, Samhita P.
Trogdon, Michael
Drawert, Brian
Yi, Tau-Mu
Petzold, Linda R.
Campàs, Otger
Coordinating cell polarization and morphogenesis through mechanical feedback
title Coordinating cell polarization and morphogenesis through mechanical feedback
title_full Coordinating cell polarization and morphogenesis through mechanical feedback
title_fullStr Coordinating cell polarization and morphogenesis through mechanical feedback
title_full_unstemmed Coordinating cell polarization and morphogenesis through mechanical feedback
title_short Coordinating cell polarization and morphogenesis through mechanical feedback
title_sort coordinating cell polarization and morphogenesis through mechanical feedback
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7872284/
https://www.ncbi.nlm.nih.gov/pubmed/33507956
http://dx.doi.org/10.1371/journal.pcbi.1007971
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