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Avalanches during epithelial tissue growth; Uniform Growth and a drosophila eye disc model

Epithelial tissues constitute an exotic type of active matter with non-linear properties reminiscent of amorphous materials. In the context of a proliferating epithelium, modeled by the quasistatic vertex model, we identify novel discrete tissue scale rearrangements, i.e. cellular rearrangement aval...

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Autores principales: Courcoubetis, George, Xu, Chi, Nuzhdin, Sergey V., Haas, Stephan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8932575/
https://www.ncbi.nlm.nih.gov/pubmed/35303738
http://dx.doi.org/10.1371/journal.pcbi.1009952
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author Courcoubetis, George
Xu, Chi
Nuzhdin, Sergey V.
Haas, Stephan
author_facet Courcoubetis, George
Xu, Chi
Nuzhdin, Sergey V.
Haas, Stephan
author_sort Courcoubetis, George
collection PubMed
description Epithelial tissues constitute an exotic type of active matter with non-linear properties reminiscent of amorphous materials. In the context of a proliferating epithelium, modeled by the quasistatic vertex model, we identify novel discrete tissue scale rearrangements, i.e. cellular rearrangement avalanches, which are a form of collective cell movement. During the avalanches, the vast majority of cells retain their neighbors, and the resulting cellular trajectories are radial in the periphery, a vortex in the core. After the onset of these avalanches, the epithelial area grows discontinuously. The avalanches are found to be stochastic, and their strength is correlated with the density of cells in the tissue. Overall, avalanches redistribute accumulated local spatial pressure along the tissue. Furthermore, the distribution of avalanche magnitudes is found to obey a power law, with an exponent consistent with sheer induced avalanches in amorphous materials. To understand the role of avalanches in organ development, we simulate epithelial growth of the Drosophila eye disc during the third instar using a computational model, which includes both chemical and mechanistic signaling. During the third instar, the morphogenetic furrow (MF), a ~10 cell wide wave of apical area constriction propagates through the epithelium. These simulations are used to understand the details of the growth process, the effect of the MF on the growth dynamics on the tissue scale, and to make predictions for experimental observations. The avalanches are found to depend on the strength of the apical constriction of cells in the MF, with a stronger apical constriction leading to less frequent and more pronounced avalanches. The results herein highlight the dependence of simulated tissue growth dynamics on relaxation timescales, and serve as a guide for in vitro experiments.
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spelling pubmed-89325752022-03-19 Avalanches during epithelial tissue growth; Uniform Growth and a drosophila eye disc model Courcoubetis, George Xu, Chi Nuzhdin, Sergey V. Haas, Stephan PLoS Comput Biol Research Article Epithelial tissues constitute an exotic type of active matter with non-linear properties reminiscent of amorphous materials. In the context of a proliferating epithelium, modeled by the quasistatic vertex model, we identify novel discrete tissue scale rearrangements, i.e. cellular rearrangement avalanches, which are a form of collective cell movement. During the avalanches, the vast majority of cells retain their neighbors, and the resulting cellular trajectories are radial in the periphery, a vortex in the core. After the onset of these avalanches, the epithelial area grows discontinuously. The avalanches are found to be stochastic, and their strength is correlated with the density of cells in the tissue. Overall, avalanches redistribute accumulated local spatial pressure along the tissue. Furthermore, the distribution of avalanche magnitudes is found to obey a power law, with an exponent consistent with sheer induced avalanches in amorphous materials. To understand the role of avalanches in organ development, we simulate epithelial growth of the Drosophila eye disc during the third instar using a computational model, which includes both chemical and mechanistic signaling. During the third instar, the morphogenetic furrow (MF), a ~10 cell wide wave of apical area constriction propagates through the epithelium. These simulations are used to understand the details of the growth process, the effect of the MF on the growth dynamics on the tissue scale, and to make predictions for experimental observations. The avalanches are found to depend on the strength of the apical constriction of cells in the MF, with a stronger apical constriction leading to less frequent and more pronounced avalanches. The results herein highlight the dependence of simulated tissue growth dynamics on relaxation timescales, and serve as a guide for in vitro experiments. Public Library of Science 2022-03-18 /pmc/articles/PMC8932575/ /pubmed/35303738 http://dx.doi.org/10.1371/journal.pcbi.1009952 Text en © 2022 Courcoubetis et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://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
Courcoubetis, George
Xu, Chi
Nuzhdin, Sergey V.
Haas, Stephan
Avalanches during epithelial tissue growth; Uniform Growth and a drosophila eye disc model
title Avalanches during epithelial tissue growth; Uniform Growth and a drosophila eye disc model
title_full Avalanches during epithelial tissue growth; Uniform Growth and a drosophila eye disc model
title_fullStr Avalanches during epithelial tissue growth; Uniform Growth and a drosophila eye disc model
title_full_unstemmed Avalanches during epithelial tissue growth; Uniform Growth and a drosophila eye disc model
title_short Avalanches during epithelial tissue growth; Uniform Growth and a drosophila eye disc model
title_sort avalanches during epithelial tissue growth; uniform growth and a drosophila eye disc model
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8932575/
https://www.ncbi.nlm.nih.gov/pubmed/35303738
http://dx.doi.org/10.1371/journal.pcbi.1009952
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