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On the origin of universal cell shape variability in confluent epithelial monolayers

Cell shape is fundamental in biology. The average cell shape can influence crucial biological functions, such as cell fate and division orientation. But cell-to-cell shape variability is often regarded as noise. In contrast, recent works reveal that shape variability in diverse epithelial monolayers...

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Detalles Bibliográficos
Autores principales: Sadhukhan, Souvik, Nandi, Saroj Kumar
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9833828/
https://www.ncbi.nlm.nih.gov/pubmed/36563034
http://dx.doi.org/10.7554/eLife.76406
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author Sadhukhan, Souvik
Nandi, Saroj Kumar
author_facet Sadhukhan, Souvik
Nandi, Saroj Kumar
author_sort Sadhukhan, Souvik
collection PubMed
description Cell shape is fundamental in biology. The average cell shape can influence crucial biological functions, such as cell fate and division orientation. But cell-to-cell shape variability is often regarded as noise. In contrast, recent works reveal that shape variability in diverse epithelial monolayers follows a nearly universal distribution. However, the origin and implications of this universality remain unclear. Here, assuming contractility and adhesion are crucial for cell shape, characterized via aspect ratio (r), we develop a mean-field analytical theory for shape variability. We find that all the system-specific details combine into a single parameter α that governs the probability distribution function (PDF) of r; this leads to a universal relation between the standard deviation and the average of r. The PDF for the scaled r is not strictly but nearly universal. In addition, we obtain the scaled area distribution, described by the parameter μ. Information of α and μ together can distinguish the effects of changing physical conditions, such as maturation, on different system properties. We have verified the theory via simulations of two distinct models of epithelial monolayers and with existing experiments on diverse systems. We demonstrate that in a confluent monolayer, average shape determines both the shape variability and dynamics. Our results imply that cell shape distribution is inevitable, where a single parameter describes both statics and dynamics and provides a framework to analyze and compare diverse epithelial systems. In contrast to existing theories, our work shows that the universal properties are consequences of a mathematical property and should be valid in general, even in the fluid regime.
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spelling pubmed-98338282023-01-12 On the origin of universal cell shape variability in confluent epithelial monolayers Sadhukhan, Souvik Nandi, Saroj Kumar eLife Developmental Biology Cell shape is fundamental in biology. The average cell shape can influence crucial biological functions, such as cell fate and division orientation. But cell-to-cell shape variability is often regarded as noise. In contrast, recent works reveal that shape variability in diverse epithelial monolayers follows a nearly universal distribution. However, the origin and implications of this universality remain unclear. Here, assuming contractility and adhesion are crucial for cell shape, characterized via aspect ratio (r), we develop a mean-field analytical theory for shape variability. We find that all the system-specific details combine into a single parameter α that governs the probability distribution function (PDF) of r; this leads to a universal relation between the standard deviation and the average of r. The PDF for the scaled r is not strictly but nearly universal. In addition, we obtain the scaled area distribution, described by the parameter μ. Information of α and μ together can distinguish the effects of changing physical conditions, such as maturation, on different system properties. We have verified the theory via simulations of two distinct models of epithelial monolayers and with existing experiments on diverse systems. We demonstrate that in a confluent monolayer, average shape determines both the shape variability and dynamics. Our results imply that cell shape distribution is inevitable, where a single parameter describes both statics and dynamics and provides a framework to analyze and compare diverse epithelial systems. In contrast to existing theories, our work shows that the universal properties are consequences of a mathematical property and should be valid in general, even in the fluid regime. eLife Sciences Publications, Ltd 2022-12-23 /pmc/articles/PMC9833828/ /pubmed/36563034 http://dx.doi.org/10.7554/eLife.76406 Text en © 2022, Sadhukhan and Nandi https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Developmental Biology
Sadhukhan, Souvik
Nandi, Saroj Kumar
On the origin of universal cell shape variability in confluent epithelial monolayers
title On the origin of universal cell shape variability in confluent epithelial monolayers
title_full On the origin of universal cell shape variability in confluent epithelial monolayers
title_fullStr On the origin of universal cell shape variability in confluent epithelial monolayers
title_full_unstemmed On the origin of universal cell shape variability in confluent epithelial monolayers
title_short On the origin of universal cell shape variability in confluent epithelial monolayers
title_sort on the origin of universal cell shape variability in confluent epithelial monolayers
topic Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9833828/
https://www.ncbi.nlm.nih.gov/pubmed/36563034
http://dx.doi.org/10.7554/eLife.76406
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