Cargando…

The role of cell geometry and cell-cell communication in gradient sensing

Cells can measure shallow gradients of external signals to initiate and accomplish a migration or a morphogenetic process. Recently, starting from mathematical models like the local-excitation global-inhibition (LEGI) model and with the support of empirical evidence, it has been proposed that cellul...

Descripción completa

Detalles Bibliográficos
Autores principales: Fiorentino, Jonathan, Scialdone, Antonio
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8963572/
https://www.ncbi.nlm.nih.gov/pubmed/35286298
http://dx.doi.org/10.1371/journal.pcbi.1009552
_version_ 1784678017566507008
author Fiorentino, Jonathan
Scialdone, Antonio
author_facet Fiorentino, Jonathan
Scialdone, Antonio
author_sort Fiorentino, Jonathan
collection PubMed
description Cells can measure shallow gradients of external signals to initiate and accomplish a migration or a morphogenetic process. Recently, starting from mathematical models like the local-excitation global-inhibition (LEGI) model and with the support of empirical evidence, it has been proposed that cellular communication improves the measurement of an external gradient. However, the mathematical models that have been used have over-simplified geometries (e.g., they are uni-dimensional) or assumptions about cellular communication, which limit the possibility to analyze the gradient sensing ability of more complex cellular systems. Here, we generalize the existing models to study the effects on gradient sensing of cell number, geometry and of long- versus short-range cellular communication in 2D systems representing epithelial tissues. We find that increasing the cell number can be detrimental for gradient sensing when the communication is weak and limited to nearest neighbour cells, while it is beneficial when there is long-range communication. We also find that, with long-range communication, the gradient sensing ability improves for tissues with more disordered geometries; on the other hand, an ordered structure with mostly hexagonal cells is advantageous with nearest neighbour communication. Our results considerably extend the current models of gradient sensing by epithelial tissues, making a step further toward predicting the mechanism of communication and its putative mediator in many biological processes.
format Online
Article
Text
id pubmed-8963572
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-89635722022-03-30 The role of cell geometry and cell-cell communication in gradient sensing Fiorentino, Jonathan Scialdone, Antonio PLoS Comput Biol Research Article Cells can measure shallow gradients of external signals to initiate and accomplish a migration or a morphogenetic process. Recently, starting from mathematical models like the local-excitation global-inhibition (LEGI) model and with the support of empirical evidence, it has been proposed that cellular communication improves the measurement of an external gradient. However, the mathematical models that have been used have over-simplified geometries (e.g., they are uni-dimensional) or assumptions about cellular communication, which limit the possibility to analyze the gradient sensing ability of more complex cellular systems. Here, we generalize the existing models to study the effects on gradient sensing of cell number, geometry and of long- versus short-range cellular communication in 2D systems representing epithelial tissues. We find that increasing the cell number can be detrimental for gradient sensing when the communication is weak and limited to nearest neighbour cells, while it is beneficial when there is long-range communication. We also find that, with long-range communication, the gradient sensing ability improves for tissues with more disordered geometries; on the other hand, an ordered structure with mostly hexagonal cells is advantageous with nearest neighbour communication. Our results considerably extend the current models of gradient sensing by epithelial tissues, making a step further toward predicting the mechanism of communication and its putative mediator in many biological processes. Public Library of Science 2022-03-14 /pmc/articles/PMC8963572/ /pubmed/35286298 http://dx.doi.org/10.1371/journal.pcbi.1009552 Text en © 2022 Fiorentino, Scialdone 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
Fiorentino, Jonathan
Scialdone, Antonio
The role of cell geometry and cell-cell communication in gradient sensing
title The role of cell geometry and cell-cell communication in gradient sensing
title_full The role of cell geometry and cell-cell communication in gradient sensing
title_fullStr The role of cell geometry and cell-cell communication in gradient sensing
title_full_unstemmed The role of cell geometry and cell-cell communication in gradient sensing
title_short The role of cell geometry and cell-cell communication in gradient sensing
title_sort role of cell geometry and cell-cell communication in gradient sensing
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8963572/
https://www.ncbi.nlm.nih.gov/pubmed/35286298
http://dx.doi.org/10.1371/journal.pcbi.1009552
work_keys_str_mv AT fiorentinojonathan theroleofcellgeometryandcellcellcommunicationingradientsensing
AT scialdoneantonio theroleofcellgeometryandcellcellcommunicationingradientsensing
AT fiorentinojonathan roleofcellgeometryandcellcellcommunicationingradientsensing
AT scialdoneantonio roleofcellgeometryandcellcellcommunicationingradientsensing