Cargando…
Contact inhibition of locomotion and mechanical cross-talk between cell–cell and cell–substrate adhesion determine the pattern of junctional tension in epithelial cell aggregates
We used a computational approach to analyze the biomechanics of epithelial cell aggregates—islands, stripes, or entire monolayers—that combines both vertex and contact-inhibition-of-locomotion models to include cell–cell and cell–substrate adhesion. Examination of the distribution of cell protrusion...
Autores principales: | , , , , , , , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
The American Society for Cell Biology
2016
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5221537/ https://www.ncbi.nlm.nih.gov/pubmed/27605701 http://dx.doi.org/10.1091/mbc.E16-04-0226 |
_version_ | 1782492838703923200 |
---|---|
author | Coburn, Luke Lopez, Hender Caldwell, Benjamin J. Moussa, Elliott Yap, Chloe Priya, Rashmi Noppe, Adrian Roberts, Anthony P. Lobaskin, Vladimir Yap, Alpha S. Neufeld, Zoltan Gomez, Guillermo A. |
author_facet | Coburn, Luke Lopez, Hender Caldwell, Benjamin J. Moussa, Elliott Yap, Chloe Priya, Rashmi Noppe, Adrian Roberts, Anthony P. Lobaskin, Vladimir Yap, Alpha S. Neufeld, Zoltan Gomez, Guillermo A. |
author_sort | Coburn, Luke |
collection | PubMed |
description | We used a computational approach to analyze the biomechanics of epithelial cell aggregates—islands, stripes, or entire monolayers—that combines both vertex and contact-inhibition-of-locomotion models to include cell–cell and cell–substrate adhesion. Examination of the distribution of cell protrusions (adhesion to the substrate) in the model predicted high-order profiles of cell organization that agree with those previously seen experimentally. Cells acquired an asymmetric distribution of basal protrusions, traction forces, and apical aspect ratios that decreased when moving from the edge to the island center. Our in silico analysis also showed that tension on cell–cell junctions and apical stress is not homogeneous across the island. Instead, these parameters are higher at the island center and scale up with island size, which we confirmed experimentally using laser ablation assays and immunofluorescence. Without formally being a three-dimensional model, our approach has the minimal elements necessary to reproduce the distribution of cellular forces and mechanical cross-talk, as well as the distribution of principal stress in cells within epithelial cell aggregates. By making experimentally testable predictions, our approach can aid in mechanical analysis of epithelial tissues, especially when local changes in cell–cell and/or cell–substrate adhesion drive collective cell behavior. |
format | Online Article Text |
id | pubmed-5221537 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2016 |
publisher | The American Society for Cell Biology |
record_format | MEDLINE/PubMed |
spelling | pubmed-52215372017-01-22 Contact inhibition of locomotion and mechanical cross-talk between cell–cell and cell–substrate adhesion determine the pattern of junctional tension in epithelial cell aggregates Coburn, Luke Lopez, Hender Caldwell, Benjamin J. Moussa, Elliott Yap, Chloe Priya, Rashmi Noppe, Adrian Roberts, Anthony P. Lobaskin, Vladimir Yap, Alpha S. Neufeld, Zoltan Gomez, Guillermo A. Mol Biol Cell Articles We used a computational approach to analyze the biomechanics of epithelial cell aggregates—islands, stripes, or entire monolayers—that combines both vertex and contact-inhibition-of-locomotion models to include cell–cell and cell–substrate adhesion. Examination of the distribution of cell protrusions (adhesion to the substrate) in the model predicted high-order profiles of cell organization that agree with those previously seen experimentally. Cells acquired an asymmetric distribution of basal protrusions, traction forces, and apical aspect ratios that decreased when moving from the edge to the island center. Our in silico analysis also showed that tension on cell–cell junctions and apical stress is not homogeneous across the island. Instead, these parameters are higher at the island center and scale up with island size, which we confirmed experimentally using laser ablation assays and immunofluorescence. Without formally being a three-dimensional model, our approach has the minimal elements necessary to reproduce the distribution of cellular forces and mechanical cross-talk, as well as the distribution of principal stress in cells within epithelial cell aggregates. By making experimentally testable predictions, our approach can aid in mechanical analysis of epithelial tissues, especially when local changes in cell–cell and/or cell–substrate adhesion drive collective cell behavior. The American Society for Cell Biology 2016-11-07 /pmc/articles/PMC5221537/ /pubmed/27605701 http://dx.doi.org/10.1091/mbc.E16-04-0226 Text en © 2016 Coburn et al. This article is distributed by The American Society for Cell Biology under license from the author(s). Two months after publication it is available to the public under an Attribution–Noncommercial–Share Alike 3.0 Unported Creative Commons License (http://creativecommons.org/licenses/by-nc-sa/3.0). “ASCB®,” “The American Society for Cell Biology®,” and “Molecular Biology of the Cell®” are registered trademarks of The American Society for Cell Biology. |
spellingShingle | Articles Coburn, Luke Lopez, Hender Caldwell, Benjamin J. Moussa, Elliott Yap, Chloe Priya, Rashmi Noppe, Adrian Roberts, Anthony P. Lobaskin, Vladimir Yap, Alpha S. Neufeld, Zoltan Gomez, Guillermo A. Contact inhibition of locomotion and mechanical cross-talk between cell–cell and cell–substrate adhesion determine the pattern of junctional tension in epithelial cell aggregates |
title | Contact inhibition of locomotion and mechanical cross-talk between cell–cell and cell–substrate adhesion determine the pattern of junctional tension in epithelial cell aggregates |
title_full | Contact inhibition of locomotion and mechanical cross-talk between cell–cell and cell–substrate adhesion determine the pattern of junctional tension in epithelial cell aggregates |
title_fullStr | Contact inhibition of locomotion and mechanical cross-talk between cell–cell and cell–substrate adhesion determine the pattern of junctional tension in epithelial cell aggregates |
title_full_unstemmed | Contact inhibition of locomotion and mechanical cross-talk between cell–cell and cell–substrate adhesion determine the pattern of junctional tension in epithelial cell aggregates |
title_short | Contact inhibition of locomotion and mechanical cross-talk between cell–cell and cell–substrate adhesion determine the pattern of junctional tension in epithelial cell aggregates |
title_sort | contact inhibition of locomotion and mechanical cross-talk between cell–cell and cell–substrate adhesion determine the pattern of junctional tension in epithelial cell aggregates |
topic | Articles |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5221537/ https://www.ncbi.nlm.nih.gov/pubmed/27605701 http://dx.doi.org/10.1091/mbc.E16-04-0226 |
work_keys_str_mv | AT coburnluke contactinhibitionoflocomotionandmechanicalcrosstalkbetweencellcellandcellsubstrateadhesiondeterminethepatternofjunctionaltensioninepithelialcellaggregates AT lopezhender contactinhibitionoflocomotionandmechanicalcrosstalkbetweencellcellandcellsubstrateadhesiondeterminethepatternofjunctionaltensioninepithelialcellaggregates AT caldwellbenjaminj contactinhibitionoflocomotionandmechanicalcrosstalkbetweencellcellandcellsubstrateadhesiondeterminethepatternofjunctionaltensioninepithelialcellaggregates AT moussaelliott contactinhibitionoflocomotionandmechanicalcrosstalkbetweencellcellandcellsubstrateadhesiondeterminethepatternofjunctionaltensioninepithelialcellaggregates AT yapchloe contactinhibitionoflocomotionandmechanicalcrosstalkbetweencellcellandcellsubstrateadhesiondeterminethepatternofjunctionaltensioninepithelialcellaggregates AT priyarashmi contactinhibitionoflocomotionandmechanicalcrosstalkbetweencellcellandcellsubstrateadhesiondeterminethepatternofjunctionaltensioninepithelialcellaggregates AT noppeadrian contactinhibitionoflocomotionandmechanicalcrosstalkbetweencellcellandcellsubstrateadhesiondeterminethepatternofjunctionaltensioninepithelialcellaggregates AT robertsanthonyp contactinhibitionoflocomotionandmechanicalcrosstalkbetweencellcellandcellsubstrateadhesiondeterminethepatternofjunctionaltensioninepithelialcellaggregates AT lobaskinvladimir contactinhibitionoflocomotionandmechanicalcrosstalkbetweencellcellandcellsubstrateadhesiondeterminethepatternofjunctionaltensioninepithelialcellaggregates AT yapalphas contactinhibitionoflocomotionandmechanicalcrosstalkbetweencellcellandcellsubstrateadhesiondeterminethepatternofjunctionaltensioninepithelialcellaggregates AT neufeldzoltan contactinhibitionoflocomotionandmechanicalcrosstalkbetweencellcellandcellsubstrateadhesiondeterminethepatternofjunctionaltensioninepithelialcellaggregates AT gomezguillermoa contactinhibitionoflocomotionandmechanicalcrosstalkbetweencellcellandcellsubstrateadhesiondeterminethepatternofjunctionaltensioninepithelialcellaggregates |