The mechanical influence of densification on epithelial architecture.

Epithelial tissues are the most abundant tissue type in animals, lining body cavities and generating compartment barriers. The function of a monolayered epithelial tissue-whether protective, secretory, absorptive, or filtrative-relies on the side-by-side arrangement of its component cells. The mecha...

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Main Authors: Christian Cammarota, Nicole S Dawney, Philip M Bellomio, Maren Jüng, Alexander G Fletcher, Tara M Finegan, Dan T Bergstralh
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2024-04-01
Series:PLoS Computational Biology
Online Access:https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1012001&type=printable
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author Christian Cammarota
Nicole S Dawney
Philip M Bellomio
Maren Jüng
Alexander G Fletcher
Tara M Finegan
Dan T Bergstralh
author_facet Christian Cammarota
Nicole S Dawney
Philip M Bellomio
Maren Jüng
Alexander G Fletcher
Tara M Finegan
Dan T Bergstralh
author_sort Christian Cammarota
collection DOAJ
description Epithelial tissues are the most abundant tissue type in animals, lining body cavities and generating compartment barriers. The function of a monolayered epithelial tissue-whether protective, secretory, absorptive, or filtrative-relies on the side-by-side arrangement of its component cells. The mechanical parameters that determine the shape of epithelial cells in the apical-basal plane are not well-understood. Epithelial tissue architecture in culture is intimately connected to cell density, and cultured layers transition between architectures as they proliferate. This prompted us to ask to what extent epithelial architecture emerges from two mechanical considerations: A) the constraints of densification and B) cell-cell adhesion, a hallmark feature of epithelial cells. To address these questions, we developed a novel polyline cell-based computational model and used it to make theoretical predictions about epithelial architecture upon changes to density and cell-cell adhesion. We tested these predictions using cultured cell experiments. Our results show that the appearance of extended lateral cell-cell borders in culture arises as a consequence of crowding-independent of cell-cell adhesion. However, cadherin-mediated cell-cell adhesion is associated with a novel architectural transition. Our results suggest that this transition represents the initial appearance of a distinctive epithelial architecture. Together our work reveals the distinct mechanical roles of densification and adhesion to epithelial layer formation and provides a novel theoretical framework to understand the less well-studied apical-basal plane of epithelial tissues.
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spelling doaj-art-c4e1ec2af1c44925ac01768b342d6c4e2024-12-11T05:31:04ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582024-04-01204e101200110.1371/journal.pcbi.1012001The mechanical influence of densification on epithelial architecture.Christian CammarotaNicole S DawneyPhilip M BellomioMaren JüngAlexander G FletcherTara M FineganDan T BergstralhEpithelial tissues are the most abundant tissue type in animals, lining body cavities and generating compartment barriers. The function of a monolayered epithelial tissue-whether protective, secretory, absorptive, or filtrative-relies on the side-by-side arrangement of its component cells. The mechanical parameters that determine the shape of epithelial cells in the apical-basal plane are not well-understood. Epithelial tissue architecture in culture is intimately connected to cell density, and cultured layers transition between architectures as they proliferate. This prompted us to ask to what extent epithelial architecture emerges from two mechanical considerations: A) the constraints of densification and B) cell-cell adhesion, a hallmark feature of epithelial cells. To address these questions, we developed a novel polyline cell-based computational model and used it to make theoretical predictions about epithelial architecture upon changes to density and cell-cell adhesion. We tested these predictions using cultured cell experiments. Our results show that the appearance of extended lateral cell-cell borders in culture arises as a consequence of crowding-independent of cell-cell adhesion. However, cadherin-mediated cell-cell adhesion is associated with a novel architectural transition. Our results suggest that this transition represents the initial appearance of a distinctive epithelial architecture. Together our work reveals the distinct mechanical roles of densification and adhesion to epithelial layer formation and provides a novel theoretical framework to understand the less well-studied apical-basal plane of epithelial tissues.https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1012001&type=printable
spellingShingle Christian Cammarota
Nicole S Dawney
Philip M Bellomio
Maren Jüng
Alexander G Fletcher
Tara M Finegan
Dan T Bergstralh
The mechanical influence of densification on epithelial architecture.
PLoS Computational Biology
title The mechanical influence of densification on epithelial architecture.
title_full The mechanical influence of densification on epithelial architecture.
title_fullStr The mechanical influence of densification on epithelial architecture.
title_full_unstemmed The mechanical influence of densification on epithelial architecture.
title_short The mechanical influence of densification on epithelial architecture.
title_sort mechanical influence of densification on epithelial architecture
url https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1012001&type=printable
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