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A comprehensive model of Drosophila epithelium reveals the role of embryo geometry and cell topology in mechanical responses

In order to understand morphogenesis, it is necessary to know the material properties or forces shaping the living tissue. In spite of this need, very few in vivo measurements are currently available. Here, using the early Drosophila embryo as a model, we describe a novel cantilever-based technique...

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Autores principales: Cheikh, Mohamad Ibrahim, Tchoufag, Joel, Osterfield, Miriam, Dean, Kevin, Bhaduri, Swayamdipta, Zhang, Chuzhong, Mandadapu, Kranthi Kiran, Doubrovinski, Konstantin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10584372/
https://www.ncbi.nlm.nih.gov/pubmed/37782009
http://dx.doi.org/10.7554/eLife.85569
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author Cheikh, Mohamad Ibrahim
Tchoufag, Joel
Osterfield, Miriam
Dean, Kevin
Bhaduri, Swayamdipta
Zhang, Chuzhong
Mandadapu, Kranthi Kiran
Doubrovinski, Konstantin
author_facet Cheikh, Mohamad Ibrahim
Tchoufag, Joel
Osterfield, Miriam
Dean, Kevin
Bhaduri, Swayamdipta
Zhang, Chuzhong
Mandadapu, Kranthi Kiran
Doubrovinski, Konstantin
author_sort Cheikh, Mohamad Ibrahim
collection PubMed
description In order to understand morphogenesis, it is necessary to know the material properties or forces shaping the living tissue. In spite of this need, very few in vivo measurements are currently available. Here, using the early Drosophila embryo as a model, we describe a novel cantilever-based technique which allows for the simultaneous quantification of applied force and tissue displacement in a living embryo. By analyzing data from a series of experiments in which embryonic epithelium is subjected to developmentally relevant perturbations, we conclude that the response to applied force is adiabatic and is dominated by elastic forces and geometric constraints, or system size effects. Crucially, computational modeling of the experimental data indicated that the apical surface of the epithelium must be softer than the basal surface, a result which we confirmed experimentally. Further, we used the combination of experimental data and comprehensive computational model to estimate the elastic modulus of the apical surface and set a lower bound on the elastic modulus of the basal surface. More generally, our investigations revealed important general features that we believe should be more widely addressed when quantitatively modeling tissue mechanics in any system. Specifically, different compartments of the same cell can have very different mechanical properties; when they do, they can contribute differently to different mechanical stimuli and cannot be merely averaged together. Additionally, tissue geometry can play a substantial role in mechanical response, and cannot be neglected.
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spelling pubmed-105843722023-10-19 A comprehensive model of Drosophila epithelium reveals the role of embryo geometry and cell topology in mechanical responses Cheikh, Mohamad Ibrahim Tchoufag, Joel Osterfield, Miriam Dean, Kevin Bhaduri, Swayamdipta Zhang, Chuzhong Mandadapu, Kranthi Kiran Doubrovinski, Konstantin eLife Computational and Systems Biology In order to understand morphogenesis, it is necessary to know the material properties or forces shaping the living tissue. In spite of this need, very few in vivo measurements are currently available. Here, using the early Drosophila embryo as a model, we describe a novel cantilever-based technique which allows for the simultaneous quantification of applied force and tissue displacement in a living embryo. By analyzing data from a series of experiments in which embryonic epithelium is subjected to developmentally relevant perturbations, we conclude that the response to applied force is adiabatic and is dominated by elastic forces and geometric constraints, or system size effects. Crucially, computational modeling of the experimental data indicated that the apical surface of the epithelium must be softer than the basal surface, a result which we confirmed experimentally. Further, we used the combination of experimental data and comprehensive computational model to estimate the elastic modulus of the apical surface and set a lower bound on the elastic modulus of the basal surface. More generally, our investigations revealed important general features that we believe should be more widely addressed when quantitatively modeling tissue mechanics in any system. Specifically, different compartments of the same cell can have very different mechanical properties; when they do, they can contribute differently to different mechanical stimuli and cannot be merely averaged together. Additionally, tissue geometry can play a substantial role in mechanical response, and cannot be neglected. eLife Sciences Publications, Ltd 2023-10-02 /pmc/articles/PMC10584372/ /pubmed/37782009 http://dx.doi.org/10.7554/eLife.85569 Text en https://creativecommons.org/publicdomain/zero/1.0/This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication (https://creativecommons.org/publicdomain/zero/1.0/) .
spellingShingle Computational and Systems Biology
Cheikh, Mohamad Ibrahim
Tchoufag, Joel
Osterfield, Miriam
Dean, Kevin
Bhaduri, Swayamdipta
Zhang, Chuzhong
Mandadapu, Kranthi Kiran
Doubrovinski, Konstantin
A comprehensive model of Drosophila epithelium reveals the role of embryo geometry and cell topology in mechanical responses
title A comprehensive model of Drosophila epithelium reveals the role of embryo geometry and cell topology in mechanical responses
title_full A comprehensive model of Drosophila epithelium reveals the role of embryo geometry and cell topology in mechanical responses
title_fullStr A comprehensive model of Drosophila epithelium reveals the role of embryo geometry and cell topology in mechanical responses
title_full_unstemmed A comprehensive model of Drosophila epithelium reveals the role of embryo geometry and cell topology in mechanical responses
title_short A comprehensive model of Drosophila epithelium reveals the role of embryo geometry and cell topology in mechanical responses
title_sort comprehensive model of drosophila epithelium reveals the role of embryo geometry and cell topology in mechanical responses
topic Computational and Systems Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10584372/
https://www.ncbi.nlm.nih.gov/pubmed/37782009
http://dx.doi.org/10.7554/eLife.85569
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