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Mechanical feedback and robustness of apical constrictions in Drosophila embryo ventral furrow formation

Formation of the ventral furrow in the Drosophila embryo relies on the apical constriction of cells in the ventral region to produce bending forces that drive tissue invagination. In our recent paper we observed that apical constrictions during the initial phase of ventral furrow formation produce e...

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Autores principales: Holcomb, Michael C., Gao, Guo-Jie Jason, Servati, Mahsa, Schneider, Dylan, McNeely, Presley K., Thomas, Jeffrey H., Blawzdziewicz, Jerzy
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8284804/
https://www.ncbi.nlm.nih.gov/pubmed/34228708
http://dx.doi.org/10.1371/journal.pcbi.1009173
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author Holcomb, Michael C.
Gao, Guo-Jie Jason
Servati, Mahsa
Schneider, Dylan
McNeely, Presley K.
Thomas, Jeffrey H.
Blawzdziewicz, Jerzy
author_facet Holcomb, Michael C.
Gao, Guo-Jie Jason
Servati, Mahsa
Schneider, Dylan
McNeely, Presley K.
Thomas, Jeffrey H.
Blawzdziewicz, Jerzy
author_sort Holcomb, Michael C.
collection PubMed
description Formation of the ventral furrow in the Drosophila embryo relies on the apical constriction of cells in the ventral region to produce bending forces that drive tissue invagination. In our recent paper we observed that apical constrictions during the initial phase of ventral furrow formation produce elongated patterns of cellular constriction chains prior to invagination and argued that these are indicative of tensile stress feedback. Here, we quantitatively analyze the constriction patterns preceding ventral furrow formation and find that they are consistent with the predictions of our active-granular-fluid model of a monolayer of mechanically coupled stress-sensitive constricting particles. Our model shows that tensile feedback causes constriction chains to develop along underlying precursor tensile stress chains that gradually strengthen with subsequent cellular constrictions. As seen in both our model and available optogenetic experiments, this mechanism allows constriction chains to penetrate or circumvent zones of reduced cell contractility, thus increasing the robustness of ventral furrow formation to spatial variation of cell contractility by rescuing cellular constrictions in the disrupted regions.
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spelling pubmed-82848042021-07-28 Mechanical feedback and robustness of apical constrictions in Drosophila embryo ventral furrow formation Holcomb, Michael C. Gao, Guo-Jie Jason Servati, Mahsa Schneider, Dylan McNeely, Presley K. Thomas, Jeffrey H. Blawzdziewicz, Jerzy PLoS Comput Biol Research Article Formation of the ventral furrow in the Drosophila embryo relies on the apical constriction of cells in the ventral region to produce bending forces that drive tissue invagination. In our recent paper we observed that apical constrictions during the initial phase of ventral furrow formation produce elongated patterns of cellular constriction chains prior to invagination and argued that these are indicative of tensile stress feedback. Here, we quantitatively analyze the constriction patterns preceding ventral furrow formation and find that they are consistent with the predictions of our active-granular-fluid model of a monolayer of mechanically coupled stress-sensitive constricting particles. Our model shows that tensile feedback causes constriction chains to develop along underlying precursor tensile stress chains that gradually strengthen with subsequent cellular constrictions. As seen in both our model and available optogenetic experiments, this mechanism allows constriction chains to penetrate or circumvent zones of reduced cell contractility, thus increasing the robustness of ventral furrow formation to spatial variation of cell contractility by rescuing cellular constrictions in the disrupted regions. Public Library of Science 2021-07-06 /pmc/articles/PMC8284804/ /pubmed/34228708 http://dx.doi.org/10.1371/journal.pcbi.1009173 Text en © 2021 Holcomb et al 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
Holcomb, Michael C.
Gao, Guo-Jie Jason
Servati, Mahsa
Schneider, Dylan
McNeely, Presley K.
Thomas, Jeffrey H.
Blawzdziewicz, Jerzy
Mechanical feedback and robustness of apical constrictions in Drosophila embryo ventral furrow formation
title Mechanical feedback and robustness of apical constrictions in Drosophila embryo ventral furrow formation
title_full Mechanical feedback and robustness of apical constrictions in Drosophila embryo ventral furrow formation
title_fullStr Mechanical feedback and robustness of apical constrictions in Drosophila embryo ventral furrow formation
title_full_unstemmed Mechanical feedback and robustness of apical constrictions in Drosophila embryo ventral furrow formation
title_short Mechanical feedback and robustness of apical constrictions in Drosophila embryo ventral furrow formation
title_sort mechanical feedback and robustness of apical constrictions in drosophila embryo ventral furrow formation
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8284804/
https://www.ncbi.nlm.nih.gov/pubmed/34228708
http://dx.doi.org/10.1371/journal.pcbi.1009173
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