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:	Michael C Holcomb, Guo-Jie Jason Gao, Mahsa Servati, Dylan Schneider, Presley K McNeely, Jeffrey H Thomas, Jerzy Blawzdziewicz
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2021
Materias:	Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/182bd432e56b4da9bba5cb57065a693d
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spelling	oai:doaj.org-article:182bd432e56b4da9bba5cb57065a693d2021-12-02T19:57:25ZMechanical feedback and robustness of apical constrictions in Drosophila embryo ventral furrow formation.1553-734X1553-735810.1371/journal.pcbi.1009173https://doaj.org/article/182bd432e56b4da9bba5cb57065a693d2021-07-01T00:00:00Zhttps://doi.org/10.1371/journal.pcbi.1009173https://doaj.org/toc/1553-734Xhttps://doaj.org/toc/1553-7358Formation 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.Michael C HolcombGuo-Jie Jason GaoMahsa ServatiDylan SchneiderPresley K McNeelyJeffrey H ThomasJerzy BlawzdziewiczPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Computational Biology, Vol 17, Iss 7, p e1009173 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Biology (General) QH301-705.5
spellingShingle	Biology (General) QH301-705.5 Michael C Holcomb Guo-Jie Jason Gao Mahsa Servati Dylan Schneider Presley K McNeely Jeffrey H Thomas Jerzy Blawzdziewicz Mechanical feedback and robustness of apical constrictions in Drosophila embryo ventral furrow formation.
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.
format	article
author	Michael C Holcomb Guo-Jie Jason Gao Mahsa Servati Dylan Schneider Presley K McNeely Jeffrey H Thomas Jerzy Blawzdziewicz
author_facet	Michael C Holcomb Guo-Jie Jason Gao Mahsa Servati Dylan Schneider Presley K McNeely Jeffrey H Thomas Jerzy Blawzdziewicz
author_sort	Michael C Holcomb
title	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_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_sort	mechanical feedback and robustness of apical constrictions in drosophila embryo ventral furrow formation.
publisher	Public Library of Science (PLoS)
publishDate	2021
url	https://doaj.org/article/182bd432e56b4da9bba5cb57065a693d
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_version_	1718375826539413504

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

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