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A Biomechanical Analysis of Ventral Furrow Formation in the Drosophila Melanogaster Embryo

The article provides a biomechanical analysis of ventral furrow formation in the Drosophila melanogaster embryo. Ventral furrow formation is the first large-scale morphogenetic movement in the fly embryo. It involves deformation of a uniform cellular monolayer formed following cellularisation, and h...

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Autores principales: Conte, Vito, Ulrich, Florian, Baum, Buzz, Muñoz, Jose, Veldhuis, Jim, Brodland, Wayne, Miodownik, Mark
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2012
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3325263/
https://www.ncbi.nlm.nih.gov/pubmed/22511944
http://dx.doi.org/10.1371/journal.pone.0034473
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author Conte, Vito
Ulrich, Florian
Baum, Buzz
Muñoz, Jose
Veldhuis, Jim
Brodland, Wayne
Miodownik, Mark
author_facet Conte, Vito
Ulrich, Florian
Baum, Buzz
Muñoz, Jose
Veldhuis, Jim
Brodland, Wayne
Miodownik, Mark
author_sort Conte, Vito
collection PubMed
description The article provides a biomechanical analysis of ventral furrow formation in the Drosophila melanogaster embryo. Ventral furrow formation is the first large-scale morphogenetic movement in the fly embryo. It involves deformation of a uniform cellular monolayer formed following cellularisation, and has therefore long been used as a simple system in which to explore the role of mechanics in force generation. Here we use a quantitative framework to carry out a systematic perturbation analysis to determine the role of each of the active forces observed. The analysis confirms that ventral furrow invagination arises from a combination of apical constriction and apical–basal shortening forces in the mesoderm, together with a combination of ectodermal forces. We show that the mesodermal forces are crucial for invagination: the loss of apical constriction leads to a loss of the furrow, while the mesodermal radial shortening forces are the primary cause of the internalisation of the future mesoderm as the furrow rises. Ectodermal forces play a minor but significant role in furrow formation: without ectodermal forces the furrow is slower to form, does not close properly and has an aberrant morphology. Nevertheless, despite changes in the active mesodermal and ectodermal forces lead to changes in the timing and extent of furrow, invagination is eventually achieved in most cases, implying that the system is robust to perturbation and therefore over-determined.
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spelling pubmed-33252632012-04-17 A Biomechanical Analysis of Ventral Furrow Formation in the Drosophila Melanogaster Embryo Conte, Vito Ulrich, Florian Baum, Buzz Muñoz, Jose Veldhuis, Jim Brodland, Wayne Miodownik, Mark PLoS One Research Article The article provides a biomechanical analysis of ventral furrow formation in the Drosophila melanogaster embryo. Ventral furrow formation is the first large-scale morphogenetic movement in the fly embryo. It involves deformation of a uniform cellular monolayer formed following cellularisation, and has therefore long been used as a simple system in which to explore the role of mechanics in force generation. Here we use a quantitative framework to carry out a systematic perturbation analysis to determine the role of each of the active forces observed. The analysis confirms that ventral furrow invagination arises from a combination of apical constriction and apical–basal shortening forces in the mesoderm, together with a combination of ectodermal forces. We show that the mesodermal forces are crucial for invagination: the loss of apical constriction leads to a loss of the furrow, while the mesodermal radial shortening forces are the primary cause of the internalisation of the future mesoderm as the furrow rises. Ectodermal forces play a minor but significant role in furrow formation: without ectodermal forces the furrow is slower to form, does not close properly and has an aberrant morphology. Nevertheless, despite changes in the active mesodermal and ectodermal forces lead to changes in the timing and extent of furrow, invagination is eventually achieved in most cases, implying that the system is robust to perturbation and therefore over-determined. Public Library of Science 2012-04-12 /pmc/articles/PMC3325263/ /pubmed/22511944 http://dx.doi.org/10.1371/journal.pone.0034473 Text en Conte et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Conte, Vito
Ulrich, Florian
Baum, Buzz
Muñoz, Jose
Veldhuis, Jim
Brodland, Wayne
Miodownik, Mark
A Biomechanical Analysis of Ventral Furrow Formation in the Drosophila Melanogaster Embryo
title A Biomechanical Analysis of Ventral Furrow Formation in the Drosophila Melanogaster Embryo
title_full A Biomechanical Analysis of Ventral Furrow Formation in the Drosophila Melanogaster Embryo
title_fullStr A Biomechanical Analysis of Ventral Furrow Formation in the Drosophila Melanogaster Embryo
title_full_unstemmed A Biomechanical Analysis of Ventral Furrow Formation in the Drosophila Melanogaster Embryo
title_short A Biomechanical Analysis of Ventral Furrow Formation in the Drosophila Melanogaster Embryo
title_sort biomechanical analysis of ventral furrow formation in the drosophila melanogaster embryo
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3325263/
https://www.ncbi.nlm.nih.gov/pubmed/22511944
http://dx.doi.org/10.1371/journal.pone.0034473
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