Geometry can provide long-range mechanical guidance for embryogenesis

Downstream of gene expression, effectors such as the actomyosin contractile machinery drive embryo morphogenesis. During Drosophila embryonic axis extension, actomyosin has a specific planar-polarised organisation, which is responsible for oriented cell intercalation. In addition to these cell rearr...

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Veröffentlicht in:PLoS computational biology 2017-03, Vol.13 (3), p.e1005443-e1005443
Hauptverfasser: Dicko, Mahamar, Saramito, Pierre, Blanchard, Guy B, Lye, Claire M, Sanson, Bénédicte, Étienne, Jocelyn
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Saramito, Pierre
Blanchard, Guy B
Lye, Claire M
Sanson, Bénédicte
Étienne, Jocelyn
description Downstream of gene expression, effectors such as the actomyosin contractile machinery drive embryo morphogenesis. During Drosophila embryonic axis extension, actomyosin has a specific planar-polarised organisation, which is responsible for oriented cell intercalation. In addition to these cell rearrangements, cell shape changes also contribute to tissue deformation. While cell-autonomous dynamics are well described, understanding the tissue-scale behaviour challenges us to solve the corresponding mechanical problem at the scale of the whole embryo, since mechanical resistance of all neighbouring epithelia will feedback on individual cells. Here we propose a novel numerical approach to compute the whole-embryo dynamics of the actomyosin-rich apical epithelial surface. We input in the model specific patterns of actomyosin contractility, such as the planar-polarisation of actomyosin in defined ventro-lateral regions of the embryo. Tissue strain rates and displacements are then predicted over the whole embryo surface according to the global balance of stresses and the material behaviour of the epithelium. Epithelia are modelled using a rheological law that relates the rate of deformation to the local stresses and actomyosin anisotropic contractility. Predicted flow patterns are consistent with the cell flows observed when imaging Drosophila axis extension in toto, using light sheet microscopy. The agreement between model and experimental data indicates that the anisotropic contractility of planar-polarised actomyosin in the ventro-lateral germband tissue can directly cause the tissue-scale deformations of the whole embryo. The three-dimensional mechanical balance is dependent on the geometry of the embryo, whose curved surface is taken into account in the simulations. Importantly, we find that to reproduce experimental flows, the model requires the presence of the cephalic furrow, a fold located anteriorly of the extending tissues. The presence of this geometric feature, through the global mechanical balance, guides the flow and orients extension towards the posterior end.
doi_str_mv 10.1371/journal.pcbi.1005443
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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 credited: Dicko M, Saramito P, Blanchard GB, Lye CM, Sanson B, Étienne J (2017) Geometry can provide long-range mechanical guidance for embryogenesis. PLoS Comput Biol 13(3): e1005443. https://doi.org/10.1371/journal.pcbi.1005443</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><rights>2017 Dicko et al 2017 Dicko et al</rights><rights>2017 Public Library of Science. 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 credited: Dicko M, Saramito P, Blanchard GB, Lye CM, Sanson B, Étienne J (2017) Geometry can provide long-range mechanical guidance for embryogenesis. 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subjects Actomyosin
Actomyosin - physiology
Animals
Biological Physics
Biology and Life Sciences
Body Patterning - physiology
Cell size
Cellular Biology
Computer Simulation
Contractility
Deformation
Development Biology
Drosophila
Drosophila - embryology
Drosophila - physiology
Embryo, Nonmammalian - embryology
Embryo, Nonmammalian - physiology
Embryogenesis
Embryonic development
Embryonic Development - physiology
Embryonic growth stage
Embryos
Epithelium
Feedback
Flow distribution
Fluid mechanics
Fruit flies
Gene expression
Geometry
Insects
Life Sciences
Light sheets
Machinery
Mechanics
Mechanics of materials
Mechanotransduction, Cellular - physiology
Microscopy
Models, Biological
Molecular Motor Proteins - physiology
Morphogenesis
Neurosciences
Observations
Physical Sciences
Physics
Physiology
Research and Analysis Methods
Rheological properties
Stress, Mechanical
Stresses
Subcellular Processes
Tissues
title Geometry can provide long-range mechanical guidance for embryogenesis
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