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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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. |
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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.</description><identifier>ISSN: 1553-7358</identifier><identifier>ISSN: 1553-734X</identifier><identifier>EISSN: 1553-7358</identifier><identifier>DOI: 10.1371/journal.pcbi.1005443</identifier><identifier>PMID: 28346461</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>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</subject><ispartof>PLoS computational biology, 2017-03, Vol.13 (3), p.e1005443-e1005443</ispartof><rights>COPYRIGHT 2017 Public Library of Science</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. 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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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.</description><subject>Actomyosin</subject><subject>Actomyosin - physiology</subject><subject>Animals</subject><subject>Biological Physics</subject><subject>Biology and Life Sciences</subject><subject>Body Patterning - physiology</subject><subject>Cell size</subject><subject>Cellular Biology</subject><subject>Computer Simulation</subject><subject>Contractility</subject><subject>Deformation</subject><subject>Development Biology</subject><subject>Drosophila</subject><subject>Drosophila - embryology</subject><subject>Drosophila - physiology</subject><subject>Embryo, Nonmammalian - embryology</subject><subject>Embryo, Nonmammalian - physiology</subject><subject>Embryogenesis</subject><subject>Embryonic development</subject><subject>Embryonic Development - physiology</subject><subject>Embryonic growth stage</subject><subject>Embryos</subject><subject>Epithelium</subject><subject>Feedback</subject><subject>Flow distribution</subject><subject>Fluid mechanics</subject><subject>Fruit flies</subject><subject>Gene expression</subject><subject>Geometry</subject><subject>Insects</subject><subject>Life Sciences</subject><subject>Light sheets</subject><subject>Machinery</subject><subject>Mechanics</subject><subject>Mechanics of materials</subject><subject>Mechanotransduction, Cellular - 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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. 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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 |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-09T15%3A56%3A05IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Geometry%20can%20provide%20long-range%20mechanical%20guidance%20for%20embryogenesis&rft.jtitle=PLoS%20computational%20biology&rft.au=Dicko,%20Mahamar&rft.date=2017-03-01&rft.volume=13&rft.issue=3&rft.spage=e1005443&rft.epage=e1005443&rft.pages=e1005443-e1005443&rft.issn=1553-7358&rft.eissn=1553-7358&rft_id=info:doi/10.1371/journal.pcbi.1005443&rft_dat=%3Cgale_plos_%3EA493714135%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1888661348&rft_id=info:pmid/28346461&rft_galeid=A493714135&rft_doaj_id=oai_doaj_org_article_aea5d6f8f3654a21b41673dabc039cd4&rfr_iscdi=true |