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Strain maps characterize the symmetry of convergence and extension patterns during zebrafish gastrulation

During gastrulation of the zebrafish embryo, the cap of blastoderm cells organizes into the axial body plan of the embryo with left–right symmetry and head–tail, dorsal–ventral polarities. Our labs have been interested in the mechanics of early development and have investigated whether these large-s...

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Autores principales: Bhattacharya, Dipanjan, Zhong, Jun, Tavakoli, Sahar, Kabla, Alexandre, Matsudaira, Paul
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8481280/
https://www.ncbi.nlm.nih.gov/pubmed/34588480
http://dx.doi.org/10.1038/s41598-021-98233-z
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author Bhattacharya, Dipanjan
Zhong, Jun
Tavakoli, Sahar
Kabla, Alexandre
Matsudaira, Paul
author_facet Bhattacharya, Dipanjan
Zhong, Jun
Tavakoli, Sahar
Kabla, Alexandre
Matsudaira, Paul
author_sort Bhattacharya, Dipanjan
collection PubMed
description During gastrulation of the zebrafish embryo, the cap of blastoderm cells organizes into the axial body plan of the embryo with left–right symmetry and head–tail, dorsal–ventral polarities. Our labs have been interested in the mechanics of early development and have investigated whether these large-scale cell movements can be described as tissue-level mechanical strain by a tectonics-based approach. The first step is to image the positions of all nuclei from mid-epiboly to early segmentation by digital sheet light microscopy, organize the surface of the embryo into multi-cell spherical domains, construct velocity fields from the movements of these domains and extract strain rate maps from the change in density of the domains. During gastrulation, tensile/expansive and compressive strains in the axial and equatorial directions are detected as anterior and posterior expansion along the anterior–posterior axis and medial–lateral compression across the dorsal–ventral axis and corresponds to the well characterized morphological movements of convergence and extension. Following gastrulation strain is represented by localized medial expansion at the onset of segmentation and anterior expansion at the onset of neurulation. In addition to linear strain, symmetric patterns of rotation/curl are first detected in the animal hemispheres at mid-epiboly and then the vegetal hemispheres by the end of gastrulation. In embryos treated with C59, a Wnt inhibitor that inhibits head and tail extension, the axial extension and vegetal curl are absent. By analysing the temporal sequence of large-scale movements, deformations across the embryo can be attributed to a combination of epiboly and dorsal convergence-extension.
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spelling pubmed-84812802021-09-30 Strain maps characterize the symmetry of convergence and extension patterns during zebrafish gastrulation Bhattacharya, Dipanjan Zhong, Jun Tavakoli, Sahar Kabla, Alexandre Matsudaira, Paul Sci Rep Article During gastrulation of the zebrafish embryo, the cap of blastoderm cells organizes into the axial body plan of the embryo with left–right symmetry and head–tail, dorsal–ventral polarities. Our labs have been interested in the mechanics of early development and have investigated whether these large-scale cell movements can be described as tissue-level mechanical strain by a tectonics-based approach. The first step is to image the positions of all nuclei from mid-epiboly to early segmentation by digital sheet light microscopy, organize the surface of the embryo into multi-cell spherical domains, construct velocity fields from the movements of these domains and extract strain rate maps from the change in density of the domains. During gastrulation, tensile/expansive and compressive strains in the axial and equatorial directions are detected as anterior and posterior expansion along the anterior–posterior axis and medial–lateral compression across the dorsal–ventral axis and corresponds to the well characterized morphological movements of convergence and extension. Following gastrulation strain is represented by localized medial expansion at the onset of segmentation and anterior expansion at the onset of neurulation. In addition to linear strain, symmetric patterns of rotation/curl are first detected in the animal hemispheres at mid-epiboly and then the vegetal hemispheres by the end of gastrulation. In embryos treated with C59, a Wnt inhibitor that inhibits head and tail extension, the axial extension and vegetal curl are absent. By analysing the temporal sequence of large-scale movements, deformations across the embryo can be attributed to a combination of epiboly and dorsal convergence-extension. Nature Publishing Group UK 2021-09-29 /pmc/articles/PMC8481280/ /pubmed/34588480 http://dx.doi.org/10.1038/s41598-021-98233-z Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Bhattacharya, Dipanjan
Zhong, Jun
Tavakoli, Sahar
Kabla, Alexandre
Matsudaira, Paul
Strain maps characterize the symmetry of convergence and extension patterns during zebrafish gastrulation
title Strain maps characterize the symmetry of convergence and extension patterns during zebrafish gastrulation
title_full Strain maps characterize the symmetry of convergence and extension patterns during zebrafish gastrulation
title_fullStr Strain maps characterize the symmetry of convergence and extension patterns during zebrafish gastrulation
title_full_unstemmed Strain maps characterize the symmetry of convergence and extension patterns during zebrafish gastrulation
title_short Strain maps characterize the symmetry of convergence and extension patterns during zebrafish gastrulation
title_sort strain maps characterize the symmetry of convergence and extension patterns during zebrafish gastrulation
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8481280/
https://www.ncbi.nlm.nih.gov/pubmed/34588480
http://dx.doi.org/10.1038/s41598-021-98233-z
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