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3D cell neighbour dynamics in growing pseudostratified epithelia

During morphogenesis, epithelial sheets remodel into complex geometries. How cells dynamically organise their contact with neighbouring cells in these tightly packed tissues is poorly understood. We have used light-sheet microscopy of growing mouse embryonic lung explants, three-dimensional cell seg...

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Autores principales: Gómez, Harold Fernando, Dumond, Mathilde Sabine, Hodel, Leonie, Vetter, Roman, Iber, Dagmar
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8570695/
https://www.ncbi.nlm.nih.gov/pubmed/34609280
http://dx.doi.org/10.7554/eLife.68135
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author Gómez, Harold Fernando
Dumond, Mathilde Sabine
Hodel, Leonie
Vetter, Roman
Iber, Dagmar
author_facet Gómez, Harold Fernando
Dumond, Mathilde Sabine
Hodel, Leonie
Vetter, Roman
Iber, Dagmar
author_sort Gómez, Harold Fernando
collection PubMed
description During morphogenesis, epithelial sheets remodel into complex geometries. How cells dynamically organise their contact with neighbouring cells in these tightly packed tissues is poorly understood. We have used light-sheet microscopy of growing mouse embryonic lung explants, three-dimensional cell segmentation, and physical theory to unravel the principles behind 3D cell organisation in growing pseudostratified epithelia. We find that cells have highly irregular 3D shapes and exhibit numerous neighbour intercalations along the apical-basal axis as well as over time. Despite the fluidic nature, the cell packing configurations follow fundamental relationships previously described for apical epithelial layers, that is, Euler's polyhedron formula, Lewis’ law, and Aboav-Weaire's law, at all times and across the entire tissue thickness. This arrangement minimises the lateral cell-cell surface energy for a given cross-sectional area variability, generated primarily by the distribution and movement of nuclei. We conclude that the complex 3D cell organisation in growing epithelia emerges from simple physical principles.
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spelling pubmed-85706952021-11-08 3D cell neighbour dynamics in growing pseudostratified epithelia Gómez, Harold Fernando Dumond, Mathilde Sabine Hodel, Leonie Vetter, Roman Iber, Dagmar eLife Cell Biology During morphogenesis, epithelial sheets remodel into complex geometries. How cells dynamically organise their contact with neighbouring cells in these tightly packed tissues is poorly understood. We have used light-sheet microscopy of growing mouse embryonic lung explants, three-dimensional cell segmentation, and physical theory to unravel the principles behind 3D cell organisation in growing pseudostratified epithelia. We find that cells have highly irregular 3D shapes and exhibit numerous neighbour intercalations along the apical-basal axis as well as over time. Despite the fluidic nature, the cell packing configurations follow fundamental relationships previously described for apical epithelial layers, that is, Euler's polyhedron formula, Lewis’ law, and Aboav-Weaire's law, at all times and across the entire tissue thickness. This arrangement minimises the lateral cell-cell surface energy for a given cross-sectional area variability, generated primarily by the distribution and movement of nuclei. We conclude that the complex 3D cell organisation in growing epithelia emerges from simple physical principles. eLife Sciences Publications, Ltd 2021-10-05 /pmc/articles/PMC8570695/ /pubmed/34609280 http://dx.doi.org/10.7554/eLife.68135 Text en © 2021, Gómez et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Cell Biology
Gómez, Harold Fernando
Dumond, Mathilde Sabine
Hodel, Leonie
Vetter, Roman
Iber, Dagmar
3D cell neighbour dynamics in growing pseudostratified epithelia
title 3D cell neighbour dynamics in growing pseudostratified epithelia
title_full 3D cell neighbour dynamics in growing pseudostratified epithelia
title_fullStr 3D cell neighbour dynamics in growing pseudostratified epithelia
title_full_unstemmed 3D cell neighbour dynamics in growing pseudostratified epithelia
title_short 3D cell neighbour dynamics in growing pseudostratified epithelia
title_sort 3d cell neighbour dynamics in growing pseudostratified epithelia
topic Cell Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8570695/
https://www.ncbi.nlm.nih.gov/pubmed/34609280
http://dx.doi.org/10.7554/eLife.68135
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