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Cell shape anisotropy contributes to self-organized feather pattern fidelity in birds

Developing tissues can self-organize into a variety of patterned structures through the stabilization of stochastic fluctuations in their molecular and cellular properties. While molecular factors and cell dynamics contributing to self-organization have been identified in vivo, events channeling sel...

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Autores principales: Curantz, Camille, Bailleul, Richard, Castro-Scherianz, María, Hidalgo, Magdalena, Durande, Melina, Graner, François, Manceau, Marie
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9584522/
https://www.ncbi.nlm.nih.gov/pubmed/36215298
http://dx.doi.org/10.1371/journal.pbio.3001807
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author Curantz, Camille
Bailleul, Richard
Castro-Scherianz, María
Hidalgo, Magdalena
Durande, Melina
Graner, François
Manceau, Marie
author_facet Curantz, Camille
Bailleul, Richard
Castro-Scherianz, María
Hidalgo, Magdalena
Durande, Melina
Graner, François
Manceau, Marie
author_sort Curantz, Camille
collection PubMed
description Developing tissues can self-organize into a variety of patterned structures through the stabilization of stochastic fluctuations in their molecular and cellular properties. While molecular factors and cell dynamics contributing to self-organization have been identified in vivo, events channeling self-organized systems such that they achieve stable pattern outcomes remain unknown. Here, we described natural variation in the fidelity of self-organized arrays formed by feather follicle precursors in bird embryos. By surveying skin cells prior to and during tissue self-organization and performing species-specific ex vivo drug treatments and mechanical stress tests, we demonstrated that pattern fidelity depends on the initial amplitude of cell anisotropy in regions of the developing dermis competent to produce a pattern. Using live imaging, we showed that cell shape anisotropy is associated with a limited increase in cell motility for sharp and precisely located primordia formation, and thus, proper pattern geometry. These results evidence a mechanism through which initial tissue properties ensure stability in self-organization and thus, reproducible pattern production.
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spelling pubmed-95845222022-10-21 Cell shape anisotropy contributes to self-organized feather pattern fidelity in birds Curantz, Camille Bailleul, Richard Castro-Scherianz, María Hidalgo, Magdalena Durande, Melina Graner, François Manceau, Marie PLoS Biol Research Article Developing tissues can self-organize into a variety of patterned structures through the stabilization of stochastic fluctuations in their molecular and cellular properties. While molecular factors and cell dynamics contributing to self-organization have been identified in vivo, events channeling self-organized systems such that they achieve stable pattern outcomes remain unknown. Here, we described natural variation in the fidelity of self-organized arrays formed by feather follicle precursors in bird embryos. By surveying skin cells prior to and during tissue self-organization and performing species-specific ex vivo drug treatments and mechanical stress tests, we demonstrated that pattern fidelity depends on the initial amplitude of cell anisotropy in regions of the developing dermis competent to produce a pattern. Using live imaging, we showed that cell shape anisotropy is associated with a limited increase in cell motility for sharp and precisely located primordia formation, and thus, proper pattern geometry. These results evidence a mechanism through which initial tissue properties ensure stability in self-organization and thus, reproducible pattern production. Public Library of Science 2022-10-10 /pmc/articles/PMC9584522/ /pubmed/36215298 http://dx.doi.org/10.1371/journal.pbio.3001807 Text en © 2022 Curantz et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Curantz, Camille
Bailleul, Richard
Castro-Scherianz, María
Hidalgo, Magdalena
Durande, Melina
Graner, François
Manceau, Marie
Cell shape anisotropy contributes to self-organized feather pattern fidelity in birds
title Cell shape anisotropy contributes to self-organized feather pattern fidelity in birds
title_full Cell shape anisotropy contributes to self-organized feather pattern fidelity in birds
title_fullStr Cell shape anisotropy contributes to self-organized feather pattern fidelity in birds
title_full_unstemmed Cell shape anisotropy contributes to self-organized feather pattern fidelity in birds
title_short Cell shape anisotropy contributes to self-organized feather pattern fidelity in birds
title_sort cell shape anisotropy contributes to self-organized feather pattern fidelity in birds
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9584522/
https://www.ncbi.nlm.nih.gov/pubmed/36215298
http://dx.doi.org/10.1371/journal.pbio.3001807
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