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Self-organized patterning of cell morphology via mechanosensitive feedback

Tissue organization is often characterized by specific patterns of cell morphology. How such patterns emerge in developing tissues is a fundamental open question. Here, we investigate the emergence of tissue-scale patterns of cell shape and mechanical tissue stress in the Drosophila wing imaginal di...

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Autores principales: Dye, Natalie A, Popović, Marko, Iyer, K Venkatesan, Fuhrmann, Jana F, Piscitello-Gómez, Romina, Eaton, Suzanne, Jülicher, Frank
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8133777/
https://www.ncbi.nlm.nih.gov/pubmed/33769281
http://dx.doi.org/10.7554/eLife.57964
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author Dye, Natalie A
Popović, Marko
Iyer, K Venkatesan
Fuhrmann, Jana F
Piscitello-Gómez, Romina
Eaton, Suzanne
Jülicher, Frank
author_facet Dye, Natalie A
Popović, Marko
Iyer, K Venkatesan
Fuhrmann, Jana F
Piscitello-Gómez, Romina
Eaton, Suzanne
Jülicher, Frank
author_sort Dye, Natalie A
collection PubMed
description Tissue organization is often characterized by specific patterns of cell morphology. How such patterns emerge in developing tissues is a fundamental open question. Here, we investigate the emergence of tissue-scale patterns of cell shape and mechanical tissue stress in the Drosophila wing imaginal disc during larval development. Using quantitative analysis of the cellular dynamics, we reveal a pattern of radially oriented cell rearrangements that is coupled to the buildup of tangential cell elongation. Developing a laser ablation method, we map tissue stresses and extract key parameters of tissue mechanics. We present a continuum theory showing that this pattern of cell morphology and tissue stress can arise via self-organization of a mechanical feedback that couples cell polarity to active cell rearrangements. The predictions of this model are supported by knockdown of MyoVI, a component of mechanosensitive feedback. Our work reveals a mechanism for the emergence of cellular patterns in morphogenesis.
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spelling pubmed-81337772021-05-21 Self-organized patterning of cell morphology via mechanosensitive feedback Dye, Natalie A Popović, Marko Iyer, K Venkatesan Fuhrmann, Jana F Piscitello-Gómez, Romina Eaton, Suzanne Jülicher, Frank eLife Developmental Biology Tissue organization is often characterized by specific patterns of cell morphology. How such patterns emerge in developing tissues is a fundamental open question. Here, we investigate the emergence of tissue-scale patterns of cell shape and mechanical tissue stress in the Drosophila wing imaginal disc during larval development. Using quantitative analysis of the cellular dynamics, we reveal a pattern of radially oriented cell rearrangements that is coupled to the buildup of tangential cell elongation. Developing a laser ablation method, we map tissue stresses and extract key parameters of tissue mechanics. We present a continuum theory showing that this pattern of cell morphology and tissue stress can arise via self-organization of a mechanical feedback that couples cell polarity to active cell rearrangements. The predictions of this model are supported by knockdown of MyoVI, a component of mechanosensitive feedback. Our work reveals a mechanism for the emergence of cellular patterns in morphogenesis. eLife Sciences Publications, Ltd 2021-03-26 /pmc/articles/PMC8133777/ /pubmed/33769281 http://dx.doi.org/10.7554/eLife.57964 Text en © 2021, Dye 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 Developmental Biology
Dye, Natalie A
Popović, Marko
Iyer, K Venkatesan
Fuhrmann, Jana F
Piscitello-Gómez, Romina
Eaton, Suzanne
Jülicher, Frank
Self-organized patterning of cell morphology via mechanosensitive feedback
title Self-organized patterning of cell morphology via mechanosensitive feedback
title_full Self-organized patterning of cell morphology via mechanosensitive feedback
title_fullStr Self-organized patterning of cell morphology via mechanosensitive feedback
title_full_unstemmed Self-organized patterning of cell morphology via mechanosensitive feedback
title_short Self-organized patterning of cell morphology via mechanosensitive feedback
title_sort self-organized patterning of cell morphology via mechanosensitive feedback
topic Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8133777/
https://www.ncbi.nlm.nih.gov/pubmed/33769281
http://dx.doi.org/10.7554/eLife.57964
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