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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Main Authors: Natalie A Dye, Marko Popović, K Venkatesan Iyer, Jana F Fuhrmann, Romina Piscitello-Gómez, Suzanne Eaton, Frank Jülicher
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2021-03-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/57964
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spelling doaj-ca64a839674142df8e8a7e282818c79f2021-05-27T14:08:16ZengeLife Sciences Publications LtdeLife2050-084X2021-03-011010.7554/eLife.57964Self-organized patterning of cell morphology via mechanosensitive feedbackNatalie A Dye0https://orcid.org/0000-0002-4859-6670Marko Popović1https://orcid.org/0000-0003-2360-3982K Venkatesan Iyer2Jana F Fuhrmann3Romina Piscitello-Gómez4Suzanne Eaton5Frank Jülicher6https://orcid.org/0000-0003-4731-9185Max Planck Institute for Molecular Cell Biology and Genetics, Dresden, Germany; Cluster of Excellence Physics of Life, Technische Universität Dresden, Dresden, Germany; Mildred Scheel Nachwuchszentrum (MSNZ) P2, Medical Faculty, Technische Universität Dresden, Dresden, GermanyInstitute of Physics, École Polytechnique Fédérale de Lausanne, Lausanne, Switzerland; Max Planck Institute for the Physics of Complex Systems, Dresden, Germany; Center for Systems Biology Dresden, Dresden, GermanyMax Planck Institute for Molecular Cell Biology and Genetics, Dresden, Germany; Cluster of Excellence Physics of Life, Technische Universität Dresden, Dresden, GermanyMax Planck Institute for Molecular Cell Biology and Genetics, Dresden, Germany; Cluster of Excellence Physics of Life, Technische Universität Dresden, Dresden, GermanyMax Planck Institute for Molecular Cell Biology and Genetics, Dresden, Germany; Cluster of Excellence Physics of Life, Technische Universität Dresden, Dresden, GermanyMax Planck Institute for Molecular Cell Biology and Genetics, Dresden, Germany; Cluster of Excellence Physics of Life, Technische Universität Dresden, Dresden, GermanyCluster of Excellence Physics of Life, Technische Universität Dresden, Dresden, Germany; Max Planck Institute for the Physics of Complex Systems, Dresden, Germany; Center for Systems Biology Dresden, Dresden, GermanyTissue 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.https://elifesciences.org/articles/57964mechanosensitivitypatterningmorphogenesisself-organizationlaser ablationmyosinVI
collection DOAJ
language English
format Article
sources DOAJ
author Natalie A Dye
Marko Popović
K Venkatesan Iyer
Jana F Fuhrmann
Romina Piscitello-Gómez
Suzanne Eaton
Frank Jülicher
spellingShingle Natalie A Dye
Marko Popović
K Venkatesan Iyer
Jana F Fuhrmann
Romina Piscitello-Gómez
Suzanne Eaton
Frank Jülicher
Self-organized patterning of cell morphology via mechanosensitive feedback
eLife
mechanosensitivity
patterning
morphogenesis
self-organization
laser ablation
myosinVI
author_facet Natalie A Dye
Marko Popović
K Venkatesan Iyer
Jana F Fuhrmann
Romina Piscitello-Gómez
Suzanne Eaton
Frank Jülicher
author_sort Natalie A Dye
title Self-organized patterning of cell morphology via mechanosensitive feedback
title_short 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_sort self-organized patterning of cell morphology via mechanosensitive feedback
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2021-03-01
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.
topic mechanosensitivity
patterning
morphogenesis
self-organization
laser ablation
myosinVI
url https://elifesciences.org/articles/57964
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AT markopopovic selforganizedpatterningofcellmorphologyviamechanosensitivefeedback
AT kvenkatesaniyer selforganizedpatterningofcellmorphologyviamechanosensitivefeedback
AT janaffuhrmann selforganizedpatterningofcellmorphologyviamechanosensitivefeedback
AT rominapiscitellogomez selforganizedpatterningofcellmorphologyviamechanosensitivefeedback
AT suzanneeaton selforganizedpatterningofcellmorphologyviamechanosensitivefeedback
AT frankjulicher selforganizedpatterningofcellmorphologyviamechanosensitivefeedback
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