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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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 |
work_keys_str_mv |
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1721425592526569472 |