Literature DB >> 34293302

Using optogenetics to link myosin patterns to contractile cell behaviors during convergent extension.

R Marisol Herrera-Perez1, Christian Cupo1, Cole Allan1, Annie Lin1, Karen E Kasza2.   

Abstract

Distinct patterns of actomyosin contractility are often associated with particular epithelial tissue shape changes during development. For example, a planar-polarized pattern of myosin II localization regulated by Rho1 signaling during Drosophila body axis elongation is thought to drive cell behaviors that contribute to convergent extension. However, it is not well understood how specific aspects of a myosin pattern influence the multiple cell behaviors, including cell intercalation, cell shape changes, and apical cell area fluctuations, that simultaneously occur during morphogenesis. Here, we developed two optogenetic tools, optoGEF and optoGAP, to activate or deactivate Rho1 signaling, respectively. We used these tools to manipulate myosin patterns at the apical side of the germband epithelium during Drosophila axis elongation and analyzed the effects on contractile cell behaviors. We show that uniform activation or inactivation of Rho1 signaling across the apical surface of the germband is sufficient to disrupt the planar-polarized pattern of myosin at cell junctions on the timescale of 3-5 min, leading to distinct changes in junctional and medial myosin patterns in optoGEF and optoGAP embryos. These two perturbations to Rho1 activity both disrupt axis elongation and cell intercalation but have distinct effects on cell area fluctuations and cell packings that are linked with changes in the medial and junctional myosin pools. These studies demonstrate that acute optogenetic perturbations to Rho1 activity are sufficient to rapidly override the endogenous planar-polarized myosin pattern in the germband during axis elongation. Moreover, our results reveal that the levels of Rho1 activity and the balance between medial and junctional myosin play key roles not only in organizing the cell rearrangements that are known to directly contribute to axis elongation but also in regulating cell area fluctuations and cell packings, which have been proposed to be important factors influencing the mechanics of tissue deformation and flow.
Copyright © 2021 Biophysical Society. Published by Elsevier Inc. All rights reserved.

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Year:  2021        PMID: 34293302      PMCID: PMC8516680          DOI: 10.1016/j.bpj.2021.06.041

Source DB:  PubMed          Journal:  Biophys J        ISSN: 0006-3495            Impact factor:   3.699


  73 in total

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Journal:  Cell       Date:  1997-12-26       Impact factor: 41.582

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Journal:  Nature       Date:  2010-11-10       Impact factor: 49.962

3.  Repression of Wasp by JAK/STAT signalling inhibits medial actomyosin network assembly and apical cell constriction in intercalating epithelial cells.

Authors:  Claire Bertet; Matteo Rauzi; Thomas Lecuit
Journal:  Development       Date:  2009-12       Impact factor: 6.868

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Authors:  Claire Bertet; Lawrence Sulak; Thomas Lecuit
Journal:  Nature       Date:  2004-06-10       Impact factor: 49.962

5.  RhoA Mediates Epithelial Cell Shape Changes via Mechanosensitive Endocytosis.

Authors:  Kate E Cavanaugh; Michael F Staddon; Edwin Munro; Shiladitya Banerjee; Margaret L Gardel
Journal:  Dev Cell       Date:  2019-12-26       Impact factor: 12.270

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Journal:  Development       Date:  1994-04       Impact factor: 6.868

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Authors:  Matthew J Kennedy; Robert M Hughes; Leslie A Peteya; Joel W Schwartz; Michael D Ehlers; Chandra L Tucker
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8.  ImageJ2: ImageJ for the next generation of scientific image data.

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Journal:  BMC Bioinformatics       Date:  2017-11-29       Impact factor: 3.169

9.  Mechanical Coupling between Endoderm Invagination and Axis Extension in Drosophila.

Authors:  Claire M Lye; Guy B Blanchard; Huw W Naylor; Leila Muresan; Jan Huisken; Richard J Adams; Bénédicte Sanson
Journal:  PLoS Biol       Date:  2015-11-06       Impact factor: 8.029

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Authors:  Giorgia Guglielmi; Joseph D Barry; Wolfgang Huber; Stefano De Renzis
Journal:  Dev Cell       Date:  2015-12-07       Impact factor: 12.270

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  1 in total

1.  Distinct spatiotemporal contribution of morphogenetic events and mechanical tissue coupling during Xenopus neural tube closure.

Authors:  Neophytos Christodoulou; Paris A Skourides
Journal:  Development       Date:  2022-07-01       Impact factor: 6.862

  1 in total

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