Literature DB >> 26102528

Interplay of cell dynamics and epithelial tension during morphogenesis of the Drosophila pupal wing.

Raphaël Etournay1, Marko Popović2, Matthias Merkel2, Amitabha Nandi2, Corinna Blasse1, Benoît Aigouy3, Holger Brandl1, Gene Myers1, Guillaume Salbreux2, Frank Jülicher2, Suzanne Eaton1.   

Abstract

How tissue shape emerges from the collective mechanical properties and behavior of individual cells is not understood. We combine experiment and theory to study this problem in the developing wing epithelium of Drosophila. At pupal stages, the wing-hinge contraction contributes to anisotropic tissue flows that reshape the wing blade. Here, we quantitatively account for this wing-blade shape change on the basis of cell divisions, cell rearrangements and cell shape changes. We show that cells both generate and respond to epithelial stresses during this process, and that the nature of this interplay specifies the pattern of junctional network remodeling that changes wing shape. We show that patterned constraints exerted on the tissue by the extracellular matrix are key to force the tissue into the right shape. We present a continuum mechanical model that quantitatively describes the relationship between epithelial stresses and cell dynamics, and how their interplay reshapes the wing.

Entities:  

Keywords:  D. melanogaster; Drosophila; cell biology; cell-dynamics; computational biology; continuum-mechanics; morphogenesis; systems biology; tissue-mechanics; wing-epithelium

Mesh:

Year:  2015        PMID: 26102528      PMCID: PMC4574473          DOI: 10.7554/eLife.07090

Source DB:  PubMed          Journal:  Elife        ISSN: 2050-084X            Impact factor:   8.140


  52 in total

1.  Tension-dependent collective cell movements in the early gastrula ectoderm of Xenopus laevis embryos.

Authors:  L V Beloussov; N N Louchinskaia; A A Stein
Journal:  Dev Genes Evol       Date:  2000-02       Impact factor: 0.900

2.  The influence of cell mechanics, cell-cell interactions, and proliferation on epithelial packing.

Authors:  Reza Farhadifar; Jens-Christian Röper; Benoit Aigouy; Suzanne Eaton; Frank Jülicher
Journal:  Curr Biol       Date:  2007-12-18       Impact factor: 10.834

3.  From the Cover: Directed, efficient, and versatile modifications of the Drosophila genome by genomic engineering.

Authors:  Juan Huang; Wenke Zhou; Wei Dong; Annie M Watson; Yang Hong
Journal:  Proc Natl Acad Sci U S A       Date:  2009-05-08       Impact factor: 11.205

4.  Imaging Drosophila pupal wing morphogenesis.

Authors:  Anne-Kathrin Classen; Benoit Aigouy; Angela Giangrande; Suzanne Eaton
Journal:  Methods Mol Biol       Date:  2008

5.  Discrete rearranging disordered patterns, part I: robust statistical tools in two or three dimensions.

Authors:  F Graner; B Dollet; C Raufaste; P Marmottant
Journal:  Eur Phys J E Soft Matter       Date:  2008-04-30       Impact factor: 1.890

6.  Direct laser manipulation reveals the mechanics of cell contacts in vivo.

Authors:  Kapil Bambardekar; Raphaël Clément; Olivier Blanc; Claire Chardès; Pierre-François Lenne
Journal:  Proc Natl Acad Sci U S A       Date:  2015-01-20       Impact factor: 11.205

7.  Cell interactions in the control of size in Drosophila wings.

Authors:  A García-Bellido; F Cortés; M Milán
Journal:  Proc Natl Acad Sci U S A       Date:  1994-10-11       Impact factor: 11.205

8.  Globally optimal stitching of tiled 3D microscopic image acquisitions.

Authors:  Stephan Preibisch; Stephan Saalfeld; Pavel Tomancak
Journal:  Bioinformatics       Date:  2009-04-03       Impact factor: 6.937

9.  The Frizzled-dependent planar polarity pathway locally promotes E-cadherin turnover via recruitment of RhoGEF2.

Authors:  Samantha J Warrington; Helen Strutt; David Strutt
Journal:  Development       Date:  2013-01-30       Impact factor: 6.868

10.  Genetic analysis of the Drosophila cdc2 homolog.

Authors:  B Stern; G Ried; N J Clegg; T A Grigliatti; C F Lehner
Journal:  Development       Date:  1993-01       Impact factor: 6.868

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  82 in total

Review 1.  Programmed and self-organized flow of information during morphogenesis.

Authors:  Claudio Collinet; Thomas Lecuit
Journal:  Nat Rev Mol Cell Biol       Date:  2021-01-22       Impact factor: 94.444

Review 2.  Taking the strain: quantifying the contributions of all cell behaviours to changes in epithelial shape.

Authors:  Guy B Blanchard
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2017-05-19       Impact factor: 6.237

Review 3.  Complex structures from patterned cell sheets.

Authors:  M Misra; B Audoly; S Y Shvartsman
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2017-05-19       Impact factor: 6.237

Review 4.  Deciphering tissue morphodynamics using bioimage informatics.

Authors:  Alexandre C Dufour; Anneliene H Jonker; Jean-Christophe Olivo-Marin
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2017-05-19       Impact factor: 6.237

5.  Tissue Flow Induces Cell Shape Changes During Organogenesis.

Authors:  Gonca Erdemci-Tandogan; Madeline J Clark; Jeffrey D Amack; M Lisa Manning
Journal:  Biophys J       Date:  2018-11-06       Impact factor: 4.033

6.  Arf6 determines tissue architecture by stabilizing intercellular adhesion.

Authors:  Joshua Greig; Natalia A Bulgakova
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2020-08-24       Impact factor: 6.237

Review 7.  Tension, contraction and tissue morphogenesis.

Authors:  Natalie C Heer; Adam C Martin
Journal:  Development       Date:  2017-12-01       Impact factor: 6.868

8.  Unified quantitative characterization of epithelial tissue development.

Authors:  Boris Guirao; Stéphane U Rigaud; Floris Bosveld; Anaïs Bailles; Jesús López-Gay; Shuji Ishihara; Kaoru Sugimura; François Graner; Yohanns Bellaïche
Journal:  Elife       Date:  2015-12-12       Impact factor: 8.140

9.  Cell volume changes contribute to epithelial morphogenesis in zebrafish Kupffer's vesicle.

Authors:  Agnik Dasgupta; Matthias Merkel; Madeline J Clark; Andrew E Jacob; Jonathan Edward Dawson; M Lisa Manning; Jeffrey D Amack
Journal:  Elife       Date:  2018-01-29       Impact factor: 8.140

Review 10.  Using cell deformation and motion to predict forces and collective behavior in morphogenesis.

Authors:  Matthias Merkel; M Lisa Manning
Journal:  Semin Cell Dev Biol       Date:  2016-08-02       Impact factor: 7.727

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