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

  1. Raphaël Etournay
  2. Marko Popović
  3. Matthias Merkel
  4. Amitabha Nandi
  5. Corinna Blasse
  6. Benoît Aigouy
  7. Holger Brandl
  8. Gene Myers
  9. Guillaume Salbreux
  10. Frank Jülicher
  11. Suzanne Eaton  Is a corresponding author
  1. Max Planck Institute of Molecular Cell Biology and Genetics, Germany
  2. Max Planck Institute for the Physics of Complex Systems, Germany
  3. Institut de Biologie du Développement de Marseille, France

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 constrains 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.

Article and author information

Author details

  1. Raphaël Etournay

    Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
    Competing interests
    No competing interests declared.
  2. Marko Popović

    Max Planck Institute for the Physics of Complex Systems, Dresden, Germany
    Competing interests
    No competing interests declared.
  3. Matthias Merkel

    Max Planck Institute for the Physics of Complex Systems, Dresden, Germany
    Competing interests
    No competing interests declared.
  4. Amitabha Nandi

    Max Planck Institute for the Physics of Complex Systems, Dresden, Germany
    Competing interests
    No competing interests declared.
  5. Corinna Blasse

    Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
    Competing interests
    No competing interests declared.
  6. Benoît Aigouy

    Institut de Biologie du Développement de Marseille, Marseille, France
    Competing interests
    No competing interests declared.
  7. Holger Brandl

    Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
    Competing interests
    No competing interests declared.
  8. Gene Myers

    Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
    Competing interests
    No competing interests declared.
  9. Guillaume Salbreux

    Max Planck Institute for the Physics of Complex Systems, Dresden, Germany
    Competing interests
    No competing interests declared.
  10. Frank Jülicher

    Max Planck Institute for the Physics of Complex Systems, Dresden, Germany
    Competing interests
    Frank Jülicher, Reviewing editor, eLife.
  11. Suzanne Eaton

    Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
    For correspondence
    eaton@mpi-cbg.de
    Competing interests
    No competing interests declared.

Copyright

© 2015, Etournay et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 8,790
    views
  • 2,475
    downloads
  • 325
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Raphaël Etournay
  2. Marko Popović
  3. Matthias Merkel
  4. Amitabha Nandi
  5. Corinna Blasse
  6. Benoît Aigouy
  7. Holger Brandl
  8. Gene Myers
  9. Guillaume Salbreux
  10. Frank Jülicher
  11. Suzanne Eaton
(2015)
Interplay of cell dynamics and epithelial tension during morphogenesis of the Drosophila pupal wing
eLife 4:e07090.
https://doi.org/10.7554/eLife.07090

Share this article

https://doi.org/10.7554/eLife.07090

Further reading

    1. Cell Biology
    Yan Song, Linda J Fothergill ... Gene W Yeo
    Research Article

    Dynamic interactions between gut mucosal cells and the external environment are essential to maintain gut homeostasis. Enterochromaffin (EC) cells transduce both chemical and mechanical signals and produce 5-hydroxytryptamine to mediate disparate physiological responses. However, the molecular and cellular basis for functional diversity of ECs remains to be adequately defined. Here, we integrated single-cell transcriptomics with spatial image analysis to identify 14 EC clusters that are topographically organized along the gut. Subtypes predicted to be sensitive to the chemical environment and mechanical forces were identified that express distinct transcription factors and hormones. A Piezo2+ population in the distal colon was endowed with a distinctive neuronal signature. Using a combination of genetic, chemogenetic, and pharmacological approaches, we demonstrated Piezo2+ ECs are required for normal colon motility. Our study constructs a molecular map for ECs and offers a framework for deconvoluting EC cells with pleiotropic functions.

    1. Cell Biology
    Kaili Du, Hongyu Chen ... Dan Li
    Research Article

    Niemann–Pick disease type C (NPC) is a devastating lysosomal storage disease characterized by abnormal cholesterol accumulation in lysosomes. Currently, there is no treatment for NPC. Transcription factor EB (TFEB), a member of the microphthalmia transcription factors (MiTF), has emerged as a master regulator of lysosomal function and promoted the clearance of substrates stored in cells. However, it is not known whether TFEB plays a role in cholesterol clearance in NPC disease. Here, we show that transgenic overexpression of TFEB, but not TFE3 (another member of MiTF family) facilitates cholesterol clearance in various NPC1 cell models. Pharmacological activation of TFEB by sulforaphane (SFN), a previously identified natural small-molecule TFEB agonist by us, can dramatically ameliorate cholesterol accumulation in human and mouse NPC1 cell models. In NPC1 cells, SFN induces TFEB nuclear translocation via a ROS-Ca2+-calcineurin-dependent but MTOR-independent pathway and upregulates the expression of TFEB-downstream genes, promoting lysosomal exocytosis and biogenesis. While genetic inhibition of TFEB abolishes the cholesterol clearance and exocytosis effect by SFN. In the NPC1 mouse model, SFN dephosphorylates/activates TFEB in the brain and exhibits potent efficacy of rescuing the loss of Purkinje cells and body weight. Hence, pharmacological upregulating lysosome machinery via targeting TFEB represents a promising approach to treat NPC and related lysosomal storage diseases, and provides the possibility of TFEB agonists, that is, SFN as potential NPC therapeutic candidates.