Differential lateral and basal tension drive folding of Drosophila wing discs through two distinct mechanisms

Research output: Contribution to journalResearch articleContributedpeer-review

Contributors

  • Liyuan Sui - , Chair of Systems Biology and Genetics (First author)
  • Silvanus Alt - , Max-Planck-Institute for the Physics of Complex Systems, The Francis Crick Institute, Max Delbrück Center for Molecular Medicine (MDC) (Author)
  • Martin Weigert - , Center for Systems Biology Dresden (CSBD), Max Planck Institute of Molecular Cell Biology and Genetics (Author)
  • Natalie Dye - , Max Planck Institute of Molecular Cell Biology and Genetics (Author)
  • Suzanne Eaton - , Chair of Developmental Cell Biology, Biotechnology Center (Author)
  • Florian Jug - , Center for Systems Biology Dresden (CSBD), Max Planck Institute of Molecular Cell Biology and Genetics (Author)
  • Eugene W. Meyers - , Center for Systems Biology Dresden (CSBD), Max Planck Institute of Molecular Cell Biology and Genetics, TUD Dresden University of Technology (Author)
  • Frank Jülicher - , Max-Planck-Institute for the Physics of Complex Systems, Center for Systems Biology Dresden (CSBD) (Author)
  • Guillaume Salbreux - , Max-Planck-Institute for the Physics of Complex Systems, The Francis Crick Institute (Author)
  • Christian Dahmann - , Chair of Systems Biology and Genetics (Author)

Abstract

Epithelial folding transforms simple sheets of cells into complex three-dimensional tissues and organs during animal development. Epithelial folding has mainly been attributed to mechanical forces generated by an apically localized actomyosin network, however, contributions of forces generated at basal and lateral cell surfaces remain largely unknown. Here we show that a local decrease of basal tension and an increased lateral tension, but not apical constriction, drive the formation of two neighboring folds in developing Drosophila wing imaginal discs. Spatially defined reduction of extracellular matrix density results in local decrease of basal tension in the first fold; fluctuations in F-actin lead to increased lateral tension in the second fold. Simulations using a 3D vertex model show that the two distinct mechanisms can drive epithelial folding. Our combination of lateral and basal tension measurements with a mechanical tissue model reveals how simple modulations of surface and edge tension drive complex three-dimensional morphological changes.

Details

Original languageEnglish
Article number4620
JournalNature Communications
Volume9
Issue number1
Publication statusPublished - 5 Nov 2018
Peer-reviewedYes

External IDs

Scopus 85056276928

Keywords

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