Coupling between dynamic 3D tissue architecture and BMP morphogen signaling during Drosophila wing morphogenesis

Jinghua Gui, Yunxian Huang, Martin Kracklauer, Daniel John Toddie-Moore, Kenji Kikushima, Stephanie Nix, Yukitaka Ishimoto, Osamu Shimmi

Research output: Contribution to journalArticleScientificpeer-review

Abstract

At the level of organ formation, tissue morphogenesis drives developmental processes in animals, often involving the rearrangement of two-dimensional (2D) structures into more complex three-dimensional (3D) tissues. These processes can be directed by growth factor signaling pathways. However, little is known about how such morphological changes affect the spatiotemporal distribution of growth factor signaling. Here, using the Drosophila pupal wing, we address how decapentaplegic (Dpp)/bone morphogenetic protein (BMP) signaling and 3D wing morphogenesis are coordinated. Dpp, expressed in the longitudinal veins (LVs) of the pupal wing, initially diffuses laterally within both dorsal and ventral wing epithelia during the inflation stage to regulate cell proliferation. Dpp localization is then refined to the LVs within each epithelial plane, but with active interplanar signaling for vein patterning/differentiation, as the two epithelia appose. Our data further suggest that the 3D architecture of the wing epithelia and the spatial distribution of BMP signaling are tightly coupled, revealing that 3D morphogenesis is an emergent property of the interactions between extracellular signaling and tissue shape changes.

Original languageEnglish
JournalProceedings of the National Academy of Sciences of the United States of America
Volume116
Issue number10
Pages (from-to)4352-4361
Number of pages10
ISSN0027-8424
DOIs
Publication statusPublished - 5 Mar 2019
MoE publication typeA1 Journal article-refereed

Fields of Science

  • BRINKER
  • CLEFT-PALATE
  • DECAPENTAPLEGIC GENE
  • DPP
  • GRADIENT
  • GROWTH
  • MECHANISMS
  • ORGANIZATION
  • PATTERNS
  • PROLIFERATION
  • bone orphogenetic protein
  • drosophila
  • epithelial morphogenesis
  • live-imaging
  • three-dimensional architecture
  • 1184 Genetics, developmental biology, physiology

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