Myoblast cytonemes mediate Wg signaling from the wing imaginal disc and Delta-Notch signaling to the air sac primordium

Elife. 2015 May 7;4:e06114. doi: 10.7554/eLife.06114.

Abstract

The flight muscles, dorsal air sacs, wing blades, and thoracic cuticle of the Drosophila adult function in concert, and their progenitor cells develop together in the wing imaginal disc. The wing disc orchestrates dorsal air sac development by producing decapentaplegic and fibroblast growth factor that travel via specific cytonemes in order to signal to the air sac primordium (ASP). Here, we report that cytonemes also link flight muscle progenitors (myoblasts) to disc cells and to the ASP, enabling myoblasts to relay signaling between the disc and the ASP. Frizzled (Fz)-containing myoblast cytonemes take up Wingless (Wg) from the disc, and Delta (Dl)-containing myoblast cytonemes contribute to Notch activation in the ASP. Wg signaling negatively regulates Dl expression in the myoblasts. These results reveal an essential role for cytonemes in Wg and Notch signaling and for a signal relay system in the myoblasts.

Keywords: D. melanogaster; Delta; Notch; Wingless; cell biology; cytoneme; developmental biology; diaphanous; frizzled; stem cells.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Air Sacs / cytology
  • Air Sacs / growth & development
  • Air Sacs / metabolism
  • Animals
  • Body Patterning / genetics
  • Drosophila Proteins / genetics*
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster / genetics*
  • Drosophila melanogaster / growth & development
  • Drosophila melanogaster / metabolism
  • Embryo, Nonmammalian
  • Fibroblast Growth Factors / genetics
  • Fibroblast Growth Factors / metabolism
  • Frizzled Receptors / genetics
  • Frizzled Receptors / metabolism
  • Gene Expression Regulation, Developmental
  • Genes, Reporter
  • Green Fluorescent Proteins / genetics
  • Green Fluorescent Proteins / metabolism
  • Imaginal Discs / cytology
  • Imaginal Discs / growth & development
  • Imaginal Discs / metabolism
  • Intracellular Signaling Peptides and Proteins / genetics*
  • Intracellular Signaling Peptides and Proteins / metabolism
  • Larva / genetics
  • Larva / growth & development
  • Larva / metabolism
  • Luminescent Proteins / genetics
  • Luminescent Proteins / metabolism
  • Membrane Proteins / genetics*
  • Membrane Proteins / metabolism
  • Myoblasts / cytology
  • Myoblasts / metabolism*
  • Protein Transport
  • Receptors, Notch / genetics*
  • Receptors, Notch / metabolism
  • Signal Transduction
  • Wings, Animal / cytology
  • Wings, Animal / growth & development
  • Wings, Animal / metabolism*
  • Wnt1 Protein / genetics*
  • Wnt1 Protein / metabolism

Substances

  • Drosophila Proteins
  • Frizzled Receptors
  • Intracellular Signaling Peptides and Proteins
  • Luminescent Proteins
  • Membrane Proteins
  • N protein, Drosophila
  • Receptors, Notch
  • Wnt1 Protein
  • delta protein
  • dpp protein, Drosophila
  • fz protein, Drosophila
  • red fluorescent protein
  • wg protein, Drosophila
  • Green Fluorescent Proteins
  • Fibroblast Growth Factors