Escargot controls the sequential specification of two tracheal tip cell types by suppressing FGF signaling in Drosophila

Development. 2016 Nov 15;143(22):4261-4271. doi: 10.1242/dev.133322. Epub 2016 Oct 14.

Abstract

Extrinsic branching factors promote the elongation and migration of tubular organs. In the Drosophila tracheal system, Branchless (Drosophila FGF) stimulates the branching program by specifying tip cells that acquire motility and lead branch migration to a specific destination. Tip cells have two alternative cell fates: the terminal cell (TC), which produces long cytoplasmic extensions with intracellular lumen, and the fusion cell (FC), which mediates branch connections to form tubular networks. How Branchless controls this specification of cells with distinct shapes and behaviors is unknown. Here we report that this cell type diversification involves the modulation of FGF signaling by the zinc-finger protein Escargot (Esg), which is expressed in the FC and is essential for its specification. The dorsal branch begins elongation with a pair of tip cells with high FGF signaling. When the branch tip reaches its final destination, one of the tip cells becomes an FC and expresses Esg. FCs and TCs differ in their response to FGF: TCs are attracted by FGF, whereas FCs are repelled. Esg suppresses ERK signaling in FCs to control this differential migratory behavior.

Keywords: Cell migration; ERK signaling; FGF signaling; Tip cell; Tubulogenesis.

MeSH terms

  • Animals
  • Cell Differentiation / genetics*
  • Cell Fusion
  • Cell Lineage / genetics*
  • Cell Movement / genetics
  • Drosophila Proteins / physiology*
  • Drosophila melanogaster* / embryology
  • Drosophila melanogaster* / genetics
  • Embryo, Nonmammalian
  • Fibroblast Growth Factors / antagonists & inhibitors
  • Fibroblast Growth Factors / genetics
  • Fibroblast Growth Factors / metabolism*
  • Gene Expression Regulation, Developmental
  • MAP Kinase Signaling System / genetics
  • Morphogenesis / genetics*
  • Signal Transduction / genetics
  • Trachea / cytology
  • Trachea / embryology*
  • Trachea / metabolism

Substances

  • Drosophila Proteins
  • esg protein, Drosophila
  • Fibroblast Growth Factors