The Arp2/3 complex and WASp are required for apical trafficking of Delta into microvilli during cell fate specification of sensory organ precursors

Nat Cell Biol. 2009 Jul;11(7):815-24. doi: 10.1038/ncb1888. Epub 2009 Jun 21.

Abstract

Cell fate decisions mediated by the Notch signalling pathway require direct cell-cell contact between adjacent cells. In Drosophila melanogaster, an external sensory organ (ESO) develops from a single sensory organ precursor (SOP) and its fate specification is governed by differential Notch activation. Here we show that mutations in actin-related protein-3 (Arp3) compromise Notch signalling, leading to a fate transformation of the ESO. Our data reveal that during ESO fate specification, most endocytosed vesicles containing the ligand Delta traffic to a prominent apical actin-rich structure (ARS) formed in the SOP daughter cells. Using immunohistochemistry and transmission electron microscopy (TEM) analyses, we show that the ARS contains numerous microvilli on the apical surface of SOP progeny. In Arp2/3 and WASp mutants, the surface area of the ARS is substantially reduced and there are significantly fewer microvilli. More importantly, trafficking of Delta-positive vesicles from the basal area to the apical portion of the ARS is severely compromised. Our data indicate that WASp-dependent Arp2/3 actin polymerization is crucial for apical presentation of Delta, providing a mechanistic link between actin polymerization and Notch signalling.

MeSH terms

  • Actin-Related Protein 2-3 Complex / genetics
  • Actin-Related Protein 2-3 Complex / metabolism
  • Actin-Related Protein 2-3 Complex / physiology*
  • Animals
  • Biological Transport / genetics
  • Biological Transport / physiology
  • Blotting, Western
  • Cell Differentiation / genetics
  • Cell Differentiation / physiology
  • Drosophila melanogaster / embryology*
  • Drosophila melanogaster / genetics
  • Drosophila melanogaster / metabolism*
  • Drosophila melanogaster / ultrastructure
  • Endocytosis / genetics
  • Endocytosis / physiology
  • Gene Expression Regulation, Developmental
  • Immunohistochemistry
  • Intracellular Signaling Peptides and Proteins
  • Membrane Proteins / metabolism*
  • Microscopy, Electron, Transmission
  • Microscopy, Immunoelectron
  • Microvilli / metabolism*
  • Microvilli / ultrastructure
  • Sense Organs / embryology*
  • Sense Organs / metabolism
  • Sense Organs / ultrastructure
  • Wiskott-Aldrich Syndrome Protein / genetics
  • Wiskott-Aldrich Syndrome Protein / metabolism
  • Wiskott-Aldrich Syndrome Protein / physiology*

Substances

  • Actin-Related Protein 2-3 Complex
  • Intracellular Signaling Peptides and Proteins
  • Membrane Proteins
  • Wiskott-Aldrich Syndrome Protein
  • delta protein