Staccato/Unc-13-4 controls secretory lysosome-mediated lumen fusion during epithelial tube anastomosis

Nat Cell Biol. 2016 Jul;18(7):727-39. doi: 10.1038/ncb3374. Epub 2016 Jun 20.

Abstract

A crucial yet ill-defined step during the development of tubular networks, such as the vasculature, is the formation of connections (anastomoses) between pre-existing lumenized tubes. By studying tracheal tube anastomosis in Drosophila melanogaster, we uncovered a key role of secretory lysosome-related organelle (LRO) trafficking in lumen fusion. We identified the conserved calcium-binding protein Unc-13-4/Staccato (Stac) and the GTPase Rab39 as critical regulators of this process. Stac and Rab39 accumulate on dynamic vesicles, which form exclusively in fusion tip cells, move in a dynein-dependent manner, and contain late-endosomal, lysosomal, and SNARE components characteristic of LROs. The GTPase Arl3 is necessary and sufficient for Stac LRO formation and promotes Stac-dependent intracellular fusion of juxtaposed apical plasma membranes, thereby forming a transcellular lumen. Concomitantly, calcium is released locally from ER exit sites and apical membrane-associated calcium increases. We propose that calcium-dependent focused activation of LRO exocytosis restricts lumen fusion to appropriate domains within tip cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Biological Transport / physiology
  • Calcium-Binding Proteins / metabolism
  • Carrier Proteins / metabolism*
  • Cell Membrane / metabolism*
  • Drosophila melanogaster
  • Epithelial Cells / cytology
  • Epithelium / metabolism
  • Exocytosis / physiology*
  • Lysosomes / metabolism*
  • Membrane Fusion / physiology*
  • Organelles / metabolism*
  • SNARE Proteins / metabolism*

Substances

  • Calcium-Binding Proteins
  • Carrier Proteins
  • SNARE Proteins
  • phorbol ester binding protein