The terminal cells of the Drosophila respiratory (tracheal) network contain seamless,
membrane bounded intracellular tubes through which air travels. The tube-containing
extensions of these cells are elaborated during chemotactic growth directed by
developmental cues in embryos and subsequently ramify in response to signals from
hypoxic tissues in larvae. Extensive membrane traffic occurs during growth, as the cell
rapidly and concomitantly elaborates two membrane domains of opposite characteristics.
The outer (basal) membrane migrates and grows with highly dynamic filopodial extensions,
while at the same time the inner tube of apical characteristics is constructed from as yet
unknown membrane sources.
We find that the membranes forming the intracellular tubules contain lipids and proteins
typical of apical plasma membranes in polarized epithelial cells. The Drosophila
synaptotagmin-like protein Bitesize (Btsz) and the activated form of its interaction partner
Moesin are also located at the growing luminal membrane. Our functional studies indicate
that the actin cytoskeleton, through its interaction with Btsz via Moesin directs apical
membrane morphogenesis to create and maintain distinct intracellular tubules.
Using real-time in vivo imaging we have analysed the assembly of the intracellular tube.
We find that ER and Golgi rapidly distribute into the developing cellular extensions prior to
the assembly of the membrane bounded tube within. Redistribution of secretory
machinery ahead of the growing tube seems to be a prerequisite for proper tube
extension.