Terminal Web and Associated Proteins Mediate Signaling to Promote Nematode Single-Cell Tubulogenesis

Abstract

Single-celled tubules represent one of the most difficult structures to form during development, requiring extension of a narrow cytoplasm surrounding a lumen exerting osmotic pressure that can burst the luminal membrane. Genetic studies on the excretory canal cell of C. elegans have revealed many proteins that regulate the cytoskeleton, vesicular transport, and physiology of the narrow canals. Here, we show that βH-spectrin SMA-1 regulates the placement of intermediate filament proteins IFA-4 and EXC-2/IFC-2 to form a terminal web around the lumen, and that the terminal web EXC-2 in turn retains a highly conserved protein (EXC-9/CRIP1) that regulates apical endosomal trafficking. EXC-1/IRG, the binding partner of EXC-9, is also localized to the apical membrane and affects apical actin placement and RAB-8-mediated vesicular transport. The results suggest that an intermediate filament protein acts in a novel signal transduction pathway to direct the traffic of vesicular cargo to locations of lengthening apical surface during single-celled tubule development.