Sequential pulses of apical epithelial secretion and endocytosis drive airway maturation in Drosophila.
The development of air-filled respiratory organs is crucial for survival at birth. We used a combination of live imaging and genetic analysis to dissect respiratory organ maturation in the embryonic Drosophila trachea. We found that tracheal tube maturation entails three precise epithelial transitions. Initially, a secretion burst deposits proteins into the lumen. Solid luminal material is then rapidly cleared from the tubes, and shortly thereafter liquid is removed. To elucidate the cellular mechanisms behind these transitions, we identified gas-filling-deficient mutants showing narrow or protein-clogged tubes. These mutations either disrupt endoplasmatic reticulum-to-Golgi vesicle transport or endocytosis. First, Sar1 is required for protein secretion, luminal matrix assembly, and diametric tube expansion. Subsequently, a sharp pulse of Rab5-dependent endocytic activity rapidly internalizes and clears luminal contents. The coordination of luminal matrix secretion and endocytosis may be a general mechanism in tubular organ morphogenesis and maturation.
Tsarouhas
Vasilios
V
Wenner-Gren Institute, Stockholm University, Department of Developmental Biology, Svante Arrheniusväg 16, Arrheniuslab E3, S-10691 Stockholm, Sweden.
Senti
Kirsten-André
KA
Jayaram
Satish Arcot
SA
Tiklová
Katarína
K
Hemphälä
Johanna
J
Adler
Jeremy
J
Samakovlis
Christos
C
D000818:Animals; D022181:COP-Coated Vesicles / Q000378:metabolism; D016764:Cell Polarity; D002470:Cell Survival; D029721:Drosophila Proteins / Q000378:metabolism; D004331:Drosophila melanogaster / Q000166:cytology* / Q000196:embryology* / Q000648:ultrastructure; D004625:Embryo, Nonmammalian / Q000166:cytology / Q000378:metabolism / Q000648:ultrastructure; D004705:Endocytosis; D004721:Endoplasmic Reticulum / Q000378:metabolism; D011992:Endosomes / Q000378:metabolism; D004847:Epithelial Cells / Q000166:cytology / Q000378:metabolism* / Q000648:ultrastructure; D004848:Epithelium / Q000378:metabolism; D006056:Golgi Apparatus / Q000378:metabolism; D008954:Models, Biological; D009154:Mutation / Q000235:genetics; D010641:Phenotype; D021122:Protein Subunits / Q000378:metabolism; D021381:Protein Transport; D014132:Trachea / Q000166:cytology / Q000196:embryology* / Q000648:ultrastructure; D015053:Zygote; D020696:rab5 GTP-Binding Proteins / Q000378:metabolism
D029721:Drosophila Proteins; D021122:Protein Subunits; D020696:rab5 GTP-Binding Proteins