The role of peripodial epithelia in development and regeneration of Drosophila imaginal discs

The eyes, legs, and wings of Drosophila melanogaster develop from epithelial invaginations called imaginal discs. These sac-like structures are a crucial model for understanding the cellular and molecular basis for developmental pattern formation and growth control during animal development. Previous studies have considered discs to be columnar epithelial monolayers and have interpreted their development in a strictly two-dimensional context. Anatomically, however, it has long been known that discs are flattened sacs comprising distinct peripodial and columnar epithelial surfaces. An important question has therefore remained unaddressed: could peripodial cells play a functional role in imaginal disc development?; Here I describe novel evidence for interaction between peripodial and columnar cells during both development and regeneration. I demonstrate that peripodial cells signal to disc columnar cells via the Hedgehog signaling pathway during wound-induced regeneration. This interaction accounts for the ability of anterior cells to assume posterior identity during the regenerative process. Consistent with a peripodial role in normal disc development, I then present descriptive analyses of intact discs which show that peripodial cells produce specialized filopodia which traverse acellular space and terminate at or near the surface of disc columnar epithelia. Subsequent surgical and genetic ablation experiments document that peripodial epithelia are essential for proper growth and patterning of imaginal discs. Finally, further descriptive studies, gene misexpression experiments and mosaic analyses are used to implicate peripodial activity of the Notch and Decapentaplegic signaling pathways in the regulation of disc development. A significant departure from previous models, these findings recast imaginal disc development as a three-dimensional problem that involves direct interaction between peripodial and columnar epithelia.