Developmental analysis and squamous morphogenesis of the peripodial epithelium in Drosophila imaginal discs

Abstract

Imaginal discs of Drosophila provide an excellent system with which to study morphogenesis, pattern formation and cell proliferation in an epithelium. Discs are sac-like in structure and are composed of two epithelial layers: an upper peripodial epithelium and lower disc proper. Although development of the disc proper has been studied extensively in terms of cell proliferation, cell signaling mechanisms and pattern formation, little is known about these same processes in the peripodial epithelium. We address this topic by focusing on morphogenesis, compartmental organization, proliferation and cell lineage of the PE in wing, second thoracic leg (T2) and eye discs. We show that a subset of peripodial cells in different imaginal discs undergo a cuboidal-to-squamous cell shape change at distinct larval stages. We find that this shape change requires both Hedgehog and Decapentapelagic, but not Wingless, signaling. Additionally, squamous morphogenesis shifts the anteroposterior (AP) compartment boundary in the peripodial epithelium relative to the stationary AP boundary in the disc proper. Finally, by lineage tracing cells in the PE, we surprisingly find that peripodial cells are displaced into the disc proper during larval development and this movement leads to Ubx repression.

Dpp signaling promotes the cuboidal-to-columnar shape transition of Drosophila wing disc epithelia by regulating Rho1

“…brk-lacZ activity was not detectable in the cuboidal cells that underwent squamous morphogenesis (Fig. 1H), consistent with a role of Dpp signaling in this process (McClure and Schubiger, 2005). Furthermore, the prospective wing disc pouch cells that began to elongate no longer displayed detectable brk-lacZ activity (Fig.…”

“…During the late second and early third instar larval stage however, cells on one side of this epithelial sac flatten and become squamous. Cells on the other side elongate and become highly columnar and pseudostratified (Ursprung, 1972;McClure and Schubiger, 2005). The transition from cuboidal to columnar cell shape might allow the accommodation of the exponentially increasing number of cells within the columnar epithelium during larval development.…”

The Complex Containing Drosophila Myb and RB/E2F2 Regulates Cytokinesis in a Histone H2Av-Dependent Manner

“…The counter was blind to the genotype and, when applicable, the egg chamber stage and clone location. In wing discs, we examined squamous peripodial epithelial cells, which were identified by their location and morphology (32). On rare occasions, cells with three or four nuclei were observed-these were included in the binucleate category to simplify the analysis.…”

“…To test if Myb plays a role in cytokinesis in other tissues, we turned to the diploid larval wing disc. Thoracic imaginal discs, such as the wing disc, contain two layers of cells: the disc proper, composed mostly of columnar cells, and the peripodial epithelium, which contains flat squamous cells ideal for visualizing binucleate cells (32). Because Myb-null Drosophila flies survive to late larval stages, we were able to analyze Myb-null cells without inducing mitotic clones.…”

Dpp-induced Egfr signaling triggers postembryonic wing development in Drosophila

“…In the late second instar, pMAD is expressed in a pattern that reflects asymmetric Dpp activity ( Fig. S1) (28). At this stage, dpp is expressed in both the distal and proximal disc proper and peripodial epithelium ( Fig.…”