Tissue remodeling during maturation of the Drosophila wing

Abstract

The final step in morphogenesis of the adult fly is wing maturation, a process not well understood at the cellular level due to the impermeable and refractive nature of cuticle synthesized some 30 h prior to eclosion from the pupal case. Advances in GFP technology now make it possible to visualize cells using fluorescence after cuticle synthesis is complete. We find that, between eclosion and wing expansion, the epithelia within the folded wing begin to delaminate from the cuticle and that delamination is complete when the wing has fully expanded. After expansion, epithelial cells lose contact with each other, adherens junctions are disrupted, and nuclei become pycnotic. The cells then change shape, elongate, and migrate from the wing into the thorax. During wing maturation, the Timp gene product, tissue inhibitor of metalloproteinases, and probably other components of an extracellular matrix are expressed that bond the dorsal and ventral cuticular surfaces of the wing following migration of the cells. These steps are dissected using the batone and Timp genes and ectopic expression of alphaPS integrin, inhibitors of Armadillo/beta-catenin nuclear activity and baculovirus caspase inhibitor p35. We conclude that an epithelial-mesenchymal transition is responsible for epithelial delamination and dissolution.

The unfulfilled/DHR51 gene of Drosophila melanogaster modulates wing expansion and fertility

“…Two pathways participate in wing expansion; a neuroendocrine cascade (McNabb et al, 1997;Park et al, 2003;Dewey et al, 2004;Luan et al, 2006) and tissue remodeling of the wing itself (Kiger et al, 2007). Given the neural localization of unf transcripts, the three sets of peptidergic neurons that comprise the neuroendocrine cascade that regulates wing expansion behaviors are candidates that may be responsible for the wing expansion defects of unf mutants.…”

Bursicon Signaling Mutations Separate the Epithelial–Mesenchymal Transition From Programmed Cell Death DuringDrosophila melanogasterWing Maturation

“…Drosophila wing development is an example of such a system, where defects in both wing patterning (Crozatier et al 2004;O'Connor et al 2006;Baker 2007) and the cellular mechanisms that regulate pupal morphogenesis of the wing structure (Dominguez-Giménez et al 2007;Srivastava et al 2007; O' Keefe et al 2007) have provided insight into underlying conserved molecular mechanisms. Recent studies on the final stages of wing maturation following eclosion (Kiger et al 2001(Kiger et al , 2007Kimura et al 2004;Link et al 2007) have added regulation of the epithelial-mesenchymal transition (EMT) and programmed cell death to the developmental mechanisms that can be addressed through study of the wing.…”

“…Shortly after eclosion, pressurization of the hemolymph initiates expansion of the folded wing blade. During this process, the dorsal and ventral epithelial cell layers delaminate from the overlying cuticle, undergo an EMT, and exit the wing blade, accompanied by initiation of a cell death program (Kiger et al 2001(Kiger et al , 2007. The dorsal and ventral wing cuticles become tightly bonded through deposition of an extracellular matrix by the departing epithelial cells and, possibly, by dispersed hemocytes also found in the wing at this time (Kiger et al 2007).…”

“…Our previous work found Armadillo/b-catenin to be an important regulator of events associated with wing maturation (Kiger et al 2001(Kiger et al , 2007. Gal4-driven ectopic expression in the wing epithelia of a number of molecules that interfere with Armadillo/b-catenin nuclear function (Pygopus, Shaggy/GSK3, stabilized Armadillo) block epithelial delamination and EMT.…”

“…The wings expand, but wing epithelia are maintained within the wing blade and the wing surfaces fail to bond. Armadillo/b-catenin signaling is central to EMT in many systems (see Kiger et al 2007). We also found that the batone mutation blocks both wing expansion and delamination of epithelial cells from the wing cuticle.…”