We all fancy a new look from time to time, but during their development many organisms can take this one step further and undergo momentous changes in shape — a phenomenon that is exemplified by insect metamorphosis. In their study in Developmental Cell, Martín-Blanco and colleagues have shed new light on some of the basic steps that underlie these processes.

In Drosophila melanogaster, the exoskeleton of the adult (or imago) develops from epithelial structures that grow inside the larval stages of the fly. These structures are known as imaginal discs and are attached to the larval epithelium by a thin stalk of cells. They contain columnar cells, which form the imaginal epithelium, and squamous cells, which make up the periodial epithelium and stalk (PS). During development, the imaginal discs move to the outside of the larval epidermis in a process known as disc eversion.

Previously, changes in cell shape were thought to be sufficient for eversion — causing the disc to move through the widened disc stalk to the outside of the larval epidermis. But now, Martín-Blanco and colleagues present a new model for imaginal disc eversion that is based on their in vivo observations of imaginal morphogenesis and their detailed study of histological sections.

They found that, initially, a positional change occurs such that the PS cells of the discs become apposed to the larval epidermis. The PS cells then undergo a pseudo-epithelial–mesenchymal transition (PEMT). During PEMT, they lose their basal membrane, and proteins from the zonula adherens and septate junctions are redistributed from the cell membrane to the cytoskeleton — thereby disrupting cell adhesion. Marked cytoskeletal reorganization occurs and the cells become motile and invade the larval epithelium. The loss of adhesion among these invading cells generates perforations in the epithelium, which coalesce with each other and the disc stalk to produce a single hole. The continued intercalation of PS cells at the edges of the hole further widens it, which allows the extrusion of the imaginal disc and leaves a stripe of PS cells surrounding the disc. These cells then make up the leading front of the disc and guide its expansion and migration across the larval epithelium.

The Jun N-terminal kinase (JNK) signalling pathway — which includes the proteins Hemipterous (the JNK-kinase homologue), Basket (the JNK homologue) and Puckered (a phosphatase that inactivates Basket) in D. melanogaster — was found to have a significant role in driving many aspects of disc eversion.

Together, these findings have produced a model for epithelial perforation that might well provide insight into analogous epithelial-invasion processes that occur in the development of other organisms.