Zona Pellucida Domain Proteins Remodel the Apical Compartment for Localized Cell Shape Changes

The zona pellucida domain (ZPD) defines a conserved family of membrane-anchored matrix proteins that are, as yet, poorly characterized with respect to their functions during development. Using genetic approaches in flies, we show here that a set of eight ZPD proteins is required for the localized reorganization of embryonic epidermal cells during morphogenesis. Despite varying degrees of sequence conservation, these ZPD proteins exert specific and nonredundant functions in the remodeling of epidermal cell shape. Each one accumulates in a restricted subregion of the apical compartment, where it organizes local interactions between the membrane and the extracellular matrix. In addition, ZPD proteins are required to sculpture the actin-rich cell extensions and maintain appropriate organization of the apical compartment. These results on ZPD proteins therefore reveal a functional subcompartmentalization of the apical membrane and its role in the polarized control of epithelial cell shape during development. [Display omitted] ► In Drosophila epidermis, shavenbaby controls ZPD gene expression ► Apical cell shape remodeling relies on the coordinated action of ZPD genes ► ZPD proteins define sub-regions in the apical extracellular matrix (aECM) ► ZPD products maintain localized apical membrane/aECM interactions.