Abstract
Epithelial morphogenesis requires cell movements and cell shape changes coordinated by modulation of the actin cytoskeleton. We identify a role for Echinoid (Ed), an immunoglobulin domain-containing cell-adhesion molecule, in the generation of a contractile actomyosin cable required for epithelial morphogenesis in both the Drosophila ovarian follicular epithelium and embryo. Analysis of ed mutant follicle cell clones indicates that the juxtaposition of wild-type and ed mutant cells is sufficient to trigger actomyosin cable formation. Moreover, in wild-type ovaries and embryos, specific epithelial domains lack detectable Ed, thus creating endogenous interfaces between cells with and without Ed; these interfaces display the same contractile characteristics as the ectopic Ed expression borders generated by ed mutant clones. In the ovary, such an interface lies between the two cell types of the dorsal appendage primordia. In the embryo, Ed is absent from the amnioserosa during dorsal closure, generating an Ed expression border with the lateral epidermis that coincides with the actomyosin cable present at this interface. In both cases, ed mutant epithelia exhibit loss of this contractile structure and subsequent defects in morphogenesis. We propose that local modulation of the cytoskeleton at Ed expression borders may represent a general mechanism for promoting epithelial morphogenesis.
Highlights
The morphogenesis of diverse epithelia during development derives from coordinated remodeling of cell shape and intercellular interactions that drives cell movements and reorganization (Pilot and Lecuit, 2005; Schöck and Perrimon, 2002b)
We demonstrate that Echinoid (Ed), a cell-adhesion molecule and adherens junction component (Bai et al, 2001; Islam et al, 2003; Spencer and Cagan, 2003; Wei et al, 2005) is required for the epithelial sheet movements that occur during appendage primordia morphogenesis and dorsal closure
Ed expression borders assemble a contractile actomyosin structure that mediates epithelial morphogenesis We demonstrate that the borders of ed mutant follicle cell clones display a reduced apical circumference and apical enrichment of Factin and p-MLC, suggesting that the juxtaposition of follicle cells with and without Ed is sufficient to trigger the assembly of an apical actomyosin cable at their interface
Summary
The morphogenesis of diverse epithelia during development derives from coordinated remodeling of cell shape and intercellular interactions that drives cell movements and reorganization (Pilot and Lecuit, 2005; Schöck and Perrimon, 2002b). These changes typically arise from modulation of the actin cytoskeleton. The follicle cell primordia that produce these appendages are specified in midoogenesis and flank the dorsal anterior midline of the epithelium. The signals that specify the fate and position of the appendage primordia are well understood (Berg, 2005; Nilson and Schüpbach, 1999; Roth, 2003), but the changes in cell shape and organization that
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