Opposing interactions between Drosophila Cut and the C/EBP encoded by Slow Border Cells direct apical constriction and epithelial invagination

Stage 10 of Drosophila oogenesis can be subdivided into stages 10A and 10B based on a change in the morphology of the centripetal follicle cells (FC) from a columnar to an apically constricted shape. This coordinated cell shape change drives epithelial cell sheet involution between the oocyte and nurse cell complex which patterns the operculum structure of the mature eggshell. We have shown previously that proper centripetal FC migration requires transient expression of the C/EBP encoded by slow border cells (slbo) at 10A, due in part to Notch activation followed by slbo autorepression (Levine et al., 2007). Here we show that decreased slbo expression in the centripetal FC coincides with increased expression of the transcription factor Cut, a Cut/Cux/CDP family member, at 10B. The 10A/10B temporal switch from Slbo to Cut expression is refined by both cross repression between Slbo and Cut, Slbo auto repression and Cut auto activation. High Cut levels are necessary and sufficient to direct polarized, supracellular accumulation of Actin, DE-cadherin and Armadillo associated with apical constriction of the centripetal FC. Separately, Slbo in the border cell rosette and Cut in the pole cells have antagonistic interactions to restrict Fas2 accumulation to the pole cells, which is important for proper border cell migration. The opposing effects of Cut and Slbo in these two tissues reflect the opposing interactions between their respective mammalian homologs CAAT Displacement Protein (CDP; now CUX1) and CAAT Enhancer Binding Protein (C/EBP) in tissue culture.