Epithelial cell extrusion underlies starvation-induced cell loss in a sea anemone

Abstract

Abstract Epithelia likely predate the last common animal ancestor, yet the evolutionary origin and nutritional regulation of epithelial remodelling remain poorly understood. Here, we show that extensive, starvation-induced cell loss in the sea anemone Nematostella vectensis is associated with epidermal cell extrusion. This process involves formation of a rosette-like arrangement in which an apoptotic, extruding cell is surrounded by a phospho-ERK1/2-positive ring of cells, accompanied by basal translocation of adherens junction components. Combining chemical perturbations with computational quantification of extrusion and cell density, we show that apoptosis is necessary but not sufficient for rosette formation, and that ERK1/2 signalling limits epidermal extrusion density. Furthermore, we find increased extrusion activity during starvation, and potential nutrient recycling via phagocytosis of extruded cells. Together, our findings indicate that epithelial cell extrusion has physiological roles in sea anemones and that its key hallmarks are likely evolutionarily ancient, predating the last common cnidarian-bilaterian ancestor.