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

Abstract

Epithelia likely predate the last common animal ancestor, yet the evolutionary origin and environmental 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, 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. We further find that extrusion activity increases during starvation, and that extruded cells may be recycled by efferocytosis. Together, our findings indicate that epithelial cell extrusion has physiological roles in sea anemones and that its key hallmarks are evolutionarily ancient, predating the last common ancestor of sea anemones, flies and vertebrates.