Cell-Cycle-Coupled Oscillations in Apical Polarity and Intercellular Contact Maintain Order in Embryonic Epithelia

Abstract

Throughout animals, embryonic cells must ultimately organize into polarized epithelial layers that provide the structural basis for gastrulation or subsequent developmental events [1]. Precisely how this primary epithelium maintains continuous integrity during rapid and repeated cell divisions has never been directly addressed, particularly in cases where early cleavages are driven in synchrony. Representing the early-branching non-bilaterian phylum Cnidaria, embryos of the sea anemone Nematostella vectensis undergo rapid synchronous cell divisions and ultimately give rise to a diploblastic epithelial body plan after gastrulation [2, 3]. Here, using live imaging of apical polarity proteins in Nematostella embryos, we demonstrate that cell polarity is established by the four-cell stage and then reiteratively lost during subsequent mitoses, correlating with transient adhesion disengagement and dramatic deformations of embryonic morphology. Intriguingly, the re-establishment of polarity and adhesion during each interphase is associated with a process of whole-embryo compaction analogous to that observed in mammals [4-7]. Because similar protein dynamics are observed in dividing epithelial cells in Drosophila melanogaster, we propose that cell-cycle-coupled oscillations in apical polarity may be conserved throughout Metazoa.

Keywords: Cnidarian; Moesin; apical polarity; cell cycle; compaction; embryonic epithelium; evolution; oscillations.