Apical contractility in growing epithelium supports robust maintenance of smooth curvatures against cell-division-induced mechanical disturbance

Abstract

In general, a rapidly growing epithelial sheet during tissue morphogenesis shows a smooth and continuous curvature on both inner cavity (apical) and basement membrane (basal) sides. For instance, epithelia of the neural tube and optic vesicle in the early embryo maintain continuous curvatures in their local domains, even during their rapid growth. However, given that cell divisions, which substantially perturb the local force balance, frequently and successively occur in an uncoordinated manner, it is not self-evident to explain how the tissue keeps a continuous curvature at large. In the majority of developing embryonic epithelia with smooth surfaces, their curvatures are apically concave, because of the presence of strong tangential contractile force on the apical side. In this numerical study, we demonstrate that tangential contractile forces on the apical surface play a critical role in the maintenance of smooth curvatures in the epithelium and reduce irregular undulations caused by uncoordinated generation of local pushing force. Using a reversible network reconnection (RNR) model, which we previously developed to make numerical analyses highly reproducible even under rapid tissue-growth conditions, we performed simulations for morphodynamics to examine the effect of apical contractile forces on the continuity of curvatures. Interestingly, the presence of apical contractile forces suppressed irregular undulations not only on the apical side but also on the basal surface. These results indicate that cellular contractile forces on the apical surface control not only the shape at a single cell level but also at a tissue level as a result of emergent mechanical coordination.