Coaction of intercellular adhesion and cortical tension specifies tissue surface tension

TLDR

During animal morphogenesis, tissues behave like liquids with a characteristic surface tension arising from collective cell adhesion and cortical tension, yet no explicit model linking these mesoscopic properties to tissue surface tension has been established. The study aims to elucidate how tissue surface tension is generated by the interplay of cell–cell adhesion and cortical tension. We demonstrate that the ratio of adhesion to cortical tension governs tissue surface tension, a minimal model that fits experimental data predicts aggregate cell shapes, and reveals a crossover from adhesion‑dominated to cortical‑tension‑dominated behavior.

Abstract

In the course of animal morphogenesis, large-scale cell movements occur, which involve the rearrangement, mutual spreading, and compartmentalization of cell populations in specific configurations. Morphogenetic cell rearrangements such as cell sorting and mutual tissue spreading have been compared with the behaviors of immiscible liquids, which they closely resemble. Based on this similarity, it has been proposed that tissues behave as liquids and possess a characteristic surface tension, which arises as a collective, macroscopic property of groups of mobile, cohering cells. But how are tissue surface tensions generated? Different theories have been proposed to explain how mesoscopic cell properties such as cell-cell adhesion and contractility of cell interfaces may underlie tissue surface tensions. Although recent work suggests that both may be contributors, an explicit model for the dependence of tissue surface tension on these mesoscopic parameters has been missing. Here we show explicitly that the ratio of adhesion to cortical tension determines tissue surface tension. Our minimal model successfully explains the available experimental data and makes predictions, based on the feedback between mechanical energy and geometry, about the shapes of aggregate surface cells, which we verify experimentally. This model indicates that there is a crossover from adhesion dominated to cortical-tension dominated behavior as a function of the ratio between these two quantities.