Cell surface mechanics and the control of cell shape, tissue patterns and morphogenesis

Key Points Biological tissues exhibit two contradictory properties: they have a robust architecture that is required for their maintenance and resistance to stress, and they can be extensively remodelled during development or regeneration. Tissue morphogenesis requires the precise control of cell shape and cell dynamics. Cell shape is governed by cell mechanics, which explains how a set of intracellular and extracellular forces controls the cell structure. Cells are complex structures, the shape of which can be adequately explained using the concept of surface tension. Surface tension is an equilibrium property that does not explain the detailed course of events but does explain the organization of a cell and of groups of contacting cells. It is possible to draw analogies between the long-term (minutes to hours) behaviour of adhering cells and viscous fluids. Tissue surface tension controlled by intercellular adhesion describes this unique property that is manifested during cell sorting. The differential adhesion hypothesis relies on this physical property. Intercellular surface tension extends and adapts the concept of tissue surface tension at the cellular level to explain cell shape and the geometry of contacting cells, such as in an epithelium. Cell shape is mainly controlled by two opposing systems: intercellular adhesion that increases the surface of contacts, and cortical tension that reduces cell contacts. The organization and dynamics of cortical actin networks and their dynamic interaction with or tethering to the plasma membrane provide a mechanistic understanding of intercellular surface tension at the molecular level. It is possible to explain several tissue morphogenetic events during development through the spatial and temporal regulation of intercellular surface tension. For example, apical cell constriction controls tissue bending whereas cell intercalation drives tissue extension. In both cases, cortical tension is controlled by myosin-II actin filaments that regulate cell contacts and cell shape. Multicellular assemblies of cells often produce geometrically ordered patterns. The spatial regulation of intercellular adhesion controls cell shape and emergent cell patterns. Many signalling pathways have been shown to control cell shape and cell surface mechanics. Recent insights from diverse disciplines point to adhesion and cortical tension as regulators of cell shape and provide insights into how cell shape controls tissue geometry. Embryo