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.
Embryonic morphogenesis requires the execution of complex mechanisms that regulate the local behaviour of groups of cells. The orchestration of such mechanisms has been mainly deciphered through the identification of conserved families of signalling pathways that spatially and temporally control cell behaviour. However, how this information is processed to control cell shape and cell dynamics is an open area of investigation. The framework that emerges from diverse disciplines such as cell biology, physics and developmental biology points to adhesion and cortical actin networks as regulators of cell surface mechanics. In this context, a range of developmental phenomena can be explained by the regulation of cell surface tension.
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We apologize to our colleagues whose work could unfortunately not be cited because of space limitations. This review is the result of stimulating discussions between the Lecuit and Lenne laboratories over the past two years. We wish to thank all of our biologist and physicist colleagues in Marseille and F. Graner (Grenoble) for their input to clarify several issues addressed here. Y. Azou, C. Bertet, M. Cavey, B. Hampoelz, L. LeGoff, M. Rauzi and P. Verant made comments on the manuscript. We thank D. Sweeton and E. Wieschaus for the image in Figure 4a, V. Morel for Figure 5a, and J. Gros for preparing Figures 4c and 4d. T.L. is supported by the National Centre for Scientific Research (CNRS), the Association pour la recherche contre le Cancer (ARC), the Fondation Schlumberger pour l'Education et la Recherche (FSER), the EMBO Young Investigator Programme, and an ANR-Blanc grant together with P-F.L. P-F.L. is supported by the CNRS, Région PACA, ANR and the European Community.
The authors declare no competing financial interests.
A diffusing substance that induces different cell fates through the formation of a concentration-dependent gradient from a localized source.
- Planar polarity
The structural asymmetry of cells in the plane of a tissue. It characterizes the direction of cell elongation, cell division, cell movement and differentiation.
The ability to undergo a persistent deformation.
- Tissue homeostasis
The property of biological tissues to remain structurally and functionally stable in a physiological environment.
The ability of intermixed, adhesive and mobile cell populations to separate into immiscible adjacent tissues.
- Surface tension
The free-energy change when the surface of a medium is increased by a unit area. Strictly speaking, the term 'interfacial tension' should be used instead of 'surface tension' when the liquid adjoins another liquid or a solid. For simplicity, we use the term 'surface tension' in this article.
- Tissue surface tension
The apparent surface tension of a tissue, caused by cohesive interactions (adhesion) between cells. Increasing adhesion in a tissue increases tissue surface tension.
- Intercellular surface tension
The apparent surface tension of two cells that are in contact, caused by the opposite effects of cortical tension and intercellular adhesion. In contrast to the case of tissue surface tension, increased adhesion lowers intercellular surface tension.
- Cortical tension
The apparent cell surface tension due to the contractile microfilaments of the cell cortex and their interaction with the membrane.
The tendency of cells with similar developmental origins to aggregate.
An iterative subdivision of the vertebrate hindbrain along the antero-posterior axis.
- Selector gene
A gene that specifies (selects) a developmental pathway, as opposed to a 'realisator' gene that executes downstream cellular responses (e.g. adhesion).
- Cell adhesion molecule
A transmembrane protein on the cell surface that binds to other cell adhesion molecules on the surface of another contacting cell or to the extracellular matrix.
- Homophilic association
Trans-association of similar cell adhesion molecules at contacting cell surfaces.
- Heterophilic association
Trans-association of different cell adhesion molecules at contacting cell surfaces.
- Nurse cells
Polyploid cells in the Drosophila melanogaster ovary that are connected by cytoplasmic bridges and feed the oocyte.
- Cell surface tension
The apparent surface tension of a cell.
The mechanical response properties of a material in response to a load. Elasticity refers to the ability to recover from a deformation. Viscosity describes a resistance to a flow due to molecular interactions.
- Adherens junction
Molecular complexes that are formed by cadherins and associated molecules stabilized by the actin cytoskeleton. They connect two contacting cells.
- Apical constriction
Reduction of the apparent apical surface area in an epithelial cell. Apical constriction drives tissue bending.
A process whereby cells exchange neighbours in a polarized fashion in the plane of a tissue during convergent extension movements.
- Convergent extension
Bilateral symmetrical movement of cells that converge towards a given axis, thereby contributing to the joint extension of the tissue. Convergent extension is driven by intercalation and polarized migration.
Region of the embryo (also called ventral plate) where the body of the embryo will develop. The rest of the cells in the blastoderm become part of a membrane (the serosa) that forms the yolk sac.
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Lecuit, T., Lenne, PF. Cell surface mechanics and the control of cell shape, tissue patterns and morphogenesis. Nat Rev Mol Cell Biol 8, 633–644 (2007). https://doi.org/10.1038/nrm2222
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