Relating cell and tissue mechanics: Implications and applications (original) (raw)
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Tissue cohesion and the mechanics of cell rearrangement
Morphogenetic processes often involve the rapid rearrangement of cells held together by mutual adhesion. The dynamic nature of this adhesion endows tissues with liquid-like properties, such that large- scale shape changes appear as tissue flows. Generally, the resistance to flow (tissue viscosity) is expected to depend on the cohesion of a tissue (how strongly its cells adhere to each other), but the exact relationship between these parameters is not known. Here, we analyse the link between cohesion and viscosity to uncover basic mechanical principles of cell rearrangement. We show that for vertebrate and invertebrate tissues, viscosity varies in proportion to cohesion over a 200-fold range of values. We demonstrate that this proportionality is predicted by a cell-based model of tissue viscosity. To do so, we analyse cell adhesion in Xenopus embryonic tissues and determine a number of parameters, including tissue surface tension (as a measure of cohesion), cell contact fluctuation and cortical tension. In the tissues studied, the ratio of surface tension to viscosity, which has the dimension of a velocity, is 1.8 μm/min. This characteristic velocity reflects the rate of cell-cell boundary contraction during rearrangement, and sets a limit to rearrangement rates. Moreover, we propose that, in these tissues, cell movement is maximally efficient. Our approach to cell rearrangement mechanics links adhesion to the resistance of a tissue to plastic deformation, identifies the characteristic velocity of the process, and provides a basis for the comparison of tissues with mechanical properties that may vary by orders of magnitude.
Surface tension determines tissue shape and growth kinetics
2018
The collective self-organization of cells into three-dimensional structures can give rise to emergent physical properties such as fluid behavior. Here, we demonstrate that tissues growing on curved surfaces develop shapes with outer boundaries of constant mean curvature, similar to the energy minimizing forms of liquids wetting a surface. The amount of tissue formed depends on the shape of the substrate, with more tissue being deposited on highly concave surfaces, indicating a mechano-biological feedback mechanism. Inhibiting cell-contractility further revealed that active cellular forces are essential for generating sufficient surface stresses for the liquid-like behavior and growth of the tissue. This suggests that the mechanical signaling between cells and their physical environment, along with the continuous reorganization of cells and matrix is a key principle for the emergence of tissue shape.
Current Opinion in Cell Biology, 2018
Biological patterns emerge through specialization of genetically identical cells to take up distinct fates according to their position within the organism. How initial symmetry is broken to give rise to these patterns remains an intriguing open question. Several theories of patterning have been proposed, most prominently Turing's reaction-diffusion model of a slowly diffusing activator and a fast diffusing inhibitor generating periodic patterns. Although these reaction-diffusion systems can generate diverse patterns, it is becoming increasingly evident that cell shape and tension anisotropies, mediated via cell-cell and/or cell-matrix contacts, also facilitate symmetry breaking and subsequent self-organized tissue patterning. This review will highlight recent studies that implicate local changes in adhesion and/or tension as key drivers of cell rearrangements. We will also discuss recent studies on the role of cadherin and integrin adhesive receptors in mediating and responding to local tissue tension asymmetries to coordinate cell fate, position and behavior essential for tissue selforganization and maintenance.
Embryonic tissues as elasticoviscous liquids
Developmental Biology, 1977
Certain embryonic cell aggregates display both solid-like and liquid-like properties in organ culture. When centrifuged against solid substrata, these aggregates undergo sudden initial deformations followed by more gradual shape changes. Thus, they are either compoundviscoelastic solids (in which cells first stretch rapidly, then slowly) or elasticoviscous liquids (in which cells first quickly stretch, but then gradually slide by one another). To distinguish between these alternatives, we have examined cell shapes in centrifugally deformed chick liver aggregates. Light and electron micrographs show that initially stretched cells within flattening aggregates gradually reassume their original undisturbed shapes during prolonged centrifugation. Therefore, although the cells themselves may react to stretching forces like elastic solids, they slowly slip past one another within aggregates to relax stretching forces, endowing the aggregates with liquid properties. Slow cell slippage can account not only for temporary elastic solidity and viscous liquid flow in cell aggregates, but also for stress-free changes in the positions and configurations of tissues migrating within developing embryos. Regulation of cell slippage properties may shift the morphogenetic dependence of embryonic tissues in successive developmental stages from intracellular to intercellular force-generating mechanisms, or vice versa.
Collective Cell Migration in Embryogenesis Follows the Laws of Wetting
Collective cell migration is a fundamental process during embryogenesis and its initial occurrence, called epiboly, is an excellent in vivo model to study the physical processes involved in collective cell movements that are key to understanding organ formation, cancer invasion, and wound healing. In zebrafish, epiboly starts with a cluster of cells at one pole of the spherical embryo. These cells are actively spreading in a continuous movement toward its other pole until they fully cover the yolk. Inspired by the physics of wetting, we determine the contact angle between the cells and the yolk during epiboly. By choosing a wetting approach, the relevant scale for this investigation is the tissue level, which is in contrast to other recent work. Similar to the case of a liquid drop on a surface, one observes three interfaces that carry mechanical tension. Assuming that interfacial force balance holds during the quasi-static spreading process, we employ the physics of wetting to predict the temporal change of the contact angle. Although the experimental values vary dramatically, the model allows us to rescale all measured contact-angle dynamics onto a single master curve explaining the collective cell movement. Thus, we describe the fundamental and complex developmental mechanism at the onset of embryogenesis by only three main parameters: the offset tension strength, a, that gives the strength of interfacial tension compared to other force-generating mechanisms; the tension ratio, d, between the different interfaces; and the rate of tension variation, l, which determines the timescale of the whole process.
A fluid-to-solid jamming transition underlies vertebrate body axis elongation
Nature, 2018
Just as in clay molding or glass blowing, sculpting biological structures requires the constituent material to locally flow like a fluid while maintaining overall mechanical integrity like a solid. Disordered soft materials, such as foams, emulsions and colloidal suspensions, switch from fluidlike to solid-like behaviors at a jamming transition 1-4. Similarly, cell collectives have been shown to display glassy dynamics in 2D and 3D 5,6 and jamming in cultured epithelial monolayers 7,8 , behaviors recently predicted theoretically 9-11 and proposed to influence asthma pathobiology 8 and tumor progression 12. However, it is unknown if these seemingly universal behaviors occur in vivo and, specifically, if they play any functional role during embryonic morphogenesis. By combining direct in vivo measurements of tissue mechanics with analysis of cellular dynamics, we show that during vertebrate body axis elongation, posterior tissues undergo a jamming transition from a fluid-like behavior at the extending end, the mesodermal progenitor zone (MPZ), to a solid-like *
Fluidization of sheet-like tissues by active cell rearrangements
arXiv (Cornell University), 2018
We theoretically explore fluidization of epithelial tissues by active T1 neighbor exchanges. We show that the geometry of cell-cell junctions encodes important information about the local features of the energy landscape, which we support by an elastic theory of T1 transformations. Using a 3D vertex model, we study tissue response to in-plane shear and we obtain a scaling relation between the effective viscosity and the active-T1 rate, which agrees with the coarse-grained theory. The impact of cell rearrangements on tissue shape is illustrated by axial compression of an epithelial tube.