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 largescale 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.
A new version of axisymmetric drop shape analysis (ADSA) called ADSA-NA (ADSA-no apex) was developed for measuring interfacial properties for drop configurations without an apex. ADSA-NA facilitates contact angle measurements on drops with a capillary protruding into the drop. Thus a much simpler experimental setup, not involving formation of a complete drop from below through a hole in the test surface, may be used. The contact angles of long-chained alkanes on a commercial fluoropolymer, Teflon AF 1600, were measured using the new method. A new numerical scheme was incorporated into the image processing to improve the location of the contact points of the liquid meniscus with the solid substrate to subpixel resolution. The images acquired in the experiments were also analyzed by a different drop shape technique called theoretical image fitting analysis-axisymmetric interfaces (TIFA-AI). The results were compared with literature values obtained by means of the standard ADSA for sessile drops with the apex. Comparison of the results from ADSA-NA with those from TIFA-AI and ADSA reveals that, with different numerical strategies and experimental setups, contact angles can be measured with an accuracy of less than 0.2 degrees. Contact angles and surface tensions measured from drops with no apex, i.e., by means of ADSA-NA and TIFA-AI, were considerably less scattered than those from complete drops with apex. ADSA-NA was also used to explore sources of improvement in contact angle resolution. It was found that using an accurate value of surface tension as an input enhances the accuracy of contact angle measurements.
Epithelia are planar tissues that undergo major morphogenetic movements during development. These movements must work in the context of the mechanical properties of epithelia. Surprisingly little is known about these mechanical properties at the time and length scales of morphogenetic processes. We show that at a time scale of hours, Xenopus gastrula ectodermal epithelium mimics an elastic solid when stretched isometrically; strikingly, its area increases twofold in the embryo by such pseudoelastic expansion. At the same time, the basal side of the epithelium behaves like a liquid and exhibits tissue surface tension that minimizes its exposed area. We measure epithelial stiffness (∼1 mN/m), surface tension (∼0.6 mJ/m 2 ), and epithelium-mesenchyme interfacial tensions and relate these to the folding of isolated epithelia and to the extent of epithelial spreading on various tissues. We propose that pseudoelasticity and tissue surface tension are main determinants of epithelial behavior at the scale of morphogenetic processes.
SummaryAdhesion differences between cell populations are in principle a source of strong morphogenetic forces promoting cell sorting, boundary formation and tissue positioning, and cadherins are main mediators of cell adhesion. However, a direct link between cadherin expression, differential adhesion and morphogenesis has not yet been determined for a specific process in vivo. To identify such a connection, we modulated the expression of C-cadherin in the Xenopus laevis gastrula, and combined this with direct measurements of cell adhesion-related parameters. Our results show that gastrulation is surprisingly tolerant of overall changes in adhesion. Also, as expected, experimentally generated, cadherin-based adhesion differences promote cell sorting in vitro. Importantly, however, such differences do not lead to the sorting of cells in the embryo, showing that differential adhesion is not sufficient to drive morphogenesis in this system. Compensatory recruitment of cadherin protein to contacts between cadherin-deprived and -overexpressing cells could contribute to the prevention of sorting in vivo.
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