The Influence of Cell Mechanics, Cell-Cell Interactions, and Proliferation on Epithelial Packing

Farhadifar, Reza; Röper, Jens-Christian; Aigouy, Benoît; Eaton, Suzanne; Jülicher, Frank

doi:10.1016/j.cub.2007.11.049

Cited by 1,159 publications

(1,909 citation statements)

References 30 publications

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“…A quantitative description of the mechanical behaviour of groups of cells in biological tissues is critical for an understanding of many fundamental biological processes, including embryogenesis [1][2][3][4][5][6][7], wound healing [8,9], stem cell dynamics, regeneration [10,11] and tumourigenesis [12][13][14][15]. Previous work demonstrates that the macroscopic response of many tissues is viscoelastic [1], where the tissue behaves as an elastic solid over short timescales and a viscous fluid over long timescales.…”

Section: Introductionmentioning

confidence: 99%

Glassy dynamics in three-dimensional embryonic tissues

Schötz

Lanio

Talbot

et al. 2013

J. R. Soc. Interface.

128

137

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Many biological tissues are viscoelastic, behaving as elastic solids on short timescales and fluids on long timescales. This collective mechanical behaviour enables and helps to guide pattern formation and tissue layering. Here, we investigate the mechanical properties of three-dimensional tissue explants from zebrafish embryos by analysing individual cell tracks and macroscopic mechanical response. We find that the cell dynamics inside the tissue exhibit features of supercooled fluids, including subdiffusive trajectories and signatures of caging behaviour. We develop a minimal, three-parameter mechanical model for these dynamics, which we calibrate using only information about cell tracks. This model generates predictions about the macroscopic bulk response of the tissue (with no fit parameters) that are verified experimentally, providing a strong validation of the model. The best-fit model parameters indicate that although the tissue is fluid-like, it is close to a glass transition, suggesting that small changes to single-cell parameters could generate a significant change in the viscoelastic properties of the tissue. These results provide a robust framework for quantifying and modelling mechanically driven pattern formation in tissues.

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Section: Introductionmentioning

confidence: 99%

Glassy dynamics in three-dimensional embryonic tissues

Schötz

Lanio

Talbot

et al. 2013

J. R. Soc. Interface.

128

137

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“…This model results in continued movement while the existing vertex models approach an equilibrium state with decreasing E [16,18] because here, γ ij obeys a different time-evolution rule than that followed by r i . In mathematical terms, for b ¼ 0 (no noise)…”

mentioning

confidence: 99%

“…To describe the dynamics of the sheet, we use a vertex model that describes the forces in each cell and the possible rearrangement of the cells [16][17][18]. In this model, cohesive cells are represented by polygons.…”

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confidence: 99%

Cell Chirality Induces Collective Cell Migration in Epithelial Sheets

2015

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During early development, epithelial cells form a monolayer sheet and migrate in a uniform direction. Here, we address how this collective migration can occur without breaking the cell-to-cell attachments. Repeated contraction and expansion of the cell-to-cell interfaces enables the cells to rearrange their positions autonomously within the sheet. We show that when the interface tension is strengthened in a direction that is tilted from the body axis, cell rearrangements occur in such a way that unidirectional movement is induced. We use a vertex model to demonstrate that such anisotropic tension can generate the unidirectional motion of cell sheets. Our results suggest that cell chirality facilitates collective cell migration during tissue morphogenesis.

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“…The differential interfacial tension hypothesis (DITH) developed by Harris (20), Brodland (21), and Graner (22) relates tissue surface tension to the tension along individual cell interfaces. The DITH theories are appealing because they recognize that individual cells are not point objects; a cell's mechanical energy changes with cell shape and the cortical tension clearly plays a role in this energy balance.Recent work has emphasized that interfacial tensions arise from a balance of adhesion, cortical tension, and cortical elasticity (17,19,23,24). However, the exact nature of this interplay remains to be elucidated.…”

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confidence: 99%

Coaction of intercellular adhesion and cortical tension specifies tissue surface tension

Manning

Foty²,

Steinberg

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

365

349

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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.differential adhesion hypothesis | differential interfacial tension hypothesis | mathematical modeling | cell aggregate geometry | self-assembly I t is well established that many tissues behave like liquids on long timescales. Cell tracking in vivo and in vitro highlights (i) largescale flows, (ii) exchange of nearest neighbors in a cellular aggregate, and (iii) rounding-up and fusion of aggregates (1). Macroscopic rheological properties such as surface tension can be measured using a tissue surface tensiometer (TST) (1-8) or micropipette aspiration (9), and surface tension can be used to explain tissue self-organization in embryogenesis (8, 10-12) or cancer (13,14). In particular, cell sorting and tissue spreading can be explained in terms of tissue surface tensions that differ among cell types (1, 3-5, 8, 15, 16).A full understanding of tissue surface tension as a driving force for biological processes is important, and knowledge of its cellular origins would allow us to intelligently design drugs and treatments to alter tissue organization. Two opposing theories about the mesoscopic origin of tissue surface tension have coexisted over the last 30 years. One, the differential adhesion hypothesis (DAH), postulates that in analogy to ordinary fluids, tissue surface tension is proportional to the intensity of the adhesive energy between the constituent cells, which are treated as point objects. The DAH has proven successful in a variety of studies with cell lines (2-5, 15) , malignant (13, 14) and embryonic tissues (1,5,8,16) and is widely accepted (12...

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The Influence of Cell Mechanics, Cell-Cell Interactions, and Proliferation on Epithelial Packing

Cited by 1,159 publications

References 30 publications

Glassy dynamics in three-dimensional embryonic tissues

Glassy dynamics in three-dimensional embryonic tissues

Cell Chirality Induces Collective Cell Migration in Epithelial Sheets

Coaction of intercellular adhesion and cortical tension specifies tissue surface tension

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