Spontaneous shear flow in confined cellular nematics

Abstract

In embryonic development or tumour evolution, cells often migrate collectively within confining tracks defined by their microenvironment1,2. In some of these situations, the displacements within a cell strand are antiparallel3, giving rise to shear flows. However, the mechanisms underlying these spontaneous flows remain poorly understood. Here, we show that an ensemble of spindle-shaped cells plated in a well-defined stripe spontaneously develops a shear flow whose characteristics depend on the width of the stripe. On wide stripes, the cells self-organize in a nematic phase with a director at a well-defined angle with the stripe’s direction, and develop a shear flow close to the stripe’s edges. However, on stripes narrower than a critical width, the cells perfectly align with the stripe’s direction and the net flow vanishes. A hydrodynamic active gel theory provides an understanding of these observations and identifies the transition between the non-flowing phase oriented along the stripe and the tilted phase exhibiting shear flow as a Fréedericksz transition driven by the activity of the cells. This physical theory is grounded in the active nature of the cells and based on symmetries and conservation laws, providing a generic mechanism to interpret in vivo antiparallel cell displacements.

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Fig. 1: Confined RPE1 cells align together with a tilt angle and develop a shear flow.
Fig. 2: Influence of the width of the confining stripe on the behaviour of the cells.
Fig. 3: Below a critical width, the cells orient along the stripe and do not flow on average.
Fig. 4: Comparison of the experimental results with the active gel theory.

Change history

  • 28 June 2019

    An amendment to this paper has been published and can be accessed via a link at the top of the paper.

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Acknowledgements

We thank the members of the Biology-inspired Physics at MesoScales (BiPMS) group and, in particular, F. Ascione, T. Sarkar and H. G. Yevick. We also thank L. Valon for suggesting the use of RPE1 cells. V.Y. gratefully acknowledges the CelTisPhyBio Labex and the EU PRESTIGE programme for financial support. G.S. is supported by the Francis Crick Institute, which receives its core funding from Cancer Research UK (FC001317), the UK Medical Research Council (FC001317) and the Wellcome Trust (FC001317). The BiPMS group and the Physical Approach of Biological Problems group are members of the CelTisPhyBio Labex. The BiPMS group is a member of the Institut Pierre-Gilles de Gennes.

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G.D. and P.S. designed the research. G.D. and V.Y. performed the experiments and C.B.-M. and G.S. developed the theory. P.S., J.P. and J.-F.J. supervised the research. All authors analysed the data and participated in writing the manuscript.

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Correspondence to J. Prost or P. Silberzan.

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Supplementary Information

Supplementary Figures 1–10, Supplementary Material, Supplementary References 1–30

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Supplementary Video 1

Shear flow of RPE1 cells in a confining stripe: RPE1 cells in a confining adhesive stripe reach a steady-state characterized by a tilt angle of the cell bodies relatively to the stripe direction and by a shear flow at the proximity of the edge. The width of the stripe is 1,000 µm and corresponds to the width of the image.

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Duclos, G., Blanch-Mercader, C., Yashunsky, V. et al. Spontaneous shear flow in confined cellular nematics. Nature Phys 14, 728–732 (2018). https://doi.org/10.1038/s41567-018-0099-7

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