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Contact enhancement of locomotion in spreading cell colonies

Nature Physics volume 13, pages 999–1005 (2017)Cite this article

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Abstract

The dispersal of cells from an initially constrained location is a crucial aspect of many physiological phenomena, ranging from morphogenesis to tumour spreading. In such processes, cell–cell interactions may deeply alter the motion of single cells, and in turn the collective dynamics. While contact phenomena like contact inhibition of locomotion are known to come into play at high densities, here we focus on the little explored case of non-cohesive cells at moderate densities. We fully characterize the spreading of micropatterned colonies of Dictyostelium discoideum cells from the complete set of individual trajectories. From data analysis and simulation of an elementary model, we demonstrate that contact interactions act to speed up the early population spreading by promoting individual cells to a state of higher persistence, which constitutes an as-yet unreported contact enhancement of locomotion. Our findings also suggest that the current modelling paradigm of memoryless active particles may need to be extended to account for the history-dependent internal state of motile cells.

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Figure 1: A highly controlled experimental set-up gives full access to colony spreading dynamics at both individual and population scales.
Figure 2: Density-dependent colony spreading.
Figure 3: Local interactions between cells lead to an increase in cell persistence.
Figure 4: Spreading colonies in individual-based models with various interaction rules.

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Acknowledgements

The authors are grateful to R. Fulcrand for his help in micro-fabrication, to V. Hakim for stimulating discussions and to C. Cottin-Bizonne for her comments on the manuscript. J.d’A. has been partially supported by the Fondation ARC pour la Recherche sur le Cancer and by the Programme d’Avenir Lyon-Saint Étienne. A.S. acknowledges funding through a PLS fellowship of the Gordon and Betty Moor foundation. J.d’A., C.R. and J.-P.R. belong to the CNRS consortium CellTiss and to the LIA ELyTLab.

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  1. Joseph d’Alessandro

    Present address: Institut Jacques Monod (IJM), CNRS UMR 7592 and Université Paris Diderot, 75013, Paris, France

Authors and Affiliations

  1. Université de Lyon, Université Claude Bernard Lyon 1, CNRS, Institut Lumière Matière, F-69622 Villeurbanne, France

    Joseph d’Alessandro, Christophe Anjard, François Detcheverry, Jean-Paul Rieu & Charlotte Rivière

  2. Department of Physics, Massachusetts Institute of Technology, Cambridge, Massachusetts, 02139, USA

    Alexandre P. Solon

  3. Center for Information Technology in Education, Tohoku University, Sendai 980-8578, Japan

    Yoshinori Hayakawa

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Contributions

J.d’A., J.-P.R. and C.R. designed experiments; J.d’A. performed experiments and analysed experimental data; J.d’A. and A.S. conceived the particle-based models; A.S. performed simulations and analysed simulation data; C.A. contributed to design of experiments in Supplementary Fig. 1 and provided AprA− cells; F.D. computed the analytical results on bimodal trajectories and helped with the fitting procedure; Y.H. assisted in the data analysis and interpretation; J.d’A. and A.S. wrote the manuscript; F.D., J.-P.R. and C.R. made substantial contributions to the manuscript; all authors discussed and interpreted the data, read and commented on the manuscript; J.-P.R. and C.R. supervised the project.

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Correspondence to Joseph d’Alessandro or Charlotte Rivière.

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d’Alessandro, J., Solon, A., Hayakawa, Y. et al. Contact enhancement of locomotion in spreading cell colonies. Nature Phys 13, 999–1005 (2017). https://doi.org/10.1038/nphys4180

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