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The cytoplasm of living cells behaves as a poroelastic material

Nature Materials volume 12, pages 253–261 (2013)Cite this article

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Abstract

The cytoplasm is the largest part of the cell by volume and hence its rheology sets the rate at which cellular shape changes can occur. Recent experimental evidence suggests that cytoplasmic rheology can be described by a poroelastic model, in which the cytoplasm is treated as a biphasic material consisting of a porous elastic solid meshwork (cytoskeleton, organelles, macromolecules) bathed in an interstitial fluid (cytosol). In this picture, the rate of cellular deformation is limited by the rate at which intracellular water can redistribute within the cytoplasm. However, direct supporting evidence for the model is lacking. Here we directly validate the poroelastic model to explain cellular rheology at short timescales using microindentation tests in conjunction with mechanical, chemical and genetic treatments. Our results show that water redistribution through the solid phase of the cytoplasm (cytoskeleton and macromolecular crowders) plays a fundamental role in setting cellular rheology at short timescales.

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Figure 1: Experimental set-up and functional form of cellular force–relaxation.
Figure 2: Poroelastic and elastic properties change in response to changes in cell volume.
Figure 3: Changes in cell volume change cytoplasmic pore size.
Figure 4: The F-actin cytoskeleton is the main biological determinant of cellular poroelastic properties.

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Acknowledgements

E.M. is in receipt of a Dorothy Hodgkin Postgraduate Award (DHPA) from the Engineering and Physical Sciences Research Council. L.M. thanks the MacArthur Foundation for support. G.T.C. is in receipt of a Royal Society University Research Fellowship. G.T.C., D.A.M. and A.J.T. are funded by Wellcome Trust grant (WT092825). M.F. was supported by a Human Frontier Science Program Young Investigator grant to G.T.C. The authors wish to acknowledge the UCL Comprehensive Biomedical Research Centre for generous funding of microscopy equipment. E.M. and G.T.C. thank R. Thorogate and C. Leung for technical help with the AFM set-up and Z. Wei for helpful discussions. We also gratefully acknowledge support of N. Ladommatos and W. Suen from Department of Mechanical Engineering at UCL.

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Authors and Affiliations

  1. London Centre for Nanotechnology, University College London, London WC1H 0AH, UK

    Emad Moeendarbary, Léo Valon, Marco Fritzsche, Andrew R. Harris & Guillaume T. Charras

  2. Department of Mechanical Engineering, University College London, London WC1E 7JE, UK

    Emad Moeendarbary

  3. Department of Physics, Ecole Normale Superieure, Paris 75005, France

    Léo Valon

  4. Department of Physics and Astronomy, University College London, London WC1E 6BT, UK

    Marco Fritzsche & Andrew R. Harris

  5. Molecular Immunology Unit, Institute of Child Health, University College London, London WC1N 1EH, UK

    Dale A. Moulding & Adrian J. Thrasher

  6. Department of Engineering Science, Institute of Biomedical Engineering, University of Oxford, Oxford OX1 3PJ, UK

    Eleanor Stride

  7. Department of Physics, School of Engineering and Applied Sciences, Harvard University, Cambridge, Massachusetts 02138, USA

    L. Mahadevan

  8. Department of Cell and Developmental Biology, University College London, London WC1E 6BT, UK

    Guillaume T. Charras

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Contributions

E.M., L.M. and G.T.C. designed the research; E.M. and L.V. performed the research with some contributions from M.F. and D.M.; E.M. analysed the data; E.M., L.V., D.A.M., A.J.T. and G.T.C. generated reagents; E.M., L.V., M.F., A.R.H., E.S. and L.M. contributed analytical tools; E.M., L.M. and G.T.C. wrote the paper.

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Correspondence to L. Mahadevan or Guillaume T. Charras.

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Moeendarbary, E., Valon, L., Fritzsche, M. et al. The cytoplasm of living cells behaves as a poroelastic material. Nature Mater 12, 253–261 (2013). https://doi.org/10.1038/nmat3517

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