Article | Published:

Liposome adhesion generates traction stress

Nature Physics volume 10, pages 163169 (2014) | Download Citation

Abstract

Mechanical forces generated by cells modulate global shape changes required for essential life processes, such as polarization, division and spreading. Although the contribution of the cytoskeleton to cellular force generation is widely recognized, the role of the membrane is considered to be restricted to passively transmitting forces. Therefore, the mechanisms by which the membrane can directly contribute to cell tension are overlooked and poorly understood. To address this, we directly measure the stresses generated during liposome adhesion. We find that liposome spreading generates large traction stresses on compliant substrates. These stresses can be understood as the equilibration of internal, hydrostatic pressures generated by the enhanced membrane tension built up during adhesion. These results underscore the role of membranes in the generation of mechanical stresses on cellular length scales and that the modulation of hydrostatic pressure due to membrane tension and adhesion can be channelled to perform mechanical work on the environment.

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References

  1. 1.

    & Endosomal recycling controls plasma membrane area during mitosis. Proc. Natl Acad. Sci. USA 104, 7939–7944 (2007).

  2. 2.

    & Membrane expansion increases endocytosis rate during mitosis. J. Cell Biol. 144, 497–506 (1999).

  3. 3.

    et al. Membrane tension maintains cell polarity by confining signals to the leading edge during neutrophil migration. Cell 148, 175–188 (2012).

  4. 4.

    , , & Temporary increase in plasma membrane tension coordinates the activation of exocytosis and contraction during cell spreading. Proc. Natl Acad. Sci. USA 108, 14467–14472 (2011).

  5. 5.

    et al. Effects of substrate stiffness on cell morphology, cytoskeletal structure, and adhesion. Cell Motil. Cytoskel. 60, 24–34 (2005).

  6. 6.

    & United we stand: Integrating the actin cytoskeleton and cell-matrix adhesions in cellular mechanotransduction. J. Cell Sci. 125, 3051–3060 (2012).

  7. 7.

    et al. Membrane tension regulates motility by controlling lamellipodium organization. Proc. Natl Acad. Sci. USA 108, 11429–11434 (2011).

  8. 8.

    & Adhesion of membranes—a theoretical perspective. Langmuir 7, 1867–1873 (1991).

  9. 9.

    & Adhesion of vesicles and membranes. Mol. Cryst. Liq. Cryst. 202, 17–25 (1991).

  10. 10.

    & Adhesion of vesicles. Phys. Rev. A 42, 4768–4771 (1990).

  11. 11.

    , & Adhesion-induced domain formation by interplay of long-range repulsion and short-range attraction force: A model membrane study. Biophys. J. 73, 245–257 (1997).

  12. 12.

    , & Adhesion-induced reorganization of charged fluid membranes. Phys. Rev. E 58, 6340–6354 (1998).

  13. 13.

    et al. Spreading dynamics of biomimetic actin cortices. Biophys. J. 100, 1400–1409 (2011).

  14. 14.

    , , & Strong adhesion of giant vesicles on surfaces: Dynamics and permeability. Langmuir 16, 6809–6820 (2000).

  15. 15.

    & Adhesion induced by mobile binders: Dynamics. Proc. Natl Acad. Sci. USA 99, 7854–7859 (2002).

  16. 16.

    & Hidden dynamics of vesicle adhesion induced by specific stickers. Phys. Rev. Lett. 93, 228101 (2004).

  17. 17.

    & Modulation of vesicle adhesion and spreading kinetics by hyaluronan cushions. Biophys. J. 93, 3300–3313 (2007).

  18. 18.

    , , & Water permeability and mechanical strength of polyunsaturated lipid bilayers. Biophys. J. 79, 321–327 (2000).

  19. 19.

    , & Dynamics of transient pores in stretched vesicles. Proc. Natl Acad. Sci. USA 96, 10591–10596 (1999).

  20. 20.

    , , & Dynamic tension spectroscopy and strength of biomembranes. Biophys. J. 85, 2342–2350 (2003).

  21. 21.

    , , & High resolution traction force microscopy based on experimental and computational advances. Biophys. J. 94, 207–220 (2008).

  22. 22.

    , , & Adhesively-tensed cell membranes: Lysis kinetics and atomic force microscopy probing. Biophys. J. 85, 2746–2759 (2003).

  23. 23.

    & Static wetting on deformable substrates, from liquids to soft solids. Soft Matter 8, 7177–7184 (2012).

  24. 24.

    , , & Mechanics of surface area regulation in cells examined with confined lipid membranes. Proc. Natl Acad. Sci. USA 108, 9084–9088 (2011).

  25. 25.

    et al. Spotted vesicles, striped micelles and Janus assemblies induced by ligand binding. Nature Mater. 8, 843–849 (2009).

  26. 26.

    , , , & Topographical pattern dynamics in passive adhesion of cell membranes. Biophys. J. 87, 3547–3560 (2004).

  27. 27.

    , , , & Adhesion promotes phase separation in mixed-lipid membranes. Europhys. Lett. 84, 48003 (2008).

  28. 28.

    , , & Adhesion-induced phase behavior of two-component membranes and vesicles. Int. J. Mol. Sci. 14, 2203–2229 (2013).

  29. 29.

    , & Blebbing dynamics during endothelial cell spreading. Eur. J. Cell Biol. 90, 37–48 (2011).

  30. 30.

    , , , & Cell blebbing and membrane area homeostasis in spreading and retracting cells. Biophys. J. 99, 1726–1733 (2010).

  31. 31.

    , , & MARCKS regulates membrane ruffling and cell spreading. Curr. Biol. 7, 611–614 (1997).

  32. 32.

    , , & Membrane tension in swelling and shrinking molluscan neurons. J. Neurosci. 18, 6681–6692 (1998).

  33. 33.

    , & 4D traction force microscopy reveals asymmetric cortical forces in migrating Dictyostelium cells. Phys. Rev. Lett. 105, 248103 (2010).

  34. 34.

    , , & Quantifying cellular traction forces in three dimensions. Proc. Natl Acad. Sci. USA 106, 22108–22113 (2009).

  35. 35.

    , , & Micropatterning tractional forces in living cells. Cell Motil. Cytoskeleton 52, 97–106 (2002).

  36. 36.

    et al. Cellular response to substrate rigidity is governed by either stress or strain. Biophys. J. 104, 19–29 (2013).

  37. 37.

    , , & Tension is required but not sufficient for focal adhesion maturation without a stress fiber template. J. Cell Biol. 196, 363–374 (2012).

  38. 38.

    & Substrate stiffness and cell area predict cellular traction stresses in single cells and cells in contact. Cell. Mol. Bioeng. 3, 68–75 (2010).

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Acknowledgements

We acknowledge financial support from NSF Grant DMR-0844115 for postdoctoral fellowship support to M.P.M. as well as the ICAM Branches Cost Sharing Fund. M.G. acknowledges support from the Burroughs Wellcome CASI award, Packard Foundation, and University of Chicago MRSEC. M.P.M. and C.S. acknowledge support from the French Agence Nationale de la Recherche (ANR) Grant ANR 12BSV5001401, and the Fondation pour la Recherche Médicale Grant DEQ20120323737. We thank U. Schwarz (University of Heidelberg) for use of traction force algorithms.

Author information

Author notes

    • Pierre Nassoy
    • , Cécile Sykes
    •  & Margaret L. Gardel

    These authors contributed equally to this work

Affiliations

  1. Institute for Biophysical Dynamics, James Franck Institute, University of Chicago, Chicago, Illinois I60637, USA

    • Michael P. Murrell
    •  & Margaret L. Gardel
  2. Institut Curie, Centre de Recherche, Laboratoire Physico-Chimie, UMR168, Paris F-75248, France

    • Michael P. Murrell
    • , Jean-François Joanny
    • , Pierre Nassoy
    •  & Cécile Sykes
  3. Centre National de la Recherche Scientifique, UMR168, Paris F-75248, France

    • Michael P. Murrell
    • , Jean-François Joanny
    • , Pierre Nassoy
    •  & Cécile Sykes
  4. Université Paris 6, Paris F-75248, France

    • Michael P. Murrell
    • , Jean-François Joanny
    • , Pierre Nassoy
    •  & Cécile Sykes
  5. Laboratoire Jean Perrin, CNRS FRE 3231, and Laboratoire de Physique Théorique de la Matière Condensée, CNRS UMR 7600, Université Pierre et Marie Curie, 4 place Jussieu, Paris F-75005, France

    • Raphaël Voituriez
  6. Institut d’Optique, LP2N, UMR 5298, Talence F-33405, France

    • Pierre Nassoy
  7. The Department of Physics, University of Chicago, Chicago, Illinois I60637, USA

    • Margaret L. Gardel

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Contributions

M.P.M. performed experiments. M.L.G. developed analytical tools. R.V., J-F.J., P.N. and C.S. contributed theory and calculations. M.P.M., R.V., J-F.J., P.N., C.S. and M.L.G. wrote the paper.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Michael P. Murrell.

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DOI

https://doi.org/10.1038/nphys2855

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