Skip to main content
Log in

The influence of inhomogeneous adhesion on the detachment dynamics of adhering cells

  • Original Paper
  • Published:
European Biophysics Journal Aims and scope Submit manuscript

Abstract

The adhesion of cells to surfaces plays a crucial role in processes related to motility and tissue growth. Nonspecific interactions with a surface, e.g., by electrostatic or van der Waals forces, can complement specific molecular interactions and can themselves support strong adhesion. In order to understand the mechanism by which cells establish an adhesive interface in the absence of specific proteins, we have studied the detachment kinetics of monocytic cells from glass surfaces coated with poly-l-lysine. We exposed adhering cells to a shear flow and studied their deformation and detachment trajectories. Our experiments reveal that between 20 and 60 parallel membrane tethers form prior to detachment from the surface. We propose that the extraction of tethers is the consequence of an inhomogeneous adhesion interface and model the detachment mechanism as the dynamic extrusion of cooperatively loaded tethers. In our model, individual tethers detach by a peeling process in which a zone of a few nanometers is loaded by the externally applied force. Our findings suggest that the formation of an inhomogeneous non-specific adhesion interface between a cell and its substrate gives rise to more complex dynamics of detachment than previously discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Bell GI (1978) Models for the specific adhesion of cells to cells. Science 200(4342):618–627

    Article  PubMed  CAS  Google Scholar 

  • Bruinsma R, Behrisch A, Sackmann E (2000) Adhesive switching of membranes: experiment and theory. Phys Rev E 61(4):4253–4267

    Article  CAS  Google Scholar 

  • Cozens-Roberts C, Quinn JA, Lauffenburger DA (1990) Receptor-mediated cell attachment and detachment kinetics I. Experimental model studies with the radial-flow detachment assay radial-flow detachment assay. Biophys J 58:857–872

    Article  PubMed  CAS  Google Scholar 

  • Dai J, Sheetz MP (1995) Mechanical properties of neuronal growth cone membranes studied by tether formation with laser optical tweezers. Biophys J 68(3):988–996

    Article  PubMed  CAS  Google Scholar 

  • Décavé E, Garrivier D, Bréchet Y, Fourcade B, Bruckert F (2002) Shear flow-induced detachment kinetics of Dictyostelium discoideum cells from solid substrate. Biophys J 82(5):2383–2395

    Article  PubMed  Google Scholar 

  • Derényi I, Jülicher F, Prost J (2002) Formation and interaction of membrane tubes. Phys Rev Lett 88(23):23–26

    Article  Google Scholar 

  • Evans E (1998) Energy landscapes of biomolecular adhesion and receptor anchoring at interfaces explored with dynamic force spectroscopy. Faraday Discuss 111:1–16

    Article  PubMed  CAS  Google Scholar 

  • Evans E (2001) Probing the relation between force—lifetime—and chemistry in single molecular bonds. Annu Rev Biophys Biomol Struct 30:105–128

    Article  PubMed  CAS  Google Scholar 

  • Evans E, Ritchie K (1997) Dynamic strength of molecular adhesion bonds. Biophys J 72(4):1541–1555

    Article  PubMed  CAS  Google Scholar 

  • Evans E, Yeung A (1994) Hidden dynamics in rapid changes of bilayer shape. Chem Phys Lipids 73(1–2):39–56

    Article  CAS  Google Scholar 

  • Evans E, Heinrich V, Leung A, Kinoshita K (2005) Nano- to micro-scale dynamics of P-selectin detachment from leukocyte interfaces. I. Membrane separation from the cytoskeleton. Biophys J 88(3):2288–2298

    Article  PubMed  CAS  Google Scholar 

  • Garrivier D, Décavé E, Bréchet Y, Bruckert F, Fourcade B (2002) Peeling model for cell detachment. Eur Phys J E 8:79–97

    PubMed  CAS  Google Scholar 

  • Gergely C et al (2000) Unbinding process of adsorbed proteins under external stress studied by atomic force microscopy spectroscopy. Proc Natl Acad Sci 97(20):10802–10807

    Article  PubMed  CAS  Google Scholar 

  • Gergely C et al (2002) Multi-bead-and-spring model to interpret protein detachment studied by AFM force spectroscopy. Biophys J 83(2):706–722

    Article  PubMed  CAS  Google Scholar 

  • Goldman AJ, Cox RG, Brenner H (1967) Slow viscous motion of a sphere parallel to a plane wall-I Motion through a quiescent fluid. Chem Eng Sci 22(4):637–651

    Article  CAS  Google Scholar 

  • Hammer DA, Lauffenburger DA (1987) A dynamical model for receptor-mediated cell adhesion to surfaces. Biophys J 52(3):475–487

    Article  PubMed  CAS  Google Scholar 

  • Hammer DA, Tirrell M (1996) Biological adhesion at interfaces. Annu Rev Mater Sci 26:591–651

    Article  Google Scholar 

  • Hategan A, Law R, Kahn S, Discher DE (2003) Adhesively-tensed cell membranes: lysis kinetics and atomic force microscopy probing. Biophys J 85(4):2746–2759

    Article  PubMed  CAS  Google Scholar 

  • Hategan A, Sengupta K, Kahn S, Sackmann E, Discher ED (2004) Topographical pattern dynamics in passive adhesion of cell membranes. Biophys J 87(5):3547–3560

    Article  PubMed  CAS  Google Scholar 

  • Hochmuth RM, Shao JY, Dai J, Sheetz MP (1996) Deformation and flow of membrane into tethers extracted from neuronal growth cones. Biophys J 70(1):358–369

    Article  PubMed  CAS  Google Scholar 

  • Hogg R, Healy TW, Fuerstenau DW (1966) Mutual coagulation of colloidal dispersions. Trans Faraday Soc 62:1638–1651

    Article  CAS  Google Scholar 

  • Koster G, Cacciuto A, Derényi I, Frenkel D, Dogterom M (2005) Force barriers for membrane tube formation. Phys Rev Lett 94(6):16–19

    Article  Google Scholar 

  • Nardi J, Feder T, Bruinsma R, Sackmann E (1997) Electrostatic adhesion between fluid membranes: phase separation and blistering. Europhys Lett 37(5):371–376

    Article  CAS  Google Scholar 

  • Nardi J, Bruinsma R, Sackmann E (1998) Adhesion-induced reorganization of charged fluid membranes. Phys Rev E 58(5):6340–6354

    Article  CAS  Google Scholar 

  • Ofek I, Hasty DL, Sharon N (2003) Anti-adhesion therapy of bacterial diseases: prospects and problems. FEMS Immunol Med Microbiol 38(3):181–191

    Article  PubMed  CAS  Google Scholar 

  • Parsegian VA, Gingell D (1972) On the electrostatic interaction across a salt solution between two bodies bearing unequal charges. Biophys J 12(9):1192–1204

    Article  PubMed  CAS  Google Scholar 

  • Pierres A et al (2003) Cell membrane alignment along adhesive surfaces: contribution of active and passive cell processes. Biophys J 84(3):2058–2070

    Article  PubMed  CAS  Google Scholar 

  • Powers T, Huber G, Goldstein R (2002) Fluid-membrane tethers: minimal surfaces and elastic boundary layers. Phys Rev E 65(4):1–11

    Google Scholar 

  • Purday HFP (1949) Streamline flow. Constable & Co Ltd

  • Ramachandran V, Williams M, Yago T, Schmidtke WD, McEver RP (2004) Dynamic alterations of membrane tethers stabilize leukocyte rolling on P-selectin. Proc Natl Acad Sci USA 101(37):13519–13524

    Article  PubMed  CAS  Google Scholar 

  • Shao JY, Hochmuth RM (1996) Micropipette suction for measuring piconewton forces of adhesion and tether formation from neutrophil membranes. Biophys J 71(5):2892–2901

    Article  PubMed  CAS  Google Scholar 

  • Shao JY, Ting-Beall HP, Hochmuth RM (1998) Static and dynamic lengths of neutrophil microvilli. Proc Natl Acad Sci USA 95(12):6797–6802

    Article  PubMed  CAS  Google Scholar 

  • Simson R et al (1998) Membrane bending modulus and adhesion energy of wild-type and mutant cells of Dictyostelium lacking talin or cortexillins. Biophys J 74(1):514–522

    Article  PubMed  CAS  Google Scholar 

  • Sundd P et al (2012) ‘Slings’ enable neutrophil rolling at high shear. Nature 488(7411):399–403

    Article  PubMed  CAS  Google Scholar 

  • Ward MD, Dembo M, Hammer DA (1994) Kinetics of cell detachment: peeling of discrete receptor clusters. Biophys J 67(6):2522–2534

    Article  PubMed  CAS  Google Scholar 

  • Waugh RE, Hochmuth RM (1987) Mechanical equilibrium of thick, hollow, liquid membrane cylinders. Biophys J 52(3):391–400

    Article  PubMed  CAS  Google Scholar 

  • Wilson CJ, Clegg RE, Leavesley DI, Pearcy MJ (2005) Mediation of biomaterial-cell interactions by adsorbed proteins: a review. Tissue Eng 11(1–2):1–18

    Article  PubMed  CAS  Google Scholar 

  • Xu G, Shao JY (2005) Double tether extraction from human neutrophils and its comparison with CD4+ T-lymphocytes. Biophys J 88(1):661–669

    Article  PubMed  CAS  Google Scholar 

  • Zhelev DV, Needham D, Hochmuth RM (1994) Role of the membrane cortex in neutrophil deformation in small pipets. Biophys J 67(2):696–705

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This research was performed within the framework of CTMM, the Center for Translational Molecular Medicine (www.ctmm.nl), project CIRCULATING CELLS (grant 01C-102), and supported by the Dutch Heart Foundation. M.W.J.P. is an employee of Philips Research.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Menno W. J. Prins.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Irmscher, M., van Laarhoven, K.A., de Jong, A.M. et al. The influence of inhomogeneous adhesion on the detachment dynamics of adhering cells. Eur Biophys J 42, 419–426 (2013). https://doi.org/10.1007/s00249-013-0891-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00249-013-0891-3

Keywords

Navigation