Skip to main content
SpringerLink
Log in

Studying Molecular Interactions at the Single Bond Level with a Laminar Flow Chamber

  • Molecular Interactions
  • Published:
Cellular and Molecular Bioengineering Aims and scope Submit manuscript

Abstract

During the last decade, many investigators developed new methodologies allowing to study ligand–receptor interactions with unprecedented accuracy, up to the single bond level. Reported results include information on bond mechanical properties, association behavior of surface-attached molecules, and dissection of energy landscapes and reaction pathways. The purpose of the present review is to discuss the potential and limitations of laminar flow chambers operated at low shear rates. This includes a brief review of basic principles, practical tips, and problems associated with data interpretation. It is concluded that flow chambers are ideally suited to analyze weak interactions between a number of biomolecules, including the main families of adhesion receptors such as selectins, integrins, cadherins, and members of the immunoglobulin superfamily. The sensitivity of the method is limited by the quality of surfaces and efficiency of the studied ligand–receptor couple rather than the hardware. Analyzing interactions with a resolution of a piconewton and a few milliseconds shows that ligand–receptor complexes may experience a number of intermediate binding states, making it necessary to examine the definition of association and dissociation rates. Finally, it is emphasized that association rates measured on surface-bound molecules are highly dependent on parameters unrelated to binding molecules.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

FIGURE 1
FIGURE 2
FIGURE 3
FIGURE 4
FIGURE 5
FIGURE 6
FIGURE 7

Similar content being viewed by others

References

  1. Alon R., S. Chen, K. D. Puri, E. B. Finger, T. A. Springer The kinetics of L-selectin tethers and the mechanics of selectin-mediated rolling. J. Cell Biol. 138:1169–1180, 1997

    Article  Google Scholar 

  2. Alon R., D. A. Hammer, T. A. Springer. Lifetime of P-selectin-carbohydrate bond and its response to tensile force in hydrodynamic flow. Nature, 374:539–542, 1995

    Article  Google Scholar 

  3. Ansari A., J. Berendzen, S. F. Bowne, H. Frauenfelder, I. E. T. Iben, T. B. Sauke, E. Shyamsunder, R. T. Young. Protein states and proteinquakes. Proc. Natl. Acad. Sci. USA 82:5000–5004, 1985

    Article  Google Scholar 

  4. Bartolo D, I. Derényi, A. Ajdari Dynamic response of adhesion complexes : beyond the single path picture. Phys. Rev. E 65:051910, 2002

    Article  Google Scholar 

  5. Baumgartner W., P. Hinterdorfer, W. Ness, A. Raab, D. Vestweber, H. Schindler, D. Drenckhahn. Cadherin interaction probed by atomic force microscopy. Proc. Natl. Acad. Sci. USA 97:4005–4010, 2000

    Article  Google Scholar 

  6. Bayas M. V., A. Leung, D. Leckband. Lifetime measurements reveal kinetic differences between homophilic cadherin bonds. Biophys. J. 90:1385–1395, 2006

    Article  Google Scholar 

  7. Bell G. I. Models for the specific adhesion of cells to cells. Science 200:618–627, 1978

    Article  Google Scholar 

  8. Bongrand P. Specific and nonspecific interactions in cell biology. J. Dispersion Sci. Technol., 19:963–978, 1998

    Article  Google Scholar 

  9. Bongrand P. Ligand–receptor interactions. Rep. Prog. Phys. 62:921–968, 1999

    Article  Google Scholar 

  10. Bongrand P., C. Capo, A. M. Benoliel, R. Depieds. Evaluation of intercellular adhesion with a very simple technique. J. Immunological Methods 28:133–141, 1979

    Article  Google Scholar 

  11. Capo C., F. Garrouste, A. M. Benoliel, P. Bongrand, A. Ryter, G. I. Bell Concanavalin A-mediated thymocyte agglutination: a model for a quantitative study of cell adhesion. J. Cell Sci. 26:21–48, 1982

    Google Scholar 

  12. Cozens-Roberts C., D. A. Lauffenburger, J. A. Quinn. Receptor-mediated cell attachment and detachment kinetics. I. Probabilistic model and analysis. Biophys. J. 58:841–856, 1990

    Google Scholar 

  13. Cretel E., A. Pierres, A.-M. Benoliel, P. Bongrand. How cells feel their environment : a focus on early dynamic events. Cell. Mol. Bioeng. 1:5–14, 2008

    Article  Google Scholar 

  14. Curtis A. S. G. The measurement of cell adhesiveness by an absolute method. J. Embryol. Exp. Morph. 22:305–325, 1969

    MathSciNet  Google Scholar 

  15. Dembo M., D. C. Torney, K. Saxman, D. Hammer. The reaction-limited kinetics of membrane-to-surface adhesion and detachment. Proc. Roy. Soc. Lond. B 234:55–83, 1988

    Google Scholar 

  16. Dudko O. K., G. Hummer, A. Szabo. Intrinsic rates and activation free energies from single-molecule pulling experiments. Phys. Rev. Lett. 96:108101, 2006

    Article  Google Scholar 

  17. Dustin M. L., S. K. Bromley, M. M. Davis, C. Zhu. Identification of self through two-dimensional chemistry and synapses. Ann. Rev. Cell Dev. Biol. 17:133–157, 2001

    Article  Google Scholar 

  18. Evans E., A. Leung, D. Hammer, S. Simon. Chemically distinct transition states govern rapid dissociation of single L-selectin bonds under force. Proc. Natl. Acad. Sci. USA. 98:3784–3789, 2001

    Article  Google Scholar 

  19. Evans E., R. Merkel, K. Ritchie, S. Tha, A. Zilker. “Picoforce method to probe submicroscopic actions in biomembrane adhesion”. In: Studying Cell Adhesion, edited by P. Bongrand, P. M. Claesson, A. S. G. Curtis, New York: Springer Verlag. 1994, pp 125–139

    Google Scholar 

  20. Eyring H. The activated complex in chemical reactions. J. Chem. Phys. 3:107–115, 1935

    Article  Google Scholar 

  21. Florin E. L., V. T. Moy, H. E. Gaub. Adhesion forces between individual ligand-receptor pairs. Science 264:415–417, 1994

    Article  Google Scholar 

  22. Foote J., C. Milstein. Kinetic maturation of an immune response. Nature 352:530–532, 1991

    Article  Google Scholar 

  23. Giannone G., B. J. Dubin-Thaler, H. G. Döbereiner, N. Kieffer, A. R. Bresnick, M. P. Sheetz. Periodic lamellipodial contractions correlate with rearward actin waves. Cell 116:431–443, 2004

    Article  Google Scholar 

  24. Goldman A. J., R. G. Cox, H. Brenner. Slow viscous motion of a sphere parallel to a plane wall. II—Couette flow. Chem. Engn. Sci. 22:653–660, 1967

    Article  Google Scholar 

  25. Gourier, C., A. Jegou, J. Husson, and F. Pincet. A nanospring named erythrocyte. The biomembrane force probe. Cell. Mol. Bioeng. 2008. doi:10.1007/s12195-008-0030-x

  26. Greenberg A. W., D. K. Brunk, D. A. Hammer. Cell-free rolling mediated by L-selectin and sialyl Lewisx reveals the shear threshold effect. Biophys. J. 79:2391–1402, 2000

    Google Scholar 

  27. Harris A. K., P. Wild, D. Stopak. Silicone rubber substrata: a new wrinkle in the study of cell locomotion. Science 208:177–179, 1980

    Article  Google Scholar 

  28. Helm C. A., W. Knoll, J. N. Israelachvili. Measurement of ligand-receptor interactions. Proc. Natl. Acad. Sci. USA 88:8169–8173, 1991

    Article  Google Scholar 

  29. Hinterdorfer P., W. Baumgartner, H. J. Gruber, K. Schilcher, H. Schindler. Detection and localization of individual antibody-antigen recognition events by atomic force microscopy. Proc. Natl. Acad. Sci. USA 93:3477–3481, 1996

    Article  Google Scholar 

  30. Kaplanski G., C. Farnarier, O. Tissot, A. Pierres, A.-M. Benoliel, M.-C. Alessi, S. Kaplanski, P. Bongrand. Granulocyte–endothelium initial adhesion. Analysis of transient binding events mediated by E-selectin in a laminar shear flow. Biophys. J., 64:1922–1933, 1993

    Google Scholar 

  31. Lawrence M. B., T. A. Springer. Leukocytes roll on a selectin at physiologic flow rates: distinction from and prerequisite for adhesion through integrins. Cell, 65:859–873, 1991

    Article  Google Scholar 

  32. Litvinov R. I., J. S. Bennett, J. W. Weisel, H. Schuman. Multi-step fibrinogen binding to the integrin αIIbβ3 detected using force spectroscopy. Biophys. J. 89:2824–2834, 2005

    Article  Google Scholar 

  33. Marshall B., M. Long, J. W. Piper, T. Yago, R. P. McEver, C. Zhu. Direct observation of catch bonds involving cell-adhesionn molecules. Nature 423:190–193, 2003

    Article  Google Scholar 

  34. Marshall B. T., K. K. Sarangapani, J. Lou, R. P. McEver, C. Zhu. Force history dependence of receptor-ligand dissociation. Biophys. J. 88:1458–1466, 2005

    Article  Google Scholar 

  35. Masson-Gadais B., A. Pierres, A. M. Benoliel, P. Bongrand, J. C. Lissitzky. Integrin alpha and beta subunit contribution to the kinetic properties of alpha 2-beta 1 collagen receptors on human keratinocytes analyzed under hydrodynamic conditions. J. Cell Sci. 112:2335–2345, 1999

    Google Scholar 

  36. Matsui K., J. J. Boniface, P. Steffner, P. A. Reay, M. M. Davis. Kinetics of T-cell receptor binding to peptide/I-Ek complexes: correlation of the dissociation rate with T-cell responsiveness. Proc. Natl. Acad. Sci. USA 91:12862–12866, 1994

    Article  Google Scholar 

  37. Mege J. L., C. Capo, A. M. Benoliel, P. Bongrand. Determination of binding strength and kinetics of binding initiation. A model study made on the adhesive properties of P388D1 macrophage-like cells. Cell Biophys. 8:141–160, 1986

    Google Scholar 

  38. Merkel R., P. Nassoy, A. Leung, K. Ritchie, E. Evans. Energy landscapes of receptor-ligand bonds explored with dynamic force spectroscopy. Nature 397:50–53, 1999

    Article  Google Scholar 

  39. Miyata H., R. Yasuda, K. Kinosita Jr. Strength and lifetime of the bond between actin and skeletal muscle alpha-actinin studied with an optical trapping technique. Biochem. Biophys. Res. Com. 1290:83–88, 1996

    Google Scholar 

  40. Neuman K. C., A. Nagy. Single-molecule force spectroscopy: optical tweezers, magnetic tweezers and atomic force microscopy. Nat. Meth. 5:491–505, 2008.

    Article  Google Scholar 

  41. Panorchan P., M. S. Thompson, K. J. Davis, Y. Tseng, K. Konstantopoulos, D. Wirtz. Single-molecule analysis of cadherin-mediated cell–cell adhesion. J. Cell Sci. 119:66–74, 2006

    Article  Google Scholar 

  42. Paschall C. D., W. H. Guilford, M. B. Lawrence. Enhancement of L-selectin, but not P-selectin, bond formation frequency by convective flow. Biophys. J. 94:1034–1045, 2008

    Article  Google Scholar 

  43. Patel K. D., M. U. Nollert, R. P. McEver. P-selectin must extend a sufficient length from the plasma membrane to mediate rolling of neutrophils, J. Cell Biol., 131:1893–1902, 1995

    Article  Google Scholar 

  44. Perez, E., F. Li, D. Tareste, and F. Pincet. The Surface Force Apparatus to reveal the energetics of biomolecules assembly. Application to DNA bases pairing and SNARE fusion proteins folding. Cell. Mol. Bioeng. 2008. doi:10.1007/s12195-008-0025-7

  45. Perret E., A. M. Benoliel, P. Nassoy, A. Pierres, V. Delmas, J. P. Thiéry, P. Bongrand, H. Feracci. Fast dissociation kinetics of the recognition between individual E-cadherin fragments revealed by flow chamber analysis. EMBO J. 21:2537–2546, 2002

    Article  Google Scholar 

  46. Perret E., A. Leung, E. Evans. Trans-bonded pairs of E-cadherin exhibit a remarkable hierarchy of mechanical strengths. Proc. Natl. Acad. Sci. USA 101:16472–16477, 2004

    Article  Google Scholar 

  47. Pierres A., A. M. Benoliel, P. Bongrand. Measuring the lifetime of bonds made between surface-linked molecules. J. Biol. Chem. 270:26586–26592, 1995

    Article  Google Scholar 

  48. Pierres A., A. M. Benoliel, P. Bongrand. The dependence of the association-rate of surface-attached adhesion molecules CD2 and CD48 on separation distance. FEBS Lett. 403:239–244, 1997

    Article  Google Scholar 

  49. Pierres A., A. M. Benoliel, P. Bongrand, P. A. van der Merwe. Determination of the lifetime and force dependence of interactions of single bonds between surface-attached CD2 and CD48 adhesion molecules. Proc. Natl. Acad. Sci. USA 93:15114–15118, 1996

    Article  Google Scholar 

  50. Pierres A., A. M. Benoliel, D. Touchard, P. Bongrand. How cells tiptoe on adhesive surfaces before sticking. Biophys. J. 94:4114–4122, 2008

    Article  Google Scholar 

  51. Pierres A., A. M. Benoliel, C. Zhu, P. Bongrand. Diffusion of microspheres in shear flow near a wall: use to measure binding rates between attached molecules. Biophys. J. 81:25–42, 2001

    Google Scholar 

  52. Pierres A., H. Feracci, V. Delmas, A. M. Benoliel, J. P. Thiéry, P. Bongrand. Experimental study of the interaction range and association rate of surface-attached cadherin 11. Proc. Natl. Acad. Sci. USA 95:9256–9261, 1998

    Article  Google Scholar 

  53. Pierres A., A. Prakasam, D. Touchard, A. M. Benoliel, P. Bongrand, and D. Leckband. Dissecting subsecond cadherin bound states reveals an efficient way for cells to achieve ultrafast probing of their environment. FEBS Lett. 581:1841–1846, 2007

    Google Scholar 

  54. Pierres A, D. Touchard, A. M. Benoliel, P. Bongrand. Dissecting streptavidin-biotin interaction with a laminar flow chamber. Biophys. J. 82:3214–3223, 2002

    Google Scholar 

  55. Pincet F., J. Husson. The solution to the streptavidin-biotin paradox: the influence of history on the strength of single molecular bonds. Biophys. J. 89:4374–4381, 2005

    Article  Google Scholar 

  56. Puech, P.-H., and C. M. Franz. Atomic Force Microscopy: a versatile tool for studying cell morphology, adhesion and mechanics. Cell. Mol. Bioeng. in press, 2008

  57. Robert P., A. M. Benoliel, A. Pierres, P. Bongrand. What is the biological relevance of the specific bond properties revealed by single molecule studies? J. Mol. Recognition. 20:432–447, 2007

    Article  Google Scholar 

  58. Robert, P., L. Limozin, A. M. Benoliel, A. Pierres, and P. Bongrand, P. Glycocalyx regulation of cell adhesion. In: Principles of Cellular Engineering, edited by M. R. King, Amsterdam: Elsevier, Academic Press, 2006, pp. 143–169

  59. Robert, P., K. Sengupta, P. H. Puech, P. Bongrand, and L. Limozin. Tuning the formation and rupture of single ligand-receptor bonds by hyaluronan-induced repulsion. Biophys. J. 95:3999–4012, 2008

    Google Scholar 

  60. Sabri S., A. Pierres, A. M. Benoliel, P. Bongrand. Influence of surface charges on cell adhesion: difference between static and dynamic conditions. Biochem. Cell Biol. 73:411–420, 1995

    Article  Google Scholar 

  61. Schmidtke D. W., S. L. Diamond. Direct observation of membrane tethers formed during neutrophil attachment to platelets or P-selectin under physiological flow. J. Cell Biol. 149:719–729, 2000

    Article  Google Scholar 

  62. Seifert U. Rupture of multiple parallel molecular bonds under dynamic loading. Phys. Rev. Lett. 84:2750–2753, 2000

    Article  Google Scholar 

  63. Sivasankar S., W. Brieher, N. Lavrik, B. Gumbiner, D. Leckband. Direct molecular force measurements of multiple adhesive interactions between cadherin ectodomains. Proc. Natl. Acad. Sci. USA 96:11820–11824, 1999

    Article  Google Scholar 

  64. Smith M. J., E. L. Berg, M. B. Lawrence. A direct comparison of selectin-mediated transient, adhesive events using high temporal resolution. Biophys. J. 77:3371–3383, 1999

    Article  Google Scholar 

  65. Tempelman L. A., D. A. Hammer. Receptor-mediated binding of IgE-sensitized rat basophilic leukemia cells to antigen-coated substrates under hydrodynamic flow. Biophys. J. 66:1231–1283, 1994

    Google Scholar 

  66. Tha S. P., J. Shuster, H. L. Goldsmith. Interaction forces between red cells agglutinated by antibody. IV Time and force dependence of break-up. Biophys. J. 50:1117–1126, 1986

    Google Scholar 

  67. Thomas W. E., E. Trintchina, M. Forero, V. Vogel, E. Sokurenko. Bacterial adhesion to target cells enhanced by shear forces. Cell 109:913–923, 2002

    Article  Google Scholar 

  68. Thoumine, O., L. Bard, E. Saint-Michel, C. Dequidt, and D. Choquet. Optical tweezers and fluorescence recovery after photo-bleaching to measure molecular interactions at the cell surface. Cell. Mol. Bioeng. 2008. doi:10.1007/s12195-008-0034-6

  69. Vitte J., A. M. Benoliel, P. Eymeric, P. Bongrand, A. Pierres. Beta 1 integrin-mediated adhesion may be initiated by multiple incomplete bonds, thus accounting for the functional importance of receptor clustering. Biophys. J. 86:4059–4074, 2004

    Article  Google Scholar 

  70. Vitte J., A. Pierres, A. M. Benoliel, P. Bongrand. Direct quantification of the modulation of interaction between cell-or surface-bound LFA-1 and ICAM-1. J. Leukocyte Biol. 76:594–602, 2004

    Article  Google Scholar 

  71. Von Andrian U. H., S. R. Hasslen, R. D. Nelson, S. L. Erlandsen, E. C. Butcher. A central role for microvillous receptor presentation in leukocyte adhesion under flow. Cell 82:989–999, 1995

    Article  Google Scholar 

  72. Weiss L. The measurement of cell adhesion. Exp. Cell Res. Suppl 8:141–153, 1961

    Article  Google Scholar 

  73. Williams A. F. Out of equilibrium. Nature 352:473–474, 1991

    Article  Google Scholar 

  74. Zhu C., M. Long M, S. E. Chesla, P. Bongrand. Measuring receptor/ligand interaction at the single-bond level: experimental and interpretative issues. Ann. Biomed. Engineering 30: 305–314, 2002

    Article  Google Scholar 

  75. Zwanzig R. Diffusion in a rough potential. Proc. Natl. Acad. Sci. USA 85:2029–2030, 1988

    Article  MathSciNet  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Lab. Adhesion and Inflammation, INSERM UMR600, CNRS UMR6212, Aix-Marseille Universités, Parc Scientifique de Luminy, Case 937, 13288, Marseille Cedex 09, France

    Anne Pierres, Anne-Marie Benoliel & Pierre Bongrand

Authors
  1. Anne Pierres
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anne-Marie Benoliel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pierre Bongrand
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pierre Bongrand.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pierres, A., Benoliel, AM. & Bongrand, P. Studying Molecular Interactions at the Single Bond Level with a Laminar Flow Chamber. Cel. Mol. Bioeng. 1, 247–262 (2008). https://doi.org/10.1007/s12195-008-0031-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12195-008-0031-9

Keywords

Search

Navigation