Adhesion is essential in biology. Intercellular interactions maintain the structural hierarchy of all multicellular organisms across all anatomical length scales. Cells transduce mechanical signals and respond by regulating adhesion, motility, and differentiation. Other adhesive interactions are central to immunity. Pathogenic microorganisms use adhesive interactions with cells in the first steps in infection. Determining the molecular mechanisms underlying these processes is central to understanding the fundamental basis of related diseases and to developing strategies to treating or preventing disease.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Israelachvili, J., Thin Film Studies Using Multiple-Beam Interferomtry. J. Coll. Int. Sci. 1973, 44, 259–272.
Israelachvili, J., Adhesion forces between surfaces in liquids and condensable vapours. Surface Science Reports 1992, 14, 110–159.
Israelachvili, J. N., Adams, G. E., Measurement of Forces between Two Mica Surfaces in Aqueous Electrolyte Solutions in the Range 0–100膗nm. J. Chem. Soc. Faraday Trans. I 1978, 75, 975–1001.
Born, M., Wolf, E., Principles of Optics. 6th ed.; Pergamon: Oxford, 1980.
Tolansky, S., Applications of multiple-beam interferometry. Nature 1951, 167, (4255), 815–6.
Leckband, D.; Israelachvili, J., Intermolecular forces in biology. Q Rev Biophys 2001, 34, (2), 105–267.
Tadmor, R.; Chen, N.; Israelachvili, J. N., Thickness and refractive index measurements using multiple beam interference fringes (FECO). J Colloid Interface Sci 2003, 264, (2), 548–53.
Tolansky, S.; Omar, M., Evaluation of small radii of curvature using the light-profile microscope. Nature 1952, 170, (4331), 758–9.
Israelachvili, J., McGuiggan, P., Adhesion and short-range forces between -surfaces: New apparatus for surface force measurements. J. Mater. Res. 1990, 5, 2223–2231.
Hunter, R., Foundations of Colloid Science. Oxford University Press: Oxford, 1989; Vol. 1.
Helm, C. A.; Israelachvili, J. N., Forces between phospholipid bilayers and relationship to membrane fusion. Methods Enzymol 1993, 220, 130–43.
Helm, C. A.; Israelachvili, J. N.; McGuiggan, P. M., Role of hydrophobic forces in bilayer adhesion and fusion. Biochemistry 1992, 31, (6), 1794–805.
Helm, C. A.; Israelachvili, J. N.; McGuiggan, P. M., Molecular mechanisms and forces involved in the adhesion and fusion of amphiphilic bilayers. Science 1989, 246, (4932), 919–22.
Leckband, D. E., Helm, C. A., Israelachvili, J., Role of Calcium in the Adhesion and Fusion of Bilayers. Biochemistry 1993, 32, 1127–1140.
Israelachvili, J., Intermolecular and Surface Forces. 2 ed.; Academic Press: New York, 1992.
Sivasankar, S., Gumbiner, BM, Leckband, D, Direct Measurements of Multiple Adhesive Alignments and Unbinding Trajectories between Cadherin Extracellular Domains. Biophys. J. 2001, 80, 1758–1768.
Johnson, K. L., Kendall, K., Roberts, A.D., Surface energy and the contact of elastic solids. Proc. R. Soc. Lond. A. 1971, 324, 301–313.
Balsera, M., Stepaniants, S., Izrailev, S., Oono, Y., Schulten, K., Reconstructing Potential Energy Functions from Simulated Force-Induced Unbinding Processes. Biophys. J. 1997, 73, 1281–1287.
Evans, E., Ritchie, K., Dynamic Strength of Molecular Adhesion Bonds. Biophys. J. 1997, 72, 1541–1555.
Dudko, O. K.; Hummer, G.; Szabo, A., Intrinsic rates and activation free energies from single-molecule pulling experiments. Phys Rev Lett 2006, 96, (10), 108101.
Hummer, G.; Szabo, A., Free energy reconstruction from nonequilibrium single-molecule pulling experiments. Proc Natl Acad Sci USA 2001, 98, (7), 3658–61.
Hummer, G.; Szabo, A., Kinetics from nonequilibrium single-molecule pulling experiments. Biophys J 2003, 85, (1), 5–15.
Hummer, G.; Szabo, A., Free energy surfaces from single-molecule force spectroscopy. Acc Chem Res 2005, 38, (7), 504–13.
Paramore, S.; Ayton, G. S.; Voth, G. A., Extending the fluctuation theorem to describe reaction coordinates. J Chem Phys 2007, 126, (5), 051102.
Li, F.; Leckband, D., Dynamic strength of molecularly bonded surfaces. J Chem Phys 2006, 125, (19), 194702.
Vijayendran, R., Hammer, D., and Leckband, D., Simulations of the adhesion between molecularly bonded surfaces in direct force measurements. J. Chem. Phys. 1998, 108, 1162–1169.
Yeung, C., Purves, T., Kloss, A. A., Kuhl, T. L., Sligar, S., Leckband, D., Cytochrome c Recognition of Immobilized, Orientational Variants of Cytochrome b5: Direct Force and Equilibrium Binding Measurements. Langmuir 1999, volume 15, 6829–6836.
Sivasankar, S., Brieher, W., Lavrik, N., Gumbiner, B., and Leckband, D., Direct Molecular Force Measurements of Multiple Adhesive Interactions Btween Cadherin Ectodomains. Proc. Natl. Acad. Sci. USA 1999, 96, 11820–11824.
Johnson, C. P.; Jensen, I. E.; Prakasam, A.; Vijayendran, R.; Leckband, D., Engineered protein A for the orientational control of immobilized proteins. Bioconjug Chem 2003, 14, (5), 974–8.
Perez, T. D.; Nelson, W. J.; Boxer, S. G.; Kam, L., E-cadherin tethered to micropatterned supported lipid bilayers as a model for cell adhesion. Langmuir 2005, 21, (25), 11963–8.
Leckband, D., Schmitt, F.-J., Israelachvili, J., Knoll, W., Direct force measurements of specific and nonspecific protein interactions. Biochemistry 1994, 33, 4611–4624.
Johnson, C. P.; Fragneto, G.; Konovalov, O.; Dubosclard, V.; Legrand, J. F.; Leckband, D. E., Structural studies of the neural-cell-adhesion molecule by X-ray and neutron reflectivity. Biochemistry 2005, 44, (2), 546–54.
Martel, L., Johnson, C., Boutet, S., Al- Kurdi, R., Konovalov, O., Robinson, I., Leckband, D., Legrand, J. F., X-Ray Reflectivity Investigation of the Structure of Cadherin Monolayers. J. Phys. IV France 2002, 12, 365–377.
Marra, J., Israelachvili, J., Direct Measurements of Forces between Phosphatidylcholine and Phosphatidylethanolamine bilayers in Aqueous Electrolyte Solutions. Biochemistry 1985, 24, 4608–4618.
Leckband, D., Müller, W., Schmitt, F.-J., and Ringsdorf, H., Molecular Mechanisms Determining the Strength of Receptor-Mediated Intermembrane Adhesion. Biophys. J. 1995, 69, 1162–1169.
Leckband, D. E., Kuhl, T. L., Wang, H. K., Müller, W., Ringsdorf, H., 4–4–20 Anti-Fluorescyl IgG Fab’ Recognition of Membrane Bound Hapten: Direct Evidence for the Role of Protein and Interfacial Structure. Biochemistry 1995, 34, 11467–11478.
Yeung, C., Leckband, D., Substrate Alterations of the Apparent Affinities of Immobilized Receptors. Langmuir 1998, Kloss, A. A., Lavrik, N., Yeung, C., Leckband, D., Effect of the microenvironment on the recognition of immobilized cytochromes by soluble redox proteins, Langmuir, 16, 3414–3421 submitted.
Yu, Z.-W., Calvert, T., Leckband, D., Molecular Forces between Membranes Displaying Neutral Glycosphingolipids: Evidence for Carbohydrate Attraction. Biochemistry 1997, 37, 1540–1550.
Prakasam, A.; Chien, Y. H.; Maruthamuthu, V.; Leckband, D. E., Calcium site mutations in cadherin: impact on adhesion and evidence of cooperativity. Biochemistry 2006, 45, (22), 6930–9.
Prakasam, A. K.; Maruthamuthu, V.; Leckband, D. E., Similarities between heterophilic and homophilic cadherin adhesion. Proc Natl Acad Sci U S A 2006, 103, (42), 15434–9.
Zhu, B.; Chappuis-Flament, S.; Wong, E.; Jensen, I. E.; Gumbiner, B. M.; Leckband, D., Functional analysis of the structural basis of homophilic cadherin adhesion. Biophys J 2003, 84, (6), 4033–42.
Johnson, C. P.; Fujimoto, I.; Perrin-Tricaud, C.; Rutishauser, U.; Leckband, D., Mechanism of homophilic adhesion by the neural cell adhesion molecule: use of multiple domains and flexibility. Proc Natl Acad Sci U S A 2004, 101, (18), 6963–8.
Johnson, C. P.; Fujimoto, I.; Rutishauser, U.; Leckband, D. E., Direct evidence that neural cell adhesion molecule (NCAM) polysialylation increases intermembrane repulsion and abrogates adhesion. J Biol Chem 2005, 280, (1), 137–45.
Bayas, M. V.; Kearney, A.; Avramovic, A.; van der Merwe, P. A.; Leckband, D. E., Impact of salt bridges on the equilibrium binding and adhesion of human CD2 and CD58. J Biol Chem 2007, 282, (8), 5589–96.
Zhu, B., Davies, E. A., van der Merwe, A., Leckband, D. , Direct measurements of heterotypic adhesion between the cell adhesion proteins CD2 and CD48. Biochemistry 2002, 42, 12163–12170.
Davis, S. J., vanderMerwe, P. A., The structure and ligand interactions of CD2: implications for T-cell function. Immunology Today 1996, 17, 177–187.
Davis, S. J., vanderMerwe, P. A., CD2-An Exception to the Immunoglobulin Superfamily Concept. Science 1996, 273, 1241–1242.
Jones, E. Y., Davis, S. J., Williams, A. F., Harlos, K., Stuart, D. I., Crystal structre at 2.8Å resolution of a soluble form of the cell adhesion molecule CD2. Natue 1992, 360, 232–239.
Bodian, D. L., Jones, E. Y., Stuart, D. I., Davis, S. J., Crystal structure of the extracellular region of the human cell adhesion molecule CD2 at 2.5 A resolution. Structure 1994, 2, 755–766.
Ikemizu, S.; Sparks, L. M.; van der Merwe, P. A.; Harlos, K.; Stuart, D. I.; Jones, E. Y.; Davis, S. J., Crystal structure of the CD2-binding domain of CD58 (lymphocyte function-associated antigen 3) at 1.8-A resolution. Proc Natl Acad Sci USA 1999, 96, (8), 4289–94.
Evans, E. J.; Castro, M. A.; O’Brien, R.; Kearney, A.; Walsh, H.; Sparks, L. M.; Tucknott, M. G.; Davies, E. A.; Carmo, A. M.; van der Merwe, P. A.; Stuart, D. I.; Jones, E. Y.; Ladbury, J. E.; Ikemizu, S.; Davis, S. J., Crystal structure and binding properties of the CD2 and CD244 (2B4)-binding protein, CD48. J Biol Chem 2006, 281, (39), 29309–20.
Wang, J. H.; Smolyar, A.; Tan, K.; Liu, J. H.; Kim, M.; Sun, Z. Y.; Wagner, G.; Reinherz, E. L., Structure of a heterophilic adhesion complex between the human CD2 and CD58 (LFA-3) counterreceptors. Cell 1999, 97, (6), 791–803.
McAlister, M. S. B., Mott, H. R., vanderMerwe, P. A., Campbell, I. D., Davis, S. J., and Driscoll, P. C., NMR Analysis of Interacting Soluble Forms of the Cell-Cell Recognition Molecules CD2 and CD48. Biochemistry 1996, 35, 5982–5991.
Davis, S. J.; Ikemizu, S.; Wild, M. K.; van der Merwe, P. A., CD2 and the nature of protein interactions mediating cell-cell recognition. Immunol Rev 1998, 163, 217–36.
Davis, S. J.; Ikemizu, S.; Evans, E. J.; Fugger, L.; Bakker, T. R.; van der Merwe, P. A., The nature of molecular recognition by T cells. Nat Immunol 2003, 4, (3), 217–24.
van der Merwe, P. A.; Davis, S. J., Molecular interactions mediating T cell antigen recognition. Annu Rev Immunol 2003, 21, 659–84.
Davis, S. J., Davies, E.A., Tucknott, M.G., Jones, E.Y., vanderMerwe, A., The role of charged residues mediating low affinity protein-protein recognition at the cell surface by CD2. Proc. Natl. Acad. Sci. USA 1998, 95, 5490–5494.
Arulanandam, A. R.; Withka, J. M.; Wyss, D. F.; Wagner, G.; Kister, A.; Pallai, P.; Recny, M. A.; Reinherz, E. L., The CD58 (LFA-3) binding site is a localized and highly charged surface area on the AGFCC’C” face of the human CD2 adhesion domain. Proc Natl Acad Sci USA 1993, 90, (24), 11613–7.
Bayas, M. V.; Schulten, K.; Leckband, D., Forced detachment of the CD2-CD58 complex. Biophys J 2003, 84, (4), 2223–33.
Israelev, S., Stepaniants, S., Balsera, M., Oono, Y., Schulten, Molecular Dynamics Study of Unbinding of the Avidin-Biotin Complex. Biophys. J. 1997, 72, 1568–1581.
Walsh, F., Doherty, P, Neural Cell Adhesion Molecules of the Immunoglobulin Superfamily. Ann. Rev. Cell. Biol. 1997, 13, 425–56.
Chothia, C., Jones, E. Y., The Molecular Structure of Cell Adhesion Molecules. Ann. Rev. Biochem. 1997, 66, 823–862.
Becker, J. W., Erickson, H. P., Hoffmann, S., Cunningham, B. A., Edelman, G. M., Topology of cell adhesion molecules. Proc. Natl. Acad. Sci. USA 1989, 86, 1088–1092.
Hall, A., Rutishauser, U., Visualization of neural cell adhesion molecule by electron microscopy. J. Cell Biol. 1987, 104, 1579–86.
Atkins, A. R., Chung, J., Songpon, D., Little, E., Edelman, G. M., Wright, P. E., Cunningham, B.A., Dyson, H.J., Solution structure of the third immunoglobulin domain of the neural cell adhesion molecule NCAM: can solution studies define the mechanism of homophilic binding? J. Mol. Biol. 2001, 311, 161–172.
Cunningham, B. A., Hemperly, J. J., Murray, B. A., Prediger, E. A., Brackenbury, R., Edelman, G. M., Neural cell adhesion molecule: structure, immunoglobulin-like domains, cell surface modulation, and alternative RNA splicing. Science 1987, 236, 799–806.
Jenson, P., Soroka, V., Thompson, N. K., Ralets, I., Berezin, V., Bock, E., Poulsen, F.M., Structure and interactions of NCAM modules 1 and 2-basic elements in neural cell adhesion. Nature Structural Biology 1999, 6, 486–493.
Kasper, C., Rasmussen, H., Kastrup, J. S., Ikemizu, S., Jones, R. Y., Berezin, V., Bock, E., Larsen, I. K., Structural basis of cell-cell adhesion by NCAM. Nature Struct. Biol. 2000, 7, 389–393.
Kiselyov, V., Berezin, V., Maar, T. E., Soroka, V., Edvardsen, K., Schousboe, A., Bock, E., The First Immunoglobulin-like Neural Cell Adhesion Molecule (NCAM) Domain is Involved in Double-reciprocal Interaction with the Second Immunoglobulin-like NCAM Domain and in Heparin Binding. J. Biol. Chem. 1997, 272, 10125–10134.
Ranheim, T. S., Edelman, G. M., Cunningham, B. A., Homophilic adhesion mediated by the neural cell adhesion molecule involves multiple immunoglobulin domains. Proc. Natl. Acad. Sci. 1996, 93, 4071–4075.
Rao, Y., Wu, X-F., Gariepy, J., Rutishauser, U., Siu, C.-H., Identification of a Peptide Sequence Involved in Homophilic Binding in the Neural Cell Adhesion Molecule NCAM. J. Cell Biol. 1992, 118, 937–949.
Soroka, V., Kiryushko, D., Novitskaya, V., Ronn, C. B., Poulson, F. M., Holm, A., Bock, E., Berezin, V., Induction of neuronal differentiation by a peptide corresponding to the homophilic binding site of the second Ig module of NCAM. J. Biol. Chem. 2002, 277, 24676–24683.
Soroka, V., Kolkova, K., Kastrup, J. S., Diederichs, K., Breed, J., Kiselyov, V. V.,Poulsen, F. M., Poulsen, F. M., Larsen, I. K., Welte, W., Berezin, V., Bock, E., Kasper, C., Structure and Interactions of NCAM Ig1–2–3 Suggest a Novel Zipper Mechanism for Homophilic Adhesion. Structure 2003, 10, 1291–1301.
Wieland, J. A., Gewirth, A., Leckband, D., Single Molecules Adhesion Measurements Reveal Two Homophilic NCAM Bonds with Mechanically Distinct Properties. J. Biol. Chem. 2005, 280, 41037–41046.
Christenson, H. K., Horn, R. G., Direct measurement of the force between solid surfaces in a polar liquid. Chem. Phys. Lett. 1983, 98, 45–48.
Christenson, H. K., Forces between solid surfaces in a binary mixture of non-polar liquids. Chem. Phys. Lett. 1985, 118, 455–458.
Christenson, H. K., Gruen, D. W. R., Horn, R. G., Israelachvili, J. N., Structuring in liquid alkanes between solid surfaces: force measurements and mean-field theory. J. Chem. Phys. 1987, 87, 1834–1841.
Heuberger, M., Zach, M., Spencer, N. D., Density fluctuations under confinement: when is a fluid not a fluid? Science 2001, 292, 905–908.
Horn, R. G., Israelachvili, J. N., Direct measurement of structural forces between two surfaces in a nonpolar liquid. J. Chem. Phys. 1981, 75, 1400–1411.
Horn, R. G., Israelachvili, J. N., Molecular organization and viscosity of a thin film of molten polymer between two surfaces as probed by force measurements. Macromolecules 1988, 21, 2836–2841.
Israelachvili, J. N., Pashley, R. M., Molecular layering of water at surfaces and origin of repulsive hydration forces. Nature 1983, 306, 249–250.
Israelachvili, J. N., Solvation forces and liquid structure, as probed by direct force measurements. Acc. Chem. Res. 1987, (20), 415–421.
Israelachvili, J. N., Kott, S. J., Liquid structuring at solid interfaces as probed by direct force measurements: the transition from simple to complex liquids and polymer fluids. J. Chem. Phys. 1988, 88, 7162–7166.
Kekicheff, P., Ducker, W. A., Ninham, B. W., Pilen, M. P., Multilayer adsorption of cytochrome c on mica around isoelectric pH. Langmuir 1990, 6, 1704–1708.
Petrov, P., Miklavcic, S., Olsson, U., Wennerstrom, H., A confined complex liquid. Oscillatory forces and lamellae formation from an L3 phase. Langmuir 1995, 11, 3928–3936.
Attard, P., Parker, J. L., Oscillatory solvation forces: A comparison of theory and experiment. J. Phys. Chem. 1992, 92, 5086–5093.
Frink, L. J., vanSwol, F., A common theoretical basis for surface forces apparatus, osmotic sress, and beam bending measurements of surface forces. Coll Surf A: Physichochem and Eng Aspects 2000, 162, 25–36.
Nelson, R. W., Bates, P. A., Rutishauser, U., Protein Determinants for Specific Polysialylation of the Neural Cell Adhesion Molecule. J. Biol. Chem. 1995, 270, 17171–17179.
El Maarouf, A.; Petridis, A. K.; Rutishauser, U., Use of polysialic acid in repair of the central nervous system. Proc Natl Acad Sci U S A 2006, 103, (45), 16989–94.
Franz, C. K.; Rutishauser, U.; Rafuse, V. F., Polysialylated neural cell adhesion molecule is necessary for selective targeting of regenerating motor neurons. J Neurosci 2005, 25, (8), 2081–91.
Rutishauser, U., Polysialic acid and the regulation of cell interactions. Curr. Op. Cell Biol. 1996, 8, 679–684.
Rutishauser, U., Grumet, M., et al, Neural cell adhesion molecule mediates initial interactions between spinal cord neurons and muscle cells in culture. J. Cell. Biol. 1983, 97, 145–152.
Rutishauser, U.; Landmesser, L., Polysialic acid in the vertebrate nervous system: a promoter of plasticity in cell-cell interactions. Trends Neurosci 1996, 19, (10), 422–7.
Tang, J.; Rutishauser, U.; Landmesser, L., Polysialic acid regulates growth cone behavior during sorting of motor axons in the plexus region. Neuron 1994, 13, (2), 405–14.
Rutishauser, U.; Landmesser, L., Polysialic acid on the surface of axons regulates patterns of normal and activity-dependent innervation. Trends Neurosci 1991, 14, (12), 528–32.
Landmesser, L.; Dahm, L.; Tang, J. C.; Rutishauser, U., Polysialic acid as a regulator of intramuscular nerve branching during embryonic development. Neuron 1990, 4, (5), 655–67.
Tanaka, F.; Otake, Y.; Nakagawa, T.; Kawano, Y.; Miyahara, R.; Li, M.; Yanagihara, K.; Inui, K.; Oyanagi, H.; Yamada, T.; Nakayama, J.; Fujimoto, I.; Ikenaka, K.; Wada, H., Prognostic significance of polysialic acid expression in resected non-small cell lung cancer. Cancer Res 2001, 61, (4), 1666–70.
Yang, P. Y., X., Rutishauser, U., Intercellular space is affected by polysialic acid content of NCAM. J. Cell Biol. 1992, 116, 1487–1496.
Acheson, A., Sunshine, J. L., Rutishauser, U., NCAM Polysialic Acid Can Regulate both Cell-Cell and Cell-Substrate Interactions. J. Cell Biol. 1991, 114, 143–153.
Yang, P., Major, D., Rutishauser, U., Role of Charge and Hydration in Effects of Polysialic Acid on Molecular Interactions on and between Cell Membranes. J. Biol. Chem. 1994, 269, 23039–23044.
Alberts, B., Bray, D., Lewis, J., Raff, M., Roberts, K., Watson, J. D., The Molecular Biology of the Cell. Garland: NY, 1983.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2008 Springer Science+Business Media, LLC
About this chapter
Cite this chapter
Leckband, D. (2008). Surface Force Apparatus Measurements of Molecular Forces in Biological Adhesion. In: Noy, A. (eds) Handbook of Molecular Force Spectroscopy. Springer, Boston, MA. https://doi.org/10.1007/978-0-387-49989-5_1
Download citation
DOI: https://doi.org/10.1007/978-0-387-49989-5_1
Publisher Name: Springer, Boston, MA
Print ISBN: 978-0-387-49987-1
Online ISBN: 978-0-387-49989-5
eBook Packages: Physics and AstronomyPhysics and Astronomy (R0)