Surface Force Apparatus Measurements of Molecular Forces in Biological Adhesion

  • Deborah Leckband

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.


Neural Cell Adhesion Molecule Adhesion Energy Molecular Force Polysialic Acid Steer Molecular Dynamic 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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  1. 1.
    Israelachvili, J., Thin Film Studies Using Multiple-Beam Interferomtry. J. Coll. Int. Sci. 1973, 44, 259–272.CrossRefGoogle Scholar
  2. 2.
    Israelachvili, J., Adhesion forces between surfaces in liquids and condensable vapours. Surface Science Reports 1992, 14, 110–159.CrossRefADSGoogle Scholar
  3. 3.
    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.CrossRefGoogle Scholar
  4. 4.
    Born, M., Wolf, E., Principles of Optics. 6th ed.; Pergamon: Oxford, 1980.Google Scholar
  5. 5.
    Tolansky, S., Applications of multiple-beam interferometry. Nature 1951, 167, (4255), 815–6.CrossRefADSGoogle Scholar
  6. 6.
    Leckband, D.; Israelachvili, J., Intermolecular forces in biology. Q Rev Biophys 2001, 34, (2), 105–267.CrossRefGoogle Scholar
  7. 7.
    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.CrossRefGoogle Scholar
  8. 8.
    Tolansky, S.; Omar, M., Evaluation of small radii of curvature using the light-profile microscope. Nature 1952, 170, (4331), 758–9.CrossRefADSGoogle Scholar
  9. 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.CrossRefADSGoogle Scholar
  10. 10.
    Hunter, R., Foundations of Colloid Science. Oxford University Press: Oxford, 1989; Vol. 1.Google Scholar
  11. 11.
    Helm, C. A.; Israelachvili, J. N., Forces between phospholipid bilayers and relationship to membrane fusion. Methods Enzymol 1993, 220, 130–43.CrossRefGoogle Scholar
  12. 12.
    Helm, C. A.; Israelachvili, J. N.; McGuiggan, P. M., Role of hydrophobic forces in bilayer adhesion and fusion. Biochemistry 1992, 31, (6), 1794–805.CrossRefGoogle Scholar
  13. 13.
    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.CrossRefADSGoogle Scholar
  14. 14.
    Leckband, D. E., Helm, C. A., Israelachvili, J., Role of Calcium in the Adhesion and Fusion of Bilayers. Biochemistry 1993, 32, 1127–1140.CrossRefGoogle Scholar
  15. 15.
    Israelachvili, J., Intermolecular and Surface Forces. 2 ed.; Academic Press: New York, 1992.Google Scholar
  16. 16.
    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.CrossRefGoogle Scholar
  17. 17.
    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.CrossRefADSGoogle Scholar
  18. 18.
    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.CrossRefGoogle Scholar
  19. 19.
    Evans, E., Ritchie, K., Dynamic Strength of Molecular Adhesion Bonds. Biophys. J. 1997, 72, 1541–1555.CrossRefGoogle Scholar
  20. 20.
    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.CrossRefADSGoogle Scholar
  21. 21.
    Hummer, G.; Szabo, A., Free energy reconstruction from nonequilibrium single-molecule pulling experiments. Proc Natl Acad Sci USA 2001, 98, (7), 3658–61.CrossRefADSGoogle Scholar
  22. 22.
    Hummer, G.; Szabo, A., Kinetics from nonequilibrium single-molecule pulling experiments. Biophys J 2003, 85, (1), 5–15.CrossRefGoogle Scholar
  23. 23.
    Hummer, G.; Szabo, A., Free energy surfaces from single-molecule force spectroscopy. Acc Chem Res 2005, 38, (7), 504–13.CrossRefGoogle Scholar
  24. 24.
    Paramore, S.; Ayton, G. S.; Voth, G. A., Extending the fluctuation theorem to describe reaction coordinates. J Chem Phys 2007, 126, (5), 051102.ADSGoogle Scholar
  25. 25.
    Li, F.; Leckband, D., Dynamic strength of molecularly bonded surfaces. J Chem Phys 2006, 125, (19), 194702.CrossRefADSGoogle Scholar
  26. 26.
    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.CrossRefGoogle Scholar
  27. 27.
    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.CrossRefGoogle Scholar
  28. 28.
    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.CrossRefADSGoogle Scholar
  29. 29.
    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.CrossRefGoogle Scholar
  30. 30.
    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.CrossRefGoogle Scholar
  31. 31.
    Leckband, D., Schmitt, F.-J., Israelachvili, J., Knoll, W., Direct force measurements of specific and nonspecific protein interactions. Biochemistry 1994, 33, 4611–4624.CrossRefGoogle Scholar
  32. 32.
    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.CrossRefGoogle Scholar
  33. 33.
    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.CrossRefGoogle Scholar
  34. 34.
    Marra, J., Israelachvili, J., Direct Measurements of Forces between Phosphatidylcholine and Phosphatidylethanolamine bilayers in Aqueous Electrolyte Solutions. Biochemistry 1985, 24, 4608–4618.CrossRefGoogle Scholar
  35. 35.
    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.CrossRefGoogle Scholar
  36. 36.
    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.CrossRefGoogle Scholar
  37. 37.
    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.Google Scholar
  38. 38.
    Yu, Z.-W., Calvert, T., Leckband, D., Molecular Forces between Membranes Displaying Neutral Glycosphingolipids: Evidence for Carbohydrate Attraction. Biochemistry 1997, 37, 1540–1550.CrossRefGoogle Scholar
  39. 39.
    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.CrossRefGoogle Scholar
  40. 40.
    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.CrossRefADSGoogle Scholar
  41. 41.
    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.CrossRefGoogle Scholar
  42. 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.CrossRefADSGoogle Scholar
  43. 43.
    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.Google Scholar
  44. 44.
    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.CrossRefGoogle Scholar
  45. 45.
    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.CrossRefGoogle Scholar
  46. 46.
    Davis, S. J., vanderMerwe, P. A., The structure and ligand interactions of CD2: implications for T-cell function. Immunology Today 1996, 17, 177–187.CrossRefGoogle Scholar
  47. 47.
    Davis, S. J., vanderMerwe, P. A., CD2-An Exception to the Immunoglobulin Superfamily Concept. Science 1996, 273, 1241–1242.CrossRefADSGoogle Scholar
  48. 48.
    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.CrossRefADSGoogle Scholar
  49. 49.
    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.CrossRefGoogle Scholar
  50. 50.
    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.CrossRefADSGoogle Scholar
  51. 51.
    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.CrossRefGoogle Scholar
  52. 52.
    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.CrossRefGoogle Scholar
  53. 53.
    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.CrossRefGoogle Scholar
  54. 54.
    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.CrossRefGoogle Scholar
  55. 55.
    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.CrossRefGoogle Scholar
  56. 56.
    van der Merwe, P. A.; Davis, S. J., Molecular interactions mediating T cell antigen recognition. Annu Rev Immunol 2003, 21, 659–84.CrossRefGoogle Scholar
  57. 57.
    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.CrossRefADSGoogle Scholar
  58. 58.
    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.CrossRefADSGoogle Scholar
  59. 59.
    Bayas, M. V.; Schulten, K.; Leckband, D., Forced detachment of the CD2-CD58 complex. Biophys J 2003, 84, (4), 2223–33.CrossRefGoogle Scholar
  60. 60.
    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.CrossRefGoogle Scholar
  61. 61.
    Walsh, F., Doherty, P, Neural Cell Adhesion Molecules of the Immunoglobulin Superfamily. Ann. Rev. Cell. Biol. 1997, 13, 425–56.Google Scholar
  62. 62.
    Chothia, C., Jones, E. Y., The Molecular Structure of Cell Adhesion Molecules. Ann. Rev. Biochem. 1997, 66, 823–862.CrossRefGoogle Scholar
  63. 63.
    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.CrossRefADSGoogle Scholar
  64. 64.
    Hall, A., Rutishauser, U., Visualization of neural cell adhesion molecule by electron microscopy. J. Cell Biol. 1987, 104, 1579–86.CrossRefGoogle Scholar
  65. 65.
    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.CrossRefGoogle Scholar
  66. 66.
    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.CrossRefADSGoogle Scholar
  67. 67.
    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.Google Scholar
  68. 68.
    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.CrossRefGoogle Scholar
  69. 69.
    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.CrossRefGoogle Scholar
  70. 70.
    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.CrossRefADSGoogle Scholar
  71. 71.
    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.CrossRefGoogle Scholar
  72. 72.
    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.CrossRefGoogle Scholar
  73. 73.
    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.CrossRefGoogle Scholar
  74. 74.
    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.CrossRefGoogle Scholar
  75. 75.
    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.CrossRefADSGoogle Scholar
  76. 76.
    Christenson, H. K., Forces between solid surfaces in a binary mixture of non-polar liquids. Chem. Phys. Lett. 1985, 118, 455–458.CrossRefADSGoogle Scholar
  77. 77.
    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.CrossRefADSGoogle Scholar
  78. 78.
    Heuberger, M., Zach, M., Spencer, N. D., Density fluctuations under confinement: when is a fluid not a fluid? Science 2001, 292, 905–908.CrossRefADSGoogle Scholar
  79. 79.
    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.CrossRefADSGoogle Scholar
  80. 80.
    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.CrossRefADSGoogle Scholar
  81. 81.
    Israelachvili, J. N., Pashley, R. M., Molecular layering of water at surfaces and origin of repulsive hydration forces. Nature 1983, 306, 249–250.CrossRefADSGoogle Scholar
  82. 82.
    Israelachvili, J. N., Solvation forces and liquid structure, as probed by direct force measurements. Acc. Chem. Res. 1987, (20), 415–421.CrossRefGoogle Scholar
  83. 83.
    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.CrossRefADSGoogle Scholar
  84. 84.
    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.CrossRefGoogle Scholar
  85. 85.
    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.CrossRefGoogle Scholar
  86. 86.
    Attard, P., Parker, J. L., Oscillatory solvation forces: A comparison of theory and experiment. J. Phys. Chem. 1992, 92, 5086–5093.CrossRefGoogle Scholar
  87. 87.
    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.CrossRefGoogle Scholar
  88. 88.
    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.CrossRefGoogle Scholar
  89. 89.
    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.CrossRefADSGoogle Scholar
  90. 90.
    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.CrossRefGoogle Scholar
  91. 91.
    Rutishauser, U., Polysialic acid and the regulation of cell interactions. Curr. Op. Cell Biol. 1996, 8, 679–684.CrossRefGoogle Scholar
  92. 92.
    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.CrossRefGoogle Scholar
  93. 93.
    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.Google Scholar
  94. 94.
    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.CrossRefGoogle Scholar
  95. 95.
    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.CrossRefGoogle Scholar
  96. 96.
    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.CrossRefGoogle Scholar
  97. 97.
    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.Google Scholar
  98. 98.
    Yang, P. Y., X., Rutishauser, U., Intercellular space is affected by polysialic acid content of NCAM. J. Cell Biol. 1992, 116, 1487–1496.CrossRefGoogle Scholar
  99. 99.
    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.CrossRefGoogle Scholar
  100. 100.
    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.Google Scholar
  101. 101.
    Alberts, B., Bray, D., Lewis, J., Raff, M., Roberts, K., Watson, J. D., The Molecular Biology of the Cell. Garland: NY, 1983.Google Scholar

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© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • Deborah Leckband
    • 1
  1. 1.Department of Chemical and Biomolecular EngineeringUniversity of Illinois at Urbana-Champaign, 127 Roger Adams Lab MC-712UrbanaUSA

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