Characterization of the physical properties of model biomembranes at the nanometer scale with the atomic force microscope

Abstract

Interaction forces and topography of mixed phospholipid–glycolipid bilayers were investigated by atomic force microscopy (AFM) in aqueous conditions with probes functionalized with self-assembled monolayers terminating in hydroxy groups. Short-range repulsive forces were measured between the hydroxy-terminated probe and the surface of the two-dimensional (2-D) solid-like domains of distearoyl-phosphatidylethanolamine (DSPE) and digalactosyldiglyceride (DGDG). The form and range of the short-range repulsive force indicated that repulsive hydration/steric forces dominate the interaction at separation distances of 0.3–1.0 nm after which the probe makes mechanical contact with the bilayers. At loads <5 nN the bilayer was elastically deformed by the probe, while at higher loads plastic deformation of the bilayer was observed. Surprisingly, a short-range repulsive force was not observed at the surface of the 2-D liquid-like dioleoylphosphatidylethanolamine (DOPE) film, despite the identical head groups of DOPE and DSPE. This provides direct evidence for the influence of the structure and mechanical properties of lipid bilayers on their interaction forces, an effect which may be of major importance in the control of biological processes such as cell adhesion and membrane fusion. The step height measured between lipid domains in the AFM topographic images was larger than could be accounted for by the thickness and mechanical properties of the molecules. A direct correlation was observed between the repulsive force range over the lipid domains and the topographic contrast, which provides direct insight into the fundamental mechanisms of AFM imaging in aqueous solutions. This study demonstrates that chemically modified AFM probes can be used in combination with patterned lipid bilayers as a novel and powerful approach to characterize the nanometer scale chemical and physical properties of heterogeneous biosurfaces such as cell membranes.

References

1. R. O. Hynes, Cell, 1992, 69, 11.
2. A. Varki, Proc. Natl. Acad. Sci. USA, 1994, 91, 7390.
3. N. Sharon and H. Lis, Science, 1989, 246, 227.
4. W. Curatolo, Biochim. Biophys. Acta., 1987, 906, 137.
5. N. Sharon and H. Lis, Sci. Am., 1993, January, 74.
6. S.-I. Hakomori, Prog. Brain Res., 1994, 101, 241.
7. R. G. Horn, Biochim. Biophys. Acta, 1984, 778, 224.
8. J. Marra, J. Colloid Interface Sci., 1985, 107, 446.
9. J. Marra and J. Israelachvili, Biochemistry, 1985, 24, 4608.
10. J. Israelachvili and H. Wennerström, Nature (London), 1996, 379, 219.
11. D. M. LeNeveu, R. P. Rand and V. A. Parsegian, Nature (London), 1976, 259, 601.
12. R. P. Rand and V. A. Parsegian, Biochim. Biophys. Acta, 1989, 988, 351.
13. S. Leikin, V. A. Parsegian, D. C. Rau and R. P. Rand, Annu. Rev. Phys. Chem., 1993, 44, 369.
14. T. J. McIntosh and S. A. Simon, Annu. Rev. Biophys. Biomol. Struct., 1994, 23, 27.
15. G. Binnig, C. F. Quate and Ch. Gerber, Phys. Rev. Lett., 1986, 56, 930.
16. A. L. Weisenhorn, B. Drake, C. B. Prater, S. A. C. Gould, P. K. Hansma, F. Ohnesorge, M. Egger, S.-P. Heyn and H. E. Gaub, Biophys. J., 1990, 58, 1251.
17. H. G. Hansma, M. Bezanilla, F. Zenhausern, M. Adrian and R. L. Sinsheimer, Nucleic Acids Res., 1993, 21, 505.
18. M. Fritz, M. Radmacher and H. E. Gaub, Biophys J., 1994, 66, 1328.
19. M. Radmacher, R. W. Tillmann, M. Fritz and H. E. Gaub, Science, 1992, 257, 1900.
20. H. G. Hansma and J. H. Hoh, Annu. Rev. Biophys. Biomol. Struct., 1994, 23, 115.
21. H.-J. Butt, K. H. Downing and P. K. Hansma, Biophys. J., 1990, 58, 1473.
22. J. A. N. Zasadzinski, C. A. Helm, M. L. Longo, A. L. Weisenhorn, S. A. C. Gould and P. K. Hansma, Biophys. J., 1991, 59, 755.
23. J. H. Hoh, G. E. Sosinksky, J.-P. Revel and P. K. Hansma, Biophys. J., 1993, 65, 149.
24. S. W. Hui, R. Viswanathan, J. A. Zasadzinski and J. N. Israelachvili, Biophys. J., 1995, 68, 171.
25. H.-J. Butt, E. K. Wolff, S. A. C. Gould, B. Dixon-Northern, C. M. Peterson and P. K. Hansma, J. Struct. Biol., 1990, 105, 54.
26. J. H. Hoh and C.-A. Schoenenberger, J. Cell Sci., 1994, 107, 1105.
27. L. K. Tamm and H. M. McConnell, Biophys. J., 1985, 47, 105.
28. E. Sackmann, Science, 1996, 271, 43.
29. J. Mou, J. Yang and Z. Shao, J. Mol. Biol., 1995, 248, 507.
30. W. A. Ducker, T. J. Senden and R. M. Pashley, Nature (London), 1991, 353, 239.
31. H.-J. Butt, Biophys. J., 1991, 60, 1438.
32. T. J. Senden, C. J. Drummond and P. Kékicheff, Langmuir, 1994, 10, 358.
33. S. J. O'Shea, M. E. Welland and T. Rayment, Appl. Phys. Lett., 1992, 60, 2356.
34. J. P. Cleveland, T. E. Schäffer and P. K. Hansma, Phys. Rev. B, 1995, 52, R8692.
35. S. Biggs, Langmuir, 1995, 11, 156.
36. R. M. Overney, D. P. Leta, C. F. Pietroski, M. H. Rafailovich, Y. Liu, J. Quinn, J. Sokolov, A. Eisenberg and G. Overney, Phys. Rev. Lett., 1996, 76, 1272.
37. G. U. Lee, D. A. Kidwell and R. J. Colton, Langmuir, 1994, 10, 354.
38. E.-L. Florin, V. T. Moy and H. E. Gaub, Science, 1994, 264, 415.
39. G. U. Lee, L. A. Chrisey and R. J. Colton, Science, 1994, 266, 771.
40. D. R. Baselt and J. D. Baldeschwieler, J. Appl. Phys., 1994, 76, 33.
41. M. Ludwig, W. Dettmann and H. E. Gaub, Biophys. J., 1997, 72, 445.
42. C. Rotsch and M. Radmacher, Langmuir, 1997, 13, 2825.
43. G. U. Lee, L. A. Chrisey, C. E. O'Ferrall, D. E. Pilloff, N. H. Turner and R. J. Colton, Isr. J. Chem., 1996, 36, 81.
44. C. D. Frisbie, L. F. Rozsnyai, A. Noy, M. S. Wrighton and C. M. Lieber, Science, 1994, 265, 2071.
45. J.-B. D. Green, M. T. McDermott and M. D. Porter, J. Phys. Chem., 1995, 99, 10960.
46. J. Marra, J. Colloid Interface Sci., 1986, 109, 11.
47. R. G. Nuzzo and D. L. Allara, J. Am. Chem. Soc., 1983, 105, 4481.
48. C. D. Bain, E. B. Troughton, Y.-T. Tao, J. Evall, G. M. Whitesides and R. G. Nuzzo, J. Am. Chem. Soc., 1989, 111, 331.
49. R. G. Nuzzo, L. H. Dubois and D. L. Allara, J. Am. Chem. Soc., 1990, 112, 558.
50. Y. F. Dufrêne, W. R. Barger, J.-B. D. Green and G. U. Lee, Langmuir, 1997, 13, 4779.
51. M. Tortonese and M. Kirk, SPIE, 1997, 3009, 53.
52. H. G. Tomkins, A User's Guide to Ellipsometry, Academic Press, Inc., San Diego, 1993.
53. S. J. O'Shea, M. E. Welland and T. Rayment, Appl. Phys. Lett., 1992, 61, 2240.
54. D. D. Koleske, W. R. Barger, G. U. Lee and R. J. Colton, Mat. Res. Soc. Symp. Proc., 1997, 464, 377.
55. K. L. Johnson, Contact Mechanics, Cambridge University Press, Cambridge, 1985.
56. E. A. Evans and R. M. Hochmuth, in Current Topics in Membranes and Transport, ed. A. Kleinzeller and F. Bronner, Academic Press, New York, 1978, pp. 1–10.
57. E. A. Evans and P. Kwok, Biochemistry, 1982, 21, 4874.
58. K. J. Tupper and D. W. Brenner, Langmuir, 1994, 10, 2335.
59. S. Manne, J. P. Cleveland, H. E. Gaub, G. D. Stucky and P. K. Hansma, Langmuir, 1994, 10, 4409.
60. S. Nir, Prog. Surf. Sci., 1976, 8, 1.
61. D. Gingell and V. A. Parsegian, J. Theor. Biol., 1972, 36, 41.
62. D. B. Hough and L. R. White, Adv. Colloid Interface Sci., 1980, 14, 3.
63. S. Marcelja and N. Radic, Chem. Phys. Lett., 1976, 42, 129.
64. J. N. Israelachvili and H. Wennerström, Langmuir, 1990, 6, 873.
65. J. N. Israelachvili and H. Wennerström, J. Phys. Chem., 1992, 96, 520.
66. J. N. Israelachvili and R. M. Pashley, Nature (London), 1982, 300, 341.
67. J. M. Boggs, Biochim. Biophys. Acta, 1987, 906, 353.
68. T. P. Weihs, Z. Nawaz, S. P. Jarvis and J. B. Pethica, Appl. Phys. Lett., 1991, 59, 3536.
69. W. A. Ducker and D. R. Clarke, Colloids Surf. A, 1994, 93, 275.