Functional analysis of the structural basis of homophilic cadherin adhesion

Biophysical Journal

Volumn 84, Issue 6, 2003, Pages 4033-4042

  Zhu, B ^a   Chappuis Flament, S ^b   Wong, E ^c   Jensen, I E ^a   Gumbiner, B M ^d   Leckband, D ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITÉ LYON 1   (France)

^c ROCKEFELLER UNIVERSITY   (United States)

^d UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CADHERIN;

ARTICLE; CELL SURFACE; EXTRACELLULAR SPACE; MOLECULAR MODEL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN STRUCTURE; TANDEM REPEAT;

EID: 0038440606     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(03)75129-7     Document Type: Article

References (52)

1. Ahrens, T., O. Pertz, D. Häussinger, C. Fauser, T. Schulthess, and J. Engel. 2002. Analysis of heterophilic and homophilic interactions of cadherins using the c-Jun/c-Fos dimerization domains. J. Biol. Chem. 277:19455-19460.
2. Baumgartner, W., P. Hinterdorfer, W. Ness, A. Rash, D. Vestweber, H. Schindler, and D. Drenckhahn. 2000. Cadherin interaction probed by atomic force microscopy. Proc. Natl. Acad. Sci. USA. 97:4005-4010.
3. Boggon, T., J. Murray, S. Chappuis-Flament, E. Wong, B. M. Gumbiner, and L. Shapiro. 2002. C-cadherin ectodomain structure and implications for cell adhesion mechanisms. Science. 296:1308-1313.
4. Brieher, W. M., A. S. Yap, and B. M. Gumbiner. 1996. Lateral dimerization is required for the homophilic binding activity of C-cadherin. J. Cell Biol. 135:487-496.
5. Chappuis-Flament, S., E. Wong, L. D. Hicks, C. M. Kay, and B. M. Gumbiner. 2001. Multiple cadherin extracellular repeats mediate homophilic binding and adhesion. J. Cell Biol. 154:231-243.
6. Chothia, C., and E. Y. Jones. 1997. The molecular structure of cell adhesion molecules. Annu. Rev. Biochem. 66:823-862.
7. Christenson, H., D. W. R. Gruen, R. G. Horn, and J. N. Israelachvili. 1987. Structuring in liquid alkanes betwen solid surfaces: Force measurements and mean field theory. J. Chem. Phys. 87:1834-1841.
8. Davis, S. J., and P. A. van der Merwe. 1996. The structure and ligand interactions of CD2: implications for T-cell function. Immunol. Today. 17:177-187.
9. Gumbiner, B. M. 1996. Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell. 84:345-357.
10. Häussinger, D., T. Ahrens, H.-J. Sass, O. Pertz, J. Engel, and S. Grzesiek. 2002. Calcium-dependent homoassociation of E-cadherin by NMR spectroscopy: changes in mobility, conformation, and mapping of contact regions. J. Mol. Biol. 324:823-839.
11. Hunter, R. 1989. Foundations of Colloid Science. Oxford University Press, Oxford.
12. Israelachvili, J. 1973. Thin film studies using Mmultiple-beam interferometry. J. Colloid Interface Sci. 44:259-272.
13. Israelachvili, J. 1987. Solvation forces and liquid structure, as probed by direct force measurements. Acc. Chem. Res. 20:415-421.
14. Israelachvili, J. 1992a. Adhesion forces between surfaces in liquids and condensable vapours. Surface Science Reports. 14:110-159.
15. Israelachvili, J. 1992b. Intermolecular and Surface Forces. Academic Press, New York.
16. Israelachvili, J. N., and G. E. Adams. 1978. Measurement of forces between two mica surfaces in aqueous electrolyte solutions in the range 0-100 nm. J. Chem. Soc. Faraday Trans. I. 75:975-1001.
17. Israelachvili, J., and R. Pashley. 1983. Molecular layering of water at surfaces and origin of repulsive hydration forces. Nature. 306:249-250.
18. Jensen, P., V. Soroka, N. K. Thompson, I. Ralets, V. Berezin, E. Bock, and F. M. Poulsen. 1999. Structure and interactions of NCAM modules 1 and 2, basic elements in neural cell adhesion. Nat. Struct. Biol. 6:486-493.
19. Johnson, K. L., K. Kendall, and A. D. Roberts. 1971. Surface energy and the contact of elastic solids. Proc. R. Soc. Lond. A. 324:301-313.
20. Kekicheff, P., W. A. Ducker, B. W. Ninham, and M. P. Pileni. 1990. Multilayer adsorption of cytochrome c on mica around isoelectric pH. Langmuir. 6:1704-1708.
21. Kiselyov, V., V. Berezin, T. E. Maar, V. Soroka, K. Edvardsen, A. Schousboe, and E. Bock. 1997. The first immunoglobulin-like neural cell adhesion molecule (NACM) domain is involved in double-reciprocal interaction with the second immunoglobulin-like NCAM domain and in hepar in binding. J. Biol. Chem. 272:10125-10134.
22. Klingelhöfer, J., O. Y. Laur, R. B. Troyanovsky, and S. M. Troyanovsky. 2002. Dynamic interplay between adhesive and lateral E-cadherin dimers. Mol. Cell. Biol. 22:7449-7458.
23. Koch, A., D. Bozic, O. Pertz, and J. Engel. 1999. Homophilic adhesion by cadherins. Curr. Opin. Struct. Biol. 9:275-281.
24. Lavrik, N., and D. Leckband. 2000. Optical and direct force measurements of the interaction between monolayers of aromatic macrocycles on surfactant monolayers. Langmuir. 16:1842-1851.
25. Leckband, D. 2002. The structure of the C-cadherin ectodomain revealed. Structure. 10:739-740.
26. Leckband, D., and J. Israelachvili. 2001. Intermolecular forces in biology. Quart. Rev. Biophys. 34:105-267.
27. Leckband, D., W. Müller, F.-J. Schmitt, and H. Ringsdorf. 1995. Molecular mechanisms determining the strength of receptor-mediated intermembrane adhesion. Biophys. J. 69:1162-1169.
28. Leckband, D., and S. Sivasankar. 2000. Mechanism of homophilic cadherin adhesion. Curr. Opin. Cell. Biol. 12:587-592.
29. Marra, J., and J. Israelachvili. 1985. Direct measurements of forces between phosphatidylcholine and phosphatidylethanolamine bilayers in aqueous electrolyte solutions. Biochemistry. 24:4608-4618.
30. Martel, L., C. Johnson, S. Boutet, R. Al-Kurdi, O. Konovalov, I. Robinson, D. Leckband, and J.-F. Legrand. 2002. X-ray reflectivity investigations of two-dimensional assemblies of C-cadherin: first steps in structural and functional studies. J. Phys. IV. 12:366-377.
31. Nagar, B., M. Overduin, M. Ikura, and J. M. Rini. 1995. Structural basis of calcium-induced E-cadherin rigidification and dimerization. Nature. 380:360-364.
32. Nose, A., K. Tsuji, and M. Takeichi. 1990. Localization of specificity determining sites in cadherin cell adhesion molecules. Cell. 61:147-155.
33. 2+ dependence and mutational analysis reveal molecular details of E-cadherin homoassociation. EMBO J. 18:1738-1747.
34. Petrov, P., S. Miklavcic, U. Olsson, and H. Wennerstrom. 1995. A confined complex liquid. Oscillatory forces and lamellae formation from an L3 phase. Langmuir. 11:3928-3936.
35. Pokutta, S., K. Herrenknecht, R. Kemler, and J. Engel. 1994. Conformational changes of the recombinant extracellular domain of E-cadherin upon calcium binding. Eur. J. Biochem. 223:1019-1026.
36. Ranheim, T. S., G. M. Edelman, and B. A. Cunningham. 1996. Homophilic adhesion mediated by the neural cell adhesion molecule involves multiple immunoglobulin domains. Proc. Natl. Acad. Sci. USA. 93:4071-4075.
37. Renaud-Young, M., and W. J. Gallin. 2002. E-cadherin EC1: heterophilic interactions, but not the conserved HAV motif, are required for adhesion. J. Biol. Chem. 277:39609-39616.
38. Shan, W.-S., H. Tankaka, G. R. Phillips, K. Arndt, M. Yoshida, D. R. Colman, and L. Shapiro. 2000. Functional cis-heterodimers of N- and R-cadherins. J. Cell Biol. 148:579-590.
39. Shapiro, L., A. M. Fannon, P. D. Kwong, A. Thompson, M. G. Lehmann, G. Grübel, J.-F. Legrand, J. Als-Nielsen, D. R. Colman, and W. A. Hendrickson. 1995. Structural basis of cell-cell adhesion of cadherins. Nature. 374:327-337.
40. Sivasankar, S., W. Brieher, N. Lavrik, B. Gumbiner, and D. Leckband. 1999. Direct molecular force measurements of multiple adhesive interactions between cadherin ectodomains. Proc. Natl. Acad. Sci. USA. 96:11820-11824.
41. Sivasankar, S., B. M. Gumbiner, and D. Leckband. 2001. Direct measurements of multiple adhesive alignments and unbinding trajectories between cadherin extracellular domains. Biophys. J. 80:1758-1768.
42. Takeichi, M. 1991. Cadherin cell adhesion receptors as a morphogenetic regulator. Science. 251:1451-1455.
43. Takeichi, M. 1995. Morphogenetic roles of classic cadherins. Curr. Opin. Cell Biol. 7:619-627.
44. Tamura, K., W.-S. Shan, W. A. Hendrickson, D. R. Colman, and L. Shapiro. 1998. Structure-function analysis of cell adhesion by neural (N-) cadherin. Neuron. 20:1153-1163.
45. Tomschy, A., C. Fauser, R. Landwehr, and J. Engel. 1996. Homophilic adhesion of E-cadherin occurs by a co-operative two-step interaction of N-terminal domains. EMBO J. 15:3507-3514.
46. Vijayendran, R., D. Hammer, and D. Leckband. 1998. Simulations of the adhesion between molecularly bonded surfaces in direct force measurements. J. Chem. Phys. 108:1162-1169.
47. Walsh, F., and P. Doherty. 1997. Neural cell adhesion molecules of the immunoglobulin superfamily. Annu. Rev. Cell Biol. 13:425-456.
48. Wong, J. Y., T. L. Kuhl, J. N. Israelachvili, N. Mullah, and S. Zalipsky. 1997. Direct measurement of a tethered ligand-receptor interaction potential. Science. 275:820-822.
49. Yap, A., W. M. Brieher, M. Ruschy, and B. M. Gumbiner. 1997a. Lateral clustering of the adhesive ectodomain: a fundamental determinant of cadherin function. Curr. Biol. 7:308-315.
50. Yap, A. S., W. M. Brieher, and B. M. Gumbiner. 1997b. Molecular and functional analysis of cadherin-based adherens junctions. Annu. Rev. Cell Dev. Biol. 13:119-146.
51. Yap, A. S., C. M. Niessen, and B. M. Gumbiner. 1998. The juxtamembrane region of the cadherin cytoplasmic tail supports lateral clustering, adhesive strengthening and interaction with p120ctn. J. Cell Biol. 141:779-789.
52. Zhu, B., E. A. Davies, P. A. van der Merwe, T. Calvert, and D. E. Leckband. 2002. Direct measurements of heterotypic adhesion between the cell surface proteins CD2 and CD48. Biochemistry. 42:12163-12170.