Stable and unstable cadherin dimers: Mechanisms of formation and roles in cell adhesion

Molecular Biology of the Cell

Volumn 18, Issue 11, 2007, Pages 4343-4352

  Troyanovsky, Regina B ^a   Laur, Oscar ^b   Troyanovsky, Sergey M ^c  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGAROSE; CADHERIN; CADMIUM; CALCIUM ION; CATENIN; MUTANT PROTEIN; UVOMORULIN;

ARTICLE; CELL ADHESION; CELL JUNCTION; CONTROLLED STUDY; CROSS LINKING; DIMERIZATION; DISSOCIATION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE;

CADHERINS; CELL ADHESION; CELL LINE, TUMOR; CLATHRIN; DIMERIZATION; ENDOCYTOSIS; HUMANS; POINT MUTATION; PROTEIN BINDING;

EID: 35848939400     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E07-01-0084     Document Type: Article

References (34)

1. Barrientos, L. G., Louis, J. M., Botos, I., Mori, T., Han, Z., O'Keefe, B. R., Boyd, M. R., Wlodawer, A., and Gronenborn, A. M. (2002). The domain-swapped dimer of cyanovirin-N is in a metastable folded state: reconciliation of X-ray and NMR structures. Structure 10, 673-686.
2. Bayas, M. V., Schulten, K., and Leckband, D. (2004). Forced dissociation of the strand dimer interface between C-cadherin ectodomains. Mech. Chem. Biosyst. 1, 101-111.
3. Boggon, T. J., Murray, J., Chappuis-Flament, S., Wong, E., Gumbiner, B. M., and Shapiro, L. (2002) C-cadherin ectodomain structure and implications for cell adhesion mechanisms. Science 296, 1308-1313.
4. Bussemakers, M. J., van Bokhoven, A., Mees, S. G., Kemler, R., and Schalken, J. A. (1993). Molecular cloning and characterization of the human E-cadherin cDNA. Mol. Biol. Rep. 17, 123-128.
5. Chen, C. P., Posy, S., Ben-Shaul, A., Shapiro, L., and Honig, B. H. (2005). Specificity of cell-cell adhesion by classic Cadherins: critical role for low-affinity dimerization through β-strand swapping. Proc. Natl. Acad. Sci. USA 102, 8531-8536.
6. Chitaev, N. A., and Troyanovsky, S. M. (1998). Adhesive but not lateral E-cadherin complexes require calcium and catenins for their formation. J. Cell Biol. 142, 837-846.
7. Gumbiner, B. M. (2005). Regulation of cadherin-mediated adhesion in morphogenesis. Nat. Rev. Mol. Cell Biol. 6, 622-634.
8. Hakansson, M., Svensson, A., Fast, J., and Linse, S. (2001). An extended hydrophobic core induces EF-hand swapping. Protein Sci. 10, 927-933.
9. Hanakawa, Y., Selwood, T., Woo, D., Lin, C., Schechter, N. M., and Stanley, J. R. (2003). Calcium-dependent conformation of desmoglein 1 is required for its cleavage by exfoliative toxin. J. Invest. Dermatol. 121, 383-389.
10. Harrison, O. J., Corps, E. M., and Kilshaw, P. J. (2005). Cadherin adhesion depends on a salt bridge at the N-terminus. J. Cell Sci. 118, 4123-4130.
11. Haussinger, D., Ahrens, T., Aberle, T., Engel, J., Stetefeld, J., and Grzesiek, S. (2004). Proteolytic E-cadherin activation followed by solution NMR and X-ray crystallography. EMBO J. 23, 1699-1708.
12. Hinrichsen, L., Harborth, J., Andrees, L., Weber, K., and Ungewickell, E. J. (2003). Effect of clathrin heavy chain- and alpha-adaptin-specific small inhibitory RNAs on endocytic accessory proteins and receptor trafficking in HeLa cells. J. Biol. Chem. 278, 45160-45170.
13. Klingelhofer, J., Laur, O. Y., Troyanovsky, R. B., and Troyanovsky, S. M. (2002). Dynamic interplay between adhesive and lateral E-cadherin dimers. Mol. Cell Biol. 22, 7449-7458.
14. Kusumi, A., Suzuki, K., and Koyasako, K. (1999). Mobility and cytoskeletal interactions of cell adhesion receptors. Curr. Opin. Cell Biol. 11, 582-590.
15. Laur, O. Y., Klingelhofer, J., Troyanovsky, R. B., and Troyanovsky, S. M. (2002). Both the dimerization and immunochemical properties of E-cadherin EC1 domain depend on Trp156 residue. Arch. Biochem. Biophys. 400, 141-147.
16. Liu, Y., and Eisenberg, D. (2002). 3D domain swapping: as domains continue to swap. Protein Sci. 11, 1285-1299.
17. Mege, R. M., Gavard, J., and Lambert, M. (2006). Regulation of cell-cell junctions by the cytoskeleton. Curr. Opin. Cell Biol. 18, 541-548.
18. Nagar, B., Overduin, M., Ikura, M., and Rini, J. M. (1996). Structural basis of calcium-induced E-cadherin rigidification and dimerization. Nature 380, 360-364.
19. Ozawa, M. (2002). Lateral dimerization of the E-cadherin extracellular domain is necessary but not sufficient for adhesive activity. J. Biol. Chem. 277, 19600-19608.
20. Ozawa, M., and Kemler, R. (1998). The membrane-proximal region of the E-cadherin cytoplasmic domain prevents dimerization and negatively regulates adhesion activity. J. Cell Biol. 142, 1605-1613.
21. Patel, S. D., Chen, C. P., Bahna, F., Honig, B., and Shapiro, L. (2003). Cadherin-mediated cell-cell adhesion: sticking together as a family. Curr. Opin. Struct. Biol. 13, 690-698.
22. Patel, S. D. et al. (2006). Type II Cadherin ectodomain structures: implications for classical cadherin specificity. Cell 124, 1255-1268.
23. 2+ dependence and mutational analysis reveal molecular details of E-cadherin homoassociation. EMBO J. 18, 1738-1747.
24. Provost, E., and Rimm, D. L. (1999). Controversies at the cytoplasmic face of the cadherin-based adhesion complex. Curr. Opin. Cell Biol. 11, 567-573.
25. Rousseau, F., Schymkowitz, J. W., Wilkinson, H. R., and Itzhaki, L. S. (2001). Three-dimensional domain swapping in p13suc1 occurs in the unfolded state and is controlled by conserved proline residues. Proc. Natl. Acad. Sci. USA 98, 5596-5601.
26. Rousseau, F., Schymkowitz, J. W., and Itzhaki, L. S. (2003) The unfolding story of three-dimensional domain swapping. Structure 11, 243-251.
27. Shan, W-S., Tanaka, H., Phillips, G. R., Arndt, K., Yoshida, M., Colman, D. R., and Shapiro, L. (2000). Functional cis-heterodimers of N- and R-cadherins. J. Cell Biol. 148, 579-590.
28. Shapiro, L., Fannon, A. M., Kwong, P. D., Thompson, A., Lehman, M. S., Grubel, G., Legran, J-F., Als-Neilsen, J., Colman, D. R., and Hendrickson, W. A. (1995). Structural basis of cell-cell adhesion by Cadherins. Nature 374, 327-337.
29. Takeichi, M. (1995). Morphogenetic roles of classic Cadherins. Curr. Opin. Cell Biol. 7, 619-6127.
30. Troyanovsky, S. M. (2005). Cadherin dimers in cell-cell adhesion. Eur. J. Cell Biol. 84, 225-233.
31. Troyanovsky, R. B., Sokolov, E., and Troyanovsky, S. M. (2003). Adhesive and lateral E-cadherin dimers are mediated by the same interface. Mol. Cell. Biol. 22, 7965-7972.
32. Troyanovsky, R. B., Sokolov, E., and Troyanovsky, S. M. (2006). Endocytosis of cadherin from intracellular junctions is the driving force for cadherin adhesive dimer disassembly. Mol. Biol. Cell 17, 3484-3493.
33. Waisberg, M., Joseph, P., Hale, B., and Beyersmann, D. (2003). Molecular and cellular mechanisms of cadmium carcinogenesis. Toxicology 192, 95-117.
34. Yap, A. S., Niessen, C. M., and Gumbiner, B. M. (1998). The juxtamembrane region of the cadherin cytoplasmic tail supports lateral clustering, adhesive strengthening, and interaction with p120ctn. J. Cell Biol. 141, 779-789.