The membrane-proximal region of the E-cadherin cytoplasmic domain prevents dimerization and negatively regulates adhesion activity

Journal of Cell Biology

Volumn 142, Issue 6, 1998, Pages 1605-1613

  Ozawa, Masayuki ^a   Kemler, Rolf ^b  

^a KAGOSHIMA UNIVERSITY   (Japan)

^b MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

Author keywords

Adhesion; Aggregation; Cadherin; Catenin; Compaction

Indexed keywords

CATENIN; UVOMORULIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL ADHESION; CROSS LINKING; DELETION MUTANT; DIMERIZATION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; LEUKEMIA CELL; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN STRUCTURE;

BINDING SITES; CADHERINS; CELL ADHESION; CELL ADHESION MOLECULES; CELL MEMBRANE; CROSS-LINKING REAGENTS; CYTOPLASM; DIMERIZATION; HUMANS; K562 CELLS; PEPTIDES; PHOSPHOPROTEINS; SEQUENCE DELETION; TRANSFECTION; TUMOR CELLS, CULTURED;

EID: 0032555935     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.142.6.1605     Document Type: Article

References (58)

1. Aberle, H., S. Butz, J. Stappert, H. Weissig, R. Kemler, and H. Hoschuetzky. 1994. Assembly of the cadherin-catenin complex in vitro with recombinant proteins. J. Cell Sci. 107:3655-3663.
2. Angres, B., A. Barth, and W.J. Nelson. 1996. Mechanism for transition from initial to stable cell-cell adhesion: Kinetic analysis of E-cadherin-mediated adhesion using a quantitative adhesion assay. J. Cell Biol. 134:549-557.
3. Bixby, J.L., and R. Zhang. 1990. Purified N-cadherin is a potent substrate for rapid induction of neurite outgrowth. J. Cell Biol. 110:1253-1260.
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. cas binds directly to E-cadherin but not to the adenomatous polyposis coli protein or α-catenin. Mol. Cell. Biol. 14:8333-8342.
6. Gumbiner, B.M. 1996. Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell. 84:345-357.
7. Hinck, L., I.S. Näthke, J. Papkoff, and W.J. Nelson. 1994. Dynamics of cadherin/catenin complex formation: Novel protein interactions and pathways of complex assembly. J. Cell Biol. 125:1327-1340.
8. Hirano, S., A. Nose, K. Hatta, A. Kawakami, and M. Takeichi. 1987. Calcium-dependent cell-cell adhesion molecules (cadherins): Subclass specificities and possible involvement of actin bundles. J. Cell Biol. 105:2501-2510.
9. Hirano, S., N. Kimoto, Y. Shimoyama, S. Hirohashi, and M. Takeichi. 1992. Identification of a neural α-catenin as a key regulator of cadherin function and multicellular organization. Cell. 70:293-301.
10. Hülsken, J., W. Birchmeier, and J. Behrens. 1994. E-cadherin and APC compete for the interaction with β-catenin and the cytoskeleton. J. Cell Biol. 127: 2061-2069.
11. Hyafil, F., D. Morello, C. Babinet, and F. Jacob. 1980. A cell surface glycoprotein involved in the compaction of embryonal carcinoma cells and cleavage stage embryos. Cell. 21:927-934.
12. Itoh, M., A. Nagafuchi, S. Moroi, and S. Tsukita. 1997. Involvement of ZO-1 in cadherin-based cell adhesion through its direct binding to α catenin and actin filaments. J. Cell Biol. 138:181-192.
13. Jaffe, S.H., R.R. Friedlander, F. Matsuzaki, K.L. Crossin, B.A. Cunningham, and G.M. Edelman. 1990. Differential effects of the cytoplasmic domains of cell adhesion molecules on cell aggregation and sorting. Proc. Natl. Acad. Sci. USA. 87:3589-3593.
14. Jou, T.-S., D.B. Stewart, J. Stappert, W.J. Nelson, and J.A. Marrs. 1995. Genetic and biochemical dissection of protein linkages in the cadherin-catenin complex. Proc. Natl. Acad. Sci. USA. 92:5067-5071.
15. Kemler, R. 1993. From cadherins to catenins: cytoplasmic protein interactions and regulation of cell adhesion. Trends Genet. 9:317-321.
16. Kreft, B., D. Berndorf, A. Böttinger, S. Finnemann, D. Wedlich, M. Hortsch, R. Tauber, and R. Gessner. 1997. LI-cadherin-mediated cell-cell adhesion does not require cytoplasmic interactions. J. Cell Biol. 136:1109-1121.
17. Kinch, M.S., G.J. Clark, C.J. Der, and K. Burridge. 1995. Tyrosine phosphorylation regulates the adhesion of ras-transformed breast epithelia. J. Cell Biol. 130:461-471.
18. Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:680-685.
19. Lampugnani, M.G., M. Corada, P. Andriopoulou, S. Esser, W. Risau, and E. Dejana. 1997. Cell confluence regulates tyrosine phosphorylation of adherens junction components in endothelial cells. J. Cell Sci. 110:2065-2077.
20. Marrs, J.A., and W.J. Nelson. 1996. Cadherin cell adhesion molecules in differentiation and embryogenesis. Int. Rev. Cytol. 165:159-205.
21. Nagafuchi, A., and M. Takeichi.1988. Cell binding function of E-cadherin is regulated by the cytoplasmic domain. EMBO (Eur. Mol. Biol. Organ.) J. 7:3679-3684.
22. Nagafuchi, A., and M. Takeichi. 1989. Transmembrane control of cadherin-mediated cell adhesion: a 94 kDa protein functionally associated with a specific region of the cytoplasmic domain of E-cadherin. Cell Regul. 1:37-44.
23. Nagafuchi, A., S. Ishihara, and S. Tsukita. 1994. The roles of catenins in the cadherin-mediated cell adhesion: Functional analysis of E-cadherin-α catenin fusion molecules. J. Cell Biol. 127:235-245.
24. Nagar, B., M. Overduin, M. Ikura, and J.M. Rini. 1996. Structural basis of calcium-induced E-cadherin rigidification and dimerization. Nature. 380:360-364.
25. Navarro, P., L. Caveda, F. Breviario, I. Mandoteanu, M.-G. Lampugnani, and R. Dejana. 1995. Catenin-dependent and -independent function of vascular endothelial cadherin. J. Biol. Chem. 270:30965-30972.
26. Navarro, P., L. Ruco, and E. Dejana. 1998. Differential localization of VE-and N-cadherins in human endothelial cells: VE-cadherin competes with N-cadherin for junctional localization. J. Cell Biol. 140:1475-1484.
27. Nieset, J.E., A.R. Redfield, F. Jin, K.A. Knudsen, K.R. Johnson, and M.J. Wheelock. 1997. Characterization of the interactions of α-catenin with α-actinin and β-catenin/plakoglobin. J. Cell Sci. 110:1013-1022.
28. Niwa, H., K. Yamamura, and J. Miyazaki. 1991. Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene. 108:193-200.
29. Nose, A., A. Nagafuchi, and M. Takeichi. 1988. Expressed recombinant cadherins mediate cell sorting in model systems. Cell. 54:993-1001.
30. Nose, A., K. Tsuji, and M. Takeichi. 1990. Localization of specificity determining sites in cadherin cell adhesion molecules. Cell. 61:147-155.
31. Ozawa, M., and R. Kemler. 1992. Molecular organization of the uvomorulin-catenin complex. J. Cell Biol. 116:989-996.
32. Ozawa, M., and R. Kemler. 1998. Altered cell adhesion activity by pervanadate due to the dissociation of α-catenin from the E-cadherin-catenin complex. J. Biol. Chem. 273:6166-6170.
33. Ozawa, M., H. Baribault, and R. Kemler. 1989. The cytoplasmic domain of the cell adhesion molecule uvomorulin associates with three independent proteins structurally related in different species. EMBO (Eur. Mol. Biol. Organ.) J. 8:1711-1717.
34. Ozawa, M., M. Ringwald, and R. Kemler. 1990. Uvomorulin-catenin complex formation is regulated by a specific domain in the cytoplasmic region of the cell adhesion molecule. Proc. Natl. Acad. Sci. USA. 87:4246-4250.
35. Paradies, N.E., and G.B. Grunwald. 1993. Purification and characterization of NCAD90, a soluble endogenous form of N-cadherin, which is generated by proteolysis during retinal development and retains adhesive and neurite-promoting function. J. Neurosci. Res. 36:33-45.
36. Payne, H.R., and L. Lemmon. 1993. Glial cells of the O-2A lineage bind preferentially to N-cadherin and develop distinct morphologies. Dev. Biol. 159: 595-607.
37. v-src, is related to cadherin-binding factors, β-catenin, plakoglobin and armadillo. Oncogene. 7:2439-2445.
38. cas associates with E-cadherin complexes. Mol. Cell. Biol. 14:8333-8342.
39. 1(E)-Catenin is an actin-binding and -bundling protein mediating the attachment of F-actin to the membrane adhesion complex. Proc. Natl. Acad. Sci. USA. 92:8813-8817.
40. Roh, J.Y., and J.R. Stanley. 1995. Intracellular domain of desmoglein 3 (pemphigus vulgaris antigen) confers adhesive function on the extracellular domain of E-cadherin without binding catenins. J. Cell Biol. 128:939-947.
41. Salomon, D., O. Ayalon, R. Patel King, R.O. Hynes, and B. Geiger. 1992. Extrajunctional distribution of N-cadherin in cultured human endothelial cells. J. Cell Sci. 102:7-17.
42. Shapiro, L., A.M. Fannon, P.D. Kwong, A. Thompson, M.S. Lehmann, G. Grübel, J.-F. Legrand, J. Als-Neilsen, D.R. Colman, and W.A. Hendrickson. 1995. Structural basis of cell-cell adhesion by cadherins. Nature. 374:327-337.
43. Shibamoto, S., M. Hayakawa, K. Takeuchi, T. Hori, K. Miyazawa, N. Kitamura, K.R. Johnson, M.J. Wheelock, N. Matsuyoshi, M. Takeichi, and F. Ito. 1995. Association of p120, a tyrosine kinase substrate, with E-cadherin/catenin complexes. J. Cell Biol. 128:949-957.
44. Shimoyama, Y., A. Nagafuchi, S. Fujita, M. Gotoh, M. Takeichi, S. Tsukita, and S. Hirohashi. 1992. Cadherin dysfunction in a human cancer cell line: possible involvement of loss of α-catenin expression in reduced cell-cell adhesiveness. Cancer Res. 52:5770-5774.
45. Skoudy, A., M.D. Llosas, and A. Garcia de Herreros. 1996. Intestinal HT-29 cells with dysfunction of E-cadherin show increased pp60src activity and tyrosine phosphorylation of p120-catenin. Biochem. J. 317:279-284.
46. Staddon, J.M., C. Smales, C. Schulze, F.S. Esch, and L.L. Rubin. 1995. p120, a p120-related protein (p100), and the cadherin/catenin complex. J. Cell Biol. 130:369-381.
47. Stappert, J., and R. Kemler. 1994. A short core region of E-cadherin is essential for catenin binding and is highly phosphorylated. Cell Adhes. Commun. 2:319-327.
48. Surani, M.A.H., S.C. Barton, and A. Burling. 1990. Differentiation of 2-cell and 8-cell mouse embryos arrested by cytoskeletal inhibitors. Exp. Cell Res. 125: 275-286.
49. Suzuki, S., K. Sano, and H. Tanihara. 1991. Diversity of the cadherin family: evidence for eight new cadherins in nervous tissue. Cell Regul. 2:261-270.
50. Takeda, H., A. Nagafuchi, S. Yonemura, S. Tsukita, J. Behrens, W. Birchmeier, and S. Tsukita. 1995. V-src kinase shifts the cadherin-based cell adhesion from the strong to the weak state and β catenin is not required for the shift. J. Cell Biol. 131:1839-1847.
51. Takeichi, M. 1977. Functional correlation between cell adhesive properties and some cell surface proteins. J. Cell Biol. 75:464-474.
52. Takeichi, M. 1991. Cadherin cell adhesion receptors as a morphogenetic regulator. Science. 251:1451-1455.
53. 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 (Eur. Mol. Biol. Organ.) J. 15:3507-3514.
54. Vestal, D.J., and B. Ranscht. 1992. Glycosyl phosphatidylinositol-anchored T-cadherin mediates calcium-dependent, homophilic cell adhesion. J. Cell Biol. 119:451-461.
55. Vestweber, D., and R. Kemler. 1985. Identification of a putative cell adhesion domain of uvomorulin. EMBO (Eur. Mol. Biol. Organ.) J. 4:3393-3398.
56. Watabe, M., A. Nagafuchi, S. Tsukita, and M. Takeichi. 1994. Induction of polarized cell-cell association and retardation of growth by activation of the E-cadherin-catenin adhesion system in a dispersed carcinoma line. J. Cell Biol. 127:247-256.
57. Wheelock, M.J., C.A. Buck, K.B. Bechtol, and C.H. Damsky. 1987. Soluble 80-kd fragment of cell-CAM 120/80 disrupt cell-cell adhesion. J. Cell Biochem. 34:187-202.
58. 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.