Coexpression of both types of desmosomal cadherin and plakoglobin confers strong intercellular adhesion

Journal of Cell Science

Volumn 111, Issue 4, 1998, Pages 495-509

  Marcozzi, Cristiana ^a   Burdett, Ian D J ^a   Buxton, Roger S ^a   Magee, Anthony I ^a  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

Adhesion; Cadherin; Desmosome; Plakoglobin

Indexed keywords

CADHERIN; DESMOCOLLIN; DESMOGLEIN; DESMOPLAKIN; PLAKOGLOBIN;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL AGGREGATION; CELL CONTACT; CELL JUNCTION; DESMOSOME; L CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; CADHERINS; CELL ADHESION; CYTOSKELETAL PROTEINS; DESMOCOLLINS; DESMOGLEIN 1; DESMOGLEINS; DESMOPLAKINS; DESMOSOMES; GAMMA CATENIN; HUMANS; L CELLS (CELL LINE); MICE; TRANSFECTION;

ANIMALIA; ARMADILLO;

EID: 0031908049     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (75)

1. Amagai, M., Karpati, S., Klaus-Kovtun, V., Udey, M. C. and Stanley, J. R. (1994). Extracellular domain of pemphigus vulgaris antigen (desmoglein 3) mediates weak homophilic adhesion. J. Invest. Dermatol. 102, 402-408.
2. Amagai, M., Fujimori, T., Masunaga, T., Shimizu, H., Nishikawa, T., Shimizu, N., Takeichi, M. and Hashimoto, T. (1995). Delayed assembly of desmosomes in keratinocytes with disrupted classic-cadherin-mediated cell adhesion by a dominant negative mutant. J. Invest. Dermatol. 104, 27-32.
3. Arnemann, J., Sullivan, K. H., Magee, A. I., King, I. A. and Buxton, R. S. (1993). Stratification-related expression of isoforms of the desmosomal cadherins in human epidermis. J. Cell Sci. 104, 741-750.
4. Bornslaeger, E. A., Corcoran, C. M., Stappenbeck, T. S. and Green, K. J. (1996). Breaking the connection: displacement of the desmosomal plaque protein desmoplakin from cell-cell interfaces disrupts anchorage of intermediate filament bundles and alters intercellular junction assembly. J. Cell Biol. 134, 985-1001.
5. Burdett, I. D. J. (1993) Internalisation of desmosomes and their entry into the endocytic pathway via late endosomes in MDCK cells: possible mechanisms for the modulation of cell adhesion by desmosomes during development. J. Cell Sci. 106, 1115-1130.
6. Buxton, R. S. and Magee, A. I. (1992). Structure and interactions of desmosomal and other cadherins. Semin Cell Biol. 3, 157-167.
7. Buxton, R. S., Cowin, P., Franke, W. W., Garrod, D. R., Green, K. J., King, I. A., Koch, P. J., Magee, A. I., Rees, D. R., Stanley, J. R. and Steinberg, M. S. (1993). Nomenclature of the desmosomal cadherins J. Cell Biol. 121. 481-483.
8. Cartaud, A., Ludosky, M. A., Courvalin, J. C. and Cartaud, J. (1990) A protein antigenically related to nuclear lamin B mediates the association of intermediate filaments with desmosomes. J. Cell Biol. 111, 581-588.
9. Chen, C. and Okayama, H. (1987). High-efficiency transformation of mammalian cells by plasmid DNA. Mol. Cell. Biol. 7, 2745-2752.
10. Chidgey, M. A., Clarke, J. P. and Garrod, D. R. (1996). Expression of full-length desmosomal glycoproteins (desmocollins) is not sufficient to confer strong adhesion on transfected L929 cells. J. Invest. Dermatol. 106, 689-695.
11. Chitaev, N. A., Leube, R. E., Troyanovsky, R. B., Eshkind, L. G., Franke, W. W. and Troyanovsky, S. M. (1996). The binding of plakoglobin to desmosomal cadherins: patterns of binding sites and topogenic potential. J. Cell Biol. 133, 359-369.
12. 2+-dependent heterophilic interaction between desmosomal cadherins, desmoglein and desmocollin, contributes to cell-cell adhesion. J. Cell Biol. 138, 193-201
13. Cochran, W. G. (1977). Sampling Techniques London: J. Wiley & Sons. Ltd.
14. Cordingley, H. C. (1997) Investigation into the role of plakoglobin in Xenopus development. PhD thesis. London University.
15. Cowin, P. and Burke, B. (1996) Cytoskeleton-membrane interactions Curr. Opin Cell Biol. 8, 56-65.
16. Cowin, P., Kapprell, H. P., Franke, W. W., Tamkun, J. and Hynes, R. O. (1986). Plakoglobin: a protein common to different kinds of intercellular adhering junctions. Cell 46, 1063-1073.
17. Edelman, G. M., Murray, B. A., Mege, R. M., Cunningham, B. A. and Gallin, W. J. (1987). Cellular expression of liver and neural cell adhesion molecules after transfection with their cDNAs results in specific cell-cell binding. Proc: Nat. Acad. Sci. USA 84, 8502-8506.
18. Franke, W. W., Cowin, P., Schmelz, M. and Kapprell, H. P. (1987a) The desmosomal plaque and the cytoskeleton. Ciba Found. Symp. 125, 26-48.
19. Franke, W. W., Kapprell, H. P. and Cowin, P. (1987b). Immunolocalization of plakoglobin in endothelial junctions: identification as a special type of zonulae adhaerentes. Biol. Cell 59, 205-218.
20. Fujimori, T. and Takeichi, M. (1993). Disruption of epithelial cell-cell adhesion by exogenous expression of a mutated nonfunctional N-cudherin. Mol. Biol. Cell 4, 37-47.
21. Fujiwara, S., Kohno, K., Iwamatsu, A., Naito, I. and Shinkai, H. (1996) Identification of a 450 kDa human epidermal autoantigen as a new member of the plectin family. J. Invest. Dermatol. 106, 1125-1130.
22. Gache, Y., Chavanas, S., Lacour, J. P., Wiche, G., Owaribe, K., Meneguzzi, G. and Ortonne, J. P. (1996). Detective expression of plectin/HD1 in epidermolysis bullosa simplex with muscular dystrophy. J. Clin. Invest. 97, 2289-2298.
23. Garrod, D. R. and Fleming, S. (1990). Early expression of desmosomal components during kidney tubule morphogenesis in human and murine embryos. Development 108, 313-321.
24. Griffiths, G. (1993). Quantitative aspects of immunocytochemistry. In Fine Structure Immunocytochemistry. pp 371-445. Berlin-Heidelberg: Springer-Verlag.
25. Griffiths, G., Warren, G., Quinn, P., Mathieu-Costello, O. and Hoppeler, H. (1984). Density of newly synthesized proteins in intracellular membranes. I. Stereological studies. J. Cell Biol. 98, 2133-2141.
26. Hatzfeld, M., Kristjansson, G. I., Plessmann, U. and Weber, K. (1994). Band 6 protein, a major constituent of desmosomes from stratified epithelia. is a novel member of the armadillo multigene family. J. Cell Sci. 107, 2259-2270.
27. Heid, H. W., Schimdt, A., Zimbelmann, R., Schafer, S., Winter-Simanowski, S., Stumpp, S., Keith, M., Figge, U., Schnolzer, M. and Franke, W. W. (1994). Cell type-specific desmosomal plaque proteins of the plakoglobin family: plakophilin I (band 6 protein). Differentation 58, 113-131.
28. Hieda, Y., Tsukita, S. and Tsukita, S. (1989). A new high molecular mass protein showing unique localization in desmosomal plaques. J. Cell Biol. 109, 1511-1518.
29. Horiguchi, Y., Furukawa, F., Fujita, M. and Imamura, S. (1994). Ulrastructural localization of E-cadherin cell adhesion molecule on the cytoplasmic membrane of keratinocytes in vivo and in vitro. J. Histochem Cytochem. 42, 1333-1340.
30. Jones, J. C. (1988). Characterization of a 125K glycoprotein associated with bovine epithelial desmosomes. J. Cell Sci. 89, 207-216.
31. Kapprell, H. P., Cowin, P. and Franke, W. W. (1987). Biochemical characterization of the soluble form of the junctional plaque protein. plakoglobin, from different cell types. Eur. J. Biochem. 166, 505-517.
32. 2+-dependent cell adhesion molecule. BioEssays 11, 88-91.
33. King, I. A., Tabiowo, A., Purkis, P., Leigh, I. and Magee, A. I. (1993) Expression of distinct desmocollin isoforms in human epidermis. J. Invent. Dermatol. 100, 373-379.
34. King, I. A., Sullivan, K. H., Bennett, R. J. and Buxton, R. S. (1995) The desmocollins of human foreskin epidermis: identification and chromosomal assignment of a third gene and expression patterns of the three isoforms. J. Invest. Dermatol. 105, 314-321.
35. King, I. A., Angst, B. D., Hunt, D. M., Kruger, M., Arnemann, J. and Buxton, R. S. (1997). Hierarchical expression of desmosomal cadherins during stratified epithelial morphogenesis in the mouse. Differentiation 62, 83-96.
36. Koch, P. J. and Franke, W. W. (1994). Desmosomal cadherins: another growing multigene family of adhesion molecules. Curr Opin Cell Biol. 6, 682-687.
37. Korman, N. J., Eyre, R. W., Klaus-Kovtun, V. and Stanley, J. R. (1989). Demonstration of an adhering-junction molecule (plakoglobin) in the autoantigens of pemphigus foliaceous and pemphigus vulgaris. New Engl. J. Med. 321, 631-635
38. Kouklis, P. D., Hutton, E. and Fuchs, E. (1994). Making a connection: direct binding between keratin intermediate filaments and desmosomal proteins. J. Cell Biol. 127, 1049-1060.
39. Kowalczyk, A. P., Palka, H. L., Luu, H. H., Nilles. L. A., Anderson, J. E., Wheelock, M. J. and Green, K. J. (1994). Posttranslational regulation of plakoglobin expression - influence of the desmosomal cadherins on plakoglobin metabolic stability. J. Biol. Chem. 269, 31214-31223.
40. Kowalczyk, A. P., Borgwardt, J. E. and Green, K. J. (1996). Analysis of desmosomal cadherin adhesive function and stoichiometry of desmosomal cadherin-plakoglobin complexes. J. Invest. Dermatol. 107, 293-300.
41. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
42. Legan, P. K., Collins, J. E. and Garrod, D. R. (1992). The molecular biology of desmosomes and hemidesmosomes: 'what's in a name'? BioEssay. 14, 385-393.
43. Legan, P. K., Yue, K. K. M., Chidgey, M. A. J., Holton, J. L., Wilkinson, R. W. and Garrod, D. R. (1994). The bovine desmocollin family: a new gene and expression patterns reflecting epithelial cell proliferation and differentiation. J. Cell Biol. 126, 507-518.
44. Lewis, J. E., Wahl, J. K. III, Sass, K. M., Jensen, P. J., Johnson, K. R. and Wheelock, M. J. (1997). Cross-talk between adherens junctions and desmosomes depends on plakoglobin. J. Cell Biol. 136, 919-934.
45. Li, Z., Colucci-Guyon, E., Pincon-Raymond, M., Mericskay, M., Pournin, S., Paulin, D. and Babinet, C. (1996). Cardiovascular lesions and skeletal myopathy in mice lacking desmin. Dev. Biol. 175, 362-366.
46. Liu, C. G., Maercker, C., Castanon, M. J., Hauptmann, R. and Wiche, G. (1996). Human plectin: organization of the gene, sequence analysis, and chromosome localization (8q24). Proc. Nut. Acad. Sci. USA 93, 4278-4283.
47. Magee, A. I. and Buxton, R. S. (1991). Transmembrane molecular assemblies regulated by the greater cadherin family. Curr. Opin. Cell Biol. 3, 854-861.
48. Mathur, M., Goodwin, L. and Cowin, P. (1994) Interactions of the cytoplasmic domain of the desmosomal cadherin Dsg1 with plakoglobin. J. Biol. Chem. 269, 14075-14080.
49. Nagafuchi, A. and Takeichi, M. (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.
50. Nagafuchi, A., Shirayoshi, Y., Okazaki, K., Yasuda, K. and Takeichi, M. (1987). Transformation of cell adhesion properties by exogenously introduced E-cadherin cDNA future 329, 341-343.
51. Nagar, B., Overduin, M., Ikura, M. and Rini, J. M. (1996) Structural basis of calcium-induced E-cadherin Modification and dimerization. Nuture 380, 360-364.
52. Nose, A., Nagafuchi, A. and Takeichi, M. (1988). Expressed recombinant cadherins mediate cell sorting in model systems. Cell 54, 993-1001.
53. Nuber, U. A., Shafer, S., Schmidt, A., Koch, P. J. and Franke, W. W. (1995). The widespread human desmocollin Dsc2 and tissue-specific patterns of synthesis of various desmocollin subtypes. Eur. J. Cell Biol. 66, 69-74.
54. Ozawa, M. and Kemler, R. (1992). Molecular organization of the uvomorulin-catenin complex. J. Cell Biol. 116, 989-996.
55. Ozawa, M., Ringwald, M. and Kemler, R. (1990). Uvomorulin-catenin complex formation is regulated by a specific domain in the cytoplasmic region of the cell adhesion molecule. Proc. Nat. Acad Sci. USA 87, 4246-4250.
56. Parker, A. E., Wheeler, G. N., Arnemann, J., Pidsley, S. C., Ataliotis, P., Thomas, C. L., Rees, D. A., Magee, A. I. and Buxton, R. S. (1991) Desmosomal glycoproterins II and III: cadherin-like junctional molecules generated by alternative splicing. J. Biol. Chem. 266, 10438-10445
57. Roh, J.-Y. and Stanley, J. R. (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.
58. Rose, O., Grund, C., Reinhardt, S., Starzinski-Powitz, A. and Franke, W. W. (1995). Contactus adherens, a special type of plaque-bearing adhering junction containing M-cadherin, in the granule cell layer of the cerebellar glomerulus. Proc. Nat. Acat. Sci. USA 92, 6022-6026.
59. Rugg, E. L., McLean, W. H. I., Lane, E. B., Pitera, R., McMillan, J. R., Dopping-Hepenstal, P. J. C., Navsaria, H. A., Leigh, I. M. and Eady. R. A. J. (1994). A functional 'knockout' of human keratin 14. Genes. Dev. 8. 2563-2573.
60. Schmidt, A., Heid, H. W., Schafer, S., Nuber, U. A., Zimbelmann, R. and Franke, W. W. (1994). Desmosomes and cytoskeletal architecture in epithelial differentiation: cell type-specific plaque components and intermediate filament anchorage. Eur: J. Cell Boil. 65, 229-245.
61. Shapiro, L., Fannon, A. M., Kwong, P. D., Thompson, A., Lehmann, M. S., Grubel, G., Legrand, J. F., Alsnielsen, J., Colman, D. R. and Hendrickson. W. A. (1995) Structural basis of cell-cell adhesion by cadherins. Nature 374, 327-337.
62. Skalli, O., Jones, J. C. R., Gagescu, R. and Goldman, R. D. (1494) IFAP-300 is common to desmosomes and hemidesmosomes and is a possible linker of intermediate filaments ID these junctions. J. Cell Biol. 125, 159-170.
63. Small, J. V. (1968). Measurements of section thickness. In Proc. 4th European Congress on Electron Microscops. vol. 1 (ed. D. S. Bocciarelli). pp. 609-610 Roma: Tipografia Poliglotta Vaticana.
64. Stappenbeck, T. S. and Green, K. J. (1992). The desmoplakin carboxyl terminus coaligns with and specifically disrupts intermediate filament networks when expressed in cultured cells. J. Cell Biol. 116, 1197- 1209.
65. Stappenbeck, T. S., Bornslaegcr, E. A., Corcoran, C. M., Luu, H. H., Virata, M. L. A. and Green, K. J. (1993). Functional analysis of desmoplakin domains: specification ot the interaction with keratin versus vimentin intermediate filament networks. J. Cell Biol. 123, 691-705.
66. Takeichi, M. (1977). Functional correlation between cell adhesive properties and some cell surface proteins. J. Cell Biol 75, 464-474.
67. Troyanovsky, S. M., Eshkind. L. G., Troyanovsky, R. B., Leube, R. E. and Franke, W. W. (1993). Contributions of cytoplasmic domains of desmosomal cadherins to desmosome assembly and intermediate filament anchorage. Cell 72, 561-574.
68. Troyanovskv, S. M., Troyanovsky, R. B., Eshkind, L. G., Krutovskikh. V. A., Leube, R. K. and Franke, W. W. (1994). Identification of the plakoglobin-binding domain in desmoglein and its role in plaque assembly and intermediate filament anchorage J. Cell Biol. 127, 151-160.
69. Troyanovsky, S. M., Troyanovsky, R. B., Eshkind. L. G., Leube, R. E. and Franke, W. W. (1994b). Identification of amino acid sequence motifs in desmocollin a desmosomal glycoprotein, that are required for plakoglobin binding and plaque formation. Proc. Nat. Acad. Sci. USA 91. 10790-10704.
70. Tsukita, S. and Tsukita, S. (1985). Desmoculmin: a calmodulin-binding high molecular weight protein isolated from desmosomes. J. Cell Biol. 101. 2070-2080.
71. Wahl, J. K., Sacco, P. A., McGranahan-Sadler, T. M., Sauppe, L. M., Wheelock, M. J. and Johnson, K. R. (1996). Plakoglobin domains that define its association with the desmosomal cadherins and the classical cadherins: identification of unique and shared domains. J. Cell Sci. 109. 1143-1154.
72. Weibel, E. R. (1979). Stereological methods. Practical Methods for Biological Morphometry vol 1. London. Academic Press.
73. Wheeler, G. N., Buxton, R. S., Parker, A. E., Arnemann, J., Rees, D. A., King, I. A. and Magee, A. I. (1991a). Desmosomal glycoproteins I. II and III: novel members of the cadherin superfamily. Biochem. Soc. Trans. 19. 1060-1064.
74. Wheeler. G. N., Parker, A. E., Thomas, C. L., Ataliotis, P., Poynter, D., Arnemann, J., Rutman, A. J., Pidsley, S. C., Watt, K. M., Rees, D. A., Buxton, R. S. and Magee, A. I. (1991b). Desmosomal glycoprotin I. a component of intercellular desmosome junctions is related to the cadherin family of cell adhesion molecules. Proc. Nat. Acat. Sci. USA 88, 4796-4800.
75. Witcher, L. L., Collins, R., Puttagunta, S., Mechanic, S. E., Munson, M., Gumbiner, B. and Cowin, P. (1996). Desmosomal cadherin binding domains ot plakoglobin. J. Biol. Chem. 271, 10904-10909.