VE-cadherin and desmoplakin are assembled into dermal microvascular endothelial intercellular junctions: A pivotal role for plakoglobin in the recruitment of desmoplakin to intercellular junctions

Journal of Cell Science

Volumn 111, Issue 20, 1998, Pages 3045-3057

  Kowalczyk, Andrew P ^a,c   Navarro, Pilar ^b   Dejana, Elisabetta ^b   Bornslaeger, Elayne A ^a   Green, Kathleen J ^a   Kopp, Daniel S ^a   Borgwardt, Jeffrey E ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Adhesion; Catenin; Cytoskeleton; Vimentin

Indexed keywords

BETA CATENIN; CADHERIN; DESMOPLAKIN; PLAKOGLOBIN;

ANIMAL CELL; ARTICLE; CELL JUNCTION; FIBROBLAST; HUMAN; HUMAN CELL; INTERMEDIATE FILAMENT; MOUSE; NONHUMAN; PRIORITY JOURNAL; VASCULAR ENDOTHELIUM;

ANIMALS; ANTIGENS, CD; CADHERINS; CELLS, CULTURED; COS CELLS; CYTOSKELETAL PROTEINS; CYTOSKELETON; DESMOPLAKINS; ENDOTHELIUM, VASCULAR; FORSKOLIN; GAMMA CATENIN; HUMANS; IMMUNOGLOBULIN G; INTERCELLULAR JUNCTIONS; INTERMEDIATE FILAMENTS; L CELLS (CELL LINE); MICE; MODELS, BIOLOGICAL; RECOMBINANT PROTEINS; TRANSFECTION;

ANIMALIA;

EID: 0031771007     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (69)

1. Aberle, H., Butz, S., Stappert, J., Weissig, H., Kemler, R. and Hoschuctzky, H. (1994). Assembly of the cadherin-catenin complex in vitro with recombinant proteins. J. Cell Sci. 107, 3655-3663.
2. Albelda, S. M., Muller, W. A., Buck, C. A. and Newman, P. J. (1991). Molecular and cellular properties of PECAM-1 (endoCAM/CD31): A novel vascular cell-cell adhesion molecule. J. Cell Biol. 114, 1059-1068.
3. Ali, J., Liao, F., Martens, E. and Muller, W. A. (1997). Vascular endothelial cadherin (VE-cadherin): cloning and role in endothelial cell-cell adhesion. Microcirculation 4, 267-277.
4. Angst, B. D., Nilles, L. A. and Green, K. J. (1990). Desmoplakin II expression is not restricted to stratified epithelia. J. Cell Sci. 97, 247-257.
5. Bach, T. L., Barsigian, C., Chalupowicz, D. G., Busier, D., Yaen, C. H., Grant, D. S. and Martinez, J. (1998). VE-cadherin mediates endothelial cell capillary tube formation in fibrin and collagen gels. Exp. Cell Res. 238, 324-334.
6. Bai, C. and Elledge, S. J. (1995). Cloning using the two-hybrid system. Meth. Enzymol. 273, 331-347.
7. Barth, A. I., Nathke, I. S. and Nelson, W. J. (1997). Cadherins, catenins and APC protein: interplay between cytoskeletal complexes and signaling pathways. Curr. Opin. Cell Biol. 9, 683-690.
8. 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.
9. Breviario, F., Caveda, L., Corada, M., Martin-Padura, I., Navarro, P., Golay, J., Introna, M., Gulino, D., Lampugnani, M. G. and Dejana, E. (1995). Functional properties of human vascular endothelial cadherin (7B4/Cadherin-5), an endotheliurn-specific cadherin. Arterioscler. Thromb. Vasc. Biol. 15, 1229-1239.
10. Coulombe, P. A. and Fuchs, E. (1994). Molecular mechanisms of keratin gene disorders and other bullous diseases of the skin. In Molecular Mechanisms of Epithelial Cell Junctions: from Development to Disease (ed. S. Citi), pp. 259-285. Austin: R. G. Landes Co.
11. Cowin, P., Kapprell, H., Franke, W. W., Tamkun, J. W. and Hynes, R. O. (1986). Plakoglobin: A protein common to different kinds of intercellular adhering junctions. Cell 46, 1063-1073.
12. Cowin, P. and Mechanic, S. (1994). Desmosomal cadherins and their cytoplasmic interactions. In Molecular Mechanisms of Epithelial Cell Junctions: from Development to Disease (ed. S. Citi), pp. 141-155. Austin: R. G. Landes Co.
13. Cowin, P. and Burke, B. (1996). Cytoskeleton-membrane interactions. Curr. Opin. Cell Biol. 8, 56-65.
14. Dejana, E., Corada, M. and Lampugnani, M. G. (1995). Endothelial cell-cell junctions. FASEB J. 9, 910-918.
15. Dejana, E. (1996). Endothelial adherens junctions: implications in the control of vascular permeability and angiogenesis. J. Clin. Invest. 98, 1949-1953.
16. Fuchs, E. (1994). Intermediate filaments and disease: mutations that cripple cell strength. J. Cell Biol 125, 511-516.
17. Fuchs, E. and Cleveland, D. W. (1998). A structural scaffolding of intermediate filaments in health and disease. Science 279, 514-519.
18. Garrod, D., Chidgey, M. and North, A. (1996). Desmosomes: differentiation, development, dynamics and disease. Curr. Opin. Cell Biol. 8, 670-678.
19. Green, K. J. and Jones, J. C. R. (1996). Desmosomes and hemidesmosomes: structure and function of molecular components. FASEB J. 10, 871-881.
20. Green, K. J., Bornslaeger, E. A., Kowalczyk, A. P., Palka, H. L. and Norvell, S. M (1997). Specificity of desmosomal plaque protein interactions with intermediate filaments: keeping adhesive junctions segregated. J. Gen. Physiol. 52, 123-139.
21. Harper, J. W., Adami, G., Wei, N., Keyomarsi, K. and Elledge, S. J. (1993). The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell 75, 805-816.
22. Herrenknecht, K., Ozawa, M., Eckerskorn, C., Lottspeich, F., Lenter, M. and Kemler, R. (1991). The uvomorulin-anchorage protein alpha catenin is a vinculin homologue. Proc. Nat. Acad. Sci. USA 88, 9156-9160.
23. Hinck, L., Nelson, W. J. and Papkoff, J. (1994). Wnt-1 modulates cell-cell adhesion in mammalian cells by stabilizing β-catenin binding to the cell adhesion protein cadherin. J. Cell Biol. 124, 729-741.
24. Huber, O., Krohn, M. and Kemler, R. (1997). A specific domain in α-catenin medites binding to β-catenin or plakoglobin. J. Cell Sci. 110, 1759-1765.
25. Jou, T.-S., Stewart, D. B., Stappert, J., Nelson, W. J. and Marrs, J. A. (1995). Genetic and biochemical dissection of protein linkages in the cadherin-catenin complex. Proc. Nat. Acad. Sci USA 92, 5067-5071.
26. Klymkowsky, M. W. and Parr, B. (1995). The body language of cells: The intimate connection between cell adhesion and behavior. Cell 83, 5-8.
27. Knudsen, K. A. and Wheelock, M. J. (1992). Plakoglobin, or an 83-kD homologue distinct from β-catenin. interacts with E-cadherin and N-cadherin. J. Cell Biol. 118, 671-679.
28. Knudsen, K. A., Soler, A. P., Johnson, K. R. and Wheelock, M. J. (1995). Interaction of α-actinin with the cadherin/catenin cell-cell adhesion complex via α-catenin. J. Cell Biol. 130, 67-77.
29. 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.
30. 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.
31. Kowalczyk, A. P., Borgwardt, J. E. and Green, K. J. (1996). Analysis of desmosomal cadherin adhesive function and stoichiometry of the desmosomal cadherin:plakoglobin complex. J. Invest. Dermatol. 107, 293-300.
32. Kowalczyk, A. P. and Green, K. J. (1996). The desmosome: A component system for adhesion and intermediate filament attachment. In Current Topics in Membranes (ed. W. J. Nelson), pp. 187-209. San Diego: Academic Press. Inc.
33. Kowalczyk, A. P., Bornslaeger, E. A., Borgwardt, J. E., Palka, H. L., Dhaliwal, A. S., Corcoran, C. M., Denning, M. F. and Green, K. J. (1997). The amino-terminal domain of desmoplakin binds to plakoglobin and clusters desmosomal cadherin-plakoglobin complexes. J. Cell Biol. 139, 773-784.
34. Lampugnani, M. G., Corada, M., Caveda, L., Breviario, F., Ayalon, O., Geier, B. and Dejana, E. (1995). The molecular organization of endothelial cell-cell junctions: Differential association of plakoglobin. β-catenin. and α-catenin with vascular endothelial cadherin (VE-cadherin). J. Cell Biol. 129, 203-217.
35. Lampugnani, M. G. and Dejana, E. (1997). Interendothelial junctions: structure, signaling and functional roles. Curr. Opin. Cell Biol. 9, 674-682.
36. Lum, H. and Malik, A. B. (1996). Mechanisms of increased endothelial permeability. Can. J. Physiol. Pharmacol. 74, 787-800.
37. 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.
38. Matsumura, T., Wolff, K. and Petzelbauer, P. (1997). Endothelial cell tube formation depends on cadherin-5 and CD31 interactions with filamentous actin. J. Immunol. 158, 3408-3416.
39. Meng, J.-J., Bornslaeger, E. A., Green, K. J., Steinert, P. M. and Ip, W. (1997). Two-hybrid analysis reveals fundamental differences in direct interactions between desmoplakin and cell type-specific intermediate filaments. J. Biol. Chem. 272, 21495-21503.
40. Minnear, F. L., DeMichele, M. A., Moon, D. G., Reider, C. L. and Fenton II, J. W. (1989). Isoproterenol reduces thrombin-inuuced pulmonary endothelial permeability in vitro. Am. J. Physiol. 257, h1613-h1623
41. Nagafuchi, A., Takeichi, M. and Tsukita, S. (1991). The 102kd cadherin-associated protein: similarity to vinculin and postranscriptional regulation of expression. Cell 65, 849-857.
42. Navarro, P., Caveda, L., Breviario, F., Mandoteanu, I., Lampugnani, M. G. and Dejana, E. (1995). Catenin-dependent and -independent functions of vascular endothelial cadherin. J. Biol. Chem. 52, 30965-30972.
43. Navarro, P., Ruco, L. and Dejana, E. (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.
44. Newman, P. J., Berndt, M. C., Gorski, J., White II, G. C., Lyman, S., Paddock, C. and Muller, W. A. (1990). PECAM-1 (CD-31) cloning and relation to adhesion molecules of the immunoglobulin gene superfamily. Science 247, 1219-1222.
45. Newman, P. J. (1997). The biology of PECAM-1. J. Clin. Invest. 99, 3-8.
46. Nieset, J. E., Redfield, A. R., Jin, F., Knudsen, K. A., Johnson, K. R. and Wheelock, M. J. (1997). Characterization of the interactions of α-catenin with α-actinin and β-catenin/plakoglobin. J. Cell Sci. 110, 1013-1022.
47. Norvell, S. M. and Green, K. J. (1998). Contributions of extracellular and intracellular domains of full length and chimeric cadherin molecules to junction assembly in epithelial cells. J. Cell Sci. 111, 1305-1318.
48. Obama, H. and Ozawa, M. (1997). Identification of the domain of α-catenin involved in its association with β-catenin and plakoglobin (γ-catenin). J. Biol. Chem. 272, 11017-11020.
49. Ozawa, M., Baribault, H. and Kemler, R. (1989). The cytoplasmic domain of the cell adhesion molecule uvomorulin associates with three independent proteins structurally related in different species. EMBO J. 8, 1711-1717.
50. Ozawa, M. and Kemler, R. (1992). Molecular organization of the uvomorulin-catenin complex. J. Cell Biol. 116, 989-996.
51. Palka, H. L. and Green, K. J. (1997). Roles of plakoglobin end domains in desmosome assembly. J. Cell Sci. 110, 2359-2371.
52. Plott, R. T., Amagai, M., Udey, M. C. and Stanley, J. R. (1994). Pemphigus vulgaris antigen lacks biochemical properties characteristic of classical cadherins. J. Invest. Dermatol. 103, 168-172.
53. Rinm, D. L., Koslov, E. R., Kebriaei, P., Cianci, C. D. and Morrow, J. S. (1995). α (E)-catenin is an actin-binding and -bundling protein mediating the attachment of F-actin to the membrane adhesion complex. Proc. Nat. Acad. Sci USA 92, 8813-8817.
54. Roh, J.-Y. and Stanley, J. R. (1995). Plakoglobin binding by human Dsg3 (pemphigus vulgaris antigen) in keratinocytes requires the cadherin-like intracytoplasmic segment. J. Invest. Dermatol. 104, 720-724.
55. Savion, N., Vlodavsky, I., Greenburg, G. and Gospodarowicz, D. (1982). Synthesis and distribution of cytoskeletal elements in endothelial cells as a function of cell growth and organization. J. Cell Physiol. 110, 129-141.
56. Schmelz, M. and Franke, W. W. (1993). Complexus adhaerentes, a new group of desmoplakin-containing junctions in endothelial cells: the syndesmos connecting retothelial cells of lymph nodes. Eur. J. Cell Biol. 61, 274-289.
57. Schmelz, M., Moll, R., Kuhn, C. and Franke, W. W. (1994). Complexus adhaerentes, a new group of desmoplakin-containing junctions in endothelial cells: II. Different types of lymphatic vessels. Differentiation 57, 97-117.
58. Schnittler, H.-J., Puschel, B. and Drenckhahn, D. (1997). Role of cadherins and plakoglobin in interendothelial adhesion under resting conditions and shear stress. Am. J. Physiol. 273, H2396-H2405
59. Smith, E. A. and Fuchs, E. (1998). Defining the interactions between intermediate filaments and desmosomes. J. Cell Biol. 141, 1229-1241.
60. 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.
61. Stappenbeck, T. S., Bornslaeger, E. A., Corcoran, C. M., Luu, H. H., Virata, M. L. A. and Green, K. J. (1993). Functional analysis of desmoplakin domains: Specification of the interaction with keratin versus vimentin intermediate filament networks. J. Cell Biol. 123, 691-705.
62. Stappenbeck, T. S., Lamb, J. A., Corcoran, C. M. and Green, K. J. (1994). Phosphorylation of the desmoplakin COOH terminus negatively regulates its interaction with keratin intermediate filament networks. J. Biol. Chem. 269, 29351-29354.
63. Stasek, J. E. Jr, Patterson, C. E. and Garcia, J. G. (1992). Protein kinase C phosphorylates caldesmon77 and vimentin and enhances albumin permeability across cultured bovine pulmonary artery endothelial cell monolayers. J. Cell Physiol. 153, 62-75.
64. Steinert, P. M. and Bale, S. J. (1993). Genetic skin diseases caused by mutations in keratin intermediate filaments. Trends Genet. 9, 280-284.
65. Tanihara, H., Kido, M., Obata, S., Heimark, R. L., Davidson, M., St John, T. and Suzuki, S. (1994). Characterization of cadherin-4 and cadherin-5 reveals new aspects of cadherins. J. Cell Sci. 107, 1694-1704.
66. Telo, P., Breviario, F., Huber, P., Panzeri, C. and Dejana, E. (1998). Identification of a novel cadherin (vascular endothelial cadherin-2) located at intercellular junctions in endothelial cells. J. Biol. Chem. 273, 17565-17572.
67. Valiron, O., Chevier, V., Usson, Y., Breviario, F., Job, D. and Dejana, E. (1996). Desmoplakin expression and organization at human umbilical vein endothelial cell-cell junctions. J. Cell Sci. 109, 2141-2149.
68. van Hinsbergh, V. W. M. (1997). Endothelial permeability for macromolecules. Arterioscler. Thromb. Vasc. Biol. 17, 1018-1023.
69. Vittet, D., Buchou, T., Schweitzer, A., Dejana, E. and Huber, P. (1997). Targetted null-mutation in the vascular endothelial-cadherin gene impairs the organization of vascular-like structures in embryoid bodies. Proc. Nat. Acad. Sci. USA 94, 6273-6278.