Involvement of ZO-1 in cadherin-based cell adhesion through its direct binding to α catenin and actin filaments

Journal of Cell Biology

Volumn 138, Issue 1, 1997, Pages 181-192

  Itoh, Masahiko ^a   Nagafuchi, Akira ^a   Moroi, Seiji ^a   Tsukita, Shoichiro ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ALPHA CATENIN; CADHERIN; CELL MEMBRANE PROTEIN;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; CELL ADHESION; CELL MEMBRANE; CONTROLLED STUDY; IMMUNOFLUORESCENCE MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN PROTEIN INTERACTION; STRUCTURE ACTIVITY RELATION;

ACTINS; ALPHA CATENIN; ANIMALS; BETA CATENIN; CADHERINS; CELL ADHESION; CELL LINE; CYTOSKELETAL PROTEINS; L CELLS (CELL LINE); MEMBRANE PROTEINS; MICE; PHOSPHOPROTEINS; RATS; RECOMBINANT FUSION PROTEINS; SPODOPTERA; TRANS-ACTIVATORS;

ANIMALIA; INSECTA; UNIDENTIFIED BACULOVIRUS;

EID: 0030748548     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.138.1.181     Document Type: Article

References (69)

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. Anderson, J.M. 1995. Zonula occludens (ZO)-1 and ZO-2: membrane-associated guanylate kinase homologues (MAGUKs) of the tight junction. Biochem. Soc. Trans. 23:470-475.
3. Anderson, J.M., B.R. Stevenson, L.A. Jesaitis, D.A. Goodenough, and M.S. Mooseker, 1988. Characterization of ZO-1, a protein component of the tight junction from mouse liver and Madin-Darby canine kidney cells. J. Cell Biol. 106:1141-1149.
4. Ando-Akatsuka, Y., M. Saitou, T. Hirase, M. Kishi, A. Sakakibara, M. Itoh, S. Yonemura, M. Furuse, and Sh. Tsukita. 1996. Interspecies diversity of the occludin sequence: cDNA cloning of human, mouse, dog, and rat-kangaroo homologues. J. Cell Biol. 133:43-47.
5. Behrens, J., J.P. von Kries, M. Kuhl, L. Bruhn, D. Wedlich, R. Grosschedl, and W. Birchmeier. 1996. Functional interaction of β-catenin with the transcription factor LEF-1. Nature (Lond.). 382:638-642.
6. Birchmeier, W. 1995. E-cadherin as a tumor (invasion) suppresser gene. Bioessays. 17:97-99.
7. Boller, K., D. Vestweber, and R. Kemler. 1985. Cell-adhesion molecule uvomorulin is localized in the intermediate junctions of adult intestinal epithelial cells. J. Cell Biol. 100:327-332.
8. Citi, S., H. Sabanay, R. Jakes, B. Geiger, and J. Kendrick-Jones. 1988. Cingulin, a new peripheral component of tight junctions. Nature (Lond.). 33:272-276.
9. Farquhar, M.G.,and G.E. Palade. 1963. Junctional complexes in various epithelia. J. Cell Biol. 17:375-409.
10. Funayama, N., F. Fagotto, P. McCrea, and B.M. Gumbiner. 1995. Embryonic axis induction by the armadillo repeat domain of β-catenin: evidence for intracellular signaling. J. Cell Biol. 128:959-968.
11. Furuse, M., T. Hirase, M. Itoh, A. Nagafuchi, S. Yonemura, Sa. Tsukita, and Sh. Tsukita. 1993. Occludin: a novel integral membrane protein localizing at tight junctions. J. Cell Biol. 123:1777-1788.
12. Furuse, M., M. Itoh, T. Hirase, A. Nagafuchi, S. Yonemura, Sa. Tsukita, and Sh. Tsukita. 1994. Direct association of occludin with ZO-1 and its possible involvement in the localization of occludin at tight junctions. J. Cell Biol. 127: 1617-1626.
13. Gottardi, C.J., M. Arpin, A.S. Fanning, and D. Louvard. 1996. The junction-associated protein, zonula occludens-1, localizes to the nucleus before the maturation and during the remodeling of cell-cell contacts. Proc. Natl. Acad. Sci. USA. 93:10779-10784.
14. Gumbiner, B. 1987. Structure, biochemistry, and assembly of epithelial tight junctions. Am. J. Physiol. 253:C749-C758.
15. Gumbiner, B. 1993, Breaking through the tight junction barrier. J. Cell Biol. 123:1631-1633.
16. Gumbiner, B. 1995. Signal transduction by β-catenin. Curr. Opin. Cell Biol. 7: 634-640.
17. Gumbiner, B., B. Stevenson, and A. Grimaldi. 1988. The role of the cell adhesion molecule uvomorulin in the formation and maintenance of the epithelial junctional complex. J. Cell Biol. 107:1575-1587.
18. Gumbiner, B., T. Lowenkopf, and D. Apatira. 1991. Identification of a 160-kDa polypeptide that binds to the tight junction protein ZO-1. Proc. Natl. Acad. Sci. USA. 88:3460-3464.
19. Heaysman, J.E., and S.M. Pegrum. 1973. Early contacts between fibroblasts. Exp. Cell Res. 78:71-78.
20. Herrenknecht, K., M. Ozawa, C. Eckerskorn, F. Lottspeich, M. Lenter, and R. Kemler. 1991. The uvomorulin-anchorage protein α-catenin is a vinculin homologue. Proc. Natl. Acad. Sci. USA. 88:9156-9160.
21. 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.
22. 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.
23. Hirao, M., N. Sato, T. Kondo, S. Yonemura, M. Monden, T. Sasaki, Y. Takai, Sh. Tsukita, and Sa. Tsukita. 1996. Regulation mechanism of ERM protein/ plasma membrane association: possible involvement of phosphatidylinositol turnover and rho-dependent signaling pathway. J. Cell Biol. 135:37-52.
24. Honig, M.B., and R.I. Hume. 1986. Fluorescent carbocyanine dyes allow living neurons of identified origin to be studied in long-term cultures. J. Cell Biol. 103:171-187.
25. Huber, O., R. Korn, J. McLaughlin, M. Ohsugi, B.G. Herrmann, and R. Kemler. 1996. Nuclear localization of β-catenin by interaction with transcription factor LEF-1. Mech. Dev. 59:3-10.
26. Itoh, M., S. Yonemura, A. Nagafuchi, Sa. Tsukita, and Sh. Tsukita, 1991. A 220-kD undercoat-constitutive protein: its specific localization at cadherin-based cell-cell adhesion sites. J. Cell Biol. 115:1449-1462.
27. Itoh, M., A. Nagafuchi, S. Yonemura, T. Kitani-Yasuda, Sa. Tsukita, and Sh. Tsukita. 1993. The 220-kD protein colocalizing with cadherins in non-epithelial cells is identical to ZO-1, a tight junction-associated protein in epithelial cells: cDNA cloning and immunoelectron microscopy. J. Cell Biol. 121:491-502.
28. Jesaitis, L.A., and D.A. Goodenough. 1994. Molecular characterization and tissue distribution of ZO-2, a tight junction protein homologous to ZO-1 and the Drosophila discs-large tumor suppresser protein. J. Cell Biol. 124:949-961.
29. Jou, T.S., D.B. Stewart, J. Stappart, 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. 9295:5067-5071.
30. Kemler, R. 1992. Classical cadherins. Semin. Cell Biol. 3:149-155.
31. Keon, B.H., S. Schäfer, C. Kuhn, C. Grund, and W.W. Franke. 1996. Symplekin, a novel type of tight junction plaque protein. J. Cell Biol. 134:1003-1018.
32. Kim, S.K. 1995. Tight junctions, membrane-associated guanylate kinases and cell signaling. Curr. Opin. Cell Biol. 7:641-649.
33. Kim, E., M. Niethammer, A. Rothschild, Y.N. Jan, and M. Sheng. 1995. Clustering of Shaker-type K+ channels by interaction with a family of membrane-associated guanylate kinases. Nature (Lond). 378:85-88.
34. Knudsen, K.A., A.P. Soler, K.R. Johnson, and M.J. Wheelock. 1995. Interaction of α-actinin with the cadherin/catenin cell-cell adhesion complex via α-catenin. J. Cell Biol. 130:67-77.
35. Kornau, H.C., L.T. Schenker, M.B. Kennedy, and P.H. Seeburg. 1995. Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95. Science (Wash. DC). 269:1737-1740.
36. Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (Lond.). 227:680-685.
37. McCrea, P.D., C.W. Turck, and B. Gumbiner. 1991. A homolog of the armadillo protein in Drosophila (plakoglobin) associated with E-cadherin. Science (Wash. DC). 254:1359-1361.
38. Miller, J.R., and R.T. Moon. 1996. Signal transduction through β-catenin and specification of cell fate during embryogenesis. Genes Dev. 10:2527-2539.
39. 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.
40. 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.
41. Nagafuchi, A., and Sh. Tsukita. 1994. The loss of the expression of α catenin, the 102kD cadherin-associated protein, in central nervous tissues during development. Dev. Growth Differ. 36:59-71.
42. Nagafuchi, A., Y. Shirayoshi, K. Okazaki, K. Yasuda, and M. Takeichi. 1987. Transformation of cell adhesion properties by exogenously introduced E-cadherin cDNA. Nature (Lond.). 329:341-343.
43. Nagafuchi, A., M. Takeichi, and Sh. Tsukita. 1991. The 102 kd cadherin-associated protein: similarity to vinculin and posttranscriptional regulation of expression. Cell. 65:849-857.
44. Nagafuchi, A., S. Ishihara, and Sh. 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.
45. Näthke, I.S., L. Hinck, J.R. Swedlow, J. Papkoff, and W.J. Nelson. 1994. Defining interactions and distribution of cadherin and catenin complexes in polarized epithelial cells. J. Cell Biol. 125:1341-1352.
46. Niethammer, M., E. Kim, and M. Sheng. 1996. Interaction between the C terminus of NMDA receptor subunits and multiple members of the PSD-95 family of membrane-associated guanylate kinases. J. Neurosci. 16:2157-2163.
47. Nose, A., A. Nagafuchi, and M. Takeichi. 1988. Expressed recombinant cadherins mediate cell sorting in model systems. Cell. 54:993-1001.
48. Oyama, T., Y. Kanai, A. Ochiai, S. Akimoto, T. Oda, K. Yanagihara, A. Nagafuchi, Sh. Tsukita, S. Shibamoto, F. Ito, et al. 1994. A truncated β-catenin disrupts the interaction between E-cadherin and α-catenin: a cause of less of intercellular adhesiveness in human cancer cell lines. Cancer Res. 54:6282-6287.
49. Ozawa, M., and R. Kemler. 1992. Molecular organization of the uvomorulin-catenin complex. J. Cell Biol. 116:989-996.
50. 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.
51. 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.
52. +-induced actin assembly. J. Cell Biol. 93:648-654.
53. Rajasekaran, A.K., M. Hojo, T. Huima, and E. Rodriguez-Boulan. 1996. Catenins and zonula occludens-1 form a complex during early stages in the assembly of tight junctions. J. Cell Biol. 132:451-463.
54. Rimm, D.L., E.R. Koslov, P. Kebriaei, C.D. Cianci, and J.S. Morrow. 1995. α1(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.
55. Rodriguez-Boulan, E., and W.J. Nelson. 1989. Morphogenesis of the polarized epithelial cell phenotype. Science (Wash. DC). 245:718-725.
56. Schneeberger, E.E., and R.D. Lynch. 1992. Structure, function, and regulation of cellular tight junctions. Am. J. Physiol. 262:L647-L661.
57. Stevenson, B.R., J.D. Siliciano, M.S. Mooseker, and D.A. Goodenough. 1986. Identification of ZO-1: a high molecular weight polypeptide associated with the tight junction (zonula occludens) in a variety of epithelia. J. Cell Biol. 103:755-766.
58. Takeichi, M. 1977. Functional correlation between cell adhesive properties and some cell surface proteins. J. Cell Biol. 75:464-4174.
59. Takeichi, M. 1988. The cadherins: cell-cell adhesion molecules controlling animal morphogenesis. Development (Camb.). 102:639-655.
60. Takeichi, M. 1991. Cadherin cell adhesion receptors as a morphogenetic regulator. Science (Wash. DC). 251:1451-1455.
61. Tsukita, Sh., and Sa. Tsukita. 1989. Isolation of cell-to-cell adherens junctions from rat liver. J. Cell Biol. 108:31-41.
62. Tsukita, Sh., Sa. Tsukita, A. Nagafuchi, and S. Yonemura, 1992. Molecular linkage between cadherins and actin filaments in cell-cell adherens junctions. Curr. Opin. Cell Biol. 4:834-839.
63. Tsukita, Sh., M. Itoh, A. Nagafuchi, S. Yonemura, and Sa. Tsukita. 1993. Submembranous junctional plaque proteins include potential tumor suppresser molecules. J. Cell Biol. 123:1049-1053.
64. Volk, T., and B. Geiger. 1984. A 135-kd membrane protein of intercellular adherens junctions. EMBO (Eur. Mol. Biol. Organ.) J. 3: 2249-2260.
65. Willott, E., M.S. Balda, M. Heintzelman, B. Jameson, and J.M. Anderson. 1992. Localization and differential expression of two isoforms of the tight junction protein ZO-1. Am. J. Physiol. 262:C1119-1124.
66. Willott, E., M.S. Balda, A.S. Fanning, B. Jameson, C. Van Itallie, and J.M. Anderson. 1993. The tight junction protein ZO-1 is homologous to the Drosophila discs-large tumor suppresser protein of septate junctions. Proc. Natl. Acad. Sci. USA. 90:7834-7831.
67. Woods, D.A., and P.J. Bryant. 1993. ZO-1, DIgA and PSD95/SAP90: Homologous proteins in tight, septate and synaptic cell junctions. Mech. Dev. 44:85-89.
68. Yonemura, S., M. Itoh, A. Nagafuchi, and Sh. Tsukita. 1995. Cell-to-cell adherens junction formation and actin filament organization: similarities and differences between non-polarized fibroblasts and polarized epithelial cells. J. Cell Sci. 108:127-142.
69. Zhong, Y., T. Saitoh, T. Minase, N. Sawada, K. Enomoto, and M. Mori. 1993. Monoclonal antibody 7H6 reacts with a novel tight junction-associated protein distinct from ZO-1, cingulin and ZO-2. J. Cell Biol. 120:477-483.