Recycling of E-cadherin: A potential mechanism for regulating cadherin dynamics

Journal of Cell Biology

Volumn 146, Issue 1, 1999, Pages 219-232

  Le, Tam Luan ^a   Yap, Alpha S ^a   Stow, Jennifer L ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Biotinylation; Clathrin coated vesicles; Endocytosis; Epithelial junctions; Epithelial morphogenesis

Indexed keywords

UVOMORULIN;

ANIMAL CELL; ARTICLE; CELL CONTACT; CELL JUNCTION; CELL TRANSPORT; CONTROLLED STUDY; ENDOCYTOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN TRANSPORT; TRANSPORT KINETICS;

ANIMALS; ANTI-BACTERIAL AGENTS; BETA CATENIN; BIOLOGICAL TRANSPORT; BIOTINYLATION; CADHERINS; CALCIUM; CELL ADHESION; CELL COUNT; CELL LINE; CELL MEMBRANE; CHELATING AGENTS; CLATHRIN; CYTOSKELETAL PROTEINS; DOGS; ENDOCYTOSIS; ENDOSOMES; INTERCELLULAR JUNCTIONS; MACROLIDES; POTASSIUM; RECEPTORS, TRANSFERRIN; SOLUBILITY; TEMPERATURE; TRANS-ACTIVATORS;

ANIMALIA;

EID: 0001331879     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.146.1.219     Document Type: Article

References (68)

1. Adams, C.L., W.J. Nelson, and S.J. Smith. 1996. Quantitative analysis of cadherin-catenin-actin reorganization during development of cell-cell adhesion. J. Cell Biol. 135:1899-1911.
2. Adams, C.L., Y.T. Chen, S.J. Smith, and W.J. Nelson. 1998. Mechanisms of epithelial cell-cell adhesion and cell compaction revealed by high-resolution tracking of E-cadherin-green fluorescent protein. J. Cell Biol. 142:1105-1119.
3. Alexander, J.S., S.A. Jackson, E. Chaney, C.G. Kevil, and F.R. Haselton. 1998. The role of cadherin endocytosis in endothelial barrier regulation: involvement of protein kinase C and actin-cadnerin interactions. Inflammation. 22: 419-433.
4. 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.
5. Bradbury, N.A., T. Jilling, G. Berta, E.J. Sorscher, R.J. Bridges, and K.L. Kirk. 1992. Regulation of plasma membrane recycling by CFTR. Science. 256: 530-532.
6. Brieher, W.M., and B.M. Gumbiner. 1994. Regulation of C-cadherin function during activin induced morphogenesis of Xenopus animal caps. J. Cell Biol. 126:519-527.
7. Brown, D., T. Katsura, and C.E. Gustafson. 1998. Cellular mechanisms of aquaporin trafficking. Am. J. Physiol. 275:F328-F331.
8. Chavrier, P., R.G. Parton, H.P. Hauri, K. Simons, and M. Zerial. 1990. Localization of low molecular weight GTP binding proteins to exocytic and endocytic compartments. Cell. 62:317-329.
9. Chen, Y.T., D.B. Stewart, and W.J. Nelson. 1999. Coupling assembly of the E-cadherin/beta-catenin complex to efficient endoplasmic reticulum exit and basal-lateral membrane targeting of E-cadherin in polarized MDCK cells. J. Cell Biol. 144:687-699.
10. Citi, S. 1992. Protein kinase inhibitors prevent junction dissociation induced by low extracellular calcium in MDCK epithelial cells. J. Cell Biol. 117:169-178.
11. Czekay, R.P., R.A. Orlando, L. Woodward, M. Lundstrom, and M.G. Farquhar. 1997. Endocytic trafficking of megalin/RAP complexes: dissociation of the complexes in late endosomes. Mol. Biol. Cell. 8:517-532.
12. de Almeida, J.B., E.J. Holtzman, P. Peters, L. Ercolani, D.A. Ausiello, and J.L. Stow. 1994. Targeting of chimeric Gαi proteins to specific membrane domains. J. Cell Sci. 107:507-515.
13. Duden, R., and W.W. Franke. 1988. Organization of desmosomal plaque proteins in cells growing at low calcium concentrations. J. Cell Biol. 107:1049-1063.
14. Dunn, K.W., T.E. McGraw, and F.R. Maxfield. 1989. Iterative fractionation of recycling receptors from lysosomally destined ligands in an early sorting endosome. J. Cell Biol. 109:3303-3314.
15. Galloway, C.J., G.E. Dean, M. Marsh, G. Rudnick, and I. Mellman. 1983. Acidification of macrophage and fibroblast endocytic vesicles in vitro. Proc. Natl. Acad. Sci. USA. 80:3334-3338.
16. Gebbink, M.F., G.C. Zondag, G.M. Koningstein, E. Feiken, R.W. Wubbolts, and W.H. Moolenaar. 1995. Cell surface expression of receptor protein tyrosine phosphatase RPTP mu is regulated by cell-cell contact. J. Cell Biol. 131:251-260.
17. Gottardi, C.J., L.A. Dunbar, and M.J. Caplan. 1995. Biotinylation and assessment of membrane polarity: caveats and methodological concerns. Am. J. Physiol. 268:F285-F295.
18. Graeve, L., K. Drickamer, and E. Rodriguez-Boulan. 1989. Functional expression of the chicken liver asialoglycoprotein receptor in the basolateral surface of MDCK cells. J. Cell Biol. 109:2809-2816.
19. Grindstaff, K.K., R.L. Bacallao, and W.J. Nelson. 1998. Apiconuclear organization of microtubules does not specify protein delivery from the trans-Golgi network to different membrane domains in polarized epithelial cells. Mol. Biol. Cell. 9:685-699.
20. Gumbiner, B., B. Stevenson, and A. Grimaldi. 1988. The role of the cell adhesion molecule uvomorulin in the formation and maintainance of the epithelial junctional complex. J. Cell Biol. 107:1575-1587.
21. Gumbiner, B.M. 1992. Epithelial morphogenesis. Cell. 69:385-387.
22. Hermiston, M.L., and J.I. Gordon. 1995. In vivo analysis of cadherin function in the mouse intestinal epithelium: essential roles in adhesion, maintainance of differentiation, and regulation of programmed cell death. J. Cell Biol. 129: 489-506.
23. Hermiston, M.L., M.H. Wong, and J.I. Gordon. 1996. Forced expression of E-cadherin in the mouse intestinal epithelium slows cell migration and provides evidence for nonautonomous regulation of cell fate in a self-renewing system. Genes Dev. 10:985-996.
24. Johnson, K.F., and S. Kornfeld. 1992. A His-Leu-Leu sequence near the carboxyl terminus of the cytoplasmic domain of the cation-dependent mannose 6-phosphate receptor is necessary for the lysosomal enzyme sorting function. J. Biol. Chem. 267:17110-17115.
25. Johnson, L.S., K.W. Dunn, B. Pytowski, and T.E. McGraw. 1993. Endosome acidification and receptor trafficking: bafilomycin A1 slows receptor externalization by a mechanism involving the receptor's internalization motif. Mol. Biol. Cell. 4:1251-1266.
26. Kartenbeck, J., E. Schmid, W.W. Franke, and B. Geiger. 1982. Different modes of internalization of proteins associated with adherens junctions and desmosomes: experimental separation of lateral contacts induces endocytosis of desmosomal plaque material. EMBO (Eur. Mol. Biol. Organ.) J. 1:725-732.
27. Kartenbeck, J., M. Schmelz, W.W. Franke, and B. Geiger. 1991. Endocytosis of junctional acadherins in bovine kidney epithelial (MBCK) cells cultured in low Ca2+ ion medium. J. Cell Biol. 113:881-892.
28. Kemler, R., M. Ozawa, and M. Ringwald. 1989. Calcium-dependent cell adhesion molecules. Curr. Opin. Cell. Biol. 1:892-897.
29. Larkin, J.M., M.S. Brown, J.L. Goldstein, and R.G.W. Anderson. 1983. Depletion of intracellular potassium arrests coated pit formation and receptor-mediated endocytosis in fibroblasts. Cell. 33:273-285.
30. Lawson, M.A., and F.R. Maxfield. 1995. Ca(2+)- and calcineurin-dependent recycling of an integrin to the front of migrating neutrophils. Nature. 377:75-79.
31. Letourneur, F., and R.D. Klausner. 1992. A novel di-leucine motif and a tyrosine-based motif independently mediate lysosomal targeting and endocytosis of CD3 chains. Cell. 69:1143-1157.
32. Lever, J.E. 1979. Inducers of mammalian cell differentiation stimulate dome formation in a differentiated kidney epithelial cell line (MDCK). Proc. Natl. Acad. Sci. USA. 76:1323-1327.
33. Levine, E., C.H. Lee, C. Kintner, and B.M. Gumbiner. 1994. Selective disruption of E-cadherin function in early Xenopus embryos by a dominant negative mutant. Development. 120:901-909.
34. Mays, R.W., K.A. Siemers, B.A. Fritz, A.W. Lowe, A.W. van Meer, and W.J. Nelson. 1995. Hierarchy of mechanisms involved in generating Na/K-ATPase polarity in MDCK epithelial cells. J. Cell Biol. 130:1105-1115.
35. McCrea, P.D., and B.M. Gumbiner. 1991. Purification of a 92-kDa cytoplasmic protein tightly associated with the cell-cell adhesion molecule E-cadherin (uvomorulin). Characterization and extractability of the protein complex from the cell cytostructure. J. Biol. Chem. 266:4514-4520.
36. McNeill, H., T.A. Ryan, S.J. Smith, and W.J. Nelson. 1993. Spatial and temporal dissection of immediate and early events following cadherin-mediated epithelial cell adhesion. J. Cell Biol. 120:1217-1226.
37. Mengaud, J., H. Ohayon, P. Gounon, R.-M. Mege, and P. Cossart. 1996. E-cadherin is the receptor for internalin, a surface protein required for entry of L. monocytogenes into epithelial cells. Cell. 84:923-932.
38. Miller, J.R., and D.R. McClay. 1997. Characterization of the role of cadherin in regulating cell adhesion during sea urchin development. Dev. Biol. 192:323-339.
39. Musil, L.S., B.A. Cunningham, G.M. Edelman, and D.A. Goodenough. 1990. Differential phosphorylation of the gap junction protein connexin43 in junctional communication-competent and -deficient cell lines. J. Cell Biol. 111: 2077-2088.
40. Myat, M.M., S. Chang, E. Rodriguez-Boulan, and A. Aderem. 1998. Identification of the basolateral targeting determinant of a peripheral membrane protein, MacMARCKS, in polarized cells. Curr. Biol. 8:677-683.
41. Narula, N., I. McMorrow, G. Plopper, J. Doherty, K.S. Matlin, B. Burke, and J.L. Stow. 1992. Identification of a 200-kD, brefeldin-sensititve protein on Golgi membranes. J. Cell Biol. 117:27-38.
42. Nathke, I.S., L. Hinck, J.R. Swedlow, J. Papkoff, and W.J. Nelson. 1994. Defining interactions and distributions of cadherin and catenin complexes in polarized epithelial cells. J. Cell Biol. 125:1341-1352.
43. Nelson, W.J., E.M. Shore, A.Z. Wang, and R.W. Hammerton. 1990. Identification of a membrane-cytoskeletal complex containing the cell adhesion molecule uvomorulin (E-cadherin), ankyrin, and fodrin in Madin-Darby canine kidney epithelial cells. J. Cell Biol. 110:349-357.
44. Ostman, A., Q. Yang, and N.K. Tonks. 1994. Expression of DEP-1, a receptor-like protein-tyrosine-phosphatase, is enhanced with increasing cell density. Proc. Natl. Acad. Sci. USA. 91:9680-9684.
45. 1 treatment retards transferrin receptor recycling more than bulk membrane recycling. J. Biol. Chem. 272:13929-13936.
46. Rea, S., and D.E. James. 1997. The biogenesis and trafficking of GLUT4 storage vesicles. Diabetes. 46:1667-1677.
47. 2+-dependent cell adhesion. EMBO (Eur. Mol. Biol. Organ.) J. 6:3647-3653.
48. Sandvig, K., and B. van Deurs. 1996. Endocytosis, intracellular transport, and cytotoxic action of Shiga toxin and ricin. Physiol. Rev. 76:949-966.
49. Shore, E.M., and W.J. Nelson. 1991. Biosynthesis of the cell adhesion molecule uvomorulin (E-cadherin) in Madin-Darby canine kidney epithelial cells. J. Cell Biol. 266:19672-19680.
50. Takeichi, M. 1977. Functional correlation between cell adhesive properties and some cell surface proteins. J. Cell Biol. 75:464-474.
51. Takeichi, M. 1991. Cadherin cell adhesion receptors as a morphogenetic regulator. Science. 251:1451-1455.
52. Takeichi, M. 1995. Morphogenetic roles of classic cadherins. Curr. Opin. Cell Biol. 7:619-627.
53. Takeichi, M., T. Atmusi, C. Yoshida, K. Uno, and T.S. Okada. 1981. Selective adhesion of embryonal carcinoma cells and differentiated cells by Ca2+-dependent sites. Dev. Biol. 87:340-350.
54. Tepass, U. 1996. Crumbs, a component of the apical membrane, is required for zonula adherens formation in primary epithelia of Drosophila. Dev. Biol. 177:217-225.
55. Trowbridge, I.S., J.F. Collawn, and C.R. Hopkins. 1993. Signal-dependent membrane protein trafficking in the endocytic pathway. Annu. Rev. Cell Biol. 9:129-161.
56. Uemura, T., H. Oda, R. Kraut, S. Hayashi, Y. Kotaoka, and M. Takeichi. 1996. Zygotic Drosophila E-cadherin expression is required for processes of dynamic epithelial cell rearrangement in the Drosophila embryo. Genes Dev. 10:659-671.
57. Vega-Salas, D.E., P.J.I. Salas, D. Gundersen, and E. Rodriguez-Boulan. 1987. Formation of the apical pole of epithelial (Madin-Darby canine kidney) cells. Polarity of an apical protein is independent of tight junctions while segregation of a basolateral marker requires cell-cell interactions. J. Cell Biol. 104:905-1007.
58. Vestweber, D., A. Gossler, K. Boller, and R. Kemler. 1987. Expression and distribution of cell adhesion molecule uvomorulin in mouse preimplantation embryos. Dev. Biol. 124:451-456.
59. Wang, A.Z., G.K. Ojakian, and W.J. Nelson. 1990. Steps in the morphogenesis of a polarized epithelium. I. Uncoupling the roles of cell-cell and cell-substratum contact in establishing plasma membrane polarity in multicellular epithelial (MDCK) cysts. J. Cell Sci. 95:137-151.
60. 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.
61. Wheelock, M.J., and P.J. Jensen. 1992. Regulation of keratinocyte intercellular junction organization and epidermal morphogenesis by E-cadherin. J. Cell Biol 117:415-425.
62. Wilson, J.M., and T.L. Colton. 1997. Targeting of an intestinal apical endosomal protein to endosomes in nonpolarized cells. J. Cell Biol. 136:319-330.
63. Winkel, G.K., J.E. Ferguson, M. Takeichi, and R. Nuccitelli. 1990. Activation of protein kinase C triggers premature compaction in the four-cell stage mouse embryo. Dev. Biol. 138:1-15.
64. Yap, A.S., B.R. Stevenson, J.R. Keast, and S.W. Manley. 1995. Cadherin-mediated adhesion and apical membrane assembly define distinct steps during thyroid epithelial polarization and lumen formation. Endocrinology. 136: 4672-4680.
65. Yap, A.S., W.M. Brieher, and B.M. Gumbiner. 1997a. Molecular and functional analysis of cadherin-based adherens junctions. Annu. Rev. Cell. Dev. Biol. 13:119-146.
66. Yap, A.S., W.M. Brieher, M. Pruschy, and B.M. Gumbiner. 1997b. Lateral clustering of the adhesive ectodomain: a fundamental determinant of cadherin function. Curr. Biol. 7:308-315.
67. 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.
68. Zhong, Y., W.M. Brieher, and B.M. Gumbiner. 1999. Analysis of C-cadherin regulation during tissue morphogenesis with an activating antibody. J. Cell Biol. 144:351-359.