Wingless signaling modulates cadherin-mediated cell adhesion in Drosophila imaginal disc cells

Journal of Cell Science

Volumn 119, Issue 12, 2006, Pages 2425-2434

  Wodarz, Andreas ^a,b   Stewart, Daniel B ^a   Nelson, W James ^a   Nusse, Roel ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Cadherin; Catenin; Cell adhesion; Wingless; Wnt

Indexed keywords

BETA CATENIN; UVOMORULIN; WNT1 PROTEIN;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL DIVISION; CELL MOTION; CELL SHAPE; CELL SPREADING; CELL SURFACE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; DROSOPHILA; EMBRYO DEVELOPMENT; GENE EXPRESSION; IMAGINAL DISC; INSECT CELL; INSECT DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANIMALS; ARMADILLO DOMAIN PROTEINS; CADHERINS; CATENINS; CELL ADHESION; CELLS, CULTURED; CYTOPLASM; DROSOPHILA; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION; MICE; PROTO-ONCOGENE PROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

ARMADILLO;

EID: 33746057468     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.02973     Document Type: Article

References (57)

1. Aberle, H., Butz, S., Stappert, J., Weissig, H., Kemler, R. and Hoschuetzky, H. (1994). Assembly of the cadherin catenin complex in vitro with recombinant proteins. J. Cell Sci. 107, 3655-3663.
2. Behrens, J., Vakaet, L., Friis, R., Winterhager, E., Van Roy, F., Mareel, M. M. and Birchmeier, W. (1993). Loss of epithelial differentiation and gain of invasiveness correlates with tyrosine phosphorylation of the E-cadherin/beta-catenin complex in cells transformed with a temperature-sensitive v-SRC gene. J. Cell Biol. 120, 757-766.
3. Bek, S. and Kemler, R. (2002). Protein kinase CKII regulates the interaction of beta-catenin with alpha-catenin and its protein stability. J. Cell Sci. 115, 4743-4753.
4. Bhanot, P., Brink, M., Harryman Samos, C., Hsieh, J. C., Wang, Y. S., Macke, J. P., Andrew, D., Nathans, J. and Nusse, R. (1996). A new member of the frizzled family from Drosophila functions as a Wingless receptor. Nature 382, 225-230.
5. Bradley, R., Cowin, P. and Brown, A. (1993). Expression of Wnt-1 in PC12 cells results in modulation of plakoglobin and E-cadherin and increased cellular adhesion. J. Cell Biol. 123, 1857-1865.
6. Brembeck, F. H., Schwarz-Romond, T., Bakkers, J., Wilhelm, S., Hammerschmidt, M. and Birchmeier, W. (2004). Essential role of BCL9-2 in the switch between beta-catenin's adhesive and transcriptional functions. Genes Dev. 18, 2225-2230.
7. Bryant, D. M. and Stow, J. L. (2004). The ins and outs of E-cadherin trafficking. Trends Cell Biol. 14, 427-434.
8. Cox, R. T., Kirkpatrick, C. and Peifer, M. (1996). Armadillo is required for adherens junction assembly, cell polarity, and morphogenesis during Drosophila embryogenesis. J. Cell Biol. 134, 133-148.
9. Danilkovitch-Miagkova, A., Miagkov, A., Skeel, A., Nakaigawa, N., Zbar, B. and Leonard, E. J. (2001). Oncogenic mutants of RON and MET receptor tyrosine kinases cause activation of the beta-catenin pathway. Mol. Cell. Biol. 21, 5857-5868.
10. Drees, F., Pokutta, S., Yamada, S., Nelson, W. J. and Weis, W. I. (2005). Alpha-catenin is a molecular switch that binds E-cadherin/ beta-catenin and regulates actin filament assembly. Cell 123, 769-772.
11. González, F., Swales, L., Bejsovec, A., Skaer, H. and Martinez-Arias, A. (1991). Secretion and movement of wingless protein in the epidermis of the Drosophila embryo. Mech. Dev. 35, 43-54.
12. Gumbiner, B. M. (1996). Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell 84, 345-357.
13. Hartenstein, V., Younossi-Hartenstein, A. and Lekven, A. (1994). Delamination and division in the Drosophila neurectoderm: spatiotempora] pattern, cytoskeletal dynamics, and common control by neurogenic and segment polarity genes. Dev. Biol. 165, 480-499.
14. Heasman, J., Crawford, A., Goldstone, K., Garner-Hamrick, P., Gumbiner, B., McCrea, P., Kintner, C., Noro, C. Y. and Wylie, C. (1994). Overexpression of cadherins and underexpression of beta-catenin inhibit dorsal mesoderm induction in early Xenopus embryos. Cell 79, 791-803.
15. 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.
16. Hoschuetzky, H., Aberle, H. and Kemler, R. (1994). Beta-catenin mediates the interaction of the cadherin-catenin complex with epidermal growth factor receptor. J. Cell Biol. 127, 1375-1380.
17. Hulsken, J., Behrens, J. and Birchmeier, W. (1994). Tumor-suppressor gene products in cell contacts: the cadherin-APC-armadillo connection. Curr. Opin. Cell Biol. 6, 711-716.
18. Jamora, C. and Fuchs, E. (2002). Intercellular adhesion, signalling and the cytoskeleton. Nat. Cell Biol. 4, E101-E108.
19. Jamora, C., DasGupta, R., Kocieniewski, P. and Fuchs, E. (2003). Links between signal transduction, transcription and adhesion in epithelial bud development. Nature 422, 317-322.
20. Klingensmith, J. and Nusse, R. (1994). Signaling by wingless in Drosophila. Dev. Biol. 166, 396-414.
21. Koelle, M. R., Talbot, W. S., Segraves, W. A., Bender, M. T., Cherbas, P. and Hogness, D. S. (1991). The Drosophila EcR gene encodes an ecdysone receptor, a new member of the steroid receptor superfamily. Cell 67, 59-77.
22. Lum, L., Zhang, C., Oh, S., Mann, R. K., von Kessler, D. P., Taipale, J., Weis-Garcia, F., Gong, R., Wang, B. and Beachy, P. A. (2003). Hedgehog signal transduction via Smoothened association with a cytoplasmic complex scaffolded by the atypical kinesin, Costal-2. Mol. Cell 12, 1261-1274.
23. Marrs, J. A., Napolitano, E. W., Murphy-Erdosh, C., Mays, R. W., Reichardt, L. F. and Nelson, W. J. (1993). Distinguishing roles of the membrane-cytoskeleton and cadherin mediated cell-cell adhesion in generating different Na+,K(+)-ATPase distributions in polarized epithelia. J. Cell Biol. 123, 149-164.
24. McCartney, B. M., McEwen, D. G., Grevengoed, E., Maddox, P., Bejsovec, A. and Peifer, M. (2001). Drosophila APC2 and Armadillo participate in tethering mitotic spindles to cortical actin. Nat. Cell Biol. 3, 933-938.
25. Nelson, W. and Nusse, R. (2004). Convergence of Wnt, beta-catenin and cadherin pathways. Science 303, 1483-1487.
26. Oda, H. and Tsukita, S. (1999). Dynamic features of adherens junctions during Drosophila embryonic epithelial morphogenesis revealed by a Dalpha-catenin-GFP fusion protein. Dev. Genes Evol. 209, 218-225.
27. Oda, H., Uemura, T., Shiomi, K., Nagafuchi, A., Tsukita, S. and Takeichi, M. (1993). Identification of a Drosophila homologue of alpha-catenin and its association with the armadillo protein. J. Cell Biol. 121, 1133-1140.
28. Oda, H., Uemura, T., Harada, Y., Iwai, Y. and Takeichi, M. (1994). A Drosophila homolog of cadherin associated with armadillo and essential for embryonic cell-cell adhesion. Dev. Biol. 165, 716-726.
29. Orsulic, S. and Peifer, M. (1996). An in vivo structure-function study of armadillo, the beta-catenin homologue, reveals both separate and overlapping regions of the protein required for cell adhesion and for wingless signaling. J. Cell Biol. 134, 1283-1300.
30. Pai, L. M., Kirkpatrick, C., Blanton, J., Oda, H., Takeichi, M. and Peifer, M. (1996). Drosophila alpha-catenin and E-cadherin bind to distinct regions of Drosophila Armadillo. J. Biol. Chem. 271, 32411-32420.
31. Peel, D. J., Johnson, S. A. and Milner, M. J. (1990). The ultrastructure of imaginal disc cells in primary cultures and during cell aggregation in continuous cell lines. Tissue Cell 22, 749-758.
32. Peifer, M. (1993). The product of the Drosophila segment polarity gene armadillo is part of a multi-protein complex resembling the vertebrate adherens junction. J. Cell Sci. 105, 993-1000.
33. Peifer, M., Pai, L. M. and Casey, M. (1994a). Phosphorylation of the Drosophila adherens junction protein Armadillo: roles for wingless signal and zeste-white 3 kinase. Dev. Biol. 166, 543-556.
34. Peifer, M., Sweeton, D., Casey, M. and Wieschaus, E. (1994b). Wingless signal and Zeste-white 3 kinase trigger opposing changes in the intracellular distribution of Armadillo. Development 120, 369-380.
35. Piedra, J., Martinez, D., Castano, J., Miravet, S., Dunach, M. and de Herreros, A. G. (2001). Regulation of beta-catenin structure and activity by tyrosine phosphorylation. J. Biol. Chem. 276, 20436-20443.
36. Riggleman, B., Wieschaus, E. and Schedl, P. (1989). Molecular analysis of the armadillo locus: uniformly distributed transcripts and a protein with novel internal repeats are associated with a Drosophila segment polarity gene. Genes Dev. 3, 96-113.
37. Sanson, B., White, P. and Vincent, J. P. (1996). Uncoupling cadherin-based adhesion from wingless signalling in Drosophila. Nature 383, 627-630.
38. Seto, E. S. and Bellen, H. J. (2004). The ins and outs of Wingless signaling. Trends Cell Biol. 14, 45-53.
39. Shariatmadari, M., Peyronnet, J., Papachristou, P., Horn, Z., Sousa, K. M., Arenas, E. and Ringstedt, T. (2005). Increased Wnt levels in the neural tube impair the function of adherens junctions during neurulation. Mol. Cell Neurosci. 30, 437-451.
40. Shiozaki, H., Kadowaki, T., Doki, Y., Inoue, M., Tamura, S., Oka, H., Iwazawa, T., Matsui, S., Shimaya, K., Takeichi, M. et al. (1995). Effect of epidermal growth factor on cadherin-mediated adhesion in a human oesophageal cancer cell line. Br. J. Cancer 71, 250-258.
41. Shore, E. M. and Nelson, W. J. (1991). Biosynthesis of the cell adhesion molecule uvomorulin (E-cadherin) in Madin-Darby canine kidney epithelial cells. J. Biol. Chem. 266, 19672-19680.
42. Siegfried, E., Wilder, E. L. and Perrimon, N. (1994). Components of wingless signalling in Drosophila. Nature 367, 76-80.
43. Sommers, C. L., Gelmann, E. P., Kemler, R., Cowin, P. and Byers, S. W. (1994). Alterations in beta-catenin phosphorylation and plakoglobin expression in human breast cancer cells. Cancer Res, 54, 3544-3552.
44. Stappert, J. and Kemler, R. (1994). A short core region of E-cadherin is essential for catenin binding and is highly phosphorylated. Cell Adhes. Commun. 2, 319-327.
45. Tepass, U. and Hartenstein, V. (1994). The development of cellular junctions in the Drosophila embryo. Dev. Biol. 161, 563-596.
46. Tepass, U., Gruszynski-DeFeo, E., Haag, T. A., Omatyar, L., Török, T. and Hartenstein, V. (1996). shotgun encodes Drosophila E-cadherin and is preferentially required during cell rearrangement in the neurectoderm and other morphogenetically active epithelia. Genes Dev. 10, 672-685.
47. Uemura, T., Oda, H., Kraut, R., Hayashi, S., Kataoka, Y. and Takeichi, M. (1996). Zygotic Drosophila E-cadherin expression is required for processes of dynamic epithelial cell rearrangement in the Drosophila embryo. Genes Dev. 10, 659-671.
48. Ulrich, F., Krieg, M., Schotz, E. M., Link, V., Castanon, L, Schnabel, V., Taubenberger, A., Mueller, D., Puech, P. H. and Heisenberg, C. P. (2005). Wnt11 functions in gastrulation by controlling cell cohesion through Rab5c and E-cadherin. Dev. Cell 9, 555-564.
49. Van den Heuvel, M., Nusse, R., Johnston, P. and Lawrence, P. A. (1989). Distribution of the wingless gene product in Drosophila embryos: a protein involved in cell-cell communication. Cell 59, 739-749.
50. Van Leeuwen, F., Harryman Samos, C. and Nusse, R. (1994). Biological activity of soluble wingless protein in cultured Drosophila imaginal disc cells. Nature 368, 342-344.
51. Vestweber, D. and Kemler, R. (1985). Identification of a putative cell adhesion domain of uvomorulin. EMBO J. 4, 3393-3398.
52. Vogelmann, R., Nguyen-Tat M. D., Giehl, K., Adler, G., Wedlich, D. and Menke, A. (2005). TGF{beta}-induced downregulation of E-cadherin-based cell-cell adhesion depends on PI3-kinase and PTEN. J. Cell Sci. 118, 4901-4912.
53. Willert, K. and Nusse, R. (1998). beta-catenin: a key mediator of Wnt signaling. Curr. Opin. Genet. Dev. 8, 95-102.
54. Wodarz, A. and Nusse, R. (1998). Mechanisms of Wnt signaling in development. Annu. Rev. Cell Dev. Biol. 14, 59-88.
55. Yamada, S., Pokutta, S., Drees, F., Weis, W. I. and Nelson, W. J. (2005). Deconstructing the Cadherin-Catenin-Actin complex. Cell 123, 889-901.
56. Yanagawa, S., Van Leeuwen, F., Wodarz, A., Klingensmith, J. and Nusse, R. (1995). The Dishevelled protein is modified by Wingless signaling in Drosophila. Genes Dev. 9, 1087-1097.
57. Yanagawa, S., Lee, J. S., Haruna, T., Oda, H., Uemura, T., Takeichi, M. and Ishimoto, A. (1997). Accumulation of armadillo induced by wingless, dishevelled, and dominant-negative zeste-white 3 leads to elevated DE-cadherin in Drosophila clone 8 wing disc cells. J Biol. Chem. 272, 25243-25251.