The C-terminal domain of Armadillo binds to hypophosphorylated Teashirt to modulate wingless signalling in Drosophila

EMBO Journal

Volumn 18, Issue 8, 1999, Pages 2208-2217

  Gallet, Armel ^a   Angelats, Corinne ^a   Erkner, Alfrun ^a   Charroux, Bernard ^a,b   Fasano, Laurent ^a   Kerridge, Stephen ^a  

^a AIX MARSEILLE UNIVERSITY   (France)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Armadillo; Drosophila; Teashirt phosphorylation; Wingless; Wnt pathway

Indexed keywords

BETA CATENIN; BINDING PROTEIN; PROTEIN KINASE; ZINC FINGER PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; DROSOPHILA; EMBRYO; EMBRYO PATTERN FORMATION; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN DNA BINDING;

EID: 0033561298     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.8.2208     Document Type: Article

References (52)

1. Aberle, H., Bauer, A., Stappert, J., Kispert, A. and Kemler, R. (1997) ß-catenin is a target for the ubiquitin-proteasome pathway. EMBO J., 16, 3797-3804.
2. Alexandre, E., Graba, Y., Fasano, L., Gallet, A., Perrin, L., De Zulueta, P., Pradel, J., Kerridge, S. and Jacq, B. (1996) The Drosophila Teashirt homeotic protein is a DNA-binding protein and modulo, a HOM-C regulated modifier of variegation, is a likely candidate for being a direct target gene. Mech. Dev., 59, 191-204.
3. Bejsovec, A. and Martinez Arias, A. (1991) Roles of wingless in patterning the larval epidermis of Drosophila. Development, 113, 471-485.
4. Bhanot, P., Brink, M., Samos, C.H., Hsieh, J.C., Wang, Y., 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. Bhat, K. (1998)frizzled and frizzled-2 play a partially redundant role in Wingless signaling and have similar requirements to wingless in neurogenesis. Cell, 95, 1027-1036.
6. Brand, A. and Perrimon, N. (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotype. Development, 118, 401-415.
7. Brunner, E., Peter, O., Schweizer, L. and Basler, K. (1997)pangolin encodes a Lef-1 homologue that acts downstream of Armadillo to transduce the Wingless signal in Drosophila. Nature, 385, 829-833.
8. Cadigan, K.M. and Nusse, R. (1997) Wnt signaling: a common theme in animal development. Genes Dev., 11, 3286-3305.
9. Cadigan, K.M., Fish, M.P., Rulifson, E.J. and Nusse, R. (1998) Wingless repression of Drosophila frizzled 2 expression shapes the Wingless morphogen gradient in the wing. Cell, 93, 767-777.
10. Cavallo, R.A., Cox, R.T., Moline, M.M., Roose, J., Polevoy, G.A., Clevers, H., Peifer, M. and Bejsovec, A. (1998) Drosophila Tcf and Groucho interact to repress Wingless signalling activity. Nature, 395, 604-608.
11. Clevers, H. and van de Wetering, M. (1997) TCF/LEF factor earn their wings. Trends Genet., 13, 485-489.
12. Cox, R.T. and Peifer, M. (1998) Wingless signaling: the inconvenient complexities of life. Curr. Biol., 8, R140-R144.
13. 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.
14. de Zulueta, P., Alexandre, E., Jacq, B. and Kerridge, S. (1994) Homeotic complex and teashirt genes co-operate to establish trunk segmental identities in Drosophila. Development, 120, 2287-2296.
15. Dougan, S.T. and DiNardo, S. (1992) wingless generates cell type diversity among engrailed expressing cells. Nature, 360, 347-350.
16. Fagotto, F., Gluck, U. and Gumbiner, B.M. (1998) Nuclear localization signal-independent and Importin/Karyopherin-independent nuclear import of ß-catenin. Curr. Biol., 8, 181-190.
17. Fasano, L., Röder, L., Core, N., Alexandre, E., Vola, C., Jacq, B. and Kerridge, S. (1991) The gene teashirt is required for the development of Drosophila embryonic trunk segments and encodes a protein with widely spaced zinc finger motifs. Cell, 64, 63-79.
18. Gallet, A., Erkner, A., Charroux, B., Fasano, L. and Kerridge, S. (1998) Trunk-specific modulation of Wingless signalling in Drosophila by Teashirt binding to Armadillo. Curr. Biol., 8, 893-902.
19. Hays, R., Gibori, G.B. and Bejsovec, A. (1997) Wingless signaling generates pattern through two distinct mechanisms. Development, 124, 3727-3736.
20. Hooper, J.E. (1994) Distinct pathways for autocrine and paracrine Wingless signalling in Drosophila embryos. Nature, 372, 461-464.
21. Hulsken, J., Birchmeier, W. and Behrens, J. (1994) E-cadherin and APC compete for the interaction with ß-catenin and the cytoskeleton. J. Cell Biol., 127, 2061-2069.
22. Klingensmith, J., Noll, E. and Perrimon, N. (1989) The segment polarity phenotype of Drosophila involves differential tendencies toward transformation and cell death. Dev. Biol., 134, 130-145.
23. Korinek, V., Barker, N., Morin, P., van Wichen, D., de Weger, R., Kinzler, K., Vogelstein, B. and Clevers, H. (1997) Constitutive transcriptional activation by a ß-catenin-Tcf complex in APC-/-colon carcinoma. Science, 275, 1784-1787.
24. Loureiro, J. and Peifer, M. (1998) Roles of Armadillo, a Drosophila catenin, during central nervous system development. Curr. Biol., 8, 622-632.
25. Manoukian, A.S., Yoffe, K.B., Wilder, E.L. and Perrimon, N. (1995) The porcupine gene is required for wingless autoregulation in Drosophila. Development, 121, 4037-4044.
26. Martinez-Arias, A., Baker, N.E. and Ingham, P.W. (1988) Role of segment polarity genes in the definition and maintenance of cell states in the Drosophila embryo. Development, 103, 157-170.
27. Miller, J.R. and Moon, R.T. (1996) Signal transduction through ß-catenin and specification of cell fate during embryogenesis. Genes Dev., 10, 2527-2539.
28. Molenaar, M., van de Wetering, M., Oosterwegel, M., Peterson-Maduro, J., Godsave, S., Korinek, V., Roose, J., Destree, O. and Clevers, H. (1996) XTcf-3 transcription factor mediates ß-catenin-induced axis formation in Xenopus embryos. Cell, 86, 391-399.
29. Müller, H.-Arno. J., Arno, J., Samanta, R. and Wieschaus, E. (1999) Wingless signaling in the Drosophila embryo: zygotic requirements and the role of frizzled genes. Development, 126, 577-587.
30. Neumann, C. and Cohen, S. (1997) Morphogens and pattern formation. Bioessays, 19, 721-729.
31. Noordermeer, J., Johnston, P., Rijsewijk, F., Nusse, R. and Lawrence, P.A. (1992) The consequences of ubiquitous expression of the wingless gene in the Drosophila embryo. Development, 116, 711-719.
32. Nusslein-Volhard;C. and Wieschaus, E. (1980) Mutations affecting segment number and polarity in Drosophila. Nature, 287, 795-801.
33. Orsulic, S. and Peifer, M. (1996) An in vivo structure-function study of Armadillo, the ß-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.
34. Pai, L.M., Kirkpatrick, C., Blanton, J., Oda, H., Takeichi, M. and Peifer, M. (1996) Drosophila α-catenin and E-cadherin bind to distinct regions of Drosophila Armadillo. J. Biol. Chem., 271, 32411-32420.
35. Pai, L.M., Orsulic, S., Bejsovec, A. and Peifer, M. (1997) Negative regulation of Armadillo, a Wingless effector in Drosophila. Development, 124, 2255-2266.
36. Peifer, M. and Wieschaus, E. (1990) The segment polarity gene armadillo encodes a functionally modular protein that is the Drosophila homolog of human plakoglobin. Cell, 63, 1167-1176.
37. Peifer, M., Orsulic, S., Pai, L.M. and Loureiro, J. (1993a) A model system for cell adhesion and signal transduction in Drosophila. Dev. Suppl., 163-176.
38. Peifer, M., Orsulic, S., Sweeton, D. and Wieschaus, E. (1993b) A role for the Drosophila segment polarity gene armadillo in cell adhesion and cytoskeletal integrity during oogenesis. Development, 118, 1191-1207.
39. Peifer, M., Berg, S. and Reynolds, A.B. (1994a) A repeating amino acid motif shared by proteins with diverse cellular roles. Cell, 76, 789-791.
40. Peifer, M., Pai, L.M. and Casey, M. (1994b) Phosphorylation of the Drosophila adherens junction protein Armadillo: roles for Wingless signal and Zeste-white 3 kinase. Dev. Biol., 166, 543-556.
41. Peifer, M., Sweeton, D., Casey, M. and Wieschaus, E. (1994c) Wingless signal and Zeste-white 3 kinase trigger opposing changes in the intracellular distribution of Armadillo. Development, 120, 369-380.
42. Perrimon, N. (1994) The genetic basis of patterned baldness in Drosophila. Cell, 76, 781-784.
43. Riggleman, B., Schedl, P. and Wieschaus, E. (1990) Spatial expression of the Drosophila segment polarity gene armadillo in post-transcriptionally regulated by wingless. Cell, 63, 549-560.
44. Röder, L., Vola, C. and Kerridge, S. (1992) The role of the teashirt gene in trunk segmental identity in Drosophila. Development, 115, 1017-1033.
45. Roose, J., Molenaar, M., Peterson, J., Hurenkamp, J., Brantjes, H., Moerer, P., van de Wetering, M., Destree, O. and Clevers, H. (1998) The Xenopus Wnt effector XTcf-3 interacts with Groucho-related transcriptional repressors. Nature, 395, 608-612.
46. Rubinfeld, B., Albert, I., Porfiri, E., Fiol, C., Munemitsu, S. and Polakis, P. (1996) Binding of GSK3β to the APC-β-catenin complex and regulation of complex assembly. Science, 272, 1023-1026.
47. Ruel, L., Bourouis, M., Heitzler, P., Pantesco, V. and Simpson, P. (1993) Drosophila shaggy kinase and rat glycogen synthase kinase-3 have conserved activities and act downstream of Notch. Nature, 362, 557-560.
48. Siegfried, E., Chou, T.B. and Perrimon, N. (1992) Wingless signaling acts through Zeste-white, 3, the Drosophila homolog of Glycogen synthase kinase-3, to regulate engrailed and establish cell fate. Cell, 71, 1167-1179.
49. van de Wetering, M. et al. (1997) Armadillo coactivates transcription driven by the product of the Drosophila segment polarity gene dTcf. Cell, 88, 789-799.
50. Waltzer, L. and Bienz, M. (1998) Drosophila CBP represses the transcription factor TCF to antagonize Wingless signalling. Nature, 395, 521-525.
51. Yano, R., Oakes, M.L., Tabb, M.M. and Nomura, M. (1994) Yeast Srp 1p has homology to armadillo/plakoglobin/β-catenin and participates in apparently multiple nuclear functions including the maintenance of the nucleolar structure. Proc. Natl Acad. Sci. USA, 91, 6880-6884.
52. Zhang, J. and Carthew, R. (1998) Interactions between Wingless and Dfz2 during Drosophila wing development. Development, 125, 3075-3085.