Pygopus and Legless target Armadillo/β-catenin to the nucleus to enable its transcriptional co-activator function

Nature Cell Biology

Volumn 6, Issue 7, 2004, Pages 626-633

  Townsley, Fiona M ^a   Cliffe, Adam ^a   Bienz, Mariann ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; APC PROTEIN; BETA CATENIN; NUCLEAR PROTEIN; PROTEIN LEGLESS; PROTEIN PYGOPUS; T CELL FACTOR PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; WNT PROTEIN;

ARTICLE; CANCER CELL; CELL ANCHORAGE; CELL MUTANT; CELL NUCLEUS; CELLULAR DISTRIBUTION; CHROMATIN STRUCTURE; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; EMBRYO CELL; GENE TARGETING; GENETIC TRANSCRIPTION; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; ARMADILLO DOMAIN PROTEINS; CARRIER PROTEINS; CELL NUCLEUS; COS CELLS; CYTOSKELETAL PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; GENES, LETHAL; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MACROMOLECULAR SUBSTANCES; MUTATION; NEOPLASMS; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS; SIGNAL TRANSDUCTION; TRANS-ACTIVATION (GENETICS); TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; WNT PROTEINS;

ARACHNIDA; ARMADILLO; DROSOPHILA MELANOGASTER; HEXAPODA; MELANOGASTER;

EID: 3242706980     PISSN: 14657392     EISSN: None     Source Type: Journal    
DOI: 10.1038/ncb1141     Document Type: Article

References (37)

1. Cadigan, K. M. & Nusse, R. Wnt signaling: a common theme in animal development. Genes Dev. 11, 3286-3305 (1997).
2. Polakis, P. Wnt signaling and cancer. Genes Dev. 14, 1837-1851 (2000).
3. Hecht, A., Vleminckx, K., Stemmler, M. P., van Roy, F. & Kemler, R. The p300/CBP acetyltransferases function as transcriptional coactivators of β-catenin in vertebrates. EMBO J. 19, 1839-1850 (2000).
4. Takemaru, K. I. & Moon, R. T. The transcriptional coactivator CBP interacts with β-catenin to activate gene expression. J. Cell Biol. 149, 249-254 (2000).
5. Barker, N. et al. The chromatin remodelling factor Brg-1 interacts with β-catenin to promote target gene activation. EMBO J. 20, 4935-4943 (2001).
6. Bienz, M. & Clevers, H. Armadillo/β-catenin signals in the nucleus - proof beyond a reasonable doubt? Nature Cell Biol. 5, 179-182 (2003).
7. Kramps, T. et al. Wnt/wingless signaling requires BCL9/Legless-mediated recruitment of Pygopus to the nuclear β-catenin-TCF complex. Cell 109, 47-60 (2002).
8. Thompson, B., Townsley, F. M., Rosin-Arbesfeld, R., Musisi, H. & Bienz, M. A new nuclear component of the Wnt signalling pathway. Nature Cell Biol. 4, 367-373 (2002).
9. Parker, D. S., Jemison, J. & Cadigan, K. M. Pygopus, a nuclear PHD-finger protein required for Wingless signaling in Drosophila. Development 129, 2565-2576 (2002).
10. Belenkaya, T. Y. et al. Pygopus encodes a nuclear protein essential for Wingless/Wnt signaling. Development 129, 4089-4101 (2002).
11. Townsley, F. M., Thompson, B. & Bienz, M. Pygopus residues required for its binding to Legless are critical for transcription and development. J. Biol. Chem. 279, 5177-5183 (2004).
12. Thompson, B. J. A Complex of Armadillo, Legless, and Pygopus coactivates dTCF to activate Wingless target genes. Curr. Biol. 14, 458-466 (2004).
13. Kudo, N. et al. Leptomycin B inhibition of signal-mediated nuclear export by direct binding to CRM1. Exp. Cell Res. 242, 540-547 (1998).
14. Fagotto, F., Gluck, U. & Gumbiner, B. M. Nuclear localization signal-independent and importin/karyopherin-independent nuclear import of β-catenin. Curr. Biol. 8, 181-190 (1998).
15. Yokoya, F., Imamoto, N., Tachibana, T. & Yoneda, Y. β-catemn can be transported into the nucleus in a Ran-unassisted manner. Mol. Biol. Cell 10, 1119-1131 (1999).
16. Wiechens, N. & Fagotto, F. CRM1- and Ran-independent nuclear export of β-catenin. Curr. Biol. 11, 18-27 (2001).
17. Rosin-Arbesfeld, R., Cliffe, A., Brabletz, T. & Bienz, M. Nuclear export of the APC tumour suppressor controls β-catenin function in transcription. EMBO J. 22, 1101-1113 (2003).
18. Peifer, M. & Wieschaus, E. The segment polarity gene armadillo encodes a functionally modular protein that is the Drosophila homolog of human plakoglobin. Cell 63, 1167-1176 (1990).
19. Peifer, M., Sweeton, D., Casey, M. & Wieschaus, E. Wingless signal and Zeste-white 3 kinase trigger opposing changes in the intracellular distribution of Armadillo, Development 120, 369-380 (1994).
20. Tolwinski, N. S. & Wieschaus, E. Armadillo nuclear import is regulated by cytoplasmic anchor Axin and nuclear anchor dTCF/Pan. Development 128, 2107-2117 (2001).
21. Zecca, M., Basler, K. & Struhl, G. Direct and long-range action of a Wingless morphogen gradient. Cell 87, 833-844 (1996).
22. Rowan, A. J. et al. APC mutations in sporadic colorectal tumors: A mutational 'hotspot' and interdependence of the 'two hits'. Proc. Natl Acad. Sci. USA 97, 3352-3357 (2000).
23. Rosin-Arbesfeld, R., Townsley, F. & Bienz, M. The APC tumour suppressor has a nuclear export function. Nature 406, 1009-1012 (2000).
24. Zhang, F., White, R. L. & Neufeld, K. L. Cell density and phosphorylation control the subcellular localization of Adenomatous Polyposis Coli protein. Mol. Cell. Biol. 21, 8143-8156 (2001).
25. -/- colon carcinoma. Science 275, 1784-1787 (1997).
26. Cox, R. T. et al. Membrane-tethered Drosophila Armadillo cannot transduce Wingless signal on its own. Development 126, 1327-1335 (1999).
27. Miller, J. R. & Moon, R. T. Analysis of the signaling activities of localization mutants of β-catenin during axis specification in Xenopus. J. Cell Biol. 139, 229-243 (1997).
28. Pai, L. M., Orsulic, S., Bejsovec, A. & Peifer, M. Negative regulation of Armadillo, a Wingless effector in Drosophila. Development 124, 2255-2266 (1997).
29. Perrimon, N. The genetic basis of patterned baldness in Drosophila. Cell 76, 781-784 (1994).
30. Kalderon, D., Roberts, B. L., Richardson, W. D. & Smith, A. E. A short amino acid sequence able to specify nuclear location. Cell 39, 499-509 (1984).
31. Hamada, F. et al. Negative regulation of Wingless signaling by D-axin, a Drosophila homolog of axin. Science 283, 1739-1742 (1999).
32. Ahmed, Y., Nouri, A. & Wieschaus, E. Drosophila Apc1 and Apc2 regulate Wingless transduction throughout development. Development 129, 1751-1762 (2002).
33. Akong, K. et al. Drosophila APC2 and APC1 play overlapping roles in Wingless signaling in the embryo and imaginal discs. Dev. Biol. 250, 91-100 (2002).
34. Hsu, S. C., Galceran, J. & Grosschedl, R. Modulation of transcriptional regulation by LEF-1 in response to Wnt-1 signaling and association with β-catenin. Mol. Cell. Biol. 18, 4807-4818 (1998).
35. Gozani, O. et al. The PHD finger of the chromatin-associated protein ING2 functions as a nuclear phosphoinositide receptor. Cell 114, 99-111 (2003).
36. Huh, W. K. et al. Global analysis of protein localization in budding yeast. Nature 425, 686-691 (2003).
37. Aasland, R., Gibson, T. J. & Stewart, A. F. The PHD finger: implications for chromatin-mediated transcriptional regulation. Trends Biochem. Sci. 20, 56-59 (1995).