C-terminal-binding protein directly activates and represses Wnt transcriptional targets in Drosophila

EMBO Journal

Volumn 25, Issue 12, 2006, Pages 2735-2745

  Fang, Ming ^a   Li, Jiong ^a   Blauwkamp, Timothy ^a   Bhambhani, Chandan ^a   Campbell, Nathan ^a,b   Cadigan, Ken M ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

Armadillo; CtBP; TCF; Wingless; Wnt

Indexed keywords

BETA CATENIN; C TERMINAL BINDING PROTEIN; DNA BINDING PROTEIN; REPRESSOR PROTEIN; T CELL FACTOR PROTEIN; UNCLASSIFIED DRUG; WNT PROTEIN;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DROSOPHILA; GENE REPRESSION; GENETIC TRANSCRIPTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

ALCOHOL OXIDOREDUCTASES; ANIMALS; ARMADILLO DOMAIN PROTEINS; CELLS, CULTURED; DNA-BINDING PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; ENHANCER ELEMENTS (GENETICS); EYE; MODELS, BIOLOGICAL; PHOSPHOPROTEINS; PROTEIN BINDING; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; TCF TRANSCRIPTION FACTORS; TRANS-ACTIVATION (GENETICS); TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; WNT PROTEINS;

ARMADILLO;

EID: 33745542960     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7601153     Document Type: Article

References (59)

1. Barker N, Hurlstone A, Musisi H, Miles A, Bienz M, Clevers H (2001) The chromatin remodelling factor Brg-1 interacts with beta-catenin to promote target gene activation. EMBO J 20: 4935-4943
2. Barolo S, Posakony JW (2002) Three habits of highly effective signaling pathways: principles of transcriptional control by developmental cell signaling. Genes Dev 16: 1167-1181
3. Bauer A, Huber O, Usseglio F, Rothbacher U, Aragnol D, Kemler R, Pradel J (2000) Pontin 52 and reptin 52 function as antagonistic regulators of beta-catenin signalling activity. EMBO J 19: 6121-6130
4. Brannon M, Brown JD, Bates R, Kimelman D, Moon RT (1999) XCtBP is a XTcf-3 co-repressor with roles throughout Xenopus development. Development 126: 3159-3170
5. Cadigan KM (2002) Regulating morphogen gradients in the Drosophila wing. Semin Cell Dev Biol 13: 83-90
6. Cadigan KM, Fish MP, Rulifson EJ, Nusse R (1998) Wingless repression of Drosophila frizzled 2 expression shapes the Wingless morphogen gradient in the wing. Cell 93: 767-777
7. Cadigan KM, Jou AD, Nusse R (2002) Wingless blocks bristle formation and morphogenetic furrow progression in the eye through repression of Daughterless. Development 129: 3393-3402
8. Cadigan KM, Nusse R (1997) Wnt signaling: a common theme in animal development. Genes Dev 11: 3286-3305
9. Cavallo RA, Cox RT, Moline MM, Roose J, Polevoy GA, Clevers H, Peifer M, Bejsovec A (1998) Drosophila Tcf and Groucho interact to repress Wingless signalling activity. Nature 395: 604-608
10. Chan SK, Struhl G (2002) Evidence that armadillo transduces wingless by mediating nuclear export or cytosolic activation of pangolin. Cell 111: 265-280
11. Chinnadurai G (2002) CtBP, an unconventional transcriptional corepressor in development and oncogenesis. Mol Cell 9: 213-224
12. Clemens JC, Worby CA, Simonson-Leff N, Muda M, Maehama T, Hemmings BA, Dixon JE (2000) Use of double-stranded RNA interference in Drosophila cell lines to dissect signal transduction pathways. Proc Natl Acad Sci USA 97: 6499-6503
13. Cox RT, Pai LM, Kirkpatrick C, Stein J, Peifer M (1999) Roles of the C terminus of Armadillo in Wingless signaling in Drosophila. Genetics 153: 319-332
14. Daniels DL, Eklof Spink K, Weis WI (2001) Beta-catenin: molecular plasticity and drug design. Trends Biochem Sci 26: 672-678
15. Daniels DL, Weis WI (2005) Beta-catenin directly displaces Groucho/TLE repressors from Tcf/Lef in Wnt-mediated transcription activation. Nat Struct Mol Biol 12: 364-371
16. DasGupta R, Kaykas A, Moon RT, Perrimon N (2005) Functional genomic analysis of the Wnt-wingless signaling pathway. Science 308: 826-833
17. Ding Y, Dale T (2002) Wnt signal transduction: kinase cogs in a nano-machine? Trends Biochem Sci 27: 327-329
18. Freeman M, Bienz M (2001) EGF receptor/Rolled MAP kinase signalling protects cells against activated Armadillo in the Drosophila eye. EMBO Rep 2: 157-162
19. Fujita N, Jaye DL, Kajita M, Geigerman C, Moreno CS, Wade PA (2003) MTA3, a Mi-2/NuRD complex subunit, regulates an invasive growth pathway in breast cancer. Cell 113: 207-219
20. Gallet A, Angelats C, Erkner A, Charroux B, Fasano L, Kerridge S (1999) The C-terminal domain of armadillo binds to hypophosphorylated teashirt to modulate wingless signalling in Drosophila. EMBO J 18: 2208-2217
21. Goto A, Aoki M, Ichihara S, Kitagawa Y (2001) Alpha-, beta- or gamma-chain-specific RNA interference of laminin assembly in Drosophila Kc167 cells. Biochem J 360: 167-172
22. Grooteclaes M, Deveraux Q, Hildebrand J, Zhang Q, Goodman RH, Frisch SM (2003) C-terminal-binding protein corepresses epithelial and proapoptotic gene expression programs. Proc Natl Acad Sci USA 100: 4568-4573
23. Hamada F, Bienz M (2004) The APC tumor suppressor binds to C-terminal binding protein to divert nuclear beta-catenin from TCF. Dev Cell 7: 677-685
24. Hecht A, Vleminckx K, Stemmler MP, van Roy F, Kemler R (2000) The p300/CBP acetyltransferases function as transcriptional coactivators of beta-catenin in vertebrates. EMBO J 19: 1839-1850
25. Hildebrand JD, Soriano P (2002) Overlapping and unique roles for C-terminal binding protein 1 (CtBP1) and CtBP2 during mouse development. Mol Cell Biol 22: 5296-5307
26. Hoffmans R, Basler K (2004) Identification and in vivo role of the Armadillo-Legless interaction. Development 131: 4393-4400
27. Hoffmans R, Stadeli R, Basler K (2005) Pygopus and legless provide essential transcriptional coactivator functions to armadillo/beta-catenin. Curr Biol 15: 1207-1211
28. Hsu SC, Galceran J, Grosschedl R (1998) Modulation of transcriptional regulation by LEF-1 in response to Wnt-1 signaling and association with beta-catenin. Mol Cell Biol 18: 4807-4818
29. Knirr S, Frasch M (2001) Molecular integration of inductive and mesoderm-intrinsic inputs governs even-skipped enhancer activity in a subset of pericardial and dorsal muscle progenitors. Dev Biol 238: 13-26
30. Kramps T, Peter O, Brunner E, Nellen D, Froesch B, Chatterjee S, Murone M, Zullig S, Basler K (2002) Wnt/wingless signaling requires BCL9/legless-mediated recruitment of pygopus to the nuclear beta-catenin-TCF complex. Cell 109: 47-60
31. Kumar V, Carlson JE, Ohgi KA, Edwards TA, Rose DW, Escalante CR, Rosenfeld MG, Aggarwal AK (2002) Transcription corepressor CtBP is an NAD(+)-regulated dehydrogenase. Mol Cell 10: 857-869
32. Lee HH, Frasch M (2000) Wingless effects mesoderm patterning and ectoderm segmentation events via induction of its downstream target sloppy paired. Development 127: 5497-5508
33. Logan CY, Nusse R (2004) The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 20: 781-810
34. Lum L, Yao S, Mozer B, Rovescalli A, Von Kessler D, Nirenberg M, Beachy PA (2003) Identification of Hedgehog pathway components by RNAi in Drosophila cultured cells. Science 299: 2039-2045
35. Nibu Y, Zhang H, Levine M (1998) Interaction of short-range repressors with Drosophila CtBP in the embryo. Science 280: 101-104
36. Nolo R, Abbott LA, Bellen HJ (2000) Senseless, a Zn finger transcription factor, is necessary and sufficient for sensory organ development in Drosophila. Cell 102: 349-362
37. Panganiban G, Sebring A, Nagy L, Carroll S (1995) The development of crustacean limbs and the evolution of arthropods. Science 270: 1363-1366
38. Parker DS, Jemison J, Cadigan KM (2002) Pygopus, a nuclear PHD-finger protein required for Wingless signaling in Drosophila. Development 129: 2565-2576
39. Phippen TM, Sweigart AL, Moniwa M, Krumm A, Davie JR, Parkhurst SM (2000) Drosophila C-terminal binding protein functions as a context-dependent transcriptional co-factor and interferes with both mad and groucho transcriptional repression. J Biol Chem 275: 37628-37637
40. Pinto D, Clevers H (2005) Wnt, stem cells and cancer in the intestine. Biol Cell 97: 185-196
41. Polakis P (2000) Wnt signaling and cancer. Genes Dev 14: 1837-1851
42. Poortinga G, Watanabe M, Parkhurst SM (1998) Drosophila CtBP: a hairy-interacting protein required for embryonic segmentation and hairy-mediated transcriptional repression. EMBO J 17: 2067-2078
43. Primus A, Freeman G (2004) The cnidarian and the canon: the role of Wnt/beta-catenin signaling in the evolution of metazoan embryos. Bioessays 26: 474-478
44. Riese J, Yu X, Munnerlyn A, Eresh S, Hsu SC, Grosschedl R, Bienz M (1997) LEF-1, a nuclear factor coordinating signaling inputs from wingless and decapentaplegic. Cell 88: 777-787
45. Robertson HM, Preston CR, Phillis RW, Johnson-Schlitz DM, Benz WK, Engels WR (1988) A stable genomic source of P element transposase in Drosophila melanogaster. Genetics 118: 461-470
46. Roose J, Clevers H (1999) TCF transcription factors: molecular switches in carcinogenesis. Biochim Biophys Acta 1424: M23-M37
47. Roose J, Molenaar M, Peterson J, Hurenkamp J, Brantjes H, Moerer P, van de Wetering M, Destree O, Clevers H (1998) The Xenopus Wnt effector XTcf-3 interacts with Groucho-related transcriptional repressors. Nature 395: 608-612
48. Schaeper U, Boyd JM, Verma S, Uhlmann E, Subramanian T, Chinnadurai G (1995) Molecular cloning and characterization of a cellular phosphoprotein that interacts with a conserved C-terminal domain of adenovirus E1A involved in negative modulation of oncogenic transformation. Proc Natl Acad Sci USA 92: 10467-10471
49. Sierra J, Yoshida T, Joazeiro CA, Jones KA (2006) The APC tumor suppressor counteracts b-catenin activation and H3K4 methylation at Wnt target genes. Genes Dev 20: 586-600
50. Sosinsky A, Bonin CP, Mann RS, Honig B (2003) Target explorer: an automated tool for the identification of new target genes for a specified set of transcription factors. Nucleic Acids Res 31: 3589-3592
51. Takemaru KI, Moon RT (2000) The transcriptional coactivator CBP interacts with beta-catenin to activate gene expression. J Cell Biol 149: 249-254
52. Thompson BJ (2004) A complex of Armadillo, Legless, and Pygopus coactivates dTCF to activate wingless target genes. Curr Biol 14: 458-466
53. Toba G, Ohsako T, Miyata N, Ohtsuka T, Seong KH, Aigaki T (1999) The gene search system. A method for efficient detection and rapid molecular identification of genes in Drosophila melanogaster. Genetics 151: 725-737
54. Valenta T, Lukas J, Korinek V (2003) HMG box transcription factor TCF-4's interaction with CtBP1 controls the expression of the Wnt target Axin2/Conductin in human embryonic kidney cells. Nucleic Acids Res 31: 2369-2380
55. van de Wetering M, Cavallo R, Dooijes D, van Beest M, van Es J, Loureiro J, Ypma A, Hursh D, Jones T, Bejsovec A, Peifer M, Mortin M, Clevers H (1997) Armadillo coactivates transcription driven by the product of the Drosophila segment polarity gene dTCF. Cell 88: 789-799
56. van Es JH, Barker N, Clevers H (2003) You Wnt some, you lose some: oncogenes in the Wnt signaling pathway. Curr Opin Genet Dev 13: 28-33
57. Willert K, Brown JD, Danenberg E, Duncan AW, Weissman IL, Reya T, Yates III JR, Nusse R (2003) Wnt proteins are lipid-modified and can act as stem cell growth factors. Nature 423: 448-452
58. Yang X, van Beest M, Clevers H, Jones T, Hursh DA, Mortin MA (2000) Decapentaplegic is a direct target of dTcf repression in the Drosophila visceral mesoderm. Development 127: 3695-3702
59. Zeng W, Wharton Jr KA, Mack JA, Wang K, Gadbaw M, Suyama K, Klein PS, Scott MP (2000) Naked cuticle encodes an inducible antagonist of Wnt signalling. Nature 403: 789-795