TCF transcription factors: Molecular switches in carcinogenesis

Biochimica et Biophysica Acta - Reviews on Cancer

Volumn 1424, Issue 2-3, 1999, Pages

  Roose, Jeroen ^a,b   Clevers, Hans ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Adenomatous polyposis coli tumor suppressor gene; cAMP response element binding binding protein; Cancer; CtBP; Groucho; Mutation; T cell factor lymphoid enhancer factor expression; T cell factor lymphoid enhancer factor knock out mouse; T cell factor lymphoid enhancer factor transcription factor; Wnt signaling; Catenin

Indexed keywords

BETA CATENIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; LYMPHOID ENHANCER FACTOR 1; TRANSCRIPTION FACTOR;

ADENOMATOUS POLYP; ANIMAL EXPERIMENT; ANIMAL MODEL; CARCINOGENESIS; CONTROLLED STUDY; GENE ACTIVATION; GENE MUTATION; KNOCKOUT MOUSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SHORT SURVEY; SIGNAL TRANSDUCTION; T LYMPHOCYTE; TUMOR SUPPRESSOR GENE;

ANIMALIA; ARMADILLO;

EID: 0032830931     PISSN: 0304419X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0304-419X(99)00026-8     Document Type: Review

References (120)

1. H. Aberle, A. Bauer, J. Stappert, A. Kispert, R. Kemler, β-Catenin is a target for the ubiquitin-proteasome pathway, EMBO J. 16 (1997) 3797.
2. B.D. Aronson, A.L. Fisher, K. Blechman, M. Caudy, J.P. Gergen, Groucho-dependent and -independent repression activities of Runt domain proteins, Mol. Cell Biol. 17 (1997) 5581.
3. J. Behrens, B.A. Jerchow, M. Wurtele, J. Grimm, C. Asbrand, R. Wirtz, M. Kuhl, D. Wedlich, W. Birchmeier, Functional interaction of an axin homolog, conductin, with β-catenin, APC, and GSK3β, Science 280 (1998) 596.
4. J. Behrens, J.P. von Kries, M. Kuhl, L. Bruhn, D. Wedlich, R. Grosschedl, W. Birchmeier, Functional interaction of β-catenin with the transcription factor LEF-1, Nature 382 (1996) 638.
5. P. Bhanot, M. Brink, C.H. Samos, J.C. Hsieh, Y. Wang, J.P. Macke, D. Andrew, J. Nathans, R. Nusse, A new member of the frizzled family from Drosophila functions as a Wingless receptor, Nature 382 (1996) 225.
6. M. Brannon, M. Gomperts, L. Sumoy, R.T. Moon, D. Kimelman, A β-catenin/XTcf-3 complex binds to the siamois promoter to regulate dorsal axis specification in Xenopus, Genes Dev. 11 (1997) 2359.
7. M. Brannon, J.D. Brown, R. Bates, D. Kimmelman, R. Moon, XCtBP is a XTcf-3 co-repressor with roles throughout Xenopus development, Development 126 (1999) 3159.
8. L. Bruhn, A. Munnerlyn, R. Grosschedl, ALY, a context-dependent coactivator of LEF-1 and AML-1, is required for TCRα enhancer function, Genes Dev. 11 (1997) 640.
9. E. Brunner, O. Peter, L. Schweizer, K. Basler, Pangolin encodes a Lef-1 homologue that acts downstream of Armadillo to transduce the Wingless signal in Drosophila, Nature 385 (1997) 829.
10. C.V. Cabrera, M.C. Alonso, P. Johnston, R.G. Phillips, P.A. Lawrence, Phenocopies induced with antisense RNA identify the wingless gene, Cell 50 (1987) 659.
11. K.M. Cadigan, R. Nusse, Wnt signaling: a common theme in animal development, Genes Dev. 11 (1997) 3286.
12. R. Calvert, P. Pothier, Migration of fetal intestinal intervillous cells in neonatal mice, Anat. Rec. 227 (1990) 199.
13. P. Carlsson, M.L. Waterman, K.A. Jones, The hLEF/TCF-1 a HMG protein contains a context-dependent transcriptional activation domain that induces the TCR α enhancer in T cells, Genes Dev. 7 (1993) 2418.
14. J. Castrop, K. van Norren, H. Clevers, A gene family of HMG box transcription factors with homology to TCF-1, Nucleic Acids Res. 20 (1992) 611.
15. R. Cavallo, R. Cox, M. Moline, J. Roose, G. Polevoy, H. Clevers, M. Peifer, A. Bejsovec, Drosophila Tcf and Groucho interact to repress Wingless signalling activity, Nature 395 (1998) 604.
16. E.F. Chan, U. Gat, J.M. McNiff, E. Fuchs, A common human skin tumor is caused by activating mutations in β-catenin, Nat. Genet. 21 (1999) 410.
17. H. Clevers, M. van de Wetering, TCF/LEF factor earn their wings, Trends Genet. 13 (1997) 485.
18. D. Cook, M.J. Fry, K. Hughes, R. Sumathipala, J.R. Woodgett, T.C. Dale, Wingless inactivates glycogen synthase kinase-3 via an intracellular signalling pathway which involves a protein kinase C, EMBO J. 15 (1996) 4526.
19. A. de La Coste, B. Romagnolo, P. Billuart, C.A. Renard, M.A. Buendia, O. Soubrane, M. Fabre, J. Chelly, C. Beldjord, A. Kahn, C. Perret, Somatic mutations of the β-catenin gene are frequent in mouse and human hepatocellular carcinomas, Proc. Natl. Acad. Sci. USA 95 (1998) 8847.
20. S. DiNardo, E. Sher, J. Heemskerk Jongens, J.A. Kassis, P.H. O'Farrell, Two-tiered regulation of spatially patterned engrailed gene expression during Drosophila embryogenesis, Nature 332 (1988) 604.
21. T. Dubnicoff, S. Valentine, G. Chen, T. Shi, J. Lengyel, Z. Paroush, A. Courey, Conversion of Dorsal from an activator to a repressor by the global corepressor Groucho, Genes Dev. 11 (1997) 2952.
22. A.L. Fisher, M. Caudy, Groucho proteins: transcriptional corepressors for specific subsets of DNA-binding transcription factors in vertebrates and invertebrates, Genes Dev. 12 (1998) 1931.
23. A.L. Fisher, S. Ohsako, M. Caudy, The WRPW motif of the hairy-related basic helix-loop-helix repressor proteins acts as a 4-amino-acid transcription repression and protein-protein interaction domain, Mol. Cell Biol. 16 (1996) 2670.
24. N. Funayama, F. Fagotto, P. McCrea, B.M. Gumbiner, Embryonic axis induction by the armadillo repeat domain of β-catenin: evidence for intracellular signaling, J. Cell Biol. 128 (1995) 959.
25. -/- mice, Genes Dev. 13 (1999) 709.
26. J. Gastrop, R. Hoevenagel, J.R. Young, H.C. Clevers, A common ancestor of the mammalian transcription factors TCF-1 and TCF-1 α/LEF-1 expressed in chicken T cells, Eur. J. Immunol. 22 (1992) 1327.
27. U. Gat, R. DasGoupta, L. Degenstein, E. Fuchs, De novo hair follicle morphogenesis and hair tumors in mice expressing a truncated β-catenin in skin, Cell 95 (1998) 1.
28. K. Giese, J. Cox, R. Grosschedl, The HMG domain of lymphoid enhancer factor 1 bends DNA and facilitates assembly of functional nucleoprotein structures, Cell 69 (1992) 185.
29. K. Giese, R. Grosschedl, LEF-1 contains an activation domain that stimulates transcription only in a specific context of factor-binding sites, EMBO J. 12 (1993) 4667.
30. K. Giese, C. Kingsley, J. Kirshner, R. Grosschedl, Assembly and function of a TCR alpha enhancer complex is dependent on LEF-1-induced DNA bending and multiple protein-protein interactions, Genes Dev. 9 (1995) 995.
31. D.I. Godfrey, A. Zlotnik, Control points in early T-cell development, Immunol. Today 14 (1993) 547.
32. M. Han, Gut reaction to Wnt signaling in worms, Cell 90 (1997) 581.
33. M. Hart, J.P. Concordet, I. Lassot, I. Albert, R. del los Santos, H. Durand, C. Perret, B. Rubinfeld, F. Margottin, R. Bernarous, P. Polakis, The F-box protein β-TrCP associates with phosphorylated β-catenin and regulates its activity in te cell, Curr. Biol. 8 (1998) 573.
34. D.A. Hartley, A. Preiss, S. Artavanis Tsakonas, A deduced gene product from the Drosophila neurogenic locus, enhancer of split, shows homology to mammalian G-protein β subunit, Cell 55 (1988) 785.
35. S. Hayashi, B. Rubinfeld, B. Souza, P. Polakis, E. Wieschaus, A.J. Levine, A Drosophila homolog of the tumor suppressor gene adenomatous polyposis coli down-regulates β-catenin but its zygotic expression is not essential for the regulation of Armadillo, Proc. Natl. Acad. Sci. USA 94 (1997) 242.
36. X. He, J.P. Saint Jeannet, J.R. Woodgett, H.E. Varmus, I.B. Dawid, Glycogen synthase kinase-3 and dorsoventral patterning in Xenopus embryos, Nature 374 (1995) 617.
37. T.C. He, A.B. Sparks, C. Rago, H. Hermeking, L. Zawel, L.T. da Costa, P.J. Morin, B. Vogelstein, K.W. Kinzler, Identification of c-MYC as a target of the APC pathway, Science 281 (1998) 1509.
38. J. Heasman, A. Crawford, K. Goldstone, P. Garner Hamrick, B. Gumbiner, P. McCrea, C. Kintner, C.Y. Noro, C. Wylie, Overexpression of cadherins and underexpression of β-catenin inhibit dorsal mesoderm induction in early Xenopus embryos, Cell 79 (1994) 791.
39. O. Huber, R. Korn, J. McLaughlin, M. Ohsugi, B.G. Herrmann, R. Kemler, Nuclear localization of β-catenin by interaction with transcription factor LEF-1, Mech. Dev. 59 (1996) 3.
40. T. Ishitani, J. Ninomiya-Tsuji, S. Nagai, M. Nishita, M. Meneghini, N. Barker, M. Waterman, B. Bowerman, H. Clevers, H. Shibaya, K. Matsumoto, The TAK1-NLK-MAPK-related pathway antagonizes signalling between β-catenin and transcription factor TCF, Nature 399 (1999) 798.
41. G. Jimenez, Z. Paroush, D. Ish Horowicz, Groucho acts as a corepressor for a subset of negative regulators, including Hairy and Engrailed, Genes Dev. 11 (1997) 3072.
42. K.W. Kinzler, B. Vogelstein, Lessons from hereditary colorectal cancer, Cell 87 (1996) 159.
43. J. Klingensmith, R. Nusse, N. Perrimon, The Drosophila segment polarity gene dishevelled encodes a novel protein required for response to the wingless signal, Genes Dev. 8 (1994) 118.
44. K.E. Koop, L.M. MacDonald, C.G. Lobe, Transcripts of Grg4, a murine groucho-related gene, are detected in adjacent tissues to other murine neurogenic gene homologues during embryonic development, Mech. Dev. 59 (1996) 73.
45. V. Korinek, N. Barker, P. Moerer, E. van Donselaar, G. Huls, P.J. Peters, H. Clevers, Depletion of epithelial stemcell compartments in the small intestine of mice lacking Tcf-4, Nat. Genet. 19 (1998) 379.
46. V. Korinek, N. Barker, P.J. Morin, D. van Wichen, R. de Weger, K.W. Kinzler, B. Vogelstein, H. Clevers, Constitutive transcriptional activation by a β-catenin-Tcf complex in APC-/- colon carcinoma, Science 275 (1997) 1784.
47. V. Korinek, N. Barker, K. Willert, M. Molenaar, J. Roose, G. Wagenaar, M. Markman, W. Lamers, O. Destree, H. Clevers, Two members of the Tcf family implicated in Wnt/β-catenin signaling during embryogenesis in the mouse, Mol. Cell. Biol. 18 (1998) 1248.
48. K. Kratochwil, M. Dull, I. Farinas, J. Galceran, R. Grosschedl, Lef1 expression is activated by BMP-4 and regulates inductive tissue interactions in tooth and hair development, Genes Dev. 10 (1996) 1382.
49. E. Latres, D. Chiaur, M. Pagano, The human F box protein β-Trcp associates with the Cul1/Skp1 complex and regulates the stability of β-catenin, Oncogene 18 (1999) 849.
50. C. Leon, C.G. Lobe, Grg3, a murine Groucho-related gene, is expressed in the developing nervous system and in mesenchyme-induced epithelial structures, Dev. Dyn. 208 (1997) 11.
51. R. Lin, S. Thompson, J.R. Priess, pop-1 encodes an HMG box protein required for the specification of a mesoderm precursor in early C. elegans embryos, Cell 83 (1995) 599.
52. C. Liu, Y. Kato, Z. Zhang, V.M. Do, B.A. Yanker, X. He, β-Trcp couples β-catenin phosphorylation-degradation and regulates Xenopus axis formation, Proc. Natl. Acad. Sci. USA 96 (1999) 6273.
53. J.J. Love, X. Li, D.A. Case, K. Giese, R. Grosschedl, P.E. Wright, Structural basis for DNA bending by the architectural transcription factor LEF-1, Nature 376 (1995) 791.
54. M. Mallo, F. Franco del Amo, T. Gridley, Cloning and developmental expression of Grg, a mouse gene related to the groucho transcript of the Drosophila enhancer of split complex, Mech. Dev. 42 (1993) 67.
55. T. Mayall, P. Sheridan, M. Montminy, K. Jones, Distinct roles for P-CREB and LEF-1 in TCR α enhancer assembly and activation on chromatin templates in vitro, Genes Dev. 11 (1997) 887.
56. K. Mayer, E. Wolff, H. Clevers, W.G. Ballhausen, The human high mobility group (HMG)-box transcription factor TCF-1: novel isoforms due to alternative splicing and usage of a new exon IXA, Biochim. Biophys. Acta 1263 (1995) 169.
57. K. Mayer, T. Hieronymus, J. Castrop, H. Clevers, W. Ballhausen, Ectopic activation of lymphoid high mobility group-box transcription factor TCF-1 and overexpression in colorectal cancer cells, Int. J. Cancer 72 (1997) 625.
58. P.D. McCrea, C.W. Turck, B. Gumbiner, A homolog of the armadillo protein in Drosophila (plakoglobin) associated with E-cadherin, Science 254 (1991) 1359.
59. A.P. McMahon, R.T. Moon, Ectopic expression of the proto-oncogene int-1 in Xenopus embryos leads to duplication of the embryonic axis, Cell 58 (1989) 1075.
60. M.D. Meneghini, T. Ishitani, J.C. Carter, N. Hisamoto, J. Ninomiga-Tsuji, C.J. Thorpe, D.R. Hamill, K. Matsumoto, B. Bowerman, MAP kinase and Wnt pathways converge to downregulate an HMG-domain repressor in Caenorhabditis elegans, Nature 399 (1999) 793.
61. J.R. Miller, R.T. Moon, Signal transduction through β-catenin and specification of cell fate during embryogenesis, Genes Dev. 10 (1996) 2527.
62. H. Miyasaka, B.K. Choudhury, E.W. Hou, S.S. Li, Molecular cloning and expression of mouse and human cDNA encoding AES and ESG proteins with strong similarity to Drosophila enhancer of split groucho protein, Eur. J. Biochem. 216 (1993) 343.
63. M. Molenaar, M. van de Wetering, M. Oosterwegel, J. Peterson Maduro, S. Godsave, V. Korinek, J. Roose, O. Destree, H. Clevers, XTcf-3 transcription factor mediates β-catenin-induced axis formation in Xenopus embryos, Cell 86 (1996) 391.
64. M. Molenaar, J. Roose, J. Peterson, S. Venanzi, H. Clevers, O. Destree, Differential expression of the HMG box transcription factors XTcf-3 and XLef-1 during early Xenopus development, Mech. Dev. 75 (1998) 151.
65. R.T. Moon, J.D. Brown, M. Torres, WNTs modulate cell fate and behavior during vertebrate development, Trends Genet. 13 (1997) 157.
66. P.J. Morin, A.B. Sparks, V. Korinek, N. Barker, H. Clevers, B. Vogelstein, K.W. Kinzler, Activation of β-catenin-Tcf signaling in colon cancer by mutations in β-catenin or APC, Science 275 (1997) 1787.
67. A.R. Moser, H.C. Pitot, W.F. Dove, A dominant mutation that predisposes to multiple intestinal neoplasia in the mouse, Science 247 (1990) 322.
68. S. Munemitsu, I. Albert, B. Souza, B. Rubinfeld, P. Polakis, Regulation of intracellular β-catenin levels by the adenomatous polyposis coli (APC) tumor-suppressor protein, Proc. Natl. Acad. Sci. USA 92 (1995) 3046.
69. A. Nagafuchi, M. Takeichi, Transmembrane control of cadherin-mediated cell adhesion: a 94 kDa protein functionally associated with a specific region of the cytoplasmic domain of E-cadherin, Cell Regul. 1 (1989) 37.
70. H. Nakagawa, Y. Murata, K. Koyama, A. Fujiyama, Y. Miyoshi, M. Monden, T. Akiyama, Y. Nakamura, Identification of a brain-specific APC homologue, APCL, and its interaction with β-catenin, Cancer Res. 58 (1998) 5176.
71. J. Noordermeer, J. Klingensmith, N. Perrimon, R. Nusse, Dishevelled and armadillo act in the wingless signalling pathway in Drosophila, Nature 367 (1994) 80.
72. R. Nusse, H.E. Varmus, Many tumors induced by the mouse mammary tumor virus contain a provirus integrated in the same region of the host genome, Cell 31 (1982) 99.
73. C. Nüsslein-Volhard, E. Wieschaus, Mutations affecting segment number and polarity in Drosophila, Nature 287 (1980) 795.
74. M. Oosterwegel, M. van de Wetering, D. Dooijes, L. Klomp, A. Winoto, K. Georgopoulos, F. Meijlink, H. Clevers, Cloning of murine TCF-1, a T cell-specific transcription factor interacting with functional motifs in the CD3-epsilon and T cell receptor α enhancers, J. Exp. Med. 173 (1991) 1133.
75. M. Oosterwegel, M. van de Wetering, J. Timmerman, A. Kruisbeek, O. Destree, F. Meijlink, H. Clevers, Differential expression of the HMG box factors TCF-1 and LEF-1 during murine embryogenesis, Development 118 (1993) 439.
76. S. Orsulic, M. Peifer, Cell-cell signalling: Wingless lands at last, Curr. Biol. 6 (1996) 1363.
77. M. Ozawa, H. Baribault, R. Kemler, The cytoplasmic domain of the cell adhesion molecule uvomorulin associates with three independent proteins structurally related in different species, EMBO J. 8 (1989) 1711.
78. S.M. Parkhurst, Groucho: making its Marx as a transcriptional co-repressor, Trends Genet. 14 (1998) 130.
79. Z. Paroush, R.L. Finley Jr., T. Kidd, S.M. Wainwright, P.W. Ingham, R. Brent, D. Ish Horowicz, Groucho is required for Drosophila neurogenesis, segmentation, and sex determination and interacts directly with hairy-related bHLH proteins, Cell 79 (1994) 805.
80. M. Peifer, P.D. McCrea, K.J. Green, E. Wieschaus, B.M. Gumbiner, The vertebrate adhesive junction proteins β-catenin and plakoglobin and the Drosophila segment polarity gene armadillo form a multigene family with similar properties, J. Cell Biol. 118 (1992) 681.
81. M. Peifer, L.M. Pai, M. Casey, Phosphorylation of the Drosophila adherens junction protein Armadillo : roles for wingless signal and zeste-white 3 kinase, Dev. Biol. 166 (1994) 543.
82. E. Pennisi, How a growth control path takes a wrong turn to cancer, Science 281 (1998) 1438.
83. M. Pinto, C.G. Lobe, Products of the grg (Groucho-related gene) family can dimerize through the amino-terminal Q domain, J. Biol. Chem. 271 (1996) 33026.
84. P. Polakis, The adenomatous poyposis coli (APC) tumor suppressor, Biochim. Biophys. Acta 1332 (1997) F127.
85. P. Polakis, The oncogenic activation of β-catenin, Curr. Opin. Genet. Dev. 9 (1999) 15.
86. J. Riese, X. Yu, A. Munnerlyn, S. Eresh, S.C. Hsu, R. Grosschedl, M. Bienz, LEF-1, a nuclear factor coordinating signaling inputs from wingless and decapentaplegic, Cell 88 (1997) 777.
87. F. Rijsewijk, M. Schuermann, E. Wagenaar, P. Parren, D. Weigel, R. Nusse, The Drosophila homolog of the mouse mammary oncogene int-1 is identical to the segment polarity gene wingless, Cell 50 (1987) 649.
88. C.E. Rocheleau, W.D. Downs, R. Lin, C. Wittmann, Y. Bei, Y.H. Cha, M. Ali, J.R. Priess, C.C. Mello, Wnt signaling and an APC-related gene specify endoderm in early C. elegans embryos, Cell 90 (1997) 707.
89. J. Roose, M. Molenaar, J. Peterson, J. Hurenkamp, H. Brantjes, P. Moerer, M. van de Wetering, O. Destree, H. Clevers, The Xenopus Wnt effector XTcf-3 interacts with Groucho-related transcriptional repressors, Nature 395 (1998) 608.
90. B. Rubinfeld, I. Albert, E. Porfiri, C. Fiol, S. Munemitsu, P. Polakis, Binding of GSK3β to the APC-β-catenin complex and regulation of complex assembly, Science 272 (1996) 1023.
91. B. Rubinfeld, P. Robbins, M. El Gamil, I. Albert, E. Porfiri, P. Polakis, Stabilization of β-catenin by genetic defects in melanoma cell lines, Science 275 (1997) 1790.
92. B. Rubinfeld, B. Souza, I. Albert, O. Muller, S.H. Chamberlain, F.R. Masiarz, S. Munemitsu, P. Polakis, Association of the APC gene product with β-catenin, Science 262 (1993) 1731.
93. B. Rubinfeld, B. Souza, I. Albert, S. Munemitsu, P. Polakis, The APC protein and E-cadherin form similar but independent complexes with α-catenin, β-catenin, and plakoglobin, J. Biol. Chem. 270 (1995) 5549.
94. M. Schilham, A. Wilson, P. Moerer, B. Benaissa-Trouw, A. Cumano, H. Clevers, Critical involvement of Tcf-1 in expansion of thymocytes, J. Immunol. 161 (1998) 3984.
95. C. Schluter, M. Duchrow, C. Wohlenberg, M.H. Becker, G. Key, H.D. Flad, J. Gerdes, The cell proliferation-associated antigen of antibody Ki-67: a very large, ubiquitous nuclear protein with numerous repeated elements, representing a new kind of cell cycle-maintaining proteins, J. Cell Biol. 123 (1993) 513.
96. E. Siegfried, E.L. Wilder, N. Perrimon, Components of wingless signalling in Drosophila, Nature 367 (1994) 76.
97. S.Y. Sokol, J. Klingensmith, N. Perrimon, K. Itoh, Dorsalizing and neuralizing properties of Xdsh, a maternally expressed Xenopus homolog of dishevelled, Development 121 (1995) 1637.
98. S. Stifani, C.M. Blaumueller, N.J. Redhead, R.E. Hill, S. Artavanis-Tsakonas, Human homologs of a Drosophila Enhancer of Split gene product define a novel family of nuclear proteins, Nat. Genet. 2 (1992) 119.
99. L.K. Su, K. Kinzler, B. Vogelstein, A.C. Preisinger, A. Moser, C. Luongo, K. Gould, W.F. Dove, Multiple intestinal neoplasia caused by a mutation in the murine homolog of the APC gene, Science 256 (1992) 668.
100. L.K. Su, B. Vogelstein, K.W. Kinzler, Association of the APC tumor suppressor protein with catenins, Science 262 (1993) 1734.
101. O. Tetsu, F. McCormick, β-Catenin regulates expression of cyclin D1 in colon carcinoma cells, Nature 398 (1999) 422.
102. C.J. Thorpe, A. Schlesinger, J.C. Carter, B. Bowerman, Wnt signaling polarizes an early C. elegans blastomere to distinguish endoderm from mesoderm, Cell 90 (1997) 695.
103. A. Travis, A. Amsterdam, C. Belanger, R. Grosschedl, LEF-1, a gene encoding a lymphoid-specific protein with an HMG domain, regulates T-cell receptor α enhancer function, Genes Dev. 5 (1991) 880.
104. M. van de Wetering, M. Oosterwegel, D. Dooijes, H. Clevers, Identification and cloning of TCF-1, a T lymphocyte-specific transcription, EMBO J. 10 (1991) 123.
105. M. van de Wetering, H. Clevers, Sequence-specific interaction of the HMG box proteins TCF-1 and SRY occurs within the minor groove of a Watson-Crick double helix, EMBO J. 11 (1992) 3039.
106. M. van de Wetering, J. Castrop, V. Korinek, H. Clevers, Extensive alternative splicing and dual promoter usage generate Tcf-1 protein isoforms with differential transcription control properties, Mol. Cell Biol. 16 (1996) 745.
107. M. van de Wetering, R. Cavallo, D. Dooijes, M. van Beest, J. van Es, J. Loureiro, A. Ypma, D. Hursh, T. Jones, A. Bejsovec, M. Peifer, M. Mortin, H. Clevers, Armadillo coactivates transcription driven by the product of the Drosophila segment polarity gene dTCF, Cell 88 (1997) 789.
108. J. van Es, C. Kirkpatrick, M. van de Wetering, M. Molenaar, A. Miles, J. Kuipers, O. Destree, M. Peifer and H. Clevers, A homologue of the adenomatous poliposis coli tumor suppressor. Curr. Biol. 9 (1999).
109. C. van Genderen, R. Okamura, I. Farinas, R. Quo, T. Parslow, L. Bruhn, R. Grosschedl, Development of several organs that require inductive epithelial-mesenchymal interactions is impaired in Lef-1-deficient mice, Genes Dev. 8 (1994) 2691.
110. A. van Ooyen, R. Nusse, Structure and nucleotide sequence of the putative mammary oncogene int-1; proviral insertions leave the protein-encoding domain intact, Cell 39 (1984) 233.
111. S. Verbeek, D. Izon, F. Hofhuis, E. Robanus Maandag, H. te Riele, M. van de Wetering, M. Oosterwegel, A. Wilson, H.R. MacDonald, H. Clevers, An HMG-box-containing T-cell factor required for thymocyte differentiation, Nature 374 (1995) 70.
112. L. Waltzer, M. Bienz, Drosophila CBP represses the transcription factor TCF to antagonize Wingless signalling, Nature 395 (1998) 521.
113. M.L. Waterman, W.H. Fischer, K.A. Jones, A thymus-specific member of the HMG protein family regulates the human T cell receptor C α enhancer, Genes Dev. 5 (1991) 656.
114. E. Wieschaus, R. Riggleman, Autonomous requirements for the segment polarity gene armadillo during Drosophila embryogenesis, Cell 49 (1987) 177.
115. A. Wilson, W. Held, H. MacDonald, Two waves of recombinase gene expression in developing thymocytes, J. Exp. Med. 179 (1994) 1355.
116. J.T. Winston, P. Strack, P. Beer-Romero, C.Y. Chu, S.J. Elledge, J.W. Harper, The SCFβ-TRCP-ubiquitin ligase complex associates specifically with phosphorylated destruction motifs in IicBα and β-catenin and stimulates IKBα ubiquitination in vitro, Genes Dev. 13 (1999) 270.
117. S. Yanagawa, F. van Leeuwen, A. Wodarz, J. Klingensmith, R. Nusse, The dishevelled protein is modified by wingless signaling in Drosophila, Genes Dev. 9 (1995) 1087.
118. C. Yost, M. Torres, J.R. Miller, E. Huang, D. Kimelman, R.T. Moon, The axis-inducing activity, stability, and subcellular distribution of β-catenin is regulated in Xenopus embryos by glycogen synthase kinase 3, Genes Dev. 10 (1996) 1443.
119. L. Zeng, F. Fagotto, T. Zhang, W. Hsu, T.J. Vasicek, W.L. Perry, J.J. Lee, S.M. Tilghman, B.M. Gumbiner, F. Costantini, The mouse fused locus encodes Axin, an inhibitor of the Wnt signaling pathway that regulates embryonic axis formation, Cell 90 (1997) 181.
120. P. Zhou, C. Byrne, J. Jacobs, E. Fuchs, Lymphoid enhancer factor 1 directs hair follicle patterning and epithelial cell fate, Genes Dev. 9 (1995) 700.