Nuclear localization and formation of β-catenin-lymphoid enhancer factor 1 complexes are not sufficient for activation of gene expression

Molecular and Cellular Biology

Volumn 19, Issue 6, 1999, Pages 4503-4515

  Prieve, Mary G ^a   Waterman, Marian L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; CELL PROTEIN; LYMPHOID ENHANCER FACTOR 1; TRANSCRIPTION FACTOR; UVOMORULIN;

ANIMAL CELL; ARTICLE; CELL NUCLEUS; CELL STRAIN COS1; CONTROLLED STUDY; GENE ACTIVATION; HUMAN; HUMAN CELL; LEUKEMIA CELL LINE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN LOCALIZATION; REPORTER GENE;

EID: 0033013369     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/mcb.19.6.4503     Document Type: Article

References (75)

1. Aberle, H., A. Bauer, J. Stappert, A. Kispert, and R. Kemler. 1997. Beta-catenin is a target for the ubiquitin-proteasome pathway. EMBO J. 16:3797-3804.
2. Adam, S. A., R. E. Sterne-Marr, and L. Gerace. 1990. Nuclear protein import in permeabilized mammalian cells requires soluble cytoplasmic factors. J. Cell Biol. 111:807-816.
3. Bauer, A., O. Huber, and R. Kemler. 1998. Pontin52, an interaction partner of beta-catenin, binds to the TATA box binding protein, Proc. Natl. Acad. Sci. USA 95:14787-14792.
4. Beals, C., N. Clipstone, S. Ho, and G. Crabtree. 1997. Nuclear localization of NF-ATc by a calcineurin-dependent, cyclosporin-sensitive intramolecular interaction. Genes Dev. 11:824-834.
5. Beals, C., C. Sheridan, C. Turck, P. Gardner, and G. Crabtree. 1997. Nuclear export of NF-ATc enhanced by glycogen synthase kinase-3. Science 275: 1930-1934.
6. Behrens, J., B.-A. Jerchow, M. Wurtele, J. Grimm, C. Asbrand, R. Wirtz, M. Kuhn, D. Wedlich, and W. Birchmeier. 1998. Functional interaction of an axin homolog, conductin, with β-catenin, APC and GSK3β. Science 280:596-599.
7. Behrens, J., J. P. van Kries, M. Kuh, L. Bruhn, D. Wedlich, R. Grosschedl, and W. Birchmeier. 1996. Functional interaction of β-catenin with the transcription factor LEF-1. Nature 382:638-642.
8. Blau, J., H. Xiao, S. McCracken, P. O'Hare, J. Greenblatt, and D. Bentley. 1996. Three functional classes of transcriptional activation domain. Mol. Cell. Biol. 16:2044-2055.
9. Brown, J., and R. Moon. 1998. Wnt signaling: why is everything so negative? Curr. Opinion Cell Biol. 10:182-187.
10. Cadigan, K., and R. Nasse. 1998. Wnt signaling: a common theme in animal development. Genes Dev. 11:3286-3305.
11. Carlsson, P., M. Waterman, and K. Jones. 1993. The hLEF/TCF-1α HMG protein contains a context-dependent transcriptional activation domain that induces the TCRα enhancer in T cells. Genes Dev. 7:2418-2430.
12. Cavallo, R. A., R. T. Cox, M. M. Moline, J. Roose, G. A. Polevoy, H. Clevers, M. Peifer, and A. Bejsovec. 1998. Drosophila Tcf and Groucho interact to repress Wingless signalling activity. Nature 395:604-608.
13. Conti, E., M Uy, L. Leighton, G. Blobel, and J. Kuriyan. 1998. Crystallo-graphic analysis of the recognition of a nuclear localization signal by the nuclear import factor karyopherin α. Cell 94:193-204.
14. Cook, D., M. Fry, K. Hughes, R. Sumathipala, J. Woodgett, and T. Dale. 1996. Wingless inactivates glycogen synthase kinase-3 via an intracellular signalling pathway which involves a protein kinase C. EMBO J. 15:4526-4536.
15. Dale, T. C. 1998. Signal transduction by the Wnt family of ligands. Biochem. J. 329:209-223.
16. Fagotto, F., N. Funayama, U. Gluck, and B. M. Gumbiner. 1996. Binding to cadherins antagonizes the signaling activity of β-catenin during axis formation in Xenopus. J. Cell Biol. 132:1105-1114.
17. Fagotto, F., U. Gluck, and B. Gumbiner. 1998. Nuclear localization signal-independent and importin/karyopherin-independent nuclear import of beta-catenin. Curr. Biol. 8:181-190.
18. Funayama, N., F. Fagotto, P. McCrea, and B. M. Gumbiner. 1995. Embryonic axis induction by the armadillo repeat domain of beta-catenin: evidence for intracellular signaling. J. Cell Biol. 128:959-968.
19. Gailet, A., A. Erkner, B. Charroux, L. Fasano, and S. Kerridge. 1998. Trunk-specific modulation of wingless signalling in Drosophila by teashirt binding to armadillo. Curr. Biol. 8:893-902.
20. Giese, K., J. Cox, and R. Grosscheldl. 1992. The HMG domain of lymphoid enhancer factor 1 bends DNA and facilitates assembly of functional nucleo-protein structures. Cell 69:185-196.
21. Giese, K., and R. Grosschedl. 1993. LEF-1 contains an activation domain that stimulates transcription only in a specific context of factor-binding sites. EMBO J. 12:4667-4676.
22. Giese, K., C. Kingsley, J. R. Kirshner, and R. Grosschedl. 1995. Assembly and function of a TCR alpha enhancer complex is dependent on LEF-1-induced DNA bending and multiple protein-protein interactions. Genes Dev. 9:995-1008.
23. Giese, K., J. Pagel, and R. Grosschedl. 1997. Functional analysis of DNA bending and unwinding by the high mobility group domain of LEF-1. Proc. Natl. Acad. Sci. USA 94:12845-12850.
24. Goodrich, J. A., T. Hoey, C. J. That, A. Admon, and R. Tjian. 1993. Drosophila TAFII40 interacts with both a VP16 activation domain and the basal transcription factor TFIIB. Cell 75:519-530.
25. Gorlich, D., S. Kostak, R. Kraft, C. Dingwall, R. A. Laskey, E. Hartmann, and S. Prehn. 1995. Two different subunits of importin cooperate to recognize nuclear localization signals and bind them to the nuclear envelope. Curr. Biol. 5:383-392.
26. Gorlich, D., and I. W. Mattaj. 1996. Nucleocytoplasmic transport. Science 271:1513-1518.
27. Hsu, S.-C., J. Galceran, and R. Grosschedl. 1998. Modulation of transcriptional regulation by LEF-1 in response to Wnt-1 signaling and association with β-catenin. Mol. Cell. Biol. 18:4807-4818.
28. Huber, A. H., W. J. Nelson, and W. I. Weis. 1997. Three-dimensional structure of the armadillo repeat region of β-catenin. Cell 90:871-882.
29. Huber, O., R. Korn, J. McLaughlin, M. Ohsugi, B. Herrmann, and R. Kemler. 1996. Nuclear localization of beta-catenin by interaction with transcription factor LEF-1. Mech. Dev. 59:3-10.
30. Hughes, C. C., and J. S. Pober. 1996. Transcriptional regulation of the interleukin-2 gene in normal human peripheral blood T cells. Convergence of costimulatory signals and differences from transformed T cells. J. Biol. Chem. 271:5369-5377.
31. Hulsken, J., W. Birchmeier, and J. Behrens. 1994. E-cadherin and APC compete for the interaction with β-catenin and the cytoskeleton. J. Cell Biol. 127:2061-2069.
32. Ikeda, S., S. Kishida, H. Yamamoto, H. Murai, S. Koyama, and A. Kikuchi. 1998. Axin, a negative regulator of the Wnt signaling pathway, forms a complex with GSK-3beta and beta-catenin and promotes GSK-3beta-dependent phosphorylation of beta-catenin. EMBO J. 17:1371-1384.
33. Kinzler, K., and B. Vogelstein. 1996. Lessons from hereditary colorectal cancer. Cell 87:159-170.
34. Kishida, S., H. Yamamoto, S. Ikeda, M. Kishida, I. Sakamoto, S. Koyama, and A. Kikuchi. 1998. Axin, a negative regulator of the wnt signaling pathway, directly interacts with adenomatous polyposis coli and regulates the stabilization of beta-catenin. J. Biol. Chem. 273:10823-10826.
35. Klingensmith, J., R. Nusse, and N. Perrimon. 1994. The Drosophila segment polarity gene dishevelled encodes a novel protein required for response to the wingless signal. Genes Dev. 8:118-130.
36. Korinek, V., N. Barker, P. Morin, D. van Wichen, R. de Weger, K. Kinzler, B. Vogelstein, and H. Clevers. 1997. Constitutive transcriptional activation by a beta-catenin-Tcf complex in APC-/- colon carcinoma. Science 275:1784-1787.
37. Korinek, V., N. Barker, K. Willert, M. Molenaar, J. Roose, G. Wagenaar, M. Markman, W. Lamers, O. Destree, and H. Clevers. 1998. Two members of the Tcf family implicated in Wnt/β-catenin signaling during embryogenesis in the mouse. Mol. Cell. Biol. 18:1248-1256.
38. Levanon, D., R. E. Goldstein, Y. Bernstein, H. Tang, D. Goldenberg, S. Stifani, Z. Paroush, and Y. Groner. 1998. Transcriptional repression by AML1 and LEF-1 is mediated by the TLE/Groucho corepressors. Proc. Natl. Acad. Sci. USA 95:11590-11595.
39. Lin, Y. S., I. Ha, E. Maldonado, D. Reinberg, and M. R. Green. 1991. Binding of general transcription factor TFIIB to an acidic activating region. Nature 353:569-571.
40. Love, J. J., X. Li, D. A. Case, K. Giese, R. Grosschedl, and P. E. Wright. 1995. Structural basis for DNA bending by the architectural transcription factor LEF-1. Nature 376:791-795.
41. Malik, H., T. Eickbush, and D. Goldfarb. 1997. Evolutionary specialization of the nuclear targeting apparatus. Proc. Natl. Acad. Sci. USA 94:13738-13742.
42. Mangalam, H. J., V. R. Albert, H. A. Ingraham, M. Kapiloff, L. Wilson, C. Nelson, H. Elsholtz, and M. G. Rosenfeld. 1989. A pituitary POU domain protein, Pit-1, activates both growth hormone and prolactin promoters transcriptionally. Genes Dev. 3:946-958.
43. Miller, J., and R. Moon. 1996. Signal transduction through beta-catenin and specification of cell fate during embryogenesis. Genes Dev. 10:2527-2539.
44. Molenaar, M., M. van de Wetering, M. Oosterwegel, J. Peterson-Maduro, S. Godsave, V. Korinek, J. Roose, O. Destree, and H. Clevers. 1996. XTCF-3 transcription factor mediates β-catenin-induced axis formation in Xenopus embryos. Cell 86:391-399.
45. Morin, P., A. Sparks, V. Korinek, N. Barter, H. Clevers, B. Vogelstein, and K. Kinzler. 1997. Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC. Science 275:1787-1790.
46. Munemitsu, S., I. Albert, B. Rubinfeld, and P. Polakis. 1996. Deletion of an amino-terminal sequence stabilizes β-catenin in vivo and promotes hyperphosphorylation of the adenomatous polyposis coli tumor suppressor protein. Mol. Cell. Biol. 16:4088-4094.
47. 46a.Munguia, J., and M. L. Waterman. Unpublished results.
48. Nigg, E. 1997. Nucleocytoplasmic transport: signals, mechanisms and regulation. Nature 386:779-787.
49. Orsulic, S., and M. Peifer. 1996. An in vivo structure-function study of armadillo, the β-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.
50. Papkoff, J., B. Rubinfeld, B. Schryver, and P. Polakis. 1996. Wnt-1 regulates free pools of catenins and stabilizes APC-catenin complexes. Mol. Cell. Biol. 16:2128-2134.
51. Peifer, M., S. Berg, and A. B. Reynolds. 1994. A repeating amino acid motif shared by proteins with diverse cellular roles. Cell 76:789-791.
52. Pinol-Roma, S., and G. Dreyfuss. 1992. Shuttling of pre-mRNA binding proteins between nucleus and cytoplasm. Nature 355:730-732.
53. Polakis, P. 1997. The adenomatous polyposis coli (APC) tumor suppressor. Biochim. Biophys. Acta 1332:F127-F147.
54. Porfiri, E., B. Rubinfeld, I. Albert, K. Hovanes, M. Waterman, and P. Polakis. 1998. Induction of a beta-catenin-LEF-1 complex by Wnt-1 and transforming mutants of beta-catenin. Oncogene 15:2833-2839.
55. 53a.Prieve, M. G. Unpublished results.
56. Prieve, M., K. L. Guttridge, J. E. Munguia, and M. Waterman. 1996. The nuclear localization signal of lymphoid enhancer factor-1 is recognized by two differentially expressed Srpl-NLS receptor proteins. J. Biol. Chem. 271: 7654-7658.
57. Prieve, M. G., K. L. Guttridge, J. Munguia, and M. L. Waterman. 1998. Differential importin a recognition and nuclear transport by nuclear localization signals within the high-mobility-group DNA binding domains of lymphoid enhancer factor 1 and T-cell factor 1. Mol. Cell. Biol. 18:4819-4832.
58. 55a.Prieve, M. G., and M. L. Waterman. Unpublished results.
59. Roose, J., M. Molenaar, J. Peterson, J. Hurenkamp, H. Brantjes, P. Moerer, M. van de Wetering, O. Destree, and H. Clevers. 1998. The Xenopus Wnt effector XTcf-3 interacts with Groucho-related transcriptional repressors. Nature 395:608-612.
60. Rubinfeld, B., I. Albert, E. Porfiri, C. Fiol, S. Munemitsu, and P. Polakis. 1996. Binding of GSK3β to the APC-beta-catenin complex and regulation of complex assembly. Science 272:1023-1026.
61. Rubinfeld, B., B. Souza, I. Albert, S. Munemitsu, and P. Polakis. 1995. The APC protein and E-cadherin form similar but independent complexes with alpha-catenin, beta-catenin, and plakoglobin. J. Biol. Chem. 270:5549-5555.
62. Simcha, I., M. Shtutman, D. Salomon, J. Zhurinsky, E. Sadot, B. Geiger, and A. Ben-Ze'ev. 1998. Differential nuclear translocation and transactivation potential of beta-catenin and plakoglobin. J. Cell Biol. 141:1433-1448.
63. Swain, S. L., M. Croft, C. Dubey, L. Haynes, P. Rogers, X. Zhang, and L. M. Bradley. 1996. From naive to memory T cells. Immunol. Rev. 150:143-167.
64. Theisen, H., J. Purcell, M. Bennett, D. Kansagara, A. Syed, and J. Marsh. 1994. Dishevelled is required during wingless signaling to establish both cell polarity and cell identity. Development 120:347-360.
65. Travis, A., A. Amsterdam, C. Belanger, and R. Grosschedl. 1991. LEF-1, a gene encoding a lymphoid-specific protein with an HMG domain, regulates T-cell receptor alpha enhancer function. Genes Dev. 5:880-894.
66. van de Wetering, M., R. Cavallo, D. Dooijes, M. van Beest, J. van Es, J. Loureiro, A. Ypma, D. Hursh, T. Jones, A Bejsovec, M. Peifer, M. Mortin, and H. Clevers. 1997. Armadillo coactivates transcription driven by the product of the Drosophila segment polarity gene dTCF. Cell 88:789-799.
67. van de Wetering, M., M. Oosterweg, D. Dooijes, and H. Clevers. 1991. Identification and cloning of TCF-1, a T lymphocyte specific transcription factor containing a sequence-specific HMG box. EMBO J. 10:123-132.
68. Waltzer, L., and M. Bienz. 1998. Drosophila CBP represses the transcription factor TCF to antagonize Wingless signalling. Nature 395:521-525.
69. Waterman, M. L., W. H. Fischer, and K. A. Jones. 1991. A thymus-specific member of the HMG protein family regulates the human T cell receptor C alpha enhancer. Genes Dev. 5:656-669.
70. Welsh, G. I., S. Miyamoto, N. T. Price, B. Safer, and C. G. Proud. 1996. T-cell activation leads to rapid stimulation of translation initiation factor eIF2B and inactivation of glycogen synthase kinase-3. J. Biol. Chem. 271:11410-11413.
71. Woodgett, J. 1994. Regulation and functions of the glycogen synthase kinase-3 subfamily. Semin. Cancer Biol. 5:269-275.
72. Yamamoto, H., S. Kishida, T. Uochi, S. Ikeda, S. Koyama, M. Asashima, and A. Kikuchi. 1998. Axil, a member of the Axin family, interacts with both glycogen synthase kinase 3β and β-catenin and inhibits axis formation of Xenopus embryos. Mol. Cell. Biol. 18:2867-2875.
73. Yost, C., H. F. Gist III, S. B. Pierce, D. M. Ferkey, M. M. Chen, and D. Kimelman. 1998. GBP, and inhibitor of GSK-3, is implicated in Xenopus development and oncogenesis. Cell 93:1031-1041.
74. Yu, G., F. Chen, G. Levesque, M. Nishimura, D.-M. Zhang, L. Levesque, E. Rogaeva, D. Xu, Y. Lian, M. Duthei, P. St. George-Hyslop, and P. E. Fraser. 1998. The presenilin 1 protein is a component of a high molecular weight intracellular complex that contains β-catenin. J. Biol. Chem. 273:16470-16475.
75. Zeng, L., F. Fagotto, T. Zhang, W. Hsu, T. J. Vasicek, W. L. Perry, J. J. Lee, S. M. Tilghman, B. M. Gumbiner, and F. Costantini. 1997. The mouse fused locus encodes Axin, an inhibitor of the Wnt signaling pathway that regulates embryonic axis formation. Cell 90:181-192.