TIP49 Regulates β-Catenin-Mediated Neoplastic Transformation and T-Cell Factor Target Gene Induction via Effects on Chromatin Remodeling

Cancer Research

Volumn 63, Issue 24, 2003, Pages 8726-8734

  Feng, Ying ^a   Lee, Nana ^b   Fearon, Eric R ^a,c  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b DNA Software Inc   (United States)

^c UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BAF 53 PROTEIN; BETA CATENIN; CARRIER PROTEIN; CYTOSKELETON PROTEIN; DNA BINDING PROTEIN; HELICASE; HISTONE; HISTONE ACETYLTRANSFERASE; HISTONE MODIFYING COFACTOR; HISTONE MODIFYING FACTOR; PROTEIN; RUVBL2 PROTEIN, HUMAN; SMALL INTERFERING RNA; T CELL FACTOR 4; T CELL FACTOR PROTEIN; TIP 49 PROTEIN; TIP 60 HISTONE ACETYLASE ASSOCIATED PROTEIN; TIP 60 PROTEIN; TRANSACTIVATION TRANSFORMATION DOMAIN ASSOCIATED PROTEIN; TRANSACTIVATOR PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ITF 2; TRANSCRIPTION FACTOR ITF-2; UNCLASSIFIED DRUG; WNT1 PROTEIN;

ACETYLATION; ANCHORAGE INDEPENDENT GROWTH; ARTICLE; BETA CATENIN GENE; BINDING SITE; CANCER CELL CULTURE; CELL IMMORTALIZATION; CELL LINE; CELL STRAIN HCT116; CELL TRANSFORMATION; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; COLON CANCER; CONTROLLED STUDY; GENE; GENE INDUCTION; GENE SEQUENCE; GENE TARGETING; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; GENETICS; HUMAN; HUMAN CELL; ITF 2 GENE; MALIGNANT TRANSFORMATION; METABOLISM; ONCOGENE C MYC; PHYSIOLOGY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN INTERACTION; REGULATORY MECHANISM; REPORTER GENE; SIGNAL TRANSDUCTION; TCF DEPENDENT GENE; TRANSCRIPTION REGULATION; TUMOR CELL;

ACETYLATION; BETA CATENIN; CARRIER PROTEINS; CELL LINE, TRANSFORMED; CELL TRANSFORMATION, NEOPLASTIC; CHROMATIN; CYTOSKELETAL PROTEINS; DNA HELICASES; DNA-BINDING PROTEINS; GENES, REPORTER; HCT116 CELLS; HISTONES; HUMANS; PROMOTER REGIONS (GENETICS); RNA, SMALL INTERFERING; TCF TRANSCRIPTION FACTORS; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRANSFECTION;

EID: 0346690269     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (68)

1. Bienz, M., and Clevers, H. Linking colorectal cancer to Wnt signaling. Cell, 103: 311-320, 2000.
2. Peifer, M., and Polakis, P. Wnt signaling in oncogenesis and embryogenesis: a look outside the nucleus. Science (Wash. DC), 287: 1606-1609, 2000.
3. Morin, P. J. β-Catenin signaling and cancer. Bioessays, 21: 1021-1030, 1999.
4. Polakis, P. Wnt signaling and cancer. Genes Dev., 14: 1837-1851, 2000.
5. Aberle, H., Bauer, A., Stappert, J., Kispert, A., and Kemler, R. β-Catenin is a target for the ubiquitin-proteasome pathway. EMBO J., 16: 3797-3804, 1997.
6. Behrens, J., Jerchow, B. A., Wurtele, M., Grimm, J., Asbrand, C., Wirtz, R., Kuhl, M., Wedlich, D., and Birchmeier, W. Functional interaction of an axin homolog, conductin, with β-catenin, APC, and GSK3β. Science (Wash. DC), 280: 596-599, 1998.
7. Hart, M. J., de los Santos, R., Albert, I. N., Rubinfeld, B., and Polakis, P. Down-regulation of β-catenin by human axin and its association with the APC tumor suppressor, β-catenin and GSK3β. Curr. Biol., 8: 573-581, 1998.
8. Jiang, J., and Struhl, G. Regulation of the Hedgehog and Wingless signalling pathways by the F-box/WD40-repeat protein Slimb. Nature (Lond.), 391: 493-496, 1998.
9. Zeng, L., Fagotto, F., Zhang, T., Hsu, W., Vasicek, T. J., Perry, W. L., III, Lee, J. J., Tilghman, S. M., Gumbiner, B. M., and Costantini, F. The mouse Fused locus encodes Axin, an inhibitor of the Wnt signaling pathway that regulates embryonic axis formation. Cell, 90: 181-192, 1997.
10. Kishida, S., Yamamoto, H., Hino, S., Ikeda, S., Kishida, M., and Kikuchi, A. DIX domains of Dv1 and axin are necessary for protein interactions and their ability to regulate β-catenin stability. Mol. Cell. Biol., 19: 4414-4422, 1999.
11. Ikeda, S., Kishida, S., Yamamoto, H., Murai, H., Koyama, S., and Kikuchi, A. Axin, a negative regulator of the Wnt signaling pathway, forms a complex with GSK-3β and β-catenin and promotes GSK-3β-dependent phosphorylation of β-catenin. EMBO J., 17: 1371-1384, 1998.
12. Fagotto, F., Gluck, U., and Gumbiner, B. M. Nuclear localization signal-independent and importin/karyopherin-independent nuclear import of β-catenin. Curr. Biol., 8: 181-190, 1998.
13. Behrens, J., von Kries, J. P., Kuhl, M., Bruhn, L., Wedlich, D., Grosschedl, R., and Birchmeier, W. Functional interaction of β-catenin with the transcription factor LEF-1. Nature (Lond.), 382: 638-642, 1996.
14. Molenaar, M., van de Wetering, M., Oosterwegel, M., Peterson-Maduro, J., Godsave, S., Korinek, V., Roose, J., Destree, O., and Clevers, H. XTcf-3 transcription factor mediates β-catenin-induced axis formation in Xenopus embryos. Cell, 86: 391-399, 1996.
15. He, T. C., Sparks, A. B., Rago, C., Hermeking, H., Zawel, L., da Costa, L. T., Morin, P. J., Vogelstein, B., and Kinzler, K. W. Identification of c-MYC as a target of the APC pathway. Science (Wash. DC), 281: 1509-1512, 1998.
16. Shtutman, M., Zhurinsky, J., Simcha, I., Albanese, C., D'Amico, M., Pestell, R., and Ben-Ze'ev, A. The cyclin D1 gene is a target of the β-catenin/LEF-1 pathway. Proc. Natl. Acad. Sci. USA, 96: 5522-5527, 1999.
17. Tetsu, O., and McCormick, F. B-Catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature (Lond.), 398: 422-426, 1999.
18. Crawford, H. C., Fingleton, B. M., Rudolph-Owen, L. A., Goss, K. J., Rubinfeld, B., Polakis. P., and Matrisian, L. M. The metalloproteinase matrilysin is a target of β-catenin transactivation in intestinal tumors. Oncogene, 18: 2883-2891, 1999.
19. Kolligs, F. T., Nieman, M. N., Winer, I., Hu, G., Mater, D. S. v., Feng, Y., Wu, R., Cho, K. R., and Fearon, E. R. ITF-2, a downstream target of the Wnt/TCF pathway, is activated in human cancers with β-catenin defects and promotes neoplastic transformation. Cancer Cells, 1: 145-155, 2002.
20. Cavallo, R. A., Cox, R. T., Moline, M. M., Roose, J., Polevoy, G. A., Clevers, H., Peifer, M., and Bejsovec, A. Drosophila Tcf and Groucho interact to repress Wingless signalling activity. Nature (Lond.), 395: 604-608, 1998.
21. Palaparti, A., Baratz, A., and Stifani, S. The Groucho/transducin-like enhancer of split transcriptional repressors interact with the genetically defined amino-terminal silencing domain of histone H3. J. Biol. Chem., 272: 26604-26610, 1997.
22. Chen, G., Fernandez, J., Mische, S., and Courey, A. J. A functional interaction between the histone deacetylase Rpd3 and the corepressor groucho in Drosophila development. Genes Dev., 13: 2218-2230, 1999.
23. Waltzer, L., and Bienz, M. Drosophila CBP represses the transcription factor TCF to antagonize Wingless signalling. Nature (Lond.), 395: 521-525, 1998.
24. Tago, K., Nakamura, T., Nishita, M., Hyodo, J., Nagai, S., Murata, Y., Adachi, S., Ohwada, S., Morishita, Y., Shibuya, H., and Akiyama, T. Inhibition of Wnt signaling by ICAT, a novel β-catenin-interacting protein. Genes Dev., 14: 1741-1749, 2000.
25. Sakamoto, I., Kishida, S., Fukui, A., Kishida, M., Yamamoto, H., Hino, S., Michiue, T., Takada, S., Asashima, M., and Kikuchi, A. A novel β-catenin-binding protein inhibits β-catenin-dependent Tcf activation and axis formation. J. Biol. Chem., 275: 32871-32878, 2000.
26. Takemaru, K., Yamaguchi, S., Lee, Y. S., Zhang, Y., Carthew, R. W., and Moon, R. T. Chibby, a nuclear β-catenin-associated antagonist of the Wnt/Wingless pathway. Nature (Lond.), 422: 905-909, 2003.
27. Hecht, A., Litterst, C. M., Huber, O., and Kemler, R. Functional characterization of multiple transactivating elements in β-catenin, some of which interact with the TATA-binding protein in vitro. J. Biol. Chem., 274: 18017-18025, 1999.
28. Hecht, A., Vleminckx, K., Stemmler, M. P., van Roy, F., and Kemler, R. The p300/CBP acetyltransferases function as transcriptional coactivators of β-catenin in vertebrates. EMBO J., 19: 1839-1850, 2000.
29. Sun, Y., Kolligs, F. T., Hottiger, M. O., Mosavin, R., Fearon, E. R., and Nabel, G. J. Regulation of β-catenin transformation by the p300 transcriptional coactivator. Proc. Natl. Acad. Sci. USA, 97: 12613-12618, 2000.
30. Takemaru, K. I., and Moon, R. T. The transcriptional coactivator CBP interacts with β-catenin to activate gene expression. J. Cell Biol., 149: 249-254, 2000.
31. 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., and Clevers, H. Armadillo coactivates transcription driven by the product of the Drosophila segment polarity gene dTCF. Cell, 88: 789-799, 1997.
32. Prieve, M. G., and Waterman, M. L. Nuclear localization and formation of β-catenin-lymphoid enhancer factor 1 complexes are not sufficient for activation of gene expression. Mol. Cell. Biol., 19: 4503-4515, 1999.
33. Barker, N., Hurlstone, A., Musisi, H., Miles, A., Bienz, M., and Clevers, H. The chromatin remodelling factor Brg-1 interacts with β-catenin to promote target gene activation. EMBO J., 20: 4935-4943, 2001.
34. Kramps, T., Peter, O., Brunner, E., Nellen, D., Froesch, B., Chatterjee, S., Murone, M., Zullig, S., and Basler, K. Wnt/wingless signaling requires BCL9/legless-mediated recruitment of pygopus to the nuclear β-catenin-TCF complex. Cell, 109: 47-60, 2002.
35. Parker, D. S., Jemison, J., and Cadigan, K. M. Pygopus, a nuclear PHD-finger protein required for Wingless signaling in Drosophila. Development (Camb.), 129: 2565-2576, 2002.
36. Thompson, B., Townsley, F., Rosin-Arbesfeld, R., Musisi, H., and Bienz, M. A new nuclear component of the Wnt signalling pathway. Nat. Cell Biol., 4: 367-373, 2002.
37. Aasland, R., Gibson, T. J., and Stewart, A. F. The PHD finger: implications for chromatin-mediated transcriptional regulation. Trends Biochem. Sci., 20: 56-59, 1995.
38. Jacobson, S., and Pillus, L. Modifying chromatin and concepts of cancer. Curr. Opin. Genet. Dev., 9: 175-184, 1999.
39. Wood, M. A., McMahon, S. B., and Cole, M. D. An ATPase/helicase complex is an essential cofactor for oncogenic transformation by c-Myc. Mol. Cell, 5: 321-330, 2000.
40. Kanemaki, M., Makino, Y., Yoshida, T., Kishimoto, T., Koga, A., Yamamoto, K., Yamamoto, M., Moncollin, V., Egly, J. M., Muramatsu, M., and Tamura, T. Molecular cloning of a rat 49-kDa TBP-interacting protein (TIP49) that is highly homologous to the bacterial RuvB. Biochem. Biophys. Res. Commun., 235: 64-68, 1997.
41. Bauer, A., Huber, O., and Kemler, R. Pontin52, an interaction partner of β-catenin, binds to the TATA box binding protein. Proc. Natl. Acad. Sci. USA, 95: 14787-14792, 1998.
42. Holzmann, K., Gerner, C., Korosec, T., Poltl, A., Grimm, R., and Sauermann, G. Identification and characterization of the ubiquitously occurring nuclear matrix protein NMP 238. Biochem. Biophys. Res. Commun., 252: 39-45, 1998.
43. Qiu, X. B., Lin, Y. L., Thome, K. C., Pian, P., Schlegel, B. P., Weremowicz, S., Parvin, J. D., and Dutta, A. An eukaryotic RuvB-like protein (RUVBL1) essential for growth. J. Biol. Chem., 273: 27786-27793, 1998.
44. Shen, X., Mizuguchi, G., Hamiche, A., and Wu, C. A chromatin remodelling complex involved in transcription and DNA processing. Nature (Lond.), 406: 541-544, 2000.
45. Ikura, T., Ogryzko, V. V., Grigoriev, M., Groisman, R., Wang, J., Horikoshi, M., Scully, R., Qin, J., and Nakatani, Y. Involvement of the TIP60 histone acetylase complex in DNA repair and apoptosis. Cell, 102: 463-473, 2000.
46. Kikuchi, N., Gohshi, T., Kawahire, S., Tachibana, T., Yoneda, Y., Isobe, T., Lim, C. R., Kohno, K., Ichimura, T., Omata, S., and Horigome, T. Molecular shape and ATP binding activity of rat p50, a putative mammalian homologue of RuvB DNA helicase. J. Biochem. (Tokyo), 125: 487-494, 1999.
47. Kanemaki, M., Kurokawa, Y., Matsu-ura, T., Makino, Y., Masani, A., Okazaki, K., Morishita, T., and Tamura, T. A. TIP49b, a new RuvB-like DNA helicase, is included in a complex together with another RuvB-like DNA helicase, TIP49a. J. Biol. Chem., 274: 22437-22444, 1999.
48. Bauer, A., Chauvet, S., Huber, O., Usseglio, F., Rothbacher, U., Aragnol, D., Kemler, R., and Pradel, J. Pontin52 and reptin52 function as antagonistic regulators of β-catenin signalling activity. EMBO J., 19: 6121-6130, 2000.
49. Gohshi, T., Shimada, M., Kawahire, S., Imai, N., Ichimura, T., Omata, S., and Horigome, T. Molecular cloning of mouse p47, a second group mammalian RuvB DNA helicase-like protein: homology with those from human and Saccharomyces cerevisiae. J. Biochem. (Tokyo), 125: 939-946, 1999.
50. Makino, Y., Kanemaki, M., Kurokawa, Y., Koji, T., and Tamura, T. A rat RuvB-like protein, TIP49a, is a germ cell-enriched novel DNA helicase. J. Biol. Chem., 274: 15329-15335, 1999.
51. Jonsson, Z. O., Dhar, S. K., Narlikar, G. J., Auty, R., Wagle, N., Pellman, D., Pratt, R. E., Kingston, R., and Dutta, A. Rvb1p and Rvb2p are essential components of a chromatin remodeling complex that regulates transcription of over 5% of yeast genes. J. Biol. Chem., 276: 16279-16288, 2001.
52. Kolligs, F. T., Hu, G., Dang, C. V., and Fearon, E. R. Neoplastic transformation of RK3E by mutant β-catenin requires deregulation of Tcf/ Lef transcription but not activation of c-myc expression. Mol. Cell. Biol., 19: 5696-5706, 1999.
53. Littlewood, T. D., Hancock, D. C., Danielian, P. S., Parker, M. G., and Evan, G. I. A modified oestrogen receptor ligand-binding domain as an improved switch for the regulation of heterologous proteins. Nucleic Acids Res., 23: 1686-1690, 1995.
54. Korinek, V., Barker, N., Morin, P. J., van Wichen, D., de Weger, R., Kinzler, K. W., Vogelstein, B., and Clevers, H. Constitutive transcriptional activation by a β-catenin-Tcf complex in APC-/- colon carcinoma. Science (Wash. DC), 275: 1784-1787, 1997.
55. Gorbalenya, A. E., Koonin, E. V., Donchenko, A. P., and Blinov, V. M. Two related superfamilies of putative helicases involved in replication, recombination, repair and expression of DNA and RNA genomes. Nucleic Acids Res., 17: 4713-4730, 1989.
56. Schmid, S. R., and Linder, P. D-E-A-D protein family of putative RNA helicases. Mol. Microbiol., 6: 283-291, 1992.
57. Mezard, C., Davies, A. A., Stasiak, A., and West, S. C. Biochemical properties of RuvBD113N: a mutation in helicase motif II of the RuvB hexamer affects DNA binding and ATPase activities. J. Mol. Biol., 271: 704-717, 1997.
58. Leung, J. Y., Kolligs, F. T., Wu, R., Zhai, Y., Kuick, R., Hanash, S., Cho, K. R., and Fearon, E. R. Activation of AXIN2 expression by β-catenir/TCF: A feedback repressor pathway regulating Wnt signaling. J. Biol. Chem., 277: 21657-21665, 2002.
59. Lustig, B., Jerchow, B., Sachs, M., Weiler, S., Pietsch, T., Karsten, U., van de Wetering, M., Clevers, H., Schlag, P. M., Birchmeier, W., and Behrens, J. Negative feedback loop of Wnt signaling through upregulation of conductin/axin2 in colorectal and liver tumors. Mol. Cell. Biol., 22: 1184-1193, 2002.
60. Jho, E. H., Zhang, T., Domon, C., Joo, C. K., Freund, J. N., and Costantini, F. Wnt/β-catenin/Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol. Cell. Biol., 22: 1172-1183, 2002.
61. Yan, D., Wiesmann, M., Rohan, M., Chan, V., Jefferson, A. B., Guo, L., Sakamoto, D., Caothien, R. H., Fuller, J. H., Reinhard, C., Garcia, P. D., Randazzo, F. M., Escobedo, J., Fantl, W. J., and Williams, L. T. Elevated expression of axin2 and hnkd mRNA provides evidence that Wnt/β-catenin signaling is activated in human colon tumors. Proc. Natl. Acad. Sci. USA, 98: 14973-14978, 2001.
62. Park, J., Wood, M. A., and Cole, M. D. BAF53 forms distinct nuclear complexes and functions as a critical c-Myc-interacting nuclear cofactor for oncogenic transformation. Mol. Cell. Biol., 22: 1307-1316, 2002.
63. Mizzen, C. A., and Allis, C. D. Linking histone acetylation to transcriptional regulation. Cell Mol. Life Sci., 54: 6-20, 1998.
64. Komberg, R. D., and Lorch, Y. Chromatin-modifying and -remodeling complexes. Curr. Opin. Genet. Dev., 9: 148-151, 1999.
65. Kingston, R. E., and Narlikar, G. J. ATP-dependent remodeling and acetylation as regulators of chromatin fluidity. Genes Dev., 13: 2339-2352, 1999.
66. Rottbauer, W., Saurin, A. J., Lickert, H., Shen, X., Burns, C. G., Wo, Z. G., Kemler, R., Kingston, R., Wu, C., and Fishman, M. Reptin and pontin antagonistically regulate heart growth in zebrafish embryos. Cell, 111: 661-672, 2002.
67. Fryer, C. J., and Archer, T. K. Chromatin remodelling by the glucocorticoid receptor requires the BRG1 complex. Nature (Lond.), 393: 88-91, 1998.
68. Kioussi, C., Briata, P., Baek, S. H., Rose, D. W., Hamblet, N. S., Herman, T., Ohgi, K. A., Lin, C., Gleiberman, A., Wang, J., Brault, V., Ruiz-Lozano, P., Nguyen, H. D., Kemler, R., Glass, C. K., Wynshaw-Boris, A., and Rosenfeld, M. G. Identification of a Wnt/Dv1/β-catenin→Pitx2 pathway mediating cell-type-specific proliferation during development. Cell, 111: 673-685, 2002.