A Functional Screen in Human Cells Identifies UBF2 as an RNA Polymerase II Transcription Factor That Enhances the β-Catenin Signaling Pathway

REFERENCES

• 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.
   PubMed Web of Science ®Google Scholar
• Bachvarov, D., and T. Moss. 1991. The RNA polymerase I transcription factor xUBF contains 5 tandemly repeated HMG homology boxes. Nucleic Acids Res. 19: 2331–2335.
   PubMedGoogle Scholar
• Barth, A. I., D. B. Stewart, and W. J. Nelson. 1999. T cell factor-activated transcription is not sufficient to induce anchorage-independent growth of epithelial cells expressing mutant beta-catenin. Proc. Natl. Acad. Sci. USA 96: 4947–4952.
   PubMedGoogle Scholar
• Bauer, A., S. Chauvet, O. Huber, F. Usseglio, U. Rothbacher, D. Aragnol, R. Kemler, and J. Pradel. 2000. Pontin52 and reptin52 function as antagonistic regulators of beta-catenin signalling activity. EMBO J. 19: 6121–6130.
   PubMed Web of Science ®Google Scholar
• Bazett-Jones, D. P., B. Leblanc, M. Herfort, and T. Moss. 1994. Short-range DNA looping by the Xenopus HMG-box transcription factor, xUBF. Science 264: 1134–1137.
   PubMedGoogle Scholar
• Beckmann, H., J. L. Chen, T. O'Brien, and R. Tjian. 1995. Coactivator and promoter-selective properties of RNA polymerase I TAFs. Science 270: 1506–1509.
   PubMedGoogle Scholar
• Behrens, J., J. P. von Kries, M. Kuhl, L. Bruhn, D. Wedlich, R. Grosschedl, and W. Birchmeier. 1996. Functional interaction of beta-catenin with the transcription factor LEF-1. Nature 382: 638–642.
   PubMed Web of Science ®Google Scholar
• Bell, S. P., R. M. Learned, H. M. Jantzen, and R. Tjian. 1988. Functional cooperativity between transcription factors UBF1 and SL1 mediates human ribosomal RNA synthesis. Science 241: 1192–1197.
   PubMed Web of Science ®Google Scholar
• Bienz, M., and H. Clevers. 2000. Linking colorectal cancer to Wnt signaling. Cell 103: 311–320.
   PubMed Web of Science ®Google Scholar
• Brabletz, T., A. Jung, S. Dag, F. Hlubek, and T. Kirchner. 1999. Beta-catenin regulates the expression of the matrix metalloproteinase-7 in human colorectal cancer. Am. J. Pathol. 155: 1033–1038.
   PubMed Web of Science ®Google Scholar
• Brannon, M., J. D. Brown, R. Bates, D. Kimelman, and R. T. Moon. 1999. XCtBP is a XTcf-3 co-repressor with roles throughout Xenopus development. Development 126: 3159–3170.
   PubMed Web of Science ®Google Scholar
• Bruhn, L., A. Munnerlyn, and R. Grosschedl. 1997. ALY, a context-dependent coactivator of LEF-1 and AML-1, is required for TCRα enhancer function. Genes Dev. 11: 640–653.
   PubMed Web of Science ®Google Scholar
• Brummelkamp, T. R., R. Bernards, and R. Agami. 2002. Stable suppression of tumorigenicity by virus-mediated RNA interference. Cancer Cell 2: 243–247.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Chen, G., J. Fernandez, S. Mische, and A. J. Courey. 1999. A functional interaction between the histone deacetylase Rpd3 and the corepressor groucho in Drosophila development. Genes Dev. 13: 2218–2230.
   PubMed Web of Science ®Google Scholar
• Collins, R. T., and J. E. Treisman. 2000. Osa-containing Brahma chromatin remodeling complexes are required for the repression of wingless target genes. Genes Dev. 14: 3140–3152.
   PubMed Web of Science ®Google Scholar
• Comai, L., N. Tanese, and R. Tjian. 1992. The TATA-binding protein and associated factors are integral components of the RNA polymerase I transcription factor, SL1. Cell 68: 965–976.
   PubMedGoogle Scholar
• Comai, L., J. C. Zomerdijk, H. Beckmann, S. Zhou, A. Admon, and R. Tjian. 1994. Reconstitution of transcription factor SL1: exclusive binding of TBP by SL1 or TFIID subunits. Science 266: 1966–1972.
   PubMedGoogle Scholar
• Copenhaver, G. P., C. D. Putnam, M. L. Denton, and C. S. Pikaard. 1994. The RNA polymerase I transcription factor UBF is a sequence-tolerant HMG-box protein that can recognize structured nucleic acids. Nucleic Acids Res. 22: 2651–2657.
   PubMedGoogle Scholar
• Crawford, H. C., B. M. Fingleton, L. A. Rudolph-Owen, K. J. Goss, B. Rubinfeld, P. Polakis, and L. M. Matrisian. 1999. The metalloproteinase matrilysin is a target of beta-catenin transactivation in intestinal tumors. Oncogene 18: 2883–2891.
   PubMed Web of Science ®Google Scholar
• Devroe, E., and P. A. Silver. 2002. Retrovirus-delivered siRNA. BMC Biotechnol. 2: 15.
   PubMedGoogle Scholar
• Dominguez, I., K. Itoh, and S. Y. Sokol. 1995. Role of glycogen synthase kinase 3 beta as a negative regulator of dorsoventral axis formation in Xenopus embryos. Proc. Natl. Acad. Sci. USA 92: 8498–8502.
   PubMed Web of Science ®Google Scholar
• Gaudilliere, B., Y. Shi, and A. Bonni. 2002. RNA interference reveals a requirement for myocyte enhancer factor 2A in activity-dependent neuronal survival. J. Biol. Chem. 277: 46442–46446.
   PubMedGoogle Scholar
• Giese, K., A. Amsterdam, and R. Grosschedl. 1991. DNA-binding properties of the HMG domain of the lymphoid-specific transcriptional regulator LEF-1. Genes Dev. 5: 2567–2578.
   PubMed Web of Science ®Google Scholar
• Giese, K., J. Cox, and R. Grosschedl. 1992. The HMG domain of lymphoid enhancer factor 1 bends DNA and facilitates assembly of functional nucleoprotein structures. Cell 69: 185–195.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Grosschedl, R., K. Giese, and J. Pagel. 1994. HMG domain proteins: architectural elements in the assembly of nucleoprotein structures. Trends Genet. 10: 94–100.
   PubMed Web of Science ®Google Scholar
• He, T. C., A. B. Sparks, C. Rago, H. Hermeking, L. Zawel, L. T. da Costa, P. J. Morin, B. Vogelstein, and K. W. Kinzler. 1998. Identification of c-MYC as a target of the APC pathway. Science 281: 1509–1512.
   PubMed Web of Science ®Google Scholar
• Hecht, A., K. Vleminckx, M. P. Stemmler, F. van Roy, and R. Kemler. 2000. The p300/CBP acetyltransferases function as transcriptional coactivators of beta-catenin in vertebrates. EMBO J. 19: 1839–1850.
   PubMed Web of Science ®Google Scholar
• Heix, J., J. C. Zomerdijk, A. Ravanpay, R. Tjian, and I. Grummt. 1997. Cloning of murine RNA polymerase I-specific TAF factors: conserved interactions between the subunits of the species-specific transcription initiation factor TIF-IB/SL1. Proc. Natl. Acad. Sci. USA 94: 1733–1738.
   PubMedGoogle Scholar
• Hershey, J. C., M. Hautmann, M. M. Thompson, L. I. Rothblum, T. A. Haystead, and G. K. Owens. 1995. Angiotensin II-induced hypertrophy of rat vascular smooth muscle is associated with increased 18 S rRNA synthesis and phosphorylation of the rRNA transcription factor, upstream binding factor. J. Biol. Chem. 270: 25096–25101.
   PubMedGoogle Scholar
• Hirt, B. 1967. Selective extraction of polyoma DNA from infected mouse cell cultures. J. Mol. Biol. 26: 365–369.
   PubMed Web of Science ®Google Scholar
• Hisatake, K., T. Nishimura, Y. Maeda, K. Hanada, C. Z. Song, and M. Muramatsu. 1991. Cloning and structural analysis of cDNA and the gene for mouse transcription factor UBF. Nucleic Acids Res. 19: 4631–4637.
   PubMedGoogle Scholar
• 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 beta-catenin. Mol. Cell. Biol. 18: 4807–4818.
   PubMed Web of Science ®Google Scholar
• Hu, C. H., B. McStay, S. W. Jeong, and R. H. Reeder. 1994. xUBF, an RNA polymerase I transcription factor, binds crossover DNA with low sequence specificity. Mol. Cell. Biol. 14: 2871–2882.
   PubMedGoogle Scholar
• Huang, R., T. Wu, L. Xu, A. Liu, Y. Ji, and G. Hu. 2002. Upstream binding factor up-regulated in hepatocellular carcinoma is related to the survival and cisplatin-sensitivity of cancer cells. FASEB J. 16: 293–301.
   PubMedGoogle Scholar
• Imai, H., M. J. Fritzler, R. Neri, S. Bombardieri, E. M. Tan, and E. K. Chan. 1994. Immunocytochemical characterization of human NOR-90 (upstream binding factor) and associated antigens reactive with autoimmune sera. Two MR forms of NOR-90/hUBF autoantigens. Mol. Biol. Rep. 19: 115–124.
   PubMed Web of Science ®Google Scholar
• Jantzen, H. M., A. Admon, S. P. Bell, and R. Tjian. 1990. Nucleolar transcription factor hUBF contains a DNA-binding motif with homology to HMG proteins. Nature 344: 830–836.
   PubMed Web of Science ®Google Scholar
• Jantzen, H. M., A. M. Chow, D. S. King, and R. Tjian. 1992. Multiple domains of the RNA polymerase I activator hUBF interact with the TATA-binding protein complex hSL1 to mediate transcription. Genes Dev. 6: 1950–1963.
   PubMedGoogle Scholar
• Korinek, V., N. Barker, P. J. Morin, D. van Wichen, R. de Weger, K. W. Kinzler, B. Vogelstein, and H. Clevers. 1997. Constitutive transcriptional activation by a beta-catenin-Tcf complex in APC−/− colon carcinoma. Science 275: 1784–1787.
   PubMed Web of Science ®Google Scholar
• Kuhn, A., R. Voit, V. Stefanovsky, R. Evers, M. Bianchi, and I. Grummt. 1994. Functional differences between the two splice variants of the nucleolar transcription factor UBF: the second HMG box determines specificity of DNA binding and transcriptional activity. EMBO J. 13: 416–424.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Matera, A. G., W. Wu, H. Imai, C. L. O'Keefe, and E. K. Chan. 1997. Molecular cloning of the RNA polymerase I transcription factor hUBF/NOR-90 (UBTF) gene and localization to 17q21.3 by fluorescence in situ hybridization and radiation hybrid mapping. Genomics 41: 135–138.
   PubMedGoogle Scholar
• Mayall, T. P., P. L. Sheridan, M. R. Montminy, and K. A. Jones. 1997. Distinct roles for P-CREB and LEF-1 in TCR alpha enhancer assembly and activation on chromatin templates in vitro. Genes Dev. 11: 887–899.
   PubMed Web of Science ®Google Scholar
• McStay, B., M. W. Frazier, and R. H. Reeder. 1991. xUBF contains a novel dimerization domain essential for RNA polymerase I transcription. Genes Dev. 5: 1957–1968.
   PubMedGoogle Scholar
• McStay, B., C. H. Hu, C. S. Pikaard, and R. H. Reeder. 1991. xUBF and Rib 1 are both required for formation of a stable polymerase I promoter complex in X. laevis. EMBO J. 10: 2297–2303.
   PubMedGoogle Scholar
• 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 beta-catenin-induced axis formation in Xenopus embryos. Cell 86: 391–399.
   PubMed Web of Science ®Google Scholar
• Morin, P. J. 1999. Beta-catenin signaling and cancer. Bioessays 21: 1021–1030.
   PubMed Web of Science ®Google Scholar
• Morin, P. J., A. B. Sparks, V. Korinek, N. Barker, H. Clevers, B. Vogelstein, and K. W. Kinzler. 1997. Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC. Science 275: 1787–1790.
   PubMed Web of Science ®Google Scholar
• Muller, T., A. Choidas, E. Reichmann, and A. Ullrich. 1999. Phosphorylation and free pool of beta-catenin are regulated by tyrosine kinases and tyrosine phosphatases during epithelial cell migration. J. Biol. Chem. 274: 10173–10183.
   PubMedGoogle Scholar
• Munemitsu, S., I. Albert, B. Rubinfeld, and P. Polakis. 1996. Deletion of an amino-terminal sequence beta-catenin in vivo and promotes hyperphosphorylation of the adenomatous polyposis coli tumor suppressor protein. Mol. Cell. Biol. 16: 4088–4094.
   PubMedGoogle Scholar
• O'Mahony, D. J., and L. I. Rothblum. 1991. Identification of two forms of the RNA polymerase I transcription factor UBF. Proc. Natl. Acad. Sci. USA 88: 3180–3184.
   PubMedGoogle Scholar
• O'Mahony, D. J., S. D. Smith, W. Xie, and L. I. Rothblum. 1992. Analysis of the phosphorylation, DNA-binding and dimerization properties of the RNA polymerase I transcription factors UBF1 and UBF2. Nucleic Acids Res. 20: 1301–1308.
   PubMedGoogle Scholar
• O'Mahony, D. J., W. Xie, S. D. Smith, H. A. Singer, and L. I. Rothblum. 1992. Differential phosphorylation and localization of the transcription factor UBF in vivo in response to serum deprivation. J. Biol. Chem. 267: 35–38.
   PubMedGoogle Scholar
• Orford, K., C. C. Orford, and S. W. Byers. 1999. Exogenous expression of beta-catenin regulates contact inhibition, anchorage-independent growth, anoikis, and radiation-induced cell cycle arrest. J. Cell Biol. 146: 855–868.
   PubMed Web of Science ®Google Scholar
• Paddison, P., A. Caudy, and G. Hannon. 2002. Stable suppression of gene expression by RNAi in mammalian cells. Proc. Natl. Acad. Sci. USA 99: 1443–1448.
   PubMed Web of Science ®Google Scholar
• Papkoff, J., and M. Aikawa. 1998. WNT-1 and HGF regulate GSK3 beta activity and beta-catenin signaling in mammary epithelial cells. Biochem. Biophys. Res. Commun. 247: 851–858.
   PubMedGoogle Scholar
• Peifer, M., and P. Polakis. 2000. Wnt signaling in oncogenesis and embryogenesis—a look outside the nucleus. Science 287: 1606–1609.
   PubMed Web of Science ®Google Scholar
• Polakis, P. 2000. Wnt signaling and cancer. Genes Dev. 14: 1837–1851.
   PubMed Web of Science ®Google Scholar
• Putnam, C. D., G. P. Copenhaver, M. L. Denton, and C. S. Pikaard. 1994. The RNA polymerase I transactivator upstream binding factor requires its dimerization domain and high-mobility-group (HMG) box 1 to bend, wrap, and positively supercoil enhancer DNA. Mol. Cell. Biol. 14: 6476–6488.
   PubMedGoogle Scholar
• Rivera, V. M., T. Clackson, S. Natesan, R. Pollock, J. F. Amara, T. Keenan, S. R. Magari, T. Phillips, N. L. Courage, F. Cerasoli, Jr., D. A. Holt, and M. Gilman. 1996. A humanized system for pharmacologic control of gene expression. Nat. Med. 2: 1028–1032.
   PubMed Web of Science ®Google Scholar
• Roach, P. J. 1991. Multisite and hierarchal protein phosphorylation. J. Biol. Chem. 266: 14139–14142.
   PubMed Web of Science ®Google Scholar
• Roose, J., and H. Clevers. 1999. TCF transcription factors: molecular switches in carcinogenesis. Biochim. Biophys. Acta 1424: M23–M37.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Sachdev, S., L. Bruhn, H. Sieber, A. Pichler, F. Melchior, and R. Grosschedl. 2001. PIASy, a nuclear matrix-associated SUMO E3 ligase, represses LEF1 activity by sequestration into nuclear bodies. Genes Dev. 15: 3088–3103.
   PubMed Web of Science ®Google Scholar
• Sadowski, H. B., and M. Z. Gilman. 1993. Cell-free activation of a DNA-binding protein by epidermal growth factor. Nature 362: 79–83.
   PubMedGoogle Scholar
• Sampson, E. M., Z. K. Haque, M. C. Ku, S. G. Tevosian, C. Albanese, R. G. Pestell, K. E. Paulson, and A. S. Yee. 2001. Negative regulation of the Wnt-beta-catenin pathway by the transcriptional repressor HBP1. EMBO J. 20: 4500–4511.
   PubMedGoogle Scholar
• Satoh, S., Y. Daigo, Y. Furukawa, T. Kato, N. Miwa, T. Nishiwaki, T. Kawasoe, H. Ishiguro, M. Fujita, T. Tokino, Y. Sasaki, S. Imaoka, M. Murata, T. Shimano, Y. Yamaoka, and Y. Nakamura. 2000. AXIN1 mutations in hepatocellular carcinomas, and growth suppression in cancer cells by virus-mediated transfer of AXIN1. Nat. Genet. 24: 245–250.
   PubMed Web of Science ®Google Scholar
• Shtutman, M., J. Zhurinsky, I. Simcha, C. Albanese, M. D'Amico, R. Pestell, and A. Ben-Ze'ev. 1999. The cyclin D1 gene is a target of the beta-catenin/LEF-1 pathway. Proc. Natl. Acad. Sci. USA 96: 5522–5527.
   PubMed Web of Science ®Google Scholar
• Sparks, A. B., P. J. Morin, B. Vogelstein, and K. W. Kinzler. 1998. Mutational analysis of the APC/beta-catenin/Tcf pathway in colorectal cancer. Cancer Res. 58: 1130–1134.
   PubMed Web of Science ®Google Scholar
• Stefanovsky, V. Y., G. Pelletier, R. Hannan, T. Gagnon-Kugler, L. I. Rothblum, and T. Moss. 2001. An immediate response of ribosomal transcription to growth factor stimulation in mammals is mediated by ERK phosphorylation of UBF. Mol. Cell 8: 1063–1073.
   PubMed Web of Science ®Google Scholar
• Sui, G., C. Soohoo, E. Affar, F. Gay, Y. Shi, W. Forrester, and Y. Shi. 2002. A DNA vector-based RNAi technology to suppress gene expression in mammalian cells. Proc. Natl. Acad. Sci. USA 99: 5515–5520.
   PubMed Web of Science ®Google Scholar
• Tanaka, M., and W. Herr. 1990. Differential transcriptional activation by Oct-1 and Oct-2: interdependent activation domains induce Oct-2 phosphorylation. Cell 60: 375–386.
   PubMedGoogle Scholar
• Tejpar, S., C. Li, C. Yu, R. Poon, H. Denys, R. Sciot, E. Van Cutsem, J. J. Cassiman, and B. A. Alman. 2001. Tcf-3 expression and beta-catenin mediated transcriptional activation in aggressive fibromatosis (desmoid tumour). Br. J. Cancer 85: 98–101.
   PubMed Web of Science ®Google Scholar
• Tetsu, O., and F. McCormick. 1999. Beta-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 398: 422–426.
   PubMed Web of Science ®Google Scholar
• Tuan, J. C., W. G. Zhai, and L. Comai. 1999. Recruitment of TATA-binding protein-TAF complex SL1 to the human ribosomal DNA promoter is mediated by the carboxy-terminal activation domain of upstream binding factor (UBF) and is regulated by UBF phosphorylation. Mol. Cell. Biol. 19: 2872–2879.
   PubMedGoogle Scholar
• Verrijzer, C. P., and R. Tjian. 1996. TAFs mediate transcriptional activation and promoter selectivity. Trends Biochem. Sci. 21: 338–342.
   PubMed Web of Science ®Google Scholar
• Voit, R., and I. Grummt. 2001. Phosphorylation of UBF at serine 388 is required for interaction with RNA polymerase I and activation of rDNA transcription. Proc. Natl. Acad. Sci. USA 98: 13631–13636.
   PubMedGoogle Scholar
• Voit, R., M. Hoffmann, and I. Grummt. 1999. Phosphorylation by G1-specific cdk-cyclin complexes activates the nucleolar transcription factor UBF. EMBO J. 18: 1891–1899.
   PubMed Web of Science ®Google Scholar
• Voit, R., A. Schnapp, A. Kuhn, H. Rosenbauer, P. Hirschmann, H. G. Stunnenberg, and I. Grummt. 1992. The nucleolar transcription factor mUBF is phosphorylated by casein kinase II in the C-terminal hyperacidic tail which is essential for transactivation. EMBO J. 11: 2211–2218.
   PubMedGoogle Scholar
• Weng, Z., M. Xin, L. Pablo, D. Grueneberg, M. Hagel, G. Bain, T. Muller, and J. Papkoff. 2002. Protection against anoikis and down-regulation of cadherin expression by a regulatable beta-catenin protein. J. Biol. Chem. 277: 18677–18686.
   PubMed Web of Science ®Google Scholar
• Wong, N. A., and M. Pignatelli. 2002. Beta-catenin—a linchpin in colorectal carcinogenesis? Am. J. Pathol. 160: 389–401.
   PubMed Web of Science ®Google Scholar
• Yap, A. S., W. M. Brieher, and B. M. Gumbiner. 1997. Molecular and functional analysis of cadherin-based adherens junctions. Annu. Rev. Cell Dev. Biol. 13: 119–146.
   PubMed Web of Science ®Google Scholar
• Zorn, A. M., G. D. Barish, B. O. Williams, P. Lavender, M. W. Klymkowsky, and H. E. Varmus. 1999. Regulation of Wnt signaling by Sox proteins: XSox17 alpha/beta and XSox3 physically interact with beta-catenin. Mol. Cell 4: 487–498.
   PubMed Web of Science ®Google Scholar