Inhibition of the Wnt Signaling Pathway by Idax, a Novel Dvl-Binding Protein

REFERENCES

• Axelrod, J. D., J. R. Miller, J. M. Shulman, R. T. Moon, and N. Perrimon. 1998. Differential recruitment of Dishevelled provides signaling specificity in the planar cell polarity and Wingless signaling pathways. Genes Dev. 12:2610–2622.
   PubMed Web of Science ®Google Scholar
• Behrens, J., B.-A. Jerchow, M. Würtele, J. Grimm, C. Asbrand, R. Wirtz, M. Kühl, D. Wedlich, and W. Birchmeier. 1998. Functional interaction of an Axin homolog, conductin, with β-catenin, APC, and GSK3β. Science 280:596–599.
   PubMed Web of Science ®Google Scholar
• Behrens, J., J. P. von Kries, M. Kühl, 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.
   PubMed Web of Science ®Google Scholar
• Boutros, M., N. Paricio, D. I. Strutt, and M. Mlodzik. 1998. Dishevelled activates JNK and discriminates between JNK pathways in planar polarity and wingless signaling. Cell 94:109–118.
   PubMed Web of Science ®Google Scholar
• Bradford, M. M.. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248–254.
   PubMed Web of Science ®Google Scholar
• Brannon, M., M. Gomperts, L. Sumoy, R. T. Moon, and D. Kimelman. 1997. A β-catenin/XTcf-3 complex binds to the siamois promoter to regulate dorsal axis specification in Xenopus. Genes Dev. 11:2359–2370.
   PubMedGoogle Scholar
• Cadigan, K. M., and R. Nusse. 1997. Wnt signaling: a common theme in animal development. Genes Dev. 11:3286–3305.
   PubMed Web of Science ®Google Scholar
• Craven, S. E., and D. S. Bredt. 1998. PDZ proteins organize synaptic signaling pathways. Cell 93:495–498.
   PubMed Web of Science ®Google Scholar
• Dale, T. C.. 1998. Signal transduction by the Wnt family of ligands. Biochem. J. 329:209–223.
   PubMed Web of Science ®Google Scholar
• Fagotto, F., E. Jho, L. Zeng, T. Kurth, T. Joos, C. Kaufmann, and F. Costantini. 1999. Domains of Axin involved in protein-protein interactions, Wnt pathway inhibition, and intracellular localization. J. Cell Biol. 145:741–756.
   PubMed Web of Science ®Google Scholar
• Funayama, N., F. Fagotto, P. McCrea, and B. M. Gumbiner. 1995. Embryonic axis induction by the armadillo repeat domain of β-catenin: evidence for intracellular signaling. J. Cell Biol. 128:959–968.
   PubMed Web of Science ®Google Scholar
• Hart, M., J.-P. Concordet, I. Lassot, I. Albert, R. del los Santos, H. Durand, C. Perret, B. Rubinfeld, F. Margottin, R. Benarous, and P. Polakis. 1999. The F-box protein β-TrCP associates with phosphorylated β-catenin and regulates its activity in the cell. Curr. Biol. 9:207–210.
   PubMed Web of Science ®Google Scholar
• Hart, M. J., R. de los Santos, I. N. Albert, B. Rubinfeld, and P. Polakis. 1998. Downregulation of β-catenin by human Axin and its association with the APC tumor suppressor, β-catenin and GSK-3β. Curr. Biol. 8:573–581.
   PubMed Web of Science ®Google Scholar
• He, T.-C., T. A. Chan, B. Vogelstein, and K. W. Kinzler. 1999. PPARδ is an APC-regulated target of nonsteroidal anti-inflammatory drugs. Cell 99:335–345.
   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
• Heisenberg, C. P., M. Tada, G. J. Rauch, L. Saúde, M. L. Concha, R. Geisler, D. L. Stemple, J. C. Smith, and S. W. Wilson. 2000. Silberblick/Wnt11 mediates convergent extension movements during zebrafish gastrulation. Nature 405:76–81.
   PubMed Web of Science ®Google Scholar
• Huber, O., R. Korn, J. McLaughlin, M. Ohsugi, B. G. Herrmann, and R. Kemler. 1996. Nuclear localization of β-catenin by interaction with transcription factor LEF-1. Mech. Dev. 59:3–10.
   PubMed Web of Science ®Google Scholar
• Huelsken, J., R. Vogel, V. Brinkmann, B. Erdmann, C. Birchmeier, and W. Birchmeier. 2000. Requirement for β-catenin in anterior-posterior axis formation in mice. J. Cell Biol. 148:567–578.
   PubMed Web of Science ®Google Scholar
• Ikeda, S., M. Kishida, Y. Matsuura, H. Usui, and A. Kikuchi. 2000. GSK-3β-dependent phosphorylation of adenomatous polyposis coli gene product can be modulated by β-catenin and protein phosphatase 2A complexed with Axin. Oncogene 19:537–545.
   PubMedGoogle Scholar
• 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-3β and β-catenin and promotes GSK-3β-dependent phosphorylation of β-catenin. EMBO J. 17:1371–1384.
   PubMed Web of Science ®Google Scholar
• Itoh, K., A. Antipova, M. J. Ratcliffe, and S. Sokol. 2000. Interaction of Dishevelled and Xenopus Axin-related protein is required for Wnt signal transduction. Mol. Cell. Biol. 20:2228–2238.
   PubMedGoogle Scholar
• Itoh, K., V. E. Krupnik, and S. Y. Sokol. 1998. Axis determination in Xenopus involves biochemical interactions of axin, glycogen synthase kinase 3 and β-catenin. Curr. Biol. 8:591–594.
   PubMedGoogle Scholar
• Kadoya, T., S. Kishida, A. Fukui, T. Hinoi, T. Michiue, M. Asashima, and A. Kikuchi. Inhibition of Wnt signaling pathway by a novel Axin-binding protein. J. Biol. Chem., in press.
   Google Scholar
• Kao, K. R., and R. P. Elinson. 1988. The entire mesodermal mantle behaves as Spemann's organizer in dorsoanterior enhanced Xenopus laevis embryos. Dev. Biol. 127:64–77.
   PubMed Web of Science ®Google Scholar
• Kikuchi, A.. 1999. Roles of Axin in the Wnt signalling pathway. Cell. Signal. 11:777–788.
   PubMed Web of Science ®Google Scholar
• Kishida, M., S. Koyama, S. Kishida, K. Matsubara, S. Nakashima, K. Higano, R. Takada, S. Takada, and A. Kikuchi. 1999. Axin prevents Wnt-3a-induced accumulation of β-catenin. Oncogene 18:979–985.
   PubMed Web of Science ®Google Scholar
• Kishida, S., H. Yamamoto, S.-I. Hino, S. Ikeda, M. Kishida, and A. Kikuchi. 1999. DIX domains of Dvl and Axin are necessary for protein interactions and their ability to regulate β-catenin stability. Mol. Cell. Biol. 19:4414–4422.
   PubMed Web of Science ®Google Scholar
• 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 β-catenin. J. Biol. Chem. 273:10823–10826.
   PubMed Web of Science ®Google Scholar
• Kitagawa, M., S. Hatakeyama, M. Shirane, M. Matsumoto, N. Ishida, K. Hattori, I. Nakamichi, A. Kikuchi, K.-I. Nakayama, and K. Nakayama. 1999. An F-box protein, FWD1, mediates ubiquitin-dependent proteolysis of β-catenin. EMBO J. 18:2401–2410.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• Klingensmith, J., Y. Yang, J. D. Axelrod, D. R. Beier, N. Perrimon, and D. J. Sussman. 1996. Conservation of dishevelled structure and function between flies and mice: isolation and characterization of Dvl2. Mech. Dev. 58:15–26.
   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 β-catenin-Tcf complex in APC−/− colon carcinoma. Science 275:1784–1787.
   PubMed Web of Science ®Google Scholar
• Kozak, M.. 1987. An analysis of 5′-noncoding sequences from 699 vertebrate messenger RNAs. Nucleic Acids Res. 15:8125–8148.
   PubMed Web of Science ®Google Scholar
• Kreig, P. A., and D. A. Melton. 1984. Functional messenger RNAs are produced by SP6 in vitro transcription of cloned cDNAs. Nucleic Acids Res. 12:7057–7070.
   PubMedGoogle Scholar
• Lee, J.-S., A. Ishimoto, and S.-I. Yanagawa. 1999. Characterization of mouse dishevelled (Dvl) proteins in Wnt/Wingless signaling pathway. J. Biol. Chem. 274:21464–21470.
   PubMedGoogle Scholar
• Lemaire, P., N. Garrett, and J. B. Gurdon. 1995. Expression cloning of Siamois, a Xenopus homeobox gene expressed in dorsal-vegetal cells of blastulae and able to induce a complete secondary axis. Cell 81:85–94.
   PubMedGoogle Scholar
• Li, L., H. Yuan, C. D. Weaver, J. Mao, G. H. Farr III, D. J. Sussman, J. Jonkers, D. Kimelman, and D. Wu. 1999. Axin and Frat1 interact with Dvl and GSK, bridging Dvl to GSK in Wnt-mediated regulation of LEF-1. EMBO J. 18:4233–4240.
   PubMed Web of Science ®Google Scholar
• Li, L., H. Yuan, W. Xie, J. Mao, A. M. Caruso, A. McMahon, D. J. Sussman, and D. Wu. 1999. Dishevelled proteins lead to two signaling pathways. J. Biol. Chem. 274:129–134.
   PubMed Web of Science ®Google Scholar
• Liu, P., M. Wakamiya, M. J. Shea, U. Albrecht, R. R. Behringer, and A. Bradley. 1999. Requirement for Wnt3 in vertebrate axis formation. Nat. Genet. 22:361–365.
   PubMed Web of Science ®Google Scholar
• Maniatis, T.. 1982. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y
   Google Scholar
• Mann, B., M. Gelos, A. Siedow, M. L. Hanski, A. Gratchev, M. Ilyas, W. F. Bodmer, M. P. Moyer, E. O. Riecken, H. J. Buhr, and C. Hanski. 1999. Target genes of β-catenin-T cell-factor/lymphoid-enhancer-factor signaling in human colorectal carcinomas. Proc. Natl. Acad. Sci. USA 96:1603–1608.
   PubMed Web of Science ®Google Scholar
• Miller, J. R., A. M. Hocking, J. D. Brown, and R. T. Moon. 1999. Mechanism and function of signal transduction by the Wnt/β-catenin and Wnt/Ca2+ pathways. Oncogene 18:7860–7872.
   PubMed Web of Science ®Google Scholar
• Molenaar, M., M. van de Wetering, M. Oosterwegel, J. Peterson-Maduro, S. Godsave, V. Korinek, J. Roose, O. Destrée, and H. Clevers. 1996. XTcf-3 transcription factor mediates β-catenin-induced axis formation in Xenopus embryos. Cell 86:391–399.
   PubMed Web of Science ®Google Scholar
• Moon, R. T., and D. Kimelman. 1998. From cortical rotation to organizer gene expression: toward a molecular explanation of axis specification in Xenopus. Bioessays 20:536–545.
   PubMedGoogle Scholar
• Moriguchi, T., K. Kawachi, S. Kamakura, N. Masuyama, H. Yamanaka, K. Matsumoto, A. Kikuchi, and E. Nishida. 1999. Distinct domains of mouse dishevelled are responsible for the c-Jun N-terminal kinase/stress-activated protein kinase activation and the axis formation in vertebrates. J. Biol. Chem. 274:30957–30962.
   PubMed Web of Science ®Google Scholar
• Nakashima, S., K. Morinaka, S. Koyama, M. Ikeda, M. Kishida, K. Okawa, A. Iwamatsu, S. Kishida, and A. Kikuchi. 1999. Small G protein Ral and its downstream molecules regulate endocytosis of EGF and insulin receptors. EMBO J. 18:3629–3642.
   PubMed Web of Science ®Google Scholar
• Peters, J. M., R. M. McKay, J. P. McKay, and J. M. Graff. 1999. Casein kinase I transduces Wnt signals. Nature 401:345–350.
   PubMed Web of Science ®Google Scholar
• Pizzuti, A., F. Amati, G. Calabrese, A. Mari, A. Colosimo, V. Silani, L. Giardino, A. Ratti, D. Penso, L. Calzà, G. Palka, G. Scarlato, G. Novelli, and B. Dallapiccola. 1996. cDNA characterization and chromosomal mapping of two human homologues of the Drosophila dishevelled polarity gene. Hum. Mol. Genet. 5:953–958.
   PubMedGoogle Scholar
• Rothbächer, U., M. N. Laurent, M. A. Deardorff, P. S. Klein, K. W. Y. Cho, and S. E. Fraser. 2000. Dishevelled phosphorylation, subcellular localization and multimerization regulate its role in early embryogenesis. EMBO J. 19:1010–1022.
   PubMed Web of Science ®Google Scholar
• Sakamoto, I., S. Kishida, A. Fukui, M. Kishida, H. Yamamoto, S.-I. Hino, T. Michiue, S. Takada, M. Asashima, and A. Kikuchi. 2000. A novel β-catenin-binding protein inhibits β-catenin-dependent tcf activation and axis formation. J. Biol. Chem. 275:32871–32878.
   PubMedGoogle Scholar
• Sakanaka, C., P. Leong, L. Xu, S. D. Harrison, and L. T. Williams. 1999. Casein kinase Iɛ in the wnt pathway: regulation of β-catenin function. Proc. Natl. Acad. Sci. USA 96:12548–12552.
   PubMed Web of Science ®Google Scholar
• Sakanaka, C., J. B. Weiss, and L. T. Williams. 1998. Bridging of β-catenin and glycogen synthase kinase-3β by Axin and inhibition of β-catenin-mediated transcription. Proc. Natl. Acad. Sci. USA 95:3020–3023.
   PubMed Web of Science ®Google Scholar
• Scharf, S. R., and J. C. Gerhart. 1980. Determination of the dorsal-ventral axis in eggs of Xenopus laevis: complete rescue of uv-impaired eggs by oblique orientation before first cleavage. Dev. Biol. 79:181–198.
   PubMedGoogle Scholar
• Shibamoto, S., K. Higano, R. Takada, F. Ito, M. Takeichi, and S. Takada. 1998. Cytoskeletal reorganization by soluble Wnt-3a protein signalling. Genes Cells 3:659–670.
   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 β-catenin/LEF-1 pathway. Proc. Natl. Acad. Sci. USA 96:5522–5527.
   PubMed Web of Science ®Google Scholar
• Smalley, M. J., E. Sara, H. Paterson, S. Naylor, D. Cook, H. Jayatilake, L. G. Fryer, L. Hutchinson, M. J. Fry, and T. C. Dale. 1999. Interaction of Axin and Dvl-2 proteins regulates Dvl-2 stimulated TCF-dependent transcription. EMBO J. 18:2823–2835.
   PubMed Web of Science ®Google Scholar
• Sokol, S. Y.. 1996. Analysis of Dishevelled signalling pathways during Xenopus development. Curr. Biol. 6:1456–1467.
   PubMedGoogle Scholar
• Songyang, Z., A. S. Fanning, C. Fu, J. Xu, S. M. Marfatia, A. H. Chishti, A. Crompton, A. C. Chan, J. M. Anderson, and L. C. Cantley. 1997. Recognition of unique carboxyl-terminal motifs by distinct PDZ domains. Science 275:73–77.
   PubMed Web of Science ®Google Scholar
• Strovel, E. T., D. Wu, and D. J. Sussman. 2000. Protein phosphatase 2Cα dephosphorylates Axin and activates LEF-1-dependent transcription. J. Biol. Chem. 275:2399–2403.
   PubMedGoogle Scholar
• Strutt, D. I., U. Weber, and M. Mlodzik. 1997. The role of RhoA in tissue polarity and Frizzled signalling. Nature 387:292–295.
   PubMedGoogle Scholar
• Sussman, D. J., J. Klingensmith, P. Salinas, P. S. Adams, R. Nusse, and N. Perrimon. 1994. Isolation and characterization of a mouse homolog of the Drosophila segment polarity gene dishevelled. Dev. Biol. 166:73–86.
   PubMedGoogle Scholar
• Tada, M., and J. C. Smith. 2000. Xwnt11 is a target of Xenopus Brachyury: regulation of gastrulation movements via Dishevelled, but not through the canonical Wnt pathway. Development 127:2227–2238.
   PubMed Web of Science ®Google Scholar
• Takada, S., K. L. Stark, M. J. Shea, G. Vassileva, J. A. McMahon, and A. P. McMahon. 1994. Wnt-3a regulates somite and tailbud formation in the mouse embryo. Genes Dev. 8:174–189.
   PubMed Web of Science ®Google Scholar
• Tetsu, O., and F. McCormick. 1999. β-Catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 398:422–426.
   PubMed Web of Science ®Google Scholar
• Theisen, H., J. Purcell, M. Bennett, D. Kansagara, A. Syed, and J. L. Marsh. 1994. Dishevelled is required during wingless signaling to establish both cell polarity and cell identity. Development 120:347–360.
   PubMed Web of Science ®Google Scholar
• Tian, Q., T. Nakayama, M. P. Dixon, and J. L. Christian. 1999. Post-transcriptional regulation of Xwnt-8 expression is required for normal myogenesis during vertebrate embryonic development. Development 126:3371–3380.
   PubMedGoogle Scholar
• van Genderen, C., R. M. Okamura, I. Fariñas, R.-G. Quo, T. G. Parslow, L. Bruhn, and R. Grosschedl. 1994. Development of several organs that require inductive epithelial-mesenchymal interactions is impaired in LEF-1-deficient mice. Genes Dev. 8:2691–2703.
   PubMed Web of Science ®Google Scholar
• Willert, K., M. Brink, A. Wodarz, H. Varmus, and R. Nusse. 1997. Casein kinase 2 associates with phosphorylates Dishevelled. EMBO J. 16:3089–3096.
   PubMed Web of Science ®Google Scholar
• Wodarz, A., and R. Nusse. 1998. Mechanisms of Wnt signaling in development. Annu. Rev. Cell Dev. Biol. 14:59–88.
   PubMed Web of Science ®Google Scholar
• Yamamoto, H., S. Kishida, M. Kishida, S. Ikeda, S. Takada, and A. Kikuchi. 1999. Phosphorylation of Axin, a Wnt signal negative regulator, by glycogen synthase kinase-3β regulates its stability. J. Biol. Chem. 274:10681–10684.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• Yanagawa, S.-I., J.-S. Lee, T. Haruna, H. Oda, T. Uemura, M. Takeichi, and A. Ishimoto. 1997. Accumulation of Armadillo induced by Wingless, Dishevelled, and dominant-negative Zeste-white 3 leads to elevated DE-cadherin in Drosophila clone 8 wing disc cells. J. Biol. Chem. 272:25243–25251.
   PubMedGoogle Scholar
• Yanagawa, S.-I., F. van Leeuwen, A. Wodarz, J. Klingensmith, and R. Nusse. 1995. The Dishevelled protein is modified by Wingless signaling in Drosophila. Genes Dev. 9:1087–1097.
   PubMed Web of Science ®Google Scholar
• Yost, C., G. H. Farr III, S. B. Pierce, D. M. Ferkey, M. M. Chen, and D. Kimelman. 1998. GBP, an inhibitor of GSK-3, is implicated in Xenopus development and oncogenesis. Cell 93:1031–1041.
   PubMed Web of Science ®Google Scholar
• Yost, C., M. Torres, J. R. Miller, E. Huang, D. Kimelman, and R. T. Moon. 1996. The axis-inducing activity, stability, and subcellular distribution of β-catenin is regulated in Xenopus embryos by glycogen synthase kinase 3. Genes Dev. 10:1443–1454.
   PubMed Web of Science ®Google Scholar
• Zeng, L., F. Fagotto, T. Zhang, W. Hsu, T. J. Vasicek, W. L. Perry III, 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.
   PubMed Web of Science ®Google Scholar