Dynamic recruitment of axin by Dishevelled protein assemblies

Journal of Cell Science

Volumn 120, Issue 14, 2007, Pages 2402-2412

  Schwarz Romond, Thomas ^a,b   Metcalfe, Ciara ^b   Bienz, Mariann ^b  

^a EMBO   (Germany)

^b MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

Axin; Casein kinase I epsilon; Dishellved; DIX domain; Wnt signalling

Indexed keywords

AXIN; CASEIN KINASE IEPSILON; DISHEVELLED 2; GREEN FLUORESCENT PROTEIN; WNT PROTEIN;

ANIMAL CELL; ARTICLE; BINDING KINETICS; BLEACHING; CELL MEMBRANE; CELL TRANSPORT; CONTROLLED STUDY; HUMAN; HUMAN CELL; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CASEIN KINASE IEPSILON; CELL LINE; DNA-BINDING PROTEINS; GENE SILENCING; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICROFILAMENT PROTEINS; PHOSPHOPROTEINS; RECEPTORS, RETINOIC ACID; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; TRANSFECTION; WNT PROTEINS;

ANIMALIA; MAMMALIA;

EID: 34547750005     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.002956     Document Type: Article

References (69)

1. Arce, L., Yokoyama, N. N. and Waterman M. L. (2006). Diversity of LEF/TCF action in development and disease. Oncogene 25, 7492-7504.
2. Axelrod, J. D., Miller, J. R., Shulman, J. M., Moon, R. T. and Perrimon, N. (1998). Differential recruitment of Dishevelled provides signaling specificity in the planar cell polarity and Wingless signaling pathways. Genes Dev. 12, 2610-2622.
3. Bienz, M. and Clevers, H. (2000). Linking colorectal cancer to Wnt signaling. Cell 103, 311-320.
4. Bilic, J., Huang, Y.-L., Davidson, G., Zimmermann, T., Crucial, C.-M., Bienz, M. and Niehrs, C (2007). Wnt induces LRP6 signalosomes and promotes Dishevelled-dependent LRP6 phosphorylation. Science 316, 1619-1622.
5. Boutros, M., Paricio, N., Strutt, D. I. and Mlodzik, M. (1998). Dishevelled activates JNK and discriminates between JNK pathways in planar polarity and wingless signaling. Cell 94, 109-118.
6. Capelluto, D. G., Kutateladze, T. G., Habas, R., Finkielstein, C. V., He, X. and Overduin, M. (2002). The DIX domain targets dishevelled to actin stress fibres and vesicular membranes. Nature 419, 726-729.
7. Carron, C., Pascal, A., Djiane, A., Boucaut, J. C., Shi D. L. and Umbhauer, M. (2003). Frizzled receptor dimerization is sufficient to activate the Wnt/β-catenin pathway. J. Cell Sci. 116, 2541-2550.
8. Chang, W., Lloyd, C. E. and Zarkower, D. (2005). DSH-2 regulates asymmetric cell division in the early C. clegans somatic gonad. Mech. Dev. 122, 781-789.
9. Cliffe, A., Hamada, F. and Bienz, M. (2003). A Role of Dishevelled in relocating Axin to the plasma membrane during Wingless signaling. Curr. Biol. 13, 960-966.
10. Cong, F., Schweizer, L. and Varmus, H. (2004a). Casein kinase Iε modulates the signaling specificities of dishevelled. Mol. Cell. Biol. 24, 2000-2011.
11. Cong, F., Schweizer, L. and Varmus, H. (2004b). Wnt signals across the plasma membrane to activate the β-catenin pathway by forming oligomers containing its receptors, Frizzled and LRP. Development 131, 5103-5115.
12. DasGupta, R., Kaykas, A., Moon, R. T. and Perrimon, N. (2005). Functional genomic analysis of the Wnt-wingless signaling pathway. Science 308, 826-833.
13. Davidson, G., Wu, W., Shen, J., Bilic, J., Fenger, U., Stannek, P., Glinka, A. and Niehrs, C. (2005). Casein kinase 1-γ. couples Wnt receptor activation to cytoplasmic signal transduction. Nature 438, 867-872.
14. Fagotto, F., Jho, E., Zeng, L., Kurth, T., Joos, T., Kaufmann, C. and Costantini, F. (1999). Domains of axin involved in protein-protein interactions, wnt pathway inhibition, and intracellular localization. J. Cell Biol. 145, 741-756.
15. Gao, Z. H., Seelling, J. M., Hill, V., Yochum, A. and Virshup, D. M. (2002). Casein kinase I phosphorylates and destabilizes the β-catenin degradation complex. Proc. Natl. Acad. Sci. USA 99, 1182-1187.
16. Hawkins, N. C., Ellis, G. C., Bowerman, B. and Garriga, G. (2005). MOM-5 Frizzled regulates the distribution of DSH-2 to control C. elegans asymmetric neuroblast divisions. Dev. Biol. 284, 246-259.
17. He, X., Saint-Jeannet, J. P., Woodgett, J. R., Varmus, H. E. and Dawid, I. B. (1995). Glycogen synthase kinase-3 and dorsoventral patterning in Xenopus embryos. Nature 374, 617-622.
18. He, X., Saint-Jeannet, J. P., Wang, Y., Nathans, J., Dawid, I. and Varmus, H. (1997). A member of the Frizzled protein family mediating axis induction by Wit-5A. Science 275, 1652-1654.
19. Hino, S., Michiue, T., Asashima, M. and Kikuchi, A. (2003). Casein kinase Iε enhances the binding of Dvl-1 to Frat-1 and is essential for Wnt-3a-induced accumulation of β-catenin. J. Biol. Chem. 278, 14066-14073.
20. Hsu, W., Zeng, L. and Costantini, F. (1999). Identification of a domain of Axin that binds to the serine/threonine protein phosphatase 2A and a self-binding domain. J. Biol. Chem. 274, 3439-3445.
21. Itoh, K., Brott, B. K., Bae, G. U., Ratcliffe, M. J. and Sokol, S. Y. (2005). Nuclear localization is required for Dishevelled function in Wnt/β-catenin signaling. J. Biol. 4, 3.
22. Julius, M. A., Schelbert, B., Hsu, W., Fitzpatrick, E., Jho, E., Fagotto, F., Costantini, F. and Kitajewski, J. (2000). Domains of axin and disheveled required for interaction and function in wnt signaling. Biochem. Biophys. Res. Commun. 276, 1162-1169.
23. Kimelman, D. and Xu, W. (2006). The β-catenin destruction complex: insights and questions from a structural perspective. Oncogene 25, 7482-7491.
24. Kishida, M., Hino, S., Michiue, T., Yamamoto, H., Kishida, S., Fakui, A., Asashima, M. and Kikuchi, A. (2001). Synergistic activation of the Wnt signaling pathway by Dvl and casein kinase Iε. J. Biol. Chem. 276, 33147-33155.
25. Kishida, S., Yamamoto, H., Hino, S., Ikeda, S., Kishida, M. and Kikuchi, A. (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.
26. Klein, T. J., Jenny, A., Djiane, A. and Mlodzik, M. (2006). CKIε/ discs overgrown promotes both Wnt-Fz/β-catenin and Fz /PCP signaling in Drosophila. Curr. Biol. 16, 1337-1343.
27. Klimowski, L. K., Garcia, B. A., Shabanowitz, J. Hunt, D. F. and Virshup, D. M. (2006). Site-specific casein kinase Iε-dependent phosphorylation of Dishevelled modulates β-catenin signaling. FEBS J. 273, 4594-4602.
28. Klingensmith, J., Nusse, R. and Perrimon, N. (1994). The Drosophila segment polarity gene dishevelled encodes a novel protein required for response to the wingless signal. Genes Dev. 8, 118-130.
29. Korinek, V., Barker, N., Morin, P. J., van Wichen, D., de Weger, R., Kinzler, K. W., Vogelstein, B. and Clevers, H. (1997). Constitutive transcriptional activation by a β-catenin-Tcf complex in APC-/- colon carcinoma. Science 275, 1784-1787.
30. Kusano, S. and Raab-Traub, N. (2002). I-mfa domain proteins interact with Axin and affect its regulation of the Wnt and c-Jun N-terminal kinase signaling pathways. Mol. Cell. Biol. 22, 6393-6405.
31. Lee, E., Salic, A., Kruger, R., Heinrich, R. and Kirschner, M. W. (2003). The roles of APC and Axin derived from experimental and theoretical analysis of the Wnt pathway. PLoS Biol. 1, E10.
32. Li, L., Yuan, H., Weaver, C. D., Mao, J., Farr, G. H., 3rd, Sussman, D. J., Jonkers, J, Kimelman, D. and Wu, D. (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.
33. Logan, C. Y. and Nusse, R. (2004). The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 20, 781-810.
34. Luo, W., Zou, H., Jin, L., Lin, S., Li, Q., Ye, Z., Rui, H. and Lin, S. C. (2004). Axin contains three separable domains that confer intramolecular, homodimeric, and heterodimeric interactions involved in distinct functions. J. Biol. Chem. 280, 5054-5060.
35. Malbon, C. C. and Wang, H. Y. (2006). Dishevelled: a mobile scaffold catalyzing development. Curr. Top. Dev. Biol. 72, 153-166.
36. McKay, R. M., Peters, J. M. and Graff, J. M. (2001). The casein kinase I family in Wnt signaling. Dev. Biol. 235, 388-396.
37. Miller, J. R., Rowning, B. A., Larabell, C. A., Yang-Snyder, J. A., Bates, R. L. and Moon, R. T. (1999). Establishment of the dorsal-ventral axis in Xenopus embryos coincides with the dorsal enrichment of dishevelled that is dependent on cortical rotation. J. Cell Biol. 146, 427-437.
38. Moriguchi, T., Kawachi, K., Kamakura S., Masuyanma, N., Yamanaka, H., Matsumoto, K., Kikuchi, A. and Nishida, E. (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.
39. Nichols, B. J. (2002). A distinct class of endosome mediates clathrin-independent endocytosis to the Golgi complex. Nat. Cell Biol. 4, 374-378.
40. Park, T. J. Gray, R. S., Sato, A., Habas, R. and Wallingford, J. B. (2005). Subcellular localization and signaling properties of dishevelled in developing vertebrate embryos. Curr. Biol. 15, 1039-1044.
41. Penton, A., Wodarz, A. and Nusse, R. (2002). A mutational analysis of dishevelled in Drosophila defines novel domains in the dishevelled protein as well as novel suppressing alleles of axin. Genetics 161, 747-762.
42. Peters, J. M., McKay, R. M., McKay, J. P. and Graff, J. M. (1999). Casein kinase I transduces Wnt signals. Nature 401, 345-350.
43. Polakis, P. (2000). Wnt signaling and cancer. Genes Dev. 14, 1837-1851.
44. Price, M. A. (2006). CKI there's more than one: casein kinase I family members in Wnt and Hedgehog signaling. Genes Dev. 20, 399-410.
45. Rodrigues, G. A. and Park, M. (1993). Dimerization mediated through a leucine zipper activates the oncogenic potential of the met receptor tyrosine kinase. Mol. Cell. Biol. 13, 6711-6722.
46. Rosin-Arbesfeld, R., Townsley, F. and Bienz, M. (2000). The APC tumour suppressor has a nuclear export function. Nature 406, 1009-1012.
47. Rothbächer, U, Laurent, M. N., Deardorff, M. A., Klein, P. S., Cho, K. W. and Fraser, S. E. (2000). Dishevelled phosphorylation, subcellular localization and multimerization regulate its role in early embryogenesis. EMBO J. 19, 1010-1022.
48. Sakanaka C. and Williams, L. T. (1999). Functional domains of axin. Importance of the c terminus as an oligomerization domain. J. Biol. Chem. 274, 14090-14093.
49. Sakanaka, C., Leong, P., Xu, L., Harrison, S. D. and Willin L. T. (1999). Casein kinase Iε in the wnt pathway: regulation of β-catenin function. Proc. Natl. Acad. Sci. USA 96, 12548-12552.
50. Schwarz-Romond, T., Asbrand, C, Bakkers, J., Kuhl, M., Schaeffer, H. J., Huelsken, J., Behrens, J., Hammerschmidt, M. and Birchmeier, W. (2002). The ankyrin repeat protein Diversin recruits Casein kinase Iε to the β-catenin degradation complex and acts in both canonical Wnt and Wnt/JNK signaling. Genes Dev. 16, 2073-2094.
51. Schwarz-Romond, T., Merrifield, C., Nichols, B. J. and Bienz, M. (2005). The Wnt signalling effector Dishevelled forms dynamic protein assemblies rather than stable associations with cytoplasmic vesicles. J. Cell Sci. 118, 5269-5277.
52. Schwarz-Romond, T., Fiedler, M., Shibata, N., Butler, P. J. G., Kikuchi, A., Yoshiki, Y. and Bienz, M. (2007). The DIX domain of Dishevelled confers Wnt signaling by dynamic polymerization. Nat. Struct. Mol. Biol. 14, 484-492.
53. Semenov, M. V. and Snyder, M. (1997). Human dishevelled genes constitute a DHR-containing multigene family. Genomics 42, 302-310.
54. Shiomi, K., Uchida, H., Keino-Masu, K. and Masu, M. (2003). Ccd1, a novel protein with a DIX domain, is a positive regulator in the Wnt signaling during zebrafish neural patterning. Curr. Biol. 13, 73-77.
55. Smalley, M. J, Sara, E., Paterson, H., Naylor, S., Cook, D, Jayatilake, H, Fryer, L. G, Hutchinson, L., Fry, M. J. and Dale, T. C. (1999). Interaction of axin and dvl-2 proteins regulates dvl-2-stimulated TCF- dependent transcription. EMBO J. 18, 2823-2835.
56. Spink, K. E., Polakis, F. and Weis, W. I. (2000). Structural basis of Lhe Axin-adenomatous polyposis coli interaction. EMBO J. 19, 2270-2279.
57. Strutt, H., Price, M. A. and Strutt, D (2006). Planar polarity is positively regulated by casein kinase Iε in Drosophila. Curr. Biol. 16, 1329-1336.
58. Tamai, K., Zeng, X., Liu, C, Zhang, X, Harada, Y, Chang, Z. and He, X. (2004). A mechanism for Wnt coreceptor activation. Mol. Cell 13, 149-156.
59. Theisen, H, Purcell, J, Bennett, M, Kansagara, D., Syed, A. and Marsh, J. L. (1994). dishevelled is required during wingless signaling to establish both cell polarity and cell identity. Development 120, 347-360.
60. Torres, M. A. and Nelson, W. J. (2000). Colocalization and redistribution of dishevelled and actin during Wnt-induced mesenchymal morphogenesis. J. Cell Biol. 149, 1433-1442.
61. Umbhauer, M., Djiane, A., Goisset, C., Penzo-Mendez, A., Riou, J. F., Boucaut, J. C. and Sid, D. L. (2000). The C-terminal cytoplasmic Lys-thr-X-X-X-Trp motif in frizzled receptors mediates Wnt/β-catenin signalling. EMBO J. 19, 4944-4954.
62. Walston, T., Tuskey, C., Edgar, L, Hawkins N., Ellis, G, Bowerman, B., Wood, W. and Hardin, J. (2004). Multiple Wnt signaling pathways converge to orient the mitotic spindle in early C. elegans embryos. Dev. Cell 7, 831-841.
63. Wharton, K. A, Jr (2003). Runnin' with the Dvl: proteins that associate with Dsh/Dvl and their significance to Wnt signal transduction. Dev. Biol. 253, 1-17.
64. Wong, H. C., Mao, J., Nguyen, J. T., Srinivas, S., Zhang, W., Liu B., Liu, L, Wu, D, and Zheng, J. (2000). Structural basis of the recognition of the dishevelled DEP domain in the Wnt signaling pathway. Nat. Struct. Biol. 7, 1178-1184.
65. Wong, H. C, Bourdelas A., Krauss, A. Lee, H. J, Shan, Y., Wu, D, Mlodzik M., Shi, D L. and Zheng, J. (2003). Direct binding of the PDZ domain of Dishevelled to a conserved internal sequence in the C-terminal region of Frizzled. Mol. Cell 12, 1251-1260.
66. Yanagawa, S, van Leeuwen, F., Wodarz, A, Klingensmith, J. and Nusse, R. (1995). The dishevelled protein is modified by wingless signaling in Drosophila. Genes Dev. 9, 1087-1097.
67. Yang-Snyder, J., Miller, J. R., Brown, J. D., Lai, C. J. and Moon, R. T. (1996). A frizzled homolog functions in a vertebrate Wnt signaling pathway. Curr. Biol. 6, 1302-1306.
68. Zeng, L., Fagotto, F., Zhang, T., Hsu, W., Vasicek, T. J. Perry, W. L., 3rd, Lee, J. J., Tilghman, S. M., Gumbiner, B. M. and Costantini, F. (1997). The mouse Fused locus encodes Axin, an inhibitor of the Wnt signaling pathway that regulates embryonic axis formation. Cell 90, 181-192.
69. Zeng, X., Tamai, K., Doble, B, Li, S., Huang, H., Habas, R., Okumura, H., Woodgett, J. and He, X. (2005). A dual-kinase mechanism for Wnt co-receptor phosphorylation and activation. Nature 438, 873-877.