The developmental biology of Dishevelled: An enigmatic protein governing cell fate and cell polarity

Development

Volumn 132, Issue 20, 2005, Pages 4421-4436

  Wallingford, John B ^a   Habas, Raymond ^b,c  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^c RUTGERS CANCER INSTITUTE OF NEW JERSEY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AXIN; BETA CATENIN; CALCIUM ION; CASEIN KINASE I; CASEIN KINASE II; DISHEVELLED PROTEIN; GLYCOGEN SYNTHASE KINASE 3; GLYPICAN; LIPOPROTEIN RECEPTOR; MEMBRANE PROTEIN; PROTEIN TYROSINE KINASE; RAC PROTEIN; RECEPTOR PROTEIN; RECEPTOR TYROSINE KINASE LIKE ORPHAN RECEPTOR 2; REGULATOR PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG; WNT PROTEIN;

CELL DIVISION; CELL FATE; CELL MIGRATION; CELL POLARITY; CELLULAR DISTRIBUTION; DEVELOPMENTAL BIOLOGY; EMBRYO AXIS; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; EMBRYO POLARITY; EMBRYO SEGMENTATION; GASTRULATION; HEART DEVELOPMENT; HUMAN; NERVOUS SYSTEM DEVELOPMENT; NERVOUS SYSTEM FUNCTION; NEURAL TUBE DEFECT; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; SOCIAL BEHAVIOR; VERTEBRATE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; CELL POLARITY; HUMANS; PHOSPHOPROTEINS; SIGNAL TRANSDUCTION; WNT PROTEINS;

ANIMALIA; HYDRA; VERTEBRATA;

EID: 27744535862     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.02068     Document Type: Review

References (202)

1. Aberle, H., Bauer, A., Stappert, J., Kispert, A. and Kemler, P. (1997). β-catenin is a target for the ubiquitin-proteasome pathway. EMBO J. 16, 3797-3804.
2. Adler, P. N. (1992). The genetic control of tissue polarity in Drosophila. BioEssays 14, 735-741.
3. Amit, S., Hatzubai, A., Birman, Y., Andersen, J. S., Ben-Shushan, E., Mann, M., Ben-Neriah, Y. and Alkalay, I. (2002). Axin-mediated CKI phosphorylation of β-catenin at Ser 45, a molecular switch for the Wnt pathway. Genes Dev. 16, 1066-1076.
4. Axelrod, J. D. (2001). Unipolar membrane association of Dishevelled mediates Frizzled planar cell polarity signaling. Genes Dev. 15, 1182-1187.
5. Axelrod, J. D., Matsuno, K., Artavanis-Tsakonas, S. and Perrimon, N. (1996). Interaction between Wingless and Notch signaling pathways mediated by dishevelled. Science 271, 1826-1832.
6. 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.
7. Baker, J. C., Beddington, R. S. and Harland, R. M. (1999). Wnt signaling in Xenopus embryos inhibits bmp4 expression and activates neural development. Genes Dev. 13, 3149-3159.
8. Bastock, R, Strutt, H. and Strutt, D. (2003). Strabismus is asymmetrically localised and binds to Prickle and Dishevelled during Drosophila planar polarity patterning. Development 130, 3007-3014.
9. Bellaiche, Y., Gho, M., Kaltschmidt, J. A., Brand, A. H. and Schweisguth, F. (2001). Frizzled regulates localization of cell-fate determinants and mitotic spindle rotation during asymmetric cell division. Nat. Cell. Biol. 3, 50-57.
10. Bienz, M. and Clevers, H. (2003). Armadillo/β-catenin signals in the nucleus - proof beyond a reasonable doubt? Nat. Cell. Biol. 5, 179-182.
11. 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.
12. Boutros, M., Mihaly, J., Bouwmeester, T. and Mlodzik, M. (2000). Signaling specificity by Frizzled receptors in Drosophila. Science 288, 1825-1828.
13. 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.
14. Chang, W., Lloyd, C. E. and Zarkower, D. (2005). DSH-2 regulates asymmetric cell division in the early C. elegans somatic gonad. Mech. Dev. 122, 781-789.
15. Chen, W., ten Berge, D., Brown, J., Ahn, S., Hu, L. A., Miller, W. E., Caron, M. G., Barak, L. S., Nusse, R. and Lefkowitz, R. J. (2003). Dishevelled 2 recruits β-arrestin 2 to mediate Wnt5A-stimulated endocytosis of Frizzled 4. Science 301, 1391-1394.
16. Cheyette, B. N., Waxman, J. S., Miller, J. R., Takemaru, K., Sheldahl, L. C., Khlebtsova, N., Fox, E. P., Earnest, T. and Moon, R. T. (2002). Dapper, a Dishevelled-associated antagonist of β-catenin and JNK signaling, is required for notochord formation. Dev. Cell 2, 449-461.
17. Choi, S. C. and Han, J. K. (2005). Rap2 is required for Wnt/β-catenin signaling pathway in Xenopus early development. EMBO J. 24, 985-996.
18. Chung, H. A., Hyodo-Miura, J., Nagamune, T. and Ueno, N. (2005). FGF signal regulates gastrulation cell movements and morphology through its target NRH. Dev. Biol. 282, 95-110.
19. Ciani, L., Krylova, O., Smalley, M. J., Dale, T. C. and Salinas, P. C. (2004). A divergent canonical WNT-signaling pathway regulates microtubule dynamics: dishevelled signals locally to stabilize microtubules. J Cell Biol. 164, 243-253.
20. 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.
21. Cohen, E. D., Mariol, M. C., Wallace, R. M., Weyers, J., Kamberov, Y. G., Pradel, J. and Wilder, E. L. (2002). DWnt4 regulates cell movement and focal adhesion kinase during Drosophila ovarian morphogenesis. Dev. Cell 2, 437-448.
22. Cong, F. and Varmus, H. (2004). Nuclear-cytoplasmic shuttling of Axin regulates subcellular localization of β-catenin. Proc. Natl. Acad. Sci. USA 101, 2882-2887.
23. Cong, F., Schweizer, L. and Varmus, H. (2004a). Casein kinase Iepsilon modulates the signaling specificities of dishevelled. Mol. Cell. Biol. 24, 2000-2011.
24. Cong, E, 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.
25. Cooper, M. T. and Bray, S. J. (1999). Frizzled regulation of Notch signalling polarizes cell fate in the Drosophila eye. Nature 397, 526-530.
26. Couso, J. P., Bishop, S. A. and Martinez Arias, A. (1994). The wingless signalling pathway and the patterning of the wing margin in Drosophila. Development 120, 621-636.
27. De Calisto, J., Araya, C., Marchant, L., Riaz, C. F. and Mayor, R. (2005). Essential role of non-canonical Wnt signalling in neural crest migration. Development 132, 2587-2597.
28. Dominguez, I, Itoh, K. and Sokol, S. Y. (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.
29. Eaton, S., Wepf, R. and Simons, K. (1996). Roles for Rac1 and Cdc42 in planar polarization and hair outgrowth in the wing of Drosophila. J Cell Biol. 135, 1277-1289.
30. Endo, Y., Wolf, V., Muraiso, K., Kamijo, K., Soon, L., Uren, A., Barshishat-Kupper, M. and Rubin, J. S. (2005). Wnt-3a-dependent cell motility involves RhoA activation and is specifically regulated by dishevelled-2. J. Biol. Chem. 280, 777-786.
31. Ewald, A. J., Peyrot, S. M., Tyszka, J. M., Fraser, S. E. and Wallingford, J. B. (2004). Regional requirements for Dishevelled signaling during Xenopus gastrulation: separable effects on blastopore closure, mesendoderm internalization and archenteron formation. Development 131, 6195-6209.
32. Fagotto, F., Jho, E., Zeng, L., Kurth, T., Joos, T., Kaufmann, C. and Costantini, E. (1999). Domains of axin involved in protein-protein interactions, Wnt pathway inhibition, and intracellular localization. J. Cell Biol. 145, 741-756.
33. Fahmy, O. G. and Fahmy, M. (1959). New mutant report. Dros. Inf. Serv. 33, 85.
34. Fan, S., Ramirez, S. H., Garcia, T. M. and Dewhurst, S. (2004). Dishevelled promotes neurite outgrowth in neuronal differentiating neuroblastoma 2A cells, via a DIX-domain dependent pathway. Brain Res. Mol. Brain Res. 132, 38-50.
35. Fanto, M. and Mlodzik, M. (1999). Asymmetric Notch activation specifies photoreceptors R3 and R4 and planar polarity in the Drosophila eye. Nature 397, 523-526.
36. Fanto, M., Weber, U., Strutt, D. I. and Mlodzik, M. (2000). Nuclear signaling by Rac and Rho GTPases is required in the establishment of epithelial planar polarity in the Drosophila eye. Curr Biol. 10, 979-988.
37. Garriock, R. J., D'Agostino, S. L., Pilcher, K. C. and Krieg, P. A. (2005). Wnt11-R, a protein closely related to mammalian Wnt11 is required for heart morphogenesis in Xenopus. Dev. Biol. 279, 179-192.
38. Gho, M. and Schweisguth, F. (1998). Frizzled signalling controls orientation of asymmetric sense organ precursor cell divisions in Drosophila. Nature 393, 178-181.
39. Gloy, J., Hikasa, H. and Sokol, S. Y. (2002). Frodo interacts with Dishevelled to transduce Wnt signals. Nat. Cell. Biol. 4, 351-357.
40. Gong, Y., Mo, C. and Fraser, S. E. (2004). Planar cell polarity signalling controls cell division orientation during zebrafish gastrulation. Nature 430, 689-693.
41. Gonzalez-Sancho, J. M., Brennan, K. R., Castelo-Soccio, L. A. and Brown, A. M. (2004). Wnt proteins induce dishevelled phosphorylation via an LRP5/6-independent mechanism, irrespective of their ability to stabilize β-catenin. Mol. Cell. Biol. 24, 4757-4768.
42. Habas, R. and Dawid, I. B. (2005). Dishevelled and Wnt signaling: is the nucleus the final frontier? J. Biol. 4, 2.
43. Habas, R., Kato, Y. and He, X. (2001). Wnt/Frizzled activation of Rho regulates vertebrate gastrulation and requires a novel Formin homology protein Daam1. Cell 107, 843-854.
44. Habas, R., Dawid, I. B. and He, X. (2003). Coactivation of Rac and Rho by Wnt/Frizzled signaling is required for vertebrate gastrulation. Genes Dev. 17, 295-309.
45. Hamblet, N. S., Lijam, N., Ruiz-Lozano, P., Wang, J., Yang, Y., Chien, K. R., Sussuman, D. J. and Wynshaw-Boris, A. (2002). Dishevelled-2 is essential for cardiac outflow tract development, somite segmentation, and neural tube clsoure. Development 129, 5827-5838.
46. Harland, R. and Gerhart, J. (1997). Formation and function of Spemann's organizer. Annu. Rev. Cell Dev. Biol. 13, 611-667.
47. He, X., Semenov, M., Tamai, K. and Zeng, X. (2004). LDL receptor-related proteins 5 and 6 in Wnt/β-catenin signaling: arrows point the way. Development 131, 1663-1677.
48. Heisenberg, C. P., Tada, M., Rauch, G. J., Saude, L., Concha, M. L., Geisler, R., Stemple, D. L., Smith, J. C. and Wilson, S. W. (2000). Silberblick/Wnt11 mediates convergent extension movements during zebrafish gastrulation. Nature 405, 76-81.
49. Heslip, T. R., Theisen, H., Walker, H. and Marsh, J. L. (1997). Shaggy and dishevelled exert opposite effects on Wingless and Decapentaplegic expression and on positional identity in imaginal discs. Development 124, 1069-1078.
50. Hikasa, H., Shibata, M., Hiratani, I. and Taira, M. (2002). The Xenopus receptor tyrosine kinase Xror2 modulates morphogenetic movements of the axial mesoderm and neuroectoderm via Wnt signaling. Development 129, 5227-5239.
51. Hino, S., Kishida, S., Michiue, T., Fukui, A., Sakamoto, I, Takada, S., Asashima, M. and Kikuchi, A. (2001). Inhibition of the Wnt signaling pathway by Idax, a novel Dvl-binding protein. Mol. Cell. Biol. 21, 330-342.
52. Hobmayer, B., Rentzsch, F., Kuhn, K., Happel, C. M., von Laue, C. C., Snyder, P., Rothbacher, U. and Holstein, T. W. (2000). WNT signalling molecules act in axis formation in the diploblastic metazoan Hydra. Nature 407, 186-189.
53. Hocevar, B. A., Mou, F., Rennolds, J. L., Morris, S. M., Cooper, J. A. and Howe, P. H. (2003). Regulation of the Wnt signaling pathway by disabled-2 (Dab2). EMBO J. 22, 3084-3094.
54. Huang, H. C. and Klein, P. S. (2004). The Frizzled family: receptors for multiple signal transduction pathways. Genome Biol. 5, 234.
55. Inobe, M., Katsube, K., Miyagoe, Y., Nabeshima, Y. and Takeda, S. (1999). Identification of EPS8 as a Dvl1-associated molecule. Biochem. Biophys. Res. Commun. 266,216-221.
56. Itoh, I, Brott, B. K., Bae, G. U., Ratcliffe, M. J. and Sokol, S. (2005). Nuclear localization is required for Dishevelled function in Wnt/β-catenin signalling. J. Biol. 4, 3.
57. Itoh, K. and Sokol, S. Y. (1997). Graded amounts of Xenopus dishevelled specify discrete anteroposterior cell fates in prospective ectoderm. Mech. Dev. 61, 113-125.
58. Itoh, K., Antipova, A., Ratcliffe, M. J. and Sokol, S. (2000). Interaction of dishevelled and Xenopus axin-related protein is required for wnt signal transduction. Mol. Cell. Biol. 20, 2228-2238.
59. Jacobson, A. G. and Gordon, R. (1976). Changes in the shape of the developing vertebrate nervous system analyzed experimentally, mathematically and by computer simulation. J. Exp. Zool. 197, 191-246.
60. Jenny, A., Reynolds-Kenneally, J., Das, G., Burnett, M. and Mlodzik, M. (2005). Diego and Prickle regulate Frizzled planar cell polarity signalling by competing for Dishevelled binding. Nat. Cell. Biol. 7, 691-697.
61. Jessen, J. R., Topczewski, J., Bingham, S., Sepich, D. S., Marlow, F., Chandrasekhar, A. and Solnica-Krezel, L. (2002). Zebrafish trilobite identifies new roles for Strabismus in gastrulation and neuronal movements. Nat. Cell. Biol. 4, 610-615.
62. 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.
63. Kaltschmidt, J. A., Davidson, C. M., Brown, N. H. and Brand, A. H. (2000). Rotation and asymmetry of the mitotic spindle direct asymmetric cell division in the developing central nervous system. Nat. Cell. Biol. 2, 7-12.
64. Keller, R. (2002). Shaping the vertebrate body plan by polarized embryonic cell movements. Science 298, 1950-1954.
65. Keller, R., Shih, J. and Domingo, C. (1992). The patterning and functioning of protrusive activity during convergence and extension of the Xenopus organiser. Dev. Suppl. 81-91.
66. Keys, D. N., Levine, M., Harland, R. M. and Wallingford, J. B. (2002). Control of intercalation is cell-autonomous in the notochord of Ciona intestinalis. Dev. Biol. 246, 329-340.
67. Kim, G. H. and Han, J. K. (2005). JNK and ROKα function in the noncanonical Wnt/RhoA signaling pathway to regulate Xenopus convergent extension movements. Dev. Dyn. 232, 958-968.
68. Kinoshita, N., Iioka, H., Miyakoshi, A. and Ueno, N. (2003). PKC delta is essential for Dishevelled function in a noncanonical Wnt pathway that regulates Xenopus convergent extension movements. Genes Dev. 17, 1663-1676.
69. Kioussi, C., Briata, P., Baek, S. H., Rose, D. W., Hamblet, N. S., Herman, T., Ohgi, K. A., Lin, C., Gleiberman, A., Wang, J. et al. (2002). Identification of a Wnt/Dvl/β-Catenin→Pitx2 pathway mediating cell-type-specific proliferation during development. Cell 111, 673-685.
70. Kirillova, I, Novikova, I, Auge, J., Audollent, S., Esnault, D., Encha-Razavi, R, Lazjuk, G., Attie-Bitach, T. and Vekemans, M. (2000). Expression of the sonic hedgehog gene in human embryos with neural tube defects. Teratology 61, 347-354.
71. 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.
72. Kishida, S., Yamamoto, H. and Kikuchi, A. (2004). Wnt-3a and Dv1 induce neurite retraction by activating Rho-associated kinase. Mol. Cell. Biol. 24, 4487-4501.
73. Klein, T. J. and Mlodzik, M. (2005). Planar cell polarization: an emerging model points in the right direction. Anna. Rev. Cell Dev. Biol. (in press).
74. 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.
75. Klingensmith, J., Yang, Y., Axelrod, J. D., Beier, D. R., Perrimon, N. and Sussman, D. J. (1996). Conservation of dishevelled structure and function between flies and mice: isolation and characterization of Dv12. Mech. Dev. 58, 15-26.
76. Krasnow, R. E., Wong, L. L. and Adler, P. N. (1995). Dishevelled is a component of the frizzled signaling pathway in Drosophila. Development 121, 4095-4102.
77. Krylova, O., Messenger, M. J. and Salinas, P. C. (2000). Dishevelled-1 regulates microtubule stability: a new function mediated by glycogen synthase kinase-30. J. Cell Biol. 151, 83-94.
78. Larabell, C. A., Torres, M., Rowning, B. A., Yost, C., Miller, J. R., Wu, M., Kimelman, D. and Moon, R. T. (1997). Establishment of the dorso-ventral axis in Xenopus embryos is presaged by early asymmetries in β-catenin that are modulated by the Wnt signaling pathway. J Cell Biol. 136, 1123-1136.
79. Lawrence, P. A. (1973). The development of spatial patterns in the integument of insects. In Developmental Systems: Insects (ed. S. J. Counce and C. H. Waddington), pp. 157-206. New York: Academic Press.
80. Lawson, A., Anderson, H. and Schoenwolf, G. C. (2001). Cellular mechanisms of neural fold formation and morphogenesis in the chick embryo. Anat. Rec. 262, 153-168.
81. Lee, J. S., Ishimoto, A. and Yanagawa, S. (1999). Characterization of mouse dishevelled (Dv1) proteins in Wnt/Wingless signaling pathway. J Biol. Chem. 274, 21464-21470.
82. Li, L., Yuan, H., Weaver, C. D., Mao, J., Farr, G. H., 3rd, Sussman, D. J., Jonkers, J., Kimelman, D. and Wu, D. (1999a). Axin and Frat1 interact with dv1 and GSK, bridging Dv1 to GSK in Wnt-mediated regulation of LEE-1. EMBO J. 18, 4233-4240.
83. Li, L., Yuan, H., Xie, W., Mao, J., Caruso, A. M., McMahon, A., Sussman, D. J. and Wu, D. (1999b). Dishevelled proteins lead to two signaling pathways. Regulation of LEF-1 and c-Jun N-terminal kinase in mammalian cells. J. Biol. Chem. 274, 129-134.
84. Li, L., Mao, J., Sun, L., Liu, W. and Wu, D. (2002). Second cysteine-rich domain of Dickkopf-2 activates canonical Wnt signaling pathway via LRP-6 independently of dishevelled. J Biol. Chem. 277, 5977-5981.
85. Lickert, H., Kutsch, S., Kanzler, B., Tamai, Y., Taketo, M. M. and Kemler, R. (2002). Formation of multiple hearts in mice following deletion of catenin in the embryonic endoderm. Dev. Cell 3, 171-181.
86. Lijam, N., Paylor, R., McDonald, M. P., Crawley, J. N., Deng, C. X., Herrup, K., Stevens, K. E., Maccaferri, G., MeBain, C. J., Sussman, D. J. et al. (1997). Social interaction and sensorimotor gating abnormalities in mice lacking Dv11 Cell 90, 895-905.
87. Liu, C., Li, Y., Semenov, M., Han, C., Baeg, G. H., Tan, Y., Zhang, Z., Lin, X. and He, X. (2002). Control of P-catenin phosphorylation/degradation by a dual-kinase mechanism. Cell 108, 837-847.
88. Logan, C. Y. and Nusse, R. (2004). The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 20, 781-810.
89. Long, J. M., LaPorte, P., Paylor, R. and Wynshaw-Boris, A. (2004). Expanded characterization of the social interaction abnormalities in mice lacking Dv11. Genes Brain Behav. 3, 51-62.
90. Lu, B., Usui, T., Uenmra, T., Jan, L. and Jan, Y. N. (1999). Flamingo controls the planar polarity of sensory bristles and asymmetric division of sensory organ precursors in Drosophila. Curr Biol. 9, 1247-1250.
91. Lu, W., Yamamoto, V., Ortega, B. and Baltimore, D. (2004a). Mammalian Ryk is a Wnt coreceptor required for stimulation of neurite outgrowth. Cell 119, 97-108.
92. Lu, X., Borchers, A. G., Jolicoeur, C., Rayburn, H., Baker, J. C. and Tessier-Lavigne, M. (2004b). PTK7/CCK-4 is a novel regulator of planar cell polarity in vertebrates. Nature 430, 93-98.
93. Luo, Z. G., Wang, Q., Zhou, J. Z., Wang, J., Luo, Z., Liu, M., He, X., Wynshaw-Boris, A., Xiong, W. C., Lu, B. et al. (2002). Regulation of AChR clustering by Dishevelled interacting with MuSK and PAK1. Neuron 35, 489-505.
94. Mao, J., Wang, J., Liu, B., Pan, W., Farr, G. H., 3rd, Flynn, C., Yuan, H., Takada, S., Kimelman, D., Li, L. et al. (2001). Low-density lipoprotein receptor-related protein-5 binds to Axin and regulates the canonical Wnt signaling pathway. Mol. Cell 7, 801-809.
95. Marlow, F., Topczewski, J., Sepich, D. and Solnica-Krezel, L. (2002). Zebrafish Rho kinase 2 acts downstream of Wnt11 to mediate cell polarity and effective convergence and extension movements. Curr. Biol. 12, 876-884.
96. Marsden, M. and DeSimone, D. W. (2001). Regulation of cell polarity, radial intercalation and epiboly in Xenopus: novel roles for integrin and fibronectin. Development 128, 3635-3647.
97. Matsui, T., Raya, A., Kawakami, Y., Callol-Massot, C., Capdevila, J., Rodriguez-Esteban, C. and Upisua Belmonte, J. C. (2005). Noncanonical Wnt signaling regulates midline convergence of organ primofdia during zebrafish development. Genes Dev. 19, 164-175.
98. McGrew, L. L., Lai, C. J. and Moon, R. T. (1995). Specification of the anteroposterior neural axis through synergistic interaction of the Wnt signaling cascade with noggin and follistatin. Dev. Biol. 172, 337-342.
99. McGrew, L. L., Hoppler, S. and Moon, R. T. (1997). Wnt and FGF pathways cooperatively pattern anteroposterior neural ectoderm in Xenopus. Mech. Dev. 69, 105-114.
100. Miller, J. R., Hocking, A. M., Brown, J. D. and Moon, R. T. (1999a). Mechanism and function of signal transduction by the Wnt/β-catenin and Wnt/Ca2+ pathways. Oncogene 18, 7860-7872.
101. Miller, J. R., Rowning, B. A., Larabell, C. A., Yang-Snyder, J. A., Bates, R. L. and Moon, R. T. (1999b). 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.
102. Miyakoshi, A., Ueno, N. and Kinoshita, N. (2004). Rho guanine nucleotide exchange factor xNET1 implicated in gastrulation movements during Xenopus development. Differentiation 72, 48-55.
103. Mlodzik, M. (2002). Planar cell polarization: do the same mechanisms regulate Drosophila tissue polarity and vertebrate gastrulation? Trends Genet. 18, 564-571.
104. Moriguchi, T., Kawachi, K., Kamakura, S., Masuyama, 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.
105. Noordermeer, J., Klingensmith, J., Perrimon, N. and Nusse, R. (1994). dishevelled and armadillo act in the wingless signalling pathway in Drosophila. Nature 367, 80-83.
106. Nubler-jung, K., Bonitz, R. and Sonnenschein, M. (1987). Cell polarity during wound healing in an insect epidermis. Development 100, 163-170.
107. Nusslein-Volhard, C. and Wieschaus, E. (1980). Mutations affecting segment number and polarity in Drosophila. Nature 287, 795-801.
108. Olson, E. N. and Schneider, M. D. (2003). Sizing up the heart: development redux in disease. Genes Dev. 17, 1937-1956.
109. Oshita, A., Kishida, S., Kobayashi, H., Michiue, T., Asahara, T., Asashima, M. and Kikuchi, A. (2003). Identification and characterization of a novel Dv1-binding protein that suppresses Wnt signalling pathway. Genes Cells 8, 1005-1017.
110. Ossipova, O., Dhawan, S., Sokol, S. and Green, J. B. (2005). Distinct PAR-1 proteins function in different branches of Wnt signaling during vertebrate development. Dev. Cell 8, 829-84 1.
111. Pan, W. J., Pang, S. Z., Huang, T., Goo, H. Y., Wu, D. and Li, L. (2004). Characterization offunction ofthree domains in dishevelled-1: DEP domain is responsible for membrane translocation of dishevelled-1. Cell Res. 14, 324-330.
112. Pandur, P., Lasche, M., Eisenberg, L. M. and Kuhl, M. (2002). Wnt-11 activation of a non-canonical Wnt signalling pathway is required for cardiogenesis. Nature 418, 636-641.
113. Park, M. and Moon, R. T. (2002). The planar cell-polarity gene stbm regulates cell behaviour and cell fate in vertebrate embryos. Nat. Cell. Biol. 4,20-25.
114. 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.
115. 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.
116. Perrimon, N. and Mahowald, A. P. (1987). Multiple functions of segment polarity genes in Drosophila. Dev. Biol. 119, 587-600.
117. Peters, J. M., McKay, R. M., McKay, J. P, and Graff, J. M. (1999). Casein kinase I transduces Wnt signals. Nature 401, 345-350.
118. Phillips, H. M., Murdoch, J. N., Chaudbry, B., Copp, A. J. and Henderson, D. J. (2005). Vang12 acts via RhoA signaling to regulate polarized cell movements during development of the proximal outflow tract. Circ. Res. 96, 292-299.
119. Pinson, K. L, Brennan, J., Monkley, S., Avery, B. J. and Skarnes, W. C. (2000). An LDL-receptor-related protein mediates Wnt signalling in mice. Nature 407, 535-538.
120. Pizzuti, A., Amati, E, Calabrese, G., Mari, A., Colosimo, A., Sihmi, V., Giardino, L., Ratti, A., Penso, D., Calza, L. et al. (1996). cDNA characterization and chromosomal mapping of two human homologues of the Drosophila dishevelled polarity gene. Hum. Mol. Genet. 5, 953-958.
121. Ratcliffe, M. J., Itoh, K. and Sokol, S. Y. (2000). A positive role for the PP2A catalytic subunit in Wnt signal transduction. J Biol. Chem. 275, 35680-35683.
122. Riggleman, B., Schedl, P. and Wieschaus, E. (1990). Spatial expression of the Drosophila segment polarity gene armadillo is posttranscriptionally regulated by wingless. Cell 63, 549-560.
123. Rosso, S. B., Sussman, D., Wynshaw-Boris, A. and Salinas, P. C. (2005). Wnt signaling through Dishevelled, Rae and JNK regulates dendritic development. Nat. Neurosci. 8, 34-42.
124. Rothbächer, U., Laurent, M. N., Blitz, I. L., Watabe, T., Marsh, J. L. and Cho, K. W. (1995). Functional conservation of the Wnt signaling pathway revealed by ectopic expression of Drosophila dishevelled in Xenopus. Dev. Biol. 170, 717-721.
125. Rothbächer, U., Laurent, M. N., Deardorff, M. A., Klein, P. S., Cho, K. W. Y. and Fraser, S. E. (2000). Dishevelled phosphorylation, subcellular localization and homornerization regulate its role in early embryogenesis. EMBO J 19, 1010-1022.
126. Rousset, R., Mack, J. A., Wharton, K. A., Jr, Axelrod, J. D., Cadigan, K. M., Fish, M. P., Nusse, R. and Scott, M. P. (2001). Naked cuticle targets dishevelled to antagonize Writ signal transduction. Genes Dev. 15, 658-671.
127. Sagot, L, Rodal, A. A., Moseley, J., Goode, B. L. and Pellman, D. (2002). An actin nucleation mechanism mediated by Bni1 and profilin. Nat. Cell. Biol. 4, 626-631.
128. Sakanaka, C., Leong, P., Xu, L., Harrison, S. D. and Williams, L. T. (1999). Casein kinase iepsilon in the writ pathway: regulation of β-catenin function.Proc. Natl. Acad. Sci. USA 96, 12548-12552.
129. Saraga-Babic, M., Sapunar, D. and Stefanovic, V. (1993). Histological features of axial structures during embryonic and fetal stages of human craniorachischisis. Acta Neuropathol. (Berl.) 86, 289-294.
130. Sasai, N., Nakazawa, Y., Haraguchi, T. and Sasai, Y. (2004). The neurotrophin-receptor-related protein NRH1 is essential for convergent extension movements. Nat. Cell. Biol. 6, 741-748.
131. Schlesinger, A., Shelton, C. A., Maloof, J. N., Meneghini, M. and Bowerman, B. (1999). Wnt pathway components orient a mitotic spindle in the early Caenorhabditis elegans embryo without requiring gene transcription in the responding cell. Genes Dev. 13, 2028-2038.
132. Schulte, G., Bryja, V., Rawal, N., Castelo-Branco, G., Sousa, K. M. and Arenas, E. (2005). Purified Wnt-5a increases differentiation of midbrain doparninergic cells and dishevelled phosphorylation. J. Neurochem. 92, 1550-1553.
133. Schweizer, L. and Varmus, H. (2003). Wnt/Wingless signaling through β-catenin requires the function of both LRP/Arrow and frizzled classes of receptors. BMC Cell Biol. 4, 4.
134. Semenov, M. V. and Snyder, M. (1997). Human dishevelled genes constitute a DHR-containing multigene family. Genomics 42, 302-3 10.
135. Seto, E. S. and Bellen, H. J. (2004). The ins and outs of Wingless signaling. Trends Cell. Biol. 14, 45-53.
136. Sheldahl, L. C., Park, M., Malbon, C. C. and Moon, R. T. (1999). Protein kinase C is differentially stimulated by Writ and Frizzled homologs in a G-protein-dependent manner. Curr. Biol. 9, 695-698.
137. Sheldahl, L. C., Slusarski, D. C., Pandur, F., Miller, J. R., Kuhl, M. and Moon, R. T. (2003). Dishevelled activates Ca2+ flux, PKC, and CamKII in vertebrate embryos. J. Cell Biol. 161, 769-777.
138. Siegfried, E., Wilder, E. L. and Perrimon, N. (1994). Components of wingless signalling in Drosophila. Nature 367, 76-80.
139. Simons, M., Gloy, J., Ganner, A., Bullerkotte, A., Bashkurov, M., Kronig, C., Schermer, B., Benzing, T., Cabello, O. A., Jenny, A. et al. (2005). Inversin, the gene product mutated in nephronophthisis type II, functions as a molecular switch between Wnt signaling pathways. Nat. Genet. 37, 537-543.
140. 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 Dv1-2 proteins regulates Dv1-2-stimulated TCF-dependent transcription. EMBO J. 18, 2823-2835.
141. Sokol, S. Y. (1996). Analysis of Dishevelled signalling pathways during Xenopus development. Curr Biol. 6, 1456-1467.
142. Sokol, S. Y., Klingensmith, J., Perrimon, N. and Itoh, K. (1995). Dorsalizing and neuralizing properties of Xdsh, a maternally expressed Xenopus homolog of dishevelled. Development 121, 1637-1647.
143. Solnica-Krezel, L. (2005). Conserved patterns of cell movements during vertebrate gastrulation. Curr. Biol. 15, R213-R228.
144. Steitz, S. A., Tsang, M. and Sussman, D. J. (1996). Wnt-mediated relocalization of dishevelled proteins. In Vitro Cell. Dev. Biol. Anim. 32,441-445.
145. Strigini, M. and Cohen, S. M. (2000). Wingless gradient formation in the Drosophila wing. Carr Biol. 10, 293-300.
146. Strovel, E. T., Wu, D. and Sussman, D. J. (2000). Protein phosphatase 2Cα dephosphorylates axin and activates LEF-1-dependent transcription. J. Biol. Chem. 275, 2399-2403.
147. Strutt, D. L, Weber, U. and Mlodzik, M. (1997). The role of RhoA in tissue polarity and Frizzled signalling. Nature 387, 292-295.
148. Strutt, D., Johnson, R., Cooper, K. and Bray, S. (2002). Asymmetric localization of frizzled and the determination of notch-dependent cell fate in the Drosophila eye. Curr Biol. 12, 813-824.
149. Sulik, K., Dehart, D. B., langaki, T., Carson, J. L., Vrablic, T., Gesteland, K. and Schoenwolf, G. C. (1994). Morphogenesis of the murine node and notochordal plate. Dev. Dyn. 201, 260-278.
150. Sun, T. Q., Lu, B., Feng, J. J., Reinhard, C., Jan, Y. N., Fantl, W. J. and Williams, L. T. (2001). PAR-I is a Dishevelled-associated kinase and a positive regulator of Wnt signalling. Nat. Cell. Biol. 3, 628-636.
151. Sussman, D. J., Klingensmith, J., Salinas, P., Adams, P. S., Nusse, R. and Perrimon, N. (1994). Isolation and characterization of a mouse homolog of the Drosophila segment polarity gene dishevelled. Dev. Biol. 166, 73-86.
152. Tada, M. and Smith, J. C. (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.
153. Tahinci, E. and Symes, YL (2003). Distinct functions of Rho and Rae are required for convergent extension during Xenopus gastrulation. Dev. Biol. 259, 318-335.
154. Tamai, K., Semenov, M., Kato, Y., Spokony, R., Liu, C., Katsuyama, Y., Hess, R, Saint-jeannet, J. P. and He, X. (2000). LDL-receptor-related proteins in Writ signal transduction. Nature 407, 530-535.
155. Tanaka, M., Kamo, T., Ota, S. and Sugimura, H. (2003). Association of Dishevelled with Eph tyrosine kinase receptor and ephrin mediates cell repulsion. EMBO J. 22, 847-858.
156. Tao, Q., Yokota, C., Puck, H., Kofron, M., Birsoy, B., Yan, D., Asashima,M., Wylie, C. C., Lin, X. and Heasman, J. (2005). Maternal wnt11 activates the canonical wnt signaling pathway required for axis formation in Xenopus embryos. Cell 120, 857-871.
157. 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.
158. Tolwinski, N. S. and Wieschaus, E. (2004). Rethinking WNT signaling. Trends Genet. 20, 177-181.
159. Tolwinski, N. S., Wehrli, M., Fives, A., Erdeniz, N., DiNardo, S. and Wieschaus, E. (2003). Wg/Wnt signal can be transmitted through arrow/LRP5,6 and Axin independently of Zw3/Gsk3β activity. Dev. Cell 4, 407-418.
160. Topczewski, J., Sepich, D. S., Myers, D. C., Walker, C., Amores, A., Lele, Z., Hammerschmidt, M., Postlethwait, J. and Solnica-Krezel, L. (2001). The zebratish glypican knypek controls cell polarity during gastrulation movements of convergent extension. Dev. Cell 1, 251-264.
161. 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.
162. Torres, M. A., Yang-Snyder, J. A., Purcell, S. M., DeMarais, A. A., McGrew, L. L. and Moon, R. T. (1996). Activities of the,Wnt-1 class of secreted signaling factors are antagonized by the Wnt-5A 'class and by a dominant negative cadherin in early Xenopus development. J Cell Biol. 133, 1123-1137.
163. Tree, D. R., Shulman, J. M., Rousset, R., Scott, M. P., Gubb, D. and Axelrod, J. D. (2002). Prickle mediates feedback amplification to generate asymmetric planar cell polarity signaling. Cell 109, 371-381.
164. Tsang, M., Lijam, N., Yang, Y., Beier, D. R., Wynshaw-Boris, A. and Sussman, D. J. (1996). Isolation and characterization of mouse dishevelled- 3. Dev. Dyn. 207, 253-262.
165. Tzahor, E. and Lassar, A. B. (2001). Wnt signals from the neural tube block ectopic cardiogenesis. Genes Dev. 15, 255-260.
166. Umbhauer, M., Djiane, A., Goisset, C., Penzo-Mendez, A., Rion, J. F., Boucaut, J. C. and Shi, 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.
167. van Noort, M., Meeldijk, J., van der Zee, R-, Destree, O. and Clevers, H. (2002). Writ signaling controls the phosphorylation status of β-catenin. J Biol. Chem. 277,17901-17905.
168. Van Straaten, H. W., Janssen, H. C., Peeters, M. C., Copp, A. J. and Hekking, J. W. (1996). Neural tube closure in the chick embryo is multiphasic. Dev. Dyn. 207, 309-318.
169. Veeman, M. T., Axelrod, J. D. and Moon, R. T. (2003). A second canon. Functions and mechanisms of β-catenin-independent Wnt signaling. Dev. Cell 5, 367-377.
170. Vinson, C. R. and Adler, P. N. (1987). Directional non-cell autonomy and the transmission of polarity information by the frizzled gene of Drosophila. Nature 329, 549-551.
171. Wakefield, J. G., Stephens, D. J. and Tavare, J. M. (2003). A role for glycogen synthase kinase-3 in mitotic spindle dynamics and chromosome alignment. J. Cell Sci. 116, 637-646.
172. Wallingford, J. B. and Harland, R. M. (2001). Xenopus Dishevelled signaling regulates both neural and mesodermal convergent extension: parallel forces elongating the body axis. Development 128, 2581-2592.
173. Wallingford, J. B. and Harland, R. M. (2002). Neural tube closure requires Dishevelled-dependent convergent extension of the midline. Development 129, 5815-5825.
174. Wallingford, J. B., Rowning, B. A., Vogeli, K. M., Rothbacher, U., Fraser, S. E. and Harland, R.M. (2000). Dishevelled controls cell polarity during Xenopus gastrulation. Nature 405, 81-85.
175. Wallingford, J. B., Fraser, S. E. and Harland, R. M. (2002). Convergent extension: the molecular control of polarized cell movement during embryonic development. Dev. Cell 2, 695-706.
176. 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.
177. Watanabe, N. and Higashida, C. (2004). Formins: processive cappers of growing actin filaments. Exp. Cell Res. 301, 16-22.
178. Wechezak, A. R. and Coan, D. E. (2005). Dvl2 silencing in postdevelopmental cells results in aberrant cell membrane activity and actin disorganization. J. Cell Physiol. 202, 867-873.
179. Wehrli, M., Dougan, S. T., Caldwell, K., O'Keefe, L., Schwartz, S., Vaizel-Ohayon, D., Schejter, E., Tomlinson, A. and DiNardo, S. (2000). arrow encodes an LDL-receptor-related protein essential for Wingless signalling. Nature 407, 527-530.
180. Weitzel, H. E., Illies, M. R., Byrum, C. A., Xu, R., Wikramanayake, A. H. and Ettensolm, C. A. (2004). Differential stability of β-catenin along the animal-vegetal axis of the sea urchin embryo mediated by dishevelled. Development 131, 2947-2956.
181. Wharton, K. A., Jr (2003). Runnin' with the Dv1: proteins that associate with Dsh/Dv1 and their significance to Wnt signal transduction. Dev. Biol. 253, 1-17.
182. Wharton, K. A., Jr, Zimmermann, G., Rousset, R. and Scott, M. P. (2001). Vertebrate proteins related to Drosophila Naked Cuticle bind Dishevelled and antagonize Wnt signaling. Dev. Biol. 234, 93-106.
183. Wiggan, O. and Hamel, P. A. (2002). Pax3 regulates morphogenetic cell behavior in vitro coincident with activation of a PCP/non-canonical Wnt-signaling cascade. J. Cell Sci. 115, 531-541.
184. Wigglesworth, V. B. (1940). Local and general factors in the development of "pattern" in Rhodnius prolixus (Herniptera). J Exp. Biol. 17, 180-200.
185. Wigglesworth, V. B. (1959). The Control of Growth and Form. Ithaca, NY: Cornell University Press.
186. Willert, K., Brink, M., Wodarz, A., Varmus, H. and Nusse, R. (1997). Casein kinase 2 associates with and phosphorylates dishevelled. EMBO J. 16, 3089-3096.
187. Winklbauer, R., Medina, A., Swain, R. K. and Steinbeisser, H. (2001). Frizzled-7 signalling controls tissue separation during Xenopus gastrulation. Nature 413, 856-860.
188. Winter, C. G., Wang, B., Ballew, A., Royou, A., Karess, R., Axelrod, J. D. and Luo, L. (2001). Drosophila Rho-associated kinase (Drok) links Frizzled-mediated planar cell polarity signaling to the actin cytoskeleton. Cell 105, 81-9 1.
189. Wolff, T. and Rubin, G. M. (1998). Strabismus, a novel gene that regulates tissue polarity and cell fate decisions in Drosophila. Development 125, 1149-1159.
190. Wong, H. C., Mao, J., Nguyen, J. T., Srinivas, S., Zhang, W., Liu, B., Li, 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.
191. Wong, H. C., Bourdelas, A., Krauss, A., Lee, H. J., Shao, 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.
192. Wong, L. L. and Adler, P. N. (1993). Tissue polarity genes of Drosophila regulate the subcellular location for prehair initiation in pupal wing cells. J. Cell Biol. 123, 209-221.
193. Wu, J., Klein, T. J. and Mlodzik, M. (2004). Subcellular localization of frizzled receptors, mediated by their cytoplasmic tails, regulates signaling pathway specificity. PLoS Biol. 2, E158.
194. Yamanaka, H., Moriguchi, T., Masuyama, N., Kusakabe, M., Hanafusa, H., Takada, R., Takada, S. and Nishida, E. (2002). INK functions in the non-canonical Wnt pathway to regulate convergent extension movements in vertebrates. EMBO Rep. 3, 69-75.
195. Yanagawa, S., van Leeuwen, F., Wodarz, A., Klingensmith, J. and Nusse, P. (1995). The dishevelled protein is modified by wingless signaling in Drosophila. Genes Dev. 9, 1087-1097.
196. Yanagawa, S., Matsuda, Y., Lee, J. S., Matsubayashi, H., Sese, S., Kadowaki, T. and Ishimoto, A. (2002). Casein kinase I phosphorylates the Armadillo protein and induces its degradation in Drosophila. EMBO J. 21, 1733-1742.
197. Yang, J., Wu, J., Tan, C. and Klein, P. S. (2003). PP2A:B56epsilon is required for Wnt/β-catenin signaling during embryonic development. Development 130, 5569-5578.
198. 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.
199. Yost, C., Torres, M., Miller, J. R, Huang, E., Kimelman, D. and Moon, R. T. (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.
200. Yost, C., Farr, G. H., 3rd, Pierce, S. B., Ferkey, D. M., Chen, M. M. and Kimelman, D. (1998). GBP, an inhibitor of GSK-3, is implicated in Xenopus development and oncogenesis. Cell 93, 1031-1041.
201. 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.
202. Zheng, L., Zhang, J. and Carthew, R. W. (1995). frizzled regulates mirror-symmetric pattern formation in the Drosophila eye. Development 121, 3045-3055.