Mechanisms of Wnt signaling in development

Annual Review of Cell and Developmental Biology

Volumn 14, Issue , 1998, Pages 59-88

  Wodarz, Andreas ^a   Nusse, Roel ^b  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b STANFORD UNIVERSITY   (United States)

Author keywords

Catenin; Frizzled; Signal transduction; Wingless; Wnt

Indexed keywords

BETA CATENIN; CASEIN KINASE I; PROTEOGLYCAN;

CAENORHABDITIS ELEGANS; DROSOPHILA; GENE DUPLICATION; GENE TARGETING; GENETIC ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; TISSUE CULTURE; TRANSCRIPTION REGULATION;

ANIMALS; BODY PATTERNING; CAENORHABDITIS ELEGANS; DROSOPHILA; EMBRYO, NONMAMMALIAN; EMBRYONIC AND FETAL DEVELOPMENT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; MICE; MICE, KNOCKOUT; MORPHOGENESIS; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS; WNT PROTEINS; ZEBRAFISH PROTEINS;

CAENORHABDITIS ELEGANS;

EID: 0032406715     PISSN: 10810706     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.cellbio.14.1.59     Document Type: Review

References (142)

1. Aberle H, Bauer A, Stappert J, Kispert A, Kemler R. 1997. beta-Catenin is a target for the ubiquitin-proteasome pathway. EMBO J. 16:3797-804
2. Adler PN. 1992. The genetic control of tissue polarity in Drosophila. BioEssays 14:735-41
3. Adler PN, Krasnow RE, Liu J. 1997. Tissue polarity points from cells that have higher Frizzled levels towards cells that have lower Frizzled levels. Curr. Biol. 7:940-49
4. Alcedo J, Ayzenzon M, Von Ohlen T, Noll M, Hooper JE. 1996. The Drosophila smoothened gene encodes a seven-pass membrane protein, a putative receptor for the hedgehog signal. Cell 86:221-32
5. Axelrod JD, Matsuno K, Artavanis-Tsakonas S, Perrimon N. 1996. Interaction between Wingless and Notch signaling pathways mediated by dishevelled. Science 271:1826-32
6. Barth AI, Näthke IS, Nelson WJ. 1997. Cadherins, catenins and APC protein: interplay between cytoskeletal complexes and signaling pathways. Curr. Opin. Cell Biol. 9:683-90
7. Baylies MK, Martinez-Arias A, Bate M. 1995. wingless is required for the formation of a subset of muscle founder cells during Drosophila embryogenesis. Development 121:3829-37
8. Behrens J, von Kries J, Kühl M, Bruhn L, Wedlich D, et al. 1996. Functional interaction of beta-catenin with the transcription factor LEF-1. Nature 382:638-42
9. Bejsovec A, Wieschaus E. 1995. Signaling activities of the Drosophila wingless gene are separately mutable and appear to be transduced at the cell surface. Genetics 139:309-20
10. Bhanot P, Brink M, Harryman Samos C, Hsieh JC, Wang Y, et al. 1996. A new member of the frizzled family from Drosophila functions as a Wingless receptor. Nature 382:225-30
11. Binari RC, Staveley BE, Johnson WA, Godavarti R, Sasisekharan R, Manoukian AS. 1997. Genetic evidence that heparin-like glycosaminoglycans are involved in wingless signaling. Development 124:2623-32
12. Bradley RS, Brown AM. 1990. The protooncogene int-1 encodes a secreted protein associated with the extracellular matrix. EMBO J. 9:1569-75
13. Brannon M, Gomperts M, Sumoy L, Moon RT, Kimelman D. 1997. A beta-catenin/XTcf-3 complex binds to the siamois promoter to regulate dorsal axis specification in Xenopus. Genes Dev. 11:2359-70
14. Brunner E, Peter O, Schweizer L, Basler K. 1997. pangolin encodes a Lef-1 homologue that acts downstream of Armadillo to transduce the Wingless signal in Drosophila. Nature 385:829-33
15. Cabrera CV, Alonso MC, Johnston P, Phillips RG, Lawrence PA. 1987. Phenocopies induced with antisense RNA identify the wingless gene. Cell 50:659-63
16. Cadigan KM, Nusse R. 1996. wingless signaling in the Drosophila eye and embryonic epidermis. Development 122:2801-12
17. Cadigan K, Fish M, Rulifson E, Nusse R. 1998. Wingless repression of Drosophila frizzled2 expression shapes the wingless morphogen gradient in the wing. Cell. In press
18. Cadigan KM, Nusse R. 1997. Wnt signaling: a common theme in animal development. Genes Dev. 11:3286-305
19. Cavallo R, Rubenstein D, Peifer M. 1997. Armadillo and dTCF: a marriage made in the nucleus. Curr. Opin. Genet. Dev. 7:459-66
20. Chen Y, Struhl G. 1996. Dual roles for patched in sequestering and transducing Hedgehog. Cell 87:553-63
21. Christian JL, Moon RT. 1993. Interactions between Xwnt-8 and Spemann organizer signaling pathways generate dorsoventral pattern in the embryonic mesoderm of Xenopus. Genes Dev. 7:13-28
22. Cook D, Fry MJ, Hughes K, Sumathipala R, Woodgett JR, Dale TC. 1996. Wingless inactivates glycogen synthase kinase-3 via an intracellular signalling pathway which involves a protein kinase C. EMBO J. 15:4526-36
23. Couso JP, Bishop SA, Martinez-Arias A. 1994. The wingless signalling pathway and the patterning of the wing margin in Drosophila. Development 120:621-36
24. Couso JP, Martinez-Arias A. 1994. Notch is required for wingless signaling in the epidermis of Drosophila. Cell 79:259-72
25. Dominguez I, Itoh K, Sokol SY. 1995. Role of glycogen synthase kinase 3 beta as a negative regulator of dorsoventral axis formation in Xenopus embryos. Proc. Natl. Acad. Sci. USA 92:8498-502
26. Doyle DA, Lee A, Lewis J, Kim E, Sheng M, MacKinnon R. 1996. Crystal structures of a complexed and peptide-free membrane protein-binding domain: molecular basis of peptide recognition by PDZ. Cell 85:1067-76
27. Du SJ, Purcell SM, Christian JL, McGrew LL, Moon RT. 1995. Identification of distinct classes and functional domains of Wnts through expression of wild-type and chimeric proteins in Xenopus embryos. Mol. Cell. Biol. 15:2625-34
28. Finch PW, He X, Kelley MJ, Uren A, Schaudies RP, et al. 1997. Purification and molecular cloning of a secreted, Frizzled-related antagonist of Wnt action. Proc. Natl. Acad. Sci. USA 94:6770-75
29. Funayama N, Fagotto F, McCrea P, Gumbiner BM. 1995. Embryonic axis induction by the armadillo repeat domain of beta-catenin: evidence for intracellular signaling. J. Cell Biol. 128:959-68
30. Goode N, Hughes K, Woodgett JR, Parker PJ. 1992. Differential regulation of glycogen synthase kinase-3 beta by protein kinase C isotypes. J. Biol. Chem. 267:16878-82
31. Guger KA, Gumbiner BM. 1995. beta-Catenin has Wnt-like activity and mimics the Nieuwkoop signaling center in Xenopus dorsal-ventral patterning. Dev. Biol. 172:115-25
32. Häcker U, Lin X, Perrimon N. 1997. The Drosophila sugarless gene modulates Wingless signaling and encodes an enzyme involved in polysaccharide biosynthesis. Development 124:3565-73
33. Haerry TE, Heslip TR, Marsh JL, O'Connor MB. 1997. Defects in glucuronate biosynthesis disrupt Wingless signaling in Drosophila, Development 124:3055-64
34. Han M. 1997. Gut reaction to Wnt signaling in worms. Cell 90:581-84
35. Hayashi S, Rubinfeld B, Souza B, Polakis P, Wieschaus E, Levine AJ. 1997. A Drosophila homolog of the tumor suppressor gene adenomatous polyposis coli down-regulates beta-catenin but its zygotic expression is not essential for the regulation of Armadillo. Proc. Natl. Acad. Sci. USA 94:242-47
36. Hays R, Gibori GB, Bejsovec A. 1997. Wingless signaling generates pattern through two distinct mechanisms. Development 124:3727-36
37. He X, Saint JJ, Wang Y, Nathans J, Dawid I, Varmus H. 1997. A member of the Frizzled protein family mediating axis induction by Wnt-5A. Science 275:1652-54
38. He X, Saint JJ, Woodgett JR, Varmus HE, Dawid IB. 1995. Glycogen synthase kinase-3 and dorsoventral patterning in Xenopus embryos. Nature 374:617-22
39. Heasman J, Crawford A, Goldstone K, Garner HP, Gumbiner BM, et al. 1994. Overexpression of cadherins and underexpression of beta-catenin inhibit dorsal mesoderm induction in early Xenopus embryos. Cell 79:791-803
40. Herman MA, Vassilieva LL, Horvitz HR, Shaw JE, Herman RK. 1995. The C. elegans gene lin-44, which controls the polarity of certain asymmetric cell divisions, encodes a Wnt protein and acts cell nonautonomously. Cell 83:101-10
41. Hinck L, Nelson WJ, Papkoff J. 1994. Wm-1 modulates cell-cell adhesion in mammalian cells by stabilizing beta-catenin binding to the cell adhesion protein cadherin. J. Cell Biol. 124:729-41
42. Hing HK, Sun X, Artavanis-Tsakonas S. 1994. Modulation of wingless signaling by Notch in Drosophila. Mech. Dev. 47:261-68
43. Hoang B, Moos MJ, Vukicevic S, Luyten FP. 1996. Primary structure and tissue distribution of FRZB, a novel protein related to Drosophila frizzled, suggest a role in skeletal morphogenesis. J. Biol. Chem. 271:26131-37
44. Hoppler S, Brown JD, Moon RT. 1996. Expression of a dominant-negative Wnt blocks induction of MyoD in Xenopus embryos. Genes Dev. 10:2805-17
45. Huber O, Korn R, McLaughlin J, Ohsugi M, Herrmann BG, Kemler R. 1996. Nuclear localization of beta-catenin by interaction with transcription factor LEF-1. Mech. Dev. 59:3-10
46. Ikeda S, Kishida S, Yamamoto H, Murai H, Koyama S, Kikuchi A. 1998. Axin, a negative regulator of the Wnt signaling pathway, forms a complex with GSK-3beta and beta-catenin and promotes GSK-3beta-dependent phosphorylation of beta-catenin. EMBO J 17:1371-84
47. Itoh K, Sokol SY. 1994. Heparan sulfate proteoglycans are required for mesoderm formation in Xenopus embryos. Development 120:2703-11
48. Jiang J, Struhl G. 1998. Regulation of the Hedgehog and Wingless signalling pathways by the F-box/WD40-repeat protein Slimb Nature 391:493-96
49. Jones KH, Liu J, Adler PN. 1996. Molecular analysis of EMS-induced frizzled mutations in Drosophila melanogaster. Genetics 142:205-15
50. Jue SF, Bradley RS, Rudnicki JA, Varmus HE, Brown AM. 1992. The mouse Wnt-J gene can act via a paracrine mechanism in transformation of mammary epithelial cells. Mol. Cell. Biol. 12:321-8
51. Kadowaki T, Wilder E, Klingensmith J, Zachary K, Perrimon N. 1996. The segment polarity gene porcupine encodes a putative multi-transmembrane protein involved in Wingless processing. Genes Dev. 10:3116-28
52. Kitajewski J, Mason JO, Varmus HE. 1992. Interaction of Wnt-1 proteins with the binding protein BiP. Mol. Cell. Biol. 12:784-90
53. Klingensmith J, Nusse R. 1994. Signaling by wingless in Drosophila. Dev. Biol. 166:396-414
54. Klingensmith J, Nusse R, Perrimon N. 1994. The Drosophila segment polarity gene dishevelled encodes a novel protein required for response to the wingless signal. Genes Dev. 8:118-30
55. Korinek V, Barker N, Morin PJ, van Wichen D, de Weger R, et al. 1997. Constitutive transcriptional activation by a beta-catenin-Tcf complex in APC-/- colon carcinoma. Science 275:1784-87
56. Krasnow RE, Wong LL, Adler PN. 1995. Dishevelled is a component of the frizzled signaling pathway in Drosophila. Development 121:4095-102
57. Larabell CA, Torres M, Rowning BA, Yost C, Miller JR, et al. 1997. Establishment of the dorso-ventral axis in Xenopus embryos is presaged by early asymmetries in beta-catenin that are modulated by the Wnt signaling pathway. J. Cell Biol. 136:1123-36
58. Leyns L, Bouwmeester T, Kim SH, Piccolo S, De Robertis E. 1997. Frzb-1 is a secreted antagonist of Wnt signaling expressed in the Spemann organizer. Cell 88:747-56
59. Lijam N, Paylor R, McDonald MP, Crawley JN, Deng CX, et al. 1997. Social interaction and sensorimotor gating abnormalities in mice lacking Dv11. Cell 90:895-905
60. Lin K, Wang S, Julius MA, Kitajewski J, Moos MJ, Luyten FP. 1997. The cysteine-rich frizzled domain of Frzb-1 is required and sufficient for modulation of Wnt signaling. Proc. Natl. Acad. Sci. USA 94:11196-200
61. Lin R, Thompson S, Priess JR. 1995. pop-1 encodes an HMG box protein required for the specification of a mesoderm precursor in early C. elegans embryos. Cell 83:599-609
62. Marigo V, Davey RA, Zuo Y, Cunningham JM, Tabin CJ. 1996. Biochemical evidence that patched is the Hedgehog receptor. Nature 384:176-79
63. Mayr T, Deutsch U, Kuhl M, Drexler HC, Lottspeich F, et al. 1997. Fritz: a secreted frizzled-related protein that inhibits Wnt activity. Mech. Dev. 63:109-25
64. McMahon AP, Bradley A. 1990. The Wnt-1 (int-1) proto-oncogene is required for development of a large region of the mouse brain. Cell 62:1073-85
65. McMahon AP, Moon RT. 1989. Ectopic expression of the proto-oncogene int-1 in Xenopus embryos leads to duplication of the embryonic axis. Cell 58:1075-84
66. Miller JR, Moon RT. 1997. Analysis of the signaling activities of localization mutants of beta-catenin during axis specification in Xenopus. J. Cell Biol. 139:229-43
67. Molenaar M, van de Wetering M, Oosterwegel M, Petersen-Maduro J, Godsave S, et al. 1996. XTcf-3 transcription factor mediates beta-catenin-induced axis formation in Xenopus embryos. Cell 86:391-99
68. Moon RT, Brown JD, Torres M. 1997a. WNTs modulate cell fate and behavior during vertebrate development. Trends Genet. 13:157-62
69. Moon RT, Brown JD, Yang-Snyder J, Miller JR. 1997b. Structurally related receptors and antagonists compete for secreted Wnt ligands. Cell 88:725-28
70. Moon RT, Campbell RM, Christian JL, McGrew LL, Shih J, Fraser S. 1993. Xwnt-5A: a maternal Wnt that affects morphogenetic movements after overexpression in embryos of Xentipus laevis. Development 119:97-111
71. Morin PJ, Sparks AB, Korinek V, Barker N, Clevers H, et al. 1997. Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC. Science 275:1787-90
72. Munemitsu S, Albert I, Rubinfeld B, Polakis P. 1996. Deletion of an amino-terminal sequence stabilizes beta-catenin in vivo and promotes hyperphosphorylation of the adenomatous polyposis coli tumor suppressor protein. Mol. Cell. Biol. 16:4088-94
73. Munemitsu S, Albert I, Souza B, Rubinfeld B, Polakis P. 1995. Regulation of intracellular beta-catenin levels by the adenomatous polyposis coli (APC) tumor-suppressor protein. Proc. Natl. Acad. Sci. USA 92:3046-50
74. Neumann CJ, Cohen SM. 1997. Long-range action of Wingless organizes the dorsal-ventral axis of the Drosophila wing. Development 124:871-80
75. Noordermeer J, Johnston P, Rijsewijk F, Nusse R, Lawrence PA. 1992 The consequences of ubiquitous expression of the wingless gene in the Drosophila embryo. Development 116:711-19
76. Noordermeer J, Klingensmith J, Perrimon N, Nusse R, 1994. Dishevelled and armadillo act in the wingless signalling pathway in Drosophila. Nature 367:80-83
77. Nusse R. 1997. A versatile transcriptional effector of Wingless signaling. Cell 89:321-23
78. Nusse R, Harryman Samos C, Brink M, Willert K, Cadigan KM, et al. 1997. Cell culture and whole animal approaches to understanding signaling by Wnt proteins in Drosophila. Cold Spring Harbor Symp. Quant. Biol. LXII:185-90
79. Nusse R, Varmus HE. 1982. Many tumors induced by the mouse mammary tumor virus contain a provirus integrated in the same region of the host genome. Cell 31:99-109
80. Nusse R, Varmus HE. 1992. Wnt genes. Cell 69:1073-87
81. Nüsslein-Volhard C, Wieschaus E. 1980. Mutations affecting segment number and polarity in Drosophila. Nature 287:795-801
82. Orsulic S, Peifer M. 1996. An in vivo structure-function study of Armadillo, the beta-catenin homologue, reveals both separate and overlapping regions of the protein required for cell adhesion and for Wingless signaling. J. Cell Biol. 134:1283-300
83. Pai LM, Orsulic S, Bejsovec A, Peifer M. 1997. Negative regulation of Armadillo, a Wingless effector in Drosophila. Development 124:2255-66
84. Papkoff J, Rubinfeld B, Schryver B, Polakis P. 1996. Wnt-1 regulates free pools of catenins and stabilizes APC-catenin complexes. Mol. Cell. Biol. 16:2128-34
85. Parr BA, McMahon AP. 1994. Wnt genes and vertebrate development. Curr. Opin. Genet. Dev. 4:523-28
86. Peifer M, Sweeton D, Casey M, Wieschaus E. 1994. Wingless signal and Zeste-white 3 kinase trigger opposing changes in the intracellular distribution of Armadillo. Development 120:369-80
87. Perrimon N. 1994. The genetic basis of patterned baldness in Drosophila. Cell 76:781-84
88. Ponting CP, Bork P. 1996. Pleckstrin's repeat performance: a novel domain in G-protein signaling? Trends Biochem. Sci. 21:245-46
89. Rattner A, Hsieh JC, Smallwood PM, Gilbert DJ, Copeland NG, et al. 1997. A family of secreted proteins contains homology to the cysteine-rich ligand-binding domain of frizzled receptors. Proc. Natl. Acad. Sci. USA 94:2859-63
90. Reichsman F, Smith L, Cumberledge S. 1996. Glycosaminoglycans can modulate extracellular localization of the wingless protein and promote signal transduction. J. Cell Biol. 135:819-27
91. Riese J, Yu X, Munnerlyn A, Eresh S, Hsu SC, et al. 1997. LEF-1, a nuclear factor coordinating signaling inputs from wingless and decapentaplegic. Cell 88:777-87
92. Riggleman B, Schedl P, Wieschaus E. 1990. Spatial expression of the Drosophila segment polarity gene armadillo is posttranscriptionally regulated by wingless. Cell 63:549-60
93. Rijsewijk F, Schuermann M, Wagenaar E, Parren P, Weigel D, Nusse R. 1987. The Drosophila homolog of the mouse mammary oncogene int-1 is identical to the segment polarity gene wingless. Cell 50:649-57
94. Rocheleau CE, Downs WD, Lin R, Wittmann C, Bei Y, et al. 1997. Wnt signaling and an APC-related gene specify endoderm in early C. elegans embryos. Cell 90:707-16
95. Rubinfeld B, Albert I, Porfiri E, Fiol C, Munemitsu S, Polakis P. 1996. Binding of GSK3beta to the APC-beta-catenin complex and regulation of complex assembly. Science 272:1023-26
96. Rubinfeld B, Robbins P, El GM, Albert I, Porfiri E, Polakis P. 1997. Stabilization of beta-catenin by genetic defects in melanoma cell lines. Science 275:1790-92
97. Rubinfeld B, Souza B, Albert I, Müller O, Chamberlain SH, et al. 1993. Association of the APC gene product with beta-catenin. Science 262:1731-34
98. Rulifson EJ, Blair SS. 1995. Notch regulates wingless expression and is not required for reception of the paracrine wingless signal during wing margin neurogenesis in Drosophila. Development 121:2813-24
99. Sakanaka C, Weiss JB, Williams LT. 1998. Bridging of beta-catenin and glycogen synthase kinase-3beta by axin and inhibition of beta-catenin-mediated transcription. Proc. Natl. Acad. Sci. USA 95:3020-23
100. Sampedro J, Johnston P, Lawrence PA. 1993. A role for wingless in the segmental gradient of Drosophila. Development 117:677-87
101. Sanson B, White P, Vincent JP. 1996. Uncoupling cadherin-based adhesion from wingless signalling in Drosophila. Nature 383:627-30
102. Sawa H, Lobel L, Horvitz HR. 1996. The Caenorhabditis elegans gene lin-17, which is required for certain asymmetric cell divisions, encodes a putative seven-transmembrane protein similar to the Drosophila frizzled protein. Genes Dev. 10:2189-97
103. Schneider S, Steinbeisser H, Warga RM, Hausen P. 1996. Beta-catenin translocation into nuclei demarcates the dorsalizing centers in frog and fish embryos. Mech. Dev. 57:191-98
104. Siegfried E, Chou TB, Perrimon N. 1992. wingless signaling acts through zeste-white 3, the Drosophila homolog of glycogen synthase kinase-3, to regulate engrailed and establish cell fate. Cell 71:1167-79
105. Siegfried E, Wilder EL, Perrimon N. 1994. Components of wingless signalling in Drosophila. Nature 367:76-80
106. Slusarski DC, Corces VG, Moon RT. 1997a. Interaction of Wnt and a Frizzled homologue triggers G-protein-linked phosphatidylinositol signalling. Nature 390:410-13
107. 2+ signaling by Wnt-5A. Dev. Biol. 182:114-20
108. Smolich BD, McMahon JA, McMahon AP, Papkoff J. 1993. Wnt family proteins are secreted and associated with the cell surface. Mol. Biol. Cell 4:1267-75
109. Sokol SY. 1996. Analysis of Dishevelled signalling pathways during Xenopus development. Curr. Biol. 6:1456-67
110. Sokol SY, Klingensmith J, Perrimon N, Itoh K. 1995. Dorsalizing and neuralizing properties of Xdsh, a maternally expressed Xenopus homolog of dishevelled. Development 121:1637-47
111. Songyang Z, Fanning AS, Fu C, Xu J, Marfatia SM, et al. 1997. Recognition of unique carboxyl-terminal motifs by distinct PDZ domains. Science 275:73-77
112. Stambolic V, Ruel L, Woodgett JR. 1996. Lithium inhibits glycogen synthase kinase-3 activity and mimics wingless signalling in intact cells. Curr. Biol. 6:1664-68
113. Stone DM, Hynes M, Armanini M, Swanson TA, Gu Q, et al. 1996. The tumour-suppressor gene patched encodes a candidate receptor for Sonic hedgehog. Nature 384:129-34
114. Strutt DI, Weber U, Mlodzik M. 1997. The role of RhoA in tissue polarity and Frizzled signalling. Nature 387:292-95
115. Su LK, Vogelstein B, Kinzler KW 1993. Association of the APC tumor suppressor protein with catenins. Science 262:1734-77
116. Theisen H, Purcell J, Bennett M, Kansagara D, Syed A, Marsh JL. 1994. dishevelled is required during wingless signaling to establish both cell polarity and cell identity. Development 120:347-60
117. Thomas KR, Capecchi MR. 1990. Targeted disruption of the murine int-1 proto-oncogene resulting in severe abnormalities in mid-brain and cerebellar development. Nature 346:847-50
118. Thorpe CJ, Schlesinger A, Carter JC, Bowerman B. 1997. Wnt signaling polarizes an early C. elegans blastomere to distinguish endoderm from mesoderm. Cell 90:695-705
119. Tomlinson A, Strapps WR, Heemskerk J. 1997. Linking Frizzled and Wnt signaling in Drosophila development. Development 124:4515-21
120. Torres MA, Yang-Snyder J, Purcell SM, DeMarais AA, McGrew LL, Moon RT. 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. 133:1123-37
121. van den Heuvel M, Harryman Samos C, Klingensmith J, Perrimon N, Nusse R. 1993, Mutations in the segment polarity genes wingless and porcupine impair secretion of the wingless protein. EMBO J. 12:5293-302
122. van den Heuvel M, Ingham PW. 1996. smoothened encodes a receptor-like serpentine protein required for hedgehog signalling. Nature 382:547-51
123. van den Heuvel M, Nusse R, Johnston P, Lawrence PA. 1989. Distribution of the wingless gene product in Drosophila embryos: a protein involved in cell-cell communication. Cell 59:739-49
124. van de Wetering M, Cavallo R, Dooijes D, van Beest M, van Es J, et al. 1997. Armadillo coactivates transcription driven by the product of the Drosophila segment polarity gene dTCF. Cell 88:789-99
125. van Leeuwen F, Harryman Samos C, Nusse R. 1994. Biological activity of soluble wingless protein in cultured Drosophila imaginal disc cells. Nature 368:342-44
126. Vinson CR, Adler PN. 1987. Directional non-cell autonomy and the transmission of polarity information by the frizzled gene of Drosophila. Nature 329:549-51
127. Vinson CR, Conover S, Adler PN. 1989. A Drosophila tissue polarity locus encodes a protein containing seven potential transmembrane domains. Nature 338:263-64
128. Vleminckx K, Wong E, Guger K, Rubinfeld B, Polakis P, Gumbiner BM. 1997. Adenomatons polyposis coli tumor suppressor protein has signaling activity in Xenopus laevis embryos resulting in the induction of an ectopic dorsoanterior axis. J. Cell Biol. 136:411-20
129. Wang S, Krinks M, Lin K, Luyten FP, Moos MJ. 1997. Frzb, a secreted protein expressed in the Spemann organizer, binds and inhibits Wnt-8. Cell 88:757-66
130. Wang Y, Macke JP, Abella BS, Andreasson K, Worley P, et al. 1996. A large family of putative transinembrane receptors homologous to the product of the Drosophila tissue polarity gene frizzled. J. Biol. Chem. 271:4468-76
131. Wang YK, Harryman Samos C, Peoples R, Perez JL, Nusse R, Francke U. 1997. A novel human homologue of the Drosophila frizzled wnt receptor gene binds wingless protein and is in the Williams syndrome deletion at 7q11.23. Hum. Mol. Genet. 6:465-72
132. Willert K, Brink M, Wodarz A, Varmus H, Nusse R. 1997. Casein kinase 2 associates with and phosphorylates dishevelled. EMBO J. 16:3089-96
133. Willert K, Nusse R. 1998. β-catenin: a key mediator of Wnt signaling. Curr. Opin. Genet. Dev. 8:95-102
134. Wong GT, Gavin BJ, McMahon AP. 1994. Differential transformation of mammary epithelial cells by Wnt genes. Mol Cell. Biol. 14:6278-86
135. Wong LL, Adler PN. 1993. Tissue polarity genes of Drosophila regulate the subcellular location for prehair initiation in pupal wing cells. J. Cell Biol. 123:209-21
136. Yanagawa S, van Leeuwen F, Wodarz A, Klingensmith J, Nusse R. 1995. The dishevelled protein is modified by wingless signaling in Drosophila. Genes Dev. 9:1087-97
137. Yanagawa S, Lee J-S, Haruna T, Oda H, Uemura T, et al. 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. 272:25243-51
138. Yang-Snyder J, Miller JR, Brown JD, Lai CJ, Moon RT. 1996. A frizzled homolog functions in a vertebrate Wnt signaling pathway. Curr. Biol. 6:1302-6
139. Yost C, Torres M, Miller JR, Huang E, Kimelman D, Moon RT. 1996, The axis-inducing activity, stability, and subcellular distribution of beta-catenin is regulated in Xenopus embryos by glycogen synthase kinase 3. Genes Dev. 10:1443-54
140. Zecca M, Basler K, Struhl G. 1996. Direct and long-range action of a wingless morphogen gradient. Cell 87:833-44
141. Zeng L, Fagotto F, Zhang T, Hsu W, Vasicek TJ. et al. 1997. The mouse Fused locus encodes Axin, an inhibitor of the Wnt signaling pathway that regulates embryonic axis formation. Cell 90:181-92
142. Zheng L, Zhang J, Carthew RW. 1995. frizzled regulates mirror-symmetric pattern formation in the Drosophila eye. Development 121:3045-55