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. 1998 Jan 15;329(Pt 2):209–223. doi: 10.1042/bj3290209

Signal transduction by the Wnt family of ligands.

T C Dale 1
PMCID: PMC1219034  PMID: 9425102

Abstract

The Wnt genes encode a large family of secreted polypeptides that mediate cell-cell communication in diverse developmental processes. The loss or inappropriate activation of Wnt expression has been shown to alter cell fate, morphogenesis and mitogenesis. Recent progress has identified Wnt receptors and components of an intracellular signalling pathway that mediate Wnt-dependent transcription. This review will highlight this 'core' Wnt signal-transduction pathway, but also aims to reveal the potential diversity of Wnt signalling targets. Particular attention will be paid to the overlap between developmental biology and oncogenesis, since recent progress shows Wnt signalling forms a paradigm for an interdisciplinary approach.

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Selected References

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  1. Aberle H., Bauer A., Stappert J., Kispert A., Kemler R. beta-catenin is a target for the ubiquitin-proteasome pathway. EMBO J. 1997 Jul 1;16(13):3797–3804. doi: 10.1093/emboj/16.13.3797. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Adler P. N. The genetic control of tissue polarity in Drosophila. Bioessays. 1992 Nov;14(11):735–741. doi: 10.1002/bies.950141103. [DOI] [PubMed] [Google Scholar]
  3. Alcedo J., Ayzenzon M., Von Ohlen T., Noll M., Hooper J. E. The Drosophila smoothened gene encodes a seven-pass membrane protein, a putative receptor for the hedgehog signal. Cell. 1996 Jul 26;86(2):221–232. doi: 10.1016/s0092-8674(00)80094-x. [DOI] [PubMed] [Google Scholar]
  4. Ault K. T., Durmowicz G., Galione A., Harger P. L., Busa W. B. Modulation of Xenopus embryo mesoderm-specific gene expression and dorsoanterior patterning by receptors that activate the phosphatidylinositol cycle signal transduction pathway. Development. 1996 Jul;122(7):2033–2041. doi: 10.1242/dev.122.7.2033. [DOI] [PubMed] [Google Scholar]
  5. Axelrod J. D., Matsuno K., Artavanis-Tsakonas S., Perrimon N. Interaction between Wingless and Notch signaling pathways mediated by dishevelled. Science. 1996 Mar 29;271(5257):1826–1832. doi: 10.1126/science.271.5257.1826. [DOI] [PubMed] [Google Scholar]
  6. Barth A. I., Pollack A. L., Altschuler Y., Mostov K. E., Nelson W. J. NH2-terminal deletion of beta-catenin results in stable colocalization of mutant beta-catenin with adenomatous polyposis coli protein and altered MDCK cell adhesion. J Cell Biol. 1997 Feb 10;136(3):693–706. doi: 10.1083/jcb.136.3.693. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Beals C. R., Sheridan C. M., Turck C. W., Gardner P., Crabtree G. R. Nuclear export of NF-ATc enhanced by glycogen synthase kinase-3. Science. 1997 Mar 28;275(5308):1930–1934. doi: 10.1126/science.275.5308.1930. [DOI] [PubMed] [Google Scholar]
  8. Behrens J., Vakaet L., Friis R., Winterhager E., Van Roy F., Mareel M. M., Birchmeier W. Loss of epithelial differentiation and gain of invasiveness correlates with tyrosine phosphorylation of the E-cadherin/beta-catenin complex in cells transformed with a temperature-sensitive v-SRC gene. J Cell Biol. 1993 Feb;120(3):757–766. doi: 10.1083/jcb.120.3.757. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Behrens J., von Kries J. P., Kühl M., Bruhn L., Wedlich D., Grosschedl R., Birchmeier W. Functional interaction of beta-catenin with the transcription factor LEF-1. Nature. 1996 Aug 15;382(6592):638–642. doi: 10.1038/382638a0. [DOI] [PubMed] [Google Scholar]
  10. Bhanot P., Brink M., Samos C. H., Hsieh J. C., Wang Y., Macke J. P., Andrew D., Nathans J., Nusse R. A new member of the frizzled family from Drosophila functions as a Wingless receptor. Nature. 1996 Jul 18;382(6588):225–230. doi: 10.1038/382225a0. [DOI] [PubMed] [Google Scholar]
  11. Binari R. C., Staveley B. E., Johnson W. A., Godavarti R., Sasisekharan R., Manoukian A. S. Genetic evidence that heparin-like glycosaminoglycans are involved in wingless signaling. Development. 1997 Jul;124(13):2623–2632. doi: 10.1242/dev.124.13.2623. [DOI] [PubMed] [Google Scholar]
  12. Birchmeier W., Hülsken J., Behrens J. E-cadherin as an invasion suppressor. Ciba Found Symp. 1995;189:124-36; discussion 136-41, 174-6. doi: 10.1002/9780470514719.ch10. [DOI] [PubMed] [Google Scholar]
  13. Blair S. S. Notch and Wingless signals collide. Science. 1996 Mar 29;271(5257):1822–1823. doi: 10.1126/science.271.5257.1822. [DOI] [PubMed] [Google Scholar]
  14. Bradbury J. M., Niemeyer C. C., Dale T. C., Edwards P. A. Alterations of the growth characteristics of the fibroblast cell line C3H 10T1/2 by members of the Wnt gene family. Oncogene. 1994 Sep;9(9):2597–2603. [PubMed] [Google Scholar]
  15. Bradley R. S., Brown A. M. A soluble form of Wnt-1 protein with mitogenic activity on mammary epithelial cells. Mol Cell Biol. 1995 Aug;15(8):4616–4622. doi: 10.1128/mcb.15.8.4616. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Bradley R. S., Cowin P., Brown A. M. Expression of Wnt-1 in PC12 cells results in modulation of plakoglobin and E-cadherin and increased cellular adhesion. J Cell Biol. 1993 Dec;123(6 Pt 2):1857–1865. doi: 10.1083/jcb.123.6.1857. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Brannon M., Kimelman D. Activation of Siamois by the Wnt pathway. Dev Biol. 1996 Nov 25;180(1):344–347. doi: 10.1006/dbio.1996.0306. [DOI] [PubMed] [Google Scholar]
  18. Brown A. M., Papkoff J., Fung Y. K., Shackleford G. M., Varmus H. E. Identification of protein products encoded by the proto-oncogene int-1. Mol Cell Biol. 1987 Nov;7(11):3971–3977. doi: 10.1128/mcb.7.11.3971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Brown A. M., Wildin R. S., Prendergast T. J., Varmus H. E. A retrovirus vector expressing the putative mammary oncogene int-1 causes partial transformation of a mammary epithelial cell line. Cell. 1986 Sep 26;46(7):1001–1009. doi: 10.1016/0092-8674(86)90699-9. [DOI] [PubMed] [Google Scholar]
  20. Brown E. M., Gamba G., Riccardi D., Lombardi M., Butters R., Kifor O., Sun A., Hediger M. A., Lytton J., Hebert S. C. Cloning and characterization of an extracellular Ca(2+)-sensing receptor from bovine parathyroid. Nature. 1993 Dec 9;366(6455):575–580. doi: 10.1038/366575a0. [DOI] [PubMed] [Google Scholar]
  21. Brunner E., Peter O., Schweizer L., Basler K. pangolin encodes a Lef-1 homologue that acts downstream of Armadillo to transduce the Wingless signal in Drosophila. Nature. 1997 Feb 27;385(6619):829–833. doi: 10.1038/385829a0. [DOI] [PubMed] [Google Scholar]
  22. Burrus L. W., McMahon A. P. Biochemical analysis of murine Wnt proteins reveals both shared and distinct properties. Exp Cell Res. 1995 Oct;220(2):363–373. doi: 10.1006/excr.1995.1327. [DOI] [PubMed] [Google Scholar]
  23. Butz S., Stappert J., Weissig H., Kemler R. Plakoglobin and beta-catenin: distinct but closely related. Science. 1992 Aug 21;257(5073):1142–1144. doi: 10.1126/science.257.5073.1142-a. [DOI] [PubMed] [Google Scholar]
  24. Byers S., Pishvaian M., Crockett C., Peer C., Tozeren A., Sporn M., Anzano M., Lechleider R. Retinoids increase cell-cell adhesion strength, beta-catenin protein stability, and localization to the cell membrane in a breast cancer cell line: a role for serine kinase activity. Endocrinology. 1996 Aug;137(8):3265–3273. doi: 10.1210/endo.137.8.8754749. [DOI] [PubMed] [Google Scholar]
  25. Cadigan K. M., Nusse R. wingless signaling in the Drosophila eye and embryonic epidermis. Development. 1996 Sep;122(9):2801–2812. doi: 10.1242/dev.122.9.2801. [DOI] [PubMed] [Google Scholar]
  26. Carnac G., Kodjabachian L., Gurdon J. B., Lemaire P. The homeobox gene Siamois is a target of the Wnt dorsalisation pathway and triggers organiser activity in the absence of mesoderm. Development. 1996 Oct;122(10):3055–3065. doi: 10.1242/dev.122.10.3055. [DOI] [PubMed] [Google Scholar]
  27. Castrop J., van Norren K., Clevers H. A gene family of HMG-box transcription factors with homology to TCF-1. Nucleic Acids Res. 1992 Feb 11;20(3):611–611. doi: 10.1093/nar/20.3.611. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Chan S. D., Karpf D. B., Fowlkes M. E., Hooks M., Bradley M. S., Vuong V., Bambino T., Liu M. Y., Arnaud C. D., Strewler G. J. Two homologs of the Drosophila polarity gene frizzled (fz) are widely expressed in mammalian tissues. J Biol Chem. 1992 Dec 15;267(35):25202–25207. [PubMed] [Google Scholar]
  29. Chitnis A., Henrique D., Lewis J., Ish-Horowicz D., Kintner C. Primary neurogenesis in Xenopus embryos regulated by a homologue of the Drosophila neurogenic gene Delta. Nature. 1995 Jun 29;375(6534):761–766. doi: 10.1038/375761a0. [DOI] [PubMed] [Google Scholar]
  30. Cook D., Fry M. J., Hughes K., Sumathipala R., Woodgett J. R., Dale T. C. Wingless inactivates glycogen synthase kinase-3 via an intracellular signalling pathway which involves a protein kinase C. EMBO J. 1996 Sep 2;15(17):4526–4536. [PMC free article] [PubMed] [Google Scholar]
  31. Couso J. P., Knust E., Martinez Arias A. Serrate and wingless cooperate to induce vestigial gene expression and wing formation in Drosophila. Curr Biol. 1995 Dec 1;5(12):1437–1448. doi: 10.1016/s0960-9822(95)00281-8. [DOI] [PubMed] [Google Scholar]
  32. Couso J. P., Martinez Arias A. Notch is required for wingless signaling in the epidermis of Drosophila. Cell. 1994 Oct 21;79(2):259–272. doi: 10.1016/0092-8674(94)90195-3. [DOI] [PubMed] [Google Scholar]
  33. Cox R. T., Kirkpatrick C., Peifer M. Armadillo is required for adherens junction assembly, cell polarity, and morphogenesis during Drosophila embryogenesis. J Cell Biol. 1996 Jul;134(1):133–148. doi: 10.1083/jcb.134.1.133. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Cross D. A., Alessi D. R., Cohen P., Andjelkovich M., Hemmings B. A. Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature. 1995 Dec 21;378(6559):785–789. doi: 10.1038/378785a0. [DOI] [PubMed] [Google Scholar]
  35. Cross D. A., Alessi D. R., Vandenheede J. R., McDowell H. E., Hundal H. S., Cohen P. The inhibition of glycogen synthase kinase-3 by insulin or insulin-like growth factor 1 in the rat skeletal muscle cell line L6 is blocked by wortmannin, but not by rapamycin: evidence that wortmannin blocks activation of the mitogen-activated protein kinase pathway in L6 cells between Ras and Raf. Biochem J. 1994 Oct 1;303(Pt 1):21–26. doi: 10.1042/bj3030021. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. DeMarais A. A., Moon R. T. The armadillo homologs beta-catenin and plakoglobin are differentially expressed during early development of Xenopus laevis. Dev Biol. 1992 Oct;153(2):337–346. doi: 10.1016/0012-1606(92)90118-z. [DOI] [PubMed] [Google Scholar]
  37. DiDonato J., Mercurio F., Rosette C., Wu-Li J., Suyang H., Ghosh S., Karin M. Mapping of the inducible IkappaB phosphorylation sites that signal its ubiquitination and degradation. Mol Cell Biol. 1996 Apr;16(4):1295–1304. doi: 10.1128/mcb.16.4.1295. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Dominguez I., Itoh K., Sokol S. Y. Role of glycogen synthase kinase 3 beta as a negative regulator of dorsoventral axis formation in Xenopus embryos. Proc Natl Acad Sci U S A. 1995 Aug 29;92(18):8498–8502. doi: 10.1073/pnas.92.18.8498. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Du S. J., Purcell S. M., Christian J. L., McGrew L. L., Moon R. T. Identification of distinct classes and functional domains of Wnts through expression of wild-type and chimeric proteins in Xenopus embryos. Mol Cell Biol. 1995 May;15(5):2625–2634. doi: 10.1128/mcb.15.5.2625. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Edwards P. A., Hiby S. E., Papkoff J., Bradbury J. M. Hyperplasia of mouse mammary epithelium induced by expression of the Wnt-1 (int-1) oncogene in reconstituted mammary gland. Oncogene. 1992 Oct;7(10):2041–2051. [PubMed] [Google Scholar]
  41. Eisenberg L. M., Ingham P. W., Brown A. M. Cloning and characterization of a novel Drosophila Wnt gene, Dwnt-5, a putative downstream target of the homeobox gene distal-less. Dev Biol. 1992 Nov;154(1):73–83. doi: 10.1016/0012-1606(92)90049-m. [DOI] [PubMed] [Google Scholar]
  42. Eldar-Finkelman H., Seger R., Vandenheede J. R., Krebs E. G. Inactivation of glycogen synthase kinase-3 by epidermal growth factor is mediated by mitogen-activated protein kinase/p90 ribosomal protein S6 kinase signaling pathway in NIH/3T3 cells. J Biol Chem. 1995 Jan 20;270(3):987–990. doi: 10.1074/jbc.270.3.987. [DOI] [PubMed] [Google Scholar]
  43. Fagotto F., Funayama N., Gluck U., Gumbiner B. M. Binding to cadherins antagonizes the signaling activity of beta-catenin during axis formation in Xenopus. J Cell Biol. 1996 Mar;132(6):1105–1114. doi: 10.1083/jcb.132.6.1105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Fagotto F., Guger K., Gumbiner B. M. Induction of the primary dorsalizing center in Xenopus by the Wnt/GSK/beta-catenin signaling pathway, but not by Vg1, Activin or Noggin. Development. 1997 Jan;124(2):453–460. doi: 10.1242/dev.124.2.453. [DOI] [PubMed] [Google Scholar]
  45. Fan M. J., Sokol S. Y. A role for Siamois in Spemann organizer formation. Development. 1997 Jul;124(13):2581–2589. doi: 10.1242/dev.124.13.2581. [DOI] [PubMed] [Google Scholar]
  46. Fialka I., Schwarz H., Reichmann E., Oft M., Busslinger M., Beug H. The estrogen-dependent c-JunER protein causes a reversible loss of mammary epithelial cell polarity involving a destabilization of adherens junctions. J Cell Biol. 1996 Mar;132(6):1115–1132. doi: 10.1083/jcb.132.6.1115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Fradkin L. G., Noordermeer J. N., Nusse R. The Drosophila Wnt protein DWnt-3 is a secreted glycoprotein localized on the axon tracts of the embryonic CNS. Dev Biol. 1995 Mar;168(1):202–213. doi: 10.1006/dbio.1995.1072. [DOI] [PubMed] [Google Scholar]
  48. Fredieu J. R., Cui Y., Maier D., Danilchik M. V., Christian J. L. Xwnt-8 and lithium can act upon either dorsal mesodermal or neurectodermal cells to cause a loss of forebrain in Xenopus embryos. Dev Biol. 1997 Jun 1;186(1):100–114. doi: 10.1006/dbio.1997.8566. [DOI] [PubMed] [Google Scholar]
  49. Gavin B. J., McMahon J. A., McMahon A. P. Expression of multiple novel Wnt-1/int-1-related genes during fetal and adult mouse development. Genes Dev. 1990 Dec;4(12B):2319–2332. doi: 10.1101/gad.4.12b.2319. [DOI] [PubMed] [Google Scholar]
  50. Gerber A. N., Klesert T. R., Bergstrom D. A., Tapscott S. J. Two domains of MyoD mediate transcriptional activation of genes in repressive chromatin: a mechanism for lineage determination in myogenesis. Genes Dev. 1997 Feb 15;11(4):436–450. doi: 10.1101/gad.11.4.436. [DOI] [PubMed] [Google Scholar]
  51. Ginsburg G. T., Kimmel A. R. Autonomous and nonautonomous regulation of axis formation by antagonistic signaling via 7-span cAMP receptors and GSK3 in Dictyostelium. Genes Dev. 1997 Aug 15;11(16):2112–2123. doi: 10.1101/gad.11.16.2112. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Goode N., Hughes K., Woodgett J. R., Parker P. J. Differential regulation of glycogen synthase kinase-3 beta by protein kinase C isotypes. J Biol Chem. 1992 Aug 25;267(24):16878–16882. [PubMed] [Google Scholar]
  53. Graba Y., Gieseler K., Aragnol D., Laurenti P., Mariol M. C., Berenger H., Sagnier T., Pradel J. DWnt-4, a novel Drosophila Wnt gene acts downstream of homeotic complex genes in the visceral mesoderm. Development. 1995 Jan;121(1):209–218. doi: 10.1242/dev.121.1.209. [DOI] [PubMed] [Google Scholar]
  54. Groden J., Thliveris A., Samowitz W., Carlson M., Gelbert L., Albertsen H., Joslyn G., Stevens J., Spirio L., Robertson M. Identification and characterization of the familial adenomatous polyposis coli gene. Cell. 1991 Aug 9;66(3):589–600. doi: 10.1016/0092-8674(81)90021-0. [DOI] [PubMed] [Google Scholar]
  55. Gumbiner B. M. Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell. 1996 Feb 9;84(3):345–357. doi: 10.1016/s0092-8674(00)81279-9. [DOI] [PubMed] [Google Scholar]
  56. Haegel H., Larue L., Ohsugi M., Fedorov L., Herrenknecht K., Kemler R. Lack of beta-catenin affects mouse development at gastrulation. Development. 1995 Nov;121(11):3529–3537. doi: 10.1242/dev.121.11.3529. [DOI] [PubMed] [Google Scholar]
  57. Haerry T. E., Heslip T. R., Marsh J. L., O'Connor M. B. Defects in glucuronate biosynthesis disrupt Wingless signaling in Drosophila. Development. 1997 Aug;124(16):3055–3064. doi: 10.1242/dev.124.16.3055. [DOI] [PubMed] [Google Scholar]
  58. Han M. Gut reaction to Wnt signaling in worms. Cell. 1997 Aug 22;90(4):581–584. doi: 10.1016/s0092-8674(00)80517-6. [DOI] [PubMed] [Google Scholar]
  59. Harrison S. C. Peptide-surface association: the case of PDZ and PTB domains. Cell. 1996 Aug 9;86(3):341–343. doi: 10.1016/s0092-8674(00)80105-1. [DOI] [PubMed] [Google Scholar]
  60. Hayashi S., Rubinfeld B., Souza B., Polakis P., Wieschaus E., Levine A. J. 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 U S A. 1997 Jan 7;94(1):242–247. doi: 10.1073/pnas.94.1.242. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. He X., Saint-Jeannet J. P., Wang Y., Nathans J., Dawid I., Varmus H. A member of the Frizzled protein family mediating axis induction by Wnt-5A. Science. 1997 Mar 14;275(5306):1652–1654. doi: 10.1126/science.275.5306.1652. [DOI] [PubMed] [Google Scholar]
  62. He X., Saint-Jeannet J. P., Woodgett J. R., Varmus H. E., Dawid I. B. Glycogen synthase kinase-3 and dorsoventral patterning in Xenopus embryos. Nature. 1995 Apr 13;374(6523):617–622. doi: 10.1038/374617a0. [DOI] [PubMed] [Google Scholar]
  63. Heasman J., Crawford A., Goldstone K., Garner-Hamrick P., Gumbiner B., McCrea P., Kintner C., Noro C. Y., Wylie C. Overexpression of cadherins and underexpression of beta-catenin inhibit dorsal mesoderm induction in early Xenopus embryos. Cell. 1994 Dec 2;79(5):791–803. doi: 10.1016/0092-8674(94)90069-8. [DOI] [PubMed] [Google Scholar]
  64. Hedgepeth C. M., Conrad L. J., Zhang J., Huang H. C., Lee V. M., Klein P. S. Activation of the Wnt signaling pathway: a molecular mechanism for lithium action. Dev Biol. 1997 May 1;185(1):82–91. doi: 10.1006/dbio.1997.8552. [DOI] [PubMed] [Google Scholar]
  65. Heemskerk J., DiNardo S., Kostriken R., O'Farrell P. H. Multiple modes of engrailed regulation in the progression towards cell fate determination. Nature. 1991 Aug 1;352(6334):404–410. doi: 10.1038/352404a0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Herman M. A., Vassilieva L. L., Horvitz H. R., Shaw J. E., Herman R. K. The C. elegans gene lin-44, which controls the polarity of certain asymmetric cell divisions, encodes a Wnt protein and acts cell nonautonomously. Cell. 1995 Oct 6;83(1):101–110. doi: 10.1016/0092-8674(95)90238-4. [DOI] [PubMed] [Google Scholar]
  67. Hinck L., Nelson W. J., Papkoff J. Wnt-1 modulates cell-cell adhesion in mammalian cells by stabilizing beta-catenin binding to the cell adhesion protein cadherin. J Cell Biol. 1994 Mar;124(5):729–741. doi: 10.1083/jcb.124.5.729. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Hinck L., Näthke I. S., Papkoff J., Nelson W. J. Beta-catenin: a common target for the regulation of cell adhesion by Wnt-1 and Src signaling pathways. Trends Biochem Sci. 1994 Dec;19(12):538–542. doi: 10.1016/0968-0004(94)90057-4. [DOI] [PubMed] [Google Scholar]
  69. Hoang B., Moos M., Jr, Vukicevic S., Luyten F. P. Primary structure and tissue distribution of FRZB, a novel protein related to Drosophila frizzled, suggest a role in skeletal morphogenesis. J Biol Chem. 1996 Oct 18;271(42):26131–26137. doi: 10.1074/jbc.271.42.26131. [DOI] [PubMed] [Google Scholar]
  70. Hochstrasser M. Protein degradation or regulation: Ub the judge. Cell. 1996 Mar 22;84(6):813–815. doi: 10.1016/s0092-8674(00)81058-2. [DOI] [PubMed] [Google Scholar]
  71. Hooper J. E. Distinct pathways for autocrine and paracrine Wingless signalling in Drosophila embryos. Nature. 1994 Dec 1;372(6505):461–464. doi: 10.1038/372461a0. [DOI] [PubMed] [Google Scholar]
  72. Hoppler S., Brown J. D., Moon R. T. Expression of a dominant-negative Wnt blocks induction of MyoD in Xenopus embryos. Genes Dev. 1996 Nov 1;10(21):2805–2817. doi: 10.1101/gad.10.21.2805. [DOI] [PubMed] [Google Scholar]
  73. Hoschuetzky H., Aberle H., Kemler R. Beta-catenin mediates the interaction of the cadherin-catenin complex with epidermal growth factor receptor. J Cell Biol. 1994 Dec;127(5):1375–1380. doi: 10.1083/jcb.127.5.1375. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Howlett A. R., Bissell M. J. The influence of tissue microenvironment (stroma and extracellular matrix) on the development and function of mammary epithelium. Epithelial Cell Biol. 1993 Apr;2(2):79–89. [PubMed] [Google Scholar]
  75. Huber A. H., Nelson W. J., Weis W. I. Three-dimensional structure of the armadillo repeat region of beta-catenin. Cell. 1997 Sep 5;90(5):871–882. doi: 10.1016/s0092-8674(00)80352-9. [DOI] [PubMed] [Google Scholar]
  76. Huber O., Korn R., McLaughlin J., Ohsugi M., Herrmann B. G., Kemler R. Nuclear localization of beta-catenin by interaction with transcription factor LEF-1. Mech Dev. 1996 Sep;59(1):3–10. doi: 10.1016/0925-4773(96)00597-7. [DOI] [PubMed] [Google Scholar]
  77. Hughes K., Nikolakaki E., Plyte S. E., Totty N. F., Woodgett J. R. Modulation of the glycogen synthase kinase-3 family by tyrosine phosphorylation. EMBO J. 1993 Feb;12(2):803–808. doi: 10.1002/j.1460-2075.1993.tb05715.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Hülsken J., Birchmeier W., Behrens J. E-cadherin and APC compete for the interaction with beta-catenin and the cytoskeleton. J Cell Biol. 1994 Dec;127(6 Pt 2):2061–2069. doi: 10.1083/jcb.127.6.2061. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Ingham P. W. Has the quest for a Wnt receptor finally frizzled out? Trends Genet. 1996 Oct;12(10):382–384. doi: 10.1016/0168-9525(96)30096-6. [DOI] [PubMed] [Google Scholar]
  80. Itoh K., Sokol S. Y. Graded amounts of Xenopus dishevelled specify discrete anteroposterior cell fates in prospective ectoderm. Mech Dev. 1997 Jan;61(1-2):113–125. doi: 10.1016/s0925-4773(96)00627-2. [DOI] [PubMed] [Google Scholar]
  81. Itoh K., Tang T. L., Neel B. G., Sokol S. Y. Specific modulation of ectodermal cell fates in Xenopus embryos by glycogen synthase kinase. Development. 1995 Dec;121(12):3979–3988. doi: 10.1242/dev.121.12.3979. [DOI] [PubMed] [Google Scholar]
  82. Jiang J., Struhl G. Complementary and mutually exclusive activities of decapentaplegic and wingless organize axial patterning during Drosophila leg development. Cell. 1996 Aug 9;86(3):401–409. doi: 10.1016/s0092-8674(00)80113-0. [DOI] [PubMed] [Google Scholar]
  83. Johnson D. E., Williams L. T. Structural and functional diversity in the FGF receptor multigene family. Adv Cancer Res. 1993;60:1–41. doi: 10.1016/s0065-230x(08)60821-0. [DOI] [PubMed] [Google Scholar]
  84. Jue S. F., Bradley R. S., Rudnicki J. A., Varmus H. E., Brown A. M. The mouse Wnt-1 gene can act via a paracrine mechanism in transformation of mammary epithelial cells. Mol Cell Biol. 1992 Jan;12(1):321–328. doi: 10.1128/mcb.12.1.321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  85. Kageura H. Activation of dorsal development by contact between the cortical dorsal determinant and the equatorial core cytoplasm in eggs of Xenopus laevis. Development. 1997 Apr;124(8):1543–1551. doi: 10.1242/dev.124.8.1543. [DOI] [PubMed] [Google Scholar]
  86. Karnovsky A., Klymkowsky M. W. Anterior axis duplication in Xenopus induced by the over-expression of the cadherin-binding protein plakoglobin. Proc Natl Acad Sci U S A. 1995 May 9;92(10):4522–4526. doi: 10.1073/pnas.92.10.4522. [DOI] [PMC free article] [PubMed] [Google Scholar]
  87. Katoh M., Hirai M., Sugimura T., Terada M. Cloning, expression and chromosomal localization of Wnt-13, a novel member of the Wnt gene family. Oncogene. 1996 Aug 15;13(4):873–876. [PubMed] [Google Scholar]
  88. Kinoshita K., Asashima M. Effect of activin and lithium on isolated Xenopus animal blastomeres and response alteration at the midblastula transition. Development. 1995 Jun;121(6):1581–1589. doi: 10.1242/dev.121.6.1581. [DOI] [PubMed] [Google Scholar]
  89. Kinzler K. W., Vogelstein B. Lessons from hereditary colorectal cancer. Cell. 1996 Oct 18;87(2):159–170. doi: 10.1016/s0092-8674(00)81333-1. [DOI] [PubMed] [Google Scholar]
  90. Klein P. S., Melton D. A. A molecular mechanism for the effect of lithium on development. Proc Natl Acad Sci U S A. 1996 Aug 6;93(16):8455–8459. doi: 10.1073/pnas.93.16.8455. [DOI] [PMC free article] [PubMed] [Google Scholar]
  91. Klingensmith J., Nusse R., Perrimon N. The Drosophila segment polarity gene dishevelled encodes a novel protein required for response to the wingless signal. Genes Dev. 1994 Jan;8(1):118–130. doi: 10.1101/gad.8.1.118. [DOI] [PubMed] [Google Scholar]
  92. Klingensmith J., Nusse R. Signaling by wingless in Drosophila. Dev Biol. 1994 Dec;166(2):396–414. doi: 10.1006/dbio.1994.1325. [DOI] [PubMed] [Google Scholar]
  93. Kofron M., Spagnuolo A., Klymkowsky M., Wylie C., Heasman J. The roles of maternal alpha-catenin and plakoglobin in the early Xenopus embryo. Development. 1997 Apr;124(8):1553–1560. doi: 10.1242/dev.124.8.1553. [DOI] [PubMed] [Google Scholar]
  94. Korinek V., Barker N., Morin P. J., van Wichen D., de Weger R., Kinzler K. W., Vogelstein B., Clevers H. Constitutive transcriptional activation by a beta-catenin-Tcf complex in APC-/- colon carcinoma. Science. 1997 Mar 21;275(5307):1784–1787. doi: 10.1126/science.275.5307.1784. [DOI] [PubMed] [Google Scholar]
  95. Krasnow R. E., Wong L. L., Adler P. N. Dishevelled is a component of the frizzled signaling pathway in Drosophila. Development. 1995 Dec;121(12):4095–4102. doi: 10.1242/dev.121.12.4095. [DOI] [PubMed] [Google Scholar]
  96. Ku M., Melton D. A. Xwnt-11: a maternally expressed Xenopus wnt gene. Development. 1993 Dec;119(4):1161–1173. doi: 10.1242/dev.119.4.1161. [DOI] [PubMed] [Google Scholar]
  97. Larabell C. A., Torres M., Rowning B. A., Yost C., Miller J. R., Wu M., Kimelman D., Moon R. T. 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. 1997 Mar 10;136(5):1123–1136. doi: 10.1083/jcb.136.5.1123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  98. Larue L., Antos C., Butz S., Huber O., Delmas V., Dominis M., Kemler R. A role for cadherins in tissue formation. Development. 1996 Oct;122(10):3185–3194. doi: 10.1242/dev.122.10.3185. [DOI] [PubMed] [Google Scholar]
  99. Levitan D., Greenwald I. Facilitation of lin-12-mediated signalling by sel-12, a Caenorhabditis elegans S182 Alzheimer's disease gene. Nature. 1995 Sep 28;377(6547):351–354. doi: 10.1038/377351a0. [DOI] [PubMed] [Google Scholar]
  100. Leyns L., Bouwmeester T., Kim S. H., Piccolo S., De Robertis E. M. Frzb-1 is a secreted antagonist of Wnt signaling expressed in the Spemann organizer. Cell. 1997 Mar 21;88(6):747–756. doi: 10.1016/s0092-8674(00)81921-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  101. Lijam N., Paylor R., McDonald M. P., Crawley J. N., Deng C. X., Herrup K., Stevens K. E., Maccaferri G., McBain C. J., Sussman D. J. Social interaction and sensorimotor gating abnormalities in mice lacking Dvl1. Cell. 1997 Sep 5;90(5):895–905. doi: 10.1016/s0092-8674(00)80354-2. [DOI] [PubMed] [Google Scholar]
  102. Lijam N., Sussman D. J. Organization and promoter analysis of the mouse dishevelled-1 gene. Genome Res. 1995 Sep;5(2):116–124. doi: 10.1101/gr.5.2.116. [DOI] [PubMed] [Google Scholar]
  103. Lin R., Thompson S., Priess J. R. pop-1 encodes an HMG box protein required for the specification of a mesoderm precursor in early C. elegans embryos. Cell. 1995 Nov 17;83(4):599–609. doi: 10.1016/0092-8674(95)90100-0. [DOI] [PubMed] [Google Scholar]
  104. López-Casillas F., Wrana J. L., Massagué J. Betaglycan presents ligand to the TGF beta signaling receptor. Cell. 1993 Jul 2;73(7):1435–1444. doi: 10.1016/0092-8674(93)90368-z. [DOI] [PubMed] [Google Scholar]
  105. Manoukian A. S., Yoffe K. B., Wilder E. L., Perrimon N. The porcupine gene is required for wingless autoregulation in Drosophila. Development. 1995 Dec;121(12):4037–4044. doi: 10.1242/dev.121.12.4037. [DOI] [PubMed] [Google Scholar]
  106. Mason J. O., Kitajewski J., Varmus H. E. Mutational analysis of mouse Wnt-1 identifies two temperature-sensitive alleles and attributes of Wnt-1 protein essential for transformation of a mammary cell line. Mol Biol Cell. 1992 May;3(5):521–533. doi: 10.1091/mbc.3.5.521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  107. Matsumine A., Ogai A., Senda T., Okumura N., Satoh K., Baeg G. H., Kawahara T., Kobayashi S., Okada M., Toyoshima K. Binding of APC to the human homolog of the Drosophila discs large tumor suppressor protein. Science. 1996 May 17;272(5264):1020–1023. doi: 10.1126/science.272.5264.1020. [DOI] [PubMed] [Google Scholar]
  108. Matsumine A., Ogai A., Senda T., Okumura N., Satoh K., Baeg G. H., Kawahara T., Kobayashi S., Okada M., Toyoshima K. Binding of APC to the human homolog of the Drosophila discs large tumor suppressor protein. Science. 1996 May 17;272(5264):1020–1023. doi: 10.1126/science.272.5264.1020. [DOI] [PubMed] [Google Scholar]
  109. McFarland K. C., Sprengel R., Phillips H. S., Köhler M., Rosemblit N., Nikolics K., Segaloff D. L., Seeburg P. H. Lutropin-choriogonadotropin receptor: an unusual member of the G protein-coupled receptor family. Science. 1989 Aug 4;245(4917):494–499. doi: 10.1126/science.2502842. [DOI] [PubMed] [Google Scholar]
  110. McMahon A. P., Joyner A. L., Bradley A., McMahon J. A. The midbrain-hindbrain phenotype of Wnt-1-/Wnt-1- mice results from stepwise deletion of engrailed-expressing cells by 9.5 days postcoitum. Cell. 1992 May 15;69(4):581–595. doi: 10.1016/0092-8674(92)90222-x. [DOI] [PubMed] [Google Scholar]
  111. Merriam J. M., Rubenstein A. B., Klymkowsky M. W. Cytoplasmically anchored plakoglobin induces a WNT-like phenotype in Xenopus. Dev Biol. 1997 May 1;185(1):67–81. doi: 10.1006/dbio.1997.8550. [DOI] [PubMed] [Google Scholar]
  112. Midgley C. A., White S., Howitt R., Save V., Dunlop M. G., Hall P. A., Lane D. P., Wyllie A. H., Bubb V. J. APC expression in normal human tissues. J Pathol. 1997 Apr;181(4):426–433. doi: 10.1002/(SICI)1096-9896(199704)181:4<426::AID-PATH768>3.0.CO;2-T. [DOI] [PubMed] [Google Scholar]
  113. Miller J. R., Moon R. T. Signal transduction through beta-catenin and specification of cell fate during embryogenesis. Genes Dev. 1996 Oct 15;10(20):2527–2539. doi: 10.1101/gad.10.20.2527. [DOI] [PubMed] [Google Scholar]
  114. Molenaar M., van de Wetering M., Oosterwegel M., Peterson-Maduro J., Godsave S., Korinek V., Roose J., Destrée O., Clevers H. XTcf-3 transcription factor mediates beta-catenin-induced axis formation in Xenopus embryos. Cell. 1996 Aug 9;86(3):391–399. doi: 10.1016/s0092-8674(00)80112-9. [DOI] [PubMed] [Google Scholar]
  115. Moon R. T., Brown J. D., Torres M. WNTs modulate cell fate and behavior during vertebrate development. Trends Genet. 1997 Apr;13(4):157–162. doi: 10.1016/s0168-9525(97)01093-7. [DOI] [PubMed] [Google Scholar]
  116. Moon R. T., Brown J. D., Yang-Snyder J. A., Miller J. R. Structurally related receptors and antagonists compete for secreted Wnt ligands. Cell. 1997 Mar 21;88(6):725–728. doi: 10.1016/s0092-8674(00)81915-7. [DOI] [PubMed] [Google Scholar]
  117. Moon R. T., Christian J. L., Campbell R. M., McGrew L. L., DeMarais A. A., Torres M., Lai C. J., Olson D. J., Kelly G. M. Dissecting Wnt signalling pathways and Wnt-sensitive developmental processes through transient misexpression analyses in embryos of Xenopus laevis. Dev Suppl. 1993:85–94. [PubMed] [Google Scholar]
  118. Moon R. T. In pursuit of the functions of the Wnt family of developmental regulators: insights from Xenopus laevis. Bioessays. 1993 Feb;15(2):91–97. doi: 10.1002/bies.950150204. [DOI] [PubMed] [Google Scholar]
  119. Moon R. T., Miller J. R. The APC tumor suppressor protein in development and cancer. Trends Genet. 1997 Jul;13(7):256–258. doi: 10.1016/s0168-9525(97)01196-7. [DOI] [PubMed] [Google Scholar]
  120. Morin P. J., Sparks A. B., Korinek V., Barker N., Clevers H., Vogelstein B., Kinzler K. W. Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC. Science. 1997 Mar 21;275(5307):1787–1790. doi: 10.1126/science.275.5307.1787. [DOI] [PubMed] [Google Scholar]
  121. Munemitsu S., Albert I., Souza B., Rubinfeld B., Polakis P. Regulation of intracellular beta-catenin levels by the adenomatous polyposis coli (APC) tumor-suppressor protein. Proc Natl Acad Sci U S A. 1995 Mar 28;92(7):3046–3050. doi: 10.1073/pnas.92.7.3046. [DOI] [PMC free article] [PubMed] [Google Scholar]
  122. Munemitsu S., Souza B., Müller O., Albert I., Rubinfeld B., Polakis P. The APC gene product associates with microtubules in vivo and promotes their assembly in vitro. Cancer Res. 1994 Jul 15;54(14):3676–3681. [PubMed] [Google Scholar]
  123. Murai H., Okazaki M., Kikuchi A. Tyrosine dephosphorylation of glycogen synthase kinase-3 is involved in its extracellular signal-dependent inactivation. FEBS Lett. 1996 Aug 26;392(2):153–160. doi: 10.1016/0014-5793(96)00806-x. [DOI] [PubMed] [Google Scholar]
  124. Noordermeer J., Klingensmith J., Perrimon N., Nusse R. dishevelled and armadillo act in the wingless signalling pathway in Drosophila. Nature. 1994 Jan 6;367(6458):80–83. doi: 10.1038/367080a0. [DOI] [PubMed] [Google Scholar]
  125. Nusse R. A versatile transcriptional effector of Wingless signaling. Cell. 1997 May 2;89(3):321–323. doi: 10.1016/s0092-8674(00)80210-x. [DOI] [PubMed] [Google Scholar]
  126. Näthke I. S., Adams C. L., Polakis P., Sellin J. H., Nelson W. J. The adenomatous polyposis coli tumor suppressor protein localizes to plasma membrane sites involved in active cell migration. J Cell Biol. 1996 Jul;134(1):165–179. doi: 10.1083/jcb.134.1.165. [DOI] [PMC free article] [PubMed] [Google Scholar]
  127. Orsulic S., Peifer M. 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. 1996 Sep;134(5):1283–1300. doi: 10.1083/jcb.134.5.1283. [DOI] [PMC free article] [PubMed] [Google Scholar]
  128. Orsulic S., Peifer M. Cell-cell signalling: Wingless lands at last. Curr Biol. 1996 Nov 1;6(11):1363–1367. doi: 10.1016/s0960-9822(96)00731-2. [DOI] [PubMed] [Google Scholar]
  129. Otte A. P., Kramer I. M., Mannesse M., Lambrechts C., Durston A. J. Characterization of protein kinase C in early Xenopus embryogenesis. Development. 1990 Oct;110(2):461–470. doi: 10.1242/dev.110.2.461. [DOI] [PubMed] [Google Scholar]
  130. Otte A. P., Moon R. T. Protein kinase C isozymes have distinct roles in neural induction and competence in Xenopus. Cell. 1992 Mar 20;68(6):1021–1029. doi: 10.1016/0092-8674(92)90074-m. [DOI] [PubMed] [Google Scholar]
  131. Oyama T., Kanai Y., Ochiai A., Akimoto S., Oda T., Yanagihara K., Nagafuchi A., Tsukita S., Shibamoto S., Ito F. A truncated beta-catenin disrupts the interaction between E-cadherin and alpha-catenin: a cause of loss of intercellular adhesiveness in human cancer cell lines. Cancer Res. 1994 Dec 1;54(23):6282–6287. [PubMed] [Google Scholar]
  132. Pai L. M., Kirkpatrick C., Blanton J., Oda H., Takeichi M., Peifer M. Drosophila alpha-catenin and E-cadherin bind to distinct regions of Drosophila Armadillo. J Biol Chem. 1996 Dec 13;271(50):32411–32420. doi: 10.1074/jbc.271.50.32411. [DOI] [PubMed] [Google Scholar]
  133. Pai L. M., Orsulic S., Bejsovec A., Peifer M. Negative regulation of Armadillo, a Wingless effector in Drosophila. Development. 1997 Jun;124(11):2255–2266. doi: 10.1242/dev.124.11.2255. [DOI] [PubMed] [Google Scholar]
  134. Papkoff J., Brown A. M., Varmus H. E. The int-1 proto-oncogene products are glycoproteins that appear to enter the secretory pathway. Mol Cell Biol. 1987 Nov;7(11):3978–3984. doi: 10.1128/mcb.7.11.3978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  135. Papkoff J. Regulation of complexed and free catenin pools by distinct mechanisms. Differential effects of Wnt-1 and v-Src. J Biol Chem. 1997 Feb 14;272(7):4536–4543. [PubMed] [Google Scholar]
  136. Papkoff J., Rubinfeld B., Schryver B., Polakis P. Wnt-1 regulates free pools of catenins and stabilizes APC-catenin complexes. Mol Cell Biol. 1996 May;16(5):2128–2134. doi: 10.1128/mcb.16.5.2128. [DOI] [PMC free article] [PubMed] [Google Scholar]
  137. Parr B. A., McMahon A. P. Dorsalizing signal Wnt-7a required for normal polarity of D-V and A-P axes of mouse limb. Nature. 1995 Mar 23;374(6520):350–353. doi: 10.1038/374350a0. [DOI] [PubMed] [Google Scholar]
  138. Peifer M., Berg S., Reynolds A. B. A repeating amino acid motif shared by proteins with diverse cellular roles. Cell. 1994 Mar 11;76(5):789–791. doi: 10.1016/0092-8674(94)90353-0. [DOI] [PubMed] [Google Scholar]
  139. Peifer M. Beta-catenin as oncogene: the smoking gun. Science. 1997 Mar 21;275(5307):1752–1753. doi: 10.1126/science.275.5307.1752. [DOI] [PubMed] [Google Scholar]
  140. Peifer M., McCrea P. D., Green K. J., Wieschaus E., Gumbiner B. M. The vertebrate adhesive junction proteins beta-catenin and plakoglobin and the Drosophila segment polarity gene armadillo form a multigene family with similar properties. J Cell Biol. 1992 Aug;118(3):681–691. doi: 10.1083/jcb.118.3.681. [DOI] [PMC free article] [PubMed] [Google Scholar]
  141. Peifer M., Orsulic S., Pai L. M., Loureiro J. A model system for cell adhesion and signal transduction in Drosophila. Dev Suppl. 1993:163–176. [PubMed] [Google Scholar]
  142. Peifer M., Orsulic S., Sweeton D., Wieschaus E. A role for the Drosophila segment polarity gene armadillo in cell adhesion and cytoskeletal integrity during oogenesis. Development. 1993 Aug;118(4):1191–1207. doi: 10.1242/dev.118.4.1191. [DOI] [PubMed] [Google Scholar]
  143. Peifer M., Pai L. M., Casey M. Phosphorylation of the Drosophila adherens junction protein Armadillo: roles for wingless signal and zeste-white 3 kinase. Dev Biol. 1994 Dec;166(2):543–556. doi: 10.1006/dbio.1994.1336. [DOI] [PubMed] [Google Scholar]
  144. Peifer M. Regulating cell proliferation: as easy as APC. Science. 1996 May 17;272(5264):974–975. doi: 10.1126/science.272.5264.974. [DOI] [PubMed] [Google Scholar]
  145. Peifer M., Sweeton D., Casey M., Wieschaus E. wingless signal and Zeste-white 3 kinase trigger opposing changes in the intracellular distribution of Armadillo. Development. 1994 Feb;120(2):369–380. doi: 10.1242/dev.120.2.369. [DOI] [PubMed] [Google Scholar]
  146. Peifer M., Wieschaus E. The segment polarity gene armadillo encodes a functionally modular protein that is the Drosophila homolog of human plakoglobin. Cell. 1990 Dec 21;63(6):1167–1176. doi: 10.1016/0092-8674(90)90413-9. [DOI] [PubMed] [Google Scholar]
  147. Perrimon N. The genetic basis of patterned baldness in Drosophila. Cell. 1994 Mar 11;76(5):781–784. doi: 10.1016/0092-8674(94)90351-4. [DOI] [PubMed] [Google Scholar]
  148. Pierce S. B., Kimelman D. Regulation of Spemann organizer formation by the intracellular kinase Xgsk-3. Development. 1995 Mar;121(3):755–765. doi: 10.1242/dev.121.3.755. [DOI] [PubMed] [Google Scholar]
  149. Pizzuti A., Amati F., Calabrese G., Mari A., Colosimo A., Silani V., Giardino L., Ratti A., Penso D., Calzà L. cDNA characterization and chromosomal mapping of two human homologues of the Drosophila dishevelled polarity gene. Hum Mol Genet. 1996 Jul;5(7):953–958. doi: 10.1093/hmg/5.7.953. [DOI] [PubMed] [Google Scholar]
  150. Plyte S. E., Hughes K., Nikolakaki E., Pulverer B. J., Woodgett J. R. Glycogen synthase kinase-3: functions in oncogenesis and development. Biochim Biophys Acta. 1992 Dec 16;1114(2-3):147–162. doi: 10.1016/0304-419x(92)90012-n. [DOI] [PubMed] [Google Scholar]
  151. Polakis P. The adenomatous polyposis coli (APC) tumor suppressor. Biochim Biophys Acta. 1997 Jun 7;1332(3):F127–F147. doi: 10.1016/s0304-419x(97)00008-5. [DOI] [PubMed] [Google Scholar]
  152. Pollack A. L., Barth A. I., Altschuler Y., Nelson W. J., Mostov K. E. Dynamics of beta-catenin interactions with APC protein regulate epithelial tubulogenesis. J Cell Biol. 1997 Jun 30;137(7):1651–1662. doi: 10.1083/jcb.137.7.1651. [DOI] [PMC free article] [PubMed] [Google Scholar]
  153. Ponting C. P., Bork P. Pleckstrin's repeat performance: a novel domain in G-protein signaling? Trends Biochem Sci. 1996 Jul;21(7):245–246. [PubMed] [Google Scholar]
  154. Ramakrishna N. R., Brown A. M. Wingless, the Drosophila homolog of the proto-oncogene Wnt-1, can transform mouse mammary epithelial cells. Dev Suppl. 1993:95–103. [PubMed] [Google Scholar]
  155. Rattner A., Hsieh J. C., Smallwood P. M., Gilbert D. J., Copeland N. G., Jenkins N. A., Nathans J. A family of secreted proteins contains homology to the cysteine-rich ligand-binding domain of frizzled receptors. Proc Natl Acad Sci U S A. 1997 Apr 1;94(7):2859–2863. doi: 10.1073/pnas.94.7.2859. [DOI] [PMC free article] [PubMed] [Google Scholar]
  156. Reichsman F., Smith L., Cumberledge S. Glycosaminoglycans can modulate extracellular localization of the wingless protein and promote signal transduction. J Cell Biol. 1996 Nov;135(3):819–827. doi: 10.1083/jcb.135.3.819. [DOI] [PMC free article] [PubMed] [Google Scholar]
  157. Riese J., Yu X., Munnerlyn A., Eresh S., Hsu S. C., Grosschedl R., Bienz M. LEF-1, a nuclear factor coordinating signaling inputs from wingless and decapentaplegic. Cell. 1997 Mar 21;88(6):777–787. doi: 10.1016/s0092-8674(00)81924-8. [DOI] [PubMed] [Google Scholar]
  158. Rocheleau C. E., Downs W. D., Lin R., Wittmann C., Bei Y., Cha Y. H., Ali M., Priess J. R., Mello C. C. Wnt signaling and an APC-related gene specify endoderm in early C. elegans embryos. Cell. 1997 Aug 22;90(4):707–716. doi: 10.1016/s0092-8674(00)80531-0. [DOI] [PubMed] [Google Scholar]
  159. Rothbächer U., Laurent M. N., Blitz I. L., Watabe T., Marsh J. L., Cho K. W. Functional conservation of the Wnt signaling pathway revealed by ectopic expression of Drosophila dishevelled in Xenopus. Dev Biol. 1995 Aug;170(2):717–721. doi: 10.1006/dbio.1995.1249. [DOI] [PubMed] [Google Scholar]
  160. Rowning B. A., Wells J., Wu M., Gerhart J. C., Moon R. T., Larabell C. A. Microtubule-mediated transport of organelles and localization of beta-catenin to the future dorsal side of Xenopus eggs. Proc Natl Acad Sci U S A. 1997 Feb 18;94(4):1224–1229. doi: 10.1073/pnas.94.4.1224. [DOI] [PMC free article] [PubMed] [Google Scholar]
  161. Rubinfeld B., Albert I., Porfiri E., Fiol C., Munemitsu S., Polakis P. Binding of GSK3beta to the APC-beta-catenin complex and regulation of complex assembly. Science. 1996 May 17;272(5264):1023–1026. doi: 10.1126/science.272.5264.1023. [DOI] [PubMed] [Google Scholar]
  162. Rubinfeld B., Robbins P., El-Gamil M., Albert I., Porfiri E., Polakis P. Stabilization of beta-catenin by genetic defects in melanoma cell lines. Science. 1997 Mar 21;275(5307):1790–1792. doi: 10.1126/science.275.5307.1790. [DOI] [PubMed] [Google Scholar]
  163. Rubinfeld B., Souza B., Albert I., Munemitsu S., Polakis P. The APC protein and E-cadherin form similar but independent complexes with alpha-catenin, beta-catenin, and plakoglobin. J Biol Chem. 1995 Mar 10;270(10):5549–5555. doi: 10.1074/jbc.270.10.5549. [DOI] [PubMed] [Google Scholar]
  164. Rubinfeld B., Souza B., Albert I., Müller O., Chamberlain S. H., Masiarz F. R., Munemitsu S., Polakis P. Association of the APC gene product with beta-catenin. Science. 1993 Dec 10;262(5140):1731–1734. doi: 10.1126/science.8259518. [DOI] [PubMed] [Google Scholar]
  165. Ruel L., Bourouis M., Heitzler P., Pantesco V., Simpson P. Drosophila shaggy kinase and rat glycogen synthase kinase-3 have conserved activities and act downstream of Notch. Nature. 1993 Apr 8;362(6420):557–560. doi: 10.1038/362557a0. [DOI] [PubMed] [Google Scholar]
  166. Rulifson E. J., Blair S. S. Notch regulates wingless expression and is not required for reception of the paracrine wingless signal during wing margin neurogenesis in Drosophila. Development. 1995 Sep;121(9):2813–2824. doi: 10.1242/dev.121.9.2813. [DOI] [PubMed] [Google Scholar]
  167. Rulifson E. J., Micchelli C. A., Axelrod J. D., Perrimon N., Blair S. S. wingless refines its own expression domain on the Drosophila wing margin. Nature. 1996 Nov 7;384(6604):72–74. doi: 10.1038/384072a0. [DOI] [PubMed] [Google Scholar]
  168. Russell J., Gennissen A., Nusse R. Isolation and expression of two novel Wnt/wingless gene homologues in Drosophila. Development. 1992 Jun;115(2):475–485. doi: 10.1242/dev.115.2.475. [DOI] [PubMed] [Google Scholar]
  169. Saito Y., Vandenheede J. R., Cohen P. The mechanism by which epidermal growth factor inhibits glycogen synthase kinase 3 in A431 cells. Biochem J. 1994 Oct 1;303(Pt 1):27–31. doi: 10.1042/bj3030027. [DOI] [PMC free article] [PubMed] [Google Scholar]
  170. Sawa H., Lobel L., Horvitz H. R. 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. 1996 Sep 1;10(17):2189–2197. doi: 10.1101/gad.10.17.2189. [DOI] [PubMed] [Google Scholar]
  171. Schlessinger J., Lax I., Lemmon M. Regulation of growth factor activation by proteoglycans: what is the role of the low affinity receptors? Cell. 1995 Nov 3;83(3):357–360. doi: 10.1016/0092-8674(95)90112-4. [DOI] [PubMed] [Google Scholar]
  172. Schneider S., Steinbeisser H., Warga R. M., Hausen P. Beta-catenin translocation into nuclei demarcates the dorsalizing centers in frog and fish embryos. Mech Dev. 1996 Jul;57(2):191–198. doi: 10.1016/0925-4773(96)00546-1. [DOI] [PubMed] [Google Scholar]
  173. Schryver B., Hinck L., Papkoff J. Properties of Wnt-1 protein that enable cell surface association. Oncogene. 1996 Jul 18;13(2):333–342. [PubMed] [Google Scholar]
  174. Schweitzer R., Howes R., Smith R., Shilo B. Z., Freeman M. Inhibition of Drosophila EGF receptor activation by the secreted protein Argos. Nature. 1995 Aug 24;376(6542):699–702. doi: 10.1038/376699a0. [DOI] [PubMed] [Google Scholar]
  175. Seifert R. A., Hart C. E., Phillips P. E., Forstrom J. W., Ross R., Murray M. J., Bowen-Pope D. F. Two different subunits associate to create isoform-specific platelet-derived growth factor receptors. J Biol Chem. 1989 May 25;264(15):8771–8778. [PubMed] [Google Scholar]
  176. Semënov M. V., Snyder M. Human dishevelled genes constitute a DHR-containing multigene family. Genomics. 1997 Jun 1;42(2):302–310. doi: 10.1006/geno.1997.4713. [DOI] [PubMed] [Google Scholar]
  177. Shieh B. H., Zhu M. Y. Regulation of the TRP Ca2+ channel by INAD in Drosophila photoreceptors. Neuron. 1996 May;16(5):991–998. doi: 10.1016/s0896-6273(00)80122-1. [DOI] [PubMed] [Google Scholar]
  178. Shimamura K., Hirano S., McMahon A. P., Takeichi M. Wnt-1-dependent regulation of local E-cadherin and alpha N-catenin expression in the embryonic mouse brain. Development. 1994 Aug;120(8):2225–2234. doi: 10.1242/dev.120.8.2225. [DOI] [PubMed] [Google Scholar]
  179. Shimizu K., Kawabe H., Minami S., Honda T., Takaishi K., Shirataki H., Takai Y. SMAP, an Smg GDS-associating protein having arm repeats and phosphorylated by Src tyrosine kinase. J Biol Chem. 1996 Oct 25;271(43):27013–27017. doi: 10.1074/jbc.271.43.27013. [DOI] [PubMed] [Google Scholar]
  180. Siegfried E., Chou T. B., Perrimon N. wingless signaling acts through zeste-white 3, the Drosophila homolog of glycogen synthase kinase-3, to regulate engrailed and establish cell fate. Cell. 1992 Dec 24;71(7):1167–1179. doi: 10.1016/s0092-8674(05)80065-0. [DOI] [PubMed] [Google Scholar]
  181. Siegfried E., Wilder E. L., Perrimon N. Components of wingless signalling in Drosophila. Nature. 1994 Jan 6;367(6458):76–80. doi: 10.1038/367076a0. [DOI] [PubMed] [Google Scholar]
  182. Slusarski D. C., Yang-Snyder J., Busa W. B., Moon R. T. Modulation of embryonic intracellular Ca2+ signaling by Wnt-5A. Dev Biol. 1997 Feb 1;182(1):114–120. doi: 10.1006/dbio.1996.8463. [DOI] [PubMed] [Google Scholar]
  183. Smith K. J., Levy D. B., Maupin P., Pollard T. D., Vogelstein B., Kinzler K. W. Wild-type but not mutant APC associates with the microtubule cytoskeleton. Cancer Res. 1994 Jul 15;54(14):3672–3675. [PubMed] [Google Scholar]
  184. Smolich B. D., McMahon J. A., McMahon A. P., Papkoff J. Wnt family proteins are secreted and associated with the cell surface. Mol Biol Cell. 1993 Dec;4(12):1267–1275. doi: 10.1091/mbc.4.12.1267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  185. Sokol S. Y. Analysis of Dishevelled signalling pathways during Xenopus development. Curr Biol. 1996 Nov 1;6(11):1456–1467. doi: 10.1016/s0960-9822(96)00750-6. [DOI] [PubMed] [Google Scholar]
  186. Sokol S. Y., Klingensmith J., Perrimon N., Itoh K. Dorsalizing and neuralizing properties of Xdsh, a maternally expressed Xenopus homolog of dishevelled. Development. 1995 Jun;121(6):1637–1647. doi: 10.1242/dev.121.6.1637. [DOI] [PubMed] [Google Scholar]
  187. Stambolic V., Ruel L., Woodgett J. R. Lithium inhibits glycogen synthase kinase-3 activity and mimics wingless signalling in intact cells. Curr Biol. 1996 Dec 1;6(12):1664–1668. doi: 10.1016/s0960-9822(02)70790-2. [DOI] [PubMed] [Google Scholar]
  188. Stark K., Vainio S., Vassileva G., McMahon A. P. Epithelial transformation of metanephric mesenchyme in the developing kidney regulated by Wnt-4. Nature. 1994 Dec 15;372(6507):679–683. doi: 10.1038/372679a0. [DOI] [PubMed] [Google Scholar]
  189. Steitz S. A., Tsang M., Sussman D. J. Wnt-mediated relocalization of dishevelled proteins. In Vitro Cell Dev Biol Anim. 1996 Jul-Aug;32(7):441–445. doi: 10.1007/BF02723007. [DOI] [PubMed] [Google Scholar]
  190. Strader C. D., Fong T. M., Tota M. R., Underwood D., Dixon R. A. Structure and function of G protein-coupled receptors. Annu Rev Biochem. 1994;63:101–132. doi: 10.1146/annurev.bi.63.070194.000533. [DOI] [PubMed] [Google Scholar]
  191. Strutt D. I., Weber U., Mlodzik M. The role of RhoA in tissue polarity and Frizzled signalling. Nature. 1997 May 15;387(6630):292–295. doi: 10.1038/387292a0. [DOI] [PubMed] [Google Scholar]
  192. Su L. K., Burrell M., Hill D. E., Gyuris J., Brent R., Wiltshire R., Trent J., Vogelstein B., Kinzler K. W. APC binds to the novel protein EB1. Cancer Res. 1995 Jul 15;55(14):2972–2977. [PubMed] [Google Scholar]
  193. Su L. K., Vogelstein B., Kinzler K. W. Association of the APC tumor suppressor protein with catenins. Science. 1993 Dec 10;262(5140):1734–1737. doi: 10.1126/science.8259519. [DOI] [PubMed] [Google Scholar]
  194. Sussman D. J., Klingensmith J., Salinas P., Adams P. S., Nusse R., Perrimon N. Isolation and characterization of a mouse homolog of the Drosophila segment polarity gene dishevelled. Dev Biol. 1994 Nov;166(1):73–86. doi: 10.1006/dbio.1994.1297. [DOI] [PubMed] [Google Scholar]
  195. Takada S., Stark K. L., Shea M. J., Vassileva G., McMahon J. A., McMahon A. P. Wnt-3a regulates somite and tailbud formation in the mouse embryo. Genes Dev. 1994 Jan;8(2):174–189. doi: 10.1101/gad.8.2.174. [DOI] [PubMed] [Google Scholar]
  196. Theisen H., Purcell J., Bennett M., Kansagara D., Syed A., Marsh J. L. dishevelled is required during wingless signaling to establish both cell polarity and cell identity. Development. 1994 Feb;120(2):347–360. doi: 10.1242/dev.120.2.347. [DOI] [PubMed] [Google Scholar]
  197. Thorpe C. J., Schlesinger A., Carter J. C., Bowerman B. Wnt signaling polarizes an early C. elegans blastomere to distinguish endoderm from mesoderm. Cell. 1997 Aug 22;90(4):695–705. doi: 10.1016/s0092-8674(00)80530-9. [DOI] [PubMed] [Google Scholar]
  198. Torres M. A., Yang-Snyder J. A., Purcell S. M., DeMarais A. A., McGrew L. L., Moon R. T. 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. 1996 Jun;133(5):1123–1137. doi: 10.1083/jcb.133.5.1123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  199. Treisman J. E., Luk A., Rubin G. M., Heberlein U. eyelid antagonizes wingless signaling during Drosophila development and has homology to the Bright family of DNA-binding proteins. Genes Dev. 1997 Aug 1;11(15):1949–1962. doi: 10.1101/gad.11.15.1949. [DOI] [PMC free article] [PubMed] [Google Scholar]
  200. Tsukamoto A. S., Grosschedl R., Guzman R. C., Parslow T., Varmus H. E. Expression of the int-1 gene in transgenic mice is associated with mammary gland hyperplasia and adenocarcinomas in male and female mice. Cell. 1988 Nov 18;55(4):619–625. doi: 10.1016/0092-8674(88)90220-6. [DOI] [PubMed] [Google Scholar]
  201. Tsunoda S., Sierralta J., Sun Y., Bodner R., Suzuki E., Becker A., Socolich M., Zuker C. S. A multivalent PDZ-domain protein assembles signalling complexes in a G-protein-coupled cascade. Nature. 1997 Jul 17;388(6639):243–249. doi: 10.1038/40805. [DOI] [PubMed] [Google Scholar]
  202. Verbeek S., Izon D., Hofhuis F., Robanus-Maandag E., te Riele H., van de Wetering M., Oosterwegel M., Wilson A., MacDonald H. R., Clevers H. An HMG-box-containing T-cell factor required for thymocyte differentiation. Nature. 1995 Mar 2;374(6517):70–74. doi: 10.1038/374070a0. [DOI] [PubMed] [Google Scholar]
  203. Vider B. Z., Zimber A., Chastre E., Prevot S., Gespach C., Estlein D., Wolloch Y., Tronick S. R., Gazit A., Yaniv A. Evidence for the involvement of the Wnt 2 gene in human colorectal cancer. Oncogene. 1996 Jan 4;12(1):153–158. [PubMed] [Google Scholar]
  204. Vinson C. R., Conover S., Adler P. N. A Drosophila tissue polarity locus encodes a protein containing seven potential transmembrane domains. Nature. 1989 Mar 16;338(6212):263–264. doi: 10.1038/338263a0. [DOI] [PubMed] [Google Scholar]
  205. Vleminckx K., Wong E., Guger K., Rubinfeld B., Polakis P., Gumbiner B. M. Adenomatous polyposis coli tumor suppressor protein has signaling activity in Xenopus laevis embryos resulting in the induction of an ectopic dorsoanterior axis. J Cell Biol. 1997 Jan 27;136(2):411–420. doi: 10.1083/jcb.136.2.411. [DOI] [PMC free article] [PubMed] [Google Scholar]
  206. Wagner U., Brownlees J., Irving N. G., Lucas F. R., Salinas P. C., Miller C. C. Overexpression of the mouse dishevelled-1 protein inhibits GSK-3beta-mediated phosphorylation of tau in transfected mammalian cells. FEBS Lett. 1997 Jul 14;411(2-3):369–372. doi: 10.1016/s0014-5793(97)00733-3. [DOI] [PubMed] [Google Scholar]
  207. Wang Q. M., Fiol C. J., DePaoli-Roach A. A., Roach P. J. Glycogen synthase kinase-3 beta is a dual specificity kinase differentially regulated by tyrosine and serine/threonine phosphorylation. J Biol Chem. 1994 May 20;269(20):14566–14574. [PubMed] [Google Scholar]
  208. Wang S., Krinks M., Lin K., Luyten F. P., Moos M., Jr Frzb, a secreted protein expressed in the Spemann organizer, binds and inhibits Wnt-8. Cell. 1997 Mar 21;88(6):757–766. doi: 10.1016/s0092-8674(00)81922-4. [DOI] [PubMed] [Google Scholar]
  209. Wang Y., Macke J. P., Abella B. S., Andreasson K., Worley P., Gilbert D. J., Copeland N. G., Jenkins N. A., Nathans J. A large family of putative transmembrane receptors homologous to the product of the Drosophila tissue polarity gene frizzled. J Biol Chem. 1996 Feb 23;271(8):4468–4476. doi: 10.1074/jbc.271.8.4468. [DOI] [PubMed] [Google Scholar]
  210. Welsh G. I., Foulstone E. J., Young S. W., Tavaré J. M., Proud C. G. Wortmannin inhibits the effects of insulin and serum on the activities of glycogen synthase kinase-3 and mitogen-activated protein kinase. Biochem J. 1994 Oct 1;303(Pt 1):15–20. doi: 10.1042/bj3030015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  211. Wilder E. L., Perrimon N. Dual functions of wingless in the Drosophila leg imaginal disc. Development. 1995 Feb;121(2):477–488. doi: 10.1242/dev.121.2.477. [DOI] [PubMed] [Google Scholar]
  212. Willert K., Brink M., Wodarz A., Varmus H., Nusse R. Casein kinase 2 associates with and phosphorylates dishevelled. EMBO J. 1997 Jun 2;16(11):3089–3096. doi: 10.1093/emboj/16.11.3089. [DOI] [PMC free article] [PubMed] [Google Scholar]
  213. Wong G. T., Gavin B. J., McMahon A. P. Differential transformation of mammary epithelial cells by Wnt genes. Mol Cell Biol. 1994 Sep;14(9):6278–6286. doi: 10.1128/mcb.14.9.6278. [DOI] [PMC free article] [PubMed] [Google Scholar]
  214. Wylie C., Kofron M., Payne C., Anderson R., Hosobuchi M., Joseph E., Heasman J. Maternal beta-catenin establishes a 'dorsal signal' in early Xenopus embryos. Development. 1996 Oct;122(10):2987–2996. doi: 10.1242/dev.122.10.2987. [DOI] [PubMed] [Google Scholar]
  215. Yanagawa S., van Leeuwen F., Wodarz A., Klingensmith J., Nusse R. The dishevelled protein is modified by wingless signaling in Drosophila. Genes Dev. 1995 May 1;9(9):1087–1097. doi: 10.1101/gad.9.9.1087. [DOI] [PubMed] [Google Scholar]
  216. Yang-Snyder J., Miller J. R., Brown J. D., Lai C. J., Moon R. T. A frizzled homolog functions in a vertebrate Wnt signaling pathway. Curr Biol. 1996 Oct 1;6(10):1302–1306. doi: 10.1016/s0960-9822(02)70716-1. [DOI] [PubMed] [Google Scholar]
  217. Yang S. D., Yu J. S., Wen Z. D. Tumor promoter phorbol ester reversibly modulates tyrosine dephosphorylation/inactivation of protein kinase FA/GSK-3 alpha in A431 cells. J Cell Biochem. 1994 Dec;56(4):550–558. doi: 10.1002/jcb.240560416. [DOI] [PubMed] [Google Scholar]
  218. Yoffe K. B., Manoukian A. S., Wilder E. L., Brand A. H., Perrimon N. Evidence for engrailed-independent wingless autoregulation in Drosophila. Dev Biol. 1995 Aug;170(2):636–650. doi: 10.1006/dbio.1995.1243. [DOI] [PubMed] [Google Scholar]
  219. Yost C., Torres M., Miller J. R., Huang E., Kimelman D., Moon R. T. The axis-inducing activity, stability, and subcellular distribution of beta-catenin is regulated in Xenopus embryos by glycogen synthase kinase 3. Genes Dev. 1996 Jun 15;10(12):1443–1454. doi: 10.1101/gad.10.12.1443. [DOI] [PubMed] [Google Scholar]
  220. Yu J. S., Yang S. D. Okadaic acid, a serine/threonine phosphatase inhibitor, induces tyrosine dephosphorylation/inactivation of protein kinase FA/GSK-3 alpha in A431 cells. J Biol Chem. 1994 May 20;269(20):14341–14344. [PubMed] [Google Scholar]
  221. Zecca M., Basler K., Struhl G. Direct and long-range action of a wingless morphogen gradient. Cell. 1996 Nov 29;87(5):833–844. doi: 10.1016/s0092-8674(00)81991-1. [DOI] [PubMed] [Google Scholar]
  222. Zeng L., Fagotto F., Zhang T., Hsu W., Vasicek T. J., Perry W. L., 3rd, Lee J. J., Tilghman S. M., Gumbiner B. M., Costantini F. The mouse Fused locus encodes Axin, an inhibitor of the Wnt signaling pathway that regulates embryonic axis formation. Cell. 1997 Jul 11;90(1):181–192. doi: 10.1016/s0092-8674(00)80324-4. [DOI] [PubMed] [Google Scholar]
  223. Zhou J., Liyanage U., Medina M., Ho C., Simmons A. D., Lovett M., Kosik K. S. Presenilin 1 interaction in the brain with a novel member of the Armadillo family. Neuroreport. 1997 Apr 14;8(6):1489–1494. doi: 10.1097/00001756-199704140-00033. [DOI] [PubMed] [Google Scholar]
  224. ten Dijke P., Miyazono K., Heldin C. H. Signaling via hetero-oligomeric complexes of type I and type II serine/threonine kinase receptors. Curr Opin Cell Biol. 1996 Apr;8(2):139–145. doi: 10.1016/s0955-0674(96)80058-5. [DOI] [PubMed] [Google Scholar]
  225. van Genderen C., Okamura R. M., Fariñas I., Quo R. G., Parslow T. G., Bruhn L., Grosschedl R. Development of several organs that require inductive epithelial-mesenchymal interactions is impaired in LEF-1-deficient mice. Genes Dev. 1994 Nov 15;8(22):2691–2703. doi: 10.1101/gad.8.22.2691. [DOI] [PubMed] [Google Scholar]
  226. van Leeuwen F., Samos C. H., Nusse R. Biological activity of soluble wingless protein in cultured Drosophila imaginal disc cells. Nature. 1994 Mar 24;368(6469):342–344. doi: 10.1038/368342a0. [DOI] [PubMed] [Google Scholar]
  227. van de Wetering M., Cavallo R., Dooijes D., van Beest M., van Es J., Loureiro J., Ypma A., Hursh D., Jones T., Bejsovec A. Armadillo coactivates transcription driven by the product of the Drosophila segment polarity gene dTCF. Cell. 1997 Mar 21;88(6):789–799. doi: 10.1016/s0092-8674(00)81925-x. [DOI] [PubMed] [Google Scholar]
  228. van den Heuvel M., Ingham P. W. smoothened encodes a receptor-like serpentine protein required for hedgehog signalling. Nature. 1996 Aug 8;382(6591):547–551. doi: 10.1038/382547a0. [DOI] [PubMed] [Google Scholar]
  229. van den Heuvel M., Klingensmith J., Perrimon N., Nusse R. Cell patterning in the Drosophila segment: engrailed and wingless antigen distributions in segment polarity mutant embryos. Dev Suppl. 1993:105–114. [PubMed] [Google Scholar]

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