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

Journal of Cell Biology

Volumn 133, Issue 5, 1996, Pages 1123-1137

  Torres, Monica A ^a   Yang Snyder, Julia A ^a   Purcell, Susan M ^a   DeMarais, Alyce A ^a,c   McGrew, L Lynn ^a   Moon, Randall T ^a,b  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c UNIVERSITY OF OKLAHOMA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CADHERIN; GENE PRODUCT;

ANIMAL TISSUE; ARTICLE; CELL ADHESION; CELL AGGREGATION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; GENE INDUCTION; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALS; BETA CATENIN; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CADHERINS; CYTOSKELETAL PROTEINS; FEMALE; GLYCOGEN SYNTHASE KINASE 3; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MICROINJECTIONS; PROTEIN SORTING SIGNALS; PROTO-ONCOGENE PROTEINS; RNA; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS; WNT PROTEINS; WNT1 PROTEIN; XENOPUS LAEVIS; XENOPUS PROTEINS; ZEBRAFISH PROTEINS;

ANIMALIA; CHRISTIA; STAPHYLOCOCCUS PHAGE 3A; VERTEBRATA;

EID: 0029939701     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.133.5.1123     Document Type: Article

References (67)

1. Behrens, J., L. Vakael, R. Friis, E. Winterhager, F. Van-Roy, M.M. Marcel, and W. Birchmeier. 1993. Loss of epithelial differentiation and gain of invasiveness correlates with tyrosine phosphorylation of E-cadherin/β-catenin complex in cells transformed with a temperature-sensitive v-SRC gene. J. Cell Biol. 120:757-766.
2. Bradley, R.S., P. Cowin, and A.M. Brown. 1993. Expression of Wnt-1 in PC12 cells results in modulation of plakoglobin and E-cadherin and increased cellular adhesion. J. Cell Biol. 123:1857-1865.
3. Brieher, W.M., and B.M. Gumbiner. 1994. Regulation of C-cadherin function during activin induced morphogenesis of Xenopus animal caps. J. Cell Biol. 126:519-527.
4. Cho, K.W., E.A. Morita, C.V. Wright, and E.M. De Robertis. 1991. Overexpression of a homeodomain protein confers axis-forming activity to uncommitted Xenopus embryonic cells. Cell. 65:55-64.
5. Chomczynski, P., and N. Sacchi. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Analyt. Biochem. 162:156-159.
6. Christian, J.L., and R.T. Moon. 1993. Interactions between Xwnt-8 and Spemann organizer signaling pathways generate dorsoventral pattern in the embryonic mesoderm of Xenopus. Genes & Dev. 7:13-28.
7. Christian. J.L., J.A. McMahon, A.P. McMahon, and R.T. Moon. 1991. Xwnt-8, a Xenopus Wnt-1/int-1-related gene responsive to mesoderm inducing factors, may play a role in ventral mesodermal patterning during embryogenesis. Development (Camb.). 111:1045-1056.
8. Cui, Y., J.D. Brown, R.T. Moon, and J.L. Christian. 1995. Xwnt-Sb: maternally expressed Xenopus Win gene with potential role in establishing the dorsoventral axis. Development (Camb.). 121:2177-2186.
9. Dealy, C.N., A. Roth, D. Ferrari, A.A. Brown, and R.A. Kosher. 1993. Wnt-5a and Wnt-7a are expressed in the developing chick limb bud in a manner suggesting roles in pattern formation along the proximodistal and dorsoventral axes. Mech. Dev. 43:175-186.
10. Detrick, R.J., D. Dickey, and C.R. Kintner. 1990. The effects of N-cadherin misexpression on morphogenesis in Xenopus embryos, Neuron. 4:493-506.
11. Dominguez, I., K. Itoh, and S.V. Sokol. 1995. Role of glycogen synthase kinase as a negative regulator of dorsoventral axis formation in Xenopus embryos. Proc. Natl. Acad. Sci. USA., 92:8498-8502.
12. Du, S., S. Purcell, J. Christian, L. McGrew, and R. Moon. 1995. Identification of distinct classes and functional domains of Wnts through expression of wildtype and chimeric proteins in Xenopus embryos. Mol. Cell. Biol. 15:262526.34.
13. Fujimori, T., S. Miyatani, and M. Takeichi. 1990. Ectopic expression of N-cadherin perturbs histogenesis in Xenopus embryos. Development (Camb.). 110:97-104.
14. Funayama, N., F. Fagotto, P. McCrea, and B.M. Gumhiner. 1995. Embryonic axis induction by the armadillo repeat domain of β-catenin: evidence for intracellularsignaling./ Cell Biol. 128:959-968.
15. Guger, K.A., and B.M. Gumbiner. 1995. β-catenin has Wnt-like activity and mimics the Nieuwkoop signaling center in Xenopus dorsal-ventral patterning. Dev. Biol. 172:115-125.
16. Hamaguchi, M., N. Matsuyoshi, Y. Ohnishi, B. Gotoh, M. Takeichi. and Y. Nagai. 1993. p60v-src causes tyrosine phosphorylalion and inactivation of the N-cadherin-catenin cell adhesion system. EMBO (Eur. Mol. Biol. Organ.) J. 12:307-314.
17. Harland, R.M. 1991. In situ hybridization: an improved whole mount method for Xenopus embryos. In Methods in Cell Biology, B.K. Kay, and H.J. Peng, editors. Academic Press Inc., San Diego. 685-695.
18. He, X., J.-P Saint-Jeannet. J.R. Woodgetl, H.E. Varmus, and I. Dawid. 1995. Glycogen synthase kinase-3 and dorsovenlral patterning in Xenopus embryos. Nature (Lond.). 374:617-622.
19. Heasman, J., A. Crawford, K. Goldstone, P. Garner Hamrick, B. Gumbiner, P. McCrea, C. Kintner, C.Y. Noro, and C. Wylie. 1994. Overexpression of cadherins and underexpression of β-catenin inhibit dorsal mesoderm induction in early Xenopus embryos. Cell. 79:791-803.
20. Hemmati-Brivanlou, A., O.G. Kelly, and D.A. Melton. 1994. Follistatin, an antagonist of activin. is expressed in the Spemann organizer and displays direct neuralizing activity. Cell. 77:283-295.
21. Hinck, L., W.J. Nelson, and J. Papkoff 1994. Wnt-1 modulates cell-cell adhesion in mammalian cells by stabilizing β-catenin binding to the cell adhesion protein cadherin. J. Cell Biol. 124:729-741.
22. Holt, C.E., P. Lemaire, and J.B. Gurdon. 1994. Cadherin-mediated cell interactions are necessary for the activation of MyoD in Xenopus mesoderm. Proc. Natl. Acad. Sci. USA. 91:10844-10848.
23. Huguet, E.L., J.A. McMahon, A.P. McMahon, R. Bicknell, and A.L. Harris. 1994. Differential expression of human Wnt genes 2, 3, 4, and 7B in human breast cell lines and normal and disease stales of human breast tissue. Cancer Res. 54:2615-2621.
24. Huguet, E.L., K. Smith, R. Bicknell, and A.L. Harris. 1995. Regulation of Wnt5a mRNA expression in human mammary epithelial cells by cell shape, confluence, and hepatocyte growth factor./. Biol. Chem. 270:12851-12856.
25. Keller, R. 1991. Early embryonic development of Xenopus laevis. Methods Cell Biol. 36:61-113.
26. Kelly. G.M., P.E. Greenstein, D.F. Erezyilmaz, and R.T. Moon. 1995. Zebrafish wnt8 and wnt8b share a common activity but are involved in distinct developmental pathways. Development (Camb.). 121:1787-1799.
27. Kessler, D.S., and D.A. Melton. 1995. Induction of dorsal mesoderm by soluble, mature Vg1 protein. Development (Camb.). 121:2155-2164.
28. Kintner, C. 1992. Regulation of embryonic cell adhesion by the cadherin cytoplasmic domain. Cell. 69:225-236.
29. Klar, A., M. Baldassare, and T.M. Jessel. 1992. F-spondin: a gene expressed at high levels in the floor plate encodes a secreted protein that promotes neural cell adhesion and neurite extension. Cell. 69:95-110.
30. Klingensmith, J., E. Noll, and N. Perrimon. 1989. The segment polarity phenotype of Drosophila involves differential tendencies toward transformation and cell death. Dev. Biol. 134:130-145.
31. Klingensmith, J., R. Nusse, and N. Perrimon. 1994. The Drosophila segment polarity gene dishevelled encodes a novel protein required for response to the wingless signal. Genes & Dev. 8:118-130.
32. Koster, J.G., K. Eizema, L.J. Peterson-Maduro, B.I. Stegeman, and O.H.J. Destree. 1996. Analysis of Wnt/Engrailed signaling in Xenopus embryos using biolistics. Dev. Biol. 173:348-352.
33. Krieg, P., and D. Melton. 1984. Functional messenger RNAs are produced by SP6 in vitro transcription of cloned DNAs. Nucleic Acids Res. 12:7057-7070.
34. Ku, M., and D.A. Melton. 1993. Xwnt-11: a maternally expressed Xenopus Wnt gene. Development (Camb.). 119:1161-1173.
35. Lamb, M.T., A. Knecht, W.C. Smith, S.E. Stachel, A.N. Economides, N. Stahl, G.D. Yancopolous, and R. Harland. 1993. Neural induction by the secreted polypeptide noggin. Science (Wash. DC). 262:713-718.
36. Levine, E., C.H. Lee, C. Kintner, and B.M. Gumbiner. 1994. Selective disruption of E-cadherin function in early Xenopus embryos by a dominant negative mutant. Development (Camb.). 120:901-910.
37. Matsuyoshi, N., M. Hamaguchi, S. Taniguchi, A. Nagafuchi, S. Tsukita, and M. Takeichi. 1992. Cadherin-mediated cell-cell adhesion is perturbed by v-src tyrosine phosphorylation in metastatic fibroblasts. J. Cell Biol. 118:703-714.
38. McCrea, P.D., C.W. Turck, and B. Gumbiner. 1991. A homolog of armadillo protein in Drosophila (plakoglobin) associated with E-cadherin. Science (Wash. DC). 254:1359-1361.
39. McGrew, L.L., A.P. Otte, and R.T. Moon. 1992. Analysis of Xwnt-4 in embryos of Xenopus laevis: a Wnt family member expressed in the brain and floor-plate. Development (Camb.). 115:463-473.
40. McMahon, A.P. 1992. The Wnt family of developmental regulators. Trends Genet. 8:1-5.
41. Moon, R.T. 1993. In pursuit of the functions of the Wnt family of developmental regulators: insights from Xenopus laevis. Bioessays. 15:91-97.
42. Moon, R.T., and J.L. Christian. 1989. Microinjection and expression of synthetic mRNAs in Xenopus: embryos. Technique (Phila.). 1:76-89.
43. Moon, R.T., R.M. Campbell, J.L. Christian, L.L. McGrew, J. Shih, and S. Fraser. 1993. Xwnt-5A: a maternal Wnt that affects morphogenetic movements after overexpression in embryos of Xenopus laevis. Development (Camb.). 119:97-111.
44. Moon, R.T., J.L. Christian, R.M. Campbell, L.L. McGrew, A.A. DeMarais, M. Torres, C.J. Lai, D.J. Olson, and G.M. Kelly. 19936. Dissecting Wnt signaling pathways and Wnt-sensitive developmental processes through transient misexpression analyses in embryos of Xenopus laevis. Dev. Suppl. 85-94.
45. Nagafuchi, A., and M. Takeichi. 1989. Transmembrane control of cadherinmediated cell adhesion: a 94 KDa protein functionally associated with a specific region of the cytoplasmic domain of E-cadherin. Cell Regul. 1:37-44.
46. Noordermeer, J., J. Klingensmith, N. Perrimon, and R. Nusse. 1994. dishevelled and armadillo act in the wingless signaling pathway in Drosophila. Nature (Lond.). 367:80-83.
47. Nusse, R., and H.E. Varmus. 1992. Wnt genes. Cell. 69:1073-1087.
48. Ozawa, M., H. Baribault, and R. Kemler. 1989. The cytoplasmic domain of the cell adhesion molecule uvomorulin associates with three Independent proteins structurally related in different species. EMBO (Eur. Mol. Biol. Organ.) J. 8:1711-1717.
49. Parr, B.A., M.J. Shea, G. Vassileva, and A.P. McMahon. 1993. Mouse Will genes exhibit discrete domains of expression in the early embryonic CNS and limb buds. Development (Camb.). 119:247-261.
50. Peifer, M., and Wieschaus, E. 1990. The segment polarity gene armadillo encodes a functionally modular protein that is the Drosophila homolog of human plakoglobin. Cell. 63:1167-1176.
51. Pierce, S.B., and D. Kimelman. 1995. Regulation of Spemann organizer formation by the intracellular kinase Xgsk-3. Development (Camb.). 121:755-765.
52. Riddle, R.D., M. Ensini, C. Nelson, T. Tsuchida, T.M. Jessel, and C. Tabin. 1995. Induction of the Lim homeobox gene Lmxl by Wnt7a establishes dorsoventral pattern in the vertebrate limb. Cell. 83:631-640.
53. Riggleman, B., P. Schedl, and E. Wieschaus. 1990. Spatial expression of the Drosophila segment polarity gene armadillo is posttranscriptionally regulated by wingless. Cell. 63:549-560.
54. Rijsewijk, F., M. Schuermann, E. Wagenaar, P. Parren, D. Weigel, and R. Nusse. 1987. The Drosophila homolog of the mouse mammary oncogene int-1 is identical to the segment polarity gene wingless. Cell. 50:649-657.
55. Sanes, J.R., J.L.R. Rubenstein, and J.-F. Nicolas. 1986. Use of a recombinant retrovirus to study post-implantation cell lineage in mouse embryos. EMBO (Eur. Mol. Biol. Organ.) J. 12:3133-3142.
56. Sater, A.K., R.A. Steinhardt, and R. Keller. 1993. Induction of neuronal differentiation by planar signals in Xenopus embryos. Dev. Dyn. 197:268-280.
57. Siegfried, E., T.B. Chou, and N. Perrimon. 1992. Wingless signaling acts through zeste-white 3, the Drosophila homolog of glycogen synthase kinase-3, to regulate engrailed and establish cell fate. Cell. 71:1167-1179.
58. Smith, J.C., B.M.J. Price, J.B.A. Green, D. Weigel, and B.C. Herrmann. 1991. Expression of a Xenopus homolog of brachyury (T) is an immediate-early response to mesoderm induction. Cell. 67:79-87.
59. Smith, W.C., and R.M. Harland. 1991. Injected Xwnt-K acts early in Xenopus embryos to promote formation of a vegetal dorsalizing center. Cell 67:753-766.
60. Sokol, S., J.L. Christian. R.T. Moon, and D.A. Melton. 1991. Injected Wnt RNA induces a complete body axis in Xenopus embryos. Cell. 67:741-752.
61. Sokol, S.V., J. Klingensmith, N. Perrimon, and K. Itoh. 1995. Dorsalizing and neuralizing properties of Xdsh, a maternally expressed Xenopus homolog of dishevelled. Development (Camb.). 121:1637-1647.
62. Takada, S., K.L. Stark, M.J. Shea, G. Vassileva, J.A. McMahon, and A.P. McMahon. 1994. Wnt-3a regulates somite and tailbud formation in the mouse embryo. Genes & Dev. 8:174-189.
63. Theisen, H., J. Purcell, M. Bennet, D. Kansagara, A. Syed, and J.L. Marsh. 1994. Dishevelled is required during wingless signaling to establish both cell polarity and cell identity. Development (Camb.). 120:347-360.
64. Thomsen, G.H., and D.A. Melton. 1993. Processed Vg1 protein is an axial mesoderm inducer in Xenopus. Cell. 74:433-441.
65. Ungar, A.R., G.M. Kelly, and R.T. Moon. 1995. Wnt-4 affects morphogenesis when misexpressed in the zebrafish embryo. Mech. Dev. 52:1-12.
66. Wolda, S.L., C.J. Moody, and R.T. Moon. 1993. Overlapping expression of Xwnt-3A and Xwnt-1 in neural tissue of Xenopus laevis embryos. Dev. Biol. 155:46-57.
67. Wong, G.T., B.J. Gavin, and A.P. McMahon. 1994. Differential transformation of mammary epithelial cells by Wnt genes. Mol Cell. Biol. 14:6278-6286.