Wnt signaling in Xenopus embryos inhibits Bmp4 expression and activates neural development

Genes and Development

Volumn 13, Issue 23, 1999, Pages 3149-3159

  Baker, Julie C ^a   Beddington, Rosa S P ^b   Harland, Richard M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

catenin; Bmp4; Mouse; Neural induction; Nieuwkoop; Wnts

Indexed keywords

BETA CATENIN; BONE MORPHOGENETIC PROTEIN; CASEIN KINASE; TRANSCRIPTION FACTOR;

ARTICLE; ECTODERM; EMBRYO; EMBRYO DEVELOPMENT; GENE EXPRESSION; GENE INDUCTION; GENE REPRESSION; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; XENOPUS;

ANIMALS; BETA CATENIN; BONE MORPHOGENETIC PROTEINS; CARRIER PROTEINS; CYTOSKELETAL PROTEINS; ECTODERM; EMBRYO, NONMAMMALIAN; EMBRYONIC AND FETAL DEVELOPMENT; EMBRYONIC INDUCTION; FETAL PROTEINS; GASTRULA; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; IN SITU HYBRIDIZATION; MICE; NERVE TISSUE PROTEINS; NERVOUS SYSTEM; PROTEINS; PROTO-ONCOGENE PROTEINS; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; RIBONUCLEOPROTEINS; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS; TRANSFORMING GROWTH FACTOR BETA; WNT PROTEINS; XENOPUS LAEVIS; XENOPUS PROTEINS; ZEBRAFISH PROTEINS;

VERTEBRATA;

EID: 0033397682     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.13.23.3149     Document Type: Article

References (92)

1. Axelrod, J.D., J.R. Miller, J.M. Shulman, R.T. Moon, and N. Perrimon. 1998. Differential recruitment of Dishevelled provides signaling specificity in the planar cell polarity and Wingless signaling pathways. Genes & Dev. 12: 2610-2622.
2. Baker, J.C. and R.M. Harland. 1996. A novel mesoderm inducer, Madr2, functions in the activin signal transduction pathway. Genes & Dev. 10: 1880-1889.
3. Bejsovec, A. and E. Wieschaus. 1995. Signaling activities of the Drosophila wingless gene are separately mutable and appear to be transduced at the cell surface. Genetics 139: 309-320.
4. Belo, J.A., T. Bouwmeester, L. Leyns, N. Kertesz, M. Gallo, M. Follettie, and E.M. De Robertis. 1997. Cerberus-like is a secreted factor with neutralizing activity expressed in the anterior primitive endoderm of the mouse gastrula. Mech. Dev. 68: 45-57.
5. Bhanot, P., M. Brink, C.H. Samos, J.C. Hsieh, Y. Wang, J.P. Macke, D. Andrew, J. Nathans, and R. Nusse. 1996. A new member of the frizzled family from Drosophila functions as a Wingless receptor. Nature 382: 225-230.
6. Bolce, M.E., A. Hemmati-Brivanlou, P.D. Kushner, and R.M. Harland. 1992. Ventral ectoderm of Xenopus forms neural tissue, including hindbrain, in response to activin. Development 115: 681-688.
7. Bouillet, P., M. Oulad-Abdelghani, S.J. Ward, S. Bronner, P. Chambon, and P. Dolle. 1996. A new mouse member of the Wnt gene family, mWnt-8, is expressed during early embryogenesis and is ectopically induced by retinoic acid. Mech. Dev. 58: 141-152.
8. Boutros, M., N. Paricio, D.I. Strutt, and M. Mlodzik. 1998. Dishevelled activates JNK and discriminates between JNK pathways in planar polarity and wingless signaling. Cell 94: 109-118.
9. Bouwmeester, T., S. Kim, Y. Sasai, B. Lu, and E.M. De Robertis. 1996. Cerberus is a head-inducing secreted factor expressed in the anterior endoderm of Spemann's organizer. Nature 382: 595-601.
10. Bradley, L.C., A. Snape, S. Bhatt, and D.G. Wilkinson. 1993. The structure and expression of the Xenopus Krox-20 gene: Conserved and divergent patterns of expression in rhombomeres and neural crest. Mech. Dev. 40: 73-84.
11. Brannon, M. and D. Kimelman. 1996. Activation of Siamois by the Wnt pathway. Dev. Biol. 180: 344-347.
12. Brannon, M., M. Gomperts, L. Sumoy, R.T. Moon, and D. Kimelman. 1997. A beta-catenin/XTcf-3 complex binds to the siamois promoter to regulate dorsal axis specification in Xenopus. Genes & Dev. 11: 2359-2370.
13. Carnac, G., L. Kodjabachian, J.B. Gurdon, and P. Lemaire. 1996. The homeobox gene Siamois is a target of the Wnt dorsalisation pathway and triggers organiser activity in the absence of mesoderm. Development 122: 3055-3065.
14. Chomczynski, P. and N. Sacchi. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenolchloroform extraction. Anal. Biochem. 162: 156-159.
15. 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.
16. Christian, J.L., D.J. Olson, and R.T. Moon. 1992. Xwnt-8 modifies the character of mesoderm induced by bFGF in isolated Xenopus ectoderm. EMBO J. 11: 33-41.
17. Darras, S., Y. Marikawa, R.P. Elinson, and P. Lemaire. 1997. Animal and vegetal pole cells of early Xenopus embryos respond differently to maternal dorsal determinants: Implications for the patterning of the organiser. Development 124: 4275-4286.
18. Deardorff, M.A., C. Tan, L.J. Conrad, and P.S. Klein. 1998. Frizzled-8 is expressed in the Spemann organizer and plays a role in early morphogenesis. Development 125: 2687-2700.
19. Dominguez, I., K. Itoh, and S.Y. Sokol. 1995. Role of glycogen synthase kinase 3 beta as a negative regulator of dorsoventral axis formation in Xenopus embryos. Proc. Natl. Acad. Sci. 92: 8498-8502.
20. Fainsod, A., H. Steinbeisser, and E.M. De Robertis. 1994. On the function of BMP-4 in patterning the marginal zone of the Xenopus embryo. EMBO J. 13: 5015-5025.
21. Fainsod, A., K. Deissler, R. Yelin, K. Marom, M. Epstein, G. Pillemer, H. Steinbeisser, and M. Blum. 1997. The dorsalizing and neural inducing gene Follistatin is an antagonist of BMP-4. Mech. Dev. 63: 39-50.
22. Feldman, B., M.A. Gates, E.S. Egan, S.T. Dougan, G. Rennebeck, H.I. Sirotkin, A.F. Schier, and W.S. Talbot. 1998. Zebrafish organizer development and germ-layer formation require nodal-related signals. Nature 395: 181-185.
23. Gallagher, B.C., A.M. Hainski, and S.A. Moody. 1991. Autonomous differentiation of dorsal axial structures from an animal cap cleavage stage blastomere. Development 112: 1103-1114.
24. Glinka, A., W. Wu, D. Onichtchouk, C. Blumenstock, and C. Niehrs. 1997. Head induction by simultaneous repression of Bmp and Wnt signalling in Xenopus. Nature 389: 517-519.
25. Hammerschmidt, M., G.N. Serbedzija, and A.P. McMahon. 1996. Genetic analysis of dorsoventral pattern formation in the zebrafish: Requirement of a BMP-like ventralizing activity and its dorsal repressor. Genes & Dev. 10: 2452-2461.
26. Hansen, C.S., C.D. Marion, K. Steele, S. George, and W.C. Smith. 1997. Direct neural induction and selective inhibition of mesoderm and epidermis inducers by Xnr3. Development 124: 483-492.
27. Harland, R.M. 1991. In situ hybridization: An improved whole mount method for Xenopus embryos. In Methods in cell biology (ed. B.K. Kay and H.B. Perg) pp. 675-685. Academic Press; San Diego, CA.
28. _. 1997. Neural induction in Xenopus. In Molecular and cellular approaches to neural development, (ed. W.M. Cowan, T.M. Jessell, and S.L. Zipursky), pp. 1-25. Oxford University Press; New York, NY.
29. He, X., J.-P. Saint-Jeannet, J.R. Woodgett, H.E. Varmus, and I.B. Dawid. 1995. Glycogen synthase kinase-3 and dorsoventral patterning in Xenopus embryos. Nature 374: 617-622.
30. He, X., J.P. Saint-Jeannet, Y. Wang, J. Nathans, I. Dawid, and H. Varmus. 1997. A member of the Frizzled protein family mediating axis induction by Wnt-5A. Science 275: 1652-1654.
31. 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 beta-catenin inhibit dorsal mesoderm induction in early Xenopus embryos. Cell 79: 791-803.
32. Hemmati-Brivanlou, A. and D.A. Melton. 1994. Inhibition of activin receptor signalling promotes neuralization in X. laevis. Cell 77: 273-281.
33. Hemmati-Brivanlou, A. and G.H. Thomsen. 1995. Ventral mesodermal patterning in Xenopus embryos: Expression patterns and activities of BMP-2 and BMP-4. Dev. Genet. 17: 78-89.
34. Hemmati-Brivanlou, A., D. Frank, M.E. Bolce, B.D. Brown, H.L. Sive, and R.M. Harland. 1990. Localization of specific mRNAs in Xenopus embryos by whole-mount in situ hybridization. Development 110: 325-330.
35. 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.
36. Hogan, B., R. Beddington, F. Costantini, and E. Lacy. 1994. Manipulating the mouse embryo: A laboratory manual 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
37. Holowacz, T. and R.P. Elinson. 1995. Properties of the dorsal activity found in the vegetal cortical cytoplasm of Xenopus eggs. Development 121: 2789-2798.
38. Hoppler, S., J.D. Brown, and R.T. Moon. 1996. Expression of a dominant-negative Wnt blocks induction of MyoD in Xenopus embryos. Genes & Dev. 10: 2805-2817.
39. Hsu, D.R., A.N. Economides, X. Wang, P.M. Eimon, and R.M. Harland. 1998. The Xenopus dorsalizing factor gremlin identifies a novel family of secreted proteins that antagonize BMP activities. Mol. Cell 1: 673-683.
40. Jones, C.M., K.M. Lyons, P.M. Lapan, C.V. Wright, and B.L. Hogan. 1992. DVR-4 (bone morphogenetic protein-4) as a posterior-ventralizing factor in Xenopus mesoderm induction. Development 115: 639-647.
41. Kageura, H. 1990. Spatial distribution of the capacity to initiate a second embryo in the 32-cell embryos of Xenopus laevis. Dev. Biol. 142: 432-438.
42. _. 1997. Activation of dorsal development by contact between the cortical dorsal determinant and the equatorial core cytoplasm in eggs of Xenopus laevis. Development 124: 1543-1551.
43. Kengaku, M., J. Capdevila, C. Rodriguez-Esteban, J. De La Pena, R.L. Johnson, J. Carlos Izpisua Belmonte, and C.J. Tabin. 1998. Distinct WNT pathways regulating AER formation and dorsoventral polarity in the chick limb bud. Nature 280: 1274-1277.
44. Knecht, A.K., P.J. Good, I.B. Dawid, and R.M. Harland. 1995. Dorsal-ventral patterning and differentiation of noggin-induced neural tissue in the absence of mesoderm. Development 121: 1927-1935.
45. LaBonne, C. and M. Bronner-Fraser. 1998. Neural crest induction in Xenopus: Evidence for a two-signal model. Development 125: 2403-2414.
46. Lamb, T.M. and R.M. Harland. 1995. Fibroblast growth factor is a direct neural inducer, which combined with noggin generates anterior-posterior neural pattern. Development 121: 3627-3636.
47. Lamb, T.M., A.K. Knecht, W.C. Smith, S.E. Stachel, A.N. Economides, N. Stahl, G.D. Yancopolous, and R.M. Harland. 1993. Neural induction by the secreted polypeptide noggin. Science 262: 713-718.
48. Larabell, C.A., M. Torres, B.A. Rowning, C. Yost, J.R. Miller, M. Wu, D. Kimelman, and R.T. Moon. 1997. Establishment of the dorso-ventral axis in Xenopus is presaged by early asymmetries in beta-catenin that are modulated by the Wnt signaling pathway. J. Cell Biol. 136: 1123-1136.
49. Lemaire, P., N. Garrett, and J.B. Gurdon. 1995. Expression cloning of siamois, a Xenopus homeobox gene expressed in dorsal-vegetal cells of blastulae and able to induce a complete secondary axis. Cell 81: 85-94.
50. Leyns, L., T. Bouwmeester, S.H. Kim, S. Piccolo, and E.M. De Robertis. 1997. Frzb-1 is a secreted antagonist of Wnt signaling expressed in the Spemann organizer. Cell 88: 747-756.
51. Li, L., H. Yuan, W. Xie, J. Mao, A.M. Caruso, A. McMahon, D.J. Sussman, and D. Wu. 1999. Dishevelled proteins lead to two signaling pathways. Regulation of LEF-1 and c-Jun N-terminal kinase in mammalian cells. J. Biol. Chem. 274: 129-134.
52. London, C., R. Akers, and Phillips. C. 1988. Expression of Epi 1, an epidermis-specific marker in Xenopus laevis embryos, is specified prior to gastrulation. Dev. Biol. 129: 380-389.
53. Maniatis, T. 1999. A ubiquitin ligase complex essential for the NF-κB, Wnt/Wingless, and Hedgehog signaling pathways. Genes & Dev. 13: 505-509.
54. Marchant, L., C. Linker, P. Ruiz, N. Guerrero, and R. Mayor. 1998. The inductive properties of mesoderm suggest that the neural crest cells are specified by a BMP gradient. Dev. Biol. 198: 319-329.
55. McGrew, L.L., C.J. Lai, and R.T. Moon. 1995. Specification of the anteroposterior neural axis through synergistic interaction of the Wnt signaling cascade with noggin and follistatin. Dev. Biol. 172: 337-342.
56. McGrew, L.L., S. Hoppler, and R.T. Moon. 1997. Wnt and FGF pathways cooperatively pattern anteroposterior neural ectoderm in Xenopus. Mech. Dev. 69: 105-114.
57. McKendry, R., S.C. Hsu, R.M. Harland, and R. Grosschedl. 1997. LEF-1/TCF proteins mediate wnt-inducible transcription from the Xenopus nodal-related 3 promoter. Dev. Biol. 192: 420-431.
58. Molenaar, M., M. van de Wetering, M. Oosterwegel, J. Peterson-Maduro, S. Godsave, V. Korinek, J. Roosc, O. Destree, and H. Clevers. 1996. Xtcf-3 transcription factor mediates β-catenin-induced axis formation in Xenopus embryos. Cell 86: 391-399.
59. 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 119: 97-111.
60. Nguyen, V.H., B. Schmid, J. Trout, S.A. Connors, M. Ekker, and M.C. Mullins. 1998. Ventral and lateral regions of the zebrafish gastrula, including the neural crest progenitors, are established by a bmp2b/swirl pathway of genes. Dev. Biol. 199: 93-110.
61. Otte, A.P. and R.T. Moon. 1992. Ectopic induction of dorsal mesoderm by overexpression of Xwnt-8 elevates the neural competence of Xenopus ectoderm. Dev. Biol. 152: 184-187.
62. Piccolo, S., Y. Sasai, B. Lu, and E.M. De Robertis. 1996. Dorsoventral patterning in Xenopus: Inhibition of ventral signals by direct binding of chordin to BMP-4. Cell 86: 589-598.
63. Piccolo, S., E. Agius, B. Lu, S. Goodman, L. Dale, and E.M. De Robertis. 1997. Cleavage of Chordin by Xolloid metalloprotease suggests a role for proteolytic processing in the regulation of Spemann organizer activity. Cell 91: 407-416.
64. Pierce, S.B. and D. Kimelman. 1995. Regulation of Spemann organizer formation by the intracellular kinase Xgsk-3. Development 121: 755-765.
65. Rocheleau, C.E., W.D. Downs, R. Lin, C. Wittmann, Y. Bei, Y.H. Cha, M. Ali, J.R. Priess, and C.C. Mello. 1997. Wnt signaling and an APC-related gene specify endoderm in early C. elegans embryos. Cell 90: 707-716.
66. Rowning, B.A., J. Wells, M. Wu, J.C. Gerhart, R.T. Moon, and C.A. Larabell. 1997. Microtubule-mediated transport of organelles and localization of beta-catenin to the future dorsal side of Xenopus eggs. Proc. Natl. Acad. Sci. 94: 1224-1229.
67. Saint-Jeannet, J.P., X. He, H.E. Varmus, and I.B. Dawid. 1997. Regulation of dorsal fate in the neuraxis by Wnt-1 and Wnt-3a. Proc. Natl. Acad. Sci. 94: 13713-13718.
68. Sasai, Y., B. Lu, H. Steinbeisser, D. Geissert, L.K. Gont, and E.M. De Robertis. 1994. Xenopus chordin: A novel dorsalizing factor activated by organizer-specific homeobox genes. Cell 79: 779-790.
69. Sasai, Y., B. Lu, H. Steinbeisser, and E.M. De Robertis. 1995. Regulation of neural induction by the Chd and Bmp-4 antagonistic patterning signals in Xenopus. Nature 376: 333-336.
70. Schneider, S., H. Steinbeisser, R.M. Warga, and P. Hausen. 1996. Beta-catenin translocation into nuclei demarcates the dorsalizing centers in frog and fish embryos. Mech. Dev. 57: 191-198.
71. Sharpe, C.R., A. Fritz, R.E. De, and J.B. Gurdon. 1987. A homeobox-containing marker of posterior neural differentiation shows the importance of predetermination in neural induction. Cell 50: 749-758.
72. 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.
73. Sive, H.L., K. Hattori, and H. Weintraub. 1989. Progressive determination during formation of the anteroposterior axis in Xenopus laevis. Cell 58: 171-180.
74. Slusarski, D.C., V.G. Corces, and R.T. Moon. 1997. Interaction of Wnt and a Frizzled homologue triggers G-protein-linked phosphatidylinositol signalling. Nature 390: 410-413.
75. Smith, W.C. and R.M. Harland. 1991. Injected Xwnt-8 RNA acts early in Xenopus embryos to promote formation of a vegetal dorsalizing center. Cell 67: 753-765.
76. _. 1992. Expression cloning of noggin, a new dorsalizing factor localized to the Spemann organizer in Xenopus embryos. Cell 70: 829-840.
77. Smith, W.C., A.K. Knecht, M. Wu, and R.M. Harland. 1993. Secreted noggin protein mimics the Spemann organizer in dorsalizing Xenopus mesoderm. Nature 361: 547-549.
78. Smith, W.C., R. McKendry, S. Ribisi, and R.M. Harland. 1995. A nodal-related gene defines a physical and functional domain within the Spemann organizer. Cell 82:37-46.
79. Sokol, S.Y. 1996. Analysis of dishevelled signalling pathways during Xenopus development. Curr. Biol. 6: 1456-1467.
80. Sokol, S. and D.A. Melton. 1991. Pre-existent pattern in Xenopus animal pole cells revealed by induction with activin. Nature 351: 409-411.
81. Sokol, S.Y., J. Klingensmith, N. Perrimon, and K. Itoh. 1995. Dorsalizing and neuralizing properties of Xdsh, a maternally expressed Xenopus homolog of dishevelled. Development 121: 1637-1647.
82. Streit, A., K.J. Lee, I. Woo, C. Roberts, T.M. Jessell, and C.D. Stern. 1998. Chordin regulates primitive streak development and the stability of induced neural cells, but is not sufficient for neural induction in the chick embryo. Development 125: 507-519.
83. Turner, D.L. and H. Weintraub. 1994. Expression of achaetescute homolog 3 in Xenopus embryos converts ectodermal cells to a neural fate. Genes & Dev. 8: 1434-1447.
84. Vleminckx, K., E. Wong, K. Guger, B. Rubinfield, P. Polakis, and B.M. Gumbiner. 1997. 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. 136: 411-420.
85. Wang, S., M. Krinks, K. Lin, F.P. Luyten, and M. Moos, Jr. 1997. Frzb, a secreted protein expressed in the Spemann organizer, binds and inhibits Wnt-8. Cell 88: 757-766.
86. Willert, K. and R. Nusse. 1998. Beta-catenin: A key mediator of Wnt signaling. Curr. Opin. Genet. Dev. 8: 95-102.
87. Wilson, P.A. and D.A. Melton. 1994. Mesodermal patterning by an inducer gradient depends on secondary cell-cell communication. Curr. Biol. 4: 676-686.
88. Yanagawa, S., F. van Leeuwen, A. Wodarz, J. Klingensmith, and R. Nusse. 1995. The dishevelled protein is modified by wingless signaling in Drosophila. Genes & Dev. 9: 1087-1097.
89. Yang-Snyder, J., J.R. Miller, J.D. Brown, C.J. Lai, and R.T. Moon. 1996. A frizzled homolog functions in a vertebrate Wnt signaling pathway. Curr. Biol. 6: 1302-1306.
90. Yost, C., M. Torres, J.R. Miller, E. Huang, D. Kimelman, and R.T. Moon. 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: 1443-1454.
91. Yost, C., G.H. Farr III, S.B. Pierce, D.M. Ferkey, M.M. Chen, and D. Kimelman. 1998. GBP, an inhibitor of GSK-3, is implicated in Xenopus development and oncogenesis. Cell 93: 1031-1041.
92. Zimmerman, L.B., J.M. De Jesus-Escobar, and R.M. Harland. 1996. The Spemann organizer signal noggin binds and inactivates bone morphogenetic protein 4. Cell 86: 599-606.