Dorsoventral patterning in Xenopus: Inhibition of ventral signals by direct binding of chordin to BMP-4

Cell

Volumn 86, Issue 4, 1996, Pages 589-598

  Piccolo, Stefano ^b   Sasai, Yoshiki ^a,b   Lu, Bin ^b   De Robertis, Eddy M ^b  

^a KYOTO UNIVERSITY FACULTY OF MEDICINE   (Japan)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; GASTRULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RECEPTOR BINDING; RECEPTOR BLOCKING; SIGNAL TRANSDUCTION; XENOPUS;

ANIMALIA;

EID: 0030598867     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)80132-4     Document Type: Article

References (48)

1. Aono, A., Hazama, M., Notoya, K., Taketomi, S., Yamasaki, H., Tsukuda, R., Sasaki, S., and Fujisawa, Y. (1995). Potent ectopic bone-inducing activity of bone morphogenetic protein 4/7 heterodimer. Biochem. Biophys. Res. Commun. 210, 670-677.
2. Attisano, L., Wrana, J.L., Cheifetz, S., and Massagué, J. (1992). Novel actin receptors: distinct genes and alternative mRNA splicing generate a repertoire of serine/threonine kinase receptors. Cell 68, 97-108.
3. Bouwmeester, T., Kim, S.-H., Sasai, Y., Lu, B., and De Robertis, E.M. (1996). Cerberus, a head-inducing secreted factor expressed in the anterior endoderm of Spemann's organizer. Nature, in press.
4. Dale, L., and Slack, J.M.W. (1987). Regional specification within the mesoderm of early embryos of Xenopus laevis. Development 100, 279-295.
5. Dale, L., Howes, G., Price, B.M.J., and Smith, J.C. (1992). Bone morphogenetic protein-4: a ventralizing factor in early Xenopus development. Development 115, 573-585.
6. Dawid, I.B. (1994). Intercellular signaling and gene regulation during early embryogenesis of Xenopus laevis. J. Biol. Chem. 269, 6259-6262.
7. De Robertis, E.M. (1995). Dismantling the organizer. Nature 374, 407-408.
8. De Robertis, E.M., and Sasai, Y. (1996). A common plan for dorsoventral patterning in Bilateria. Nature 380, 37-40.
9. Fainsod, A., Steinbeisser, H., and De Robertis, E.M. (1994). On the function of BMP-4 in patterning the marginal zone of the Xenopus embryo. EMBO J. 13, 5015-5025.
10. Ferguson, E.L., and Anderson, K.V. (1992a). decapentaplegic acts as a morphogen to organize dorsal-ventral pattern in the Drosophila embryo. Cell 71, 451-461.
11. Ferguson, E.L., and Anderson, K.V. (1992b). Localized enhancement and repression of the activity of the TGF-β family member, decapentaplegic, is necessary for dorsal-ventral pattern formation in the Drosophila embryo. Development 114, 583-597.
12. François, V., and Bier, E. (1995). Xenopus chordin and Drosophila sog genes encode homologous proteins functioning in dorsal-ventral axis formation. Cell 80, 19-20.
13. François, V., Solloway, M., O'Neill, J.W., Emery, J., and Bier, E. (1994). Dorsal-ventral patterning of the Drosophila embryo depends on a putative negative growth factor encoded by the short gastrulation gene. Genes Dev. 8, 2602-2616.
14. Frolik, C.A., Wakefield, L.M., Smith, D.M., and Sporn, M.B. (1984). Characterization of a membrane receptor for transforming growth factor-β in normal rat kidney fibroblasts. J. Biol. Chem. 259, 10995-11000.
15. Graff, J.M., Scott Thies, R., Song, J.J., Celeste, A.J., and Melton, D.A. (1994). Studies with a Xenopus BMP receptor suggest that ventral mesoderm-inducing signals override dorsal signals in vivo. Cell 79, 169-179.
16. Hamburger, V. (1988). The Heritage of Experimental Embryology: Hans Spemann and the Organizer. (Oxford: Oxford University Press).
17. Harland, R.M. (1994). The transforming growth factor-β family and induction of the vertebrate mesoderm: bone morphogenetic proteins are ventral inducers. Proc. Natl. Acad. Sci. 91, 10243-10246.
18. Hazama, M., Aono, A., Ueno, N., and Fujisawa, Y. (1995). Efficient expression of a heterodimer of bone morphogenetic protein sub-units using a baculovirus expression system. Biochem. Biophys. Res. Commun. 209, 859-866.
19. Hemmati-Brivanlou, A., Kelly, O.G., and Melton, D.A. (1994). Follistatin, an antagonist of activin, is expressed in the Spemann organizer and displays direct neuralizing activity. Cell 77, 283-295.
20. Hawley, S.H.B., Wünnenberg-Stapleton, K., Hashimoto, C., Laurent, M.N., Watabe, T., Blumberg, B.W., and Cho, K.W.Y. (1995). Disruption of BMP signals in embryonic Xenopus ectoderm leads to direct neural induction. Genes Dev. 9, 2923-2935.
21. Holley, S.A., Jackson, P.D., Sasai, Y., Lu, B., De Robertis, E.M., Huffman, F.M., and Ferguson, E.L. (1995). A conserved system for dorsal-ventral patterning in insects and vertebrates involving short gastrulation and chordin. Nature 376, 249-253.
22. Holley, S.A., Neul, J.L., Attisano, L., Wrana, J.L., Sasai, Y., O'Connor, M.B., De Robertis, E.M., and Ferguson, E.L. (1996). The Xenopus Dorsalizing Factor NOGGIN Ventralizes Drosophila Embryos by Preventing DPP from Activating Its Receptor. Cell 86, this issue.
23. Jones, C.M., Lyons, K.M., Lapan, P.M., Wright, C.V.E., and Hogan, B.L.M. (1992). DVR-4 (bone morphogenetic protein-4) as a posterior-ventralizing factor in Xenopus mesoderm induction. Development 115, 639-647.
24. Jones, C.M., Dale, L., Hogan, B.L.M., Wright, C.V.E., and Smith, J.C. (1996). Bone morphogenetic protein-4 (BMP-4) acts during gastrula stages to cause ventralization of Xenopus embryos. Development 122, 1545-1554.
25. Katagiri, T., Yamaguchi, A., Ikeda, T., Yoshiki, S., Wozney, J.M., Rosen, V., Wang, E.A., Tanaka, H., Omura, S., and Suda, T. (1990). The nonosteogenic mouse pluripotent cell line C3H10t1/2 is induced to differentiate into osteoblastic cells by recombinant human bone morphogenetic protein-2. Biochem. Biophys. Res. Commun. 172, 295-299.
26. Lamb, T.M., and Harland, R.M. (1995). Fibroblast growth factor is a direct neural inducer, which combined with noggin generates anterior-posterior neural pattern. Development 121, 3627-3636.
27. Lamb, T.M., Knecht, A.K., Smith, W.C., Stachel, S.E., Economides, A.N., Stahl, N., Yancopoulos, G.D., and Harland, R.M. (1993). Neural induction by secreted polypeptide noggin. Science 262, 713-178.
28. Massagué, J. (1987). Identification of receptors for type-β transforming growth factor. Meth. Enzymol. 46, 174-195.
29. Masuhara, K., Nakase, T., Suzuki, S., Takaoka, K., Matsui, M., and Anderson, H.C. (1995). Use of monoclonal antibody to detect bone morphogenetic protein-4 (BMP-4). Bone 16, 91-96.
30. Nellen, D., Burke, R., Struhl, G., and Basler, K. (1996). Direct and long range action of a DPP morphogen gradient. Cell 85, 357-368.
31. Padgett, R.W., Wozney, J.M., and Gelbart, W.M. (1993). Human BMP sequences can confer normal dorsal-ventral patterning in the Drosophila embryo. Proc. Natl. Acad. Sci. USA 90, 2905-2909.
32. Penton, A., Chen, Y., Staehling-Hampton, K., Wrana, J.L., Attisano, L., Szidonya, J., Cassill, J.A., Massagué, J., and Hoffman, F.M. (1994). Identification of two bone morphogenetic protein type I receptors in Drosophila and evidence that Brk25D is a decapentaplegic receptor. Cell 78, 239-250.
33. Re'em-Kalma, Y., Lamb, T., and Frank, D. (1995). Competition between noggin and bone morphogenetic protein-4 activities may regulate dorsalization during Xenopus development. Proc. Natl. Acad. Sci. USA 92, 12141-12145.
34. Sasai, Y., Lu, B., Steinbeisser, H., Geissert, D., Gont, L.K., and De Robertis, E.M. (1994). Xenopus chordin: a novel dorsalizing factor activated by organizer-specific homeobox genes. Cell 79, 779-790.
35. Sasai, Y., Lu, B., Steinbeisser, H., and De Robertis, E.M. (1995). Regulation of neural induction by the chd and BMP-4 antagonistic patterning signals in Xenopus. Nature 376, 333-336.
36. Schmidt, J.E., François, V., Bier, E., and Kimelman, D. (1995). Drosophila short gastrulation induces an ectopic axis in Xenopus: evidence for conserved mechanisms of dorsal-ventral patterning. Development 121, 4319-4328.
37. Smith, W.C., and Harland, R.M. (1992). Expression cloning of noggin, a new dorsalizing factor localized to the Spemann organizer in Xenopus embryos. Cell 70, 829-840.
38. Smith, W.C., Knecht, A.K., Wu, M., and Harland, R.M. (1993). Secreted noggin protein mimics the Spemann organizer in dorsalizing Xenopus mesoderm. Nature 361, 547-549.
39. Spemann, H., and Mangold, H. (1924). Uberinduktion von embryonalanlagen durch implantation artfremder organisatoren. Roux's Arch. Entw. Mech. 100, 599-638.
40. Steinbeisser, H., Fainsod, A., Niehrs, C., Sasai, Y., and De Robertis, E.M. (1995). The role of gsc and BMP-4 in dorsal-ventral patterning of the marginal zone in Xenopus: a loss-of-function study using antisense RNA. EMBO J. 14, 5230-5243.
41. Suzuki, A., Scott Thies, R., Yamaji, N., Song, J.J., Wozney, J.M., Murakami, K., and Ueno, N. (1994). A truncated bone morphogenetic protein receptor affects dorsal-ventral patterning in the early Xenopus embryo. Proc. Natl. Acad. Sci. USA 91, 10255-10259.
42. Taira, M., Otani, H., Saint-Jeannet, J.P., and Dawid, I. (1994). Role of the LIM class homeodomain protein Xlim-1 in neural and muscle induction by the Spemann organizer in Xenopus. Nature 372, 677-679.
43. Wharton, K.A., Ray, R.P., and Gelbart, W.M. (1993). An activity gradient of decapentaplegic is necessary for the specification of dorsal pattern elements in the Drosophila embryo. Development 117, 807-822.
44. Wilson, P.A., and Hemmati-Brivanlou, A. (1995). Induction of epidermis and inhibition of neural fate by BMP-4. Nature 376, 331-333.
45. Wrana, J.L., Attisano, L., Wieser, R., Ventura, F., and Massagué, J. (1994). Mechanism of activation of the TGF-β receptor. Nature 370, 341-347.
46. Xu, R.J., Kim, J., Taira, M., Zhan, S., Sredni, D., and Kung, H. (1995). A dominant-negative bone morphogenetic protein-4 receptor causes neuralization in Xenopus ectoderm. Biochem. Biophys. Res. Commun. 272, 212-219.
47. Yamashita, H., ten Dijke, P., Huylebroeck, D., Sampath, T.K., Andries, M., Smith, J.C., Heldin, C.H., and Miyazono, K. (1995). Osteogenic protein-1 binds to activin type II receptors and induces certain activin-like effects. J. Cell Biol. 130, 217-226.
48. Zimmerman, L.B, De Jesus-Escobar, J.M., and Harland, R.M. (1996). The Spemann organizer signal noggin binds and inactivates bone morphogenetic protein-4. Cell, this issue.