Depletion of Bmp2, Bmp4, Bmp7 and Spemann organizer signals induces massive brain formation in Xenopus embryos

Development

Volumn 132, Issue 15, 2005, Pages 3381-3392

  Reversade, Bruno ^a   Kuroda, Hiroki ^a   Lee, Hojoon ^a   Mays, Ashley ^a   De Robertis, Edward M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

BMP; Brain induction; Chordin; Dorsoal ventral patterning; Morpholino; Sizzled; Spemann organizer

Indexed keywords

BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; CHORDIN; NOGGIN; OLIGOMER; OSTEOGENIC PROTEIN 1;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; EMBRYONIC STRUCTURES; GENE ACTIVITY; GENE EXPRESSION; IN VIVO STUDY; INHIBITION KINETICS; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TAIL; XENOPUS LAEVIS;

ANIMALS; BASE SEQUENCE; BODY PATTERNING; BONE MORPHOGENETIC PROTEINS; BRAIN; EMBRYO, NONMAMMALIAN; GLYCOPROTEINS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MOLECULAR SEQUENCE DATA; MORPHOGENESIS; MORPHOLINES; PROTEINS; SIGNAL TRANSDUCTION; TAIL; TRANSFORMING GROWTH FACTOR BETA; XENOPUS LAEVIS; XENOPUS PROTEINS;

ANIMALIA; CERBERUS; XENOPUS LAEVIS;

EID: 24344442989     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.01901     Document Type: Article

References (57)

1. Baker, J. C., Beddington, R. S. and Harland, R. M. (1999). Wnt signaling in Xenopus embryos inhibits bmp4 expression and activates neural development. Genes Dev. 13, 3149-3159.
2. Barth, K. A., Kishimoto, Y., Rohr, K. B., Seydler, C., Schulte-Merker, S. and Wilson, S. W. (1999). Bmp activity establishes a gradient of positional information throughout the entire neural plate. Development 126, 4977-4987.
3. Collavin, L. and Kirschner, M. W. (2003). The secreted Frizzled-related protein Sizzled functions as a negative feedback regulator of extreme ventral mesoderm. Development 130, 805-816.
4. Dale, L., Howes, G., Price, B. M. and Smith, J. C. (1992). Bone morphogenetic protein 4, a ventralizing factor in early Xenopus development. Development 115, 573-585.
5. De Robertis, E. M. and Kuroda, H. (2004). Dorsal-ventral patterning and neural induction in Xenopus embryos. Annu. Rev. Cell. Dev. Biol. 20, 285-308.
6. De Robertis, E. M., Larrain, J., Oelgeschlager, M. and Wessely, O. (2000). The establishment of Spemann's organizer and patterning of the vertebrate embryo. Nat. Rev. Genet. 1, 171-181.
7. Delaune, E., Lemaire, P. and Kodjabachian, L. (2005). Neural induction in Xenopus requires early FGF signalling in addition to BMP inhibition. Development 132, 299-310.
8. Faure, S., Lee, M. A., Keller, T., ten Dijke, P. and Whitman, M. (2000). Endogenous patterns of TGFbeta superfamily signaling during early Xenopus development. Development 127, 2917-2931.
9. Foley, A. C., Skromne, I. and Stern, C. D. (2000). Reconciling different models of forebrain induction and patterning: a dual role for the hypoblast. Development 127, 3839-3854.
10. Fujiwara, T., Dunn, N. R. and Hogan, B. L. (2001). Bone morphogenetic protein 4 in the extraembryonic mesoderm is required for allantois development and the localization and survival of primordial germ cells in the mouse. Proc. Natl. Acad. Sci. USA 98, 13739-13744.
11. Glinka, A., Wu, W., Onichtchouk, D., Blumenstock, C. and Niehrs, C. (1997). Head induction by simultaneous repression of Bmp and Wnt signalling in Xenopus. Nature 389, 517-519.
12. Gonzalez, E. M., Fekany-Lee, K., Carmany-Rampey, A., Erter, C., Topczewski, J., Wright, C. V. and Solnica-Krezel, L. (2000). Head and trunk in zebrafish arise via coinhibition of BMP signaling by bozozok and chordino. Genes Dev. 14, 3087-3092.
13. Hammerschmidt, M. and Mullins, M. C. (2002). Dorsoventral patterning in the zebrafish: bone morphogenetic proteins and beyond. Results Probl. Cell Differ. 40, 72-95.
14. Harland, R. (2000). Neural induction. Curr. Opin. Genet. Dev. 10, 357-362.
15. Harland, R. and Gerhart, J. (1997). Formation and function of Spemann's organizer. Annu. Rev. Cell. Dev. Biol. 13, 611-667.
16. Hawley, S. H., Wunnenberg-Stapleton, K., Hashimoto, C., Laurent, M. N., Watabe, T., Blumberg, B. W. and Cho, K. W. (1995). Disruption of BMP signals in embryonic Xenopus ectoderm leads to direct neural induction. Genes Dev. 9, 2923-2935.
17. Heasman, J., Kofron, M. and Wylie, C. (2000). Beta-catenin signaling activity dissected in the early Xenopus embryo: a novel antisense approach. Dev. Biol. 222, 124-134.
18. Hogan, B. L. (1996). Bone morphogenetic proteins: multifunctional regulators of vertebrate development. Genes Dev. 10, 1580-1594.
19. Hudson, C. and Woodland, H. R. (1998). Xpat, a gene expressed specifically in germ plasm and primordial germ cells of Xenopus laevis. Mech. Dev. 73, 159-168.
20. Kao, K. R. and Elinson, R. P. (1988). The entire mesodermal mantle behaves as Spemann's organizer in dorsoanterior enhanced Xenopus laevis embryos. Dev. Biol. 127, 64-77.
21. Khokha, M. K., Yeh, J., Grammer, T. C. and Harland, R. M. (2005). Depletion of three BMP antagonists from Spemann's organizer leads to a catastrophic loss of dorsal structures. Dev. Cell 8, 401-411.
22. Kurata, T., Nakabayashi, J., Yamamoto, T. S., Mochii, M. and Ueno, N. (2001). Visualization of endogenous BMP signaling during Xenopus development. Differentiation 67, 33-40.
23. Kuroda, H., Wessely, O. and Robertis, E. M. (2004). Neural Induction in Xenopus: Requirement for Ectodermal and Endomesodermal Signals via Chordin, Noggin, beta-Catenin, and Cerberus. PLoS Biol. 2, E92.
24. Kuroda, H., Fuentealba, L., Ikeda, A., Reversade, B. and De Robertis, E. M. (2005). Default neural induction: neuralization of dissociated Xenopus cells is mediated by Ras/MAPK activation. Genes Dev. 19, 1022-1027.
25. Lall, S. and Patel, N. H. (2001). Conservation and divergence in molecular mechanisms of axis formation. Annu. Rev. Genet. 35, 407-437.
26. Linker, C. and Stern, C. D. (2004). Neural induction requires BMP inhibition only as a late step, and involves signals other than FGF and Wnt antagonists. Development 131, 5671-5681.
27. Massague, J. (2003). Integration of Smad and MAPK pathways: a link and a linker revisited. Genes Dev. 17, 2993-2997.
28. Mead, P. E., Brivanlou, I. H., Kelley, C. M. and Zon, L. I. (1996). BMP-4-responsive regulation of dorsal-ventral patterning by the homeobox protein Mix.1. Nature 382, 357-360.
29. Mullins, M. C., Hammerschmidt, M., Kane, D. A., Odenthal, J., Brand, M., van Eeden, F. J., Furutani-Seiki, M., Granato, M., Haffter, P., Heisenberg, C. P. et al. (1996). Genes establishing dorsoventral pattern formation in the zebrafish embryo: the ventral specifying genes. Development 123, 81-93.
30. Munoz-Sanjuan, I. and Brivanlou, A. H. (2002). Neural induction, the default model and embryonic stem cells. Nat. Rev. Neurosci. 3, 271-280.
31. Myers, D. C., Sepich, D. S. and Solnica-Krezel, L. (2002). Bmp activity gradient regulates convergent extension during zebrafish gastrulation. Dev. Biol. 243, 81-98.
32. Nguyen, V. H., Trout, J., Connors, S. A., Andermann, P., Weinberg, E. and Mullins, M. C. (2000). Dorsal and intermediate neuronal cell types of the spinal cord are established by a BMP signaling pathway. Development 127, 1209-1220.
33. Niehrs, C. (2004). Regionally specific induction by the Spemann-Mangold organizer. Nat. Rev. Genet. 5, 425-434.
34. Oelgeschläger, M., Kuroda, H., Reversade, B. and De Robertis, E. M. (2003). Chordin is required for the Spemann organizer transplantation phenomenon in Xenopus embryos. Dev. Cell 4, 219-230.
35. 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.
36. Pera, E. M., Ikeda, A., Eivers, E. and De Robertis, E. M. (2003). Integration of IGF, FGF, and anti-BMP signals via Smad1 phosphorylation in neural induction. Genes Dev. 17, 3023-3028.
37. Persson, U., Izumi, H., Souchelnytskyi, S., Itoh, S., Grimsby, S., Engstrom, U., Heldin, C. H., Funa, K. and ten Dijke, P. (1998). The L45 loop in type I receptors for TGF-beta family members is a critical determinant in specifying Smad isoform activation. FEBS Lett. 434, 83-87.
38. Piccolo, S., Sasai, Y., Lu, B. and De Robertis, E. M. (1996). Dorsoventral patterning in Xenopus: inhibition of ventral signals by direct binding of chordin to BMP-4. Cell 86, 589-598.
39. Piccolo, S., Agius, E., Leyns, L., Bhattacharyya, S., Grunz, H., Bouwmeester, T. and De Robertis, E. M. (1999). The head inducer Cerberus is a multifunctional antagonist of Nodal, BMP and Wnt signals. Nature 397, 707-710.
40. Sater, A. K., El-Hodiri, H. M., Goswami, M., Alexander, T. B., Al-Sheikh, O., Elkin, L. D. and Akif Uzman, J. (2003). Evidence for antagonism of BMP-4 signals by MAP kinase during Xenopus axis determination and neural specification. Differentiation 71, 434-444.
41. Schmid, B., Furthauer, M., Connors, S. A., Trout, J., Thisse, B., Thisse, C. and Mullins, M. C. (2000). Equivalent genetic roles for bmp7/snailhouse and bmp2b/swirl in dorsoventral pattern formation. Development 127, 957-967.
42. Spemann, H. (1938). Embryonic Development and Induction. New Haven, CT.: Yale University Press.
43. Stern, C. D. (2004). Neural Induction. in Gastrulation: from Cells to Embryo. (ed. C. D. Stern) pp. 419-432. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
44. Stern, C. D. (2005). Neural induction: old problem, new findings, yet more questions. Development 132, 2007-2021.
45. Streit, A., Lee, K. J., Woo, I., Roberts, C., Jessell, T. M. and Stern, C. D. (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.
46. Tucker, A. S. and Slack, J. M. (2004). Independent induction and formation of the dorsal and ventral fins in Xenopus laevis. Dev. Dyn. 230, 461-467.
47. Urist, M. R., Mikulski, A. and Lietze, A. (1979). Solubilized and insolubilized bone morphogenetic protein. Proc. Natl. Acad. Sci. USA 76, 1828-1832.
48. Von Bubnoff, A., Schmidt, J. E. and Kimelman, D. (1996). The Xenopus laevis homeobox gene Xgbx-2 is an early marker of anteroposterior patterning in the ectoderm. Mech. Dev. 54, 149-160.
49. Wagner, D. S. and Mullins, M. C. (2002). Modulation of BMP activity in dorsal-ventral pattern formation by the chordin and ogon antagonists. Dev. Biol. 245, 109-123.
50. Wawersik, S., Evola, C. and Whitman, M. (2005). Conditional BMP inhibition in Xenopus reveals stage-specific roles for BMPs in neural and neural crest induction. Dev. Biol. 277, 425-442.
51. Weaver, C. and Kimelman, D. (2004). Move it or lose it: axis specification in Xenopus. Development 131, 3491-3499.
52. Winnier, G., Blessing, M., Labosky, P. A. and Hogan, B. L. (1995). Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev. 9, 2105-2116.
53. Yamamoto, T. S., Takagi, C., Hyodo, A. C. and Ueno, N. (2001). Suppression of head formation by Xmsx-1 through the inhibition of intracellular nodal signaling. Development 128, 2769-2779.
54. Ying, Q. L., Nichols, J., Chambers, I. and Smith, A. (2003). BMP induction of Id proteins suppresses differentiation and sustains embryonic stem cell self-renewal in collaboration with STAT3. Cell 115, 281-292.
55. Zakin, L., Reversade, B., Kuroda, H., Lyons, K. M. and De Robertis, E. M. (2005). Sirenomelia in Bmp7 and Tsg compound mutant mice: requirement for Bmp signaling in the development of ventral posterior mesoderm. Development 132, 2489-2499.
56. Zhao, G. Q. (2003). Consequences of knocking out BMP signaling in the mouse. Genesis 35, 43-56.
57. 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 86, 599-606.