In Xenopus embryos, BMP heterodimers are not required for mesoderm induction, but BMP activity is necessary for dorsal/ventral patterning

Developmental Biology

Volumn 216, Issue 1, 1999, Pages 29-40

  Eimon, Peter M ^a   Harland, Richard M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Bone morphogenetic protein 2; Bone morphogenetic protein 4; Bone morphogenetic protein 7; Cerberus; Gremlin; Heterodimer; Mesoderm induction; Noggin; Xenopus laevis

Indexed keywords

BONE MORPHOGENETIC PROTEIN; PROTEIN INHIBITOR;

ANIMAL TISSUE; ARTICLE; EMBRYO DEVELOPMENT; GASTRULATION; MESODERM; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TISSUE INDUCTION; XENOPUS;

ANIMALIA; CERBERUS; VERTEBRATA; XENOPUS LAEVIS;

EID: 0032740678     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1006/dbio.1999.9496     Document Type: Article

References (73)

1. Aono A., Hazama M., Notoya K., Taketomi S., Yamasaki H., Tsukuda R., Sasaki S., Fujisawa Y. Potent ectopic bone-inducing activity of bone morphogenetic protein-4/7 heterodimer. Biochem. Biophys. Res. Commun. 210:1995;670-677.
2. Artinger M., Blitz I., Inoue K., Tran U., Cho K. W. Interaction of goosecoid and brachyury in Xenopus mesoderm patterning. Mech. Dev. 65:1997;187-196.
3. Bouwmeester T., Kim S., Sasai Y., Lu B., De Robertis E. M. Cerberus is a head-inducing secreted factor expressed in the anterior endoderm of Spemann's organizer. Nature. 382:1996;595-601.
4. Chang C., Wilson P. A., Mathews L. S., Hemmati-Brivanlou A. A Xenopus type I activin receptor mediates mesodermal but not neural specification during embryogenesis. Development. 124:1997;827-837.
5. Cho K. W., Blumberg B., Steinbeisser H., De Robertis E. M. Molecular nature of Spemann's organizer: The role of the Xenopus homeobox gene goosecoid. Cell. 67:1991;1111-1120.
6. Christian J. L., Olson D. J., Moon R. T. Xwnt-8 modifies the character of mesoderm induced by bFGF in isolated Xenopus ectoderm. EMBO J. 11:1992;33-41.
7. Clement J. H., Fettes P., Knochel S., Lef J., Knochel W. Bone morphogenetic protein 2 in the early development of Xenopus laevis. Mech. Dev. 52:1995;357-370.
8. Condie B. G., Harland R. M. Posterior expression of a homeobox gene in early Xenopus embryos. Development. 101:1987;93-105.
9. Dale L., Howes G., Price B. M., Smith J. C. Bone morphogenetic protein 4: A ventralizing factor in early Xenopus development. Development. 115:1992;573-585.
10. Fainsod A., Deissler K., Yelin R., Marom K., Epstein M., Pillemer G., Steinbeisser H., Blum M. The dorsalizing and neural inducing gene Follistatin is an antagonist of BMP-4. Mech. Dev. 63:1997;39-50.
11. Fainsod A., Steinbeisser H., De Robertis E. M. On the function of BMP-4 in patterning the marginal zone of the Xenopus embryo. EMBO J. 13:1994;5015-5025.
12. Graff J. M., Bansal A., Melton D. A. Xenopus Mad proteins transduce distinct subsets of signals for the TGF beta superfamily. Cell. 85:1996;479-487.
13. Graff J. M., Thies R. S., Song J. J., Celeste A. J., Melton D. A. Studies with a Xenopus BMP receptor suggest that ventral mesoderm-inducing signals override dorsal signals in vivo. Cell. 79:1994;169-179.
14. Green J. B., New H. V., Smith J. C. Responses of embryonic Xenopus cells to activin and FGF are separated by multiple dose thresholds and correspond to distinct axes of the mesoderm. Cell. 71:1992;731-739.
15. Green J. B., Smith J. C. Graded changes in dose of a Xenopus activin A homologue elicit stepwise transitions in embryonic cell fate. Nature. 347:1990;391-394.
16. Harland R., Gerhart J. Formation and function of Spemann's organizer. Annu. Rev. Cell. Dev. Biol. 13:1997;611-667.
17. Harland R. M. The transforming growth factor beta family and induction of the vertebrate mesoderm: bone morphogenetic proteins are ventral inducers. Proc. Natl. Acad. Sci. USA. 91:1994;10243-10246.
18. Hazama M., Aono A., Ueno N., Fujisawa Y. Efficient expression of a heterodimer of bone morphogenetic protein subunits using a baculovirus expression system. Biochem. Biophys. Res. Commun. 209:1995;859-866.
19. Hemmati-Brivanlou A., Kelly O. G., Melton D. A. Follistatin, an antagonist of activin, is expressed in the Spemann organizer and displays direct neuralizing activity. Cell. 77:1994;283-295.
20. Hemmati-Brivanlou A., Melton D. A. A truncated activin receptor inhibits mesoderm induction and formation of axial structures in Xenopus embryos. Nature. 359:1992;609-614.
21. Hemmati-Brivanlou A., Thomsen G. H. Ventral mesodermal patterning in Xenopus embryos: Expression patterns and activities of BMP-2 and BMP-4. Dev. Genet. 17:1995;78-89.
22. Hsu D. R., Economides A. N., Wang X., Eimon P. M., Harland R. M. The Xenopus dorsalizing factor gremlin identifies a novel family of secreted proteins that antagonize BMP activities. Mol. Cell. 1:1998;673-683.
23. Jones C. M., Dale L., Hogan B. L., Wright C. V., Smith J. C. Bone morphogenetic protein-4 (BMP-4) acts during gastrula stages to cause ventralization of Xenopus embryos. Development. 122:1996;1545-1554.
24. Jones C. M., Kuehn M. R., Hogan B. L., Smith J. C., Wright C. V. Nodal-related signals induce axial mesoderm and dorsalize mesoderm during gastrulation. Development. 121:1995;3651-3662.
25. Jones C. M., Lyons K. M., Lapan P. M., Wright C. V., Hogan B. L. DVR-4 (bone morphogenetic protein-4) as a posterior-ventralizing factor in Xenopus mesoderm induction. Development. 115:1992;639-647.
26. Joseph E. M., Melton D. A. Xnr4: A Xenopus nodal-related gene expressed in the Spemann organizer. Dev. Biol. 184:1997;367-372.
27. Kimelman D., Kirschner M. Synergistic induction of mesoderm by FGF and TGF-β and the identification of a messenger RNA coding for FGF in the early Xenopus embryo. Cell. 51:1987;869-878.
28. Kishimoto Y., Lee K. H., Zon L., Hammerschmidt M., Schulte-Merker S. The molecular nature of zebrafish swirl: BMP2 function is essential during early dorsoventral patterning. Development. 124:1997;4457-4466.
29. Koenig B. B., Cook J. S., Wolsing D. H., Ting J., Tiesman J. P., Correa P. E., Olson C. A., Pecquet A. L., Ventura F., Grant R. A., Chen G.-X., Wrana J. L., Massagué J., Rosenbaum J. S. Characterization and cloning of a receptor for BMP-2 and BMP-4 from NIH 3T3 cells. Mol. Cell. Biol. 14:1994;5961-5974.
30. Koster M., Plessow S., Clement J. H., Lorenz A., Tiedemann H., Knochel W. Bone morphogenetic protein 4 (BMP-4), a member of the TGF-beta family, in early embryos of Xenopus laevis: Analysis of mesoderm inducing activity. Mech. Dev. 33:1991;191-199.
31. Krieg P. A., Melton D. A. Functional messenger RNAs are produced by SP6 in vitro transcription of cloned cDNAs. Nucleic Acids Res. 12:1984;7057-7070.
32. Latinkic B. V., Smith J. C. Goosecoid and mix.1 repress Brachyury expression and are required for head formation in Xenopus. Development. 126:1999;1769-1779.
33. Liu F., Ventura F., Doody J., Massague J. Human type II receptor for bone morphogenic proteins (BMPs): Extension of the two-kinase receptor model to the BMPs. Mol. Cell. Biol. 15:1995;3479-3486.
34. Lustig K. D., Kroll K. L., Sun E. E., Kirschner M. W. Expression cloning of a Xenopus T-related gene (Xombi) involved in mesodermal patterning and blastopore lip formation. Development. 122:1996;4001-4012.
35. Macias-Silva M., Hoodless P. A., Tang S. J., Buchwald M., Wrana J. L. Specific activation of Smad1 signaling pathways by the BMP7 type I receptor, ALK2. J. Biol. Chem. 273:1998;25628-25636.
36. Maeno M., Ong R. C., Suzuki A., Ueno N., Kung H. F. A truncated bone morphogenetic protein 4 receptor alters the fate of ventral mesoderm to dorsal mesoderm: Roles of animal pole tissue in the development of ventral mesoderm. Proc. Natl. Acad. Sci. USA. 91:1994;10260-10264.
37. Mishina Y., Suzuki A., Ueno N., Behringer R. R. Bmpr encodes a type I bone morphogenetic protein receptor that is essential for gastrulation during mouse embryogenesis. Genes Dev. 9:1995;3027-3037.
38. 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., Jiang Y. J., Kelsh R. N., Nusslein-Volhard C. Genes establishing dorsoventral pattern formation in the zebrafish embryo: The ventral specifying genes. Development. 123:1996;81-93.
39. Niehrs C., Keller R., Cho K. W., De Robertis E. M. The homeobox gene goosecoid controls cell migration in Xenopus embryos. Cell. 72:1993;491-503.
40. Nishimatsu S., Suzuki A., Shoda A., Murakami K., Ueno N. Genes for bone morphogenetic proteins are differentially transcribed in early amphibian embryos. Biochem. Biophys. Res. Commun. 186:1992;1487-1495.
41. Nishimatsu S., Thomsen G. Ventral mesoderm induction and patterning by bone morphogenetic protein heterodimers in Xenopus embryos. Mech. Dev. 74:1998;75-88.
42. Onichtchouk D., Gawantka V., Dosch R., Delius H., Hirschfeld K., Blumenstock C., Niehrs C. The Xvent-2 homeobox gene is part of the BMP-4 signalling pathway controlling [correction of controling] dorsoventral patterning of Xenopus mesoderm. Development. 122:1996;3045-3053.
43. Osada S. I., Wright C. V. Xenopus nodal-related signaling is essential for mesendodermal patterning during early embryogenesis. Development. 126:1999;3229-3240.
44. Peng H. B. Appendix A: Solutions and protocols. Kay B. K., Peng H. B. Xenopus laevis: Practical Uses in Cell and Molecular Biology. 1991;661-662 Academic Press, San Diego.
45. Piccolo S., Agius E., Leyns L., Bhattacharyya S., Grunz H., Bouwmeester T., DeRobertis E. M. The head inducer Cerberus is a multifunctional antagonist of Nodal, BMP, and Wnt signals. Nature. 397:1999;707-710.
46. Piccolo S., Sasai Y., Lu B., De Robertis E. M. Dorsoventral patterning in Xenopus: Inhibition of ventral signals by direct binding of chordin to BMP-4. Cell. 86:1996;589-598.
47. Rosenzweig B. L., Imamura T., Okadome T., Cox G. N., Yamashita H., ten Dijke P., Heldin C. H., Miyazono K. Cloning and characterization of a human type II receptor for bone morphogenetic proteins. Proc. Natl. Acad. Sci. USA. 92:1995;7632-7636.
48. Ruiz i Altaba A., Melton D. A. Bimodal and graded expression of the Xenopus homeobox gene Xhox3 during embryonic development. Development. 106:1989;173-183.
49. Ryan K., Garrett N., Mitchell A., Gurdon J. B. Eomesodermin, a key early gene in Xenopus mesoderm differentiation. Cell. 87:1996;989-1000.
50. Sasai Y., Lu B., Steinbeisser H., Geissert D., Gont L. K., De Robertis E. M. Xenopus chordin: A novel dorsalizing factor activated by organizer-specific homeobox genes. Cell. 79:1994;779-790.
51. Schmidt J., Francois V., Bier E., Kimelman D. Drosophila short gastrulation induces an ectopic axis in Xenopus: Evidence for conserved mechanisms of dorsal-ventral patterning. Development. 121:1995a;4319-4328.
52. Schmidt J. E., Suzuki A., Ueno N., Kimelman D. Localized BMP-4 mediates dorsal/ventral patterning in the early Xenopus embryo. Dev. Biol. 169:1995b;37-50.
53. Schulte-Merker S., Smith J. C., Dale L. Effects of truncated activin and FGF receptors and of follistatin on the inducing activities of BVg1 and activin: Does activin play a role in mesoderm induction? EMBO J. 13:1994;3533-3541.
54. Slack J. M., Darlington B. G., Heath J. K., Godsave S. F. Mesoderm induction in early Xenopus embryos by heparin-binding growth factors. Nature. 326:1987;197-200.
55. Smith W. C., Harland R. M. Expression cloning of noggin, a new dorsalizing factor localized to the Spemann organizer in Xenopus embryos. Cell. 70:1992;829-840.
56. Smith W. C., McKendry R., Ribisi S., Harland R. M. A nodal-related gene defines a physical and functional domain within the Spemann organizer. Cell. 82:1995;37-46.
57. Steinbeisser H., De Robertis E. M. Xenopus goosecoid: A gene expressed in the prechordal plate that has dorsalizing activity. Comptes Rendus. 316:1993;959-971.
58. Steinbeisser H., De Robertis E. M., Ku M., Kessler D. S., Melton D. A. Xenopus axis formation: Induction of goosecoid by injected Xwnt-8 and activin mRNAs. Development. 118:1993;499-507.
59. Stennard F., Carnac G., Gurdon J. B. The Xenopus T-box gene, Antipodean, encodes a vegetally localised maternal mRNA and can trigger mesoderm formation. Development. 122:1996;4179-4188.
60. Suzuki A., Kaneko E., Maeda J., Ueno N. Mesoderm induction by BMP-4 and -7 heterodimers. Biochem. Biophys. Res. Commun. 232:1997;153-156.
61. Suzuki A., Thies R. S., Yamaji N., Song J. J., Wozney J. M., Murakami K., Ueno N. A truncated bone morphogenetic protein receptor affects dorsal-ventral patterning in the early Xenopus embryo. Proc. Natl. Acad. Sci. USA. 91:1994;10255-10259.
62. ten Dijke P., Yamashita H., Ichijo H., Franzen P., Laiho M., Miyazono K., Heldin C. H. Characterization of type I receptors for transforming growth factor-beta and activin. Science. 264:1994a;101-104.
63. ten Dijke P., Yamashita H., Sampath T. K., Reddi A. H., Estevez M., Riddle D. L., Ichijo H., Heldin C. H., Miyazono K. Identification of type I receptors for osteogenic protein-1 and bone morphogenetic protein-4. J. Biol. Chem. 269:1994b;16985-16988.
64. Thomsen G., Woolf T., Whitman M., Sokol S., Vaughan J., Vale W., Melton D. A. Activins are expressed early in Xenopus embryogenesis and can induce axial mesoderm and anterior structures. Cell. 63:1990;485-493.
65. Thomsen G. H., Melton D. A. Processed Vg1 protein is an axial mesoderm inducer in Xenopus. Cell. 74:1993;433-441.
66. Turner D. L., Weintraub H. Expression of achaete-scute homolog 3 in Xenopus embryos converts ectodermal cells to a neural fate. Genes Dev. 8:1994;1434-1447.
67. von Dassow G., Schmidt J. E., Kimelman D. Induction of the Xenopus organizer: Expression and regulation of Xnot, a novel FGF and activin-regulated homeo box gene. Genes Dev. 7:1993;355-366.
68. Watabe T., Kim S., Candia A., Rothbacher U., Hashimoto C., Inoue K., Cho K. W. Molecular mechanisms of Spemann's organizer formation: Conserved growth factor synergy between Xenopus and mouse. Genes Dev. 9:1995;3038-3050.
69. Wilson P. A., Hemmati-Brivanlou A. Induction of epidermis and inhibition of neural fate by Bmp-4. Nature. 376:1995;331-333.
70. Winnier G., Blessing M., Labosky P. A., Hogan B. L. M. Bone morphogenic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev. 9:1995;2105-2116.
71. Yamashita H., ten Dijke P., Huylebroeck D., Sampath T. K., Andries M., Smith J. C., Heldin C. H., Miyazono K. Osteogenic protein-1 binds to activin type II receptors and induces certain activin-like effects. J. Cell Biol. 130:1995;217-226.
72. Zhang J., King M. L. Xenopus VegT RNA is localized to the vegetal cortex during oogenesis and encodes a novel T-box transcription factor involved in mesodermal patterning. Development. 122:1996;4119-4129.
73. Zimmerman L. B., De Jesus-Escobar J. M., Harland R. M. The Spemann organizer signal noggin binds and inactivates bone morphogenetic protein 4. Cell. 86:1996;599-606.