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JOURNAL ARTICLES
Activin-mediated mesoderm induction requires FGF
R.A. Cornell, D. Kimelman
Development 1994 120: 453-462;

Summary

The early patterning of mesoderm in the Xenopus embryo requires signals from several intercellular factors, including mesoderm-inducing agents that belong to the fibroblast growth factor (FGF) and TGF-beta families. In animal hemisphere explants (animal caps), basic FGF and the TGF-beta family member activin are capable of converting pre-ectodermal cells to a mesodermal fate, although activin is much more effective at inducing dorsal and anterior mesoderm than is basic FGF. Using a dominant-negative form of the Xenopus type 1 FGF receptor, we show that an FGF signal is required for the full induction of mesoderm by activin. Animal caps isolated from embryos that have been injected with the truncated FGF receptor and cultured with activin do not extend and the induction of some genes, including cardiac actin and Xbra, is greatly diminished, while the induction of other genes, including the head organizer-specific genes gsc and Xlim-1, is less sensitive. These results are consistent with the phenotype of the truncated FGF receptor-injected embryo and imply that the activin induction of mesoderm depends on FGF, with some genes requiring a higher level of FGF signaling than others.

REFERENCES

    1. Amaya E.,
    2. Musci T. J.,
    3. Kirschner M. W.
    (1991) Expression of a dominant negative mutant of the FGF receptor disrupts mesoderm formation in Xenopus embryos. Cell 66, 257–70
    OpenUrlCrossRefPubMedWeb of Science
    1. Amaya E.,
    2. Stein P. A.,
    3. Musci T. J.,
    4. Kirschner M. W.
    (1993) FGF signaling in the early specification of mesoderm in Xenopus. Development 118, 477–487
    OpenUrlAbstract
    1. Blumberg B.,
    2. Wright C. V. E.,
    3. De Robertis E. M.,
    4. Cho K. W. Y.
    (1991) Organizer-specific homeobox genes in Xenopus laevis embryos. Science 253, 194–196
    OpenUrlAbstract/FREE Full Text
    1. Cho K. W. Y.,
    2. Blumberg B.,
    3. Steinbesser H.,
    4. De Robertis E. M.
    (1991) Molecular nature of Spemann's organizer: the role of the Xenopus homeobox gene goosecoid. Cell 67, 1111–1120
    OpenUrlCrossRefPubMedWeb of Science
    1. Christian J. L.,
    2. McMahon J. A.,
    3. McMahon A. P.,
    4. Moon R. T.
    (1991) Xwnt −8, a XenopusWnt −1/ int −1-related gene responsive to mesoderm inducing factors, may play a role in ventral mesodermal patterning during embryogenesis. Development 111, 1045–56
    OpenUrlAbstract/FREE Full Text
    1. Christian J. L.,
    2. Olson D. J.,
    3. Moon R. T.
    (1992) Xwnt −8 modifies the character of mesoderm induced by bFGF in isolated Xenopus ectoderm. EMBO J 11, 33–41
    OpenUrlPubMedWeb of Science
    1. Dale L.,
    2. Howes G.,
    3. Price B. M. J.,
    4. Smith J. C.
    (1992) Bone morphogenetic protein 4: a ventralizing factor in early Xenopus development. Development 115, 573–585
    OpenUrlAbstract
    1. Frank D.,
    2. Harland R. M.
    (1991) Transient expression of XMyoD in non-somite mesoderm of Xenopus gastrulae. Development 113, 1387–1393
    OpenUrlAbstract
    1. Green B. A.,
    2. Smith J. C.
    (1990) Graded changes in dose of a Xenopus activin A homologue elicit stepwise transitions in embryonic cell fate. Nature 347, 391–394
    OpenUrlCrossRefPubMed
    1. Green J. B. A.,
    2. Howes G.,
    3. Symes K.,
    4. Cooke J.,
    5. Smith J. C.
    (1990) The biological effects of XTC-MIF: quantitative comparison with Xenopus bFGF. Development 108, 173–183
    OpenUrlAbstract
    1. Green J. B. A.,
    2. New H. V.,
    3. Smith J. C.
    (1992) 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, 1–20
    OpenUrlCrossRefPubMedWeb of Science
    1. Hopwood N. D.,
    2. Pluck A.,
    3. Gurdon J. B.
    (1989) MyoD expression in the forming somites is an early response to mesoderm induction in Xenopus embryos. EMBO 8, 3409–3417
    OpenUrlPubMedWeb of Science
    1. Isaacs H. V.,
    2. Tannahill D.,
    3. Slack J. M. W.
    (1992) Expression of a novel FGF in the Xenopus embryo. A new candidate inducing factor for mesoderm formation and anteroposterior specification. Development 114, 711–720
    OpenUrlAbstract
    1. Jonas E.,
    2. Sargent T. D.,
    3. Dawid I. B.
    (1985) Epidermal keratin gene expressed in embryos of Xenopus laevis. Proc. Natl. Acad. Sci. USA 82, 5413–5417
    OpenUrlAbstract/FREE Full Text
    1. Jones C. M.,
    2. Lyons K. M.,
    3. Lapan P. M.,
    4. Wright C. V. E.,
    5. Hogan B. L. M.
    (1992) DVR-4 (bone morphogenetic protein-4) as a posterior ventralizing factor in Xenopus mesoderm induction. Development 115, 639–647
    OpenUrlAbstract
    1. Kimelman D.,
    2. Abraham J. A.,
    3. Haaparanta T.,
    4. Palisi T. M.,
    5. Kirschner M.
    (1988) The presence of FGF in the frog egg: its role as a natural mesoderm inducer. Science 242, 1053–1056
    OpenUrlAbstract/FREE Full Text
    1. Kimelman D.,
    2. Christian J. L.,
    3. Moon R. T.
    (1992) Synergistic principles of development: overlapping patterning systems in Xenopus mesoderm induction. Development 116, 1–9
    OpenUrlAbstract
    1. Kimelman D.,
    2. Kirschner M.
    (1987) Synergistic induction of mesoderm by FGF and TGF-β and the identification of an mRNA coding for FGF in the early Xenopus embryo. Cell 51, 869–877
    OpenUrlCrossRefPubMedWeb of Science
    1. Kintner C. R.,
    2. Melton D. A.
    (1987) Expression of Xenopus N-CAM RNA in ectoderm is an early response to neural induction. Development 99, 311–.
    OpenUrlAbstract
    1. Krieg P.,
    2. Melton D.
    (1984) Functional messenger RNAs are produced by SP6 in vitro transcription of cloned DNAs. Nucl. Acids Res 12, 7057–7070
    OpenUrlAbstract/FREE Full Text
    1. Krieg P. A.,
    2. Melton D. A.
    (1985) Developmental regulation of a gastrula-specific gene injected into fertilized Xenopus eggs. EMBO J 4, 3463–3471
    OpenUrlPubMedWeb of Science
    1. Krieg P. A.,
    2. Varnum S.,
    3. Wormington M. W.,
    4. Melton D. A.
    (1989) The mRNA encoding elongation factor 1-(EF-1) is a major transcript of the midblastula transition. Dev. Biol 133, 93–100
    OpenUrlCrossRefPubMedWeb of Science
    1. LaBonne C.,
    2. Whitman M.
    (1994) Mesoderm induction by activin requires FGF mediated intracellular signals. Development 120,
    1. Lee P. L.,
    2. Johnson D. E.,
    3. Cousens L. S.,
    4. Fried V. A.,
    5. Williams L. T.
    (1989). Purification and complementary DNA cloning of a receptor for basic fibroblast growth factor. Science 245, 57–60
    OpenUrlCrossRefPubMedWeb of Science
    1. MacNicol A. M.,
    2. Muslin A. J.,
    3. Williams L. T.
    (1993) Raf-1 kinase is essential for early Xenopus development and mediates the induction of mesoderm by FGF. Cell 73, 571–584
    OpenUrlAbstract/FREE Full Text
    1. Melton D. A.,
    2. Krieg P. A.,
    3. Rebagliati M. R.,
    4. Maniatis T.,
    5. Zinn K.,
    6. Green M. R.
    (1984) Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter. Nucl. Acids Res 12, 7035–7056
    OpenUrlCrossRefPubMed
    1. Mohun T. J.,
    2. Brennan S.,
    3. Dathan N.,
    4. Fairman S.,
    5. Gurdon J. B.
    (1984) Cell type-specific activation of actin genes in the early amphibian embryo. Nature 311, 716–721
    OpenUrlCrossRefPubMedWeb of Science
    1. Newport J.,
    2. Kirschner M. W.
    (1982) A major developmental transition in early Xenopus embryos. I. Characterization and timing of cellular changes at the midblastula stage. Cell 30, 675–686
    OpenUrlAbstract/FREE Full Text
    1. Northrop J.,
    2. Kimelman D.
    (1993) Dorsal-ventral differences in response to FGF mediated induction in Xenopus. Dev. Biol. in press,
    1. Sargent M. G.,
    2. Bennett M. F.
    (1990). Identification in Xenopus of a structural homologue of the Drosophila gene Snail. Development 109, 967–973
    OpenUrlAbstract
    1. Sive H. L.
    (1993) The frog prince-cess: A molecular formula for dorsoventral patterning in Xenopus. Genes Dev 7, 1–12
    OpenUrlCrossRefPubMedWeb of Science
    1. Slack J. M. W.,
    2. Isaacs H. V.
    (1989) Presence of basic fibroblast growth factor in the early Xenopus embryo. Development 105, 147–153
    OpenUrlPubMedWeb of Science
    1. Smith J. C.,
    2. Price B. M. J.,
    3. Green J. B. A.,
    4. Weigel D.,
    5. Herrmann B. G.
    (1991) Expression of a Xenopus homolog of brachyury (T) is an immediate-early response to mesoderm induction. Cell 67, 79–87
    OpenUrlAbstract
    1. Smith J. C.,
    2. Slack J. M.
    (1983) Dorsalization and neural induction: properties of the organizer in Xenopus laevis. J. Embryol. Exp. Morph 78, 299–317
    OpenUrlCrossRefPubMedWeb of Science
    1. Smith J. C.,
    2. Symes K.,
    3. Hynes R. O.,
    4. DeSimone D.
    (1990) Mesoderm induction and the control of gastrulation in Xenopus laevis: the roles of fibronectin and integrins. Development 108, 229–238
    OpenUrlCrossRefPubMedWeb of Science
    1. Smith W. C.,
    2. Harland R. M.
    (1991) Injected Xwnt −8 acts early in Xenopus embryos to promote formation of a vegetal dorsalizing center. Cell 67, 753–766
    OpenUrlCrossRefPubMedWeb of Science
    1. Smith W. C.,
    2. Harland R. M.
    (1992) Expression cloning of noggin, a new dorsalizing factor localized in the Spemann organizer in Xenopus embryos. Cell 70, 829–840
    OpenUrlAbstract/FREE Full Text
    1. Sokol S. Y.,
    2. Melton D. A.
    (1992) Interaction of Wnt and activin in dorsal mesoderm induction in Xenopus. Dev. Biol 154, 348–55
    OpenUrlAbstract/FREE Full Text
    1. Taira M.,
    2. Jamrich M.,
    3. Good P. J.,
    4. Dawid I. B.
    (1992) The LIM domain-containing homeobox gene Xlim-1 is expressed specfically in the organizer region of Xenopus gastrula embryos. Genes Dev 6, 356–366
    OpenUrlCrossRefPubMedWeb of Science
    1. Tannahill D.,
    2. Isaacs H. V.,
    3. Close M. J.,
    4. Peters G.,
    5. Slack J. M. W.
    (1992) Developmental expression of the Xenopusint −2 (FGF-3) gene: activation by mesodermal and neural induction. Development 115, 695–702
    OpenUrlAbstract/FREE Full Text
    1. Ullrich A.,
    2. Schlessinger J.
    (1990) Signal transduction by receptors with tyrosine kinase activity. Cell 61, 203–212
    OpenUrlCrossRefPubMed
    1. von Dassow G.,
    2. Schmidt J. E.,
    3. Kimelman D.
    (1993) Induction of the Xenopus organizer: expression and regulation of Xnot, a novel FGF and activin-regulated homeobox gene. Genes Dev 7, 355–366
    1. Whitman M.,
    2. Melton D. A.
    (1992) Involvement of p21rasin Xenopus mesoderm induction. Nature 357, 252–254
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JOURNAL ARTICLES
Activin-mediated mesoderm induction requires FGF
R.A. Cornell, D. Kimelman
Development 1994 120: 453-462;
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