Advertisement
JOURNAL ARTICLES
Fibroblast growth factor is a direct neural inducer, which combined with noggin generates anterior-posterior neural pattern
T.M. Lamb, R.M. Harland
Development 1995 121: 3627-3636;

Summary

Neural tissue in developing Xenopus embryos is induced by signals from the dorsal mesoderm. Induction of anterior neural tissue could be mediated by noggin, a secreted polypeptide found in dorsal mesoderm. We show that bFGF, a known mesoderm inducer of blastula staged ectoderm, induces neural tissue from gastrula stage ectoderm. The type of neural tissue induced by bFGF from stage 10.25 ectoderm is posterior, as marked by Hox B9 expression. When bFGF and noggin are combined on early gastrula stage ectoderm, a more complete neural pattern is generated and no mesodermal tissue is detected. Explants treated with noggin and bFGF elongate and display distinct anterior and posterior ends marked by otx2 and Hox B9 expression, respectively. Furthermore, treatment of early gastrula ectoderm with noggin and bFGF results in the induction of En-2, a marker of the midbrain-hindbrain junction and Krox 20, a marker of the third and fifth rhombomeres of the hindbrain. Neither of these genes is induced by noggin alone or bFGF alone at this stage, suggesting a synergy in anterior-posterior neural patterning. The response of later gastrula (stage 11–12) ectoderm to bFGF changes so that Krox 20 and En-2 are induced by bFGF alone, while induction of more posterior tissue marked by Hox B9 is eliminated. The dose of bFGF affects the amount of neural tissue induced, but has little effect on the anterior-posterior character, rather the age of the ectoderm treated is the determinant of the response. Thus, an FGF signal may account for posterior neural induction, and anterior-posterior neural patterning could be partly explained by the actions of noggin and FGF, together with the changing response of the ectoderm to these factors.

Reference

    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, 257–270
    OpenUrlCrossRefPubMedWeb of Science
    1. Amaya E.,
    2. Stein P. A.,
    3. Musci T. J.,
    4. Kirschner M. W.
    (1993) FGF signalling in the early specification of mesoderm in Xenopus. Development 118, 477–487
    OpenUrlAbstract
    1. Balak K.,
    2. Jacobson M.,
    3. Sunshine J.,
    4. Rutishauser U.
    (1987) Neural cell adhesion molecule expression in Xenopus embryos. Dev. Biol 119, 540–550
    OpenUrlCrossRefPubMedWeb of Science
    1. Bieker J. J.,
    2. Yazdani-Buicky M.
    (1992) Distribution of type II collagen mRNA in Xenopus embryos visualized by whole-mount in situ hybridization. J. Histochem. Cytochem 40, 1117–1120
    OpenUrlAbstract/FREE Full Text
    1. Blitz I. L.,
    2. Cho K. W. Y.
    (1995) Anterior neurectoderm is progressively induced during gastrulation: the role of the Xenopus homeobox gene orthodenticle. Development 121, 993–1004
    OpenUrlAbstract
    1. Blumberg B.,
    2. Wright C. V.,
    3. De Robertis E. M.,
    4. Cho K. W.
    (1991) Organizer-specific homeobox genes in Xenopus laevis embryos. Science 253, 194–196
    OpenUrlAbstract/FREE Full Text
    1. Bolce M. E.,
    2. Hemmati-Brivanlou A.,
    3. Kushner P. D.,
    4. Harland R. M.
    (1992) Ventral ectoderm of Xenopus forms neural tissue, including hindbrain, in response to activin. Development 115, 681–688
    OpenUrlAbstract
    1. Bradley L. C.,
    2. Snape A.,
    3. Bhatt S.,
    4. Wilkinson D. G.
    (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
    OpenUrlCrossRefPubMedWeb of Science
    1. Cho K. W.,
    2. Blumberg B.,
    3. Steinbeisser 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. Condie B. G.,
    2. Harland R. M.
    (1987) Posterior expression of a homeobox gene in early Xenopus embryos. Development 101, 93–105
    OpenUrlAbstract/FREE Full Text
    1. Deng C. X.,
    2. Wynshaw-Boris A.,
    3. Shen M. M.,
    4. Daugherty C.,
    5. Ornitz D. M.,
    6. Leder P.
    (1994) Murine FGFR-1 is required for early postimplantation growth and axial organization. Genes Dev 8, 3045–3057
    OpenUrlAbstract/FREE Full Text
    1. Dixon J. E.,
    2. Kintner C. R.
    (1989) Cellular contacts required for neural induction in Xenopus embryos: evidence for two signals. Development 106, 749–757
    OpenUrlAbstract/FREE Full Text
    1. Doniach T.
    (1993) Planar and vertical induction of anteroposterior pattern during the development of the amphibian central nervous system. J. Neurobiol 24, 1256–1275
    OpenUrlCrossRefPubMedWeb of Science
    1. Doniach T.,
    2. Phillips C. R.,
    3. Gerhart J. C.
    (1992) Planar induction of anteroposterior pattern in the developing central nervous system of Xenopus laevis. Science 257, 542–545
    OpenUrlAbstract/FREE Full Text
    1. Feldman B.,
    2. Poueymirou W.,
    3. Papaioannou V.E.,
    4. DeChiara T.M.,
    5. Goldfarb M.
    (1995) Requirement of FGF-4 for postimplantation mouse development. Science 267, 246–9
    OpenUrlAbstract/FREE Full Text
    1. Godsave S.,
    2. Dekker E. J.,
    3. Holling T.,
    4. Pannese M.,
    5. Boncinelli E.,
    6. Durston A.
    (1994) Expression patterns of Hoxb genes in the Xenopus embryo suggest roles in anteroposterior specification of the hindbrain and in dorsoventral patterning of the mesoderm. Dev. Bio.l 166, 465–476
    OpenUrlCrossRefPubMedWeb of Science
    1. Godsave S. F.,
    2. Slack J. M.
    (1991) Single cell analysis of mesoderm formation in the Xenopus embryo. Development 111, 523–530
    OpenUrlAbstract
    1. Gospodarowicz D.
    (1990) Fibroblast growth factor and its involvement in developmental processes. Curr. Top. Dev. Bio.l 24, 57–93
    OpenUrlCrossRefPubMed
    1. Green J. B.,
    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.,
    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, 731–739
    OpenUrlCrossRefPubMedWeb of Science
    1. Grunz H.,
    2. Tacke L.
    (1989) Neural differentiation of Xenopus laevis ectoderm takes place after disaggregation and delayed reaggregation without inducer. Cell Differ. De 28, 211–217
    OpenUrlCrossRefPubMedWeb of Science
    1. Gurdon J. B.,
    2. Fairman S.,
    3. Mohun T. J.,
    4. Brennan S.
    (1985) Activation of muscle-specific actin genes in Xenopus development by an inducer between animal and vegetal cells of a blastula. Cell 41, 913–922
    OpenUrlCrossRefPubMedWeb of Science
    1. Harland R. M.
    (1994) Neural induction in Xenopus. Curr. Opin. Genet. Dev 4, 543–549
    OpenUrlCrossRefPubMed
    1. Hebert J.M.,
    2. Rosenquist T.,
    3. Gotz J.,
    4. Martin G.R.
    (1994) FGF5 as a regulator of the hair growth cycle: evidence from targeted and spontaneous mutations. Cell 78, 1017–1025
    OpenUrlCrossRefPubMedWeb of Science
    1. Hemmati-Brivanlou A.,
    2. de la Torre J. R.,
    3. Holt C.,
    4. Harland R. M.
    (1991) Cephalic expression and molecular characterization of Xenopus En-2. Development 111, 715–724
    OpenUrlAbstract
    1. Hemmati-Brivanlou A.,
    2. Frank D.,
    3. Bolce M. E.,
    4. Brown B. D.,
    5. Sive H. L.,
    6. Harland R. M.
    (1990) Localization of specific mRNAs in Xenopus embryos by whole-mount in situ hybridization. Development 110, 325–330
    OpenUrlAbstract/FREE Full Text
    1. Hemmati-Brivanlou A.,
    2. Kelly O. G.,
    3. Melton D. A.
    (1994) Follistatin, an antagonist of activin, is expressed in the Spemann organizer and displays direct neuralizing activity. Cell 77, 283–295
    OpenUrlCrossRefPubMedWeb of Science
    1. Hemmati-Brivanlou A.,
    2. Melton D. A.
    (1992) A truncated activin receptor inhibits mesoderm induction and formation of axial structures in Xenopus embryos [see comments]. Nature 359, 609–614
    OpenUrlCrossRefPubMed
    1. Hemmati-Brivanlou A.,
    2. Melton D. A.
    (1994) Inhibition of activin receptor signaling promotes neuralization in Xenopus. Cell 77, 273–281
    OpenUrlCrossRefPubMedWeb of Science
    1. Hemmati-Brivanlou A.,
    2. Stewart R. M.,
    3. Harland R. M.
    (1990) Region-specific neural induction of an engrailed protein by anterior notochord in Xenopus. Science 250, 800–802
    OpenUrlAbstract/FREE Full Text
    1. Isaacs H. V.,
    2. Tannahill D.,
    3. Slack J. M.
    (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. Keller R. E.,
    2. Danilchik M.,
    3. Gimlich R.,
    4. Shih J.
    (1985) The function and mechanism of convergent extension during gastrulation of Xenopus laevis. J Embryol. Exp. Morph 89, 185–209
    1. Kengaku M.,
    2. Okamoto H.
    (1993) Basic fibroblast growth factor induces differentiation of neural tube and neural crest lineages of cultured ectoderm cells from Xenopus gastrula. Development 119, 1067–1078
    OpenUrlAbstract
    1. Kimelman D.,
    2. Abraham J. A.,
    3. Haaparanta T.,
    4. Palisi T. M.,
    5. Kirschner M. W.
    (1988) The presence of fibroblast growth factor in the frog egg: its role as a natural mesoderm inducer. Science 242, 1053–1056
    OpenUrlAbstract/FREE Full Text
    1. Kintner C. R.,
    2. Dodd J.
    (1991) Hensen's node induces neural tissue in Xenopus ectoderm. Implications for the action of the organizer in neural induction. Development 113, 1495–1505
    OpenUrlAbstract
    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, 311–325
    OpenUrlAbstract
    1. Knecht A. K.,
    2. Good P. J.,
    3. Dawid I. B.,
    4. Harland R. M.
    (1995) Dorsal-ventral patterning and differentiation of noggin-induced neural tissue in the absence of mesoderm. Development 121, 1927–1936
    OpenUrlAbstract
    1. Lamb T. M.,
    2. Knecht A. K.,
    3. Smith W. C.,
    4. Stachel S. E.,
    5. Economides A. N.,
    6. Stahl N.,
    7. Yancopolous G. D.,
    8. Harland R. M.
    (1993) Neural induction by the secreted polypeptide noggin. Science 262, 713–718
    OpenUrlAbstract/FREE Full Text
    1. Mansour S. L.,
    2. Goddard J. M.,
    3. Capecchi M. R.
    (1993) Mice homozygous for a targeted disruption of the proto-oncogene int-2 have developmental defects in the tail and inner ear. Development 117, 13–28
    OpenUrlAbstract/FREE Full Text
    1. Pannese M.,
    2. Polo C.,
    3. Andreazzoli M.,
    4. Vignali R.,
    5. Kablar B.,
    6. Barsacchi G.,
    7. Boncinelli E.
    (1995) The Xenopus homologue of Otx2 is a maternal homeobox gene that demarcates and specifies anterior body regions. Development 121, 707–720
    OpenUrlAbstract
    1. Placzek M.,
    2. Yamada T.,
    3. Tessier-Lavigne M.,
    4. Jessell T.,
    5. Dodd J.
    (1991) Control of dorsoventral pattern in vertebrate neural development: induction and polarizing properties of the floor plate. Development 2, 105–122
    1. Richter K.,
    2. Good P. J.,
    3. Dawid I. B.
    (1990) A developmentally regulated, nervous system-specific gene in Xenopus encodes a putative RNA-binding protein. New Biol 2, 556–565
    OpenUrlPubMed
    1. Saha M. S.,
    2. Grainger R. M.
    (1992) A labile period in the determination of the anterior-posterior axis during early neural development in Xenopus. Neuron 8, 1003–1014
    OpenUrlCrossRefPubMedWeb of Science
    1. Servetnick M.,
    2. Grainger R. M.
    (1991) Changes in neural and lens competence in Xenopus ectoderm: evidence for an autonomous developmental timer. Development 112, 177–188
    OpenUrlAbstract
    1. Sharpe C. R.,
    2. Gurdon J. B.
    (1990) The induction of anterior and posterior neural genes in Xenopus laevis. Development 109, 765–774
    OpenUrlAbstract/FREE Full Text
    1. Sive H. L.,
    2. Hattori K.,
    3. Weintraub H.
    (1989) Progressive determination during formation of the anteroposterior axis inXenopus laevis. Cell 58, 171–180
    OpenUrlCrossRefPubMedWeb of Science
    1. Slack J. M. W.
    (1994) Inducing factors in Xenopus early embryos. Current Biology 4, 116–126
    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, 147–154
    OpenUrlAbstract
    1. Smith J. C.,
    2. Price B. M.,
    3. Green J. B.,
    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
    OpenUrlCrossRefPubMedWeb of Science
    1. Smith W. C.,
    2. Harland R. M.
    (1992) Expression cloning of noggin, a new dorsalizing factor localized to the Spemann organizer in Xenopus embryos. Cell 70, 829–840
    OpenUrlCrossRefPubMedWeb of Science
    1. Smith W. C.,
    2. Knecht A. K.,
    3. Wu M.,
    4. Harland R. M.
    (1993) Secreted noggin protein mimics the Spemann organizer in dorsalizing Xenopus mesoderm. Nature 361, 547–549
    OpenUrlCrossRefPubMed
    1. Smith W. C.,
    2. McKendry R.,
    3. Ribisi S.,
    4. Harland R. M.
    (1995) A nodal-related gene defines a physical and functional domain within the Spemann organizer. Cell 82, 37–46
    OpenUrlCrossRefPubMedWeb of Science
    1. Streit A.,
    2. Stern C. D.,
    3. Thery C.,
    4. Ireland G. W.,
    5. Aparicio S.,
    6. Sharpe M. J.,
    7. Gherardi E.
    (1995) A role for HGF/SF in neural induction and its expression in Hensen's node during gastrulation. Development 121, 813–824
    OpenUrlAbstract
    1. Su M. W.,
    2. Suzuki H. R.,
    3. Bieker J. J.,
    4. Solursh M.,
    5. Ramirez F.
    (1991) Expression of two nonallelic type II procollagen genes during Xenopus laevis embryogenesis is characterized by stage-specific production of alternatively spliced transcripts. J. Cell Biol 115, 565–575
    OpenUrlAbstract/FREE Full Text
    1. Thisse C.,
    2. Thisse B.,
    3. Halpern M. E.,
    4. Postlethwait J. H.
    (1994) Goosecoid expression in neurectoderm and mesendoderm is disrupted in zebrafish cyclops gastrulas. Dev. Biol 164, 420–429
    OpenUrlCrossRefPubMedWeb of Science
    1. Wilkinson D. G.,
    2. Bhatt S.,
    3. Chavrier P.,
    4. Bravo R.,
    5. Charnay P.
    (1989) Segment-specific expression of a zinc-finger gene in the developing nervous system of the mouse. Nature 337, 461–464
    OpenUrlCrossRefPubMed
    1. Williams E. J.,
    2. Furness J.,
    3. Walsh F. S.,
    4. Doherty P.
    (1994) Characterisation of the second messenger pathway underlying neurite outgrowth stimulated by FGF. Development 120, 1685–1693
    OpenUrlAbstract
    1. Wilson P. A.,
    2. Hemmati-Brivanlou A.
    (1995) Induction of epidermis and inhibition of neural fate by BMP 4. Nature 538, 331–333
    OpenUrl
    1. Wilson P. A.,
    2. Melton D. A.
    (1994) Mesodermal patterning by an inducer gradient depends on secondary cell-cell communication. Curr. Biol 4, 676–686
    OpenUrlCrossRefPubMedWeb of Science
    1. Wright C. V.,
    2. Morita E. A.,
    3. Wilkin D. J.,
    4. De Robertis E. M.
    (1990) The Xenopus XIHbox 6 homeo protein, a marker of posterior neural induction, is expressed in proliferating neurons. Development 109, 225–234
    OpenUrlAbstract
    1. Yamada T.,
    2. Placzek M.,
    3. Tanaka H.,
    4. Dodd J.,
    5. Jessell T. M.
    (1991) Control of cell pattern in the developing nervous system: polarizing activity of the floor plate and notochord. Cell 64, 635–647
    OpenUrlCrossRefPubMedWeb of Science
    1. Yamaguchi T. P.,
    2. Harpal K.,
    3. Henkemeyer M.,
    4. Rossant J.
    (1994) fgfr-1 is required for embryonic growth and mesodermal patterning during mouse gastrulation. Genes Dev 8, 3032–3044
    OpenUrlAbstract/FREE Full Text
Back to top

 Download PDF

Email
JOURNAL ARTICLES
Fibroblast growth factor is a direct neural inducer, which combined with noggin generates anterior-posterior neural pattern
T.M. Lamb, R.M. Harland
Development 1995 121: 3627-3636;
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
Alerts

Article navigation

Other journals from The Company of Biologists

Advertisement

An interview with Swathi Arur

Swathi Arur joined the team at Development as an Academic Editor in 2020. Her lab uses multidisciplinary approaches to understand female germline development and fertility. We met with her over Zoom to hear more about her life, her career and her love for C. elegans.

Jim Wells and Hanna Mikkola join our team of Editors

We are pleased to welcome James (Jim) Wells and Hanna Mikkola to our team of Editors. Jim joins us a new Academic Editor, taking over from Gordan Keller, and Hanna joins our team of Associate Editors. Find out more about their research interests and areas of expertise.

New funding scheme supports sustainable events

As part of our Sustainable Conferencing Initiative, we are pleased to announce funding for organisers that seek to reduce the environmental footprint of their event. The next deadline to apply for a Scientific Meeting grant is 26 March 2021.

Read & Publish participation continues to grow

“I’d heard of Read & Publish deals and knew that many universities, including mine, had signed up to them but I had not previously understood the benefits that these deals bring to authors who work at those universities.”

Professor Sally Lowell (University of Edinburgh) shares her experience of publishing Open Access as part of our growing Read & Publish initiative. We now have over 150 institutions in 15 countries and four library consortia taking part – find out more and view our full list of participating institutions.

Upcoming special issues

Imaging Development, Stem Cells and Regeneration
Submission deadline: 30 March 2021
Publication: mid-2021

The Immune System in Development and Regeneration
Guest editors: Florent Ginhoux and Paul Martin
Submission deadline: 1 September 2021
Publication: Spring 2022

Both special issues welcome Review articles as well as Research articles, and will be widely promoted online and at key global conferences.

Development presents...

Our successful webinar series continues into 2021, with early-career researchers presenting their papers and a chance to virtually network with the developmental biology community afterwards. Here, Michèle Romanos talks about her new preprint, which mixes experimentation in quail embryos and computational modelling to understand how heterogeneity in a tissue influences cell rate.

Save your spot at our next session:

10 March
Time: 9:00 (GMT)
Chaired by: Thomas Lecuit

Join our mailing list to receive news and updates on the series.