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Making a Neural Tube: Neural Induction and Neurulation

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Summary

The future central nervous system is derived from an unspecified sheet of ectoderm, with fate being instructed by signals emanating, in the main, from a specialized region of the early embryo, the organizer. The organizer secretes signals that have the net effect of inhibiting the BMP pathway, be it by extra-cellular antagonism or by intracellular modulation of the ability of the cell to perceive BMP signals. Other factors also play a role in neural induction, for example, the FGF family of molecules, but their exact role in neural induction remain unknown. As more players are identified in what undoubtedly will be a signaling network leading to neural induction, the exact molecular mechanism of neural induction can be established.

Once induced, the neuroepithelium rolls into the neural tube. One model, and one that has gained widespread acceptance, is the hinge point model. In this model, both extrinsic (i.e., outside the neural plate) and intrinsic forces cooperate and synergize in bending the neural plate. Although the cellular behaviors of much of this process have been well characterized, the molecular bases for these behaviors have so far proved elusive. The relationship between induction of the neuroepithelium and its subsequent morphological movements is of particular interest to the developmental neurobiologist.

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References

  • Abercrombie, M. and Bellairs, R., 1954, The effects in chick blastoderms of replacing the primitive node by a graft of posterior primitive streak. J. Embryol. Exp. Morph. 2:55–72.

    Google Scholar 

  • Afrakhte, M., Moren, A., Jossan, S., Itoh, S., Sampath, K., Westermark, B. et al., 1998, Induction of inhibitory Smad6 and Smad7 mRNA by TGF-beta family members, Biochem. Biophys. Res. Commun. 249: 505–511.

    Article  CAS  PubMed  Google Scholar 

  • Alvarez, I.S. and Schoenwolf, G.C., 1992, Expansion of surface epithelium provides the major extrinsic force for bending of the neural plate, J. Exp. Zool. 261:340–348.

    Article  CAS  PubMed  Google Scholar 

  • Attisano, L. and Tuen Lee-Hoeflich, S. 2001, The Smads, Genome Biol. 2:3010.1–3010.8.

    Article  Google Scholar 

  • Bachiller, D., Klingensmith, J., Kemp, C., Belo, J.A., Anderson, R.M., May, S.R. et al., 2000, The organizer factors Chordin and Noggin are required for mouse forebrain development, Nature 403:658–661.

    CAS  ADS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Barth, L.G., 1941, Neural differentiation without organizer, J. Exp. Zool. 87:471–481.

    Article  Google Scholar 

  • Beddington, R.S., 1994, Induction of a second neural axis by the mouse node, Development 120:613–620.

    CAS  PubMed  Google Scholar 

  • Beddington, R., 1998, Mouse mutagenesis: From gene to phenotype and back again, Curr. Biol. 8:R840–R842.

    Article  CAS  PubMed  Google Scholar 

  • Bhushan, A., Chen, Y., and Vale, W., 1998, Smad7 inhibits mesoderm formation and promotes neural cell fate in Xenopus embryos, Dev. Biol. 200:260–268.

    Article  CAS  PubMed  Google Scholar 

  • Biehs, B., Francois, V., and Bier, E., 1996, The Drosophila short gastrulation gene prevents Dpp from autoactivating and suppressing neurogenesis in the neuroectoderm, Genes Dev. 10:2922–2934.

    CAS  PubMed  Google Scholar 

  • Boterenbrood, E.C. and Nieuwkoop, P.D., 1973, The formation of the mesoderm in urodelean amphibians. V. Its regional induction by the endoderm, Wilhelm Roux’Arch. Dev. Biol. 173:319–332.

    Google Scholar 

  • Bouwmeester, T., Kim, S., Sasai, Y., Lu, B., and De Robertis, E.M., 1996, Cerberus is a head-inducing secreted factor expressed in the anterior endoderm of Spemann’s organizer, Nature 382:595–601.

    Article  CAS  ADS  PubMed  Google Scholar 

  • Callebaut, M. and Van Nueten, E., 1994, Rauber’s (Koller’s) sickle: The early gastrulation organizer of the avian blastoderm, Eur. J. Morph. 32:35–48.

    CAS  Google Scholar 

  • Capecchi, M.R., 1989, The new mouse genetics: Altering the genome by gene targeting, Trends Genet. 5:70–76.

    Article  CAS  PubMed  Google Scholar 

  • Colas, J.F. and Schoenwolf, G.C., 2001, Towards a cellular and molecular understanding of neurulation. Dev. Dyn. 221:117–145.

    Article  CAS  PubMed  Google Scholar 

  • Connolly, D.J., Patel, K., Seleiro, E.A., Wilkinson, D.G., and Cooke, J., 1995, Cloning, sequencing, and expressional analysis of the chick homologue of follistatin, Dev. Genet. 17:65–77.

    Article  CAS  PubMed  Google Scholar 

  • Connolly, D.J., Patel, K., and Cooke, J., 1997, Chick noggin is expressed in the organizer and neural plate during axial development, but offers no evidence of involvement in primary axis formation, Int. J. Dev. Biol. 41:389–396.

    CAS  PubMed  Google Scholar 

  • Cornell, R.A., Musci, T.J., and Kimelman, D., 1995, FGF is a prospective competence factor for early activin-type signals in Xenopus mesoderm induction, Development 121:2429–2437.

    CAS  PubMed  Google Scholar 

  • Cruz, Y.P., 1997, Mammals. In Embryology: Constructing the Organism (S.C. Gilbert and A.M. Raunio, eds.), Sinauer, Sunderland, MA, pp. 459–492.

    Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • Darnell, D.K., Stark, M.R., and Schoenwolf, G.C., 1999, Timing and cell interactions underlying neural induction in the chick embryo, Development 126:2505–2514.

    CAS  PubMed  Google Scholar 

  • Degen, W.G., Weterman, M.A., van Groningen, J.J., Cornelissen, I.M., Lemmers, J.P., Agterbos, M.A. et al., 1996, Expression of nma, a novel gene, inversely correlates with the metastatic potential of human melanoma cell lines and xenografts, Int. J. Cancer 65:460–465.

    Article  CAS  PubMed  Google Scholar 

  • Driever, W., 1995, Axis formation in zebrafish, Curr. Opin. Genet. Dev. 5:610–618.

    Article  CAS  PubMed  Google Scholar 

  • Dudley, A.T. and Robertson, E.J., 1997, Overlapping expression domains of bone morphogenetic protein family members potentially account for limited tissue defects in BMP7 deficient embryos, Dev. Dyn 208:349–362.

    Article  CAS  PubMed  Google Scholar 

  • Dudley, A.T., Lyons, K.M., and Robertson, E.J., 1995, A requirement for bone morphogenetic protein-7 during development of the mammalian kidney and eye, Genes Dev. 9:2795–2807.

    CAS  PubMed  Google Scholar 

  • Faure, S., de Santa Barbara, P., Roberts, D.J., Whitman, M., 2002, Endogenous patterns of BMP signaling during early chick development, Dev. Biol. 244(1):44–65.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • Feldman, B., Gates, M.A., Egan, E.S., Dougan, S.T., Rennebeck, G., Sirotkin, H.I. et al., 1998, Zebrafish organizer development and germ-layer formation require nodal-related signals, Nature 395:181–185.

    CAS  ADS  PubMed  Google Scholar 

  • Geinitz, B., 1925, Embryonale transplantation zwischen Urodelen und Anuren, Roux Arch. Entwicklungsmech 106:357–408.

    Google Scholar 

  • Gimlich, R.L. and Cooke, J., 1983, Cell lineage and the induction of second nervous systems in amphibian development, Nature 306:471–473.

    Article  CAS  PubMed  Google Scholar 

  • Godsave, S.F. and Slack, J.M., 1989. Clonal analysis of mesoderm induction in Xenopus laevis, Dev. Biol. 134:486–490.

    Article  CAS  PubMed  Google Scholar 

  • Gomez-Skarmeta, J., de La Calle-Mustienes, E., and Modolell, J., 2001, The Wnt-activated Xiro1 gene encodes a repressor that is essential for neural development and downregulates Bmp4, Development 128:551–560.

    CAS  PubMed  Google Scholar 

  • Gritsman, K., Zhang, J., Cheng, S., Heckscher, E., Talbot, W.S., and Schier, A.F., 1999, The EGF-CFC protein one-eyed pinhead is essential for nodal signaling, Cell 97:121–132.

    Article  CAS  PubMed  Google Scholar 

  • Grotewold, L., Plum, M., Dildrop, R., Peters, T., and Ruther, U., 2001, Bambi is coexpressed with Bmp-4 during mouse embryogenesis, Mech. Dev. 100:327–330.

    Article  CAS  PubMed  Google Scholar 

  • Grunz, H., 1997, Neural induction in amphibians, Curr. Top. Dev. Biol. 35:191–228.

    CAS  PubMed  Google Scholar 

  • Grunz, H. and Tacke, L., 1989, Neural differentiation of Xenopus laevis ectoderm takes place after disaggregation and delayed reaggregation without inducer, Cell. Diff. Dev. 28:211–217.

    Article  CAS  Google Scholar 

  • Grunz, H. and Tacke, L., 1990, Extracellular matrix components prevent neural differentiation of disaggregated Xenopus ectoderm cells, Cell. Diff. Dev. 32:117–123.

    Article  CAS  Google Scholar 

  • Hackett, D.A., Smith, J.L., and Schoenwolf, G.C., 1997, Epidermal ectoderm is required for full elevation and for convergence during bending of the avian neural plate, Dev. Dyn. 210:1–11.

    Article  Google Scholar 

  • Hemmati-Brivanlou, A. and Melton, D.A., 1992, A truncated activin receptor inhibits mesoderm induction and formation of axial structures in Xenopus embryos, Nature 359:609–614.

    Article  CAS  ADS  PubMed  Google Scholar 

  • Hemmati-Brivanlou, A. and Melton, D.A., 1994, Inhibition of activin receptor signaling promotes neuralization in Xenopus, Cell 77:273–281.

    CAS  PubMed  Google Scholar 

  • Hemmati-Brivanlou, A. and Thomsen, G.H., 1995, Ventral mesodermal patterning in Xenopus embryos: Expression patterns and activities of BMP-2 and BMP-4, Dev. Genet. 17:78–89.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • Holley, S.A., Jackson, P.D., Sasai, Y., Lu, B., De Robertis, E.M., Hoffmann, F.M. et al., 1995, A conserved system for dorsal-ventral patterning in insects and vertebrates involving sog and chordin, Nature 376:249–253.

    Article  CAS  ADS  PubMed  Google Scholar 

  • Holley, S.A., Neul, J.L., Attisano, L., Wrana, J.L., Sasai, Y., O’Connor, M.B. et al., 1996, The Xenopus dorsalizing factor noggin ventralizes Drosophila embryos by preventing DPP from activating its receptor, Cell 86:607–617.

    Article  CAS  PubMed  Google Scholar 

  • Holtfreter, J., 1933a, Nachweis der Induktionsfähigkelt abgetöteter Kiemteille, Roux Arch. Entwicklungsmech 129:584–633.

    Google Scholar 

  • Holtfreter, J., 1933b, Die totale Exogastrulation, eine Selbstrablösung des Ektoderms vom Entomesoderm, Roux Arch. Entwicklungsmech 129:669–793.

    Google Scholar 

  • Holtfreter, J., 1944, Neural differentiation of ectoderm through exposure to saline solution, J. Exp. Zool. 98:169–209.

    Google Scholar 

  • Holtfreter, J., 1947, Neural induction in explants that have passed through a sublethal cytolysis, J. Exp. Zool. 106:197–222.

    Article  CAS  PubMed  Google Scholar 

  • Hsu, D.R., Economides, A.N., Wang, X., Eimon, P.M., and Harland, R.M., 1998, The Xenopus dorsalizing factor Gremlin identifies a novel family of secreted proteins that antagonize BMP activities, Mol. Cell 1:673–683.

    Article  CAS  PubMed  Google Scholar 

  • Iemura, S., Yamamoto, T.S., Takagi, C., Uchiyama, H., Natsume, T., Shimasaki, S. et al., 1998, Direct binding of follistatin to a complex of bone-morphogenetic protein and its receptor inhibits ventral and epidermal cell fates in early Xenopus embryo, Proc. Natl. Acad. Sci. USA 95:9337–9342.

    Article  CAS  ADS  PubMed  Google Scholar 

  • Imai, Y., Gates, M.A., Melby, A.E., Kimelman, D., Schier, A.F., and Talbot, W.S., 2001, The homeobox genes vox and vent are redundant repressors of dorsal fates in zebrafish, Development 128:2407–2420.

    CAS  PubMed  Google Scholar 

  • Imamura, T., Takase, M., Nishihara, A., Oeda, E., Hanai, J., Kawabata, M. et al., 1997, Smad6 inhibits signalling by the TGF-beta superfamily, Nature 389:622–626.

    CAS  ADS  PubMed  Google Scholar 

  • Inoue, H., Imamura, T., Ishidou, Y., Takase, M., Udagawa, Y., Oka, Y. et al., 1998, Interplay of signal mediators of decapentaplegic (Dpp): Molecular characterization of mothers against dpp, Medea, and daughters against dpp, Mol. Biol. Cell. 9:2145–2156.

    CAS  PubMed  Google Scholar 

  • Jacobson, M., 1984, Cell lineage analysis of neural induction: Origins of cells forming the induced nervous system, Dev. Biol. 102:122–129.

    Article  CAS  PubMed  Google Scholar 

  • Jones, C.M., Lyons, K.M., Lapan, P.M., Wright, C.V., and Hogan, B.L., 1992, DVR-4 (bone morphogenetic protein-4) as a posterior-ventralizing factor in Xenopus mesoderm induction, Development 115:639–647.

    CAS  PubMed  Google Scholar 

  • Jones, C.M., Broadbent, J., Thomas, P.Q., Smith, J.C., and Beddington, R.S., 1999, An anterior signalling centre in Xenopus revealed by the homeobox gene XHex, Curr. Biol. 9:946–954.

    CAS  PubMed  Google Scholar 

  • Joubin, K. and Stern, C.D., 1999, Molecular interactions continuously define the organizer during the cell movements of gastrulation, Cell 98:559–571.

    Article  CAS  PubMed  Google Scholar 

  • Kane, D.A. and Kimmel, C.B., 1993, The zebrafish midblastula transition, Development 119:447–456.

    CAS  PubMed  Google Scholar 

  • Keller, R. and Winklbauer, R., 1992, Cellular basis of amphibian gastrulation, Curr. Top. Dev. Biol. 27:39–89.

    CAS  PubMed  Google Scholar 

  • Kengaku, M. and 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.

    CAS  PubMed  Google Scholar 

  • Khaner, O., 1998, The ability to initiate an axis in the avian blastula is concentrated mainly at a posterior site, Dev. Biol. 194:257–266.

    Article  CAS  PubMed  Google Scholar 

  • Khaner, O. and Eyal-Giladi, H., 1986, The embryo-forming potency of the posterior marginal zone in stages X through XII of the chick, Dev. Biol. 115:275–281.

    Article  CAS  PubMed  Google Scholar 

  • Kintner, C.R. and Melton, D.A., 1987, Expression of Xenopus N-CAM RNA in ectoderm is an early response to neural induction, Development 99:311–325.

    CAS  PubMed  Google Scholar 

  • Klingensmith, J., Ang, S.L., Bachiller, D., and Rossant, J., 1999, Neural induction and patterning in the mouse in the absence of the node and its derivatives, Dev. Biol. 216:535–549.

    Article  CAS  PubMed  Google Scholar 

  • Kretzschmar, M., Doody, J., and Massague, J., 1997, Opposing BMP and EGF signalling pathways converge on the TGF-beta family mediator Smad1, Nature 389:618–622.

    CAS  ADS  PubMed  Google Scholar 

  • Kretzschmar, M., Doody, J., Timokhina, I., and Massague, J., 1999, A mechanism of repression of TGFbeta/ Smad signaling by oncogenic Ras, Genes Dev. 13:804–816.

    CAS  PubMed  Google Scholar 

  • Ladher, R.K., Church, V.L., Allen, S., Robson, L., Abdelfattah, A., Brown, N.A. et al., 2000, Cloning and expression of the Wnt antagonists Sfrp-2 and Frzb during chick development, Dev. Biol. 218:183–198.

    Article  CAS  PubMed  Google Scholar 

  • Lagna, G., Hata, A., Hemmati-Brivanlou, A., and Massague, J., 1996, Partnership between DPC4 and SMAD proteins in TGF-beta signalling pathways, Nature 383:832–836.

    Article  CAS  ADS  PubMed  Google Scholar 

  • Lamb, T.M., Knecht, A.K., Smith, W.C., Stachel, S.E., Economides, A.N., Stahl, N. et al., 1993, Neural induction by the secreted polypeptide noggin, Science 262:713–718.

    CAS  ADS  PubMed  Google Scholar 

  • Langeland, J. and Kimmel, C.B., 1997, Fishes. In Embryology: Constructing the Organism (S.C. Gilbert and A.M. Raunio, eds.), Sinauer, Sunderland, MA, pp. 383–408.

    Google Scholar 

  • Launay, C., Fromentoux, V., Shi, D.L., and Boucaut, J.C., 1996, A truncated FGF receptor blocks neural induction by endogenous Xenopus inducers, Development 122:869–880.

    CAS  PubMed  Google Scholar 

  • Lawson, A. and Schoenwolf, G.C., 2001, New insights into critical events of avian gastrulation, Anat. Rec. 262:238–252.

    CAS  PubMed  Google Scholar 

  • Lawson, A., Anderson, H., and Schoenwolf, G.C., 2001, Cellular mechanisms of neural fold formation and morphogenesis in the chick embryo, Anat. Rec. 262:153–168.

    CAS  PubMed  Google Scholar 

  • LeSeur, J.A., Fortuno, E.S., 3rd, McKay, R.M., and Graff, J.M., 2002, Smad10 is required for formation of the frog nervous system, Dev. Cell. 2:771–783.

    Google Scholar 

  • Liu, F., Hata, A., Baker, J.C., Doody, J., Carcamo, J., Harland, R.M. et al., 1996, A human Mad protein acting as a BMP-regulated transcriptional activator, Nature 381:620–623.

    CAS  ADS  PubMed  Google Scholar 

  • Malacinski, G.M., Bessho, T., Yokota, C., Fukui, A., and Asashima, M., 1997, An essay on the similarities and differences between inductive interactions in anuran and urodele embryos, Cell. Mol. Life. Sci. 53: 410–417.

    Article  CAS  PubMed  Google Scholar 

  • Marx, A., 1925, Experimentelle Untersuchungen zur Frage der Determination der Medullarplatte, Roux Arch. Entwicklungsmech 105:20–44.

    Google Scholar 

  • Massague, J. and Chen, Y.G., 2000, Controlling TGF-beta signaling, Genes Dev. 14:627–644.

    CAS  PubMed  Google Scholar 

  • Moon, R.T. and Kimelman, D., 1998, From cortical rotation to organizer gene expression: Toward a molecular explanation of axis specification in Xenopus, Bioessays 20:536–545.

    Article  CAS  PubMed  Google Scholar 

  • Moustakas, A. and Heldin, C.H., 2002, From mono-to oligo-Smads: The heart of the matter in TGF-beta signal transduction, Genes Dev. 16:1867–1871.

    Article  CAS  PubMed  Google Scholar 

  • Mullins, M.C. and Nusslein-Volhard, C., 1993, Mutational approaches to studying embryonic pattern formation in the zebrafish, Curr. Opin. Genet. Dev. 3:648–654.

    Article  CAS  PubMed  Google Scholar 

  • Muñoz-Sanjuan, I. and Hemmati-Brivanlou, A., 2002, Neural induction, the default model and embryonic stem cells, Nat. Rev. Neurosci. 3:271–280.

    PubMed  Google Scholar 

  • Nakao, A., Afrakhte, M., Moren, A., Nakayama, T., Christian, J.L., Heuchel, R. et al., 1997, Identification of Smad7, a TGFbeta-inducible antagonist of TGF-beta signalling, Nature 389:631–635.

    CAS  ADS  PubMed  Google Scholar 

  • Newport, J. and Kirschner, M., 1982, A major developmental transition in early Xenopus embryos: II. Control of the onset of transcription, Cell 30:687–696.

    CAS  PubMed  Google Scholar 

  • Nieuwkoop, P.D., 1969, The formation of mesoderm in Urodelean amphibians. I. Induction by the endoderm, Wilhelm Roux’ Arch. Dev. Biol. 162:341–373.

    Google Scholar 

  • Nieuwkoop, P.D., 1999, The neural induction process; its morphogenetic aspects, Int. J. Dev. Biol. 43:615–623.

    CAS  PubMed  Google Scholar 

  • Nieuwkoop, P. and Faber, J., 1967. Normal table of Xenopus laevis, North-Holland Publishing Company, Amsterdam, pp. 1–252.

    Google Scholar 

  • Onichtchouk, D., Chen, Y.G., Dosch, R., Gawantka, V., Delius, H., Massague, J. et al. 1999, Silencing of TGF-beta signalling by the pseudoreceptor BAMBI, Nature 401:480–485.

    CAS  ADS  PubMed  Google Scholar 

  • Onichtchouk, D., Glinka, A., and Niehrs, C., 1998, Requirement for Xvent-1 and Xvent-2 gene function in dorsoventral patterning of Xenopus mesoderm, Development 125:1447–1456.

    CAS  PubMed  Google Scholar 

  • Oppenheimer, J., 1936, Transplantation experiments on developing teleosts (Fundulus and Perca), J. Exp. Zool. 72:409–437.

    Google Scholar 

  • Osada, J., and Maeda, N., 1998, Preparation of knockout mice, Meth. Mol. Biol. 110:79–92.

    CAS  Google Scholar 

  • Pera, E.M., Wessely, O., Li, S.Y., and De Robertis, E.M., 2001, Neural and head induction by insulin-like growth factor signals, Dev. Cell 1:655–665.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Psychoyos, D. and Stern, C.D., 1996, Restoration of the organizer after radical ablation of Hensen’s node and the anterior end of the primitive streak in the chick embryo, Development 122:3263–3273.

    CAS  PubMed  Google Scholar 

  • Rossant, J., Bernelot-Moens, C., and Nagy, A., 1993, Genome manipulation in embryonic stem cells, Philos. Trans. R. Soc. Lond. B. Biol. Sci. 339:207–215.

    CAS  ADS  PubMed  Google Scholar 

  • Sasai, Y. and De Robertis, E.M., 1997, Ectodermal patterning in vertebrate embryos, Dev. Biol. 182:5–20.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Sato, S.M. and Sargent, T.D., 1989, Development of neural inducing capacity in dissociated Xenopus embryos, Dev. Biol. 134:263–266.

    Article  CAS  PubMed  Google Scholar 

  • Sausedo, R.A., Smith, J.L., and Schoenwolf, G.C., 1997, Role of nonrandomly oriented cell division in shaping and bending of the neural plate, J. Comp. Neurol. 381:473–488.

    Article  CAS  PubMed  Google Scholar 

  • Saxén, L., 1961, Transfilter neural induction of amphibian ectoderm, Dev. Biol. 3:140–152.

    PubMed  Google Scholar 

  • Scherer, A. and Graff, J.M., 2000, Calmodulin differentially modulates Smad1 and Smad2 signaling, J. Biol. Chem. 275:41430–41438.

    CAS  PubMed  Google Scholar 

  • Schoenwolf, G.C., 1979, Histological and ultrastructural observations of tail bud formation in the chick embryo, Anat. Rec. 193:131–147.

    Article  CAS  PubMed  Google Scholar 

  • Schoenwolf, G.C., 1984. Histological and ultrastructural studies of secondary neurulation in mouse embryos. Am. J. Anat. 169:361–376.

    Article  CAS  PubMed  Google Scholar 

  • Schoenwolf, G.C., 1988, Microsurgical analyses of avian neurulation: Separation of medial and lateral tissues, J. Comp. Neurol. 276:498–507.

    Article  CAS  PubMed  Google Scholar 

  • Schoenwolf, G.C., 1997, Reptiles and birds. In Embryology: Constructing the Organism (S.C. Gilbert and A.M. Raunio, eds.), Sinauer, Sunderland, MA, pp. 437–458.

    Google Scholar 

  • Schoenwolf, G.C., 2001, Laboratory Studies of Vertebrate and Invertebrate Embryos. Guide and Atlas of Descriptive and Experimental Development, Prentice Hall, Upper Saddle River, NJ, pp. 100, 101.

    Google Scholar 

  • Schoenwolf, G.C. and Alvarez, I.S., 1989, Roles of neuroepithelial cell rearrangement and division in shaping of the avian neural plate. Development 106:427–439.

    CAS  PubMed  Google Scholar 

  • Schoenwolf, G.C. and DeLongo, J., 1980, Ultrastructure of secondary neurulation in the chick embryo, Am. J. Anat. 158:43–63.

    CAS  PubMed  Google Scholar 

  • Schoenwolf, G.C. and Franks, M.V., 1984, Quantitative analyses of changes in cell shapes during bending of the avian neural plate, Dev. Biol. 105:257–272.

    Article  CAS  PubMed  Google Scholar 

  • Schoenwolf, G.C. and Smith, J.L., 1990. Mechanisms of neurulation: Traditional viewpoint and recent advances, Development 109: 243–270.

    CAS  PubMed  Google Scholar 

  • Schoenwolf, G.C., Everaert, S., Bortier, H., and Vakaet, L., 1989, Neural plate-and neural tube-forming potential of isolated epiblast areas in avian embryos, Anat. Embryol. 179:541–549.

    Article  CAS  PubMed  Google Scholar 

  • Smith, J.C., 1989, Mesoderm induction and mesoderm-inducing factors in early amphibian development, Development 105:665–677.

    CAS  PubMed  Google Scholar 

  • Smith, J.L. and Schoenwolf, G.C., 1987, Cell cycle and neuroepithelial cell shape during bending of the chick neural plate, Anat. Rec. 218:196–206.

    Article  CAS  PubMed  Google Scholar 

  • Smith, J.L. and Schoenwolf, G.C., 1988, Role of cell-cycle in regulating neuroepithelial cell shape during bending of the chick neural plate, Cell. Tissue Res. 252:491–500.

    Article  CAS  PubMed  Google Scholar 

  • Smith, J.L. and Schoenwolf, G.C., 1989, Notochordal induction of cell wedging in the chick neural plate and its role in neural tube formation, J. Exp. Zool. 250:49–62.

    Article  CAS  PubMed  Google Scholar 

  • Smith, J.L. and Schoenwolf, G.C., 1997, Neurulation: Coming to closure, Trends Neurosci. 20:510–517.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • Smith, W.C., McKendry, R., Ribisi, S., Jr., and Harland, R.M., 1995, A nodalrelated gene defines a physical and functional domain within the Spemann organizer, Cell 82:37–46.

    CAS  PubMed  Google Scholar 

  • Soriano, P., 1995, Gene targeting in ES cells, Annu. Rev. Neurosci. 18:1–18.

    Article  CAS  PubMed  Google Scholar 

  • Souchelnytskyi, S., Nakayama, T., Nakao, A., Moren, A., Heldin, C.H., Christian, J.L. et al. 1998, Physical and functional interaction of murine and Xenopus Smad7 with bone morphogenetic protein receptors and transforming growth factor-beta receptors, J. Biol. Chem. 273:25364–25370.

    Article  CAS  PubMed  Google Scholar 

  • Spemann, H. and Mangold, H., 1924, Über die Inducktion won Embryoanalagen durch Implantation artfremder Organisatoren, Roux Arch. Entwicklungsmech 100:599–638.

    Google Scholar 

  • Spemann, H. and Mangold, H., 2001, Induction of embryonic primordia by implantation of organizers from a different species. 1923, Int. J. Dev. Biol. 45:13–38.

    CAS  PubMed  Google Scholar 

  • St-Jacques, B. and McMahon, A.P., 1996, Early mouse development: Lessons from gene targeting, Curr. Opin. Genet. Dev. 6:439–444.

    Article  CAS  PubMed  Google Scholar 

  • Stanford, W.L., Cohn, J.B., and Cordes, S.P., 2001, Gene-trap mutagenesis: Past, present and beyond, Nat. Rev. Genet. 2:756–768.

    Article  CAS  PubMed  Google Scholar 

  • Streit, A. and Stern, C.D., 1999, Establishment and maintenance of the border of the neural plate in the chick: Involvement of FGF and BMP activity, Mech. Dev. 82:51–66.

    Article  CAS  ADS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • Streit, A., Berliner, A.J., Papanayotou, C., Sirulnik, A., and Stern, C.D., 2000, Initiation of neural induction by FGF signalling before gastrulation, Nature 406:74–78.

    Article  CAS  ADS  PubMed  Google Scholar 

  • Tam, P.P. and Steiner, K.A., 1999, Anterior patterning by synergistic activity of the early gastrula organizer and the anterior germ layer tissues of the mouse embryo, Development 126:5171–5179.

    CAS  PubMed  Google Scholar 

  • Thomas, P. and Beddington, R., 1996, Anterior primitive endoderm may be responsible for patterning the anterior neural plate in the mouse embryo, Curr. Biol. 6:1487–1496.

    Article  CAS  PubMed  Google Scholar 

  • Tiedemann, H. and Tiedemann, H., 1956, Versuche zur chemischen kennzeichnung von embryonale induktionsstoffen, Z. Physiol. Chem. 306:7–32.

    CAS  Google Scholar 

  • Toivonen, S. and Wartiovaara, J., 1976, Mechanisms of cell interaction during primary embryonic induction studied in transfilter experiments, Differentiation 5:61–66.

    CAS  PubMed  Google Scholar 

  • Trindade, M., Tada, M., and Smith, J.C., 1999, DNA-binding specificity and embryological function of Xom (Xvent-2), Dev. Biol. 216:442–456.

    Article  CAS  PubMed  Google Scholar 

  • Tsang, M., Kim, R., de Caestecker, M.P., Kudoh, T., Roberts, A.B., and Dawid, I.B., 2000, Zebrafish nma is involved in TGFbeta family signaling, Genesis 28:47–57.

    Article  CAS  PubMed  Google Scholar 

  • Tsukazaki, T., Chiang, T.A., Davison, A.F., Attisano, L., and Wrana, J.L., 1998, SARA, a FYVE domain protein that recruits Smad2 to the TGFbeta receptor, Cell 95:779–791.

    Article  CAS  PubMed  Google Scholar 

  • Tsuneizumi, K., Nakayama, T., Kamoshida, Y., Kornberg, T.B., Christian, J.L., and Tabata, T., 1997, Daughters against dpp modulates dpp organizing activity in Drosophila wing development, Nature 389: 627–631.

    CAS  ADS  PubMed  Google Scholar 

  • van Straaten, H.W., Hekking, J.W., Beursgens, J.P., Terwindt-Rouwenhorst, E., and Drukker, J., 1989, Effect of the notochord on proliferation and differentiation in the neural tube of the chick embryo, Development 107:793–803.

    PubMed  Google Scholar 

  • Vincent, J.P. and Gerhart, J.C., 1987, Subcortical rotation in Xenopus eggs: An early step in embryonic axis specification, Dev. Biol. 123:526–539.

    Article  CAS  PubMed  Google Scholar 

  • von Bubnoff, A. and Cho, K.W., 2001, Intracellular BMP signaling regulation in vertebrates: Pathway or network?, Dev. Biol. 239:1–14.

    Google Scholar 

  • Waddington, C.H., 1932. Experiments on the development of chick and duck embryos, cultivated in vitro, Philos. Trans. R. Soc. Lond. B. Biol. Sci. 221:179–230.

    ADS  Google Scholar 

  • Waddington, C.H., 1934, Experiments on embryonic induction. J. Exp. Biol. 11:211–227.

    Google Scholar 

  • Waddington, C.H. and Schmidt, G.A., 1933, Induction by heteroplastic grafts of primitive streak in birds, Roux Arch. Entwicklungsmech 128: 522–563.

    Google Scholar 

  • Warga, R.M. and Kimmel, C.B., 1990, Cell movements during epiboly and gastrulation in zebrafish, Development 108:569–580.

    CAS  PubMed  Google Scholar 

  • Weinstein, D.C. and Hemmati-Brivanlou, A., 1999, Neural induction, Ann. Rev. Cell. Dev. Biol. 15:411–433.

    CAS  Google Scholar 

  • Wilson, S.I. and Edlund, T., 2001, Neural induction: Toward a unifying mechanism, Nat. Neurosci. 4(Suppl):1161–1168.

    CAS  PubMed  Google Scholar 

  • Wilson, P.A. and Hemmati-Brivanlou, A., 1995, Induction of epidermis and inhibition of neural fate by Bmp-4, Nature 376:331–333.

    Article  CAS  ADS  PubMed  Google Scholar 

  • Wilson, S.I., Graziano, E., Harland, R., Jessell, T.M., and Edlund, T., 2000, An early requirement for FGF signalling in the acquisition of neural cell fate in the chick embryo, Curr. Biol. 10:421–429.

    Article  CAS  PubMed  Google Scholar 

  • Wilson, S.I., Rydstrom, A., Trimborn, T., Willert, K., Nusse, R., Jessell, T.M. et al. 2001, The status of Wnt signalling regulates neural and epidermal fates in the chick embryo, Nature 411:325–330.

    CAS  ADS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • Wrana, J.L., Attisano, L., Wieser, R., Ventura, F., and Massague, J., 1994, Mechanism of activation of the TGF-beta receptor, Nature 370:341–347.

    Article  CAS  ADS  PubMed  Google Scholar 

  • Yuan, S. and Schoenwolf, G.C., 1998, De novo induction of the organizer and formation of the primitive streak in an experimental model of notochord reconstitution in avian embryos, Development 125: 201–213.

    CAS  PubMed  Google Scholar 

  • Yuan, S. and Schoenwolf, G.C., 1999, Reconstitution of the organizer is both sufficient and required to re-establish a fully patterned body plan in avian embryos, Development 126:2461–2473.

    CAS  PubMed  Google Scholar 

  • Yuan, S., Darnell, D.K., and Schoenwolf, G.C., 1995, Identification of inducing, responding, and suppressing regions in an experimental model of notochord formation in avian embryos, Dev. Biol. 172:567–584.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, H. and Bradley, A., 1996, Mice deficient for BMP2 are nonviable and have defects in amnion/chorion and cardiac development, Development 122:2977–2986.

    CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Zimmerman, C.M., Kariapper, M.S., and Mathews, L.S., 1998, Smad proteins physically interact with calmodulin, J. Biol. Chem. 273:677–680.

    CAS  PubMed  Google Scholar 

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Ladher, R., Schoenwolf, G.C. (2005). Making a Neural Tube: Neural Induction and Neurulation. In: Rao, M.S., Jacobson†, M. (eds) Developmental Neurobiology. Springer, Boston, MA. https://doi.org/10.1007/0-387-28117-7_1

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