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JOURNAL ARTICLES
Mechanisms of dorsal-ventral patterning in noggin-induced neural tissue
A.K. Knecht, R.M. Harland
Development 1997 124: 2477-2488;

Summary

We have investigated mechanisms of dorsal-ventral patterning of neural tissue, using Xenopus ectoderm neuralized by noggin protein. This tissue appears to be patterned dorsoventrally; cp1-1, a gene expressed in the dorsal brain, and etr-1, a gene largely excluded from the dorsal brain, are expressed in separate territories in noggin-treated explants (Knecht, A. K., Good, P. J., Dawid, I. B. and Harland, R. M. (1995) Development 121, 1927–1936). Here we show further evidence that this pattern represents a partial dorsal-ventral organization. Additionally, we test two mechanisms that could account for this pattern: a dose-dependent response to a gradient of noggin protein within the explant, and regulative cell-cell interactions. We show that noggin exhibits concentration-dependent effects, inducing cp1-1 at low doses but repressing it at high doses. Since noggin acts by antagonizing Bone Morphogenetic Protein (BMP) signaling, this result suggests that BMPs also may act in a dose-dependent manner in vivo. However, in the absence of a noggin gradient, regulative cell-cell interactions can also pattern the tissue. Such regulation is facilitated by increased motility of noggin-treated cells. Finally, the response of cells to both of these patterning mechanisms is ultimately controlled by a third process, the changing competence of the responding tissue.

REFERENCES

    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. Chiang C.,
    2. Litingtung Y.,
    3. Lee E.,
    4. Young K. E.,
    5. Corden J. L.,
    6. Westphal H.,
    7. Beachy P. A.
    (1996) Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 383, 407–413
    OpenUrlCrossRefPubMedWeb of Science
    1. Clement J. H.,
    2. Fettes P.,
    3. Knöchel S.,
    4. Lef J.,
    5. Knöchel W.
    (1995) Bone morphogenetic protein 2 in the early development of Xenopus laevis. Mech. Dev 52, 357–370
    OpenUrlCrossRefPubMed
    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. Cooke J.,
    2. Smith J. C.,
    3. Smith E. J.,
    4. Yaqoob M.
    (1987) The organization of mesodermal pattern in Xenopus laevis: experiments using a Xenopus mesoderm-inducing factor. Development 101, 893–908
    OpenUrlAbstract/FREE Full Text
    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. Dickinson M.,
    2. Selleck M.,
    3. McMahon A.,
    4. Bronner-Fraser M.
    (1995) Dorsalization of the neural tube by the non-neural ectoderm. Development 121, 2099–2106
    OpenUrlAbstract
    1. Eagleson G. W.,
    2. Harris W. A.
    (1990) Mapping of the presumptive brain regions in the neural plate of Xenopus laevis. J. Neurobiol 21, 427–440
    OpenUrlCrossRefPubMedWeb of Science
    1. Echelard Y.,
    2. Epstein D. J.,
    3. St-Jacques B.,
    4. Shen L.,
    5. Mohler J.,
    6. McMahon J. A.,
    7. McMahon A. P.
    (1993) Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell 75, 1417–1430
    OpenUrlCrossRefPubMedWeb of Science
    1. Ericson J.,
    2. Muhr J.,
    3. Placzek M.,
    4. Lints T.,
    5. Jessell T. M.,
    6. Edlund T.
    (1995) Sonic hedgehog induces the differention of ventral forebrain neurons: a common signal for ventral patterning with the neural tube. Cell 81, 747–756
    OpenUrlCrossRefPubMedWeb of Science
    1. Fainsod A.,
    2. Steinbeisser H.,
    3. De Robertis E. M.
    (1994) On the function of BMP-4 in patterning the marginal zone of the Xenopus embryo. EMBO J 13, 5015–5025
    OpenUrlPubMedWeb of Science
    1. Ferguson E. L.,
    2. Anderson K. V.
    (1992) decapentaplegic acts as a morphogen to organize dorsal-ventral pattern in the Drosophila embryo. Cell 71, 451–461
    OpenUrlCrossRefPubMedWeb of Science
    1. Gerhart J. C.,
    2. Danilchik M.,
    3. Doniach T.,
    4. Roberts S.,
    5. Rowning B.,
    6. Stewart R.
    (1989) Cortical rotation of the Xenopus egg: consequences for the anteroposterior pattern of embryonic dorsal development. Development 107, 37–51
    1. Godsave S. F.,
    2. Slack J. M. W.
    (1989) Clonal analysis of mesoderm induction in Xenopus laevis. Dev. Biol 134, 486–490
    OpenUrlCrossRefPubMedWeb of Science
    1. Green J. 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. Grunz H.,
    2. Tacke L.
    (1989) Neural differentiation of Xenopus laevis ectoderm takes place after disaggregation and delayed reaggregation without inducer. Cell Diff. Dev 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. 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. Hemmati-Brivanlou A.,
    2. Melton D. A.
    (1994) Inhibition of activin receptor signalling promotes neuralization in Xenopus. Cell 77, 273–281
    OpenUrlCrossRefPubMedWeb of Science
    1. Hemmati-Brivanlou A.,
    2. 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
    OpenUrlCrossRefPubMedWeb of Science
    1. Jacobson A. G.,
    2. Sater A. K.
    (1988) Features of embryonic induction. Development 104, 341–359
    OpenUrlAbstract/FREE Full Text
    1. Jonas E. A.,
    2. Snape A. M.,
    3. Sargent T. D.
    (1989) Transcriptional regulation of a Xenopus embryonic epidermal keratin gene. Development 106, 399–405
    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. 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. 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. Koenig B. B.,
    2. Cook J. S.,
    3. Wolsing D. H.,
    4. Ting J.,
    5. Tiesman J. P.,
    6. Correa P. E.,
    7. Olson C. A.,
    8. Pecquet A. L.,
    9. Ventura F.,
    10. Grant R. A.,
    11. Chen G.-X.,
    12. Wrana J. L.,
    13. Massague J.,
    14. Rosenbaum J. S.
    (1994) Characterization and cloning of a receptor for BMP-2 and BMP-4 from NIH 3T3 cells. Mol. Cell. Biol 14, 5961–5974
    OpenUrlAbstract/FREE Full Text
    1. Krauss S.,
    2. Concordet J. P.,
    3. Ingham P. W.
    (1993) A functionally conserved homolog of the Drosophila segment polarity gene hh is expressed in tissues with polarizing activity in zebrafish embryos. Cell 75, 1431–1444
    OpenUrlCrossRefPubMedWeb of Science
    1. Krieg P. A.,
    2. Varnum S. M.,
    3. Wormington W. M.,
    4. Melton D. A.
    (1989) The mRNA encoding elongation factor 1-alpha (EF-1alpha) is a major transcript at the midblastula transition in Xenopus. Dev. Biol 133, 93–100
    OpenUrlCrossRefPubMedWeb of Science
    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. Liem K. F. J.,
    2. Tremml G.,
    3. Roelink H.,
    4. Jessell T. M.
    (1995) Dorsal differentiation of neural plate cells induced by BMP-mediated signals from epidermal ectoderm. Cell 82, 969–979
    OpenUrlCrossRefPubMedWeb of Science
    1. London C.,
    2. Akers R.,
    3. Phillips C.
    (1988) Expression of Epi 1, an epidermis-specific marker in Xenopus laevis embryos, is specified prior to gastrulation. Dev. Biol 129, 380–389
    OpenUrlCrossRefPubMedWeb of Science
    1. Moury J. D.,
    2. Jacobson A. G.
    (1989) Neural fold formation at newly created boundaries between neural plate and epidermis in the axolotl. Dev. Biol 133, 44–57
    OpenUrlCrossRefPubMedWeb of Science
    1. Muskavitch M. A.
    (1994) Delta-notch signaling and Drosophila cell fate choice. Dev. Biol 166, 415–430
    OpenUrlCrossRefPubMedWeb of Science
    1. Nellen D.,
    2. Burke R.,
    3. Struhl G.,
    4. Basler K.
    (1996) Direct and long-range action of a DPP morphogen gradient. Cell 85, 357–368
    OpenUrlCrossRefPubMedWeb of Science
    1. Otte A. P.,
    2. Kraner I. M.,
    3. Durston A. J.
    (1991) Protein kinase C and regulation of the local competence of Xenopus ectoderm. Science 251, 570–573
    OpenUrlAbstract/FREE Full Text
    1. Otte A. P.,
    2. Moon R. T.
    (1992) Ectopic induction of dorsal mesoderm by overexpression of Xwnt −8 elevates the neural competence of Xenopus ectoderm. Dev. Biol 152, 184–187
    OpenUrlCrossRefPubMed
    1. Papalopulu N.,
    2. Kintner C.
    (1996) A posteriorising factor, retinoic acid, reveals that anteroposterior patterning controls the timing of neuronal differentiation in Xenopus neuroectoderm. Development 122, 3409–3418
    OpenUrlAbstract
    1. Roelink H.,
    2. Porter J. A.,
    3. Chiang C.,
    4. Tanabe Y.,
    5. Chang D. T.,
    6. Beachy P. A.,
    7. Jessell T. M.
    (1995) Floor plate and motor neuron induction by different concentrations of the amino-terminal cleavage product of sonic hedgehog autoproteolysis. Cell 81, 445–455
    OpenUrlCrossRefPubMedWeb of Science
    1. Saha M. S.,
    2. Michel R. B.,
    3. Gulding K. M.,
    4. Grainger R. M.
    (1993) A Xenopus homeobox gene defines dorsal-ventral domains in the developing brain. Development 118, 193–202
    OpenUrlAbstract
    1. Sargent T. D.,
    2. Jamrich M.,
    3. Dawid I. B.
    (1986) Cell interactions and the control of gene activity during early development in Xenopus laevis. Dev. Biol 114, 238–246
    OpenUrlCrossRefPubMedWeb of Science
    1. Savage R.,
    2. Phillips C. R.
    (1989) Signals from the dorsal blastopore lip region during gastrulation bias the ectoderm toward a nonepidermal pathway of differentiation in Xenopus laevis. Dev. Biol 133, 157–168
    OpenUrlCrossRefPubMedWeb of Science
    1. Schmidt J. E.,
    2. Suzuki A.,
    3. Ueno N.,
    4. Kimelman D.
    (1995) Localized BMP-4 mediates dorsal/ventral patterning in the early Xenopus embryo. Dev. Biol 169, 37–50
    OpenUrlCrossRefPubMedWeb of Science
    1. Selleck M. A. J.,
    2. Bronner-Fraser M.
    (1995) Origins of the avian neural crest: the role of neural plate/epidermal interactions. Development 121, 525–538
    OpenUrlAbstract
    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. Fritz A.,
    3. De Robertis E. M.,
    4. Gurdon J. B.
    (1987) A homeobox-containing marker of posterior neural differentiation shows the importance of predetermination in neural induction. Cell 50, 749–758
    OpenUrlCrossRefPubMedWeb of Science
    1. Sive H. L.,
    2. Hattori K.,
    3. Weintraub H.
    (1989) Progressive determination during formation of the anteroposterior axis in Xenopus laevis. Cell 58, 171–180
    OpenUrlCrossRefPubMedWeb of Science
    1. Slack J. M. W.,
    2. Forman D.
    (1980) An interaction between dorsal and ventral regions of the marginal zone in early amphibian embryos. J. Embryol. Exp. Morph 56, 283–299
    OpenUrlPubMedWeb of Science
    1. Smith J.,
    2. Schoenwolf G. C.
    (1989) Notochordal induction of cell wedging in the chick neural plate and its role in neural tube formation. J. Exp. Zool 25, 49–62
    OpenUrl
    1. Smith W. C.,
    2. Harland R. M.
    (1991) Injected Xwnt-8 RNA acts early in Xenopus embryos to promote formation of a vegetal dorsalizing center. Cell 67, 753–765
    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. von Straaten H. W. M.,
    2. Hekking E. J. L. M.,
    3. Wiertz-Hoessels F. T.,
    4. Drukker J.
    (1988) Effects of the notochord on the differentiation of a floor plate area in the neural tube of the chick embryo. Anat. Embryol 177, 317–324
    OpenUrlCrossRefPubMed
    1. Wilson P. A.,
    2. Hemmati-Brivanlou A.
    (1995) Induction of epidermis and inhibition of neural fate by Bmp-4. Nature 376, 331–333
    OpenUrlCrossRefPubMedWeb of Science
    1. Wilson P. A.,
    2. Melton D. A.
    (1994) Mesodermal patterning by an inducer gradient depends on secondary cell-cell communication. Current Biol 4, 676–686
    OpenUrlCrossRefPubMedWeb of Science
    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. Zimmerman L. B.,
    2. DeJesús-Escobar J. M.,
    3. Harland R. M.
    (1996) The Spemann organizer signal noggin binds and inactivates Bone Morphogenetic Protein 4. Cell 86, 599–606
    OpenUrlCrossRefPubMedWeb of Science
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JOURNAL ARTICLES
Mechanisms of dorsal-ventral patterning in noggin-induced neural tissue
A.K. Knecht, R.M. Harland
Development 1997 124: 2477-2488;
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