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JOURNAL ARTICLES
Regulation of Spemann organizer formation by the intracellular kinase Xgsk-3
S.B. Pierce, D. Kimelman
Development 1995 121: 755-765;

Summary

Dorsal axis formation in the Xenopus embryo can be induced by the ectopic expression of several Wnt family members. In Drosophila, the protein encoded by the Wnt family gene, wingless, signals through a pathway that antagonizes the effects of the serine/threonine kinase zeste-white 3/shaggy. We describe the isolation and characterization of a Xenopus homolog of zeste-white 3/shaggy, Xgsk-3. A kinase-dead mutant of Xgsk-3, Xgsk-3K-->R, has a dominant negative effect and mimics the ability of Wnt to induce a secondary axis by induction of an ectopic Spemann organizer. Xgsk-3K-->R, like Wnt, induces dorsal axis formation when expressed in the deep vegetal cells, which do not contribute to the axis. These results indicate that the dorsal fate is actively repressed by Xgsk-3, which must be inactivated for dorsal axis formation to occur. Furthermore, our work suggests that the effects of Xgsk-3K-->R are mediated by an additional intercellular signal.

Reference

    1. Bejsovec A.,
    2. Martinez-Arias A.
    (1991) Roles of wingless in patterning the larval epidermis of Drosophila. Development 113, 471–485
    OpenUrlAbstract
    1. Bianchi M. W.,
    2. Guivarc'h D.,
    3. Thomas M.,
    4. Woodgett J. R.
    (1994) Arabidopsis homologs of the shaggy and GSK-3 protein kinases: molecular cloning and functional expression in Escherichia coli. Mol. Gen. Genet 242, 337–45
    OpenUrlCrossRefPubMedWeb of Science
    1. Bianchi M. W.,
    2. Plyte S. E.,
    3. Kreis M.,
    4. Woodgett J. R.
    (1993) A saccharomyces cerevisiae protein-serine kinase related to mammalian glycogen synthase kinase-3 and the Drosophila melanogaster gene shaggy product. Gene 134, 51–56
    OpenUrlCrossRefPubMed
    1. Bourouis M.,
    2. Moore P.,
    3. Ruel L.Y.G.,
    4. Heitzler P.,
    5. Simpson P.
    (1990) An early embryonic product of the gene shaggy encodes a serine/threonine protein kinase related to the CDC28/cdc2+subfamily. EMBO J 9, 2877–2884
    OpenUrlPubMedWeb of Science
    1. Busa W. B.,
    2. Gimlich R. L.
    (1989) Lithium induced teratogenesis in frog embryos prevented by a polyphosphoinositide cycle intermediate or a diacylglycerol analog. Dev. Biol 132, 315–24
    OpenUrlCrossRefPubMedWeb of Science
    1. Chakrabarti A.,
    2. Matthews G.,
    3. Colman A.,
    4. Dale L.
    (1992) Secretory and inductive properties of Drosophila wingless protein in Xenopus oocytes and embryos. Development 115, 355–369
    OpenUrlAbstract
    1. Cho K. W. Y.,
    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. 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. Cornell R. A.,
    2. Kimelman D.
    (1994) Activin-mediated mesoderm induction requires FGF. Development 120, 453–462
    OpenUrlAbstract
    1. Cornell R. A.,
    2. Kimelman D.
    (1994) Combinatorial signaling in development. Bioessays 16, 577–581
    OpenUrlCrossRefPubMed
    1. Diaz-Benjumea F. J.,
    2. Cohen S. M.
    (1994) wingless acts through the shaggy/zeste-white3 kinase to direct dorsal-ventral axis formation in the Drosophila leg. Development 120, 1661–1670
    OpenUrlAbstract
    1. Gimlich R. L.,
    2. Gerhart J. C.
    (1984) Early cellular interactions promote embryonic axis formation in Xenopus laevis. Dev. Biol 104, 117–130
    OpenUrlCrossRefPubMedWeb of Science
    1. Graves L. M.,
    2. Northrop J. L.,
    3. Potts B. C.,
    4. Krebs E. G.,
    5. Kimelman D.
    (1994) FGF, but not activin, is a potent inducer of MAP kinase in Xenopus explants. Proc. Natl. Acad. Sci. USA 91, 1662–1666
    OpenUrlAbstract/FREE Full Text
    1. Guthrie S.,
    2. Turin L.,
    3. Warner A.
    (1988) Patterns of junctional communication during development of the early amphibian embryo. Development 103, 769–783
    OpenUrlAbstract/FREE Full Text
    1. Guthrie S. C.
    (1984) Patterns of junctional communication in the early amphibian embryo. Nature 311, 149–151
    OpenUrlCrossRefPubMed
    1. Hanks S. K.,
    2. Quinn A. M.,
    3. Hunter T.
    (1988) The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241, 42–52
    OpenUrlAbstract/FREE Full Text
    1. Hartley R. S.,
    2. Lewellyn A. L.,
    3. Maller J. L.
    (1994) MAP kinase is activated during mesoderm induction in Xenopus laevis. Dev. Biol 163, 521–524
    OpenUrlCrossRefPubMedWeb of Science
    1. Ho S. N.,
    2. Hunt H. D.,
    3. Horton R. M.,
    4. Pullen J. K.,
    5. Pease L. R.
    (1989) Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77, 51–59
    OpenUrlCrossRefPubMedWeb of Science
    1. Jones E. A.,
    2. Woodland H. R.
    (1987) The development of animal cap cells in Xenopus: a measure of the start of animal cap competence to form mesoderm. Development 101, 557–563
    OpenUrlAbstract
    1. Kao K. R.,
    2. Elinson R. P.
    (1988) The entire mesodermal mantle behaves as Spemann's organizer in dorsoanterior enhanced Xenopus laevis embryos. Dev. Biol 127, 64–77
    OpenUrlCrossRefPubMedWeb of Science
    1. Kao K. R.,
    2. Masui Y.,
    3. Elinson R. P.
    (1986) Lithium induced respecification of pattern in Xenopus laevis embryos. Nature 322, 371–373
    OpenUrlCrossRefPubMedWeb of Science
    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. 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. 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, 463–472
    OpenUrlAbstract
    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
    OpenUrlCrossRefPubMedWeb of Science
    1. Malacinski G. M.,
    2. Brothers J.,
    3. Chung H.-M.
    (1977) Destruction of components of the neural induction system of the amphibian egg with ultraviolet irradiation. Dev. Biol 56, 24–39
    OpenUrlCrossRefPubMedWeb of Science
    1. Maslanski J. A.,
    2. Leshko L.,
    3. Busa W. B.
    (1992) Lithium-sensitive production of inositol phosphates during amphibian embryonic mesoderm induction. Science 256, 243–245
    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
    OpenUrlAbstract/FREE Full Text
    1. Nagajski D. J.,
    2. Guthrie S. C.,
    3. Ford C. C.,
    4. Warner A. E.
    (1989). Thecorrelation between patterns of dye transfer through gap junctions and future developmental fate in Xenopus: the consequences of u.v. irradiation and lithium treatment. Development 105, 747–752
    OpenUrlAbstract/FREE Full Text
    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
    OpenUrlCrossRefPubMedWeb of Science
    1. Nishida E.,
    2. Gotoh Y.
    (1993) The MAP kinase cascade is essential for diverse signal transduction pathways. Trends Biochem. Sci 18, 128–131
    OpenUrlCrossRefPubMedWeb of Science
    1. Noordermeer J.,
    2. Klingensmith J.,
    3. Perrimon N.,
    4. Nusse R.
    (1994) dishevelled and armadillo act in the Wingless signalling pathway in Drosophila. Nature 367, 80–83
    OpenUrlCrossRefPubMedWeb of Science
    1. Olson D. J.,
    2. Christian J. L.,
    3. Moon R. T.
    (1991) Effect of wnt −1 and related proteins on gap junctional communication in Xenopus embryos. Science 252, 1173–1176
    OpenUrlFREE Full Text
    1. Pay A.,
    2. Honak C.,
    3. Bogre L.,
    4. Meskiene I.,
    5. Mairinger T.
    (1993) The MsK family of alfalfa protein kinase genes encodes homologues of shaggy /glycogen synthase kinase-3 and shows differential expression patterns in plant organs and development. Plant J 3, 847–856
    OpenUrlCrossRefPubMed
    1. Puziss J. W.,
    2. Hardy T. A.,
    3. Johnson R. B.,
    4. Roach P. J.,
    5. Hieter P.
    (1994) MDS1, a dosage suppressor of an mck1 mutant, encodes a putative yeast homolog of gycogen synthase kinase 3. Mol. Cell Biol 14, 831–839
    OpenUrlAbstract/FREE Full Text
    1. Sanger F.,
    2. Nicklen S.,
    3. Coulson A. R.
    (1977) DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74, 5436–5467
    OpenUrl
    1. Scharf S. R.,
    2. Gerhart J. C.
    (1980) Determination of the dorsal-ventral axis in eggs of Xenopus laevis: complete rescue of uv-impaired eggs by oblique orientation before first cleavage. Dev. Biol 79, 181–198
    OpenUrlCrossRefPubMedWeb of Science
    1. Siegfried E.,
    2. Chou T.,
    3. Perrimon N.
    (1992) wingless signaling acts through zeste-white 3, the Drosophila homolog of glycogen synthase kinase-3, to regulate engrailed and establish cell fate. Cell 71, 1167–1179
    OpenUrlCrossRefPubMedWeb of Science
    1. Siegfried E.,
    2. Wilder E. L.,
    3. Perrimon N.
    (1994) Components of wingless signaling in Drosophila. Nature 367, 76–80
    OpenUrlCrossRefPubMedWeb of Science
    1. Sive H. L.
    (1993) The frog prince-cess: A molecular formula for dorsoventral patterning in Xenopus. Genes Dev 7, 1–12
    OpenUrlFREE Full Text
    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
    OpenUrlCrossRefPubMedWeb of Science
    1. Sokol S.,
    2. Christian J. L.,
    3. Moon R. T.,
    4. Melton D. A.
    (1991) Injected wnt RNA induces a complete body axis in Xenopus embryos. Cell 67, 741–752
    OpenUrlCrossRefPubMedWeb of Science
    1. Struhl G.,
    2. Basler K.
    (1993) Organizing activity of wingless protein in Drosophila. Cell 72, 527–540
    OpenUrlCrossRefPubMedWeb of Science
    1. Sutherland C.,
    2. Leighton I. A.,
    3. Cohen P.
    (1993) Inactivation of glycogen synthase kinase-3by phosphorylation: new kinase connections in insulin and growth-factor signalling. Biochem. J 296, 15–19
    1. Thomsen G. H.,
    2. Melton D. A.
    (1993) Processed Vg-1 protein is an axial mesoderm inducer in Xenopus. Cell 74, 433–441
    OpenUrlCrossRefPubMedWeb of Science
    1. Thuringer F.,
    2. Bienz M.
    (1993) Indirect regulation of a homeotic Drosophila gene mediated by extracellular signaling. Proc. Natl. Acad. Sci. USA 90, 3899–3903
    OpenUrlAbstract/FREE Full Text
    1. Turner D. L.,
    2. Weintraub H.
    (1994) Expression of achaete-scute homolog 3 in Xenopus embryos converts ectodermal cells to a neural fate. Genes Dev 8, 1434–1447
    OpenUrlAbstract/FREE Full Text
    1. Vincent J.,
    2. Lawrence P. A.
    (1994) Drosophila wingless sustains engrailed expression only in adjoining cells: evidence from mosaic embryos. Cell 77, 909–915
    OpenUrlCrossRefPubMedWeb of Science
    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
    OpenUrlAbstract/FREE Full Text
    1. Warner A. E.,
    2. Guthrie C.,
    3. Gilula N. B.
    (1984) Antibodies to gap-junctional protein selectively disrupt gap junctional communication in the early amphibian embryo. Nature 311, 127–131
    OpenUrlCrossRefPubMed
    1. Woodgett J. R.
    (1990) Molecular cloning and expression of glycogen synthase kinase-3/Factor A. EMBO J 9, 2431–2438
    OpenUrlPubMedWeb of Science
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JOURNAL ARTICLES
Regulation of Spemann organizer formation by the intracellular kinase Xgsk-3
S.B. Pierce, D. Kimelman
Development 1995 121: 755-765;
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