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JOURNAL ARTICLES
Properties of the dorsal activity found in the vegetal cortical cytoplasm of Xenopus eggs
T. Holowacz, R.P. Elinson
Development 1995 121: 2789-2798;

Summary

The Xenopus egg contains a maternal dorsal determinant that is specifically localized to the vegetal cortex. We have previously shown that vegetal cortical cytoplasm can generate a full dorsal axis when it is injected into ventral vegetal blastomeres of a cleavage-stage embryo. In this study, we have defined further the properties of the dorsal activity. The cortical dorsal activity arises during oocyte maturation after germinal vesicle breakdown. When injected into the four extreme animal pole blastomeres of ultraviolet-ventralized 32-cell embryos, vegetal cortical cytoplasm partially rescued dorsal axial structures. As revealed by lineage tracing, these axial structures formed ectopically from the progeny of the cells that were injected. Injection of animal cortical cytoplasm had no effect. When mid-blastula (stage 8) animal caps from these injected embryos were isolated and cultured, both vegetal cortex-enriched and animal cortex-enriched animal caps produced only epidermis. Therefore vegetal cortex, on its own, is not a mesoderm inducer. Between stage 8 (blastula) and stage 10 (gastrula), a ventral mesoderm-inducing signal spreads from vegetal cells towards the animal pole. We tested whether this natural mesoderm-inducing factor interacts with the activity found in the vegetal cortex. Injection of vegetal cortex enhanced the formation of neural tissue and cement gland when animal caps were isolated at stage 10. When cultured from stage 8 in the presence of the ventral mesoderm-inducing fibroblast growth factor, animal caps enriched in vegetal cortex developed significantly more neural tissue and cement gland than ones enriched in animal cortex. These results indicate that the dorsal activity localized to the egg vegetal cortex alters the response of cells to mesoderm inducers.

Reference

    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. Cooke J.,
    2. Symes K.,
    3. Smith E. J.
    (1989) Potentiation by the lithium ion of morphogenetic responses to a Xenopus inducing factor. Development 105, 549–558
    OpenUrlAbstract/FREE Full Text
    1. Dale L.,
    2. Matthew G.,
    3. Tabe L.,
    4. Colman A.
    (1989) Developmental expression of the protein product of Vg1, a localized maternal mRNA in the frog Xenopus laevis. EMBO J 8, 1057–1065
    OpenUrlPubMedWeb of Science
    1. Elinson R. P.,
    2. Pasceri P.
    (1989) Two UV-sensitive targets in dorsoanterior specification of frog embryos. Development 106, 511–518
    OpenUrlAbstract
    1. Elinson R. P.,
    2. King M. L.,
    3. Forristall C.
    (1993) Isolated vegetal cortex from Xenopus oocytes selectively retains localized mRNAs. Dev. Biol 160, 554–562
    OpenUrlCrossRefPubMed
    1. Forristall C.,
    2. Pondel M.,
    3. Chen L.,
    4. King M. L.
    (1995) Patterns of localization and cytoskeletal association of two vegetally localized RNAs, Vg1 and Xcat-2. Development 121, 201–208
    OpenUrlAbstract
    1. Fujisue M.,
    2. Kobayakawa Y.,
    3. Yamana K.
    (1993) Occurrence of dorsal axis-inducing activity around the vegetal pole of an uncleaved Xenopus egg and displacement to the equatorial region by cortical rotation. Development 118, 163–170
    OpenUrlAbstract/FREE Full Text
    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. Gimlich R. L.,
    2. Braun J.
    (1985) Improved fluorescent compounds for tracing cell lineage. Dev. Biol 109, 509–514
    OpenUrlCrossRefPubMedWeb of Science
    1. Graff J. M.,
    2. Thies R. S.,
    3. Song J. J.,
    4. Celeste A. J.,
    5. Melton D. A.
    (1994) Studies with a Xenopus BMP receptor suggest that ventral mesoderm-inducing signals override dorsal signals in vivo. Cell 79, 169–179
    OpenUrlCrossRefPubMedWeb of Science
    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, 731–739
    OpenUrlCrossRefPubMedWeb of Science
    1. Hausen P.,
    2. Wang H. Y.,
    3. Dreyer C.,
    4. Stick R.
    (1985) Distribution of nuclear proteins during maturation of the Xenopus oocyte. J. Embryol. Exp. Morph 89, 17–34
    1. He X.,
    2. Saint-Jeannet J.-P.,
    3. Woodgett J. R.,
    4. Varmus H. E.,
    5. Dawid I. B.
    (1995) Glycogen synthase kinase-3 and dorsoventral patterning in Xenopus embryos. Nature 374, 617–622
    OpenUrlCrossRefPubMedWeb of Science
    1. Holowacz T.,
    2. Elinson R. P.
    (1993) Cortical cytoplasm, which induces dorsal axis formation in Xenopus, is inactivated by UV-irradiation of the oocyte. Development 119, 277–285
    OpenUrlAbstract
    1. Houliston E.,
    2. Elinson R. P.
    (1991) Patterns of microtubule polymerization relating to cortical rotation in Xenopus laevis eggs. Development 112, 107–117
    OpenUrlAbstract
    1. Imoh H.,
    2. Okamoto M.,
    3. Eguchi G.
    (1983) Accumulation of annulate lamellae in the subcortical layer during progesterone-induced oocyte maturation in Xenopus laevis. Dev. Growth Diff 25, 1–10
    OpenUrlCrossRef
    1. Jones E. A.,
    2. Woodland H. R.
    (1987) The development of animal caps in Xenopus: A measure of the start of animal cap competence to form mesoderm. Development 101, 557–563
    OpenUrlAbstract
    1. Jones E. A.,
    2. Woodland H. R.
    (1989) Spatial aspects of neural induction in Xenopus laevis. Development 107, 785–791
    OpenUrlAbstract/FREE Full Text
    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. 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. Elinson R. P.
    (1989) Dorsalization of mesoderm by lithium. Dev. Biol 132, 81–90
    OpenUrlCrossRefPubMedWeb of Science
    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. Klymkowsky M. W.,
    2. Maynell L. A.,
    3. Polson A. G.
    (1987) Polar asymmetry in the organization of the cortical cytokeratin system of Xenopus laevis oocytes and embryos. Development 100, 543–557
    OpenUrlAbstract
    1. Klymkowsky M. W.,
    2. Maynell L.A.
    (1989) MPF-induced breakdown of cytokeratin filament organization in the maturing Xenopus oocyte depends upon the translation of maternal mRNAs. Dev. Biol 134, 479–485
    OpenUrlCrossRefPubMed
    1. Klymkowsky M. W.,
    2. Maynell L. A.,
    3. Nislow C.
    (1991) Cytokeratin phosphorylation, cytokeratin filament severing and the solubilization of the maternal mRNA Vg1. J. Cell Biol 114, 787–797
    OpenUrlAbstract/FREE Full Text
    1. Kondo M.,
    2. Tashiro K.,
    3. Fujii G.,
    4. Asano M.,
    5. Miyoshi R.,
    6. Yamada R.,
    7. Muramatsu M.,
    8. Shiokawa K.
    (1991) Activin receptor mRNA isexpressed early in Xenopus embryogenesis and the level of the expression affects the body axis formation. Biochem. Biophys. Res. Comm 181, 684–690
    OpenUrlCrossRefPubMedWeb of Science
    1. Ku M.,
    2. Melton D. A.
    (1993) Xwnt-11: a maternally expressed Xenopus wnt gene. Development 119, 1161–1173
    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. Malacinski G. M.,
    2. Benford H.,
    3. Chung H.-M.
    (1975) Association of an ultraviolet irradiation sensitive cytoplasmic localization with the future dorsal side of the amphibian egg. J. Exp. Zool 191, 97–110
    OpenUrlCrossRefPubMed
    1. McCrea P. D.,
    2. Brieher W. M.,
    3. Gumbiner B. M.
    (1993) Induction of a secondary body axis in Xenopus by antibodies to-catenin. J. Cell Biol 123, 477–484
    OpenUrlAbstract/FREE Full Text
    1. Mosquera L.,
    2. Forristall C.,
    3. Zhou Y.,
    4. King M. L.
    (1993) A mRNA localized to the vegetal cortex of Xenopus oocytes encodes a protein with a nanos -like zinc finger domain. Development 117, 377–386
    OpenUrlAbstract/FREE Full Text
    1. Sasai Y.,
    2. Lu B.,
    3. Steinbesser H.,
    4. Geissert D.,
    5. Gont L. K.,
    6. De Robertis E. M.
    (1994) Xenopus chordin: a novel dorsalizing factor activated by organizer-specific homeobox genes. Cell 79, 779–790
    OpenUrlCrossRefPubMedWeb of Science
    1. Schneider S.,
    2. Herrenknecht K.,
    3. Butz S.,
    4. Kemler R.,
    5. Hausen P.
    (1993) Catenins in Xenopus embryogenesis and their relation to the cadherin-mediated cell-cell adhesion system. Development 118, 629–640
    OpenUrlAbstract
    1. Slack J. M. W.,
    2. Darlington B. G.,
    3. Heath J. K.,
    4. Godsave S. F.
    (1987) Mesoderm induction in early Xenopus embryos by heparin-binding growth factors. Nature 326, 197–200
    OpenUrlCrossRefPubMed
    1. Slack J. M. W.,
    2. Isaacs H. V.,
    3. Darlington B. G.
    (1988) Inductive effects of fibroblast growth factor and lithium ion on Xenopus blastula ectoderm. Development 103, 581–590
    OpenUrlAbstract
    1. Smith J. C.,
    2. Dale L.,
    3. Slack J. M. W.
    (1985) Cell lineage of labels and region-specific markers in the analysis of inductive interactions. J. Embryol. Exp. Morph 89, 317–331
    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. 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. Sokol S. Y.,
    2. Melton D. A.
    (1992) Interaction of Wnt and activin in dorsal mesoderm induction in Xenopus. Dev. Biol 154, 348–355
    OpenUrlCrossRefPubMedWeb of Science
    1. Sokol S. Y.
    (1993) Mesoderm formation in Xenopus ectodermal explants overexpressing Xwnt8: evidence for a cooperating signal reaching the animal pole by gastrulation. Development 118, 1335–1342
    OpenUrlAbstract/FREE Full Text
    1. Tannahill D.,
    2. Melton D. A.
    (1989) Localized synthesis of the Vg1 protein during early Xenopus development. Development 106, 775–785
    OpenUrlAbstract/FREE Full Text
    1. Thomsen G.,
    2. Woolf T.,
    3. Whitman M.,
    4. Sokol S.,
    5. Vaughan J.,
    6. Vale W.,
    7. Melton D. A.
    (1990) Activins are expressed early in Xenopus embryogenesis and can induce axial mesoderm and anterior structures. Cell 63, 485–493
    OpenUrlCrossRefPubMedWeb of Science
    1. Thomsen G. H.,
    2. Melton D. A.
    (1993) Processed Vg1 protein is an axial mesoderm inducer in Xenopus. Cell 74, 433–441
    OpenUrlCrossRefPubMedWeb of Science
    1. Weeks D. L.,
    2. Melton D. A.
    (1987) A maternal mRNA localized to the vegetal hemisphere in Xenopus eggs codes for a growth factor related to TGF-. Cell 51, 861–868
    OpenUrlCrossRefPubMedWeb of Science
    1. Youn B. W.,
    2. Malacinski G. M.
    (1981) Axial structure development in ultraviolet-irradiated (notochord-defective) amphibian embryos. Dev. Biol 83, 339–352
    OpenUrlCrossRefPubMedWeb of Science
    1. Yuge M.,
    2. Kobayakawa Y.,
    3. Fujisue M.,
    4. Yamana K.
    (1990) A cytoplasmic determinant for dorsal axis formation in an early embryo of Xenopus laevis. Development 110, 1051–1056
    OpenUrlAbstract/FREE Full Text
    1. Zhang S. C.,
    2. Masui Y.
    (1992) Activation of Xenopus laevis eggs in the absence of intracellular Ca activity by the protein phosphorylation inhibitor, 6-dimethylamonopurine (6-DMAP). J. Exp. Zool 262, 317–329
    OpenUrlCrossRefPubMedWeb of Science
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JOURNAL ARTICLES
Properties of the dorsal activity found in the vegetal cortical cytoplasm of Xenopus eggs
T. Holowacz, R.P. Elinson
Development 1995 121: 2789-2798;
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