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JOURNAL ARTICLES
Structure of the zebrafish snail1 gene and its expression in wild-type, spadetail and no tail mutant embryos
C. Thisse, B. Thisse, T.F. Schilling, J.H. Postlethwait
Development 1993 119: 1203-1215;

Summary

Mesoderm formation is critical for the establishment of the animal body plan and in Drosophila requires the snail gene. This report concerns the cloning and expression pattern of the structurally similar gene snail1 from zebrafish. In situ hybridization shows that the quantity of snail1 RNA increases at the margin of the blastoderm in cells that involute during gastrulation. As gastrulation begins, snail1 RNA disappears from the dorsal axial mesoderm and becomes restricted to the paraxial mesoderm and the tail bud. snail1 RNA increases in cells that define the posterior border of each somite and then disappears when somitic cells differentiate. Later in development, expression appears in cephalic neural crest derivatives. Many snail1-expressing cells were missing from mutant spadetail embryos and the quantity of snail1 RNA was greatly reduced in mutant no tail embryos. The work presented here suggests that snail1 is involved in morphogenetic events during gastrulation, somitogenesis and development of the cephalic neural crest, and that no tail may act as a positive regulator of snail1.

REFERENCES

    1. Alberga A.,
    2. Boulay J. L.,
    3. Kempe E.,
    4. Dennefeld C.,
    5. Haenlin M.
    (1991). The snail gene required for mesoderm formation in Drosophila is expressed dynamically in derivatives of all three germ-layers. Development 111, 983–992
    OpenUrlAbstract/FREE Full Text
    1. Boulay J. L.,
    2. Dennenfeld C.,
    3. Alberga A.
    (1987). The Drosophila developmental gene snail encodes a protein with nucleic acid binding fingers. Nature 330, 392–395
    OpenUrl
    1. Blumberg B.,
    2. Wright C. V. E.,
    3. De Robertis E. M.,
    4. Cho K. W. Y.
    (1991). Organizer-specific homeobox genes in Xenopus laevis embryos. Science 253, 194–196
    OpenUrlAbstract/FREE Full Text
    1. Chesley P.
    (1935). Development of the short-tailed mutation in the house mouse. J. Exp. Zool 70, 429–459
    OpenUrlCrossRefWeb of Science
    1. Cho K.,
    2. Blumberg B.,
    3. Steinbeisser H.,
    4. De Robertis E.
    (1991). Molecular nature of the Spemann's organizer: the role of the Xenopus homeobox gene goosecoid. Cell 67, 1111–1120
    OpenUrlCrossRefPubMedWeb of Science
    1. El Baradi T.,
    2. Pieler T.
    (1991). Zinc finger proteins: what we know and what we would like to know. Mech. Dev 35, 155–169
    OpenUrlCrossRefPubMedWeb of Science
    1. Felsenfeld A. L.,
    2. Curry M.,
    3. Kimmel C. B.
    (1991). The fub-1 mutation blocks initial myofibril formation in zebrafish muscle pioneer cells. Dev. Biol 148, 23–30
    OpenUrlCrossRefPubMedWeb of Science
    1. Gluecksohn-Schoenheimer S.
    (1944). The development of the normal and homozygous Brachyury (T/T) mouse embryos in the extraembryonic coelom of the chick. Proc. Nat. Acad. Sci.USA 30, 134–140
    OpenUrlFREE Full Text
    1. Harland R. M.
    (1991). In situ hybridization: an improved whole-mount method for Xenopus embryos. Meth. Cell Biol 36, 685–695
    OpenUrlCrossRefPubMedWeb of Science
    1. Herrmann B. G.,
    2. Labeit S.,
    3. Poustka A.,
    4. King T. R.,
    5. Lehrach H.
    (1990). Cloning of the T gene required in the mesoderm formation in the mouse. Nature 343, 617–622
    OpenUrlCrossRefPubMed
    1. Ho R. K.,
    2. Kane D. A.
    (1990). Cell-autonomous action of the zebrafish spadetail-1 mutation in specific mesodermal precursors. Nature 348, 728–730
    OpenUrlCrossRefPubMed
    1. Hopwood N. D.
    (1990). Cellular and genetic responses to mesoderm induction in Xenopus. BioEssays 12, 465–471
    OpenUrlCrossRefPubMed
    1. Hopwood V. D.,
    2. Pluck A.,
    3. Gurdon J. B.
    (1989). A Xenopus mRNA related to Drosophila twist is expressed in response to induction in the mesoderm and the neural crest cells. Cell 59, 893–903
    OpenUrlCrossRefPubMedWeb of Science
    1. Jessell T. M.,
    2. Melton D. A.
    (1992). Diffusible factors in vertebrate embryonic induction. Cell 68, 257–270
    OpenUrlCrossRefPubMedWeb of Science
    1. Jiang J.,
    2. Kosman D.,
    3. Ip Y. T.,
    4. Levine M.
    (1991). The dorsal morphogen gradient regulates the mesoderm determinant twist in early Drosophila embryo. Genes Dev 5, 1881–1891
    OpenUrlAbstract/FREE Full Text
    1. Kimmel C. B.
    (1989). Genetic and early development of the zebrafish embryos. Genetics 103, 125–136
    OpenUrl
    1. Kimmel C. B.,
    2. Warga R. M.
    (1987). Cell lineages generating axial muscle in the Zebrafish embryo. Nature 327, 234–237
    OpenUrlCrossRefPubMed
    1. Kimmel C. B.,
    2. Sepich D. S.,
    3. Trevarrow B.
    (1988). Development of segmentation in zebrafish. Development 104, 197–207
    OpenUrlAbstract/FREE Full Text
    1. Kimmel C. B.,
    2. Warga R. M.,
    3. Schilling T. F.
    (1990). Origin and organization of the zebrafish fate map. Development 108, 581–594
    OpenUrlAbstract/FREE Full Text
    1. Kimmel C. B.,
    2. Kane D. A.,
    3. Walker C.,
    4. Warga C. M.,
    5. Rothman M. B.
    (1989). A mutation that changes cell movement and cell fate in zebrafish embryo. Nature 337, 358–362
    OpenUrlCrossRefPubMed
    1. Lawrence P. A.
    (1989). Cell lineage and cell states in the Drosophila embryo. CIBA Found. Symp 144, 130–149
    OpenUrl
    1. Lin H. C.,
    2. Lei S.,
    3. Wilcox G.
    (1985). An improved DNA sequencing strategy. Anal. Biochem 147, 114–119
    OpenUrlCrossRefPubMedWeb of Science
    1. Martinez-Ariaz A.,
    2. Lawrence P. A.
    (1985). Parasegments and compartments in the Drosophila embryo. Nature 313, 639–642
    OpenUrlCrossRefPubMedWeb of Science
    1. Nieto M. A.,
    2. Bennett M. F.,
    3. Sargent M. G.,
    4. Wilkinson D. G.
    (1992). Cloning and developmental expression of Sna, a murine homologue of the Drosophila snail gene. Development 116, 227–237
    OpenUrlAbstract
    1. Ohara O.,
    2. Dorit R. L.,
    3. Gilbert W.
    (1989). One-sided polymerase chain reaction: the amplification of cDNA. Proc. Nat. Acad. Sci. USA 86, 5673–5677
    OpenUrlAbstract/FREE Full Text
    1. Pan D.,
    2. Huang J. D.,
    3. Courey A. J.
    (1991). Functional analyses of the Drosophila twist promoter reveals a dorsal binding ventral activator region. Genes Dev 5, 1892–1901
    OpenUrlCrossRefPubMedWeb of Science
    1. Roth S.,
    2. Stein D.,
    3. Nusslein-Volhard C.
    (1989). A gradient of nuclear localization of the dorsal protein determines dorso-ventral pattern in the Drosophila embryo. Cell 59, 1189–1202
    OpenUrlCrossRefPubMedWeb of Science
    1. Rushlow C.,
    2. Frasch M.,
    3. Doyle H.,
    4. Levine M.
    (1989). Maternal regulation of zerknullt: a homeobox gene controlling differentiation of dorsal tissues in Drosophila. Nature 330, 583–586
    OpenUrlAbstract/FREE Full Text
    1. Sargent M. G.,
    2. Bennett M. F.
    (1990). Identification in Xenopus of a structural homologue of the Drosophila gene snail. Development 109, 967–973
    OpenUrlAbstract/FREE Full Text
    1. Schulte-Merker S.,
    2. Ho R.,
    3. Herrmann B.,
    4. Nusslein-Volhard C.
    (1992). The protein product of the zebrafish homologue of the mouse T gene is expressed in nuclei of the germ-ring and the notochord of the early embryo. Development 116, 1021–1023
    OpenUrlAbstract/FREE Full Text
    1. Smith D. E.,
    2. Franco Del Amo F.,
    3. Gridley T.
    (1992). Isolation of Sna, a mouse gene homologous to the Drosophila genes snail and escargot: its expression pattern suggests multiple roles during post-implantation. Development 116, 1033–1039
    OpenUrlCrossRefPubMedWeb of Science
    1. Smith W. C.,
    2. Price B. M. J.,
    3. Green J. B. A.,
    4. Weigel D.,
    5. Herrmann B. G.
    (1991). Expression of a Xenopus homolog of Xbra (T) is an immediate-early response to mesoderm induction. Cell 67, 79–87
    OpenUrl
    1. Steward R.
    (1989). Relocalization of the dorsal protein from the cytoplasm to the nuclei correlates with its function. Cell 59, 1179–1188
    OpenUrlCrossRefPubMedWeb of Science
    1. Streisinger G. F.,
    2. Singer C.,
    3. Walker C.,
    4. Knauber D.,
    5. Dover N.
    (1986). Segregation analysis and gene-centromere distances in zebrafish. Genetics 112, 311–319
    OpenUrlCrossRefPubMedWeb of Science
    1. Thisse C.,
    2. Thisse B.
    (1992). Formation of the mesoderm in Drosophila involves a cascade of transcriptional regulation. Development 1992, 173–181
    OpenUrlPubMedWeb of Science
    1. Thisse C.,
    2. Perrin-Schmitt F.,
    3. Stoetzel C.,
    4. Thisse B.
    (1991). Sequence specific transactivation of the Drosophila twist gene by the dorsal gene product. Cell 65, 1191–1201
    OpenUrlCrossRefPubMedWeb of Science
    1. Thisse B.,
    2. Stoetzel C.,
    3. Gorostiza-Thisse C.,
    4. Perrin-Schmitt F.
    (1988). Sequence of the twist gene and nuclear localization of its protein in endomesodermal cells of early Drosophila embryos. EMBO J 7, 2175–2183
    OpenUrlPubMedWeb of Science
    1. Whiteley M.,
    2. Noguchi P. D.,
    3. Sensabaigh S. M.,
    4. Odenwald W. F.,
    5. Kassis K. A.
    (1992). The Drosophila gene escargot encodes a zinc finger motif found in snail -related genes. Mech. Dev 36, 117–127
    OpenUrlCrossRefPubMedWeb of Science
    1. Wilkinson D.,
    2. Krumlauf R.
    (1990). Molecular approaches to the segmentation of the hindbrain. Trends Neurosci 13, 235–240
    OpenUrlCrossRefPubMedWeb of Science
    1. Wilkinson D. G.,
    2. Bhatt S.,
    3. Herrmann B. G.
    (1990). Expression pattern of the mouse T gene and its role in mesoderm formation. Nature 343, 657–659
    OpenUrlCrossRefPubMed
    1. Wolf C.,
    2. Thisse C.,
    3. Stoetzel C.,
    4. Thisse B.,
    5. Gerlinger P.,
    6. Perrin-Schmitt F.
    (1991). The M- twist gene of Mus is expressed in subsets of mesodermal cells and is closely related to the Xenopus X-twi and the Drosophila twist genes. Dev. Biol 143, 363–373
    OpenUrlCrossRefPubMedWeb of Science
    1. Yanagisawa K. O.,
    2. Fujimoto H.,
    3. Urushihara H.
    (1981). Effects of the Brachyury (T) mutation on morphogenetic movement in the mouse embryo. Dev. Biol 87, 242–248
    OpenUrlCrossRefPubMed
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JOURNAL ARTICLES
Structure of the zebrafish snail1 gene and its expression in wild-type, spadetail and no tail mutant embryos
C. Thisse, B. Thisse, T.F. Schilling, J.H. Postlethwait
Development 1993 119: 1203-1215;
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