Advertisement
JOURNAL ARTICLES
The expression of a zebrafish gene homologous to Drosophila snail suggests a conserved function in invertebrate and vertebrate gastrulation
M. Hammerschmidt, C. Nusslein-Volhard
Development 1993 119: 1107-1118;

Summary

Snail, a zinc finger protein, is required for the formation of the ventral furrow and the mesoderm during gastrulation of the Drosophila embryo. snail homologues have been cloned from Xenopus and mouse. We have isolated a zebrafish homologue of snail, designated sna-1. Like its Drosophila counterpart, Sna-1 protein is nuclear. Maternal and zygotic sna-1 transcripts are ubiquitously distributed in zebrafish embryos of cleavage and blastula stages. In gastrulating embryos, sna-1 is expressed in involuting cells of the germ ring, but not in those at the dorsal midline, the presumptive notochordal region. After involution, the expression is maintained in the paraxial mesoderm and becomes prominent in the muscle pioneer precursors, followed by expression at the posterior somite boundaries. Later, sna-1 is expressed in neural crest and mesodermal derivatives of the head region. Sna-1 expression is induced in animal cap cells by activin A. The early sna-1 expression pattern in gastrulating zebrafish no tail (ntl) mutant embryos is normal except a reduction in the level of sna-1 transcription, suggesting that Ntl protein is not the key activator of sna-1 transcription in vivo, but might be involved in the enhancement or maintenance of sna-1 transcription. Data obtained in studies with ectopic ntl expression support this model.

REFERENCES

    1. Amaya E.,
    2. Musci T. J.,
    3. Kirschner M. W.
    (1991). Expression of a dominant negative mutant of the FGF receptor disrupts mesoderm formation in Xenopus embryos. Cell 66, 257–270
    OpenUrlCrossRefPubMedWeb of Science
    1. Boulay J. L.,
    2. Dennefels C.,
    3. Alberga A.
    (1987). The Drosophila developmental gene snail encodes a protein with nucleic acid binding fingers. Nature 330, 395–398
    OpenUrlCrossRefPubMed
    1. Bronner-Fraser M.,
    2. Artinger M.,
    3. Muschler J.,
    4. Horwitz A. F.
    (1992). Developmentally regulated expression of6 integrin in avian embryos. Development 115, 197–211
    OpenUrlAbstract
    1. Chesley P.
    (1935). Development of the short-tailed mutation in the house mouse. J. Exp. Zool 70, 429–459
    OpenUrlCrossRefWeb of Science
    1. Collodi P.,
    2. Yuto K.,
    3. Ernst T.,
    4. Miranda C.,
    5. Buhler D. R.,
    6. Barnes D. W.
    (1992). Culture of cells from zebrafish (Brachydanio rerio) embryo and adult tissues. Cell Biol. Tox 8, 43–61
    OpenUrlCrossRefPubMedWeb of Science
    1. Cunliffe V.,
    2. Smith J. C.
    (1992). Ectopic mesoderm formation in Xenopus embryos caused by widespread expression of a Brachyury homologue. Nature 358, 427–430
    OpenUrlCrossRefPubMed
    1. Driever W.,
    2. Siegel V.,
    3. Nusslein-Volhard C.
    (1990). Autonomousdetermination of anterior structures in the early Drosophila embryo by the bicoid morphogen. Development 109, 811–820
    OpenUrlAbstract/FREE Full Text
    1. Ekker M.,
    2. Wegner J.,
    3. Akimenko M. A.,
    4. Westerfield M.
    (1992). Coordinate expression of three zebrafish engrailed genes. Development 116, 1001–1010
    OpenUrlAbstract/FREE Full Text
    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. Halpern M. E.,
    2. Ho R. K.,
    3. Walker C.,
    4. Kimmel C. B.
    (1993). Induction of muscle pioneers and floor plate is distinguished by the zebrafish no tail mutation. Cell 75, 1–20
    OpenUrlCrossRefPubMedWeb of Science
    1. Hatta K.,
    2. BreMiller R.,
    3. Westerfield M.,
    4. Kimmel C.B.
    (1991). Diversity of expression of engrailed -like antigens in zebrafish. Development 112, 821–832
    OpenUrlAbstract
    1. Hemmati-Brivanlou A.,
    2. Melton D. A.
    (1992). A truncated activin receptor inhibits mesoderm induction and formation of axial structures in Xenopus embryos. Nature 359, 609–614
    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 mesoderm formation in the mouse. Nature 343, 617–622
    OpenUrlCrossRefPubMed
    1. Ho R. K.,
    2. Kane D. A.
    (1990). Cell-autonomous action of zebrafish spt-1 mutation in specific mesodermal precursors. Nature 348, 728–730
    OpenUrlCrossRefPubMed
    1. Hopwood N.,
    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. Cell 59, 893–903
    OpenUrlCrossRefPubMedWeb of Science
    1. Keynes R. J.,
    2. Stern C. D.
    (1984). Segmentation in the vertebrate nervous system. Nature 310, 786–789
    OpenUrlCrossRefPubMedWeb of Science
    1. Kimmel C. B.,
    2. Kane D. A.,
    3. Walker C.,
    4. Warga R. M.,
    5. Rothmann M. A.
    (1989). A mutation that changes cell movement and cell fate in the zebrafish embryo. Nature 337, 358–362
    OpenUrlCrossRefPubMed
    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. Laemmli U. K.
    (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685
    OpenUrlCrossRefPubMedWeb of Science
    1. Layer P. G.,
    2. Alber R.,
    3. Rathjen F. G.
    (1988). Sequential activation of butyrylcholinesterase in rostral half somites and acetylcholinesterase in motoneurones and myotomes preceding growth of motor axons. Development 102, 387–396
    OpenUrlAbstract
    1. McGinnis W.,
    2. Krumlauf R.
    (1992). Homeobox genes and axial patterning. Cell 68, 283–302
    OpenUrlCrossRefPubMedWeb of Science
    1. Myers P. Z.,
    2. Eisen J. S.,
    3. Westerfield M.
    (1986). Development and axonal outgrowth of identified motoneurons in the zebrafish. J. Neurosci 6, 2278–2289
    OpenUrlAbstract
    1. Nieto M. A.,
    2. Bennet 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. Raible D. W.,
    2. Wood A.,
    3. Hodson W.,
    4. Henion P. D.,
    5. Weston J.A.,
    6. Eisen J. S.
    (1992). Segregation and early dispersal of neural crest cells in the embryonic zebrafish. Dev. Dynamics 195, 29–42
    OpenUrlCrossRefPubMedWeb of Science
    1. Rickmann M.,
    2. Fawcett J. W.,
    3. Keynes R. J.
    (1985). The migration of neural crest cells and the growth of motor axons through the rostral half of the chick embryo. J. Embryol. Exp. Morph 90, 437–455
    OpenUrlPubMedWeb of Science
    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. K.,
    3. Herrmann B. G.,
    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, 1021–1032
    OpenUrlAbstract/FREE Full Text
    1. Smith D. E.,
    2. Del Amo F. 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 postimplantation development. Development 116, 1033–1039
    OpenUrlAbstract/FREE Full Text
    1. Smith J. C.
    (1989). Mesoderm induction and mesoderm-inducing factors in early amphibian development. Development 105, 665–677
    OpenUrlFREE Full Text
    1. Smith J. 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 Brachyury (T) is an immediate-early response to mesoderm induction. Cell 67, 79–87
    OpenUrlCrossRefPubMedWeb of Science
    1. Solursh M.,
    2. Drake C.,
    3. Meier S.
    (1987). The migration of myogenic cells from the somite at the wing level in avian embryos. Dev. Biol 102, 509–513
    OpenUrlCrossRef
    1. St. Johnston D.,
    2. Nusslein-Volhard C.
    (1992). The origin of pattern and polarity in the Drosophila embryo. Cell 68, 201–219
    OpenUrlCrossRefPubMedWeb of Science
    1. Thisse B.,
    2. Stoetzel C.,
    3. Gorostiza-Thisse C.,
    4. Schmitt-Perrin 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. Towbin H.,
    2. Stacklin T.,
    3. Gurdon J.
    (1979). Electrophoretic transfer of protein from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. Proc. Natl. Acad. Sci. USA 76, 4350–4357
    OpenUrlAbstract/FREE Full Text
    1. Warga R. M.,
    2. Kimmel C. B.
    (1990). Cell movements during epiboly and gastrulation in zebrafish. Development 108, 569–580
    OpenUrlAbstract/FREE Full Text
    1. Whiteley M.,
    2. Nogushi P. D.,
    3. Sensabaugh S. M.,
    4. Odenwald W. F.,
    5. Kassis J. 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. Wolf C.,
    2. Thisse C.,
    3. Stoetzel C.,
    4. Thisse B.,
    5. Gerlinger P.,
    6. Perrin-Schmitt F.
    (1991). The m-twist gene in Mus is expressed in subsets of mesodermal cells and is closely related to the Xenopus X-twi and the Drosophilatwist genes. Dev. Biol 143, 363–373
    OpenUrlCrossRefPubMedWeb of Science
    1. Yanagisawa K. O.,
    2. Fufimoto H.,
    3. Urshihara H.
    (1981). Effects of the Brachyury (T) mutation on morphogenetic movement in the mouse embryo. Dev. Biol 87, 242–248
    OpenUrlCrossRefPubMed
Back to top

 Download PDF

Email
JOURNAL ARTICLES
The expression of a zebrafish gene homologous to Drosophila snail suggests a conserved function in invertebrate and vertebrate gastrulation
M. Hammerschmidt, C. Nusslein-Volhard
Development 1993 119: 1107-1118;
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
Alerts

Article navigation

Other journals from The Company of Biologists

Advertisement

An interview with Swathi Arur

Swathi Arur joined the team at Development as an Academic Editor in 2020. Her lab uses multidisciplinary approaches to understand female germline development and fertility. We met with her over Zoom to hear more about her life, her career and her love for C. elegans.

Jim Wells and Hanna Mikkola join our team of Editors

We are pleased to welcome James (Jim) Wells and Hanna Mikkola to our team of Editors. Jim joins us a new Academic Editor, taking over from Gordan Keller, and Hanna joins our team of Associate Editors. Find out more about their research interests and areas of expertise.

New funding scheme supports sustainable events

As part of our Sustainable Conferencing Initiative, we are pleased to announce funding for organisers that seek to reduce the environmental footprint of their event. The next deadline to apply for a Scientific Meeting grant is 26 March 2021.

Read & Publish participation continues to grow

“I’d heard of Read & Publish deals and knew that many universities, including mine, had signed up to them but I had not previously understood the benefits that these deals bring to authors who work at those universities.”

Professor Sally Lowell (University of Edinburgh) shares her experience of publishing Open Access as part of our growing Read & Publish initiative. We now have over 150 institutions in 15 countries and four library consortia taking part – find out more and view our full list of participating institutions.

Upcoming special issues

Imaging Development, Stem Cells and Regeneration
Submission deadline: 30 March 2021
Publication: mid-2021

The Immune System in Development and Regeneration
Guest editors: Florent Ginhoux and Paul Martin
Submission deadline: 1 September 2021
Publication: Spring 2022

Both special issues welcome Review articles as well as Research articles, and will be widely promoted online and at key global conferences.

Development presents...

Our successful webinar series continues into 2021, with early-career researchers presenting their papers and a chance to virtually network with the developmental biology community afterwards. Here, Michèle Romanos talks about her new preprint, which mixes experimentation in quail embryos and computational modelling to understand how heterogeneity in a tissue influences cell rate.

Save your spot at our next session:

10 March
Time: 9:00 (GMT)
Chaired by: Thomas Lecuit

Join our mailing list to receive news and updates on the series.