The Drosophila gene snail encodes a zinc-finger protein that is required zygotically for mesoderm formation. Snail acts as a transcriptional repressor during the period of mesoderm formation by preventing expression of mesectodermal and ectodermal genes in the mesoderm anlage. A Xenopus homolog (xsnail) of snail has been cloned and it too is expressed early in the mesodermal germ layer. We have isolated cDNA clones of a mouse gene (termed Sna) closely related to snail and xsnail and another Drosophila gene termed escargot that also encodes a zinc-finger protein. Sna encodes a 264 amino acid protein that contains four zinc fingers. Developmental RNA blot analysis showed that Sna transcripts are expressed throughout postimplantation development. Analysis of the spatial and temporal localization of Sna transcripts by in situ hybridization to both whole-mount and sectioned embryos revealed that, in the gastrulating embryo, Sna is expressed throughout the primitive streak and in the entire mesodermal germ layer. By 9.5 days post coitum (dpc) Sna is expressed at high levels in cephalic neural crest and limb bud mesenchyme. In fact, by 10.5 dpc Sna expression is observed in most mesenchymal cells, whether of neural crest or mesodermal origin. Later in gestation, high levels of Sna expression are observed in condensing cartilage and in the mesenchymal component of several tissues (lung, kidney, teeth and vibrissae) that undergo epithelial-mesenchymal inductive interactions during development. These results suggest multiple roles for the Sna gene in gastrulation and organogenesis during murine development.

REFERENCES

Alberga
A.
,
Boulay
J.-L.
,
Kempe
E.
,
Dennefeld
C.
,
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
Amaya
E.
,
Musci
T. J.
,
Kirschner
M. W.
(
1991
)
Expression of a dominant negative mutant of the FGF receptor disrupts mesoderm formation in Xenopus embryos.
Cell
66
,
257
270
Anderson
K. V.
(
1987
)
Dorsal-ventral embryonic pattern genes of Drosophila.
Trends Genet
3
,
91
96
Boulay
J. L.
,
Dennefeld
C.
,
Alberga
A.
(
1987
)
The Drosophila developmental gene snail encodes a protein with nucleic acid binding fingers.
Nature
330
,
395
398
Chomczynski
P.
,
Sacchi
N.
(
1987
)
Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction.
Analyt. Biochem
162
,
156
159
Devereux
J.
,
Haeberli
P.
,
Smithies
O.
(
1984
)
A comprehensive set of sequence analysis programs for the VAX.
Nucl. Acids Res
12
,
387
395
Fahrner
K.
,
Hogan
B. L. M.
,
Flavell
R. A.
(
1987
)
Transcription of the H-2 and Qa genes in embryonic and adult mice.
EMBO J
6
,
1265
1271
Franco del Amo
F.
,
Smith
D. E.
,
Swiatek
P. J.
,
Gendron-Maguire
M.
,
Greenspan
R. J.
,
McMahon
A. P.
,
Gridley
T.
(
1992
)
Expression of Motch, a mouse homolog of Drosophila Notch, suggests an important role in early postimplantation mouse development.
Development
115
,
737
745
Gibson
T. J.
,
Postma
J. P. M.
,
Brown
R. S.
,
Argos
P.
(
1988
)
A model for the tertiary structure of the 28 residues DNA-binding motif (zinc-finger) common to many transcriptional regulatory proteins.
Protein Engineering
20
,
209
218
Grau
Y.
,
Carteret
C.
,
Simpson
P.
(
1984
)
Mutations and chromosomal rearrangements affecting the expression of snail, a gene involved in embryonic patterning in Drosophila.
Genetics
108
,
347
360
Gridley
T.
(
1991
)
Insertional versus targeted mutagenesis in mice.
New Biologist
3
,
1025
1034
Hardy
M. H.
(
1992
)
The secret life of the hair follicle.
Trends Genet
8
,
55
61
Haub
O.
,
Goldfarb
M.
(
1991
)
Expression of the fibroblast growth factor-5 gene in the mouse embryo.
Development
112
,
397
406
Hebert
J. M.
,
Boyle
M.
,
Martin
G. R.
(
1991
)
mRNA localization studies suggest that murine FGF-5 plays a role in gastrulation.
Development
112
,
407
415
Hemmati-Brivanlou
A.
,
Frank
D.
,
Bolce
M. E.
,
Brown
B. D.
,
Sive
H. L.
,
Harland
R. M.
(
1990
)
Localization of specific mRNAs in Xenopus embryos by whole-mount in situ hybridization.
Development
110
,
325
330
Herrmann
B. G.
(
1991
).
Expression pattern of the Brachury gene in whole-mount TWis /TWis mutant embryos..
Development
113
,
913
917
Hopwood
N. D.
(
1990
)
Cellular and genetic responses to mesoderm induction in Xenopus.
BioEssays
12
,
465
471
Hopwood
N. D.
,
Pluck
A.
,
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
Isaacs
H. V.
,
Tannahill
D.
,
Slack
J. M. W.
(
1992
)
Expression of a novel FGF in the Xenopus embryo. A new candidate inducing factor for mesoderm formation and anteroposterior specification.
Development
114
,
711
720
Jessell
T. M.
,
Melton
D. A.
(
1992
)
Diffusible factors in vertebrate embryonic induction.
Cell
68
,
257
270
Kasai
Y.
,
Nambu
J. R.
,
Lieberman
P. M.
,
Crews
S. T.
(
1992
)
Dorsal-ventral patterning in Drosophila: DNA binding of snail protein to the single-minded gene.
Proc. Natl. Acad. Sci. USA
89
,
3414
3418
Kessel
M.
,
Gruss
P.
(
1990
)
Murine developmental control genes.
Science
249
,
374
379
Kimelman
D.
,
Abraham
J. A.
,
Haaparanta
T.
,
Palisi
T. M.
,
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
Kosman
D.
,
Ip
Y. T.
,
Levine
M.
,
Arora
K.
(
1991
)
Establishment of the mesoderm-neuroectoderm boundary in the Drosophila embryo.
Science
254
,
118
122
Kozak
M.
(
1987
)
An analysis of 5-noncoding sequences from 699 vertebrate messenger RNAs.
Nucl. Acids Res
15
,
8125
8148
Leptin
M.
(
1991
)
twist and snail as positive and negative regulators during Drosophila mesoderm development.
Genes Dev
5
,
1568
1576
Leptin
M.
,
Grunewald
B.
(
1990
)
Cell shape changes during gastrulation in Drosophila.
Development
110
,
73
84
Lumsden
A. G. S.
(
1988
)
Spatial organization of the epithelium and the role of neural crest cells in the initiation of the mammalian tooth germ.
Development
103
,
155
169
Maden
M.
,
Holder
N.
(
1992
)
The involvement of retinoic acid in the development of the vertebrate central nervous system.
Development
2
,
87
94
Manova
K.
,
Paynton
B. V.
,
Bacharova
R. F.
(
1992
)
Expression of activins and TGF1 and 2 RNAs in early postimplantation mouse embryos and uterine decidua.
Mech. Dev
36
,
141
152
Mitrani
E.
,
Ziv
T.
,
Thomsen
G.
,
Shimoni
Y.
,
Melton
D. A.
,
Bril
A.
(
1990
)
Activin can induce the formation of axial structures and is expressed in the hypoblast of the chick.
Cell
63
,
495
501
Nambu
J. R.
,
Franks
R. G.
,
Hu
S.
,
Crews
S. T.
(
1990
)
The single-minded gene of Drosophila is required for the expression of genes important for the development of CNS midline cells.
Cell
63
,
63
75
Nietfeld
W.
,
El-Baradi
T.
,
Mentzl
H.
,
Pieler
T.
,
Koster
M.
,
Poting
A.
,
Knochel
W.
(
1989
)
Second order repeats in Xenopuslaevis finger proteins.
J. Molec. Biol
208
,
639
659
Niswander
L.
,
Martin
G. R.
(
1992
)
Fgf-4 expression during gastrulation, myogenesis, limb and tooth development in the mouse.
Development
114
,
755
768
Noden
D.
(
1988
)
Interactions and fates of avian craniofacial mesenchyme.
Development
103
,
121
140
Rossant
J.
,
Hopkins
N.
(
1992
)
Of fin and fur: mutational analysis of vertebrate embryonic development.
Genes Dev
6
,
1
13
Ruberte
E.
,
Dolle
P.
,
Chambon
P.
,
Morriss-Kay
G.
(
1991
)
Retinoic acid receptors and cellular retinoid binding proteins. II. Their differential pattern of transcription during early morphogenesis in mouse embryos.
Development
111
,
45
60
Rushlow
C.
,
Arora
K.
(
1990
)
Dorsal ventral polarity and pattern formation in the Drosophila embryo.
Seminars in Cell Bio
1
,
137
149
Rushlow
C.
,
Warrior
R.
(
1992
)
The rel family of proteins.
BioEssays
14
,
89
95
Sargent
M. G.
,
Bennett
M. F.
(
1990
)
Identification in Xenopus of a structural homologue of the Drosophila gene snail.
Development
109
,
967
973
Simpson
P.
(
1983
)
Maternal-zygotic gene interactions during formation of the dorsoventral pattern in Drosophila embryos.
Genetics
105
,
615
632
Slack
J. M. W.
,
Isaacs
H. V.
(
1989
)
Presence of basic fibroblast growth factor in the early Xenopus embryo.
Development
105
,
147
153
Slager
H. G.
,
Lawson
K. A.
,
van den Eijnden-van Raaij
A. J. M.
,
de Laat
S. W.
,
Mummery
C. L.
(
1991
)
Differential localization of TGF2 in mouse preimplantation and early postimplantation development.
Dev. Biol
145
,
205
218
Smith
J. C.
(
1989
)
Mesoderm induction and mesoderm-inducing factors in early amphibian development.
Development
105
,
665
677
St. Johnston
D.
,
Nusslein-Volhard
C.
(
1992
)
The origin of pattern and polarity in the Drosophila embryo.
Cell
68
,
201
219
Stern
C. D.
(
1992
)
Mesoderm induction and development of the embryonic axis in amniotes.
Trends Genet
8
,
158
163
Tautz
D.
,
Pfeifle
C.
(
1989
)
A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback.
Chromosoma
98
,
81
85
Thesleff
I.
,
Vainio
S.
,
Jalkanen
M.
(
1989
)
Cell-matrix interactions in tooth development.
Int. J. Dev. Biol
33
,
91
97
Thisse
B.
,
Stoetzel
C.
,
Gorostiza
T. C.
,
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
Thomsen
G.
,
Woolf
T.
,
Whitman
M.
,
Sokol
S.
,
Vaughan
J.
,
Vale
W.
,
Melton
D. A.
(
1990
)
Activins are expressed in Xenopus embryogenesis and can induce axial mesoderm and anterior structures.
Cell
63
,
485
493
Whiteley
M.
,
Noguchi
P. D.
,
Sensabaugh
S. M.
,
Odenwald
W. F.
,
Kassis
J. A.
(
1992
)
The Drosophila gene escargot encodes a zinc finger motif found in snail -related genes.
Mech. Dev
36
,
117
127
Wilkinson
D. G.
,
Bhatt
S.
,
Herrmann
B. G.
(
1990
)
Expression pattern of the mouse T gene and its role in mesoderm formation.
Nature
343
,
657
659
Wilkinson
D. G.
,
Peters
G.
,
Dickson
C.
,
McMahon
A. P.
(
1988
)
Expression of the FGF-related proto-oncogene int-2 during gastrulation and neurulation in the mouse.
EMBO J
7
,
691
695
Wolf
C.
,
Thisse
C.
,
Stoetzel
C.
,
Thisse
B.
,
Gerlinger
P.
,
Perrin-Schmitt
F.
(
1991
)
The M-twist 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
Yanagisawa
K. O.
,
Fujimoto
H.
,
Urushihara
H.
(
1981
)
Effects of the Brachyury (T) mutation on morphogenetic movement in the mouse embryo.
Dev. Biol
87
,
242
248
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