Neural development in Drosophila is promoted by a family of basic helix-loop-helix (bHLH) transcription factors encoded within the Achaete Scute-Complex (AS-C). XASH-3, a Xenopus homolog of the Drosophila AS-C genes, is expressed during neural induction within a portion of the dorsal ectoderm that gives rise to the neural plate and tube. Here, we show that XASH-3, when expressed with the promiscuous binding partner XE12, specifically activates the expression of neural genes in naive ectoderm, suggesting that XASH-3 promotes neural development. Moreover, XASH-3/XE12 RNA injections into embryos lead to hypertrophy of the neural tube. Interestingly, XASH-3 misexpression does not lead to the formation of ectopic neural tissue in ventral regions, suggesting that the domain of XASH proneural function is restricted in the embryo. In contrast to the neural inducer noggin, which permanently activates the NCAM gene, the activation of neural genes by XASH-3/XE12 is not stable in naive ectoderm, yet XASH-3/XE12 powerfully and stably activates NCAM, Neurofilament and type III beta-tubulin gene expression in noggin-treated ectoderm. These results show that the XASH-3 promotes neural development, and suggest that its activity depends on additional factors which are induced in ectoderm by factors such as noggin.
REFERENCES
Alonso
M. C.
, Cabrera
C. V.
(1988
) The achaete-scute gene complex of Drosophila melanogaster comprises four homologous genes.
EMBO J
7
, 2585
–91
Artavanis-Tsakonas
S.
, Simpson
P.
(1991
) Choosing a cell fate: a view from the Notch locus.
Trends Genet
7
, 403
–8
Benezra
R.
, Davis
R. L.
, Lockshon
D.
, Turner
D. L.
, Weintraub
H.
(1990
) The protein Id: a negative regulator of helix-loop-helix DNA binding proteins.
Cell
61
, 49
–59
Campos-Ortega
J.
, Jan
Y.
(1991
) Genetic and molecular basis of neurogenesis in Drosophila melanogaster.
Ann. Rev. Neurosci
14
, 399
–420
Campuzano
S.
, Modollel
J.
(1992
) Patterning of the Drosophila nervous system: the achaete-scute gene complex.
Trends Genet
8
, 202
–208
Cubas
P.
, Modolell
J.
(1992
) The extramacrochaetae gene provides information for sensory organ patterning.
EMBO J
11
, 3385
–3393
Dixon
J. E.
, Kintner
C. R.
(1989
) Cellular contacts required for neural induction in Xenopus embryos: evidence for two signals.
Development
106
, 749
–757
Dominguez
M.
, Campuzano
S.
(1993
) asense, a member of the Drosophila achaete-scute complex, is a proneural and neural differentiation gene.
EMBO J
12
, 2049
–2060
Ellis
H. M.
, Spann
D. R.
, Posakony
J. W.
(1990
) extramacrochaetae, a negative regulator of sensory organ development in Drosophila, defines a new class of helix-loop-helix proteins.
Cell
61
, 27
–38
Ferguson
E. L.
, Anderson
K. V.
(1992
) decapentaplegic acts as a morphogen to organize dorsal-ventral pattern in the Drosophila embryo.
Cell
71
, 451
–461
Ferreiro
B.
, Skoglund
P.
, Bailey
A.
, Dorsky
R.
, Harris
W. A.
(1993
) XASH-1, a Xenopus homolog of achaete-scute: a proneural gene in anterior regions of the vertebrate CNS.
Mech. Dev
40
, 25
–36
Garrell
J.
, Modolell
J.
(1990
) The Drosophilaextramacrochaetae locus, an antagonist of proneural genes that, like these genes, encodes a helix-loop-helix protein.
Cell
61
, 39
–48
Ghysen
A.
, Dambly
C. C.
(1988
) From DNA to form: the achaete-scute complex.
Genes Dev
2
, 495
–501
Green
J. B.
, Smith
J. C.
(1991
) Growth factors as morphogens: do gradients and thresholds establish body plan?.
Trends Genet
7
, 245
–250
Guillemot
F.
, Lo
L.-C.
, Johnson
J.
, Auerbach
A.
, Anderson
D.
, Joyner
A.
(1993
) Mammalian achaete-scute homolog-1 is required for the early development of olfactory and autonomic neurons.
Cell
75
, 1
–20
Harland
R. M.
(1991
) In situ hybridization: an improved whole-mount method for Xenopus embryos.
Methods Cell Biol
36
, 685
–95
Hopwood
N. D.
, Gurdon
J. B.
(1990
) Activation of muscle genes without myogenesis by ectopic expression of MyoD in frog embryo cells.
Nature
347
, 197
–200
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
Jarman
A.
, Grau
Y.
, Jan
L.
, Jan
Y.
(1993
) atonal is a proneural gene that directs chordotonal organ formation in the Drosophila peripheral nervous system.
Cell
73
, 1307
–1321
Jimenez
F.
, Campos-Ortega
J.
(1990
) Defective neuroblastcommitment in mutants of the achaete-scute complex and adjacent genes of D. melanogaster.
Neuron
5
, 81
–89
Johnson
J. E.
, Birren
S. J.
, Anderson
D. J.
(1990
) Two rat homologues of Drosophilaachaete-scute specifically expressed in neuronal precursors.
Nature
346
, 858
–861
Kintner
C.
(1992
) Molecular bases of early neural development in Xenopus embryos.
Ann. Rev. Neurosci
15
, 251
–284
Kintner
C. R.
, Melton
D. M.
(1987
) Expression of XenopusN-CAM RNA is an early response of ectoderm to induction.
Development
99
, 311
–325
Kosman
D.
, Ip
Y. T.
, Levine
M.
, Arora
K.
(1991
) Establishment of the mesoderm-neuroectoderm boundary in the Drosophila embryo.
Science
254
, 118
–122
Lamb
T. M.
, Knecht
A. K.
, Smith
W. C.
, Stachel
S. E.
, Economides
A. N.
, Stahl
N.
, Yancopolous
G. D.
, Harland
R. M.
(1993
) Neural induction by the secreted polypeptide noggin.
Science
262
, 713
–718
Lassar
A. B.
, Buskin
J. N.
, Lockshon
D.
, Davis
R. L.
, Apone
S.
, Hauschka
S. D.
, Weintraub
H.
(1989
) MyoD is a sequence-specific DNA binding protein requiring a region of myc homology to bind to the muscle creatine kinase enhancer.
Cell
58
, 823
–31
Murre
C.
, McCaw
P. S.
, Baltimore
D.
(1989
) A new DNA binding and dimerization motif in immunoglobulin enhancer binding, daughterless, MyoD, and myc proteins.
Cell
56
, 777
–783
Murre
C.
, McCaw
P. S.
, Vaessin
H.
, Caudy
M.
, Jan
L. Y.
, Jan
Y. N.
, Cabrera
C. V.
, Buskin
J. N.
, Hauschka
S. D.
, Lassar
A. B.
(1989
) Interactions between heterologous helix-loop-helix proteins generate complexes that bind specifically to a common DNA sequence.
Cell
58
, 537
–44
Parkhurst
S. M.
, Bopp
D.
, IshHorowicz
D.
(1990
) X:A ratio, the primary sex-determining signal in Drosophila, is transduced by helix-loop-helix proteins.
Cell
63
, 1179
–1191
Rashbass
J.
, Taylor
M.
, Gurdon
J.
(1992
) The DNA-binding protein E12 co-operates with XMyoD in the activation of muscle specific gene expression in Xenopus embryos.
EMBO J
11
, 2981
–2990
Rodriguez
I.
, Hernandez
R.
, Modolell
J.
, Ruiz Gomez
M.
(1990
) Competence to develop sensory organs is temporally and spatially regulated in Drosophila epidermal primordia.
EMBO J
9
, 3583
–3592
Ruezinsky
D.
, Beckmann
H.
, Kadesch
T.
(1991
) Modulation of the IgH enhancer's cell type specificity through a genetic switch.
Genes Dev
5
, 29
–37
Sharpe
C. R.
, Fritz
A.
, DeRobertis
E. M.
, Gurdon
J. B.
(1987
) A homoeobox-containing marker of posterior neural differentiation shows the importance of predetermination in neural induction.
Cell
50
, 749
–758
Slack
J. M.
, Tannahill
D.
(1992
) Mechanism of anteroposterior axis specification in vertebrates. Lessons from the amphibians.
Development
114
, 285
–302
Taira
M.
, Jamrich
M.
, Good
P.
, Dawid
I.
(1992
) The LIM domain-containing homeobox gene Xlim-1 is expressed specifically in the organizer region of Xenopus gastrula embryos.
Genes Dev
6
, 356
–366
Turner
D. L.
, Weintraub
H.
(1994
) Expression of achaete-scute homolog 3 in Xenopus embryos converts ectodermal cells to a neural fate.
Genes Dev
8
, 1434
–1447
Weintraub
H.
, Davis
R.
, Tapscott
S.
, Thayer
M.
, Krause
M.
, Benezra
R.
, Blackwell
T. K.
, Turner
D.
, Rupp
R.
, Hollenberg
S.
(1991
) The myoD gene family: nodal point during specification of the muscle cell lineage.
Science
251
, 761
–766
Weintraub
H.
, Dwarki
V. J.
, Verma
I.
, Davis
R.
, Hollenberg
S.
, Snider
L.
, Lassar
A.
, Tapscott
S. J.
(1991
) Muscle-specific transcriptional activation by MyoD.
Genes Dev
5
, 1377
–1386
Zimmerman
K.
, Shih
J.
, Bars
J.
, Collazo
A.
, Anderson
D. J.
(1993
) XASH-3, a novel Xenopus achaete-scute homolog, provides an early marker of planar neural induction and position along the mediolateral axis of the neural plate.
Development
119
, 221
–232
This content is only available via PDF.
© 1994 by Company of Biologists
1994
