Differentiation in the Drosophila eye imaginal disc traverses the disc as a wave moving from posterior to anterior. The propagation of this wave is driven by hedgehog protein secreted by the differentiated cells in the posterior region of the disc. Hedgehog induces decapentaplegic expression at the front of differentiation, in the morphogenetic furrow. We have identified a gene, shortsighted, which is expressed in a hedgehog-dependent stripe in the undifferentiated cells just anterior to the furrow and which appears to be involved in the transmission of the differentiation-inducing signal; a reduction in shortsighted function leads to a delay in differentiation and to a loss of photoreceptors in the adult. shortsighted is also required for a morphogenetic movement in the brain that reorients the second optic lobe relative to the first. shortsighted encodes a cytoplasmic leucine zipper protein with homology to a mouse gene, TSC-22, which is transcriptionally induced in response to TGF-beta.

Reference

Baker
N. E.
,
Mlodzik
M.
,
Rubin
G. M.
(
1990
)
Spacing differentiation in the developing Drosophila eye: a fibrinogen-related lateral inhibitor encoded by scabrous.
Science
250
,
1370
1377
Basler
K.
,
Struhl
G.
(
1994
)
Compartment boundaries and the control of Drosophila limb pattern by hedgehog protein.
Nature
368
,
208
214
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
Blackman
R. K.
,
Sanicola
M.
,
Raftery
L. A.
,
Gillevet
T.
,
Gelbart
W. M.
(
1991
)
An extensive 3 cis -regulatory region directs the imaginal disc expression of decapentaplegic, a member of the TGF-family in Drosophila.
Development
111
,
657
665
Bohmann
D.
,
Ellis
M. C.
,
Staszewski
L. M.
,
Mlodzik
M.
(
1994
)
Drosophila jun mediates ras -dependent photoreceptor determination.
Cell
78
,
973
986
Brown
N. L.
,
Sattler
C. A.
,
Markey
D. R.
,
Carroll
S. B.
(
1991
)
hairy gene function in the Drosophila eye: normal expression is dispensable but ectopic expression alters cell fates.
Development
113
,
1245
56
Brummel
T. J.
,
Twombly
V.
,
Marques
G.
,
Wrana
J. L.
,
Newfeld
S. J.
,
Attisano
L.
,
Massague
J.
,
O'Connor
M. B.
,
Gelbart
W. M.
(
1994
)
Characterization and relationship of dpp receptors encoded by the saxophone and thick veins genes in Drosophila.
Cell
78
,
251
262
Busch
S. J.
,
Sassone-Corsi
P.
(
1990
)
Dimers, leucine zippers and DNA-binding domains.
Trends Genet
6
,
36
40
Campbell
G.
,
Weaver
T.
,
Tomlinson
A.
(
1993
)
Axis specification in the developing Drosophila appendage: the role of wingless, decapentaplegic, and the homeobox gene aristaless.
Cell
74
,
1113
1123
Couso
J. P.
,
Bate
M.
,
Martinez Arias
A.
(
1993
)
A wingless -dependent polar coordinate system in Drosophila imaginal discs.
Science
259
,
484
489
Couso
J. P.
,
Bishop
S. A.
,
Martinez Arias
A.
(
1994
)
The wingless signaling pathway and the patterning of the wing margin in Drosophila.
Development
120
,
621
636
Couso
J. P.
,
Martinez Arias
A.
(
1994
)
Notch is required for wingless signaling in the epidermis of Drosophila.
Cell
79
,
259
272
Diaz-Benjumea
F. J.
,
Cohen
B.
,
Cohen
S. M.
(
1994
)
Cell interaction between compartments establishes the proximal-distal axis of Drosophila legs.
Nature
372
,
175
179
Echelard
Y.
,
Epstein
D. J.
,
St-Jacques
B.
,
Shen
L.
,
Mohler
J.
,
McMahon
J. A.
,
McMahon
A. P.
(
1993
)
Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity.
Cell
75
,
1417
1430
Edgar
B. A.
,
O'Farrell
P. H.
(
1989
)
Genetic control of cell division patterns in the Drosophila embryo.
Cell
57
,
177
187
Felsenfeld
A. L.
,
Kennison
J. A.
(
1995
)
Positional signaling by hedgehog in Drosophila imaginal disc development.
Development
121
,
1
10
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
Fiscbach
K. F.
,
Technau
G.
(
1984
)
Cell degeneration in the developing optic lobes of the sine oculis and small optic-lobes mutants of Drosophila melanogaster.
Dev. Biol
104
,
219
239
Hamil
K. G.
,
Hall
S. H.
(
1994
)
Cloning of rat Sertoli cell follicle-stimulating hormone primary response complementary deoxyribonucleic acid: regulation of TSC-22 gene expression.
Endocrinology
134
,
1205
1212
Hay
B. A.
,
Wolff
T.
,
Rubin
G. M.
(
1994
)
Expression of baculovirus P35 prevents cell death in Drosophila.
Development
120
,
2121
2129
Heberlein
U.
,
Wolff
T.
,
Rubin
G. M.
(
1993
)
The TGFhomolog dpp and the segment polarity gene hedgehog are required for propagation of a morphogenetic wave in the Drosophila retina.
Cell
75
,
913
926
Jarman
A. P.
,
Grell
E. H.
,
Ackerman
L.
,
Jan
L. Y.
,
Jan
Y. N.
(
1994
)
atonal is the proneural gene for Drosophila photoreceptors.
Nature
369
,
398
400
Jiang
J.
,
Struhl
G.
(
1995
)
Protein kinase A and hedgehog signaling in Drosophila limb development.
Cell
80
,
563
572
Kaphingst
K.
,
Kunes
S.
(
1994
)
Pattern formation in the visual centers of the Drosophila brain: wingless acts via decapentaplegic to specify the dorsoventral axis.
Cell
78
,
437
448
Karpen
G. H.
,
Spradling
A. C.
(
1992
)
Analysis of subtelomeric heterochromatin in the Drosophila minichromosome Dp1187 by single P-element insertional mutagenesis.
Genetics
132
,
737
753
Kassis
J. A.
,
Noll
E.
,
VanSickle
E. P.
,
Odenwald
W. F.
,
Perrimon
N.
(
1992
)
Altering the insertional specificity of a Drosophila transposable element.
Proc. Natl. Acad. Sci. USA
89
,
1919
1923
Kimmel
B. E.
,
Heberlein
U.
,
Rubin
G. M.
(
1990
)
The homeodomain protein rough is expressed in a subset of cells in the developing Drosophila eye where it can specify photoreceptor cell subtype.
Genes Dev
4
,
712
727
Kingsley
D.
(
1994
)
The TGF-superfamily: new members, new receptors, and new genetic tests of function in different organisms.
Genes Dev
8
,
133
146
Kolodkin
A. L.
,
Pickup
A. T.
,
Lin
D. M.
,
Goodman
C. S.
,
Banerjee
U.
(
1994
)
Characterization of Star and its interactions with sevenless and EGF receptor during photoreceptor cell development in Drosophila.
Development
120
,
1731
1745
Krauss
S.
,
Concordet
J. P.
,
Ingham
P. W.
(
1993
)
A functionally conserved homolog of the Drosophila segment polarity gene hh is expressed in tissues with polarizing activity in zebrafish embryos.
Cell
75
,
1431
1444
Kunes
S.
,
Steller
H.
(
1993
)
Topography in the Drosophila visual system.
Curr. Opin. Neurobiol
3
,
53
59
Lai
Z.
,
Rubin
G. M.
(
1992
)
Negative control of photoreceptor development in Drosophila by the product of the yan gene, an ETS domain protein.
Cell
70
,
609
620
Lee
J. J.
,
von Kessler
D. P.
,
Parks
S.
,
Beachy
P. A.
(
1992
)
Secretion and localized transcription suggest a role in positional signaling for products of the segmentation gene hedgehog.
Cell
71
,
33
50
Lepage
T.
,
Cohen
S. M.
,
Diaz-Benjumea
F. J.
,
Parkhurst
S. M.
(
1995
)
Signal transduction by cAMP-dependent protein kinase A in Drosophila limb patterning.
Nature
373
,
711
715
Li
W.
,
Ohlmeyer
J. T.
,
Lane
M. E.
,
Kalderon
D.
(
1995
)
Function of protein kinase A in hedgehog signal transduction and Drosophila imaginal disc development.
Cell
80
,
553
562
Ma
C.
,
Zhou
Y.
,
Beachy
P. A.
,
Moses
K.
(
1993
)
The segment polaritygene hedgehog is required for progression of the morphogenetic furrow in the developing Drosophila eye.
Cell
75
,
927
938
Massague
J.
(
1992
)
Receptors for the TGF-family.
Cell
69
,
1067
1070
Masucci
J. D.
,
Miltenberger
R. J.
,
Hoffmann
F. M.
(
1990
)
Pattern-specific expression of the Drosophila decapentaplegic gene in imaginal discs is regulated by 3cis-regulatory elements.
Genes Dev
4
,
2011
2023
Meyerowitz
E. M.
,
Kankel
D. R.
(
1978
)
A genetic analysis of visual system development in Drosophila melanogaster.
Dev. Biol
62
,
112
142
Mismer
D.
,
Rubin
G. M.
(
1987
)
Analysis of the promoter of the ninaE opsin gene in Drosophila melanogaster.
Genetics
116
,
565
578
Mlodzik
M.
,
Baker
N. E.
,
Rubin
G. M.
(
1990
)
Isolation and expression of scabrous, a gene regulating neurogenesis in Drosophila.
Genes Dev
4
,
1848
1861
Naumann
M.
,
Nieters
A.
,
Hatada
E. N.
,
Scheidereit
C.
(
1993
)
NF-B precursor p100 inhibits nuclear translocation and DNA binding of NF- B/ rel -factors.
Oncogene
8
,
2275
2281
Nellen
D.
,
Affolter
A.
,
Basler
K.
(
1994
)
Receptor serine/threonine kinases implicated in the control of Drosophila body pattern by decapentaplegic.
Cell
78
,
225
237
Nolan
G. P.
,
Baltimore
D.
(
1992
)
The inhibitory ankyrin and activator Rel proteins.
Curr. Op. Gen. Dev
2
,
211
220
Nusse
R.
,
Varmus
H. E.
(
1992
)
Wnt genes.
Cell
69
,
1073
1087
Pan
D.
,
Rubin
G. M.
(
1995
)
cAMP-dependent protein kinase and hedgehog act antagonistically in regulating decapentaplegic transcription in Drosophila imaginal discs.
Cell
80
,
543
552
Penton
A.
,
Chen
Y.
,
Staehling-Hampton
K.
,
Wrana
J. L.
,
Attisano
L.
,
Szidonya
J.
,
Cassill
J. A.
,
Massague
J.
,
Hoffmann
F. M.
(
1994
)
Identification of two bone morphogenetic protein type I receptors in Drosophila and evidence that Brk25D is a decapentaplegic receptor.
Cell
78
,
239
250
Pertovaara
L.
,
Sistonen
L.
,
Bos
T. J.
,
Vogt
P. K.
,
Keski-Oja
J.
,
Alitalo
K.
(
1989
)
Enhanced jun gene expression is an early genomic response to transforming growth factorstimulation.
Mol. Cell Biol
9
,
1255
1262
Ready
D. F.
,
Hanson
T. E.
,
Benzer
S.
(
1976
)
Development of the Drosophila retina, a neurocrystalline lattice.
Dev. Biol
53
,
217
240
Riddle
R. D.
,
Johnson
R. L.
,
Tabin
C.
(
1993
)
Sonic hedgehog mediates the polarizing activity of the ZPA.
Cell
75
,
1401
1416
Robinow
S.
,
White
K.
(
1991
)
Characterization and spatial distribution of the ELAV protein during Drosophila melanogaster development.
J. Neurobiol
22
,
443
461
Selleck
S. B.
,
Steller
H.
(
1991
)
The influence of retinal innervation on neurogenesis in the first optic ganglion of Drosophila.
Neuron
6
,
83
99
Shibanuma
M.
,
Kuroki
T.
,
Nose
K.
(
1992
)
Isolation of a gene encoding a putative leucine zipper structure that is induced by transforming growth factor1 and other growth factors.
J. Biol. Chem
267
,
10219
10224
Struhl
G.
,
Basler
K.
(
1993
)
Organizing activity of wingless protein in Drosophila.
Cell
72
,
527
540
Strutt
D. I.
,
Wiersdorff
V.
,
Mlodzik
M.
(
1995
)
Regulation of furrow progression in the Drosophila eye by cAMP-dependent protein kinase A.
Nature
373
,
705
709
Tabata
T.
,
Kornberg
T. B.
(
1994
)
Hedgehog is a signaling protein with a key role in patterning Drosophila imaginal discs.
Cell
76
,
89
102
Tamkun
J. W.
,
Deuring
R.
,
Scott
M. P.
,
Kissinger
M.
,
Pattatucci
A. M.
,
Kaufman
T. C.
,
Kennison
J. A.
(
1992
)
brahma: a regulator of Drosophila homeotic genes structurally related to the yeast transcriptional activator SNF2/SWI2.
Cell
68
,
561
572
Tomlinson
A.
,
Ready
D. F.
(
1987
)
Cell fate in the Drosophila ommatidium.
Dev. Biol
123
,
264
275
Török
T.
,
Tick
G.
,
Alvarado
M.
,
Kiss
I.
(
1993
)
P-lacW insertional mutagenesis on the second chromosome of Drosophila melanogaster: isolation of lethals with different overgrowth phenotypes.
Genetics
135
,
71
80
Van Doren
M.
,
Ellis
H. M.
,
Posakony
J. W.
(
1991
)
The Drosophila extramacrochaetae protein antagonizes sequence-specific DNA binding by daughterless/achaete-scute protein complexes.
Development
113
,
245
255
Williams
J. A.
,
Paddock
S. W.
,
Carroll
S. B.
(
1993
)
Pattern formation in a secondary field: a hierarchy of regulatory genes subdivides the developing Drosophila wing disc into discrete subregions.
Development
117
,
571
584
Xie
T.
,
Finelli
A.
,
Padgett
R.W.
(
1994
)
The Drosophila saxophone gene: a serine-threonine kinase receptor of the TGF-superfamily.
Science
263
,
1756
1759
Xu
T.
,
Rubin
G.M.
(
1993
)
Analysis of genetic mosaics in developing and adult Drosophila tissues.
Development
117
,
1223
1237
Zipursky
S. L.
,
Rubin
G. M.
(
1994
)
Determination of neuronal cell fate: lessons from the R7 neuron of Drosophila.
Annu. Rev. Neurosci
17
,
373
397
This content is only available via PDF.