Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.


Science 6 September 1996:
Vol. 273. no. 5280, pp. 1373 - 1377
DOI: 10.1126/science.273.5280.1373

Reports

Antagonistic Interactions Between Wingless and Decapentaplegic Responsible for Dorsal-Ventral Pattern in the Drosophila Leg

William J. Brook and Stephen M. Cohen *

Subdivision of the limb primordia of Drosophila into anterior and posterior compartments triggers cell interactions that pattern the legs and wings. A comparable compartment-based mechanism is used to pattern the dorsal-ventral axis of the wing. Evidence is presented here for a mechanism based on cell interaction, rather than on compartment formation, that distinguishes dorsal from ventral in the leg. Mutual repression by Wingless and Decapentaplegic signaling systems generates a stable regulatory circuit by which each gene maintains its own expression in a spatially restricted domain. Compartment-independent patterning mechanisms may be used by other organisms during development.

European Molecular Biology Laboratory, Meyerhofstr 1, 69117 Heidelberg, Germany.
*   To whom correspondence should be addressed. E-mail: scohen{at}embl-heidelberg.de



THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
The Tbx20 homologs midline and H15 specify ventral fate in the Drosophila melanogaster leg.
P. C. Svendsen, A. Formaz-Preston, S. M. Leal, and W. J. Brook (2009)
Development 136, 2689-2693
   Abstract »    Full Text »    PDF »
The microRNA miR-8 is a conserved negative regulator of Wnt signaling.
J. A. Kennell, I. Gerin, O. A. MacDougald, and K. M. Cadigan (2008)
PNAS 105, 15417-15422
   Abstract »    Full Text »    PDF »
Ero1L, a thiol oxidase, is required for Notch signaling through cysteine bridge formation of the Lin12-Notch repeats in Drosophila melanogaster.
A.-C. Tien, A. Rajan, K. L. Schulze, H. D. Ryoo, M. Acar, H. Steller, and H. J. Bellen (2008)
J. Cell Biol. 182, 1113-1125
   Abstract »    Full Text »    PDF »
Reciprocal roles for bowl and lines in specifying the peripodial epithelium and the disc proper of the Drosophila wing primordium.
D. Nusinow, L. Greenberg, and V. Hatini (2008)
Development 135, 3031-3041
   Abstract »    Full Text »    PDF »
Pygopus activates Wingless target gene transcription through the mediator complex subunits Med12 and Med13.
I. Carrera, F. Janody, N. Leeds, F. Duveau, and J. E. Treisman (2008)
PNAS 105, 6644-6649
   Abstract »    Full Text »    PDF »
Logic of Wg and Dpp induction of distal and medial fates in the Drosophila leg.
C. Estella and R. S. Mann (2008)
Development 135, 627-636
   Abstract »    Full Text »    PDF »
Recruitment of cells into the Drosophila wing primordium by a feed-forward circuit of vestigial autoregulation.
M. Zecca and G. Struhl (2007)
Development 134, 3001-3010
   Abstract »    Full Text »    PDF »
The O-fucosyltransferase O-fut1 is an extracellular component that is essential for the constitutive endocytic trafficking of Notch in Drosophila.
T. Sasamura, H. O. Ishikawa, N. Sasaki, S. Higashi, M. Kanai, S. Nakao, T. Ayukawa, T. Aigaki, K. Noda, E. Miyoshi, et al. (2007)
Development 134, 1347-1356
   Abstract »    Full Text »    PDF »
Sprinter: a novel transmembrane protein required for Wg secretion and signaling.
R. M. Goodman, S. Thombre, Z. Firtina, D. Gray, D. Betts, J. Roebuck, E. P. Spana, and E. M. Selva (2006)
Development 133, 4901-4911
   Abstract »    Full Text »    PDF »
An Unconventional Nuclear Localization Motif Is Crucial for Function of the Drosophila Wnt/Wingless Antagonist Naked Cuticle.
S. Waldrop, C.-C. Chan, T. Cagatay, S. Zhang, R. Rousset, J. Mack, W. Zeng, M. Fish, M. Zhang, M. Amanai, et al. (2006)
Genetics 174, 331-348
   Abstract »    Full Text »    PDF »
Senseless and Daughterless confer neuronal identity to epithelial cells in the Drosophila wing margin.
H. Jafar-Nejad, A.-C. Tien, M. Acar, and H. J. Bellen (2006)
Development 133, 1683-1692
   Abstract »    Full Text »    PDF »
Internalization is required for proper Wingless signaling in Drosophila melanogaster..
E. S. Seto and H. J. Bellen (2006)
J. Cell Biol. 173, 95-106
   Abstract »    Full Text »    PDF »
Signaling interactions between squamous and columnar epithelia of the Drosophila wing disc.
S. K. Pallavi and L. S. Shashidhara (2005)
J. Cell Sci. 118, 3363-3370
   Abstract »    Full Text »    PDF »
Coordinated development of muscles and tendons of the Drosophila leg.
C. Soler, M. Daczewska, J. P. Da Ponte, B. Dastugue, and K. Jagla (2004)
Development 131, 6041-6051
   Abstract »    Full Text »    PDF »
A Screen for Genes That Interact With the Drosophila Pair-Rule Segmentation Gene fushi tarazu.
M. W. Kankel, D. M. Duncan, and I. Duncan (2004)
Genetics 168, 161-180
   Abstract »    Full Text »    PDF »
Opposing inputs by Hedgehog and Brinker define a stripe of hairy expression in the Drosophila leg imaginal disc.
C. Kwon, R. Hays, J. Fetting, and T. V. Orenic (2004)
Development 131, 2681-2692
   Abstract »    Full Text »    PDF »
Patched controls the Hedgehog gradient by endocytosis in a dynamin-dependent manner, but this internalization does not play a major role in signal transduction.
C. Torroja, N. Gorfinkiel, and I. Guerrero (2004)
Development 131, 2395-2408
   Abstract »    Full Text »    PDF »
Genetic characterization of the Drosophila homologue of coronin.
V. Bharathi, S. K. Pallavi, R. Bajpai, B. S. Emerald, and L. S. Shashidhara (2004)
J. Cell Sci. 117, 1911-1922
   Abstract »    Full Text »    PDF »
Drosophila Twins regulates Armadillo levels in response to Wg/Wnt signal.
R. Bajpai, K. Makhijani, P. R. Rao, and L. S. Shashidhara (2004)
Development 131, 1007-1016
   Abstract »    Full Text »    PDF »
Hedgehog Signaling in the Drosophila Eye and Head: An Analysis of the Effects of Different patched Trans-heterozygotes.
C. Thomas and P. W. Ingham (2003)
Genetics 165, 1915-1928
   Abstract »    Full Text »    PDF »
neurotic, a novel maternal neurogenic gene, encodes an O-fucosyltransferase that is essential for Notch-Delta interactions.
T. Sasamura, N. Sasaki, F. Miyashita, S. Nakao, H. O. Ishikawa, M. Ito, M. Kitagawa, K. Harigaya, E. Spana, D. Bilder, et al. (2003)
Development 130, 4785-4795
   Abstract »    Full Text »    PDF »
Egfr/Ras pathway mediates interactions between peripodial and disc proper cells in Drosophila wing discs.
S. K. Pallavi and L. S. Shashidhara (2003)
Development 130, 4931-4941
   Abstract »    Full Text »    PDF »
Splits ends is a tissue/promoter specific regulator of Wingless signaling.
H. V. Lin, D. B. Doroquez, S. Cho, F. Chen, I. Rebay, and K. M. Cadigan (2003)
Development 130, 3125-3135
   Abstract »    Full Text »    PDF »
Regulation of Wingless and Vestigial expression in wing and haltere discs of Drosophila.
M. Prasad, R. Bajpai, and L. S. Shashidhara (2003)
Development 130, 1537-1547
   Abstract »    Full Text »    PDF »
The ubiquitin ligase Hyperplastic discs negatively regulates hedgehog and decapentaplegic expression by independent mechanisms.
J. D. Lee, K. Amanai, A. Shearn, and J. E. Treisman (2003)
Development 129, 5697-5706
   Abstract »    Full Text »    PDF »
Segmental relationship between somites and vertebral column in zebrafish.
E. M. Morin-Kensicki, E. Melancon, and J. S. Eisen (2003)
Development 129, 3851-3860
   Abstract »    Full Text »    PDF »
Repression of Teashirt marks the initiation of wing development.
J. Wu and S. M. Cohen (2003)
Development 129, 2411-2418
   Abstract »    Full Text »    PDF »
Subdivision of the Drosophila wing imaginal disc by EGFR-mediated signaling.
M. Zecca and G. Struhl (2003)
Development 129, 1357-1368
   Abstract »    Full Text »    PDF »
Development of the Drosophila genital disc requires interactions between its segmental primordia.
N. Gorfinkiel, L. Sanchez, and I. Guerrero (2003)
Development 130, 295-305
   Abstract »    Full Text »    PDF »
Different mechanisms initiate and maintain wingless expression in the Drosophila wing hinge.
D. d. A. Rodriguez, J. Terriente, M. I. Galindo, J. P. Couso, and F. J. Diaz-Benjumea (2002)
Development 129, 3995-4004
   Abstract »    Full Text »    PDF »
pygopus encodes a nuclear protein essential for Wingless/Wnt signaling.
T. Y. Belenkaya, C. Han, H. J. Standley, X. Lin, D. W. Houston, J. Heasman, and X. Lin (2002)
Development 129, 4089-4101
   Abstract »    Full Text »    PDF »
Expression of Wnt ligands and Frizzled receptors in colonic mucosa and in colon carcinoma.
R F Holcombe, J L Marsh, M L Waterman, F Lin, T Milovanovic, and T Truong (2002)
Mol. Pathol. 55, 220-226
   Abstract »    Full Text »    PDF »
The transcriptional repressor Brinker antagonizes Wingless signaling.
E. Saller, A. Kelley, and M. Bienz (2002)
Genes & Dev. 16, 1828-1838
   Abstract »    Full Text »    PDF »
Hox gene control of segment-specific bristle patterns in Drosophila.
M. Rozowski and M. Akam (2002)
Genes & Dev. 16, 1150-1162
   Abstract »    Full Text »    PDF »
Grunge, related to human Atrophin-like proteins, has multiple functions in Drosophila development.
A. Erkner, A. Roure, B. Charroux, M. Delaage, N. Holway, N. Core, C. Vola, C. Angelats, F. Pages, L. Fasano, et al. (2002)
Development 129, 1119-1129
   Abstract »    Full Text »    PDF »
The establishment of segmentation in the Drosophila leg.
C. Rauskolb (2001)
Development 128, 4511-4521
   Abstract »    Full Text »    PDF »
Regulation of Apterous activity in Drosophila wing development.
U. Weihe, M. Milan, and S. M. Cohen (2001)
Development 128, 4615-4622
   Abstract »    Full Text »    PDF »
Simultaneous Detection of RNA and Protein by In Situ Hybridization and Immunological Staining.
H. Nagaso, T. Murata, N. Day, and K. K. Yokoyama (2001)
J. Histochem. Cytochem. 49, 1177-1182
   Abstract »    Full Text »    PDF »
The EGF receptor and notch signaling pathways control the initiation of the morphogenetic furrow during Drosophila eye development.
J. P. Kumar and K. Moses (2001)
Development 128, 2689-2697
   Abstract »    Full Text »    PDF »
The Drosophila sex determination hierarchy modulates wingless and decapentaplegic signaling to deploy dachshund sex-specifically in the genital imaginal disc.
E. Keisman and B. Baker (2001)
Development 128, 1643-1656
   Abstract »    PDF »
Sex determination genes control the development of the Drosophila genital disc, modulating the response to Hedgehog, Wingless and Decapentaplegic signals.
L Sanchez, N Gorfinkiel, and I Guerrero (2001)
Development 128, 1033-1043
   Abstract »    PDF »
The Hox gene Abdominal-B antagonizes appendage development in the genital disc of Drosophila.
B Estrada and E Sanchez-Herrero (2001)
Development 128, 331-339
   Abstract »    PDF »
Osa-containing Brahma chromatin remodeling complexes are required for the repression of Wingless target genes.
R. T. Collins and J. E. Treisman (2000)
Genes & Dev. 14, 3140-3152
   Abstract »    Full Text »
Signaling Specificity by Frizzled Receptors in Drosophila.
M. Boutros, J. Mihaly, T. Bouwmeester, and M. Mlodzik (2000)
Science 288, 1825-1828
   Abstract »    Full Text »    PDF »
Tissue- and stage-specific modulation of Wingless signaling by the segment polarity gene lines.
V. Hatini, P. Bokor, R. Goto-Mandeville, and S. DiNardo (2000)
Genes & Dev. 14, 1364-1376
   Abstract »    Full Text »
The combgap locus encodes a zinc-finger protein that regulates cubitus interruptus during limb development in Drosophila melanogaster.
P. Svendsen, S. Marshall, M Kyba, and W. Brook (2000)
Development 127, 4083-4093
   Abstract »    PDF »
Correlation of diversity of leg morphology in Gryllus bimaculatus (cricket) with divergence in dpp expression pattern during leg development.
N Niwa, Y Inoue, A Nozawa, M Saito, Y Misumi, H Ohuchi, H Yoshioka, and S Noji (2000)
Development 127, 4373-4381
   Abstract »    PDF »
Wingless and its signalling pathway have common and separable functions during tracheal development.
M Llimargas (2000)
Development 127, 4407-4417
   Abstract »    PDF »
Control of tracheal tubulogenesis by Wingless signaling.
T Chihara and S Hayashi (2000)
Development 127, 4433-4442
   Abstract »    PDF »
Temporal regulation of apterous activity during development of the Drosophila wing.
M Milan and S. Cohen (2000)
Development 127, 3069-3078
   Abstract »    PDF »
Morphogenetic furrow initiation and progression during eye development in Drosophila: the roles of decapentaplegic, hedgehog and eyes absent.
J Curtiss and M Mlodzik (2000)
Development 127, 1325-1336
   Abstract »    PDF »
Negative Regulation of Wingless Signaling by D-Axin, a Drosophila Homolog of Axin.
F. Hamada, Y. Tomoyasu, Y. Takatsu, M. Nakamura, S. Nagai, A. Suzuki, F. Fujita, H. Shibuya, K. Toyoshima, N. Ueno, et al. (1999)
Science 283, 1739-1742
   Abstract »    Full Text »
Proximal to distal cell communication in the Drosophila leg provides a basis for an intercalary mechanism of limb patterning.
S Goto and S Hayashi (1999)
Development 126, 3407-3413
   Abstract »    PDF »
Wingless, decapentaplegic and EGF receptor signaling pathways interact to specify dorso-ventral pattern in the adult abdomen of Drosophila.
A Kopp, R. Blackman, and I Duncan (1999)
Development 126, 3495-3507
   Abstract »    PDF »
Patterning of Drosophila leg sensory organs through combinatorial signaling by hedgehog, decapentaplegic and wingless.
R Hays, K. Buchanan, C Neff, and T. Orenic (1999)
Development 126, 2891-2899
   Abstract »    PDF »
hedgehog and engrailed: pattern formation and polarity in the Drosophila abdomen.
P. Lawrence, J Casal, and G Struhl (1999)
Development 126, 2431-2439
   Abstract »    PDF »
Wnt-7a in feather morphogenesis: involvement of anterior-posterior asymmetry and proximal-distal elongation demonstrated with an in vitro reconstitution model.
R. Widelitz, T. Jiang, C. Chen, N. Stott, and C. Chuong (1999)
Development 126, 2577-2587
   Abstract »    PDF »
Hedgehog is required for activation of engrailed during regeneration of fragmented Drosophila imaginal discs.
M. Gibson and G Schubiger (1999)
Development 126, 1591-1599
   Abstract »    PDF »
Signaling by the TGF-beta homolog decapentaplegic functions reiteratively within the network of genes controlling retinal cell fate determination in Drosophila.
R Chen, G Halder, Z Zhang, and G Mardon (1999)
Development 126, 935-943
   Abstract »    PDF »
Proximodistal axis formation in the Drosophila leg: subdivision into proximal and distal domains by Homothorax and Distal-less.
J Wu and S. Cohen (1999)
Development 126, 109-117
   Abstract »    PDF »
Beadex encodes an LMO protein that regulates Apterous LIM-homeodomain activity in Drosophila wing development: a model for LMO oncogene function.
M. Milán, F. J. Diaz-Benjumea, and S. M. Cohen (1998)
Genes & Dev. 12, 2912-2920
   Abstract »    Full Text »
A novel homeobox gene mediates the Dpp signal to establish functional specificity within target cells.
H. Nakagoshi, M. Hoshi, Y.-i. Nabeshima, and F. Matsuzaki (1998)
Genes & Dev. 12, 2724-2734
   Abstract »    Full Text »
Boundary Formation in Drosophila Wing: Notch Activity Attenuated by the POU Protein Nubbin.
C. J. Neumann and S. M. Cohen (1998)
Science 281, 409-413
   Abstract »    Full Text »
Notch signalling mediates segmentation of the Drosophila leg.
J. de Celis, D. Tyler, J de Celis, and S. Bray (1998)
Development 125, 4617-4626
   Abstract »    PDF »
Role of dpp signalling in prepattern formation of the dorsocentral mechanosensory organ in Drosophila melanogaster.
Y Tomoyasu, M Nakamura, and N Ueno (1998)
Development 125, 4215-4224
   Abstract »    PDF »
Generation of multiple antagonistic domains along the proximodistal axis during Drosophila leg development.
M Abu-Shaar and R. Mann (1998)
Development 125, 3821-3830
   Abstract »    PDF »
slimb coordinates wg and dpp expression in the dorsal-ventral and anterior-posterior axes during limb development.
N. Theodosiou, S Zhang, W. Wang, and T Xu (1998)
Development 125, 3411-3416
   Abstract »    PDF »
decapentaplegic and wingless are regulated by eyes absent and eyegone and interact to direct the pattern of retinal differentiation in the eye disc.
D. Hazelett, M Bourouis, U Walldorf, and J. Treisman (1998)
Development 125, 3741-3751
   Abstract »    PDF »
A molecular basis for transdetermination in Drosophila imaginal discs: interactions between wingless and decapentaplegic signaling.
L Maves and G Schubiger (1998)
Development 125, 115-124
   Abstract »    PDF »
Establishing primordia in the Drosophila eye-antennal imaginal disc: the roles of decapentaplegic, wingless and hedgehog.
J Royet and R Finkelstein (1997)
Development 124, 4793-4800
   Abstract »    PDF »
Spitz and Wingless, emanating from distinct borders, cooperate to establish cell fate across the Engrailed domain in the Drosophila epidermis.
L O'Keefe, S. Dougan, L Gabay, E Raz, B. Shilo, and S DiNardo (1997)
Development 124, 4837-4845
   Abstract »    PDF »
Different levels of Ras activity can specify distinct transcriptional and morphological consequences in early Drosophila embryos.
S Greenwood and G Struhl (1997)
Development 124, 4879-4886
   Abstract »    PDF »
The roles of hedgehog and engrailed in patterning adult abdominal segments of Drosophila.
A Kopp, M. Muskavitch, and I Duncan (1997)
Development 124, 3703-3714
   Abstract »    PDF »
Control of cell fate and polarity in the adult abdominal segments of Drosophila by optomotor-blind.
A Kopp and I Duncan (1997)
Development 124, 3715-3726
   Abstract »    PDF »
Cell cycle progression, growth and patterning in imaginal discs despite inhibition of cell division after inactivation of Drosophila Cdc2 kinase.
K Weigmann, S. Cohen, and C. Lehner (1997)
Development 124, 3555-3563
   Abstract »    PDF »
Hedgehog organises the pattern and polarity of epidermal cells in the Drosophila abdomen.
G Struhl, D. Barbash, and P. Lawrence (1997)
Development 124, 2143-2154
   Abstract »    PDF »
Hedgehog acts by distinct gradient and signal relay mechanisms to organise cell type and cell polarity in the Drosophila abdomen.
G Struhl, D. Barbash, and P. Lawrence (1997)
Development 124, 2155-2165
   Abstract »    PDF »
Expression and function of clift in the development of somatic gonadal precursors within the Drosophila mesoderm.
M Boyle, N Bonini, and S DiNardo (1997)
Development 124, 971-982
   Abstract »    PDF »
Shaggy and dishevelled exert opposite effects on Wingless and Decapentaplegic expression and on positional identity in imaginal discs.
T. Heslip, H Theisen, H Walker, and J. Marsh (1997)
Development 124, 1069-1078
   Abstract »    PDF »
Long-range action of Wingless organizes the dorsal-ventral axis of the Drosophila wing.
C. Neumann and S. Cohen (1997)
Development 124, 871-880
   Abstract »    PDF »
Role of decapentaplegic in initiation and progression of the morphogenetic furrow in the developing Drosophila retina.
F Chanut and U Heberlein (1997)
Development 124, 559-567
   Abstract »    PDF »
Developmental Control of Cell Cycle Regulators: A Fly's Perspective.
B. A. Edgar and C. F. Lehner (1996)
Science 274, 1646-1652
   Abstract »    Full Text »
A hierarchy of cross-regulation involving Notch, wingless, vestigial and cut organizes the dorsal/ventral axis of the Drosophila wing.
C. Neumann and S. Cohen (1996)
Development 122, 3477-3485
   Abstract »    PDF »
Notch signaling directly controls cell proliferation in the Drosophila wing disc.
A. Baonza and A. Garcia-Bellido (2000)
PNAS 97, 2609-2614
   Abstract »    Full Text »    PDF »



To Advertise     Find Products


Science. ISSN 0036-8075 (print), 1095-9203 (online)