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Science 29 March 1996:
Vol. 271. no. 5257, pp. 1826 - 1832
DOI: 10.1126/science.271.5257.1826
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Research Articles

Interaction Between Wingless and Notch Signaling Pathways Mediated by Dishevelled

Jeffrey D. Axelrod, Kenji Matsuno, Spyros Artavanis-Tsakonas, Norbert Perrimon *

In Drosophila, the Wingless and Notch signaling pathways function in many of the same developmental patterning events. Genetic analysis demonstrates that the dishevelled gene, which encodes a molecule previously implicated in implementation of the Wingless signal, interacts antagonistically with Notch and one of its known ligands, Delta. A direct physical interaction between Dishevelled and the Notch carboxyl terminus, distal to the cdc10/ankyrin repeats, suggests a mechanism for this interaction. It is proposed that Dishevelled, in addition to transducing the Wingless signal, blocks Notch signaling directly, thus providing a molecular mechanism for the inhibitory cross talk observed between these pathways.

J. D. Axelrod is in the Department of Genetics, Harvard Medical School, 200 Longwood Avenue, Boston, MA 02115, USA, and in the Department of Pathology, Brigham and Women's Hospital, Boston, MA 02115, USA. K. Matsuno and S. Artavanis-Tsakonas are at the Howard Hughes Medical Institute and in the Departments of Cell Biology and Biology, Boyer Center for Molecular Medicine, Yale University School of Medicine, New Haven, CT 06536, USA. N. Perrimon is at the Howard Hughes Medical Institute and in the Department of Genetics, Harvard Medical School, 200 Longwood Avenue, Boston, MA 02115, USA.
* To whom correspondence should be addressed.


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J. Neurosci. 19, 4229-4237
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Genetics 152, 567-576
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Domains of Axin Involved in Protein-Protein Interactions, Wnt Pathway Inhibition, and Intracellular Localization.
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J. Cell Biol. 145, 741-756
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Notch Signaling: Cell Fate Control and Signal Integration in Development.
S. Artavanis-Tsakonas, M. D. Rand, and R. J. Lake (1999)
Science 284, 770-776
   Abstract »    Full Text »
Direct Interaction of Alzheimer's Disease-related Presenilin 1 with Armadillo Protein p0071.
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J. Biol. Chem. 274, 9141-9148
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Composite signalling from Serrate and Delta establishes leg segments in Drosophila through Notch.
S. Bishop, T Klein, A. Arias, and J. Couso (1999)
Development 126, 2993-3003
   Abstract »    PDF »
A developmental pathway controlling outgrowth of the Xenopus tail bud.
C. Beck and J. Slack (1999)
Development 126, 1611-1620
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Genetic Characterization of the Drosophila melanogaster Suppressor of deltex Gene: A Regulator of Notch Signaling.
M. Fostier, D. A. P. Evans, S. Artavanis-Tsakonas, and M. Baron (1998)
Genetics 150, 1477-1485
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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
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Differential recruitment of Dishevelled provides signaling specificity in the planar cell polarity and Wingless signaling pathways.
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Genes & Dev. 12, 2610-2622
   Abstract »    Full Text »
LIN-12/Notch signaling: lessons from worms and flies.
I. Greenwald (1998)
Genes & Dev. 12, 1751-1762
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The beta-catenin homolog BAR-1 and LET-60 Ras coordinately regulate the Hox gene lin-39 during Caenorhabditis elegans vulval development.
D. Eisenmann, J. Maloof, J. Simske, C Kenyon, and S. Kim (1998)
Development 125, 3667-3680
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Systematic gain-of-function genetics in Drosophila.
P Rorth, K Szabo, A Bailey, T Laverty, J Rehm, G. Rubin, K Weigmann, M Milan, V Benes, W Ansorge, et al. (1998)
Development 125, 1049-1057
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Wnt signaling: a common theme in animal development.
K. M. Cadigan and R. Nusse (1997)
Genes & Dev. 11, 3286-3305
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Notch-1 Controls the Expression of Fatty Acid-activated Transcription Factors and Is Required for Adipogenesis.
C. Garces, M. J. Ruiz-Hidalgo, J. F. de Mora, C. Park, L. Miele, J. Goldstein, E. Bonvini, A. Porras, and J. Laborda (1997)
J. Biol. Chem. 272, 29729-29734
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Genetics of Aging.
C. E. Finch and R. E. Tanzi (1997)
Science 278, 407-411
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eyelid antagonizes wingless signaling during Drosophila development and has homology to the Bright family of DNA-binding proteins.
J. E. Treisman, A. Luk, G. M. Rubin, and U. Heberlein (1997)
Genes & Dev. 11, 1949-1962
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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
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Linking Frizzled and Wnt signaling in Drosophila development.
A Tomlinson, W. Strapps, and J Heemskerk (1997)
Development 124, 4515-4521
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Transcriptional regulation of Notch and Delta: requirement for neuroblast segregation in Drosophila.
L Seugnet, P Simpson, and M Haenlin (1997)
Development 124, 2015-2025
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The function and regulation of cut expression on the wing margin of Drosophila: Notch, Wingless and a dominant negative role for Delta and Serrate.
C. Micchelli, E. Rulifson, and S. Blair (1997)
Development 124, 1485-1495
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Long-range action of Wingless organizes the dorsal-ventral axis of the Drosophila wing.
C. Neumann and S. Cohen (1997)
Development 124, 871-880
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An Antisense Oligonucleotide to the Notch Ligand Jagged Enhances Fibroblast Growth Factor-induced Angiogenesis in Vitro.
A. B. Zimrin, M. S. Pepper, G. A. McMahon, F. Nguyen, R. Montesano, and T. Maciag (1996)
J. Biol. Chem. 271, 32499-32502
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Signal transduction through beta-catenin and specification of cell fate during embryogenesis..
J R Miller and R T Moon (1996)
Genes & Dev. 10, 2527-2539
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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
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wingless signaling in the Drosophila eye and embryonic epidermis.
K. Cadigan and R Nusse (1996)
Development 122, 2801-2812
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Subcellular localization of Suppressor of Hairless in Drosophila sense organ cells during Notch signalling.
M Gho, M Lecourtois, G Geraud, J. Posakony, and F Schweisguth (1996)
Development 122, 1673-1682
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Suppression of Erythroid but Not Megakaryocytic Differentiation of Human K562 Erythroleukemic Cells by Notch-1.
L. T. Lam, C. Ronchini, J. Norton, A. J. Capobianco, and E. H. Bresnick (2000)
J. Biol. Chem. 275, 19676-19684
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Phosphorylation of Ser2078 Modulates the Notch2 Function in 32D Cell Differentiation.
J. Ingles-Esteve, L. Espinosa, L. A. Milner, C. Caelles, and A. Bigas (2001)
J. Biol. Chem. 276, 44873-44880
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Loss of presenilin 1 is associated with enhanced beta -catenin signaling and skin tumorigenesis.
X. Xia, S. Qian, S. Soriano, Y. Wu, A. M. Fletcher, X.-J. Wang, E. H. Koo, X. Wu, and H. Zheng (2001)
PNAS 98, 10863-10868
   Abstract »    Full Text »    PDF »


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