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Science 17 May 1996:
Vol. 272. no. 5264, pp. 1020 - 1023
DOI: 10.1126/science.272.5264.1020
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Reports

Binding of APC to the Human Homolog of the Drosophila Discs Large Tumor Suppressor Protein

Akihiko Matsumine, Akiko Ogai, Takao Senda, Nobuaki Okumura, Kiyotoshi Satoh, Gyeong-Hun Baeg, Takeo Kawahara, Shigeru Kobayashi, Masato Okada, Kumao Toyoshima, Tetsu Akiyama *

The adenomatous polyposis coli gene (APC) is mutated in familial adenomatous polyposis and in sporadic colorectal tumors, and its product binds to the adherens junction protein beta -catenin. Overexpression of APC blocks cell cycle progression. The APC-beta -catenin complex was shown to bind to DLG, the human homolog of the Drosophila discs large tumor suppressor protein. This interaction required the carboxyl-terminal region of APC and the DLG homology repeat region of DLG. APC colocalized with DLG at the lateral cytoplasm in rat colon epithelial cells and at the synapse in cultured hippocampal neurons. These results suggest that the APC-DLG complex may participate in regulation of both cell cycle progression and neuronal function.

A. Matsumine, A. Ogai, K. Satoh, G.-H. Baeg, T. Akiyama, Department of Oncogene Research, Institute for Microbial Diseases, Osaka University, Suita, Osaka 565, Japan.
T. Senda, T. Kawahara, S. Kobayashi, Department of Anatomy I, Nagoya University School of Medicine, Nagoya, Aichi 466, Japan.
N. Okumura and M. Okada, Division of Protein Metabolism, Institute for Protein Research, Osaka University, Suita, Osaka 565, Japan.
K. Toyoshima, The Center for Adult Diseases, Osaka 537, Japan.
* To whom correspondence should be addressed.


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Y. Kawasaki, T. Senda, T. Ishidate, R. Koyama, T. Morishita, Y. Iwayama, O. Higuchi, and T. Akiyama (2000)
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K. Kawahara, T. Morishita, T. Nakamura, F. Hamada, K. Toyoshima, and T. Akiyama (2000)
J. Biol. Chem. 275, 8369-8374
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The {beta}-Catenin Binding Domain of Adenomatous Polyposis Coli Is Sufficient for Tumor Suppression.
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The Tight Junction Protein ZO-1 Establishes a Link between the Transmembrane Protein Occludin and the Actin Cytoskeleton.
A. S. Fanning, B. J. Jameson, L. A. Jesaitis, and J. M. Anderson (1998)
J. Biol. Chem. 273, 29745-29753
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Localization of Postsynaptic Density-93 to Dendritic Microtubules and Interaction with Microtubule-Associated Protein 1A.
J. E. Brenman, J. R. Topinka, E. C. Cooper, A. W. McGee, J. Rosen, T. Milroy, H. J. Ralston, and D. S. Bredt (1998)
J. Neurosci. 18, 8805-8813
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A Role for Cyclin-Dependent Kinase(s) in the Modulation of Fast Anterograde Axonal Transport: Effects Defined by Olomoucine and the APC Tumor Suppressor Protein.
N. Ratner, G. S. Bloom, and S. T. Brady (1998)
J. Neurosci. 18, 7717-7726
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Human CASK/LIN-2 Binds Syndecan-2 and Protein 4.1 and Localizes to the Basolateral Membrane of Epithelial Cells.
A. R. Cohen, D. F. Wood, S. M. Marfatia, Z. Walther, A. H. Chishti, and J. M. Anderson (1998)
J. Cell Biol. 142, 129-138
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Direct Interaction of CASK/LIN-2 and Syndecan Heparan Sulfate Proteoglycan and Their Overlapping Distribution in Neuronal Synapses.
Y.-P. Hsueh, F.-C. Yang, V. Kharazia, S. Naisbitt, A. R. Cohen, R. J. Weinberg, and M. Sheng (1998)
J. Cell Biol. 142, 139-151
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Plasma Membrane Ca2+ ATPase Isoform 4b Binds to Membrane-associated Guanylate Kinase (MAGUK) Proteins via Their PDZ (PSD-95/Dlg/ZO-1) Domains.
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J. Biol. Chem. 273, 1591-1595
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Tight junctions.
M. Balda and K Matter (1998)
J. Cell Sci. 111, 541-547
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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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MAGI-1, a Membrane-associated Guanylate Kinase with a Unique Arrangement of Protein-Protein Interaction Domains.
I. Dobrosotskaya, R. K. Guy, and G. L. James (1997)
J. Biol. Chem. 272, 31589-31597
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Mal3, the Fission Yeast Homologue of the Human APC-interacting Protein EB-1 Is Required for Microtubule Integrity and the Maintenance of Cell Form.
J. D. Beinhauer, I. M. Hagan, J. H. Hegemann, and U. Fleig (1997)
J. Cell Biol. 139, 717-728
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Human Homologue of the Drosophila Discs Large Tumor Suppressor Binds to p56lck Tyrosine Kinase and Shaker Type Kv1.3 Potassium Channel in T Lymphocytes.
T. Hanada, L. Lin, K. G. Chandy, S. S. Oh, and A. H. Chishti (1997)
J. Biol. Chem. 272, 26899-26904
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Binding of high-risk human papillomavirus E6 oncoproteins to the human homologue of the Drosophila discs large tumor suppressor protein.
T. Kiyono, A. Hiraiwa, M. Fujita, Y. Hayashi, T. Akiyama, and M. Ishibashi (1997)
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Inhibition of patterned cell shape change and cell invasion by Discs large during Drosophila oogenesis.
S. Goode and N. Perrimon (1997)
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Phosphorylation of the Tumor Suppressor Adenomatous Polyposis Coli (APC) by the Cyclin-dependent Kinase p34cdc2.
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J. Biol. Chem. 272, 21681-21684
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Characterization of the Interactions between PDZ Domains of the Protein-tyrosine Phosphatase PTPL1 and the Carboxyl-terminal Tail of Fas.
J. Saras, U. Engstrom, L. J. Gonez, and C.-H. Heldin (1997)
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Characterization of Guanylate Kinase-Associated Protein, a Postsynaptic Density Protein at Excitatory Synapses That Interacts Directly with Postsynaptic Density-95/Synapse-Associated Protein 90.
S. Naisbitt, E. Kim, R. J. Weinberg, A. Rao, F.-C. Yang, A. M. Craig, and M. Sheng (1997)
J. Neurosci. 17, 5687-5696
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Binding of human virus oncoproteins to hDlg/SAP97, a mammalian homolog of the Drosophila discs large tumor suppressor protein.
S. S. Lee, R. S. Weiss, and R. T. Javier (1997)
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Localized gene action controlling intestinal neoplasia in mice.
K. A. Gould and W. F. Dove (1997)
PNAS 94, 5848-5853
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The N-terminal Domain of Human GABA Receptor rho 1 Subunits Contains Signals for Homooligomeric and Heterooligomeric Interaction.
A. S. Hackam, T.-L. Wang, W. B. Guggino, and G. R. Cutting (1997)
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Nuclear and cytoplasmic localizations of the adenomatous polyposis coli protein.
K. L. Neufeld and R. L. White (1997)
PNAS 94, 3034-3039
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The Molecular Interaction of Fas and FAP-1. A TRIPEPTIDE BLOCKER OF HUMAN Fas INTERACTION WITH FAP-1 PROMOTES Fas-INDUCED APOPTOSIS.
J. Yanagisawa, M. Takahashi, H. Kanki, H. Yano-Yanagisawa, T. Tazunoki, E. Sawa, T. Nishitoba, M. Kamishohara, E. Kobayashi, S. Kataoka, et al. (1997)
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Activation of beta -Catenin-Tcf Signaling in Colon Cancer by Mutations in beta -Catenin or APC.
P. J. Morin, A. B. Sparks, V. Korinek, N. Barker, H. Clevers, B. Vogelstein, and K. W. Kinzler (1997)
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The PI 3-kinase/Akt signaling pathway delivers an anti-apoptotic signal..
S G Kennedy, A J Wagner, S D Conzen, J Jordan, A Bellacosa, P N Tsichlis, and N Hay (1997)
Genes & Dev. 11, 701-713
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GKAP, a Novel Synaptic Protein That Interacts with the Guanylate Kinase-like Domain of the PSD-95/SAP90 Family of Channel Clustering Molecules.
E. Kim, S. Naisbitt, Y.-P. Hsueh, A. Rao, A. Rothschild, A. M. Craig, and M. Sheng (1997)
J. Cell Biol. 136, 669-678
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Adenomatous Polyposis Coli Tumor Suppressor Protein Has Signaling Activity in Xenopus laevis Embryos Resulting in the Induction of an Ectopic Dorsoanterior Axis.
K. Vleminckx, E. Wong, K. Guger, B. Rubinfeld, P. Polakis, and B. M. Gumbiner (1997)
J. Cell Biol. 136, 411-420
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A Drosophila homolog of the tumor suppressor gene adenomatous polyposis coli down-regulates beta -catenin but its zygotic expression is not essential for the regulation of Armadillo.
S. Hayashi, B. Rubinfeld, B. Souza, P. Polakis, E. Wieschaus, and A. J. Levine (1997)
PNAS 94, 242-247
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Lano, a Novel LAP Protein Directly Connected to MAGUK Proteins in Epithelial Cells.
H. Saito, M.-J. Santoni, J.-P. Arsanto, F. Jaulin-Bastard, A. Le Bivic, S. Marchetto, S. Audebert, D. Isnardon, J. Adelaide, D. Birnbaum, et al. (2001)
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GAKIN, a Novel Kinesin-like Protein Associates with the Human Homologue of the Drosophila Discs Large Tumor Suppressor in T Lymphocytes.
T. Hanada, L. Lin, E. V. Tibaldi, E. L. Reinherz, and A. H. Chishti (2000)
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Complex Formation of Adenomatous Polyposis Coli Gene Product and Axin Facilitates Glycogen Synthase Kinase-3beta -dependent Phosphorylation of beta -Catenin and Down-regulates beta -Catenin.
T. Hinoi, H. Yamamoto, M. Kishida, S. Takada, S. Kishida, and A. Kikuchi (2000)
J. Biol. Chem. 275, 34399-34406
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PAPIN. A NOVEL MULTIPLE PSD-95/Dlg-A/ZO-1 PROTEIN INTERACTING WITH NEURAL PLAKOPHILIN-RELATED Armadillo REPEAT PROTEIN/delta -CATENIN AND p0071.
M. Deguchi, T. Iizuka, Y. Hata, W. Nishimura, K. Hirao, I. Yao, H. Kawabe, and Y. Takai (2000)
J. Biol. Chem. 275, 29875-29880
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The ERBB2/HER2 Receptor Differentially Interacts with ERBIN and PICK1 PSD-95/DLG/ZO-1 Domain Proteins.
F. Jaulin-Bastard, H. Saito, A. Le Bivic, V. Ollendorff, S. Marchetto, D. Birnbaum, and J.-P. Borg (2001)
J. Biol. Chem. 276, 15256-15263
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