Modulation of the oncogenic potential of β-catenin by the subcellular distribution of plakoglobin

Molecular Carcinogenesis

Volumn 46, Issue 10, 2007, Pages 824-838

  Li, Laiji ^a   Chapman, Kimberly ^a   Hu, Xiuying ^a   Wong, Annissa ^a   Pasdar, Manijeh ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Apoptosis; Carcinogenesis; Cell adhesion; Tumor biology

Indexed keywords

ALPHA CATENIN; BETA CATENIN; CADHERIN; LAMIN; NERVE CELL ADHESION MOLECULE; PLAKOGLOBIN; PROTEIN BCL 2; TUBULIN;

ARTICLE; CARCINOGENICITY; CELL ADHESION; CELLULAR DISTRIBUTION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN INTERACTION; PROTEIN LOCALIZATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TONGUE CARCINOMA; TUMOR SUPPRESSOR GENE;

APOPTOSIS; BETA CATENIN; CELL ADHESION; CELL LINE; CELL LINE, TUMOR; CELL NUCLEUS; GAMMA CATENIN; HUMANS; PROTO-ONCOGENE PROTEINS C-BCL-2; SIGNAL TRANSDUCTION; TCF TRANSCRIPTION FACTORS; TRANS-ACTIVATION (GENETICS); TRANSFECTION;

EID: 35048897998     PISSN: 08991987     EISSN: 10982744     Source Type: Journal    
DOI: 10.1002/mc.20310     Document Type: Article

References (63)

1. Peifer M, McCrea PD, Green KJ, Wieschaus E, Gumbiner BM. The vertebrate adhesive junction proteins β-catenin and plakoglobin and the Drosophila segment polarity gene armadillo form a multigene family with similar properties. J Cell Biol 1992;118:681-691.
2. Gelderloos JA, Witcher L, Cowin P, Klymkowsky MW. Cytoskeletal-membrane interactions and signal transduction. Austin, Texas, USA: Landes Bioscience; 1997; pp 13-29.
3. Zhurinsky J, Shtutman M, Ben-Ze'ev A. Plakoglobin and β-catenin: Protein interactions, regulation and biological roles. J Cell Sci 2000;113:3127-3139.
4. Wheelock MJ, Johnson KR. Cadherins as modulators of cellular phenotype. Annu Rev Cell Dev Biol 2003;19:207-235.
5. Yin T, Green KJ. Regulation of desmosome assembly and adhesion. Semin Cell Dev Biol 2004;15:665-677.
6. Hinck L, Nathke IS, Papkoff J, Nelson WJ. Dynamics of cadherin/catenin complex formation: Novel protein interactions and pathways of complex assembly. J Cell Biol 1994;125:1327-1340.
7. Lewis J, Wahl JK III, Sass KM, Jensen PJ, Johnson KR, Wheelock MJ. Cross talk between adherens junctions and desmosomes depends on plakoglobin. J Cell Biol 1997;136:919-934.
8. Parker HR, Li Z, Sheinin H, Lauzon G, Pasdar M. Plakoglobin induces desmosome formation and epidermoid phenotype in N-cadherin-expressing squamous carcinoma cells deficient in plakoglobin and E-cadherin. Cell Motil Cytoskeleton 1998;40:87-100.
9. Yin T, Getsios S, Caldelari R, et al. Mechanisms of plakoglobin-dependent adhesion: Desmosome-specific functions in assembly and regulation by epidermal growth factor receptor. J Biol Chem 2005;280:40355-40363.
10. Nelson WJ, Nusse R. Convergence of Wnt, β-catenin, and Cadherin pathways. Science 2004;303:1483-1487.
11. Brembeck FH, Rosario M, Birchmeier W. Balancing cell adhesion and Wnt signaling, the key role of beta-catenin. Curr Opin Genet Dev 2006;16:51-59.
12. Bradley RS, Cowin P, Brown AM. Expression of Wnt-1 in PC12 cells results in modulation of plakoglobin and E-cadherin and increased cellular adhesion. J Cell Biol 1993;123:1857-1865.
13. Solanas G, Miravet S, Casagolda D, et al. β-Catenin and plakoglobin N- and C-tails determine ligand specificity. J Biol Chem 2004;279:49849-49856.
14. Zhurinsky J, Shtutman M, Ben-Ze'ev A. Differential mechanisms of LEF/TCF family-dependent transcriptional activation by β-catenin and plakoglobin. Mol Cell Biol 2000b;20:4238-4252.
15. Miravet S, Piedra J, Miro F, Harte E, Garcia de Herreros AG, Dunach M. The transcriptional factor Tcf-4 contains different binding sites for β-catenin and plakoglobin. J Biol Chem 2002;277:1884-1891.
16. Rieger-Christ KM, Ng L, Hanley RS, et al. Restoration of plakoglobin expression in bladder carcinoma cell lines suppresses cell migration and tumorigenic potential. Br J Cancer 2005;92:2153-2159.
17. Winn RA, Bremnes RM, Bemis L, et al. γ-Catenin expression is reduced or absent in a subset of human lung cancers and reexpression inhibits transformed cell growth. Oncogene 2002;21:7497-7506.
18. Pantel K, Passlick B, Vogt J, et al. Reduced expression of plakoglobin indicates an unfavorable prognosis in subsets of patients with non-small-cell lung cancer. J Clin Oncol 1998;16:1407-1413.
19. Simcha I, Geiger B, Yehuda-Levenberg S, Salomon D, BenZe'ev A. Suppression of tumorigenicity by plakoglobin: An augmenting effect of N-cadherin. J Cell Biol 1996;133:199-209.
20. Hakimelahi S, Parker HR, Gilchrist AJ, et al. Plakoglobin regulates the expression of the anti-apoptotic protein Bcl-2. J Biol Chem 2000;275:10905- 10911.
21. Salomon D, Sacco PA, Roy SG, etal. Regulation of β-catenin levels and localization by overexpression of plakoglobin and inhibition of the ubiquitin-proteosome system. J Cell Biol 1997;139:1325-1335.
22. Raurell I, Castano J, Franci C, Garcia de Herreros A, Dunach M. Presenilin-1 interacts with plakoglobin and enhances plakoglobin-Tcf-4 association. Implications for the regulation of beta-catenin/Tcf-4-dependent transcription. J Biol Chem 2006;281:1401-1411.
23. El-Bahrawy M, Poulsom R, Rowan AJ, Tomlinson IT, Alison MR. Characterization of the E-cadherin/catenin complex in colorectal carcinoma cell lines. Int J Exp Pathol 2004;85:65-74.
24. Pasdar M, Nelson WJ. Regulation of desmosome assembly in epithelial cells: Kinetics of synthesis, transport, and stabilization of desmoglein I, a major protein of the membrane core domain. J Cell Biol 1989;109:163-177.
25. Pasdar M, Li Z, Chlumecky V. Plakoglobin: Kinetics of synthesis, phosphorylation, stability, and interactions with desmoglein and E-cadherin. Cell Motil Cytoskeleton 1995;32:258-272.
26. Wen W, Meinkoth JL, Tsien RY, Taylor SS. Identification of a signal for rapid export of proteins from the nucleus. Cell 1995;82:463-473.
27. Kalderon D, Roberts BL, Richardson WD, Smith AE. A short amino acid sequence able to specify nuclear location. Cell 1984;39:499-509.
28. Kozak M. Selection of initiation sites by eukaryotic ribosomes: Effect of inserting AUG triplets upstream from the coding sequence for preproinsulin. Nucleic Acids Res 1984;12:857-872.
29. Miller JR, Moon RT. Analysis of the signaling activities of localization mutants of β-catenin during axis specification in Xenopus. J Cell Biol 1997;139:229-243.
30. Cox RT, Pai LM, Miller JR, et al. Membrane-tethered Drosophila Armadillo cannot transduce Wingless signal on its own. Development 1999;126:1327-1335.
31. Klymkowsky MW, Williams BO, Barish GD, Varmus HE, Vourgourakis YE. Membrane-anchored plakoglobins have multiple mechanisms of action in Wnt signaling. Mol Biol Cell 1999;10:3151-3169.
32. Li Z, Gallin WJ, Lauzon GJ, Pasdar M. L-CAM expression induces fibroblast-epidermoid transition in squamous carcinoma cells and down-regulates the endogenous N-cadherin. J Cell Sci 1998;111:1005-1019.
33. Kolligs FT, Kolligs B, Hajra KM, et al. γ-Catenin is regulated by the APC tumor suppressor and its oncogenic activity is distinct from that of β-catenin. Genes Dev 2000;14:1319-1331.
34. Korinek V, Barker N, Morin PJ, et al. Constitutive transcriptional activation by a β-catenin-TCF complex in APC-/-colon carcinoma. Science 1997;275:1784-1787.
35. Smirnova IV, Bittel DC, Ravindra R, Jiang H, Andrews GK. Zinc and cadmium can promote rapid nuclear translocation of metal response element-binding transcription factor-1. J Biol Chem 2000;275:9377-9384.
36. Han AC, Soler AP, Tang CK, Knudsen KA, Salazar H. Nuclear localization of E-cadherin expression in Merkel cell carcinoma. Arch Pathol Lab Med 2000;124:1147-1151.
37. Clavel CE, Nollet F, Berx G, et al. Expression of the E-cadherin-catenin complex in lung neuroendocrine tumours. J Pathol 2001;194:20-26.
38. Giannini A, Mazor M, Orme M, Vivanco M, Waxman J, Kypta R. Nuclear export of alpha-catenin: Overlap between nuclear export signal sequences and the β-catenin binding site. Exp Cell Res 2004;295:150-160.
39. Albuquerque ML, Flozak AS. Wound closure in sheared endothelial cells is enhanced by modulation of vascular endothelial-cadherin expression and localization. Exp Biol Med Maywood 2002;227:1006-1016.
40. Orsulic S, Huber O, Aberle H, Arnold S, Kemler R. E-cadherin binding prevents β-catenin nuclear localization and β-catenin/LEF-1-mediated transactivation. J Cell Sci 1999;112:1237-1245.
41. Gottardi CJ, Wong E, Gumbiner BM. E-Cadherin suppresses cellular transformation by inhibiting β-catenin signaling in an adhesion-independent manner. J Cell Biol 2001;153:1049-1059.
42. Giannini AL, Vivanco M, Kypta RM. α-Catenin inhibits β-catenin signaling by preventing formation of a β-catenin-T-cell factor-DNA complex. J Biol Chem 2000;275:21883-21888.
43. Gottardi CJ, Gumbiner BM. Distinct molecular forms of β-catenin are targeted to adhesive or transcriptional complexes. J Cell Biol 2004;167:339-349.
44. Ilyas M, Tomlinson IP, Rowan A, Pignatelli M, Bodmer WF. β-Catenin mutations in cell lines established from human colorectal cancers. PNAS, USA 1997;94:10330-10334.
45. Giannini AL, Vivanco M, Kypta RM. Analysis of β-catenin aggregation and localization using GFP fusion proteins: Nuclear import of α-catenin by the β-catenin/Tcf complex. Exp Cell Res 2000a;255:207-220.
46. Knudsen KA, Wheelock MJ. Plakoglobin, or an 83-kD homologue distinct from β-catenin, interacts with E-cadherin and N-cadherin. J Cell Biol 1992;118:671-679.
47. Sacco PA, McGranahan TM, Wheelock MJ, Johnson KR. Identification of plakoglobin domains required for association with N-cadherin and alpha-catenin. J Biol Chem 1995;20:201-206.
48. Chitaev N, Leube R, Troyanovsky R, Eshkind L, Franke W, Troyanovsky S. The binding of plakoglobin to desmosomal Cadherins: Patterns of binding sites and topogenic potential. J Cell Biol 1996;133:359-369.
49. Yamada T, Takaoka AS, Naishiro Y, et al. Transactivation of the multidrug resistance 1 gene by T-cell factor 4/β-catenin complex in early colorectal carcinogenesis. Cancer Res 2000;60:4761-4766.
50. Dash PR, Whitley GS, Ayling LJ, Johnstone AP, Cartwright JE. Trophoblast apoptosis is inhibited by hepatocyte growth factor through the Akt and β-catenin mediated up-regulation of inducible nitric oxide synthase. Cell Signal 2005;17:571-580.
51. Sinha D, Wang Z, Ruchalski KL, et al. Lithium activates the Wnt and phosphatidylinositol 3-kinase Akt signaling pathways to promote cell survival in the absence of soluble survival factors. Am J Physiol Renal Physiol 2005;288:F703-F713.
52. Ma H, Nguyen C, Lee KS, Kahn M. Differential roles for the coactivators CBP and p300 on TCF/β-catenin-mediated survivin gene expression. Oncogene 2005;24:3619-3631.
53. Kaga S, Zhan L, Altaf E, Maulik N. Glycogen synthase kinase-3beta/beta- catenin promotes angiogenic and anti-apoptotic signaling through the induction of VEGF, Bcl-2 and survivin expression in rat ischemic preconditioned myocardium. J Mol Cell Cardiol 2006;40:138-147.
54. Kim TH, Xiong H, Zhang Z, Ren B. β-Catenin activates the growth factor endothelin-1 in colon cancer cells. Oncogene 2005;24:597-604.
55. Maeda O, Usami N, Kondo M, et al. Plakoglobin (γ-catenin) has TCF/LEF family-dependent transcriptional activity in β-catenin-deficient cell line. Oncogene 2004;23:964-972.
56. Takemaru KI, Moon RT. The transcriptional coactivator CBP interacts with β-catenin to activate gene expression. J Cell Biol 2000;149:249-254.
57. Bauer A, Chauvet S, Huber O, et al. Pontin52 and reptin52 function as antagonistic regulators of β-catenin signalling activity. EMBO J 2000;19:6121-6130.
58. Billin AN, Thirlwell H, Ayer DE. β-Catenin-histone deacetylase interactions regulate the transition of LEF1 from a transcriptional repressor to an activator. Mol Cell Biol 2000;20:6882-6890.
59. Barker N, Hurlstone A, Musisi H, Miles A, Bienz M, Clevers H. The chromatin remodeling factor Brg-1 interacts with β-catenin to promote target gene activation. EMBO J 2001;20:4935-4943.
60. Shtutman M, Zhurinsky J, Oren M, Levina E, Ben-Ze'ev A. PML is a target gene of β-catenin and plakoglobin, and coactivates β-catenin-mediated transcription. Cancer Res 2002;62:5947-5954.
61. Koh SS, Li H, Lee YH, Widelitz RB, Chuong CM, Stallcup MR. Synergistic coactivator function by coactivator-associated arginine methyltransferase (CARM) 1 and β-catenin with two different classes of DNA-binding transcriptional activators. J Biol Chem 2002;277:26031-26035.
62. Hu MC, Rosenblum ND. Smad1, β-catenin and Tcf4 associate in a molecular complex with the Myc promoter in dysplastic renal tissue and cooperate to control Myc transcription. Development 2005;132:215-225.
63. Canes D, Chiang GJ, Billmeyer BR, et al. Histone deacetylase inhibitors upregulate plakoglobin expression in bladder carcinoma cells and display antineoplastic activity in vitro and in vivo. Int J Cancer 2005;113:841-848.