P120-catenin in cancer - mechanisms, models and opportunities for intervention

Journal of Cell Science

Volumn 126, Issue 16, 2013, Pages 3515-3525

  Schackmann, Ron C J ^a   Tenhagen, Milou ^a   van de Ven, Robert A H ^a   Derksen, Patrick W B ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Cancer; Kaiso; Metastasis; Mouse models; Oncogene; P120; Tumor suppressor

Indexed keywords

COLONY STIMULATING FACTOR 1; GAMMA SECRETASE; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; GROWTH FACTOR RECEPTOR; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MONOCYTE CHEMOTACTIC PROTEIN 1; PROTEIN P120; RAC1 PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; UVOMORULIN;

ALTERNATIVE RNA SPLICING; APOPTOSIS; ARTICLE; BLADDER CANCER; BREAST CANCER; CANCER GROWTH; CARBOXY TERMINAL SEQUENCE; CELL JUNCTION; CELL MATURATION; CELL MEMBRANE; CELL MIGRATION; CELL POLARITY; COLON CANCER; DIFFERENTIAL DIAGNOSIS; DNA BINDING; DOWN REGULATION; ENDOCYTOSIS; EXON; GENE EXPRESSION; GENE REPRESSION; HUMAN; LUNG CANCER; LUNG NON SMALL CELL CANCER; LYMPH NODE METASTASIS; MICROTUBULE; NEOPLASM; NONHUMAN; NONSENSE MUTATION; NUCLEAR EXPORT SIGNAL; NUCLEAR LOCALIZATION SIGNAL; PANCREAS CANCER; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SQUAMOUS CELL CARCINOMA; START CODON; STOMACH CANCER; TUMOR GROWTH;

CANCER; KAISO; METASTASIS; MOUSE MODELS; ONCOGENE; P120; TUMOR SUPPRESSOR;

ANIMALS; CARCINOMA; CATENINS; HUMANS; ONCOGENES;

EID: 84883313434     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.134411     Document Type: Article

References (142)

1. Aho, S., Levänsuo, L., Montonen, O., Kari, C., Rodeck, U. and Uitto, J. (2002). Specific sequences in p120ctn determine subcellular distribution of its multiple isoforms involved in cellular adhesion of normal and malignant epithelial cells. J. Cell Sci. 115, 1391-1402.
2. Alemà, S. and Salvatore, A. M. (2007). p120 catenin and phosphorylation: Mechanisms and traits of an unresolved issue. Biochim. Biophys. Acta 1773, 47-58.
3. Anastasiadis, P. Z. (2007). p120-ctn: A nexus for contextual signaling via Rho GTPases. Biochim. Biophys. Acta 1773, 34-46.
4. Anastasiadis, P. Z. and Reynolds, A. B. (2000). The p120 catenin family: complex roles in adhesion, signaling and cancer. J. Cell Sci. 113, 1319-1334.
5. Anastasiadis, P. Z., Moon, S. Y., Thoreson, M. A., Mariner, D. J., Crawford, H. C., Zheng, Y. and Reynolds, A. B. (2000). Inhibition of RhoA by p120 catenin. Nat. Cell Biol. 2, 637-644.
6. Arthur, W. T. and Burridge, K. (2001). RhoA inactivation by p190RhoGAP regulates cell spreading and migration by promoting membrane protrusion and polarity. Mol. Biol. Cell 12, 2711-2720.
7. Baki, L., Marambaud, P., Efthimiopoulos, S., Georgakopoulos, A., Wen, P., Cui, W., Shioi, J., Koo, E., Ozawa, M., Friedrich, V. L., Jr et al. (2001). Presenilin-1 binds cytoplasmic epithelial cadherin, inhibits cadherin/p120 association, and regulates stability and function of the cadherin/catenin adhesion complex. Proc. Natl. Acad. Sci. USA 98, 2381-2386.
8. Balanis, N., Yoshigi, M., Wendt, M. K., Schiemann, W. P. and Carlin, C. R. (2011). b3 integrin-EGF receptor cross-talk activates p190RhoGAP in mouse mammary gland epithelial cells. Mol. Biol. Cell 22, 4288-4301.
9. Bellovin, D. I., Bates, R. C., Muzikansky, A., Rimm, D. L. and Mercurio, A. M. (2005). Altered localization of p120 catenin during epithelial to mesenchymal transition of colon carcinoma is prognostic for aggressive disease. Cancer Res. 65, 10938-10945.
10. Berx, G., Nollet, F. and van Roy, F. (1998). Dysregulation of the E-cadherin/catenin complex by irreversible mutations in human carcinomas. Cell Adhes. Commun. 6, 171-184.
11. Boussadia, O., Kutsch, S., Hierholzer, A., Delmas, V. and Kemler, R. (2002). E-cadherin is a survival factor for the lactating mouse mammary gland. Mech. Dev. 115, 53-62.
12. Bremm, A., Walch, A., Fuchs, M., Mages, J., Duyster, J., Keller, G., Hermannstädter, C., Becker, K. F., Rauser, S., Langer, R. et al. (2008). Enhanced activation of epidermal growth factor receptor caused by tumor-derived E-cadherin mutations. Cancer Res. 68, 707-714.
13. Bustos, R. I., Forget, M. A., Settleman, J. E. and Hansen, S. H. (2008). Coordination of Rho and Rac GTPase function via p190B RhoGAP. Curr. Biol. 18, 1606-1611.
14. Carnahan, R. H., Rokas, A., Gaucher, E. A. and Reynolds, A. B. (2010). The molecular evolution of the p120-catenin subfamily and its functional associations. PLoS ONE 5, e15747.
15. Castaño, J., Solanas, G., Casagolda, D., Raurell, I., Villagrasa, P., Bustelo, X. R., García de Herreros, A. and Duñach, M. (2007). Specific phosphorylation of p120-catenin regulatory domain differently modulates its binding to RhoA. Mol. Cell. Biol. 27, 1745-1757.
16. Ceteci, F., Ceteci, S., Karreman, C., Kramer, B. W., Asan, E., Götz, R. and Rapp, U. R. (2007). Disruption of tumor cell adhesion promotes angiogenic switch and progression to micrometastasis in RAF-driven murine lung cancer. Cancer Cell 12, 145-159.
17. Chen, X. and Gumbiner, B. M. (2006). Crosstalk between different adhesion molecules. Curr. Opin. Cell Biol. 18, 572-578.
18. Chen, X., Kojima, S., Borisy, G. G. and Green, K. J. (2003). p120 catenin associates with kinesin and facilitates the transport of cadherin-catenin complexes to intercellular junctions. J. Cell Biol. 163, 547-557.
19. Cheng, Z., Assfag, V., Shi, X., Lin, S., Xia, J., Yang, P., Hüser, N. and Shen, F. (2012). Effect of p120 catenin silencing on biological behaviors of PANC-1 cells. Huazhong Univ. Sci. Technolog. Med. Sci. 32, 707-712.
20. Chetty, R., Jain, D. and Serra, S. (2008). p120 catenin reduction and cytoplasmic relocalization leads to dysregulation of E-cadherin in solid pseudopapillary tumors of the pancreas. Am. J. Clin. Pathol. 130, 71-76.
21. Cheung, L. W., Leung, P. C. and Wong, A. S. (2010). Cadherin switching and activation of p120 catenin signaling are mediators of gonadotropin-releasing hormone to promote tumor cell migration and invasion in ovarian cancer. Oncogene 29, 2427-2440.
22. Choi, H. J. and Weis, W. I. (2005). Structure of the armadillo repeat domain of plakophilin 1. J. Mol. Biol. 346, 367-376.
23. Christiansen, J. H., Monkley, S. J. and Wainwright, B. J. (1996). Murine WNT11 is a secreted glycoprotein that morphologically transforms mammary epithelial cells. Oncogene 12, 2705-2711.
24. Chung, Y., Lam, A. K., Luk, J. M., Law, S., Chan, K. W., Lee, P. Y. and Wong, J. (2007). Altered E-cadherin expression and p120 catenin localization in esophageal squamous cell carcinoma. Ann. Surg. Oncol. 14, 3260-3267.
25. Cozzolino, M., Stagni, V., Spinardi, L., Campioni, N., Fiorentini, C., Salvati, E., Alemà, S. and Salvatore, A. M. (2003). p120 Catenin is required for growth factor-dependent cell motility and scattering in epithelial cells. Mol. Biol. Cell 14, 1964-1977.
26. Dabbs, D. J., Bhargava, R. and Chivukula, M. (2007). Lobular versus ductal breast neoplasms: the diagnostic utility of p120 catenin. Am. J. Surg. Pathol. 31, 427-437.
27. Dai, S. D., Wang, Y., Zhang, J. Y., Zhang, D., Zhang, P. X., Jiang, G. Y., Han, Y., Zhang, S., Cui, Q. Z. and Wang, E. H. (2011). Upregulation of d-catenin is associated with poor prognosis and enhances transcriptional activity through Kaiso in non-small-cell lung cancer. Cancer Sci. 102, 95-103.
28. Daniel, J. M. (2007). Dancing in and out of the nucleus: p120(ctn) and the transcription factor Kaiso. Biochim. Biophys. Acta 1773, 59-68.
29. Daniel, J. M. and Reynolds, A. B. (1999). The catenin p120(ctn) interacts with Kaiso, a novel BTB/POZ domain zinc finger transcription factor. Mol. Cell. Biol. 19, 3614-3623.
30. Daniel, J. M., Spring, C. M., Crawford, H. C., Reynolds, A. B. and Baig, A. (2002). The p120(ctn)-binding partner Kaiso is a bi-modal DNA-binding protein that recognizes both a sequence-specific consensus and methylated CpG dinucleotides. Nucleic Acids Res. 30, 2911-2919.
31. Dannhardt, G. and Kiefer, W. (2001). Cyclooxygenase inhibitors-current status and future prospects. Eur. J. Med. Chem. 36, 109-126.
32. Davis, M. A. and Reynolds, A. B. (2006). Blocked acinar development, E-cadherin reduction, and intraepithelial neoplasia upon ablation of p120-catenin in the mouse salivary gland. Dev. Cell 10, 21-31.
33. Davis, M. A., Ireton, R. C. and Reynolds, A. B. (2003). A core function for p120-catenin in cadherin turnover. J. Cell Biol. 163, 525-534.
34. Del Valle-Pérez, B., Casagolda, D., Lugilde, E., Valls, G., Codina, M., Dave, N., de Herreros, A. G. and Duñach, M. (2011). Wnt controls the transcriptional activity of Kaiso through CK1e-dependent phosphorylation of p120-catenin. J. Cell Sci. 124, 2298-2309.
35. Derksen, P. W., Liu, X., Saridin, F., van der Gulden, H., Zevenhoven, J., Evers, B., van Beijnum, J. R., Griffioen, A. W., Vink, J., Krimpenfort, P. et al. (2006). Somatic inactivation of E-cadherin and p53 in mice leads to metastatic lobular mammary carcinoma through induction of anoikis resistance and angiogenesis. Cancer Cell 10, 437-449.
36. Derksen, P. W., Braumuller, T. M., van der Burg, E., Hornsveld, M., Mesman, E., Wesseling, J., Krimpenfort, P. and Jonkers, J. (2011). Mammary-specific inactivation of E-cadherin and p53 impairs functional gland development and leads to pleomorphic invasive lobular carcinoma in mice. Dis. Model. Mech. 4, 347-358.
37. Dillon, D. A., D'Aquila, T., Reynolds, A. B., Fearon, E. R. and Rimm, D. L. (1998). The expression of p120ctn protein in breast cancer is independent of alpha- and beta-catenin and E-cadherin. Am. J. Pathol. 152, 75-82.
38. Donaldson, N. S., Pierre, C. C., Anstey, M. I., Robinson, S. C., Weerawardane, S. M. and Daniel, J. M. (2012). Kaiso represses the cell cycle gene cyclin D1 via sequence-specific and methyl-CpG-dependent mechanisms. PLoS ONE 7, e50398.
39. Elia, L. P., Yamamoto, M., Zang, K. and Reichardt, L. F. (2006). p120 catenin regulates dendritic spine and synapse development through Rho-family GTPases and cadherins. Neuron 51, 43-56.
40. Etienne-Manneville, S. and Hall, A. (2002). Rho GTPases in cell biology. Nature 420, 629-635.
41. Ferber, E. C., Kajita, M., Wadlow, A., Tobiansky, L., Niessen, C., Ariga, H., Daniel, J. and Fujita, Y. (2008). A role for the cleaved cytoplasmic domain of E-cadherin in the nucleus. J. Biol. Chem. 283, 12691-12700.
42. Fortini, M. E. (2002). Gamma-secretase-mediated proteolysis in cell-surface-receptor signalling. Nat. Rev. Mol. Cell Biol. 3, 673-684.
43. Franz, C. M. and Ridley, A. J. (2004). p120 catenin associates with microtubules: inverse relationship between microtubule binding and Rho GTPase regulation. J. Biol. Chem. 279, 6588-6594.
44. Fujita, Y., Krause, G., Scheffner, M., Zechner, D., Leddy, H. E., Behrens, J., Sommer, T. and Birchmeier, W. (2002). Hakai, a c-Cbl-like protein, ubiquitinates and induces endocytosis of the E-cadherin complex. Nat. Cell Biol. 4, 222-231.
45. Fujita, H., Fukumoto, Y., Saji, K., Sugimura, K., Demachi, J., Nawata, J. and Shimokawa, H. (2010). Acute vasodilator effects of inhaled fasudil, a specific Rhokinase inhibitor, in patients with pulmonary arterial hypertension. Heart Vessels 25, 144-149.
46. Fukuhara, S., Chikumi, H. and Gutkind, J. S. (2001). RGS-containing RhoGEFs: the missing link between transforming G proteins and Rho? Oncogene 20, 1661-1668.
47. Gamallo, C., Palacios, J., Suarez, A., Pizarro, A., Navarro, P., Quintanilla, M. and Cano, A. (1993). Correlation of E-cadherin expression with differentiation grade and histological type in breast carcinoma. Am. J. Pathol. 142, 987-993.
48. Gold, J. S., Reynolds, A. B. and Rimm, D. L. (1998). Loss of p120ctn in human colorectal cancer predicts metastasis and poor survival. Cancer Lett. 132, 193-201.
49. Hanahan, D. and Weinberg, R. A. (2011). Hallmarks of cancer: the next generation. Cell 144, 646-674.
50. Hartsock, A. and Nelson, W. J. (2012). Competitive regulation of E-cadherin juxtamembrane domain degradation by p120-catenin binding and Hakai-mediated ubiquitination. PLoS ONE 7, e37476.
51. Hatzfeld, M. (1999). The armadillo family of structural proteins. Int. Rev. Cytol. 186, 179-224.
52. Hatzfeld, M. (2005). The p120 family of cell adhesion molecules. Eur. J. Cell Biol. 84, 205-214.
53. Holsinger, L. J., Ward, K., Duffield, B., Zachwieja, J. and Jallal, B. (2002). The transmembrane receptor protein tyrosine phosphatase DEP1 interacts with p120(ctn). Oncogene 21, 7067-7076.
54. Hong, J. Y., Park, J. I., Cho, K., Gu, D., Ji, H., Artandi, S. E. and McCrea, P. D. (2010). Shared molecular mechanisms regulate multiple catenin proteins: canonical Wnt signals and components modulate p120-catenin isoform-1 and additional p120 subfamily members. J. Cell Sci. 123, 4351-4365.
55. Hosking, C. R., Ulloa, F., Hogan, C., Ferber, E. C., Figueroa, A., Gevaert, K., Birchmeier, W., Briscoe, J. and Fujita, Y. (2007). The transcriptional repressor Glis2 is a novel binding partner for p120 catenin. Mol. Biol. Cell 18, 1918-1927.
56. Ii, M., Yamamoto, H., Adachi, Y., Maruyama, Y. and Shinomura, Y. (2006). Role of matrix metalloproteinase-7 (matrilysin) in human cancer invasion, apoptosis, growth, and angiogenesis. Exp. Biol. Med. (Maywood) 231, 20-27.
57. Ishizaki, Y., Omori, Y., Momiyama, M., Nishikawa, Y., Tokairin, T., Manabe, M. and Enomoto, K. (2004). Reduced expression and aberrant localization of p120catenin in human squamous cell carcinoma of the skin. J. Dermatol. Sci. 34, 99-108.
58. Israely, I., Costa, R. M., Xie, C. W., Silva, A. J., Kosik, K. S. and Liu, X. (2004). Deletion of the neuron-specific protein delta-catenin leads to severe cognitive and synaptic dysfunction. Curr. Biol. 14, 1657-1663.
59. Jeanes, A., Gottardi, C. J. and Yap, A. S. (2008). Cadherins and cancer: how does cadherin dysfunction promote tumor progression? Oncogene 27, 6920-6929.
60. Jones, J., Wang, H., Zhou, J., Hardy, S., Turner, T., Austin, D., He, Q., Wells, A., Grizzle, W. E. and Yates, C. (2012). Nuclear Kaiso indicates aggressive prostate cancers and promotes migration and invasiveness of prostate cancer cells. Am. J. Pathol. 181, 1836-1846.
61. Kalluri, R. and Weinberg, R. A. (2009). The basics of epithelial-mesenchymal transition. J. Clin. Invest. 119, 1420-1428.
62. Kantidze, O. L., Kamalyukova, I. M. and Razin, S. V. (2009). Association of the mammalian transcriptional regulator kaiso with centrosomes and the midbody. Cell Cycle 8, 2303-2304.
63. Karatzas, G., Karayiannakis, A. J., Syrigos, K. N., Chatzigianni, E., Papanikolaou, S., Simatos, G., Papanikolaou, D. and Bogris, S. (2000). Expression patterns of the E-cadherin-catenin cell-cell adhesion complex in gastric cancer. Hepatogastroenterology 47, 1465-1469.
64. Karayiannakis, A. J., Syrigos, K. N., Alexiou, D., Kalahanis, N., Rosenberg, T., Bastounis, E. and Pignatelli, M. (1999). Expression patterns of the novel catenin p120cas in gastrointestinal cancers. Anticancer Res. 19 5C, 4401-4405.
65. Karin, M. (2009). NF-kappaB as a critical link between inflammation and cancer. Cold Spring Harb. Perspect. Biol. 1, a000141.
66. Keilhack, H., Hellman, U., van Hengel, J., van Roy, F., Godovac-Zimmermann, J. and Böhmer, F. D. (2000). The protein-tyrosine phosphatase SHP-1 binds to and dephosphorylates p120 catenin. J. Biol. Chem. 275, 26376-26384.
67. Keirsebilck, A., Bonné, S., Staes, K., van Hengel, J., Nollet, F., Reynolds, A. and van Roy, F. (1998). Molecular cloning of the human p120ctn catenin gene (CTNND1): expression of multiple alternatively spliced isoforms. Genomics 50, 129-146.
68. Kelly, K. F., Spring, C. M., Otchere, A. A. and Daniel, J. M. (2004). NLS-dependent nuclear localization of p120ctn is necessary to relieve Kaiso-mediated transcriptional repression. J. Cell Sci. 117, 2675-2686.
69. Kim, S. W., Park, J. I., Spring, C. M., Sater, A. K., Ji, H., Otchere, A. A., Daniel, J. M. and McCrea, P. D. (2004). Non-canonical Wnt signals are modulated by the Kaiso transcriptional repressor and p120-catenin. Nat. Cell Biol. 6, 1212-1220.
70. Kiss, A., Troyanovsky, R. B. and Troyanovsky, S. M. (2008). p120-catenin is a key component of the cadherin-gamma-secretase supercomplex. Mol. Biol. Cell 19, 4042-4050.
71. Kouchi, Z., Barthet, G., Serban, G., Georgakopoulos, A., Shioi, J. and Robakis, N. K. (2009). p120 catenin recruits cadherins to gamma-secretase and inhibits production of Abeta peptide. J. Biol. Chem. 284, 1954-1961.
72. Kurley, S. J., Bierie, B., Carnahan, R. H., Lobdell, N. A., Davis, M. A., Hofmann, I., Moses, H. L., Muller, W. J. and Reynolds, A. B. (2012). p120-catenin is essential for terminal end bud function and mammary morphogenesis. Development 139, 1754-1764.
73. Lyons, T. R., O'Brien, J., Borges, V. F., Conklin, M. W., Keely, P. J., Eliceiri, K. W., Marusyk, A., Tan, A. C. and Schedin, P. (2011). Postpartum mammary gland involution drives progression of ductal carcinoma in situ through collagen and COX-2. Nat. Med. 17, 1109-1115.
74. Mani, S. A., Yang, J., Brooks, M., Schwaninger, G., Zhou, A., Miura, N., Kutok, J. L., Hartwell, K., Richardson, A. L. and Weinberg, R. A. (2007). Mesenchyme Forkhead 1 (FOXC2) plays a key role in metastasis and is associated with aggressive basal-like breast cancers. Proc. Natl. Acad. Sci. USA 104, 10069-10074.
75. Mann, K. M., Ward, J. M., Yew, C. C., Kovochich, A., Dawson, D. W., Black, M. A., Brett, B. T., Sheetz, T. E., Dupuy, A. J., Chang, D. K. et al.; AUSTRALIAN PANCREATIC CANCER GENOME INITIATIVE (2012). Sleeping Beauty mutagenesis reveals cooperating mutations and pathways in pancreatic adenocarcinoma. Proc. Natl. Acad. Sci. USA 109, 5934-5941.
76. Marambaud, P., Shioi, J., Serban, G., Georgakopoulos, A., Sarner, S., Nagy, V., Baki, L., Wen, P., Efthimiopoulos, S., Shao, Z. et al. (2002). A presenilin-1/gamma-secretase cleavage releases the E-cadherin intracellular domain and regulates disassembly of adherens junctions. EMBO J. 21, 1948-1956.
77. Marciano, D. K., Brakeman, P. R., Lee, C. Z., Spivak, N., Eastburn, D. J., Bryant, D. M., Beaudoin, G. M., 3rd, Hofmann, I., Mostov, K. E. and Reichardt, L. F. (2011). p120 catenin is required for normal renal tubulogenesis and glomerulogenesis. Development 138, 2099-2109.
78. Mateus, A. R., Seruca, R., Machado, J. C., Keller, G., Oliveira, M. J., Suriano, G. and Luber, B. (2007). EGFR regulates RhoA-GTP dependent cell motility in E-cadherin mutant cells. Hum. Mol. Genet. 16, 1639-1647.
79. Mayerle, J., Friess, H., Büchler, M. W., Schnekenburger, J., Weiss, F. U., Zimmer, K. P., Domschke, W. and Lerch, M. M. (2003). Up-regulation, nuclear import, and tumor growth stimulation of the adhesion protein p120 in pancreatic cancer. Gastroenterology 124, 949-960.
80. Menke, A. and Giehl, K. (2012). Regulation of adherens junctions by Rho GTPases and p120-catenin. Arch. Biochem. Biophys. 524, 48-55.
81. Miyashita, Y. and Ozawa, M. (2007). Increased internalization of p120-uncoupled E-cadherin and a requirement for a dileucine motif in the cytoplasmic domain for endocytosis of the protein. J. Biol. Chem. 282, 11540-11548.
82. Mo, Y. Y. and Reynolds, A. B. (1996). Identification of murine p120 isoforms and heterogeneous expression of p120cas isoforms in human tumor cell lines. Cancer Res. 56, 2633-2640.
83. Mohammed, S. I., Dhawan, D., Abraham, S., Snyder, P. W., Waters, D. J., Craig, B. A., Lu, M., Wu, L., Zheng, R., Stewart, J. et al. (2006). Cyclooxygenase inhibitors in urinary bladder cancer: in vitro and in vivo effects. Mol. Cancer Ther. 5, 329-336.
84. Montonen, O., Aho, M., Uitto, J. and Aho, S. (2001). Tissue distribution and cell type-specific expression of p120ctn isoforms. J. Histochem. Cytochem. 49, 1487-1496.
85. Mortazavi, F., An, J., Dubinett, S. and Rettig, M. (2010). p120-catenin is transcriptionally downregulated by FOXC2 in non-small cell lung cancer cells. Mol. Cancer Res. 8, 762-774.
86. Musgrove, E. A., Caldon, C. E., Barraclough, J., Stone, A. and Sutherland, R. L. (2011). Cyclin D as a therapeutic target in cancer. Nat. Rev. Cancer 11, 558-572.
87. Nagafuchi, A., Shirayoshi, Y., Okazaki, K., Yasuda, K. and Takeichi, M. (1987). Transformation of cell adhesion properties by exogenously introduced E-cadherin cDNA. Nature 329, 341-343.
88. Nakashima, S., Tabuchi, K., Shimokawa, S., Fukuyama, K., Mineta, T. and Abe, M. (1998). Combination therapy of fasudil hydrochloride and ozagrel sodium for cerebral vasospasm following aneurysmal subarachnoid hemorrhage. Neurol Med Chir (Tokyo) 38, 805-810, discussion 810-811.
89. Nanes, B. A., Chiasson-MacKenzie, C., Lowery, A. M., Ishiyama, N., Faundez, V., Ikura, M., Vincent, P. A. and Kowalczyk, A. P. (2012). p120-catenin binding masks an endocytic signal conserved in classical cadherins. J. Cell Biol. 199, 365-380.
90. Noren, N. K., Liu, B. P., Burridge, K. and Kreft, B. (2000). p120 catenin regulates the actin cytoskeleton via Rho family GTPases. J. Cell Biol. 150, 567-580.
91. Palacios, F., Tushir, J. S., Fujita, Y. and D'Souza-Schorey, C. (2005). Lysosomal targeting of E-cadherin: a unique mechanism for the down-regulation of cell-cell adhesion during epithelial to mesenchymal transitions. Mol. Cell. Biol. 25, 389-402.
92. Palka, H. L., Park, M. and Tonks, N. K. (2003). Hepatocyte growth factor receptor tyrosine kinase met is a substrate of the receptor protein-tyrosine phosphatase DEP-1. J. Biol. Chem. 278, 5728-5735.
93. Park, J. I., Ji, H., Jun, S., Gu, D., Hikasa, H., Li, L., Sokol, S. Y. and McCrea, P. D. (2006). Frodo links Dishevelled to the p120-catenin/Kaiso pathway: distinct catenin subfamilies promote Wnt signals. Dev. Cell 11, 683-695.
94. Patel, R. A., Forinash, K. D., Pireddu, R., Sun, Y., Sun, N., Martin, M. P., Schönbrunn, E., Lawrence, N. J. and Sebti, S. M. (2012). RKI-1447 is a potent inhibitor of the Rho-associated ROCK kinases with anti-invasive and antitumor activities in breast cancer. Cancer Res. 72, 5025-5034.
95. Perez-Moreno, M., Davis, M. A., Wong, E., Pasolli, H. A., Reynolds, A. B. and Fuchs, E. (2006). p120-catenin mediates inflammatory responses in the skin. Cell 124, 631-644.
96. Perez-Moreno, M., Song, W., Pasolli, H. A., Williams, S. E. and Fuchs, E. (2008). Loss of p120 catenin and links to mitotic alterations, inflammation, and skin cancer. Proc. Natl. Acad. Sci. USA 105, 15399-15404.
97. Perl, A. K., Wilgenbus, P., Dahl, U., Semb, H. and Christofori, G. (1998). A causal role for E-cadherin in the transition from adenoma to carcinoma. Nature 392, 190-193.
98. Prokhortchouk, A., Hendrich, B., Jørgensen, H., Ruzov, A., Wilm, M., Georgiev, G., Bird, A. and Prokhortchouk, E. (2001). The p120 catenin partner Kaiso is a DNA methylation-dependent transcriptional repressor. Genes Dev. 15, 1613-1618.
99. Prokhortchouk, A., Sansom, O., Selfridge, J., Caballero, I. M., Salozhin, S., Aithozhina, D., Cerchietti, L., Meng, F. G., Augenlicht, L. H., Mariadason, J. M. et al. (2006). Kaiso-deficient mice show resistance to intestinal cancer. Mol. Cell. Biol. 26, 199-208.
100. Qian, X., Karpova, T., Sheppard, A. M., McNally, J. and Lowy, D. R. (2004). E-cadherin-mediated adhesion inhibits ligand-dependent activation of diverse receptor tyrosine kinases. EMBO J. 23, 1739-1784.
101. Reddy, P., Liu, L., Ren, C., Lindgren, P., Boman, K., Shen, Y., Lundin, E., Ottander, U., Rytinki, M. and Liu, K. (2005). Formation of E-cadherin-mediated cell-cell adhesion activates AKT and mitogen activated protein kinase via phosphatidylinositol 3 kinase and ligand-independent activation of epidermal growth factor receptor in ovarian cancer cells. Mol. Endocrinol. 19, 2564-2578.
102. Reynolds, A. B., Daniel, J., McCrea, P. D., Wheelock, M. J., Wu, J. and Zhang, Z. (1994). Identification of a new catenin: the tyrosine kinase substrate p120cas associates with E-cadherin complexes. Mol. Cell. Biol. 14, 8333-8342.
103. Riggleman, B., Schedl, P. and Wieschaus, E. (1990). Spatial expression of the Drosophila segment polarity gene armadillo is posttranscriptionally regulated by wingless. Cell 63, 549-560.
104. Roczniak-Ferguson, A. and Reynolds, A. B. (2003). Regulation of p120-catenin nucleocytoplasmic shuttling activity. J. Cell Sci. 116, 4201-4212.
105. Ruzov, A., Savitskaya, E., Hackett, J. A., Reddington, J. P., Prokhortchouk, A., Madej, M. J., Chekanov, N., Li, M., Dunican, D. S., Prokhortchouk, E. et al. (2009). The non-methylated DNA-binding function of Kaiso is not required in early Xenopus laevis development. Development 136, 729-738.
106. Sadot, E., Simcha, I., Shtutman, M., Ben-Ze'ev, A. and Geiger, B. (1998). Inhibition of beta-catenin-mediated transactivation by cadherin derivatives. Proc. Natl. Acad. Sci. USA 95, 15339-15344.
107. Sato, K., Watanabe, T., Wang, S., Kakeno, M., Matsuzawa, K., Matsui, T., Yokoi, K., Murase, K., Sugiyama, I., Ozawa, M. et al. (2011). Numb controls E-cadherin endocytosis through p120 catenin with aPKC. Mol. Biol. Cell 22, 3103-3119.
108. Schackmann, R. C., van Amersfoort, M., Haarhuis, J. H., Vlug, E. J., Halim, V. A., Roodhart, J. M., Vermaat, J. S., Voest, E. E., van der Groep, P., van Diest, P. J. et al. (2011). Cytosolic p120-catenin regulates growth of metastatic lobular carcinoma through Rock1-mediated anoikis resistance. J. Clin. Invest. 121, 3176-3188.
109. Schackmann, R. C., Klarenbeek, S., Vlug, E. J., Stelloo, S., van Amersfoort, M., Tenhagen, M., Braumuller, T. M., Vermeulen, J. F., van der Groep, P., Peeters, T. et al. (2013). Loss of p120-catenin induces metastatic progression of breast cancer by inducing anoikis resistance and augmenting growth factor receptor signaling. Cancer Res. [Epub ahead of print] doi: 10.1158/0008-5472.CAN-13-0180.
110. Shibamoto, S., Hayakawa, M., Takeuchi, K., Hori, T., Miyazawa, K., Kitamura, N., Johnson, K. R., Wheelock, M. J., Matsuyoshi, N., Takeichi, M. et al. (1995). Association of p120, a tyrosine kinase substrate, with E-cadherin/catenin complexes. J. Cell Biol. 128, 949-957.
111. Shibata, T., Kokubu, A., Sekine, S., Kanai, Y. and Hirohashi, S. (2004). Cytoplasmic p120ctn regulates the invasive phenotypes of E-cadherin-deficient breast cancer. Am. J. Pathol. 164, 2269-2278.
112. Skoudy, A., Gomez, S., Fabre, M. and Garcia de Herreros, A. (1996). p120-catenin expression in human colorectal cancer. Int. J. Cancer 68, 14-20.
113. Slorach, E. M., Chou, J. and Werb, Z. (2011). Zeppo1 is a novel metastasis promoter that represses E-cadherin expression and regulates p120-catenin isoform expression and localization. Genes Dev. 25, 471-484.
114. Smalley-Freed, W. G., Efimov, A., Burnett, P. E., Short, S. P., Davis, M. A., Gumucio, D. L., Washington, M. K., Coffey, R. J. and Reynolds, A. B. (2010). p120-catenin is essential for maintenance of barrier function and intestinal homeostasis in mice. J. Clin. Invest. 120, 1824-1835.
115. Smalley-Freed, W. G., Efimov, A., Short, S. P., Jia, P., Zhao, Z., Washington, M. K., Robine, S., Coffey, R. J. and Reynolds, A. B. (2011). Adenoma formation following limited ablation of p120-catenin in the mouse intestine. PLoS ONE 6, e19880.
116. Soto, E., Yanagisawa, M., Marlow, L. A., Copland, J. A., Perez, E. A. and Anastasiadis, P. Z. (2008). p120 catenin induces opposing effects on tumor cell growth depending on E-cadherin expression. J. Cell Biol. 183, 737-749.
117. Soubry, A., van Hengel, J., Parthoens, E., Colpaert, C., Van Marck, E., Waltregny, D., Reynolds, A. B. and van Roy, F. (2005). Expression and nuclear location of the transcriptional repressor Kaiso is regulated by the tumor microenvironment. Cancer Res. 65, 2224-2233.
118. Soubry, A., Staes, K., Parthoens, E., Noppen, S., Stove, C., Bogaert, P., van Hengel, J. and van Roy, F. (2010). The transcriptional repressor Kaiso localizes at the mitotic spindle and is a constituent of the pericentriolar material. PLoS ONE 5, e9203.
119. Spasic, D. and Annaert, W. (2008). Building gamma-secretase: the bits and pieces. J. Cell Sci. 121, 413-420.
120. Stairs, D. B., Bayne, L. J., Rhoades, B., Vega, M. E., Waldron, T. J., Kalabis, J., Klein-Szanto, A., Lee, J. S., Katz, J. P., Diehl, J. A. et al. (2011). Deletion of p120-catenin results in a tumor microenvironment with inflammation and cancer that establishes it as a tumor suppressor gene. Cancer Cell 19, 470-483.
121. Stephens, P. J., Tarpey, P. S., Davies, H., Van Loo, P., Greenman, C., Wedge, D. C., Nik-Zainal, S., Martin, S., Varela, I., Bignell, G. R. et al.; Oslo Breast Cancer Consortium (OSBREAC) (2012). The landscape of cancer genes and mutational processes in breast cancer. Nature 486, 400-404.
122. Tak, P. P. and Firestein, G. S. (2001). NF-kappaB: a key role in inflammatory diseases. J. Clin. Invest. 107, 7-11.
123. Takahashi, K. and Suzuki, K. (1996). Density-dependent inhibition of growth involves prevention of EGF receptor activation by E-cadherin-mediated cell-cell adhesion. Exp. Cell Res. 226, 214-222.
124. Talvinen, K., Tuikkala, J., Nykänen, M., Nieminen, A., Anttinen, J., Nevalainen, O. S., Hurme, S., Kuopio, T. and Kronqvist, P. (2010). Altered expression of p120catenin predicts poor outcome in invasive breast cancer. J. Cancer Res. Clin. Oncol. 136, 1377-1387.
125. Taniuchi, K., Nakagawa, H., Hosokawa, M., Nakamura, T., Eguchi, H., Ohigashi, H., Ishikawa, O., Katagiri, T. and Nakamura, Y. (2005). Overexpressed P-cadherin/CDH3 promotes motility of pancreatic cancer cells by interacting with p120ctn and activating rho-family GTPases. Cancer Res. 65, 3092-3099.
126. Tarcic, G., Boguslavsky, S. K., Wakim, J., Kiuchi, T., Liu, A., Reinitz, F., Nathanson, D., Takahashi, T., Mischel, P. S., Ng, T. et al. (2009). An unbiased screen identifies DEP-1 tumor suppressor as a phosphatase controlling EGFR endocytosis. Curr. Biol. 19, 1788-1798.
127. Thoreson, M. A. and Reynolds, A. B. (2002). Altered expression of the catenin p120 in human cancer: implications for tumor progression. Differentiation 70, 583-589.
128. Tian, H., Sanders, E., Reynolds, A., van Roy, F. and van Hengel, J. (2012). Ocular anterior segment dysgenesis upon ablation of p120 catenin in neural crest cells. Invest. Ophthalmol. Vis. Sci. 53, 5139-5153.
129. Uysal-Onganer, P. and Kypta, R. M. (2012). Wnt11 in 2011 - the regulation and function of a non-canonical Wnt. Acta Physiol. (Oxf.) 204, 52-64.
130. van Hengel, J., Vanhoenacker, P., Staes, K. and van Roy, F. (1999). Nuclear localization of the p120(ctn) Armadillo-like catenin is counteracted by a nuclear export signal and by E-cadherin expression. Proc. Natl. Acad. Sci. USA 96, 7980-7985.
131. Vasanth, S., ZeRuth, G., Kang, H. S. and Jetten, A. M. (2011). Identification of nuclear localization, DNA binding, and transactivating mechanisms of Kruppel-like zinc finger protein Gli-similar 2 (Glis2). J. Biol. Chem. 286, 4749-4759.
132. Vermeulen, J. F., van de Ven, R. A., Ercan, C., van der Groep, P., van der Wall, E., Bult, P., Christgen, M., Lehmann, U., Daniel, J., van Diest, P. J. et al. (2012). Nuclear Kaiso expression is associated with high grade and triple-negative invasive breast cancer. PLoS ONE 7, e37864.
133. Vleminckx, K., Vakaet, L., Jr, Mareel, M., Fiers, W. and van Roy, F. (1991). Genetic manipulation of E-cadherin expression by epithelial tumor cells reveals an invasion suppressor role. Cell 66, 107-119.
134. Wang, Z. and Li, S. S. (2010). Numb: A new player in EMT. Cell Adh. Migr. 4, 176-179.
135. Wang, Z., Sandiford, S., Wu, C. and Li, S. S. (2009). Numb regulates cell-cell adhesion and polarity in response to tyrosine kinase signalling. EMBO J. 28, 2360-2373.
136. Wildenberg, G. A., Dohn, M. R., Carnahan, R. H., Davis, M. A., Lobdell, N. A., Settleman, J. and Reynolds, A. B. (2006). p120-catenin and p190RhoGAP regulate cell-cell adhesion by coordinating antagonism between Rac and Rho. Cell 127, 1027-1039.
137. Yamada, S., Pokutta, S., Drees, F., Weis, W. I. and Nelson, W. J. (2005). Deconstructing the cadherin-catenin-actin complex. Cell 123, 889-901.
138. Yanagisawa, M. and Anastasiadis, P. Z. (2006). p120 catenin is essential for mesenchymal cadherin-mediated regulation of cell motility and invasiveness. J. Cell Biol. 174, 1087-1096.
139. Yanagisawa, M., Kaverina, I. N., Wang, A., Fujita, Y., Reynolds, A. B. and Anastasiadis, P. Z. (2004). A novel interaction between kinesin and p120 modulates p120 localization and function. J. Biol. Chem. 279, 9512-9521.
140. Yoshida-Noro, C., Suzuki, N. and Takeichi, M. (1984). Molecular nature of the calcium-dependent cell-cell adhesion system in mouse teratocarcinoma and embryonic cells studied with a monoclonal antibody. Dev. Biol. 101, 19-27.
141. Zhang, P. X., Wang, Y., Liu, Y., Jiang, G. Y., Li, Q. C. and Wang, E. H. (2011). p120-catenin isoform 3 regulates subcellular localization of Kaiso and promotes invasion in lung cancer cells via a phosphorylation-dependent mechanism. Int. J. Oncol. 38, 1625-1635.
142. Zondag, G. C., Reynolds, A. B. and Moolenaar, W. H. (2000). Receptor protein-tyrosine phosphatase RPTPmu binds to and dephosphorylates the catenin p120(ctn). J. Biol. Chem. 275, 11264-11269.