Dysregulation of the E-Cadherin/Catenin Complex by Irreversible Mutations in Human Carcinomas

Cell Communication and Adhesion

Volumn 6, Issue 2-3, 1998, Pages 171-184

  Berx, Geert ^a   Nollet, Friedel ^a   Van Roy, Frans ^a  

^a GHENT UNIVERSITY   (Belgium)

Author keywords

Breast cancer; Catenins; E cadherin gene; Gastric cancer; Oncogene; Tumour suppressor

Indexed keywords

CATENIN; UVOMORULIN;

BREAST CARCINOMA; CARCINOGENESIS; CARCINOMA; CELL ADHESION; COLON TUMOR; COMPLEX FORMATION; CONFERENCE PAPER; GENE MUTATION; HUMAN; HUMAN CELL; MAJOR CLINICAL STUDY; MELANOMA; ONCOGENE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; STOMACH CARCINOMA; TUMOR SUPPRESSOR GENE;

BETA CATENIN; BREAST NEOPLASMS; CADHERINS; CYTOSKELETAL PROTEINS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MUTATION; STOMACH NEOPLASMS; TRANS-ACTIVATORS;

EID: 0031742474     PISSN: 10615385     EISSN: None     Source Type: Journal    
DOI: 10.3109/15419069809004474     Document Type: Article

References (88)

1. Aberle, H., Butz, S., Stappert, J., Weissig, H., Kemler, R. and Hoschuetzky, H. (1994) Assembly of the cadherin catenin complex in vitro with recombinant proteins. J. Cell Sci. 107, 3655-3663.
2. Aberle, H., Bierkamp, C., Torchard, D., Serova, O., Wagner, T., Natt, E., Wirsching, J., Heidkamper, C., Montagna, M., Lynch, H.T., Lenoir, G.M., Scherer, G., Feunteun, J. and Kemler, R. (1995) The human plakoglobin gene localizes on chromosome 17q21 and is subjected to loss of heterozygosity in breast and ovarian cancers. Proc. Natl. Acad. Sci. USA 92, 6384-6388.
3. Aberle, H., Bauer, A., Stappert, J., Kispert, A. and Kemler, R. (1997) Beta-catenin is a target for the ubiquitin-proteasome pathway. EMBO J. 16, 3797-3804.
4. Beaudet, A.L. and Tsui, L.-C. (1993) A suggested nomenclature for designating mutations. Hum. Mutat. 2, 245-248.
5. Becker, K.-F., Atkinson. M J., Reich, U., Huang, H.-H., Nekarda, H., Siewert, J.R. and Höfler, H. (1993) Exon skipping in the E-cadherin gene transcript in metastatic human gastric carcinomas. Hum. Molec. Genet. 2, 803-804.
6. Becker, K.-F., Atkinson, M.J., Reich, U., Becker, I., Nekarda, H., Siewert, J.R. and Höfler, H. (1994) E-cadherin gene mutations provide clues to diffuse type gastric carcinomas. Cancer Res. 54, 3845-3852
7. Behrens, J., von Kries, J.P., Kühl, M., Bruhn, L., Wedlich, D., Grosschedl, R. and Birchmeier, W. (1996) Functional interaction of beta-catenin with the transcription factor LEF-1. Nature 382, 638-642.
8. Berx, G., Staes, K., van Hengel, J., Molemans, F., Bussemakers, M.J.G., van Bokhoven, A. and van Roy, F. (1995a) Cloning and characterization of the human invasion suppressor gene E-cadherin (CDH1). Genomics 26, 281-289.
9. Berx, G , Cleton-Jansen, A.-M., Nollet, F , de Leeuw, W.J.F , van de Vijver, M J., Cornelisse, C. and van Roy, F. (1995b) E-cadherin is a tumor/invasion suppressor gene mutated in human lobular breast cancers. EMBO J. 14, 6107-6115.
10. Berx, G., Cleton-Jansen, A.-M., Strumane, K., de Leeuw, W.J.F , Nollet, F , van Roy, F.M. and Cornelisse, C. (1996) E-cadherin is inactivated in a majority of invasive human lobular breast cancers by truncation mutations throughout its extracellular domain Oncogene 13, 1919-1925.
11. Birchmeier, W. and Behrens, J. (1994) Cadherin expression in carcinomas: Role in the formation of cell junctions and the prevention of invasiveness. Biochim. Biophys. Acta - Rev. Cancer 1198, 11-26.
12. Brabant, G., Hoangvu, C., Cetin, Y., Dralle, H , Scheumann, G., Molne, J., Hansson, G., Jansson, S., Ericson, L.E. and Nilsson, M. (1993) E-cadherin - a differentiation marker in thyroid malignancies. Cancer Res. 53, 4987-4993.
13. Bracke, M.E., van Roy, F.M. and Mareel, M.M. (1996) The E-cadherin/catenin complex in invasion and metastasis. In Current Topics Microbiology and Immunology: Attempts to Understand Metastasis Formation I, Vol. 213/I, U. Günthert and W Birchmeier, eds., Springer Verlag, Berlin, pp. 123-161.
14. Bussemakers, M.J., van-Bokhoven, A., Mees, S.G., Kemler, R. and Schalken, J.A. (1993) Molecular cloning and characterization of the human E-cadherin cDNA. Mol. Biol Rep. 17, 123-128.
15. Candidus, S., Bischoff, P., Becker, K.F. and Hofler, H. (1996) No evidence for mutations in the alpha- and beta-catenin genes in human gastric and breast carcinomas. Cancer Res. 56, 49-52.
16. Carter, B.S., Ewing, C.M., Ward, W.S., Treiger, B.F., Aalders, T.W., Schalken, J.A., Epstein, J.I. and Isaacs, W B. (1990) Allelic loss of chromosomes 16q and 10q in human prostate cancer. Proc. Natl. Acad. Sci. USA 87, 8751-8755.
17. Cleton-Jansen, A.-M., Moerland, E.W., Kuipers-Dijkshoorn, N.J., Callen, D.F., Sutherland, G.R., Hansen, B., Devilee, P. and Cornelisse, C.J (1994) At least two different regions are involved in allelic imbalance on chromosome arm 16q in breast cancer. Gene Chromos. Cancer 9, 101-107.
18. Cowin, P (1994) Unraveling the cytoplasmic interactions of the cadherin superfamily. Proc. Natl. Acad. Sci. USA 91, 10759-10761.
19. Daar, I.O. and Maquat, L.E. (1988) Premature translation termination mediates triosphosphate isomerase mRNA degradation. Mol. Cell. Biol. 8, 802-813.
20. de Leeuw, W.J.F., Berx, G., Vos, C.B.J., Peterse, J.L., van de Vijver, M.J., Litvinov, S., van Roy, F.M., Cornelisse, C.J. and Cleton-Jansen, A.-M. (1997) Simultaneous loss of E-cadherin and catenins in invasive lobular breast cancer and lobular carcinoma in situ J Pathol. 183, 404-411.
21. Ewing, C.M., Ru, N., Morton, R.A., Robinson, J.C., Wheelock, M.J., Johnson, K.R., Barrett, J.C. and Isaacs, W.B. (1995) Chromosome 5 suppresses tumorigenicity of PC3 prostate cancer cells correlation with re-expression of alpha-catenin and restoration of E-cadherin function. Cancer Res. 55, 4813-4817.
22. Frixen, U.H., Behrens, J , Sachs, M., Eberle, G., Voss, B., Warda, A., Lochner, D. and Birchmeier, W. (1991) E-cadherin-mediated cell-cell adhesion prevents invasiveness of human carcinoma cells. J Cell Biol. 113, 173-185.
23. Furukawa, Y., Nakatsuru, S., Nagafuchi, A., Tsukita, S., Muto, T., Nakamura, Y. and Horii, A (1994) Structure, expression and chromosome assignment of the human catenin (cadherin-associated protein) alpha-1 gene (CTNNA1). Cyrogenet. Cell Genet. 65, 74-78.
24. 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.
25. Graff, J.R , Herman, J.G., Lapidus, R G., Chopra, H., Xu, R., Jarrard, D F , Isaacs, W.B., Pitha, P.M., Davidson, N.E. and Baylin, S.B. (1995) E-cadherin expression is silenced by DNA hypermethylation in human breast and prostate carcinomas. Cancer Res. 55, 5195-5199.
26. Guilford, P., Hopkins, J., Harraway, J., McLeod, M., McLeod, N., Harawira, P., Taite, H., Scoular, R., Miller, A. and Reeve, A.E. (1998) E-cadherin germline mutations in familial gastric cancer. Nature 392, 402-405.
27. Hennig, G., Behrens, J., Truss, M., Frisch, S., Reichmann, E. and Birchmeier, W. (1995) Progression of carcinoma cells is associated with alterations in chromatin structure and factor binding at the E-cadherin promoter in vivo. Oncogene 11, 475-484.
28. Herman, J.G., Graff, J.R., Myohanen, S., Nelkin, B.D. and Baylin, S.B. (1996) Methylation-specific PCR: A novel PCR assay for methylation status of CpG islands. Proc. Natl. Acad. Sci. USA 93, 9821-9826.
29. Herrenknecht, K., Ozawa, M., Eckerskorn, C., Lottspeich, F., Lenter, M. and Kemler, R. (1991) The uvomorulin-anchorage protein alpha-catenin is a vinculin homologue. Proc. Natl. Acad. Sci. USA 88, 9156-9160.
30. Hirano, S., Kimoto, N., Shimoyama, Y., Hirohashi, S. and Takeichi, M. (1992) Identification of a neural alpha-catenin as a key regulator of cadherin function and multicellular organization. Cell 70, 293-301.
31. Hülsken, J., Birchmeier, W. and Behrens, J. (1994) E-cadherin and APC compete for the interaction with beta-catenin and the cytoskeleton. J. Cell Biol. 127, 2061-2069.
32. Ilyas, M., Tomlinson, I.P.M., Rowan, A., Pignatelli, M. and Bodmer, W.F. (1997) Beta-catenin mutations in cell lines established from human colorectal cancers. Proc. Natl. Acad. Sci. USA 94, 10330-10334.
33. Ji, X.D., Woodard, A.S., Rimm, D.L. and Fearon, E.R. (1997) Transcriptional defects underlie loss of E-cadherin expression in breast cancer. Cell Growth Differ. 8, 773-778.
34. Jou, T.S., Stewart, D.B., Stappert, J., Nelson, W.J. and Marrs, J.A. (1995) Genetic and biochemical dissection of protein linkages in the cadherin-catenin complex. Proc Natl. Acad. Sci. USA 92, 5067-5071.
35. Kadowaki, T., Shiozaki, H., Inoue, M., Tamura, S., Oka, H., Doki, Y., Iihara, K., Matsui, S., Iwazawa, T., Nagafuchi, A., Tsukita, S. and Mori, T., (1994) E-cadherin and alpha-catenin expression in human esophageal cancer. Cancer Res. 54, 291-296.
36. Kanai, Y., Ushijima, S , Hui, A.M., Ochiai, A., Tsuda, H , Sakamoto, M. and Hirohashi, S. (1997) The E-cadherin gene is silenced by CpG methylation in human hepatocellular carcinomas. Int. J. Cancer 71, 355-359.
37. Kas, K., Voz, M.L., Roijer, E., Astrom, A.K., Meyen, E., Stenman, G. and Vande Ven, W.J M. (1997) Promoter swapping between the genes for a novel zinc finger protein and beta-catenin in pleiomorphic adenomas with t(3;8)(p21;q12) translocations. Nat. Genet. 15, 170-174.
38. Kawanishi, J., Kato, J., Sasaki, K., Fujii, S., Watanabe, N. and Niitsu, Y. (1995) Loss of E-cadherin-dependent cell-cell adhesion due to mutation of the beta-catenin gene in a human cancer cell line, HSC-39. Mol. Cell. Biol. 15, 1175-1181.
39. Knudsen, K.A , Soler, A.P., Johnson, K.R. and Wheelock, M.J (1995) Interaction of alpha-actinin with the cadherin/catenin cell-cell adhesion complex via alpha-catenin. J. Cell Biol. 130, 67-77.
40. Kok, K., van den Berg, A., Veldhuis, P.M.J.F., van der Veen, A.Y., Franke, M., Schoenmakers, E.F.P.M., Hulsbeek, M.M.F., van der Hout, A.H., de Leij, L., van de Ven, W. and Buys, C.H.C.M. (1994) A homozygous deletion in a small cell lung cancer cell line involving a 3p21 region with a marked instability in yeast artifical chromosomes. Cancer Res. 54, 4183-4187.
41. Korinek, V., Barker, N., Morin, P.J., van Wichen, D., de Weger, R., Kanzler, K.W., Vogelstein, B. and Clevers, H. (1997) Constitutive transcriptional activation by a beta-catenin-Tcf complex in APC-/- colon carcinoma. Science 275, 1784-1786.
42. Kraus, C., Liehr, T., Hulsken, J., Behrens, J., Birchmeier, W., Grzeschik, K.H. and Ballhausen, W.G. (1994) Localization of the human beta-catenin gene (CTNNB1) to 3p21. a region implicated in tumor development. Genomics 23, 272-274.
43. Li, C., Berx, G., Larsson, C., Auer, G., Aspenblad, U., Pan, Y., Sundelin, B., Ekman, M., van Roy, F. and Bergerheim, U.S.R. Lack of somatic E-cadherin mutations in prostate cancer and localization of distinct deleted regions on chromosome 16q associated with metastases (Submitted for publication).
44. Mansouri, A., Spurr, N., Goodfellow, P.N. and Kemler, R. (1988) Characterization and chromosomal localization of the gene encoding the human cell adhesion molecule uvomorulin. Differentiation 38, 67-71.
45. Mareel, M., Berx, G., Van Roy, F. and Bracke, M. (1996) The cadherin/catenin complex: a target for antiinvasive therapy? J. Cell. Biochem. 61, 524-530.
46. Merlo, A., Herman, J.G., Mao, L., Lee, D.J., Gabrielson, E., Burger, P.C., Baylin, S.B. and Sidransky, D. (1995) 5′ CpG island methylation is associated with transcriptional silencing of the tumour suppressor p16/CDKN2/MTS1 in human cancers. Nature Med. 1, 686-692.
47. Miller, J.R. and Moon, R.T. (1996) Signal transduction through beta-catenin and specification of cell fate during embryo-genesis. Gene Develop. 10, 2527-2539.
48. Molenaar, M., van de Wetering, M., Oosterwegel, M., Peterson-Maduro, J., Godsave, S., Korinek, V., Roose, J., Destrée, O. and Clevers, H. (1996) XTcf-3 transcription factor mediates beta-catenin-induced axis formation in Xenopus embryos. Cell 86, 391-399.
49. Moll, R., Mitze, M., Frixen, U.H. and Birchmeier, W. (1993) Differential loss of E-cadherin expression in infiltrating ductal and lobular breast carcinomas. Am. J. Pathol. 143, 1731-1742.
50. Morin, P.J , Sparks, A B., Korinek, V., Barker, N., Clevers, H., Vogelstein, B. and Kinzler, K.W. (1997) Activation of beta-catenin-Tcf signalling in colon cancer by mutations in beta-catenin or APC. Science 275, 1787-1789.
51. Morton, R.A., Ewing, C.M., Nagafuchi, A., Tsukita, S. and Isaacs, W.B. (1993) Reduction of E-cadherin levels and deletion of the alpha-catenin gene in human prostate cancer cells. Cancer Res. 53, 3585-3590.
52. Muta, H , Noguchi, M., Kanai, Y., Ochiai, A., Nawata, H. and Hirohashi, S. (1996) E-cadherin gene mutations in signet ring cell carcinoma of the stomach. Jpn. J. Cancer Res. 87, 843-848.
53. Nagafuchi, A., Takeichi, M. and Tsukita, S. (1991) The 102 kd cadherin-associated protein: Similarity to vinculin and post-transcriptional regulation of expression. Cell 65, 849-857.
54. Natt, E , Magenis, R.E., Zimmer, J., Mansouri, A. and Scherer, G (1989) Regional assignment of the human loci for uvomorulin (UVO) and chymotrypsinogen B (CTRB) with the help of two overlapping deletions on the long arm of chromosome 16. Cytogenet. Cell Genet. 50, 145-148.
55. Navarro, P., Gomez, M., Pizarro, A., Gamallo, C., Quintanilla, M. and Cano, A. (1991) A role for the E-cadherin cell-cell adhesion molecule during tumor progression of mouse epidermal carcinogenesis. J. Cell Biol 115, 517-533.
56. Nollet, F , van Hengel, J., Berx, G , Molemans, F. and van Roy, F. (1995) Isolation and characterization of a human pseudogene (CTNNAP1) for alpha-E-catenin (CTNNA1): Assignment of the pseudogene to 5q22 and the alpha-E-catenin gene to 5q31. Genomics 26, 410-413.
57. Nollet, F., Berx, G., Molemans, F. and van Roy, F. (1996) Genomic organization of the human beta-catenin gene (CTNNB1). Genomics 32, 413-424.
58. Nollet, F., van den Berg, A., Kersemaekers, A.-M., Cleton-Jansen, A.-M., Berx, G., van der Veen, A.Y., Eichperger, C., Wieland, I., De Grève, J., Liefers, G.-J., Xiao, W.-H., Buys, C.H.C.M., Cornelisse, C. and van Roy, F. (1997) Allelic imbalance at the beta-catenin gene (CTNNB1 at 3p22-21.3) in various human tumor types. Int. J. Oncol. 11, 311-318.
59. Oda, T., Kanai, Y., Shimoyama, Y., Nagafuchi, A., Tsukita, S. and Hirohashi, S. (1993) Cloning of the human alpha-catenin cDNA and its aberrant messenger RNA in a human cancer cell line. Biochem. Biophys. Res. Commun. 193, 897-904.
60. Oda, T., Kanai, Y., Oyama, T., Yoshiura, K., Shimoyama, Y., Birchmeier, W., Sugimura, T. and Hirohashi, S. (1994) E-cadherin gene mutations in human gastric carcinoma cell lines. Proc. Natl. Acad. Sci. USA 91, 1858-1862.
61. Ohtani-Fujita, N., Aoike, A., Osifchin, N.E., Robbins, P.D. and Sakai, T. (1993) CpG methylation inactivates the promotor activity of the human retinoblastoma tumor suppressor gene. Oncogene 8, 1063-1067.
62. Oyama, T., Kanai, Y., Ochiai, A., Akimoto, S., Oda, T., Yanagihara, K., Nagafuchi, A., Tsukita, S., Shibamoto, S., Ito, F., Takeichi, M., Matsuda, H. and Hirohashi, S. (1994) A truncated beta-catenin disrupts the interaction between E-cadherin and alpha-catenin: a cause of loss of intercellular adhesiveness in human cancer cell lines. Cancer Res. 54, 6282-6287.
63. Ozawa, M., Terada, H. and Pedraza, C. (1995) The fourth armadillo repeat of plakoglobin (gamma-catenin) is required for its high affinity binding to the cytoplasmic domains of E-cadherin and desmosomal cadherin dsg2, and the tumor suppressor APC protein. Journal of Biochemistry 118, 1077-1082.
64. Peifer, M., Sweeton, D., Casey, M. and Wieschaus, E. (1994) Wingless signal and zeste-white 3 kinase trigger opposing changes in the intracellular distribution of armadillo. Development 120, 369-380.
65. Rasbridge, S.A , Gillett, C.E., Sampson, S.A., Walsh, F.S. and Millis, R.R. (1993) Epithelial (E-) and placental (P-) cadherin cell adhesion molecule expression in breast carcinoma. J. Pathol. 169, 245-250.
66. 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 p120(cas) associates with E-cadherin complexes. Mol. Cell. Biol. 14, 8333-8342.
67. Rimm, D.L., Sinard, J.H. and Morrow, J.S. (1995) Reduced alpha-catenin and E-cadherin expression in breast cancer. Lab Invest. 72, 506-512.
68. Risinger, J.I , Berchuck, A., Kohler, M.F. and Boyd, J. (1994) Mutations of the E-cadherin gene in human gynecologic cancers. Nat. Genet. 7, 98-102.
69. Robbins, P.F., ElGamil, M., Li, Y.F., Kawakami, Y., Loftus, D., Appella, E. and Rosenberg, S.A. (1996) A mutated beta-catenin gene encodes a melanoma-specific antigen recognized by tumor infiltrating lymphocytes. J. Exp. Med. 183, 1185-1192.
70. Rubinfeld, B., Robbins, P., El-Gamil, M., Albert, I., Porfiri, E and Polakis, P. (1997) Stabilization of beta-catenin by genetic defects in melanoma cell lines Science 275, 1790-1792.
71. Sato, T., Tanigami, A., Yamakawa, K , Akiyama, F., Kasumi, F., Sakamoto, G. and Nakamura, Y (1990) Allelotype of breast cancer: cumulative allele losses promote tumor progression in primary breast cancer. Cancer Res. 50, 7184-7189.
72. Soares, P., Berx, G., van Roy, F. and Sobrinho-Simoes, M. (1997) E-cadherin gene alterations are rare events in thyroid tumors. Int. J. Cancer 70, 32-38.
73. Sommers, C.L., Thompson, E.W., Torri, J.A., Kemler, R., Gelmann, E.P. and Byers, S.W. (1991) Cell adhesion molecule uvomorulin expression in human breast cancer cell lines: relationship to morphology and invasive capacities. Cell Growth Differ. 2, 365-372.
74. Takayama, T., Shiozaki, H., Inoue, M., Tarawa, S., Oka, H., Kadowaki, T., Takatsuka, Y., Nagafuchi, A., Tsukita, S. and Mon, T. (1994) Expression of E-cadherin and alpha-catenin molecules in human breast cancer tissues and association with clinicopathological features. Int. J. Oncol. 5, 775-780.
75. Takayama, T., Shiozaki, H., Shibamoto, S., Oka, H., Kimura, Y., Tamura, S., Inoue, M., Monden, T., Ito, F. and Monden, M. (1996) Beta-catenin expression in human cancers. Am. J. Pathol. 148, 39-46.
76. Takeichi, M., Hirano, S., Matsuyoshi, N. and Fujimori, T. (1992) Cytoplasmic control of cadherin-mediated cell-cell adhesion. Cold Spring Harbor Symp. Quant. Biol. 57, 327-334.
77. Tamura, G., Sakata, K., Nishizuka, S., Maesawa, C., Suzuki, Y., Iwaya, T., Terashima, M., Saito, K. and Satodate, R. (1996) Inactivation of the E-cadherin gene in primary gastric carcinomas and gastric carcinoma cell lines. Jpn. J. Cancer Res. 87, 1153-1159.
78. Trent, J.M., Wiltshire, R., Su, L.K., Nicolaides, N.C., Vogelstein, B. and Kinzler, K.W. (1995) The gene for the APC-binding protein beta-catenin (CTNNB1) maps to chromosome 3p22, a region frequently altered in human malignancies. Cytogenet. Cell Genet. 71, 343-344.
79. Uchida, N., Shimamura, K , Miyatani, S., Copeland, N.G., Gilbert, D.J., Jenkins, N.A. and Takeichi, M. (1994) Mouse alpha-N-catenin: Two isoforms, specific expression in the nervous system, and chromosomal localization of the gene. Dev. Biol. 163, 75-85.
80. Umbas, R., Schalken, J.A., Aalders, T W., Carter, B.S., Karthaus, H.F.M., Schaafsma, H.E., Debruyne, F.M.J. and Isaacs, W.B. (1992) Expression of the cellular adhesion molecule E-cadherin is reduced or absent in high-grade prostate cancer. Cancer Res. 52, 5104-5109.
81. Van Hengel, J., Nollet, F., Berx, G., van Roy, N., Speleman, F. and van Roy, F. (1995) Assignment of the human β-catenin gene (CTNNB1) to 3p22-p21.3 by fluorescence in situ hybridization. Cytogenet. Cell Genet. 70, 68-70.
82. Vermeulen, S.J., Bruyneel, E.A., Bracke, M.E., De Bruyne, G.K., Vennekens, K.M., Vleminckx, K.L., Berx, G.J., van Roy, F.M and Marcel, M M. (1995) Transition from the noninvasive to the invasive phenotype and loss of alpha-catenin in human colon cancer cells. Cancer Res. 55, 4722-4728.
83. Vermeulen, S., Nollet, F., Teugels, E., Malfait, F., Vennekens, K.M., Malfait, F., Phillippé, J., Speleman, F., Bracke, M.E., van Roy, F.M. and Marcel, M. (1998) The alpha-E-catenin gene (CTNNA1) acts as an invasion-suppressor gene in human colon cancer cells (Submitted for publication).
84. Vleminckx, K., Vakaet Jr., L , 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.
85. Vos, C.B.J , Cleton-Jansen, A.-M., de Leeuw, W.J.F., ter Haar, N.T., Berx, G., van Roy, F., Cornelisse, C.J., Peterse, J.L. and van de Vijver, M J. (1997) E-cadherin inactivation in lobular carcinoma in situ of the breast: An early event in tumourigenesis. Br. J. Cancer 76, 1131-1133.
86. Watabe, M., Nagafuchi, A., Tsukita, S. and Takeichi, M. (1994) Induction of polarized cell-cell association and retardation of growth by activation of the E-cadherin catenin adhesion system in a dispersed carcinoma line. J. Cell Biol. 127, 247-256.
87. Whitehead, I., Kirk, H. and Kay, R. (1995) Expression cloning of oncogenes by retroviral transfer of cDNA libraries. Mol. Cell. Biol. 15, 704-710.
88. Yoshiura, K., Kanai, Y., Ochiai, A., Shimoyama, Y., Sugimura, T. and Hirohashi, S. (1995) Silencing of the E-cadherin invasion-suppressor gene by CpG methylation in human carcinomas. Proc. Natl. Acad. Sci. USA 92, 7416-7419.