The interactions of APC, E-cadherin and β-catenin in tumour development and progression

Journal of Pathology

Volumn 182, Issue 2, 1997, Pages 128-137

  Ilyas, M ^a   Tomlinson, I P M ^b  

^a JOHN RADCLIFFE HOSPITAL   (United Kingdom)

^b INSTITUTE OF CANCER RESEARCH   (United Kingdom)

Author keywords

catenin; Adenomatous polyposis coli (APC); E cadherin; Tumour initiation; Tumour progression

Indexed keywords

BETA CATENIN; UVOMORULIN;

AMINO TERMINAL SEQUENCE; BINDING SITE; CANCER INVASION; COLON POLYPOSIS; GENE EXPRESSION; GENE MUTATION; GENE STRUCTURE; GROWTH REGULATION; IMMUNOHISTOCHEMISTRY; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REVIEW; TUMOR GROWTH;

BETA CATENIN; CADHERINS; COLORECTAL NEOPLASMS; CYTOSKELETAL PROTEINS; GENE EXPRESSION; GENES, APC; HUMANS; MUTATION; NEOPLASMS; TRANS-ACTIVATORS;

EID: 0030818746     PISSN: 00223417     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9896(199706)182:2<128::AID-PATH839>3.0.CO;2-Q     Document Type: Review

References (83)

1. Boudreau N, Werb Z, Bissell M. Suppression of apoptosis by basement membrane requires three-dimensional tissue organisation and withdrawal from the cell cycle. Proc Natl Acad Sci USA 1996; 93: 3509-3513.
2. Pignatelli M, Vessey CJ. Adhesion molecule: novel molecular tools in tumor pathology. Hum Pathol 1994; 25: 849-856.
3. Stallmach A, von-Lampe B, Matthes H, et al. Diminished expression of integrin adhesion molecules on human colonic epithelial cells during the benign to malign tumour transformation. Gut 1992; 33: 342-346.
4. Malchiodi-Albedi F, Cassano AM, Ciaralli F, et al. Ultrastructural immunolocalization of Iaminin and fibronectin in human large intestinal mucosa. J Submicrosc Cytol Pathol 1990; 22: 153-158.
5. Fearon ER, Vogelstein B. A genetic model for colorectal tumorigenesis. Cell 1990; 61: 759-767.
6. Powell SM, Zilz N, Beazer-Barclay Y, et al. APC mutations occur early during colorectal tumorigenesis. Nature 1992; 359: 235-237.
7. Nakamura Y. The role of the adenomatous polyposis coli (APC) gene in human cancers. Adv Cancer Res 1993; 62: 65-87.
8. Cottrell S, Bicknell D, Kaklamanis L, et al. Molecular analysis of APC mutations in familial adenomatous polyposis and sporadic colon carcinomas. Lancet 1992; 340: 626-630.
9. Phillips R, Spigelman A, Thomson J. Familial Adenomatous Polyposis and Other Polyposis Syndromes. London: Edward Anorld, 1994.
10. Rubinfeld B, Albert I, Porfiri E, et al. Binding of GSK3β to the APC-β-catenin complex and regulation of complex assembly. Science 1996; 272: 1023-1026.
11. Munemitsu S, Souza B, Muller O, et al. The APC gene product associates with microtubules in vivo and promotes their assembly in vitro. Cancer Res 1994; 54: 3676-3681.
12. Matsumine A, Ogai A, Senda T, et al. Binding af APC to the human homolog of the Drosophila Discs Large Tumour suppressor protein. Science 1996; 272: 1020-1023.
13. Peifer M. Regulating cell proliferation: as easy as APC. Science 1996; 272: 974-975.
14. Munemitsu S, Albert I, Souza B, et al. Regulation of intracellular beta-catenin levels by the adenomatous polyposis coli (APC) tumor-suppressor protein. Proc Natl Acad Sci USA 1995; 92: 3046-3050.
15. Takeichi M. The cadherins: cell-cell adhesion molecules controlling animal morphogenesis. Development 1988; 102: 639-655.
16. Nagar B, Overduin M, Ikura M, et al. Structural basis of calcium-induced E-cadherin rigidification and dimerization. Nature 1996; 380: 360-364.
17. Shapiro L, Fannon AM, Kwong PD, et al. Structural basis of cell-cell adhesion by cadherins. Nature 1995; 374: 327-337.
18. Overduin M, Harvey T, Bagby S, et al. Solution structure of the epithelial cadherin domain responsible for selective cell adhesion. Science 1995; 267: 386-389.
19. Gumbiner BM, McCrea PD. Catenins as mediators of the cytoplasmic functions of cadherins. J Cell Sci Suppl 1993; 17: 155-158,
20. Oyama T, Kanai Y, Ochiai A, et al. 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 1994; 54: 6282-6287.
21. Morton RA, Ewing CM, Nagafuchi A, et al. Reduction of E-cadherin levels and deletion of the alpha-catenin gene in human prostate cancer cells. Cancer Res 1993; 53: 3585-3590.
22. Nagafuchi A, Ishihara S, Tsukita S. The roles of catenins in the cadherin-mediated cell adhesion: functional analysis of E-cadherin-alpha-catenin fusion molecules. J Cell Biol 1994; 127: 235-245.
23. Dogan A, Wang ZD, Spencer J. E cadherin expression in intestinal epithelium. J Clin Pathol 1995; 48: 143-146.
24. Cowin P. Unraveling the cytoplasmic interactions of the cadherin super-family. Proc Natl Acad Sci USA 1994; 91: 10759-10761.
25. Salomon R, Diaz-Cano S. Introduction to apoptosis. Diagn Mol Pathol 1995; 4: 235-238.
26. Vleminckx K, Vakaet L Jr, Mareel M, et al. Genetic manipulation of E-cadherin expression by epithelial tumor cells reveals an invasion suppressor role. Cell 1991; 66: 107-119.
27. Shiozaki H, Kadowaki T, Doki Y, et al. Effect of epidermal growth factor on cadherin-mediated adhesion in a human oesophageal cancer cell line. Br J Cancer 1995; 71: 250-258.
28. Ochiai A, Akimoto S, Kanai Y, et al. c-erbB-2 gene product associates with catenins in human cancer cells. Biochem Biophys Res Commun 1994; 205: 73-78.
29. Shibamoto S, Hayakawa M, Takeuchi K, et al. Tyrosine phosphorylation of beta-catenin and plakoglobin enhanced by hepatocyte growth factor and epidermal growth factor in human carcinoma cells. Cell Adhes Commun 1994; 1: 295-305.
30. Behrens J, Vakaet L, Friis R, et al. Loss of epithelial differentiation and gain of invasiveness correlates with tyrosine phosphorylation of the E-cadherin/ beta-catenin complex in cells transformed with a temperature-sensitive v-SRC gene. J Cell Biol 1993; 120: 757-766.
31. Cartwright CA, Meisler AI, Eckhart W. Activation of the pp60c-src protein kinase is an early event in colonic carcinogenesis. Proc Natl Acad Sci USA 1990; 87: 558-562.
32. Graff JR, Herman JG, Lapidus RG, et al. E-cadherin expression is silenced by DNA hypermethylation in human breast and prostate carcinomas. Cancer Res 1995; 55: 5195-5199.
33. Hulsken J, Birchmeier W, Behrens J. E-cadherin and APC compete for the interaction with beta-catenin and the cytoskeleton. J Cell Biol 1994; 127: 2061-2069.
34. Peifer M. Cell adhesion and signal transduction: the Armadillo connection. Trends Cell Biol 1995; 5: 224-229.
35. Peifer M, Berg S, Reynolds AB. A repeating amino acid motif shared by proteins with diverse cellular roles. Cell 1994; 76: 789-791.
36. Butz S, Stappert J, Weissig H, et al. Plakoglobin and beta-catenin: distinct but closely related. Science 1992; 257: 1142-1144.
37. Rubinfeld B, Souza B, Albert I, et al. The APC protein and E-cadherin form similar but independent complexes with alpha-catenin, beta-catenin, and plakoglobin. J Biol Chem 1995; 270: 5549-5555.
38. Gumbiner BM. Signal transduction of beta-catenin. Curr Opin Cell Biol 1995; 7: 634-640.
39. Papkoff J, Rubinfeld B, Schryver B, et al. Wnt-l regulates free pools of catenins and stabilizes APC-catenin complexes. Mol Cell Biol 1996; 16: 2128-2134.
40. Inomata M, Ochiai A, Akimoto S, et al. Alteration of β-catenin expression in colonic epithelial cells of familial adenomatous polyposis patients. Cancer Res 1996; 56: 2213-2217.
41. Deschner EE. Adenomas: preneoplastic events, growth and development in man and experimental systems. Pathol Annu 1983; 1: 205-219.
42. Mills S, Shepherd N, Hall P, et al. Proliferative compartment deregulation in the non-neoplastic colonie epithelium of familial adenomatous polyposis. Gut 1995; 36: 391-394.
43. Nakamura S, Goto J, Kitayama Y, et al. Flow cytometric analysis of DNA synthetic phase fraction of the normal appearing colonie mucosa in patients with colorectal neoplasms. Gut 1995; 37: 398-401.
44. Hermiston M, Gordon J. Inflammatory bowel disease and adenomas in mice expressing a dominant negative N-cadherin. Science 1996; 270: 1203-1207.
45. Groden J, Joslyn G, Samowitz W, et al. Response of colon cancer cell lines to the introduction of APC, a colon-specific tumor suppressor gene. Cancer Res 1995; 55: 1531-1539.
46. Gagliardi G, Kandemir O, Liu D, et al. Changes in E-cadherin immunoreactivity in the adenoma-carcinoma sequence of the large bowel. Virchows Arch 1995; 426: 149-154.
47. Van-Aken J, Cuvelier CA, De-Wever N, et al. Immunohistochemical analysis of E-cadherin expression in human colorectal tumours. Pathol Ras Pract 1993; 189: 975-978.
48. Takayama T, Shiozaki H, Shibamoto S, et al. β-catenin expression in human cancers. Am J Pathol 1996; 148: 39-46.
49. Cowley GP, Smith ME. Modulation of E-cadherin expression and morphological phenotype in the intravascular component of adenocarcinomas. Int J Cancer 1995; 60: 325-329.
50. Phillips SM, Morton DG, Lee SJ, et al. Loss of heterozygosity of the retinoblastoma and adenomatous polyposis susceptibility gene loci and in chromosomes 10p, 10q and 16q in human prostate cancer. Br J Urol 1994; 73: 390-395.
51. Suzuki Y, Tamura G, Maesawa C, et al. Analysis of genetic alterations in renal cell carcinoma using the polymerase chain reaction. Virchows Arch 1994; 424: 453-457.
52. Peng HQ, Bailey D, Bronson D, et al. Loss of heterozygosity of tumor suppressor genes in testis cancer. Cancer Res 1995; 55: 2871-2875.
53. Jones MH, Koi S, Fujimoto I, et al. Allelotype of uterine cancer by analysis of RFLP and microsatellite polymorphisms: frequent loss of heterozygosity on chromosome arms 3p, 9q, 10q, and 17p. Genes Chromosomes Cancer 1994; 9: 119-123.
54. Medeiros AC, Nagai MA, Neto MM, et al. Loss of heterozygosity affecting the APC and MCC genetic loci in patients with primary breast carcinomas. Cancer Epidemiol Biomarkers Prev 1994; 3: 331-333.
55. Kashiwaba M, Tamura G, Ishida M. Aberrations of the APC gene in primary breast carcinoma. J Cancer Res Clin Oncol 1994; 120: 727-731.
56. Neuman WL, Wasylyshyn ML, Jacoby R, et al. Evidence for a common molecular pathogenesis in colorectal, gastric, and pancreatic cancer. Genes Chromosomes Cancer 1991; 3: 468-473.
57. Fong KM, Zimmerman PV, Smith PJ. Tumor progression and loss of heterozygosity at 5q and 18q in non-small cell lung cancer. Cancer Res 1995: 55: 220-223.
58. Hosoe S, Ueno K, Shigedo Y, et al. A frequent deletion of chromosome 5q21 in advanced small cell and non-small cell carcinoma of the lung. Cancer Res 1994; 54: 1787-1790.
59. Tamura G, Maesawa C, Suzuki Y, et al. Primary gastric carcinoma cells frequently lose heterozygosity at the APC and MCC genetic loci. Jpn J Cancer Res 1993; 84: 1015-1018.
60. Nakatsuru S, Yanagisawa A, Ichii S, et al. Somatic mutation of the APC gene in gastric cancer: frequent mutations in very well differentiated adenocarcinoma and signet-ring cell carcinoma. Hum Mol Genet 1992; 1: 559-563.
61. Allan GJ, Cottrell S, Trowsdale J, et al. Loss of heterozygosity on chromosome 5 in sporadic ovarian carcinoma is a late event and is not associated with mutations in APC at 5q21-22. Hum Mutat 1994; 3:283-291.
62. Weitzel JN, Patel J, Smith DM, et al. Molecular genetic changes associated with ovarian cancer. Gynecol Oncol 1994; 55: 245-252.
63. Aoki T, Mori T, Du X, et al. Allelotype study of esophageal carcinoma. Genes Chromosomes Cancer 1994; 10: 177-182.
64. Boynton RF, Blount PL, Yin J, et al. Loss of heterozygosity involving the APC and MCC genetic loci occurs in the majority of human esophageal cancers. Proc Natl Acad Sci USA 1992; 89: 3385-3388.
65. Blount PL, Meltzer SJ, Yin J, et al. Clonal ordering of 17p and 5q allelic losses in Barrett dysplasia and adenocarcinoma. Proc Natl Acad Sci USA 1993; 90: 3221-3225.
66. Bongiorno PF, al-Kasspooles M, Lee SW, et al. E-cadherin expression in primary and metastatic thoracic neoplasms and in Barrett's oesophagus. Br J Cancer 1995; 71: 166-172.
67. Sorscher SM, Russack V, Cagle M, et al. Immunolocalization of E-cadherin in human head and neck cancer. Arch Pathol Lab Med 1995; 119: 82-84.
68. Vessey CJ, Wilding J, Folarin N, et al. Altered expression and function of E-cadherin in cervical intraepithelial neoplasia and invasive squamous cell carcinoma. J Pathol 1995; 176: 151-159.
69. Pignatelli M, Ansari TW, Gunter P, et al. Loss of membranous E-cadherin expression in pancreatic cancer: correlation with lymph node metastasis. high grade, and advanced stage. J Pathol 1994; 174: 243-248.
70. Ruggeri B, Caamano J, Slaga TJ, et al. Alterations in the expression of uvomorulin and Na +,K(+)-adenosine triphosphatase during mouse skin tumor progression. Am J Pathol 1992; 140: 1179-1185.
71. Sakuragi N, Nishiya M, Ikeda K, et al. Decreased E-cadherin expression in endometrial carcinoma is associated with tumor dedifferentiation and deep myometrial invasion. Gynecol Oncol 1994; 53: 183-189.
72. Risinger JI, Berchuck A, Kohler MF, et al. Mutations of the E-cadherin gene in human gynecologic cancers. Nature Genet 1994; 7: 98-102.
73. Umbas R, Schalken JA, Aalders TW, et al. Expression of the cellular adhesion molecule E-cadherin is reduced or absent in high-grade prostate cancer. Cancer Res 1992; 52: 5104-5109.
74. Umbas R, Isaacs WB, Bringuier PP, et al. Decreased E-cadherin expression is associated with poor prognosis in patients with prostate cancer. Cancer Res 1994; 54: 3929-3933.
75. Isaacs WB, Bova GS, Morton RA, et al. Molecular biology of prostate cancer progression. Cancer Surv 1995; 23: 19-32.
76. Palacios J, Benito N, Pizarro A, et al. Relationship between ERBB2 and E-cadherin expression in human breast cancer. Virchows Arch 1995; 427: 259-263.
77. Gamallo C, Palacios J, Suarez A, et al. Correlation of E-cadherin expression with differentiation grade and histological type in breast carcinoma. Am J Pathol 1993; 142: 987-993.
78. Berx G, Cleton-Jansen AM, Nollet F, et al. E-cadherin is a tumour/invasion suppressor gene mutated in human lobular breast cancers. EMBO J 1995; 14: 6107-6115.
79. Mayer B, Johnson JP, Leitl F, et al. E-cadherin expression in primary and metastatic gastric cancer: down-regulation correlates with cellular dedifferentiation and glandular disintegration. Cancer Res 1993; 53: 1690-1695.
80. Becker KF, Atkinson MJ, Reich U. et al. E-cadherin gene mutations provide clues to diffuse type gastric carcinomas. Cancer Res 1994; 54: 3845-3852.
81. Shiozaki H, Iihira K, Oka H, et al. Immunohistochemical detection of α-catenin expression in human cancers. Am J Pathol 1994; 144: 667-674.
82. Matsui S, Shiozaki H, Inoue M, et al. Immunohistochemical evaluation of alpha-catenin expression in human gastric cancer. Virchows Arch 1994; 424: 375-381.
83. Oda T, Kanai Y, Oyama T, et al. E-cadherin gene mutations in human gastric carcinoma cell lines. Proc Natl Acad Sci USA 1994; 91: 1858-1862.