Invasion and metastasis in colorectal cancer: Epithelial-mesenchymal transition, mesenchymal-epithelial transition, stem cells and β-catenin

Cells Tissues Organs

Volumn 179, Issue 1-2, 2005, Pages 56-65

  Brabletz, Thomas ^a   Hlubek, Falk ^a   Spaderna, Simone ^a   Schmalhofer, Otto ^a   Hiendlmeyer, Elke ^a   Jung, Andreas ^a   Kirchner, Thomas ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

catenin; Colorectal cancer; EMT; MET; Tumor invasion

Indexed keywords

BETA CATENIN; WNT PROTEIN;

ARTICLE; BINDING SITE; CANCER CELL; CANCER INVASION; CELL DIFFERENTIATION; COLORECTAL CANCER; EMBRYO DEVELOPMENT; EPITHELIUM CELL; GENE CONTROL; GENE EXPRESSION; HISTOGENESIS; HUMAN; MESENCHYME; METASTASIS; MORPHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; STEM CELL; TUMOR CELL; TUMOR GROWTH;

BETA CATENIN; CELL NUCLEUS; COLORECTAL NEOPLASMS; CYTOSKELETAL PROTEINS; DISEASE PROGRESSION; EMBRYONIC DEVELOPMENT; EPITHELIAL CELLS; EPITHELIUM; GENES, APC; HUMANS; IMMUNOHISTOCHEMISTRY; MESODERM; MODELS, BIOLOGICAL; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; SIGNAL TRANSDUCTION; STEM CELLS; TRANS-ACTIVATORS;

EID: 22144497081     PISSN: 14226405     EISSN: None     Source Type: Journal    
DOI: 10.1159/000084509     Document Type: Article

References (68)

1. Al-Hajj, M., M.W. Becker, M. Wicha, I. Weissman, M.F. Clarke (2004) Therapeutic implications of cancer stem cells. Curr Opin Genet Dev 14: 43-47.
2. Barker, N., G. Huls, V. Korinek, H. Clevers (1999) Restricted high level expression of Tcf-4 protein in intestinal and mammary gland epithelium. Am J Pathol 154: 29-35.
3. Barker, N., A. Hurlstone, H. Musisi, A. Miles, M. Bienz, H. Clevers (2001) The chromatin remodelling factor Brg-1 interacts with beta-catenin to promote target gene activation. EMBO J 20: 4935-4943.
4. Bates, R.C., A.M. Mercurio (2003) Tumor necrosis factor-alpha stimulates the epithelial-to-mesenchymal transition of human colonic organoids. Mol Biol Cell 14: 1790-1800.
5. Batsche, E., C. Muchardt, J. Behrens, H.C. Hurst, C. Cremisi (1998) RB and c-Myc activate expression of the E-cadherin gene in epithelial cells through interaction with transcription factor AP-2. Mol Cell Biol 18: 3647-3658.
6. Behrens, J. (1999) Cadherins and catenins: Role in signal transduction and tumor progression. Cancer Metastasis Rev 18: 15-30.
7. Bienz, M., H. Clevers (2000) Linking colorectal cancer to Wnt signaling. Cell 103: 311-320.
8. Brabletz, T., K. Herrmann, A. Jung, G. Faller, T. Kirchner (2000) Expression of nuclear beta-catenin and c-myc is correlated with tumor size but not with proliferative activity of colorectal adenomas. Am J Pathol 156: 865-870.
9. Brabletz, T., A. Jung, S. Dag, F. Hlubek, T. Kirchner (1999) β-Catenin regulates the expression of the matrix metalloproteinase-7 in human colorectal cancer. Am J Pathol 155: 1033-1038.
10. Brabletz, T., A. Jung, K. Hermann, K. Gunther, W. Hohenberger, T. Kirchner (1998) Nuclear overexpression of the oncoprotein beta-catenin in colorectal cancer is localized predominantly at the invasion front. Pathol Res Pract 194: 701-704.
11. Brabletz, T., A. Jung, S. Reu, M. Porzner, F. Hlubek, L. Kunz-Schughart, R. Knuechel, T. Kirchner (2001) Variable beta-catenin expression in colorectal cancer indicates a tumor progression driven by the tumor environment. Proc Natl Acad Sci USA 98: 10356-10361.
12. Cavallo, R.A., R.T. Cox, M.M. Moline, J. Roose, G.A. Polevoy, H. Clevers, M. Peifer, A. Bejsovec (1998) Drosophila Tcf and Groucho interact to repress Wingless signalling activity. Nature 395: 604-608.
13. Clevers, H., M. van de Wetering (1997) TCF/LEF factor earn their wings. Trends Genet 13: 485-489.
14. Conacci-Sorrell, M., I. Simcha, T. Ben-Yedidia, J. Blechman, P. Savagner, A. Ben-Ze'ev (2003) Autoregulation of E-cadherin expression by cadherin-cadherin interactions: The roles of beta-catenin signaling, Slug, and MAPK. J Cell Biol 163: 847-857.
15. Crawford, H.C., B.M. Fingleton, L.A. Rudolph-Owen, K.J. Heppner Goss, B. Rubinfeld, P. Polakis, L.M. Matrisian (1999) The metalloproteinase Matrilysin is a target of β-catenin transactivation in intestinal tumors. Oncogene 18: 2883-2891.
16. Dihlmann, S., J. Gebert, A. Siermann, C. Herfarth, M. von Knebel Doeberitz (1999) Dominant negative effect of the APC1309 mutation: A possible explanation for genotype-phenotype correlations in familial adenomatous polyposis. Cancer Res 59: 1857-1860.
17. Eger, A., A. Stockinger, B. Schaffhauser, H. Beug, R. Foisner (2000) Epithelial mesenchymal transition by c-Fos estrogen receptor activation involves nuclear translocation of beta-catenin and upregulation of beta-catenin/lymphoid enhancer binding factor-1 transcriptional activity. J Cell Biol 148: 173-188.
18. Freier, S., O. Weiss, M. Eran, A. Flyvbjerg, R. Dahan, I. Nephesh, T. Safra, E. Shiloni, I. Raz (1999) Expression of the insulin-like growth factors and their receptors in adenocarcinoma of the colon. Gut 44: 704-708.
19. Fujita, M., Y. Furukawa, T. Tsunoda, T. Tanaka, M. Ogawa, Y. Nakamura (2001) Up-regulation of the ectodermal-neural cortex 1 (ENC1)gene, a downstream target of the beta-catenin/T-cell factor complex, in colorectal carcinomas. Cancer Res 61: 7722-7726.
20. Gaire, M., Z. Magbanua, S. McDonnell, L. McNeil, D.H. Lovett, L.M. Matrisian (1994) Structure and expression of the human gene for the matrix metalloproteinase matrilysin. J Biol Chem 269: 2032-2040.
21. Galzie, Z., D.G. Fernig, J.A. Smith, G.J. Poston, A.R. Kinsella (1997) Invasion of human colorectal carcinoma cells is promoted by endogenous basic fibroblast growth factor. Int J Cancer 71: 390-395.
22. Gavert, N., M. Conacci-Sorrell, D. Gast, A. Schneider, P. Altevogt, T. Brabletz, A. Ben-Ze'ev (2005) L1, a novel target of β-catenin signaling, transforms cells and is expressed at the invasive front of colon cancers. J Cell Biol, 165: 633-642.
23. Gradl, D., M. Kuhl, D. Wedlich (1999) The Wnt/ Wg signal transducer beta-catenin controls fibronectin expression. Mol Cell Biol 19: 5576-5587.
24. Groden, J., A. Thliveris, W. Samowitz, M. Carlson, L. Gelbert, H. Albertsen, G. Joslyn, J. Stevens, L. Spirio, M. Robertson, et al. (1991) Identification and characterization of the familial adenomatous polyposis coli gene. Cell 66: 589-600.
25. Hassan, A.B., J.A. Howell (2000) Insulin-like growth factor II supply modifies growth of intestinal adenoma in Apc(Min/+) mice. Cancer Res 60: 1070-1076.
26. Hlubek, F., A. Jung, N. Kotzor, T. Kirchner, T. Brabletz (2001) Expression of the invasion factor laminin γ2 in colorectal carcinomas is regulated by β-catenin. Cancer Res 61: 8089-8093.
27. Hovanes, K., T.W. Li, J.E. Munguia, T. Truong, T. Milovanovic, J. Lawrence Marsh, R.F. Hoicombe, M.L. Waterman (2001) Beta-catenin-sensitive isoforms of lymphoid enhancer factor-1 are selectively expressed in colon cancer. Nat Genet 28: 53-57.
28. Huang, J., N. Papadopoulos, A.J. McKinley, S.M. Farrington, L.J. Curtis, A.H. Wyllie, S. Zheng, J.K. Willson, S.D. Markowitz, P. Morin, K.W. Kinzler, B. Vogelstein, M.G. Dunlop (1996) APC mutations in colorectal tumors with mismatch repair deficiency. Proc Natl Acad Sci USA 93: 9049-9054.
29. Huelsken, J., R. Vogel, B. Erdmann, G. Cotsarelis, W. Birchmeier (2001) Beta-catenin controls hair follicle morphogenesis and stem cell differentiation in the skin. Cell 105: 533-545.
30. Inomata, M., A. Ochiai, S. Akimoto, S. Kitano, S. Hirohashi (1996) Alteration of beta-catenin expression in colonic epithelial cells of familial adenomatous polyposis patients. Cancer Res 56: 2213-2217.
31. Jass, J.R., M. Barker, L. Fraser, M.D. Walsh, V.L. Whitehall, B. Gabrielli, J. Young, B.A. Leggett (2003) APC mutation and tumour budding in colorectal cancer. J Clin Pathol 56: 69-73.
32. Jung, A., M. Schrauder, U. Oswald, C. Knoll, P. Sellberg, R. Palmqvist, G. Niedobitek, T. Brabletz, T. Kirchner (2001) The invasion front of human colorectal adenocarcinomas shows co-localization of nuclear beta-catenin, cyclin D(1), and p16(INK4A) and is a region of low proliferation. Am J Pathol 159: 1613-1617.
33. Kedinger, M., I. Duluc, C. Fritsch, O. Lorentz, M. Plateroti, J.N. Freund (1998) Intestinal epithelial-mesenchymal cell interactions. Ann NY Acad Sci 859: 1-17.
34. Kinzler, K.W., M.C. Nilbert, L.K. Su, B. Vogelstein, T.M. Bryan, D.B. Levy, K.J. Smith, A.C. Preisinger, P. Hedge, D. McKechnie, et al. (1991) Identification of FAP locus genes from chromosome 5q21. Science 253: 661-665.
35. Kirchner, T., T. Brabletz (2000a) Patterning and nuclear beta-catenin expression in the colonic adenoma-carcinoma sequence: Analogies with embryonic gastrulation. Am J Pathol 157: 1113-1121.
36. Kirchner, T., T. Brabletz (2000b) Patterning and nuclear beta-catenin expression in the colonic adenoma-carcinoma sequence: Analogies with embryonic gastrulation. Am J Pathol 157: 1113-1121.
37. Korinek, V., N. Barker, P. Moerer, E. van Donselaar, G. Huls, P.J. Peters, H. Clevers (1998) Depletion of epithelial stem-cell compartments in the small intestine of mice lacking Tcf-4. Nat Genet 19: 379-383.
38. Korinek, V., N. Barker, P.J. Morin, D. van Wichen, R. de Weger, K.W. Kinzler, B. Vogelstein, H. Clevers (1997) Constitutive transcriptional activation by a beta-catenin-Tcf complex in APC-/- colon carcinoma. Science 275: 1784-1787.
39. Lickert, H., C. Domon, G. Huls, C. Wehrle, I. Duluc, H. Clevers, B.I. Meyer, J.N. Freund, R. Kemler (2000) Wnt/(beta)-catenin signaling regulates the expression of the homeobox gene Cdx1 in embryonic intestine. Development 127: 3805-3813.
40. Liotta, L.A., E.C. Kohn (2001) The microenvironment of the tumour-host interface. Nature 411: 375-379.
41. Liotta, L.A., W.G. Stetler-Stevenson (1991) Tumor invasion and metastasis: An imbalance of positive and negative regulation. Cancer Res 51: 5054s-5059s.
42. Liu, D., I. el-Hariry, A.J. Karayiannakis, J. Wilding, R. Chinery, W. Kmiot, P.D. McCrea, W.J. Gullick, M. Pignatelli (1997) Phosphorylation of beta-catenin and epidermal growth factor receptor by intestinal trefoil factor. Lab Invest 77: 557-563.
43. Logan, C.Y., J.R. Miller, M.J. Ferkowicz, D.R. McClay (1999) Nuclear beta-catenin is required to specify vegetal cell fates in the sea urchin embryo. Development 126: 345-357.
44. Mariadason, J.M., M. Bordonaro, F. Aslam, L. Shi, M. Kuraguchi, A. Velcich, L.H. Augenlicht (2001) Down-regulation of beta-catenin TCF signaling is linked to colonic epithelial cell differentiation. Cancer Res 61: 3465-3471.
45. Marotta, A., C. Tan, V. Gray, S. Malik, S. Gallinger, J. Sanghera, B. Dupuis, D. Owen, S. Dedhar, B. Salh (2001) Dysregulation of integrin-linked kinase (ILK) signaling in colonic polyposis. Oncogene 20: 6250-6257.
46. Morali, O.G., V. Delmas, R. Moore, C. Jeanney, J.P. Thiery, L. Larue (2001) IGF-II induces rapid beta-catenin relocation to the nucleus during epithelium to mesenchyme transition. Oncogene 20: 4942-4950.
47. Morin, P.J., A.B. Sparks, V. Korinek, N. Barker, H. Clevers, B. Vogelstein, K.W. Kinzler(1997) Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC. Science 275: 1787-1790.
48. Naishiro, Y., T. Yamada, A.S. Takaoka, R. Hayashi, F. Hasegawa, K. Imai, S. Hirohashi (2001) Restoration of epithelial cell polarity in a colorectal cancer cell line by suppression of beta-catenin/T-cell factor 4-mediated gene transactivation. Cancer Res 61: 2751-2758.
49. Nguyen, B.P., M.C. Ryan, S.G. Gil, W.G. Carter (2000) Deposition of laminin 5 in epidermal wounds regulates integrin signaling and adhesion. Curr Opin Cell Biol 12: 554-562.
50. Nishita, M., M.K. Hashimoto, S. Ogata, M.N. Laurent, N. Ueno, H. Shibuya, K.W. Cho (2000) Interaction between Wnt and TGF-beta signalling pathways during formation of Spemann's organizer. Nature 403: 781-785.
51. Noe, V., B. Fingleton, K. Jacobs, H.C. Crawford, S. Vermeulen, W. Steelant, E. Bruyneel, L.M. Matrisian, M. Mareel (2001) Release of an invasion promoter E-cadherin fragment by matrilysin and stromelysin-1. J Cell Sci 114: 111-118.
52. Novak, A., S.C. Hsu, C. Leung-Hagesteijn, G. Radeva, J. Papkoff, R. Montesano, C. Roskelley, R. Grosschedl, S. Dedhar (1998) Cell adhesion and the integrin-linked kinase regulate the LEF-1 and beta-catenin signaling pathways. Proc Natl Acad Sci USA 95: 4374-4379.
53. Oyama, T., Y. Kanai, A. Ochiai, S. Akimoto, T. Oda, K. Yanagihara, A. Nagafuchi, S. Tsukita, S. Shibamoto, F. Ito, et al. (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.
54. Palmqvist, R., J.N. Rutegard, B. Bozoky, G. Landberg, R. Stenling (2000) Human colorectal cancers with an intact p16/Cyclin D1/pRb pathway have up-regulated p16 expression and decreased proliferation in small invasive tumor clusters. Am J Pathol 157: 1947-1953.
55. Persad, S., A.A. Troussard, T.R. McPhee, D.J. Mulholland, S. Dedhar (2001) Tumor suppressor PTEN inhibits nuclear accumulation of beta-catenin and T cell/lymphoid enhancer factor 1-mediated transcriptional activation. J Cell Biol 153: 1161-1174.
56. Riese, J., X. Yu, A. Munnerlyn, S. Eresh, S.C. Hsu, R. Grosschedl, M. Bienz (1997) LEF-1, a nuclear factor coordinating signaling inputs from wingless and decapentaplegic. Cell 88: 777-787.
57. Rockman, S.P., S.A. Currie, M. Ciavarella, E. Vincan, C. Dow, R.J. Thomas, W.A. Phillips (2001) Id2 is a target of the beta-catenin/TCF pathway in colon carcinoma. J Biol Chem 25: 25.
58. Ropponen, K.M., M.J. Eskelinen, P.K. Lipponen, E. Alhava, V.M. Kosma (1998) Expression of CD44 and variant proteins in human colorectal cancer and its relevance for prognosis. Scand J Gastroenterol 33: 301-309.
59. Rubinfeld, B., B. Souza, I. Albert, O. Muller, S.H. Chamberlain, F.R. Masiarz, S. Munemitsu, P. Polakis (1993) Association of the APC gene product with beta-catenin. Science 262: 1731-1734.
60. Schuhmacher, C., I. Becker, S. Oswald, M.J. Atkinson, H. Nekarda, K.F. Becker, J. Mueller, J.R. Siewert, H. Holler (1999) Loss of immunohistochemical E-cadherin expression in colon cancer is not due to structural gene alterations. Virchows Arch 434: 489-495.
61. Shtutman, M., J. Zhurinsky, I. Simcha, C. Albanese, M. D'Amico, R. Pestell, A. Ben-Ze'ev (1999) The cyclin D1 gene is a target of the beta-catenin/LEF-1 pathway. Proc Natl Acad Sci USA 96: 5522-5527.
62. Sordat, I., F.T. Bosman, G. Dorta, P. Rousselle, D. Aberdam, A.L. Blum, B. Sordat (1998) Differential expression of laminin-5 subunits and integrin receptors in human colorectal neoplasia. J Pathol 185: 44-52.
63. Tetsu, O., F. McCormick (1999) Beta-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 398: 422-426.
64. Thiery, J.P. (2002) Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2: 442-454.
65. Wielenga, V.J., R. Smits, V. Korinek, L. Smit, M. Kielman, R. Fodde, H. Clevers, S.T. Pals (1999) Expression of CD44 in Ape and Tcf mutant mice implies regulation by the WNT pathway. Am J Pathol 154: 515-523.
66. Woodhouse, E.C., R.F. Chuaqui, L.A. Liotta (1997) General mechanisms of metastasis. Cancer 80: 1529-1537.
67. Zhang, T., T. Otevrel, Z. Gao, S.M. Ehrlich, J.Z. Fields, B.M. Boman (2001a) Evidence that APC regulates survivin expression: A possible mechanism contributing to the stem cell origin of colon cancer. Cancer Res 61: 8664-8667.
68. Zhang, X., J.P. Gaspard, D.C. Chung (2001b) Regulation of vascular endothelial growth factor by the WNT and K-ras pathways in colonic neoplasia. Cancer Res 61: 6050-6054.