Molecular mechanisms of hepatic metastasis in colorectal cancer

Journal of Surgical Oncology

Volumn 92, Issue 4, 2005, Pages 347-359

  Rudmik, L R ^a,b   Magliocco, A M ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b NONE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

2,4 THIAZOLIDINEDIONE DERIVATIVE; ANTIDIABETIC AGENT; ATM PROTEIN; BETA INTERFERON; BETA1 INTEGRIN; BRCA1 PROTEIN; BUTYRIC ACID; CHEMOKINE RECEPTOR CXCR4; DEATH RECEPTOR 4; DEATH RECEPTOR 5; DNA; HISTONE DEACETYLASE INHIBITOR; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERCELLULAR ADHESION MOLECULE 1; MATRILYSIN; MATRIX METALLOPROTEINASE; MITOGEN ACTIVATED PROTEIN KINASE; OSTEOPONTIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; ROSIGLITAZONE; SCATTER FACTOR; SMALL INTERFERING RNA; SOMATOMEDIN RECEPTOR; TRICHOSTATIN A; TROGLITAZONE; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UROKINASE; UROKINASE RECEPTOR; VASCULOTROPIN;

ANGIOGENESIS; APOPTOSIS; CANCER INVASION; CANCER RISK; CELL ADHESION; CELL DIFFERENTIATION; CELL SURVIVAL; COLORECTAL CANCER; CPG ISLAND; DNA METHYLATION; DRG 1 GENE; DRUG TARGETING; ENZYME ACTIVATION; ENZYME INHIBITION; EXTRACELLULAR MATRIX; GENE; GENE EXPRESSION REGULATION; HUMAN; IMMUNE SYSTEM; LIVER CARCINOGENESIS; LIVER METASTASIS; METASTASIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; REVIEW;

EID: 28844498773     PISSN: 00224790     EISSN: None     Source Type: Journal    
DOI: 10.1002/jso.20393     Document Type: Review

References (122)

1. Jemal A, Tiwari RC, Murray T, et al.: Cancer statistics, 2004. CA Cancer J Clin 2004;54:8-29.
2. Zucker S, Vacirca J: Role of matrix metalloproteinases (MMPs) in colorectal cancer. Cancer Metastasis Rev 2004;23:101-117.
3. Zucker S: A critical appraisal of the role of proteolytic enzymes in cancer invasion: Emphasis on tumor surface proteinases. Cancer Invest 1988;6:219-231.
4. Nagase H, Woessner JF, Jr.: Matrix metalloproteinases. J Biol Chem 1999;274:21491-21494.
5. Werb Z: ECM and cell surface proteolysis: Regulating cellular ecology. Cell 1997;91:439-442.
6. Sternlicht MD, Werb Z: How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol 2001;17:463-516.
7. Yoshimoto M, Itoh F, Yamamoto H, et al.: Expression of MMP-7(PUMP-1) mRNA in human colorectal cancers. Int J Cancer 1993;54:614-618.
8. Newell KJ, Witty JP, Rodgers WH, et al.: Expression and localization of matrix-degrading metalloproteinases during colorectal tumorigenesis. Mol Carcinog 1994;10:199-206.
9. Nagashima Y, Hasegawa S, Koshikawa N, et al.: Expression of matrilysin in vascular endothelial cells adjacent to matrilysin-producing tumors. Int J Cancer 1997;72:441-445.
10. Ishikawa T, Ichikawa Y, Mitsuhashi M, et al.: Matrilysin is associated with progression of colorectal tumor. Cancer Lett 1996;107:5-10.
11. Adachi Y, Yamamoto H, Itoh F, et al.: Contribution of matrilysin (MMP-7) to the metastatic pathway of human colorectal cancers. Gut 1999;45:252-258.
12. Kioi M, Yamamoto K, Higashi S, et al.: Matrilysin (MMP-7) induces homotypic adhesion of human colon cancer cells and enhances their metastatic potential in nude mouse model. Oncogene 2003;22:8662-8670.
13. Crowley CW, Cohen RL, Lucas BK, et al.: Prevention of metastasis by inhibition of the urokinase receptor. Proc Natl Acad Sci USA 1993;90:5021-5025.
14. Xing RH, Rabbani SA: Overexpression of urokinase receptor in breast cancer cells results in increased tumor invasion, growth and metastasis. Int J Cancer 1996;67:423-429.
15. Dano K, Romer J, Nielsen BS, et al.: Cancer invasion and tissue remodeling-Cooperation of protease systems and cell types. Apmis 1999;107:120-127.
16. Ossowski L, Aguirre-Ghiso JA: Urokinase receptor and integrin partnership: Coordination of signaling for cell adhesion, migration and growth. Curr Opin Cell Biol 2000;12:613-620.
17. Ahmed N, Oliva K, Wang Y, et al.: Downregulation of urokinase plasminogen activator receptor expression inhibits Erk signalling with concomitant suppression of invasiveness due to loss of uPAR-beta1 integrin complex in colon cancer cells. Br J Cancer 2003;89:374-384.
18. Ganesh S, Sier CF, Heerding MM, et al.: Urokinase receptor and colorectal cancer survival. Lancet 1994;344:401-402.
19. Moriyama T, Kataoka H, Hamasuna R, et al.: Simultaneous up-regulation of urokinase-type plasminogen activator (uPA) and uPA receptor by hepatocyte growth factor/scatter factor in human glioma cells. Clin Exp Metastasis 1999;17:873-879.
20. Lengyel E, Wang H, Gum R, et al.: Elevated urokinase-type plasminogen activator receptor expression in a colon cancer cell line is due to a constitutively activated extracellular signal-regulated kinase-1-dependent signaling cascade. Oncogene 1997;14:2563-2573.
21. Allgayer H, Wang H, Gallick GE, et al.: Transcriptional induction of the urokinase receptor gene by a constitutively active Src. Requirement of an upstream motif (-152/-135) bound with Sp1. J Biol Chem 1999;274:18428-18437.
22. Ahmed N, Oliva K, Wang Y, et al.: Proteomic profiling of proteins associated with urokinase plasminogen activator receptor in a colon cancer cell line using an antisense approach. Proteomics 2003;3:288-298.
23. Guo YS, Hellmich MR, Wen XD, et al.: Activator protein-1 transcription factor mediates bombesin-stimulated cyclooxygenase-2 expression in intestinal epithelial cells. J Biol Chem 2001;276:22941-22947.
24. Kitayama J, Nagawa H, Tsuno N, et al.: Laminin mediates tethering and spreading of colon cancer cells in physiological shear flow. Br J Cancer 1999;80:1927-1934.
25. Denhardt DT, Noda M, O'Regan AW, et al.: Osteopontin as a means to cope with environmental insults: Regulation of inflammation, tissue remodeling, and cell survival. J Clin Invest 2001;107:1055-1061.
26. Tuck AB, Elliott BE, Hota C, et al.: Osteopontin-induced, integrin-dependent migration of human mammary epithelial cells involves activation of the hepatocyte growth factor rece-ptor (Met). J Cell Biochem 2000;78:465-475.
27. Sodek J, Ganss B, McKee MD: Osteopontin. Crit Rev Oral Biol Med 2000;11:279-303.
28. Furger KA, Menon RK, Tuckl AB, et al.: The functional and clinical roles of osteopontin in cancer and metastasis. Curr Mol Med 2001;1:621-632.
29. Agrawal D, Chen T, Irby R, et al.: Osteopontin identified as colon cancer tumor progression marker. C R Biol 2003;326:1041-1043.
30. Yeatman TJ, Chambers AF: Osteopontin and colon cancer progression. Clin Exp Metastasis 2003;20:85-90.
31. El-Tanani MK, Barraclough R, Wilkinson MC, et al.: Regulatory region of metastasis-inducing DNA is the binding site for T cell factor-4. Oncogene 2001;20:1793-1797.
32. Tuck AB, Chambers AF: The role of osteopontin in breast cancer: Clinical and experimental studies. J Mammary Gland Biol Neoplasia 2001;6:419-429.
33. Tuck AB, Arsenault DM, O'Malley FP, et al.: Osteopontin induces increased invasiveness and plasminogen activator expression of human mammary epithelial cells. Oncogene 1999;18:4237-4246.
34. Tuck AB, Hota C, Chambers AF: Osteopontin(OPN)-induced increase in human mammary epithelial cell invasiveness is urokinase (uPA)-dependent. Breast Cancer Res Treat 2001;70:197-204.
35. Termuhlen PM, Curley SA, Talamonti MS, et al.: Site-specific differences in pp60c-src activity in human colorectal metastases. J Surg Res 1993;54:293-298.
36. Talamonti MS, Roh MS, Curley SA, et al.: Increase in activity and level of pp60c-src in progressive stages of human colorectal cancer. J Clin Invest 1993;91:53-60.
37. Cartwright CA, Kamps MP, Meisler AI, et al.: pp60c-src activation in human colon carcinoma. J Clin Invest 1989;83:2025-2033.
38. 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.
39. Cartwright CA, Coad CA, Egbert BM: Elevated c-Src tyrosine kinase activity in premalignant epithelia of ulcerative colitis. J Clin Invest 1994;93:509-515.
40. Jones RJ, Avizienyte E, Wyke AW, et al.: Elevated c-Src is linked to altered cell-matrix adhesion rather than proliferation in KM12C human colorectal cancer cells. Br J Cancer 2002;87:1128-1135.
41. Avizienyte E, Wyke AW, Jones RJ, et al.: Src-induced deregulation of E-cadherin in colon cancer cells requires integrin signalling. Nat Cell Biol 2002;4:632-638.
42. Brunton VG, Ozanne BW, Paraskeva C, et al.: A role for epidermal growth factor receptor, c-Src and focal adhesion kinase in an in vitro model for the progression of colon cancer. Oncogene 1997;14:283-293.
43. Wagner HE, Toth CA, Steele GD, Jr., et al.: Metastatic potential of human colon cancer cell lines: Relationship to cellular differentiation and carcinoembryonic antigen production. Clin Exp Metastasis 1992;10:25-31.
44. Jessup JM, Petrick AT, Toth CA, et al.: Carcinoembryonic antigen: Enhancement of liver colonisation through retention of human colorectal carcinoma cells. Br J Cancer 1993;67:464-470.
45. Benchimol S, Fuks A, Jothy S, et al.: Carcinoembryonic antigen, a human tumor marker, functions as an intercellular adhesion molecule. Cell 1989;57:327-334.
46. Thomas P, Gangopadhyay A, Steele G Jr., et al.: The effect of transfection of the CEA gene on the metastatic behavior of the human colorectal cancer cell line MIP-101. Cancer Lett 1995;92:59-66.
47. Hashino J, Fukuda Y, Oikawa S, et al.: Metastatic potential of human colorectal carcinoma SW1222 cells transfected with cDNA encoding carcinoembryonic antigen. Clin Exp Metastasis 1994;12:324-328.
48. Gangopadhyay A, Lazure DA, Thomas P: Adhesion of colorectal carcinoma cells to the endothelium is mediated by cytokines from CEA stimulated Kupffer cells. Clin Exp Metastasis 1998;16:703-712.
49. Folkman J: The role of angiogenesis in tumor growth. Semin Cancer Biol 1992;3:65-71.
50. Keck PJ, Hauser SD, Krivi G, et al.: Vascular permeability factor, an endothelial cell mitogen related to PDGF. Science 1989;246:1309-1312.
51. Leung DW, Cachianes G, Kuang WJ, et al.: Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 1989;246:1306-1309.
52. Plouet J, Schilling J, Gospodarowicz D: Isolation and characterization of a newly identified endothelial cell mitogen produced by AtT-20 cells. EMBO J 1989;8:3801-3806.
53. Senger DR, Galli SJ, Dvorak AM, et al.: Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science 1983;219:983-985.
54. Dvorak HF, Brown LF, Detmar M, et al.: Vascular permeability factor/vascular endothelial growth factor, microvascular hyperpermeability, and angiogenesis. Am J Pathol 1995;146:1029-1039.
55. Nicosia RF: What is the role of vascular endothelial growth factor-related molecules in tumor angiogenesis? Am J Pathol 1998;153:11-16.
56. Tischer E, Mitchell R, Hartman T, et al.: The human gene for vascular endothelial growth factor. Multiple protein forms are encoded through alternative exon splicing. J Biol Chem 1991;266:11947-11954.
57. Peters KG, De Vries C, Williams LT: Vascular endothelial growth factor receptor expression during embryogenesis and tissue repair suggests a role in endothelial differentiation and blood vessel growth. Proc Natl Acad Sci USA 1993;90:8915-8919.
58. Veikkola T, Karkkainen M, Claesson-Welsh L, et al.: Regulation of angiogenesis via vascular endothelial growth factor receptors. Cancer Res 2000;60:203-212.
59. Takahashi Y, Kitadai Y, Bucana CD, et al.: Expression of vascular endothelial growth factor and its receptor, KDR, correlates with vascularity, metastasis, and proliferation of human colon cancer. Cancer Res 1995;55:3964-3968.
60. Kang SM, Maeda K, Chung YS, et al.: Vascular endothelial growth factor expression correlates with hematogenous metastasis and prognosis in colorectal carcinoma. Oncologic Reports 1997;4:381-384.
61. Ishigami SI, Arii S, Furutani M, et al.: Predictive value of vascular endothelial growth factor (VEGF) in metastasis and prognosis of human colorectal cancer. Br J Cancer 1998;78:1379-1384.
62. Takebayashi Y, Aklyama S, Yamada K, et al.: Angiogenesis as an unfavorable prognostic factor in human colorectal carcinoma. Cancer 1996;78:226-231.
63. Vermeulen PB, Van den Eynden GG, Huget P, et al.: Prospective study of intratumoral microvessel density, p53 expression and survival in colorectal cancer. Br J Cancer 1999;79:316-322.
64. Berney CR, Yang JL, Fisher RJ, et al.: Vascular endothelial growth factor expression is reduced in liver metastasis from colorectal cancer and correlates with urokinase-type plasminogen activator. Anticancer Res 1998;18:973-977.
65. Jung YD, Ahmad SA, Akagi Y, et al.: Role of the tumor microenvironment in mediating response to anti-angiogenic therapy. Cancer Metastasis Rev 2000;19:147-157.
66. Baker EA, Bergin FG, Leaper DJ: Plasminogen activator system, vascular endothelial growth factor, and colorectal cancer progression. MoI Pathol 2000;53:307-312.
67. Konno H, Abe J, Kaneko T, et al.: Urokinase receptor and vascular endothelial growth factor are synergistically associated with the liver metastasis of colorectal cancer. Jpn J Cancer Res 2001;92:516-523.
68. Takahashi Y, Bucana CD, Liu W, et al.: Platelet-derived endothelial cell growth factor in human colon cancer angiogenesis: Role of infiltrating cells. J Natl Cancer Inst 1996;88:1146-1151.
69. Amaya H, Tanigawa N, Lu C, et al.: Association of vascular endothelial growth factor expression with tumor angiogenesis, survival and thymidine phosphorylase/platelet-derived endothelial cell growth factor expression in human colorectal cancer. Cancer Lett 1997;119:227-235.
70. Beckner ME: Factors promoting tumor angiogenesis. Cancer Invest 1999;17:594-623.
71. Takebayashi Y, Akiyama S, Akiba S, et al.: Clinicopathologic and prognostic significance of an angiogenic factor, thymidine phosphorylase, in human colorectal carcinoma. J Natl Cancer Inst 1996;88:1110-1117.
72. Saito S, Tsuno N, Nagawa H, et al.: Expression of platelet-derived endothelial cell growth factor correlates with good prognosis in patients with colorectal carcinoma. Cancer 2000;88:42-49.
73. Wiley SR, Schooley K, Smolak PJ, et al.: Identification and characterization of a new member of the TNF family that induces apoptosis. Immunity 1995;3:673-682.
74. Pitti RM, Marsters SA, Ruppert S, et al.: Induction of apoptosis by Apo-2 ligand, a new member of the tumor necrosis factor cytokine family. J Biol Chem 1996;271:12687-12690.
75. Nagata S: Apoptosis by death factor. Cell 1997;88:355-365.
76. Kashii Y, Giorda R, Herberman RB, et al.: Constitutive expression and role of the TNF family ligands in apoptotic killing of tumor cells by human NK cells. J Immunol 1999;163:5358-5366.
77. Johnsen AC, Haux J, Steinkjer B, et al.: Regulation of APO-2 ligand/trail expression in NK cells-involvement in NK cell-mediated cytotoxicity. Cytokine 1999;11:664-672.
78. Kayagaki N, Yamaguchi N, Nakayama M, et al.: Expression and function of TNF-related apoptosis-inducing ligand on murine activated NK cells. J Immunol 1999;163:1906-1913.
79. Takeda K, Hayakawa Y, Smyth MJ, et al.: Involvement of tumor necrosis factor-related apoptosis-inducing ligand in surveillance of tumor metastasis by liver natural killer cells. Nat Med 2001;7:94-100.
80. Kayagaki N, Yamaguchi N, Nakayama M, et al.: Type I interferons (IFNs) regulate tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) expression on human T cells: A novel mechanism for the antitumor effects of type I IFNs. J Exp Med 1999;189:1451-1460.
81. Pan G, O'Rourke K, Chinnaiyan AM, et al.: The receptor for the cytotoxic ligand TRAIL. Science 1997;276:111-113.
82. Walczak H, Degli-Esposti MA, Johnson RS, et al.: TRAIL-R2: A novel apoptosis-mediating receptor for TRAIL. EMBO J 1997;16:5386-5397.
83. Degli-Esposti MA, Dougall WC, Smolak PJ, et al.: The novel receptor TRAIL-R4 induces NF-kappaB and protects against TRAIL-mediated apoptosis, yet retains an incomplete death domain. Immunity 1997;7:813-820.
84. Pan G, Ni J, Wei YF, et al.: An antagonist decoy receptor and a death domain-containing receptor for TRAIL. Science 1997;277:815-818.
85. Sheridan JP, Marsters SA, Pitti RM, et al.: Control of TRAIL-induced apoptosis by a family of signaling and decoy receptors. Science 1997;277:818-821.
86. Strater J, Hinz U, Walczak H, et al.: Expression of TRAIL and TRAIL receptors in colon carcinoma: TRAIL-R1 is an independent prognostic parameter. Clin Cancer Res 2002;8:3734-3740.
87. Chaudhary PM, Eby M, Jasmin A, et al.: Death receptor 5, a new member of the TNFR family, and DR4 induce FADD-dependent apoptosis and activate the NF-kappaB pathway. Immunity 1997;7:821-830.
88. Cretney E, Takeda K, Yagita H, et al.: Increased susceptibility to tumor initiation and metastasis in TNF-related apoptosis-inducing ligand-deficient mice. J Immunol 2002;168:1356-1361.
89. Kondo H, Tanaka N, Naomoto Y, et al.: Antitumor effect of recombinant human interferon-beta and interferon-gamma in combination against human colon cancer cell line in vitro and in nude mice. Jpn J Cancer Res 1987;78:1258-1265.
90. Toth CA, Thomas P: The effect of interferon treatment on 14 human colorectal cancer cell lines: Growth and carcinoembryonic antigen secretion in vitro. J Interferon Res 1990;10:579-588.
91. Zimmer R, Thomas P: Expression profiling and interferon-beta regulation of liver metastases in colorectal cancer cells. Clin Exp Metastasis 2002;19:541-550.
92. Toth CA, Thomas P: Type I interferon resistance in a colorectal cancer cell line is associated with a more aggressive phenotype in vivo. Br J Cancer 1992;65:365-368.
93. Brune B, Lapetina EG: Protein thiol modification of glyceraldehyde-3- phosphate dehydrogenase as a target for nitric oxide signaling. Genet Eng (NY) 1995;17:149-164.
94. Xie K, Bielenberg D, Huang S, et al.: Abrogation of tumorigenicity and metastasis of murine and human tumor cells by transfection with the murine IFN-beta gene: Possible role of nitric oxide. Clin Cancer Res 1997;3:2283-2294.
95. Jessup JM, Battle P, Waller H, et al.: Reactive nitrogen and oxygen radicals formed during hepatic ischemia-reperfusion kill weakly metastatic colorectal cancer cells. Cancer Res 1999;59:1825-1829.
96. Edmiston KH, Shoji Y, Mizoi T, et al.: Role of nitric oxide and superoxide anion in elimination of low metastatic human colorectal carcinomas by unstimulated hepatic sinusoidal endothelial cells. Cancer Res 1998;58:1524-1531.
97. Hakam A, Yeatman TJ, Lu L, et al.: Expression of insulin-like growth factor-1 receptor in human colorectal cancer. Hum Pathol 1999;30:1128-1133.
98. Berezney R, Coffey DS: Identification of a nuclear protein matrix. Biochem Biophys Res Commun 1974;60:1410-1417.
99. Fey EG, Bangs P, Sparks C, et al.: The nuclear matrix: Defining structural and functional roles. Crit Rev Eukaryot Gene Expr 1991;1:127-143.
100. Fey EG, Penman S: Nuclear matrix proteins reflect cell type of origin in cultured human cells. Proc Natl Acad Sci USA 1988;85:121-125.
101. Brunagel G, Schoen RE, Bauer AJ, et al.: Nuclear matrix protein alterations associated with colon cancer metastasis to the liver. Clin Cancer Res 2002;8:3039-3045.
102. Jordan NJ, Kolios G, Abbot SE, et al.: Expression of functional CXCR4 chemokine receptors on human colonic epithelial cells. J Clin Invest 1999;104:1061-1069.
103. Taichman RS, Cooper C, Keller ET, et al.: Use of the stromal cell-derived factor-1/CXCR4 pathway in prostate cancer metastasis to bone. Cancer Res 2002;62:1832-1837.
104. Scotton CJ, Wilson JL, Milliken D, et al.: Epithelial cancer cell migration: A role for chemokine receptors? Cancer Res 2001;61:4961-4965.
105. Muller A, Homey B, Soto H, et al.: Involvement of chemokine receptors in breast cancer metastasis. Nature 2001;410:50-56.
106. Koshiba T, Hosotani R, Miyamoto Y, et al.: Expression of stromal cell-derived factor 1 and CXCR4 ligand receptor system in pancreatic cancer: A possible role for tumor progression. Clin Cancer Res 2000;6:3530-3535.
107. Ben-Baruch A, Michiel DF, Oppenheim JJ: Signals and receptors involved in recruitment of inflammatory cells. J Biol Chem 1995;270:11703-11706.
108. Zeelenberg IS, Ruuls-Van Stalle L, et al.: The chemokine receptor CXCR4 is required for outgrowth of colon carcinoma micrometastases. Cancer Res 2003;63:3833-3839.
109. Michalopoulos GK, DeFrances MC: Liver regeneration. Science 1997;276:60-66.
110. Vigna E, Naldini L, Tamagnone L, et al.: Hepatocyte growth factor and its receptor, the tyrosine kinase encoded by the c-MET proto-oncogene. Cell Mol Biol (Noisy-le-grand) 1994;40:597-604.
111. Noji S, Tashiro K, Koyama E, et al.: Expression of hepatocyte growth factor gene in endothelial and Kupffer cells of damaged rat livers, as revealed by in situ hybridization. Biochem Biophys Res Commun 1990;173:42-47.
112. Di Renzo MF, Olivero M, Giacomini A, et al.: Overexpression and amplification of the met/HGF receptor gene during the progression of colorectal cancer. Clin Cancer Res 1995;1:147-154.
113. Singh RK, Tsan R, Radinsky R: Influence of the host microenvironment on the clonal selection of human colon carcinoma cells during primary tumor growth and metastasis. Clin Exp Metastasis 1997;15:140-150.
114. Herynk MH, Stoeltzing O, Reinmuth N, et al.: Down-regulation of c-Met inhibits growth in the liver of human colorectal carcinoma cells. Cancer Res 2003;63:2990-2996.
115. 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.
116. Hiscox S, Jiang WG: Hepatocyte growth factor/scatter factor disrupts epithelial tumour cell-cell adhesion: Involvement of beta-catenin. Anticancer Res 1999;19:509-517.
117. Herynk MH, Tsan R, Radinsky R, et al.: Activation of c-Met in colorectal carcinoma cells leads to constitutive association of tyrosine-phosphorylated beta-catenin. Clin Exp Metastasis 2003;20:291-300.
118. van Beizen N, Dinjens WN, Diesveld MP, et al.: A novel gene which is up-regulated during colon epithelial cell differentiation and down-regulated in colorectal neoplasms. Lab Invest 1997;77:85-92.
119. Guan RJ, Ford HL, Fu Y, et al.: Drg-1 as a differentiation-related, putative metastatic suppressor gene in human colon cancer. Cancer Res 2000;60:749-755.
120. Mangelsdorf DJ, Thummel C, Beato M, et al.: The nuclear receptor superfamily: The second decade. Cell 1995;83:835-839.
121. Jones PA, Laird PW: Cancer epigenetics comes of age. Nat Genet 1999;21:163-167.
122. Gardiner-Garden M, Frommer M: CpG islands in vertebrate genomes. J Mol Biol 1987;196:261-282.