Promoter methylation in the genesis of gastrointestinal Cancer

Yonsei Medical Journal

Volumn 50, Issue 3, 2009, Pages 309-321

  Boland, Clement Richard ^a   Shin, Sung Kwan ^a,b   Goel, Ajay ^a  

^a BAYLOR UNIVERSITY MEDICAL CENTER   (United States)

^b Yonsei University College of Medicine   (South Korea)

Author keywords

Chromosomal instability; CIMP; Colorectal cancer; Hepatocellular carcinoma; HNPCC; Lynch syndrome; Microsatellite instability; Promoter methylation

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; APC PROTEIN; AZACITIDINE; B RAF KINASE; BETA CATENIN; BIOLOGICAL MARKER; EPIGALLOCATECHIN GALLATE; FLUOROURACIL; GENE PRODUCT; K RAS PROTEIN; METHYLATED DNA PROTEIN CYSTEINE METHYLTRANSFERASE; NETRIN 1 RECEPTOR; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN DCC; PROTEIN HIC1; PROTEIN MINT 1; PROTEIN MINT 2; PROTEIN MINT 31; PROTEIN MLH1; PROTEIN P16; PROTEIN P53; PROTEIN RAR BETA 2; PROTEIN UNC5C; TISSUE INHIBITOR OF METALLOPROTEINASE 3; TRANSCRIPTION FACTOR RUNX3; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; CANCER INHIBITION; CARCINOGENESIS; CHROMOSOMAL INSTABILITY; CHROMOSOME REARRANGEMENT; COLORECTAL CANCER; CPG ISLAND; DIGESTIVE SYSTEM CANCER; DNA METHYLATION; DRUG POTENCY; EPIGENETICS; FAMILIAL CANCER; GENE AMPLIFICATION; GENE DELETION; GENE LOCUS; GENE MUTATION; GENE SEQUENCE; GENE SILENCING; GENETIC ASSOCIATION; GENETIC HETEROGENEITY; HUMAN; JC VIRUS; LIVER CELL CARCINOMA; MICROSATELLITE INSTABILITY; MISMATCH REPAIR; NONHUMAN; PHENOTYPE; PROMOTER REGION; REVIEW; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR GENE;

COLORECTAL NEOPLASMS; DNA METHYLATION; GASTROINTESTINAL NEOPLASMS; HUMANS; MICROSATELLITE INSTABILITY; PROMOTER REGIONS, GENETIC;

EID: 67651173046     PISSN: 05135796     EISSN: None     Source Type: Journal    
DOI: 10.3349/ymj.2009.50.3.309     Document Type: Review

References (80)

1. Vogelstein B, Fearon ER, Kern SE, Hamilton SR, Preisinger AC, Nakamura Y, et al. Allelotype of colorectal carcinomas. Science 1989;244:207-11.
2. Goel A, Arnold CN, Niedzwiecki D, Chang DK, Ricciardiello L, Carethers JM, et al. Characterization of sporadic colon cancer by patterns of genomic instability. Cancer Res 2003;63:1608-14.
3. Li R, Sonik A, Stindl R, Rasnick D, Duesberg P. Aneuploidy vs. gene mutation hypothesis of cancer: recent study claims mutation but is found to support aneuploidy. Proc Natl Acad Sci U S A 2000;97:3236-41.
4. Lengauer C, Kinzler KW, Vogelstein B. Genetic instability in colorectal cancers. Nature 1997;386:623-7.
5. Nishida N, Nagasaka T, Kashiwagi K, Boland CR, Goel A. High copy amplification of the Aurora-A gene is associated with chromosomal instability phenotype in human colorectal cancers. Cancer Biol Ther 2007;6:525-33.
6. Rodriguez J, Frigola J, Vendrell E, Risques RA, Fraga MF, Morales C, et al. Chromosomal instability correlates with genome-wide DNA demethylation in human primary colorectal cancers. Cancer Res 2006;66:8462-9468.
7. Sieber OM, Heinimann K, Gorman P, Lamlum H, Crabtree M, Simpson CA, et al. Analysis of chromosomal instability in human colorectal adenomas with two mutational hits at APC. Proc Natl Acad Sci U S A 2002;99:16910-5.
8. Boland CR, Komarova NL, Goel A. Chromosomal instability and cancer: not just one CINgle mechanism. Gut 2009;58:163-4.
9. Muleris M, Chalastanis A, Meyer N, Lae M, Dutrillaux B, Sastre-Garau X, et al. Chromosomal instability in near-diploid colorectal cancer: a link between numbers and structure. PLoS ONE 2008;3: e1632.
10. Duval A, Reperant M, Compoint A, Seruca R, Ranzani GN, Iacopetta B, et al. Target gene mutation profile differs between gastrointestinal and endometrial tumors with mismatch repair deficiency. Cancer Res 2002;62:1609-12.
11. Markowitz S, Wang J, Myeroff L, Parsons R, Sun L, Lutterbaugh J, et al. Inactivation of the type II TGF-beta receptor in colon cancer cells with microsatellite instability. Science 1995;268:1336-8.
12. Rampino N, Yamamoto H, Ionov Y, Li Y, Sawai H, Reed JC, et al. Somatic frameshift mutations in the BAX gene in colon cancers of the microsatellite mutator phenotype. Science 1997;275:967-9.
13. Grady WM, Carethers JM. Genomic and epigenetic instability in colorectal cancer pathogenesis. Gastroenterology 2008;135:1079-99.
14. Toyota M, Ahuja N, Ohe-Toyota M, Herman JG, Baylin SB, Issa JP. CpG island methylator phenotype in colorectal cancer. Proc Natl Acad Sci U S A 1999;96:8681-6.
15. Herman JG, Baylin SB. Gene silencing in cancer in association with promoter hypermethylation. N Engl J Med 2003;349:2042-54.
16. Yamashita K, Dai T, Dai Y, Yamamoto F, Perucho M. Genetics supersedes epigenetics in colon cancer phenotype. Cancer Cell 2003;4:121-31.
17. Ahuja N, Mohan AL, Li Q, Stolker JM, Herman JG, Hamilton SR, et al. Association between CpG island methylation and microsatellite instability in colorectal cancer. Cancer Res 1997;57:3370-4.
18. Kane MF, Loda M, Gaida GM, Lipman J, Mishra R, Goldman H, et al. Methylation of the hMLH1 promoter correlates with lack of expression of hMLH1 in sporadic colon tumors and mismatch repair-defective human tumor cell lines. Cancer Res 1997;57:808-11.
19. Weisenberger DJ, Siegmund KD, Campan M, Young J, Long TI, Faasse MA, et al. CpG island methylator phenotype underlies sporadic microsatellite instability and is tightly associated with BRAF mutation in colorectal cancer. Nat Genet 2006;38:787-93.
20. Eads CA, Danenberg KD, Kawakami K, Saltz LB, Danenberg PV, Laird PW. CpG island hypermethylation in human colorectal tumors is not associated with DNA methyltransferase overexpression. Cancer Res 1999;59:2302-6.
21. Samowitz WS, Albertsen H, Herrick J, Levin TR, Sweeney C, Murtaugh MA, et al. Evaluation of a large, population-based sample supports a CpG island methylator phenotype in colon cancer. Gastroenterology 2005;129:837-45.
22. Goel A, Nagasaka T, Arnold CN, Inoue T, Hamilton C, Niedzwiecki D, et al. The CpG island methylator phenotype and chromosomal instability are inversely correlated in sporadic colorectal cancer. Gastroenterology 2007;132:127-38.
23. Ogino S, Odze RD, Kawasaki T, Brahmandam M, Kirkner GJ, Laird PW, et al. Correlation of pathologic features with CpG island methylator phenotype (CIMP) by quantitative DNA methylation analysis in colorectal carcinoma. Am J Surg Pathol 2006;30:1175-83.
24. Tuupanen S, Karhu A, Järvinen H, Mecklin JP, Launonen V, Aaltonen LA. No evidence for dual role of loss of heterozygosity in hereditary non-polyposis colorectal cancer. Oncogene 2007;26: 2513-7.
25. Kaz A, Kim YH, Dzieciatkowski S, Lynch H, Watson P, Kay Washington, et al. Evidence for the role of aberrant DNA methylation in the pathogenesis of Lynch syndrome adenomas. Int J Cancer 2007;120:1922-9.
26. Wood LD, Parsons DW, Jones S, Lin J, Sjöblom T, Leary RJ, et al. The genomic landscapes of human breast and colorectal cancers. Science 2007;318:1108-13.
27. Nagasaka T, Goel A, Notohara K, Takahata T, Sasamoto H, Uchida T, et al. Methylation pattern of the O6-methylguanine-DNA methyltransferase gene in colon during progressive colorectal tumorigenesis. Int J Cancer 2008;122:2429-36.
28. Forrester K, Almoguera C, Han K, Grizzle WE, Perucho M. Detection of high incidence of K-ras oncogenes during human colon tumorigenesis. Nature 1987;327:298-303.
29. Bos JL, Fearon ER, Hamilton SR, Verlaan-de Vries M, van Boom JH, van der Eb AJ, et al. Prevalence of ras gene mutations in human colorectal cancers. Nature 1987;327:293-7.
30. Davies H, Bignell GR, Cox C, Stephens P, Edkins S, Clegg S, et al. Mutations of the BRAF gene in human cancer. Nature 2002; 417:949-54.
31. Nagasaka T, Koi M, Kloor M, Gebert J, Vilkin A, Nishida N, et al. Mutations in both KRAS and BRAF may contribute to the methylator phenotype in colon cancer. Gastroenterology 2008; 134:1950-60, 1960.e1.
32. Aaltonen LA, Peltomäki P, Mecklin JP, Järvinen H, Jass JR, Green JS, et al. Replication errors in benign and malignant tumors from hereditary nonpolyposis colorectal cancer patients. Cancer Res 1994;54:1645-8.
33. Tannergård P, Liu T, Weger A, Nordenskjöld M, Lindblom A. Tumorigenesis in colorectal tumors from patients with hereditary non-polyposis colorectal cancer. Hum Genet 1997;101:51-5.
34. Esteller M, Fraga MF, Guo M, Garcia-Foncillas J, Hedenfalk I, Godwin AK, et al. DNA methylation patterns in hereditary human cancers mimic sporadic tumorigenesis. Hum Mol Genet 2001;10: 3001-7.
35. Sanchez de Abajo A, de la Hoya M, van Puijenbroek M, Godino J, Díaz-Rubio E, Morreau H, et al. Dual role of LOH at MMR loci in hereditary non-polyposis colorectal cancer? Oncogene 2006;25: 2124-30.
36. Kim WS, Son HJ, Park JO, Song SY, Park C. Promoter methylation and down-regulation of DAPK is associated with gastric atrophy. Int J Mol Med 2003;12:827-30.
37. Garcia-Manero G, Bueso-Ramos C, Daniel J, Williamson J, Kantarjian HM, Issa JP. DNA methylation patterns at relapse in adult acute lymphocytic leukemia. Clin Cancer Res 2002;8:1897-903.
38. Shen L, Ahuja N, Shen Y, Habib NA, Toyota M, Rashid A, et al. DNA methylation and environmental exposures in human hepatocellular carcinoma. J Natl Cancer Inst 2002;94:755-61.
39. Nishida N, Nishimura T, Nagasaka T, Ikai I, Goel A, Boland CR. Extensive methylation is associated with beta-catenin mutations in hepatocellular carcinoma: evidence for two distinct pathways of human hepatocarcinogenesis. Cancer Res 2007;67:4586-94.
40. Nishida N, Nagasaka T, Nishimura T, Ikai I, Boland CR, Goel A. Aberrant methylation of multiple tumor suppressor genes in aging liver, chronic hepatitis, and hepatocellular carcinoma. Hepatology 2008;47:908-18.
41. Greger V, Passarge E, Höpping W, Messmer E, Horsthemke B. Epigenetic changes may contribute to the formation and spontaneous regression of retinoblastoma. Hum Genet 1989;83:155-8.
42. Robertson KD, Wolffe AP. DNA methylation in health and disease. Nat Rev Genet 2000;1:11-9.
43. Li E. Chromatin modification and epigenetic reprogramming in mammalian development. Nat Rev Genet 2002;3:662-73.
44. Slattery ML, Curtin K, Sweeney C, Levin TR, Potter J, Wolff RK, et al. Diet and lifestyle factor associations with CpG island methylator phenotype and BRAF mutations in colon cancer. Int J Cancer 2007;120:656-63.
45. Samowitz WS, Albertsen H, Sweeney C, Herrick J, Caan BJ, Anderson KE, et al. Association of smoking, CpG island methylator phenotype, and V600E BRAF mutations in colon cancer. J Natl Cancer Inst 2006;98:1731-8.
46. Kaneko Y, Sakurai S, Hironaka M, Sato S, Oguni S, Sakuma Y, et al. Distinct methylated profiles in Helicobacter pylori dependent and independent gastric MALT lymphomas. Gut 2003;52:641-6.
47. Maekita T, Nakazawa K, Mihara M, Nakajima T, Yanaoka K, Iguchi M, et al. High levels of aberrant DNA methylation in Helicobacter pylori-infected gastric mucosae and its possible association with gastric cancer risk. Clin Cancer Res 2006;12:989-95.
48. Chan AO, Peng JZ, Lam SK, Lai KC, Yuen MF, Cheung HK, et al. Eradication of Helicobacter pylori infection reverses E-cadherin promoter hypermethylation. Gut 2006;55:463-8.
49. Perri F, Cotugno R, Piepoli A, Merla A, Quitadamo M, Gentile A, et al. Aberrant DNA methylation in non-neoplastic gastric mucosa of H. Pylori infected patients and effect of eradication. Am J Gastroenterol 2007;102:1361-71.
50. Goel A, Li MS, Nagasaka T, Shin SK, Fuerst F, Ricciardiello L, et al. Association of JC virus T-antigen expression with the methylator phenotype in sporadic colorectal cancers. Gastroenterology 2006;130:1950-61.
51. Herath NI, Leggett BA, MacDonald GA. Review of genetic and epigenetic alterations in hepatocarcinogenesis. J Gastroenterol Hepatol 2006;21:15-21.
52. Kang GH, Lee S, Kim WH, Lee HW, Kim JC, Rhyu MG, et al. Epstein-barr virus-positive gastric carcinoma demonstrates frequent aberrant methylation of multiple genes and constitutes CpG island methylator phenotype-positive gastric carcinoma. Am J Pathol 2002;160:787-94.
53. Ohm JE, McGarvey KM, Yu X, Cheng L, Schuebel KE, Cope L, et al. A stem cell-like chromatin pattern may predispose tumor suppressor genes to DNA hypermethylation and heritable silencing. Nat Genet 2007;39:237-42.
54. Ohm JE, Baylin SB. Stem cell chromatin patterns: an instructive mechanism for DNA hypermethylation? Cell Cycle 2007;6:1040-43.
55. Rashid A, Shen L, Morris JS, Issa JP, Hamilton SR. CpG island methylation in colorectal adenomas. Am J Pathol 2001;159:1129-35.
56. Chan AO, Broaddus RR, Houlihan PS, Issa JP, Hamilton SR, Rashid A. CpG island methylation in aberrant crypt foci of the colorectum. Am J Pathol 2002;160:1823-30.
57. Shin SK, Nagasaka T, Jung BH, Matsubara N, Kim WH, Carethers JM, et al. Epigenetic and genetic alterations in Netrin-1 receptors UNC5C and DCC in human colon cancer. Gastroenterology 2007;133:1849-57.
58. Ahlquist DA, Skoletsky JE, Boynton KA, Harrington JJ, Mahoney DW, Pierceall WE, et al. Colorectal cancer screening by detection of altered human DNA in stool: feasibility of a multitarget assay panel. Gastroenterology 2000;119:1219-27.
59. Müller HM, Oberwalder M, Fiegl H, Morandell M, Goebel G, Zitt M, et al. Methylation changes in faecal DNA: a marker for colorectal cancer screening? Lancet 2004;363:1283-5.
60. Nagasaka T, Goel A, Matsubara N, Tanaka N. Detection of fecal DNA methylation for colorectal neoplasia: does it lead to an optimal screening test? Acta Med Okayama 2006;60:249-56.
61. Chen WD, Han ZJ, Skoletsky J, Olson J, Sah J, Myeroff L, et al. Detection in fecal DNA of colon cancer-specific methylation of the nonexpressed vimentin gene. J Natl Cancer Inst 2005;97:1124-32.
62. Zou H, Taylor WR, Harrington JJ, Hussain FT, Cao X, Loprinzi CL, et al. High detection rates of colorectal neoplasia by stool DNA testing with a novel digital melt curve assay. Gastroenterology 2009;136:459-70.
63. Esteller M. Epigenetics in cancer. N Engl J Med 2008;358:1148-59.
64. Mitsuno M, Kitajima Y, Ide T, Ohtaka K, Tanaka M, Satoh S, et al. Aberrant methylation of p16 predicts candidates for 5-fluorouracil-based adjuvant therapy in gastric cancer patients. J Gastroenterol 2007;42:866-73.
65. Stresemann C, Lyko F. Modes of action of the DNA methyltransferase inhibitors azacytidine and decitabine. Int J Cancer 2008; 123:8-13.
66. Arnold CN, Goel A, Boland CR. Role of hMLH1 promoter hypermethylation in drug resistance to 5-fluorouracil in colorectal cancer cell lines. Int J Cancer 2003;106:66-73.
67. Oki Y, Issa JP. Review: recent clinical trials in epigenetic therapy. Rev Recent Clin Trials 2006;1:169-82.
68. Kaminskas E, Farrell A, Abraham S, Baird A, Hsieh LS, Lee SL, et al. Approval summary: azacitidine for treatment of myelodysplastic syndrome subtypes. Clin Cancer Res 2005;11:3604-8.
69. Hellebrekers DM, Griffioen AW, van Engeland M. Dual targeting of epigenetic therapy in cancer. Biochim Biophys Acta 2007;1775:76-91.
70. Walker DL, Padgett BL, ZuRhein GM, Albert AE, Marsh RF. Human papovavirus (JC): induction of brain tumors in hamsters. Science 1973;181:674-6.
71. Gordon J, Khalili K. The human polyomavirus, JCV, and neurological diseases (review). Int J Mol Med 1998;1:647-55.
72. Boland CR, Luciani MG, Gasche C, Goel A. Infection, inflammation, and gastrointestinal cancer. Gut 2005;54:1321-31.
73. Laghi L, Randolph AE, Chauhan DP, Marra G, Major EO, Neel JV, et al. JC virus DNA is present in the mucosa of the human colon and in colorectal cancers. Proc Natl Acad Sci U S A 1999; 96:7484-9.
74. Ricciardiello L, Laghi L, Ramamirtham P, Chang CL, Chang DK, Randolph AE, et al. JC virus DNA sequences are frequently present in the human upper and lower gastrointestinal tract. Gastroenterology 2000;119:1228-35.
75. Jung WT, Li MS, Goel A, Boland CR. JC virus T-antigen expression in sporadic adenomatous polyps of the colon. Cancer 2008; 112:1028-36.
76. Enam S, Del Valle L, Lara C, Gan DD, Ortiz-Hidalgo C, Palazzo JP, et al. Association of human polyomavirus JCV with colon cancer: evidence for interaction of viral T-antigen and beta-catenin. Cancer Res 2002;62:7093-101.
77. Casini B, Borgese L, Del Nonno F, Galati G, Izzo L, Caputo M, et al. Presence and incidence of DNA sequences of human polyoma-viruses BKV and JCV in colorectal tumor tissues. Anticancer Res 2005;25:1079-85.
78. Theodoropoulos G, Panoussopoulos D, Papaconstantinou I, Gazouli M, Perdiki M, Bramis J, et al. Assessment of JC polyoma virus in colon neoplasms. Dis Colon Rectum 2005;48:86-91.
79. Ricciardiello L, Baglioni M, Giovannini C, Pariali M, Cenacchi G, Ripalti A, et al. Induction of chromosomal instability in colonic cells by the human polyomavirus JC virus. Cancer Res 2003;63: 7256-62.
80. Goel A, Nagasaka T, Arnold CN, Inoue T, Hamilton C, Niedzwiecki D, et al. The CpG island methylator phenotype and chromosomal instability are inversely correlated in sporadic colorectal cancer. Gastroenterology 2007;132:127-38.