Identification and validation of highly frequent CpG island hypermethylation in colorectal adenomas and carcinomas

International Journal of Cancer

Volumn 129, Issue 12, 2011, Pages 2855-2866

  Øster, Bodil ^a   Thorsen, Kasper ^a,b   Lamy, Philippe ^a   Wojdacz, Tomasz K ^b   Hansen, Lise Lotte ^b   Birkenkamp Demtröder, Karin ^a   Sørensen, Karina D ^a   Laurberg, Søren ^a   Ørntoft, Torben F ^a   Andersen, Claus L ^a  

^a AARHUS UNIVERSITY HOSPITAL   (Denmark)

^b AARHUS UNIVERSITY   (Denmark)

Author keywords

colorectal cancer; DNA methylation; gene expression; genome wide; microarray

Indexed keywords

ABHD9 GENE; ADULT; AGED; AOX1 GENE; ARTICLE; CLINICAL ARTICLE; CNRIP1 GENE; COLORECTAL ADENOMA; COLORECTAL CARCINOMA; CONTROLLED STUDY; CPG ISLAND; DIFFERENTIAL DIAGNOSIS; DNA DETERMINATION; DNA METHYLATION; DNA MICROARRAY; DSC3 GENE; EXON; EYA4 GENE; FEMALE; FLI1 GENE; GENE EXPRESSION; GENE FREQUENCY; GENE FUNCTION; GENE IDENTIFICATION; GENETIC CORRELATION; GENETIC TRANSCRIPTION; HIGH RESOLUTION MELTING ANALYSIS; HUMAN; IRF4 GENE; JAM2 GENE; MALE; MLH1 GENE; NRG1 GENE; ONCOGENE; PRIORITY JOURNAL; PROMOTER REGION; RAMP2 GENE; RERG GENE; STGALNAC5 GENE; TWIST1 GENE; VALIDATION STUDY; ADENOMA; CARCINOMA; COLORECTAL TUMOR; GENETICS; METABOLISM; MIDDLE AGED;

NEU DIFFERENTIATION FACTOR; NRG1 PROTEIN, HUMAN;

ADENOMA; AGED; CARCINOMA; COLORECTAL NEOPLASMS; CPG ISLANDS; DNA METHYLATION; HUMANS; MALE; MIDDLE AGED; NEUREGULIN-1;

EID: 84855180008     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.25951     Document Type: Article

References (44)

1. Ahuja N, Mohan AL, Li Q, Stolker JM, Herman JG, Hamilton SR, Baylin SB, Issa JP,. Association between CpG island methylation and microsatellite instability in colorectal cancer. Cancer Res 1997; 57: 3370-4. (Pubitemid 27355477)
2. Toyota M, Ahuja N, Ohe-Toyota M, Herman JG, Baylin SB, Issa JP,. CpG island methylator phenotype in colorectal cancer. Proc Natl Acad Sci USA 1999; 96: 8681-6. (Pubitemid 29354851)
3. Issa JP, Zehnbauer BA, Kaufmann SH, Biel MA, Baylin SB,. HIC1 hypermethylation is a late event in hematopoietic neoplasms. Cancer Res 1997; 57: 1678-81. (Pubitemid 27199658)
4. Dominguez G, Carballido J, Silva J, Silva JM, Garcia JM, Menendez J, Provencio M, Espana P, Bonilla F,. p14ARF promoter hypermethylation in plasma DNA as an indicator of disease recurrence in bladder cancer patients. Clin Cancer Res 2002; 8: 980-5. (Pubitemid 35177345)
5. Wei SH, Chen CM, Strathdee G, Harnsomburana J, Shyu CR, Rahmatpanah F, Shi H, Ng SW, Yan PS, Nephew KP, Brown R, Huang TH,. Methylation microarray analysis of late-stage ovarian carcinomas distinguishes progression-free survival in patients and identifies candidate epigenetic markers. Clin Cancer Res 2002; 8: 2246-52. (Pubitemid 34753597)
6. el-Deiry WS, Nelkin BD, Celano P, Yen RW, Falco JP, Hamilton SR, Baylin SB,. High expression of the DNA methyltransferase gene characterizes human neoplastic cells and progression stages of colon cancer. Proc Natl Acad Sci USA 1991; 88: 3470-4. (Pubitemid 21916643)
7. de Caceres II, Cortes-Sempere M, Moratilla C, Machado-Pinilla R, Rodriguez-Fanjul V, Manguan-Garcia C, Cejas P, Lopez-Rios F, Paz-Ares L, de CJ, Nistal M, Belda-Iniesta C, et al. IGFBP-3 hypermethylation-derived deficiency mediates cisplatin resistance in non-small-cell lung cancer. Oncogene 2010; 29: 1681-90.
8. 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. (Pubitemid 36750389)
9. Suraweera N, Duval A, Reperant M, Vaury C, Furlan D, Leroy K, Seruca R, Iacopetta B, Hamelin R,. Evaluation of tumor microsatellite instability using five quasimonomorphic mononucleotide repeats and pentaplex PCR. Gastroenterology 2002; 123: 1804-11. (Pubitemid 35408304)
10. Wojdacz TK, Dobrovic A,. Methylation-sensitive high resolution melting (MS-HRM): a new approach for sensitive and high-throughput assessment of methylation. Nucleic Acids Res 2007; 35: e41.
11. Andersen CL, Jensen JL, Orntoft TF,. Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res 2004; 64: 5245-50. (Pubitemid 39006544)
12. Birkenkamp-Demtroder K, Wagner L, Brandt SF, Bording AL, Gartner W, Scherubl H, Heine B, Christiansen P, Orntoft TF,. Secretagogin is a novel marker for neuroendocrine differentiation. Neuroendocrinology 2005; 82: 121-38.
13. Osborn NK, Zou H, Molina JR, Lesche R, Lewin J, Lofton-Day C, Klatt KK, Harrington JJ, Burgart LJ, Ahlquist DA,. Aberrant methylation of the eyes absent 4 gene in ulcerative colitis-associated dysplasia. Clin Gastroenterol Hepatol 2006; 4: 212-8. (Pubitemid 43199692)
14. Schatz P, Distler J, Berlin K, Schuster M,. Novel method for high throughput DNA methylation marker evaluation using PNA-probe library hybridization and MALDI-TOF detection. Nucleic Acids Res 2006; 34: e59.
15. Herman JG, Merlo A, Mao L, Lapidus RG, Issa JP, Davidson NE, Sidransky D, Baylin SB,. Inactivation of the CDKN2/p16/MTS1 gene is frequently associated with aberrant DNA methylation in all common human cancers. Cancer Res 1995; 55: 4525-30.
16. Gonzalez-Zulueta M, Bender CM, Yang AS, Nguyen T, Beart RW, Van Tornout JM, Jones PA,. Methylation of the 5' CpG island of the p16/CDKN2 tumor suppressor gene in normal and transformed human tissues correlates with gene silencing. Cancer Res 1995; 55: 4531-5.
17. Glockner SC, Dhir M, Yi JM, McGarvey KE, Van NL, Louwagie J, Chan TA, Kleeberger W, de Bruine AP, Smits KM, Khalid-de Bakker CA, Jonkers DM, et al. Methylation of TFPI2 in stool DNA: a potential novel biomarker for the detection of colorectal cancer. Cancer Res 2009; 69: 4691-9.
18. Ausch C, Kim YH, Tsuchiya KD, Dzieciatkowski S, Washington MK, Paraskeva C, Radich J, Grady WM,. Comparative analysis of PCR-based biomarker assay methods for colorectal polyp detection from fecal DNA. Clin Chem 2009; 55: 1559-63.
19. Belshaw NJ, Elliott GO, Williams EA, Bradburn DM, Mills SJ, Mathers JC, Johnson IT,. Use of DNA from human stools to detect aberrant CpG island methylation of genes implicated in colorectal cancer. Cancer Epidemiol Biomarkers Prev 2004; 13: 1495-501. (Pubitemid 39202317)
20. Dickinson RE, Dallol A, Bieche I, Krex D, Morton D, Maher ER, Latif F,. Epigenetic inactivation of SLIT3 and SLIT1 genes in human cancers. Br J Cancer 2004; 91: 2071-8. (Pubitemid 40128774)
21. Zhang W, Glockner SC, Guo M, Machida EO, Wang DH, Easwaran H, Van NL, Herman JG, Schuebel KE, Watkins DN, Ahuja N, Baylin SB,. Epigenetic inactivation of the canonical Wnt antagonist SRY-box containing gene 17 in colorectal cancer. Cancer Res 2008; 68: 2764-72. (Pubitemid 351556274)
22. Irizarry RA, Ladd-Acosta C, Wen B, Wu Z, Montano C, Onyango P, Cui H, Gabo K, Rongione M, Webster M, Ji H, Potash JB, et al. The human colon cancer methylome shows similar hypo- and hypermethylation at conserved tissue-specific CpG island shores. Nat Genet 2009; 41: 178-86.
23. Caldwell GM, Jones C, Gensberg K, Jan S, Hardy RG, Byrd P, Chughtai S, Wallis Y, Matthews GM, Morton DG,. The Wnt antagonist sFRP1 in colorectal tumorigenesis. Cancer Res 2004; 64: 883-8. (Pubitemid 38176888)
24. Shames DS, Girard L, Gao B, Sato M, Lewis CM, Shivapurkar N, Jiang A, Perou CM, Kim YH, Pollack JR, Fong KM, Lam CL, et al. A genome-wide screen for promoter methylation in lung cancer identifies novel methylation markers for multiple malignancies. PLoS Med 2006; 3: e486.
25. Yagi K, Akagi K, Hayashi H, Nagae G, Tsuji S, Isagawa T, Midorikawa Y, Nishimura Y, Sakamoto H, Seto Y, Aburatani H, Kaneda A,. Three DNA methylation epigenotypes in human colorectal cancer. Clin Cancer Res 2010; 16: 21-33.
26. Model F, Osborn N, Ahlquist D, Gruetzmann R, Molnar B, Sipos F, Galamb O, Pilarsky C, Saeger HD, Tulassay Z, Hale K, Mooney S, et al. Identification and validation of colorectal neoplasia-specific methylation markers for accurate classification of disease. Mol Cancer Res 2007; 5: 153-63. (Pubitemid 46423996)
27. Bernet A, Mazelin L, Coissieux MM, Gadot N, Ackerman SL, Scoazec JY, Mehlen P,. Inactivation of the UNC5C Netrin-1 receptor is associated with tumor progression in colorectal malignancies. Gastroenterology 2007; 133: 1840-8. (Pubitemid 350186160)
28. Shin SK, Nagasaka T, Jung BH, Matsubara N, Kim WH, Carethers JM, Boland CR, Goel A,. Epigenetic and genetic alterations in Netrin-1 receptors UNC5C and DCC in human colon cancer. Gastroenterology 2007; 133: 1849-57. (Pubitemid 350180802)
29. Okada T, Suehiro Y, Ueno K, Mitomori S, Kaneko S, Nishioka M, Okayama N, Sakai K, Higaki S, Hazama S, Hirata H, Sakaida I, et al. TWIST1 hypermethylation is observed frequently in colorectal tumors and its overexpression is associated with unfavorable outcomes in patients with colorectal cancer. Genes Chromosomes Cancer 2010; 49: 452-62.
30. Zou H, Osborn NK, Harrington JJ, Klatt KK, Molina JR, Burgart LJ, Ahlquist DA,. Frequent methylation of eyes absent 4 gene in Barrett's esophagus and esophageal adenocarcinoma. Cancer Epidemiol Biomarkers Prev 2005; 14: 830-4. (Pubitemid 40478544)
31. Feng Q, Balasubramanian A, Hawes SE, Toure P, Sow PS, Dem A, Dembele B, Critchlow CW, Xi L, Lu H, McIntosh MW, Young AM, et al. Detection of hypermethylated genes in women with and without cervical neoplasia. J Natl Cancer Inst 2005; 97: 273-82. (Pubitemid 40310275)
32. Fackler MJ, McVeigh M, Evron E, Garrett E, Mehrotra J, Polyak K, Sukumar S, Argani P,. DNA methylation of RASSF1A, HIN-1, RAR-beta, Cyclin D2 and Twist in in situ and invasive lobular breast carcinoma. Int J Cancer 2003; 107: 970-5. (Pubitemid 37429839)
33. Renard I, Joniau S, van CB, Collette C, Naome C, Vlassenbroeck I, Nicolas H, de LJ, Straub J, Van CW, Hamida W, Hellel M, et al. Identification and Validation of the Methylated TWIST1 and NID2 Genes through Real-Time Methylation-Specific Polymerase Chain Reaction Assays for the Noninvasive Detection of Primary Bladder Cancer in Urine Samples. Eur Urol 2009.
34. Tsou JA, Galler JS, Siegmund KD, Laird PW, Turla S, Cozen W, Hagen JA, Koss MN, Laird-Offringa IA,. Identification of a panel of sensitive and specific DNA methylation markers for lung adenocarcinoma. Mol Cancer 2007; 6: 70.
35. Kang GH, Lee S, Cho NY, Gandamihardja T, Long TI, Weisenberger DJ, Campan M, Laird PW,. DNA methylation profiles of gastric carcinoma characterized by quantitative DNA methylation analysis. Lab Invest 2008; 88: 161-70. (Pubitemid 351161274)
36. Weisenberger DJ, Siegmund KD, Campan M, Young J, Long TI, Faasse MA, Kang GH, Widschwendter M, Weener D, Buchanan D, Koh H, Simms L, 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. (Pubitemid 43980599)
37. Cottrell S, Jung K, Kristiansen G, Eltze E, Semjonow A, Ittmann M, Hartmann A, Stamey T, Haefliger C, Weiss G,. Discovery and validation of 3 novel DNA methylation markers of prostate cancer prognosis. J Urol 2007; 177: 1753-8. (Pubitemid 46560648)
38. Gort EH, Suijkerbuijk KP, Roothaan SM, Raman V, Vooijs M, van der Wall E, van Diest PJ,. Methylation of the TWIST1 promoter, TWIST1 mRNA levels, and immunohistochemical expression of TWIST1 in breast cancer. Cancer Epidemiol Biomarkers Prev 2008; 17: 3325-30.
39. Rakyan VK, Down TA, Maslau S, Andrew T, Yang TP, Beyan H, Whittaker P, McCann OT, Finer S, Valdes AM, Leslie RD, Deloukas P, et al. Human aging-associated DNA hypermethylation occurs preferentially at bivalent chromatin domains. Genome Res 2010; 20: 434-9.
40. Bronner CE, Baker SM, Morrison PT, Warren G, Smith LG, Lescoe MK, Kane M, Earabino C, Lipford J, Lindblom A,. Mutation in the DNA mismatch repair gene homologue hMLH1 is associated with hereditary non-polyposis colon cancer. Nature 1994; 368: 258-61.
41. Chua YL, Ito Y, Pole JC, Newman S, Chin SF, Stein RC, Ellis IO, Caldas C, O'Hare MJ, Murrell A, Edwards PA,. The NRG1 gene is frequently silenced by methylation in breast cancers and is a strong candidate for the 8p tumour suppressor gene. Oncogene 2009; 28: 4041-52.
42. Buac K, Xu M, Cronin J, Weeraratna AT, Hewitt SM, Pavan WJ,. NRG1/ERBB3 signaling in melanocyte development and melanoma: inhibition of differentiation and promotion of proliferation. Pigment Cell Melanoma Res 2009; 22: 773-84.
43. Frigola J, Song J, Stirzaker C, Hinshelwood RA, Peinado MA, Clark SJ,. Epigenetic remodeling in colorectal cancer results in coordinate gene suppression across an entire chromosome band. Nat Genet 2006; 38: 540-9.
44. Coolen MW, Stirzaker C, Song JZ, Statham AL, Kassir Z, Moreno CS, Young AN, Varma V, Speed TP, Cowley M, Lacaze P, Kaplan W, et al. Consolidation of the cancer genome into domains of repressive chromatin by long-range epigenetic silencing (LRES) reduces transcriptional plasticity. Nat Cell Biol 2010; 12: 235-46.