DNA demethylation in normal colon tissue predicts predisposition to multiple cancers

Oncogene

Volumn 31, Issue 48, 2012, Pages 5029-5037

  Kamiyama, H ^a   Suzuki, K ^a   Maeda, T ^a   Koizumi, K ^b   Miyaki, Y ^b   Okada, S ^a   Kawamura, Y J ^a   Samuelsson, J K ^c,d   Alonso, S ^d   Konishi, F ^a   Perucho, M ^c,d,e  

^a JICHI MEDICAL UNIVERSITY   (Japan)

^b HAMAMATSU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c BURNHAM INSTITUTE   (United States)

^d Institute of Predictive and Personalized Medicine of Cancer IMPPC   (Spain)

^e INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

colon cancer; DNA demethylation; epigenetics; metachronous; synchronous

Indexed keywords

LONG INTERSPERSED NUCLEOTIDE ELEMENT 1; PROTEIN; UNCLASSIFIED DRUG;

ADULT; AGED; AGING; AMINO ACID SEQUENCE; ARTICLE; CANCER LOCALIZATION; CANCER PATIENT; CANCER RISK; CANCER SUSCEPTIBILITY; COLON MUCOSA; CONTROLLED STUDY; DISEASE SEVERITY; DNA METHYLATION; FEMALE; GROUPS BY AGE; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; MICROSATELLITE INSTABILITY; MULTIPLE CANCER; PREDICTION; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION;

AGED; COLON; DNA METHYLATION; FEMALE; GENETIC PREDISPOSITION TO DISEASE; HUMANS; LONG INTERSPERSED NUCLEOTIDE ELEMENTS; MALE; MIDDLE AGED; NEOPLASMS; POLYMERASE CHAIN REACTION;

EID: 84870552726     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2011.652     Document Type: Article

References (44)

1. Bouvier AM, Latournerie M, Jooste V, Lepage C, Cottet V, Faivre J. The lifelong risk of metachronous colorectal cancer justifies long-term colonoscopic follow-up. Eur J Cancer 2008; 44: 522-527.
2. Lynch HT, Smyrk TC, Watson P, Lanspa SJ, Lynch JF, Lynch PM et al. Genetics, natural history, tumor spectrum, and pathology of hereditary nonpolyposis colorectal cancer: an updated review. Gastroenterology 1993; 104: 1535-1549. (Pubitemid 23235432)
3. Rex DK, Kahi CJ, Levin B, Smith RA, Bond JH, Brooks D et al. Guidelines for colonoscopy surveillance after cancer resection: a consensus update by the American Cancer Society and the US Multi-Society Task Force on Colorectal Cancer. Gastroenterology 2006; 130: 1865-1871. (Pubitemid 43668858)
4. Braakhuis BJ, Tabor MP, Kummer JA, Leemans CR, Brakenhoff RH. A genetic explanation of Slaughter's concept of field cancerization: evidence and clinical implications. Cancer Res 2003; 63: 1727-1730. (Pubitemid 36460827)
5. Slaughter DP, Southwick HW, Smejkal W. Field cancerization in oral stratified squamous epithelium; clinical implications of multicentric origin. Cancer 1953; 6: 963-968.
6. Deng G, Lu Y, Zlotnikov G, Thor AD, Smith HS. Loss of heterozygosity in normal tissue adjacent to breast carcinomas. Science 1996; 274: 2057-2059. (Pubitemid 27020695)
7. Ahlquist T, Lind GE, Costa VL, Meling GI, Vatn M, Hoff GS et al. Gene methylation profiles of normal mucosa, and benign and malignant colorectal tumors identify early onset markers. Mol Cancer 2008; 7: 94.
8. Belshaw NJ, Pal N, Tapp HS, Dainty JR, Lewis MP, Williams MR et al. Patterns of DNA methylation in individual colonic crypts reveal aging and cancer-related field defects in the morphologically normal mucosa. Carcinogenesis 2010; 31: 1158-1163.
9. Konishi K, Shen L, Jelinek J, Watanabe Y, Ahmed S, Kaneko K et al. Concordant DNA methylation in synchronous colorectal carcinomas. Cancer Prev Res (Phila) 2009; 2: 814-822.
10. Menigatti M, Truninger K, Gebbers JO, Marbet U, Marra G, Schar P. Normal colorectal mucosa exhibits sex- and segment-specific susceptibility to DNA methylation at the hMLH1 and MGMT promoters. Oncogene 2009; 28: 899-909.
11. Paun BC, Kukuruga D, Jin Z, Mori Y, Cheng Y, Duncan M et al. Relation between normal rectal methylation, smoking status, and the presence or absence of colorectal adenomas. Cancer 2010; 116: 4495-4501.
12. Ushijima T. Epigenetic field for cancerization. J Biochem Mol Biol 2007; 40: 142-150. (Pubitemid 46515191)
13. Worthley DL, Whitehall VL, Buttenshaw RL, Irahara N, Greco SA, Ramsnes I et al. DNA methylation within the normal colorectal mucosa is associated with pathway-specific predisposition to cancer. Oncogene 2010; 29: 1653-1662.
14. Svrcek M, Buhard O, Colas C, Coulet F, Dumont S, Massaoudi I et al. Methylation tolerance due to an O6-methylguanine DNA methyltransferase (MGMT) field defect in the colonic mucosa: an initiating step in the development of mismatch repair-deficient colorectal cancers. Gut 2010; 59: 1516-1526.
15. Gonzalo V, Lozano JJ, Munoz J, Balaguer F, Pellise M, Rodriguez de Miguel C et al. Aberrant gene promoter methylation associated with sporadic multiple colorectal cancer. PLoS One 2010; 5: e8777.
16. Feinberg AP, Vogelstein B. Hypomethylation distinguishes genes of some human cancers from their normal counterparts. Nature 1983; 301: 89-92. (Pubitemid 13154475)
17. Feinberg AP, Tycko B. The history of cancer epigenetics. Nat Rev Cancer 2004; 4: 143-153. (Pubitemid 38198742)
18. Eden A, Gaudet F, Waghmare A, Jaenisch R. Chromosomal instability and tumors promoted by DNA hypomethylation. Science 2003; 300: 455. (Pubitemid 36444319)
19. Gaudet F, Hodgson JG, Eden A, Jackson-Grusby L, Dausman J, Gray JW et al. Induction of tumors in mice by genomic hypomethylation. Science 2003; 300: 489-492. (Pubitemid 36444330)
20. Kawakami K, Matsunoki A, Kaneko M, Saito K, Watanabe G, Minamoto T. Long interspersed nuclear element-1 hypomethylation is a potential biomarker for the prediction of response to oral fluoropyrimidines in microsatellite stable and CpG island methylator phenotype-negative colorectal cancer. Cancer Sci 2011; 102: 166-174.
21. Sunami E, de Maat M, Vu A, Turner RR, Hoon DS. LINE-1 hypomethylation during primary colon cancer progression. PLoS One 2011; 6: e18884.
22. Ibrahim AE, Arends MJ, Silva AL, Wyllie AH, Greger L, Ito Y et al. Sequential DNA methylation changes are associated with DNMT3B overexpression in colorectal neoplastic progression. Gut 2011; 60: 499-508.
23. Ogino S, Nosho K, Kirkner GJ, Kawasaki T, Chan AT, Schernhammer ES et al. A cohort study of tumoral LINE-1 hypomethylation and prognosis in colon cancer. J Natl Cancer Inst 2008; 100: 1734-1738.
24. Yamashita K, Dai T, Dai Y, Yamamoto F, Perucho M. Genetics supersedes epigenetics in colon cancer phenotype. Cancer Cell 2003; 4: 121-131. (Pubitemid 37040828)
25. Suzuki K, Suzuki I, Leodolter A, Alonso S, Horiuchi S, Yamashita K et al. Global DNA demethylation in gastrointestinal cancer is age dependent and precedes genomic damage. Cancer Cell 2006; 9: 199-207. (Pubitemid 43357946)
26. Suter CM, Martin DI, Ward RL. Hypomethylation of L1 retrotransposons in colorectal cancer and adjacent normal tissue. Int J Colorectal Dis 2004; 19: 95-101. (Pubitemid 38239827)
27. Horii J, Hiraoka S, Kato J, Harada K, Kuwaki K, Fujita H et al. Age-related methylation in normal colon mucosa differs between the proximal and distal colon in patients who underwent colonoscopy. Clin Biochem 2008; 41: 1440- 1448.
28. Nosho K, Kure S, Irahara N, Shima K, Baba Y, Spiegelman D et al. A prospective cohort study shows unique epigenetic, genetic, and prognostic features of synchronous colorectal cancers. Gastroenterology 2009; 137: 1609-1620, e1-3.
29. Suzuki K, Ohnami S, Tanabe C, Sasaki H, Yasuda J, Katai H et al. The genomic damage estimated by arbitrarily primed PCR DNA fingerprinting is useful for the prognosis of gastric cancer. Gastroenterology 2003; 125: 1330-1340. (Pubitemid 37409753)
30. Weisenberger DJ, Campan M, Long TI, Kim M, Woods C, Fiala E et al. Analysis of repetitive element DNA methylation by MethyLight. Nucleic Acids Res 2005; 33: 6823-6836. (Pubitemid 41830488)
31. Ionov Y, Peinado MA, Malkhosyan S, Shibata D, Perucho M. Ubiquitous somatic mutations in simple repeated sequences reveal a new mechanism for colonic carcinogenesis. Nature 1993; 363: 558-561. (Pubitemid 23186645)
32. Vilar E, Gruber SB. Microsatellite instability in colorectal cancer-the stable evidence. Nat Rev Clin Oncol 2010; 7: 153-162.
33. Estecio MR, Gharibyan V, Shen L, Ibrahim AE, Doshi K, He R et al. LINE-1 hypomethylation in cancer is highly variable and inversely correlated with microsatellite instability. PLoS One 2007; 2: e399.
34. Brenner H, Hoffmeister M, Stegmaier C, Brenner G, Altenhofen L, Haug U. Risk of progression of advanced adenomas to colorectal cancer by age and sex: estimates based on 840 149 screening colonoscopies. Gut 2007; 56: 1585-1589. (Pubitemid 350033198)
35. Ehrlich M. DNA methylation in cancer: too much, but also too little. Oncogene 2002; 21: 5400-5413. (Pubitemid 34983477)
36. Qu GZ, Grundy PE, Narayan A, Ehrlich M. Frequent hypomethylation in Wilms tumors of pericentromeric DNA in chromosomes 1 and 16. Cancer Genet Cytogenet 1999; 109: 34-39. (Pubitemid 29061521)
37. Xu GL, Bestor TH, Bourc'his D, Hsieh CL, Tommerup N, Bugge M et al. Chromosome instability and immunodeficiency syndrome caused by mutations in a DNA methyltransferase gene. Nature 1999; 402: 187-191.
38. Zeimet AG, Fiegl H, Goebel G, Kopp F, Allasia C, Reimer D et al. DNA ploidy, nuclear size, proliferation index and DNA-hypomethylation in ovarian cancer. Gynecol Oncol 2011; 121: 24-31.
39. Umar A, Risinger JI, Hawk ET, Barrett JC. Testing guidelines for hereditary nonpolyposis colorectal cancer. Nat Rev Cancer 2004; 4: 153-158. (Pubitemid 38198743)
40. Kim H, Jen J, Vogelstein B, Hamilton SR. Clinical and pathological characteristics of sporadic colorectal carcinomas with DNA replication errors in microsatellite sequences. Am J Pathol 1994; 145: 148-156. (Pubitemid 24217493)
41. Thibodeau SN, Bren G, Schaid D. Microsatellite instability in cancer of the proximal colon. Science 1993; 260: 816-819. (Pubitemid 23167612)
42. Perucho M. Cancer of the microsatellite mutator phenotype. Biol Chem 1996; 377: 675-684. (Pubitemid 26418091)
43. Tsao JL, Yatabe Y, Salovaara R, Jarvinen HJ, Mecklin JP, Aaltonen LA et al. Genetic reconstruction of individual colorectal tumor histories. Proc Natl Acad Sci USA 2000; 97: 1236-1241. (Pubitemid 30080842)
44. R Development Core Team. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing: Vienna, Austria, 2009.