DNA hypermethylation appears early and shows increased frequency with dysplasia in Lynch syndrome-associated colorectal adenomas and carcinomas

Clinical Epigenetics

Volumn 7, Issue 1, 2015, Pages

  Valo, Satu ^a   Kaur, Sippy ^a   Ristimäki, Ari ^a,b   Renkonen Sinisalo, Laura ^b   Järvinen, Heikki ^b   Mecklin, Jukka Pekka ^c   Nyström, Minna ^a   Peltomäki, Päivi ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

^c UNIVERSITY OF EASTERN FINLAND   (Finland)

Author keywords

Adenoma carcinoma sequence; Colorectal cancer; CpG island methylator phenotype; DNA methylation; Lynch syndrome; MS MLPA

Indexed keywords

MISMATCH REPAIR PROTEIN;

ADULT; ALLELE; ARTICLE; CANCER GROWTH; CARCINOGENESIS; CIMP GENE; CLINICAL ARTICLE; COLONOSCOPY; COLORECTAL ADENOMA; COLORECTAL CARCINOMA; CONTROLLED STUDY; CPG ISLAND; DISEASE ASSOCIATION; DNA METHYLATION; DYSPLASIA; EARLY DIAGNOSIS; EPIGENETICS; GENE; GENE LOCUS; GENE MUTATION; GENETIC ASSOCIATION; GENETIC PREDISPOSITION; HEREDITARY NONPOLYPOSIS COLORECTAL CANCER; HETEROZYGOTE; HUMAN; HUMAN CELL; HUMAN TISSUE; MISMATCH REPAIR; MMR GENE; PRIORITY JOURNAL; PROMOTER REGION; PROSPECTIVE STUDY; PROTEIN DEPLETION; PROTEIN EXPRESSION; RETROSPECTIVE STUDY; SFRP1 GENE; SLC5A8 GENE; TUMOR SUPPRESSOR GENE;

EID: 84937407003     PISSN: 18687075     EISSN: 18687083     Source Type: Journal    
DOI: 10.1186/s13148-015-0102-4     Document Type: Article

References (56)

1. Vasen HF, Blanco I, Aktan-Collan K, Gopie JP, Alonso A, Aretz S, et al. Revised guidelines for the clinical management of Lynch syndrome (HNPCC): recommendations by a group of European experts. Gut. 2013;62(6):812–23. doi:10.1136/gutjnl-2012-304356.
2. Geiersbach KB, Samowitz WS. Microsatellite instability and colorectal cancer. Arch Pathol Lab Med. 2011;135(10):1269–77. doi:10.5858/arpa.2011-0035-RA.
3. 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(5):808–11.
4. Veigl ML, Kasturi L, Olechnowicz J, Ma AH, Lutterbaugh JD, Periyasamy S, et al. Biallelic inactivation of hMLH1 by epigenetic gene silencing, a novel mechanism causing human MSI cancers. Proc Natl Acad Sci U S A. 1998;95(15):8698–702.
5. Lao VV, Grady WM. Epigenetics and colorectal cancer. Nat Rev Gastroenterol Hepatol. 2011;8(12):686–700. doi:10.1038/nrgastro.2011.173.
6. Kim YH, Petko Z, Dzieciatkowski S, Lin L, Ghiassi M, Stain S, et al. CpG island methylation of genes accumulates during the adenoma progression step of the multistep pathogenesis of colorectal cancer. Genes, Chromosomes Cancer. 2006;45(8):781–9. doi:10.1002/gcc.20341.
7. Beggs AD, Jones A, El-Bahrawy M, Abulafi M, Hodgson SV, Tomlinson IP. Whole-genome methylation analysis of benign and malignant colorectal tumours. J Pathol. 2013;229(5):697–704. doi:10.1002/path.4132.
8. Nosho K, Irahara N, Shima K, Kure S, Kirkner GJ, Schernhammer ES, et al. Comprehensive biostatistical analysis of CpG island methylator phenotype in colorectal cancer using a large population-based sample. PLoS One. 2008;3(11):e3698. doi:10.1371/journal.pone.0003698.
9. McCabe MT, Brandes JC, Vertino PM. Cancer DNA methylation: molecular mechanisms and clinical implications. Clinical cancer research: an official journal of the American Association for Cancer Research. 2009;15(12):3927–37. doi:10.1158/1078-0432.CCR-08-2784.
10. Mecklin JP, Aarnio M, Laara E, Kairaluoma MV, Pylvanainen K, Peltomaki P, et al. Development of colorectal tumors in colonoscopic surveillance in Lynch syndrome. Gastroenterology. 2007;133(4):1093–8. doi:10.1053/j.gastro.2007.08.019.
11. Pussila M, Sarantaus L, Dermadi Bebek D, Valo S, Reyhani N, Ollila S, et al. Cancer-predicting gene expression changes in colonic mucosa of Western diet fed Mlh1+/− mice. PLoS One. 2013;8(10):e76865. doi:10.1371/journal.pone.0076865.
12. Deng G, Chen A, Hong J, Chae HS, Kim YS. Methylation of CpG in a small region of the hMLH1 promoter invariably correlates with the absence of gene expression. Cancer Res. 1999;59(9):2029–33.
13. Berg M, Hagland HR, Soreide K. Comparison of CpG island methylator phenotype (CIMP) frequency in colon cancer using different probe- and gene-specific scoring alternatives on recommended multi-gene panels. PLoS One. 2014;9(1):e86657. doi:10.1371/journal.pone.0086657.
14. Issa JP. CpG-island methylation in aging and cancer. Curr Top Microbiol Immunol. 2000;249:101–18.
15. 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(5):1823–30. doi:10.1016/S0002-9440(10)61128-5.
16. Shen L, Kondo Y, Rosner GL, Xiao L, Hernandez NS, Vilaythong J, et al. MGMT promoter methylation and field defect in sporadic colorectal cancer. J Natl Cancer Inst. 2005;97(18):1330–8. doi:10.1093/jnci/dji275.
17. De Jong AE, Morreau H, Van Puijenbroek M, Eilers PH, Wijnen J, Nagengast FM, et al. The role of mismatch repair gene defects in the development of adenomas in patients with HNPCC. Gastroenterology. 2004;126(1):42–8.
18. Kaz A, Kim YH, Dzieciatkowski S, Lynch H, Watson P, Kay Washington M, et al. Evidence for the role of aberrant DNA methylation in the pathogenesis of Lynch syndrome adenomas. International journal of cancer Journal international du cancer. 2007;120(9):1922–9. doi:10.1002/ijc.22544.
19. Ollikainen M, Hannelius U, Lindgren CM, Abdel-Rahman WM, Kere J, Peltomaki P. Mechanisms of inactivation of MLH1 in hereditary nonpolyposis colorectal carcinoma: a novel approach. Oncogene. 2007;26(31):4541–9. doi:10.1038/sj.onc.1210236.
20. Rahner N, Friedrichs N, Steinke V, Aretz S, Friedl W, Buettner R, et al. Coexisting somatic promoter hypermethylation and pathogenic MLH1 germline mutation in Lynch syndrome. J Pathol. 2008;214(1):10–6. doi:10.1002/path.2263.
21. Parsons MT, Buchanan DD, Thompson B, Young JP, Spurdle AB. Correlation of tumour BRAF mutations and MLH1 methylation with germline mismatch repair (MMR) gene mutation status: a literature review assessing utility of tumour features for MMR variant classification. J Med Genet. 2012;49(3):151–7. doi:10.1136/jmedgenet-2011-100714.
22. Moreira L, Munoz J, Cuatrecasas M, Quintanilla I, Leoz ML, Carballal S, et al. Prevalence of somatic mutl homolog 1 promoter hypermethylation in Lynch syndrome colorectal cancer. Cancer. 2015;121(9):1395–404. doi:10.1002/cncr.29190.
23. Nakagawa H, Chadwick RB, Peltomaki P, Plass C, Nakamura Y, de La Chapelle A. Loss of imprinting of the insulin-like growth factor II gene occurs by biallelic methylation in a core region of H19-associated CTCF-binding sites in colorectal cancer. Proc Natl Acad Sci U S A. 2001;98(2):591–6. doi:10.1073/pnas.011528698.
24. Nagasaka T, Rhees J, Kloor M, Gebert J, Naomoto Y, Boland CR, et al. Somatic hypermethylation of MSH2 is a frequent event in Lynch syndrome colorectal cancers. Cancer Res. 2010;70(8):3098–108. doi:10.1158/0008-5472.CAN-09-3290.
25. Yurgelun MB, Goel A, Hornick JL, Sen A, Turgeon DK, Ruffin MT, et al. Microsatellite instability and DNA mismatch repair protein deficiency in Lynch syndrome colorectal polyps. Cancer prevention research. 2012;5(4):574–82. doi:10.1158/1940-6207.CAPR-11-0519.
26. Lynch HT, Snyder CL, Shaw TG, Heinen CD, Hitchins MP. Milestones of Lynch syndrome: 1895–2015. Nat Rev Cancer. 2015;15(3):181–94. doi:10.1038/nrc3878.
27. Kloor M, Huth C, Voigt AY, Benner A, Schirmacher P, von Knebel Doeberitz M, et al. Prevalence of mismatch repair-deficient crypt foci in Lynch syndrome: a pathological study. Lancet Oncol. 2012;13(6):598–606. doi:10.1016/S1470-2045(12)70109-2.
28. Carmona FJ, Esteller M. Epigenomics of human colon cancer. Mutat Res. 2010;693(1–2):53–60. doi:10.1016/j.mrfmmm.2010.07.007.
29. 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(4):499–508. doi:10.1136/gut.2010.223602.
30. Homfray TF, Cottrell SE, Ilyas M, Rowan A, Talbot IC, Bodmer WF, et al. Defects in mismatch repair occur after APC mutations in the pathogenesis of sporadic colorectal tumours. Hum Mutat. 1998;11(2):114–20. doi:10.1002/(SICI)1098-1004(1998)11:2<114::AID-HUMU3>3.0.CO;2-J.
31. Beggs AD, Domingo E, Abulafi M, Hodgson SV, Tomlinson IP. A study of genomic instability in early preneoplastic colonic lesions. Oncogene. 2013;32(46):5333–7. doi:10.1038/onc.2012.584.
32. Burt RW. Colonic polyps in Lynch syndrome. Dis Colon Rectum. 2015;58(4):371–2. doi:10.1097/DCR.0000000000000332.
33. Noffsinger AE, Hart J. Serrated adenoma: a distinct form of non-polypoid colorectal neoplasia? Gastrointest Endosc Clin N Am. 2010;20(3):543–63. doi:10.1016/j.giec.2010.03.012.
34. Rijcken FE, van der Sluis T, Hollema H, Kleibeuker JH. Hyperplastic polyps in hereditary nonpolyposis colorectal cancer. Am J Gastroenterol. 2003;98(10):2306–11. doi:10.1111/j.1572-0241.2003.07629.x.
35. Arasaradnam RP, Commane DM, Bradburn D, Mathers JC. A review of dietary factors and its influence on DNA methylation in colorectal carcinogenesis. Epigenetics: official journal of the DNA Methylation Society. 2008;3(4):193–8.
36. Suzuki H, Watkins DN, Jair KW, Schuebel KE, Markowitz SD, Chen WD, et al. Epigenetic inactivation of SFRP genes allows constitutive WNT signaling in colorectal cancer. Nat Genet. 2004;36(4):417–22. doi:10.1038/ng1330.
37. Hinoue T, Weisenberger DJ, Lange CP, Shen H, Byun HM, Van Den Berg D, et al. Genome-scale analysis of aberrant DNA methylation in colorectal cancer. Genome Res. 2012;22(2):271–82. doi:10.1101/gr.117523.110.
38. 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(8):1727–30.
39. 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(11):1653–62. doi:10.1038/onc.2009.449.
40. 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(11):1516–26. doi:10.1136/gut.2009.194787.
41. 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(5):1609–20. doi:10.1053/j.gastro.2009.08.002. e1-3.
42. Thangaraju M, Cresci G, Itagaki S, Mellinger J, Browning DD, Berger FG, et al. Sodium-coupled transport of the short chain fatty acid butyrate by SLC5A8 and its relevance to colon cancer. Journal of gastrointestinal surgery: official journal of the Society for Surgery of the Alimentary Tract. 2008;12(10):1773–81. doi:10.1007/s11605-008-0573-0. discussion 81–2.
43. Li H, Myeroff L, Smiraglia D, Romero MF, Pretlow TP, Kasturi L, et al. SLC5A8, a sodium transporter, is a tumor suppressor gene silenced by methylation in human colon aberrant crypt foci and cancers. Proc Natl Acad Sci U S A. 2003;100(14):8412–7. doi:10.1073/pnas.1430846100.
44. Luo Y, Wong CJ, Kaz AM, Dzieciatkowski S, Carter KT, Morris SM, et al. Differences in DNA methylation signatures reveal multiple pathways of progression from adenoma to colorectal cancer. Gastroenterology. 2014;147(2):418–29. doi:10.1053/j.gastro.2014.04.039. e8.
45. Kodach LL, Jacobs RJ, Voorneveld PW, Wildenberg ME, Verspaget HW, van Wezel T, et al. Statins augment the chemosensitivity of colorectal cancer cells inducing epigenetic reprogramming and reducing colorectal cancer cell ‘stemness’ via the bone morphogenetic protein pathway. Gut. 2011;60(11):1544–53. doi:10.1136/gut.2011.237495.
46. Thiel A, Heinonen M, Kantonen J, Gylling A, Lahtinen L, Korhonen M, et al. BRAF mutation in sporadic colorectal cancer and Lynch syndrome. Virchows Archiv: an international journal of pathology. 2013;463(5):613–21. doi:10.1007/s00428-013-1470-9.
47. Loukola A, Eklin K, Laiho P, Salovaara R, Kristo P, Jarvinen H, et al. Microsatellite marker analysis in screening for hereditary nonpolyposis colorectal cancer (HNPCC). Cancer Res. 2001;61(11):4545–9.
48. Esemuede I, Forslund A, Khan SA, Qin LX, Gimbel MI, Nash GM, et al. Improved testing for microsatellite instability in colorectal cancer using a simplified 3-marker assay. Ann Surg Oncol. 2010;17(12):3370–8. doi:10.1245/s10434-010-1147-4.
49. Nygren AO, Ameziane N, Duarte HM, Vijzelaar RN, Waisfisz Q, Hess CJ, et al. Methylation-specific MLPA (MS-MLPA): simultaneous detection of CpG methylation and copy number changes of up to 40 sequences. Nucleic Acids Res. 2005;33(14):e128. doi:10.1093/nar/gni127.
50. MRC Holland. http://mrc-holland.com. Accessed 5 March 2015.
51. Pavicic W, Perkio E, Kaur S, Peltomaki P. Altered methylation at microRNA-associated CpG islands in hereditary and sporadic carcinomas: a methylation-specific multiplex ligation-dependent probe amplification (MS-MLPA)-based approach. Mol Med. 2011;17(7–8):726–35. doi:10.2119/molmed.2010.00239.
52. 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(7):787–93. doi:10.1038/ng1834.
53. Ogino S, Kawasaki T, Kirkner GJ, Kraft P, Loda M, Fuchs CS. Evaluation of markers for CpG island methylator phenotype (CIMP) in colorectal cancer by a large population-based sample. The Journal of molecular diagnostics: JMD. 2007;9(3):305–14. doi:10.2353/jmoldx.2007.060170.
54. EMBOSS CpGplot. http://www.ebi.ac.uk/Tools/seqstats/emboss_cpgplot. Accessed 5 March 2015.
55. CpG Island Searcher. http://cpgislands.usc.edu. Accessed 5 March 2015.
56. Niskakoski A, Kaur S, Staff S, Renkonen-Sinisalo L, Lassus H, Jarvinen HJ, et al. Epigenetic analysis of sporadic and Lynch-associated ovarian cancers reveals histology-specific patterns of DNA methylation. Epigenetics: official journal of the DNA Methylation Society. 2014;9(12):1577–87. doi:10.4161/15592294.2014.983374.