Aberrant DNA methylation profiles of inherited and sporadic colorectal cancer

Clinical Epigenetics

Volumn 7, Issue 1, 2015, Pages

  Sahnane, Nora ^a   Magnoli, Francesca ^a   Bernasconi, Barbara ^a   Tibiletti, Maria Grazia ^b   Romualdi, Chiara ^c   Pedroni, Monica ^d   De Leon, Maurizio Ponz ^d   Magnani, Giulia ^d   Reggiani Bonetti, Luca ^e   Bertario, Lucio ^f   Signoroni, Stefano ^f   Capella, Carlo ^a   Sessa, Fausto ^a   Furlan, Daniela ^a  

^a UNIVERSITY OF INSUBRIA   (Italy)

^b OSPEDALE DI CIRCOLO   (Italy)

^c UNIVERSITY OF PADOVA   (Italy)

^d UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^e UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^f NATIONAL CANCER INSTITUTE   (Italy)

Author keywords

Colorectal cancer; Early onset colorectal cancer; Gene hypermethylation; LINE 1; Lynch syndrome; Microsatellite instability

Indexed keywords

ESTROGEN RECEPTOR; TRANSCRIPTION FACTOR GATA 5; WT1 PROTEIN;

ADULT; AGED; ARTICLE; CANCER PROGNOSIS; CHROMOSOMAL INSTABILITY; COLORECTAL CANCER; CONTROLLED STUDY; DISEASE ASSOCIATION; DNA METHYLATION; EPIGENETICS; FEMALE; GENE DELETION; GENE LOSS; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; ONCOGENE K RAS; PHENOTYPE; PRIORITY JOURNAL; TUMOR SUPPRESSOR GENE;

EID: 84951024460     PISSN: 18687075     EISSN: 18687083     Source Type: Journal    
DOI: 10.1186/s13148-015-0165-2     Document Type: Article

References (65)

1. 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;229:697-704.
2. 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;22:271-82.
3. Nejman D, Straussman R, Steinfeld I, Ruvolo M, Roberts D, Yakhini Z, et al. Molecular rules governing de novo methylation in cancer. Cancer Res. 2014;74:1475-83.
4. Yagi K, Akagi K, Hayashi H, Nagae G, Tsuji S, Isagawa T, et al. Three DNA methylation epigenotypes in human colorectal cancer. Clin Cancer Res. 2009;16:21-33.
5. Baylin SB, Jones PA. A decade of exploring the cancer epigenome—biological and translational implications. Nat Rev Cancer. 2011;11:726-34.
6. Lange CP, Campan M, Hinoue T, Schmitz RF, van der Meulen-De Jong AE, Slingerland H, et al. Genome-scale discovery of DNA-methylation biomarkers for blood-based detection of colorectal cancer. PLoS One. 2012;7:e50266.
7. Lofton-Day C, Model F, Devos T, Tetzner R, Distler J, Schuster M, et al. DNA methylation biomarkers for blood-based colorectal cancer screening. Clin Chem. 2008;54:414-23.
8. Warren JD, Xiong W, Bunker AM, Vaughn CP, Furtado LV, Roberts WL, et al. Septin 9 methylated DNA is a sensitive and specific blood test for colorectal cancer. BMC Med. 2011;9:133.
9. 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;31:1158-63.
10. 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.
11. Jass JR. Classification of colorectal cancer based on correlation of clinical, morphological and molecular features. Histopathol. 2007;50:113-30.
12. 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.
13. Network CGA. Comprehensive molecular characterization of human colon and rectal cancer. Nature. 2012;487:330-7.
14. Fang M, Ou J, Hutchinson L, Green MR. The BRAF oncoprotein functions through the transcriptional repressor MAFG to mediate the CpG island methylator phenotype. Mol Cell. 2014;55:904-15.
15. Nazemalhosseini Mojarad E, Kuppen PJ, Aghdaei HA, Zali MR. The CpG island methylator phenotype (CIMP) in colorectal cancer. Gastroenterol Hepatol Bed Bench. 2013;6:120-8.
16. Sproul D, Meehan RR. Genomic insights into cancer-associated aberrant CpG island hypermethylation. Brief Funct Genomics. 2013;12:174-90.
17. Chalitchagorn K, Shuangshoti S, Hourpai N, Kongruttanachok N, Tangkijvanich P, Thong-ngam D, et al. Distinctive pattern of LINE-1 methylation level in normal tissues and the association with carcinogenesis. Oncogene. 2004;23:8841-6.
18. Feinberg AP, Vogelstein B. Hypomethylation of ras oncogenes in primary human cancers. Biochem Biophys Res Commun. 1983;111:47-54.
19. 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.
20. Gasior SL, Wakeman TP, Xu B, Deininger PL. The human LINE-1 retrotransposon creates DNA double-strand breaks. J Mol Biol. 2006;357:1383-93.
21. 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;300:489-92.
22. 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.
23. Yamada Y, Jackson-Grusby L, Linhart H, Meissner A, Eden A, Lin H, et al. Opposing effects of DNA hypomethylation on intestinal and liver carcinogenesis. Proc Natl Acad Sci U S A. 2005;102:13580-5.
24. Hur K, Cejas P, Feliu J, Moreno-Rubio J, Burgos E, Boland CR, et al. Hypomethylation of long interspersed nuclear element-1 (LINE-1) leads to activation of proto-oncogenes in human colorectal cancer metastasis. Gut. 2014;63:635-46.
25. Baba Y, Murata A, Watanabe M, Baba H. Clinical implications of the LINE-1 methylation levels in patients with gastrointestinal cancer. Surg Today. 2014;44:1807-16.
26. Miousse IR, Chalbot MC, Aykin-Burns N, Wang X, Basnakian A, Kavouras IG, et al. Epigenetic alterations induced by ambient particulate matter in mouse macrophages. Environ Mol Mutagen. 2014;55:428-35.
27. Murata A, Baba Y, Watanabe M, Shigaki H, Miyake K, Ishimoto T, et al. Methylation levels of LINE-1 in primary lesion and matched metastatic lesions of colorectal cancer. Br J Cancer. 2013;109:408-15.
28. Baba Y, Huttenhower C, Nosho K, Tanaka N, Shima K, Hazra A, et al. Epigenomic diversity of colorectal cancer indicated by LINE-1 methylation in a database of 869 tumors. Mol Cancer. 2010;9:125.
29. Goel A, Xicola RM, Nguyen TP, Doyle BJ, Sohn VR, Bandipalliam P, et al. Aberrant DNA methylation in hereditary nonpolyposis colorectal cancer without mismatch repair deficiency. Gastroenterol. 2010;138:1854-62.
30. Antelo M, Balaguer F, Shia J, Shen Y, Hur K, Moreira L, et al. A high degree of LINE-1 hypomethylation is a unique feature of early-onset colorectal cancer. PLoS One. 2012;7:e45357.
31. Inamura K, Yamauchi M, Nishihara R, Lochhead P, Qian ZR, Kuchiba A, et al. Tumor LINE-1 methylation level and microsatellite instability in relation to colorectal cancer prognosis. J Natl Cancer Inst. 2014;106:9.
32. Kirzin S, Marisa L, Guimbaud R, De Reynies A, Legrain M, Laurent-Puig P, et al. Sporadic early-onset colorectal cancer is a specific sub-type of cancer: a morphological, molecular and genetics study. PLoS One. 2014;9:e103159.
33. Magnani G, Furlan D, Sahnane, N., Reggiani Bonetti L, Domati F, and Pedroni M. Molecular features and methylation status in early onset (=40 year) colorectal cancer: a population based, case-control study. Gastroenterology Research and Practice 2015;in press.
34. Bardhan K, Liu K. Epigenetics and colorectal cancer pathogenesis. Cancers (Basel). 2013;5:676-713.
35. Colussi D, Brandi G, Bazzoli F, Ricciardiello L. Molecular pathways involved in colorectal cancer: implications for disease behavior and prevention. Int J Mol Sci. 2013;14:16365-85.
36. Sunami E, de Maat M, Vu A, Turner RR, Hoon DS. LINE-1 hypomethylation during primary colon cancer progression. PLoS One. 2011;6:e18884.
37. Matsunoki A, Kawakami K, Kotake M, Kaneko M, Kitamura H, Ooi A, et al. LINE-1 methylation shows little intra-patient heterogeneity in primary and synchronous metastatic colorectal cancer. BMC Cancer. 2012;12:574.
38. 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.
39. Hubbard JM, Grothey A. Adolescent and young adult colorectal cancer. J Natl Compr Canc Netw. 2013;11:1219-25.
40. Mork ME, You YN, Ying J, Bannon SA, Lynch PM, Rodriguez-Bigas MA, et al. High prevalence of hereditary cancer syndromes in adolescents and young adults with colorectal cancer. J Clin Oncol. 2015;33(31):3544-9.
41. Rodriguez-Bigas MA, Mahoney MC, Weber TK, Petrelli NJ. Colorectal cancer in patients aged 30 years or younger. Surg Oncol. 1996;5:189-94.
42. Ogino S, Kawasaki T, Kirkner GJ, Loda M, Fuchs CS. CpG island methylator phenotype-low (CIMP-low) in colorectal cancer: possible associations with male sex and KRAS mutations. J Mol Diagn. 2006;8:582-8.
43. Zampieri M, Ciccarone F, Calabrese R, Franceschi C, Burkle A, Caiafa P. Reconfiguration of DNA methylation in aging. Mech Ageing Dev. 2015;151:60-70.
44. Hiltunen MO, Koistinaho J, Alhonen L, Myohanen S, Marin S, Kosma VM, et al. Hypermethylation of the WT1 and calcitonin gene promoter regions at chromosome 11p in human colorectal cancer. Br J Cancer. 1997;76:1124-30.
45. Jia Y, Guo M. Epigenetic changes in colorectal cancer. Chin J Cancer. 2013;32:21-30.
46. Ottaviano YL, Issa JP, Parl FF, Smith HS, Baylin SB, Davidson NE. Methylation of the estrogen receptor gene CpG island marks loss of estrogen receptor expression in human breast cancer cells. Cancer Res. 1994;54:2552-5.
47. Xu XL, Yu J, Zhang HY, Sun MH, Gu J, Du X, et al. Methylation profile of the promoter CpG islands of 31 genes that may contribute to colorectal carcinogenesis. World J Gastroenterol. 2004;10:3441-54.
48. Valo S, Kaur S, Ristimaki A, Renkonen-Sinisalo L, Jarvinen H, Mecklin JP, et al. DNA hypermethylation appears early and shows increased frequency with dysplasia in Lynch syndrome-associated colorectal adenomas and carcinomas. Clin Epigenetics. 2015;7:71.
49. Mima K, Nishihara R, Qian ZR, Cao Y, Sukawa Y, Nowak JA, et al., Fusobacterium nucleatum in colorectal carcinoma tissue and patient prognosis. Gut 2015. doi: 10.1136/gutjnl-2015-310101
50. Tahara T, Yamamoto E, Suzuki H, Maruyama R, Chung W, Garriga J, et al. Fusobacterium in colonic flora and molecular features of colorectal carcinoma. Cancer Res. 2014;74:1311-8.
51. Ogino S, Lochhead P, Chan AT, Nishihara R, Cho E, Wolpin BM, et al. Molecular pathological epidemiology of epigenetics: emerging integrative science to analyze environment, host, and disease. Mod Pathol. 2013;26:465-84.
52. 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;49:151-7.
53. Roberts SA, Gordenin DA. Hypermutation in human cancer genomes: footprints and mechanisms. Nat Rev Cancer. 2014;14:786-800.
54. Greenman C, Stephens P, Smith R, Dalgliesh GL, Hunter C, Bignell G, et al. Patterns of somatic mutation in human cancer genomes. Nature. 2007;446:153-8.
55. Hodgkinson A, Eyre-Walker A. Variation in the mutation rate across mammalian genomes. Nat Rev Genet. 2011;12:756-66.
56. Vogelstein B, Papadopoulos N, Velculescu VE, Zhou S, Diaz Jr LA, Kinzler KW. Cancer genome landscapes. Science. 2013;339:1546-58.
57. Hamilton SR, Vogelstein B, Kudo S, Riboli E, Nakamura S, Hainaut P, et al. Tumours of the Colon and Rectum. In: Hamilton SR, Aaltonen LA, editors. WHO Classification Pathology & Genetics, Tumours of the Digestive System. Lyon: IARC Press; 2000. p. 103-44.
58. Edge SB BD, Compton CC, Fritz AG, Greene FL, Trotti A. Colon and rectum. In: Edge SB, editor. TNM classification of malignant tumors. New York: Springer; 2010. p. 173-206.
59. Yang AS, Estecio MR, Doshi K, Kondo Y, Tajara EH, Issa JP. A simple method for estimating global DNA methylation using bisulfite PCR of repetitive DNA elements. Nucleic Acids Res. 2004;32:e38.
60. Stefanoli M, La Rosa S, Sahnane N, Romualdi C, Pastorino R, Marando A, et al. Prognostic relevance of aberrant DNA methylation in g1 and g2 pancreatic neuroendocrine tumors. Neuroendocrinol. 2014;100:26-34.
61. Furlan D, Sahnane N, Mazzoni M, Pastorino R, Carnevali I, Stefanoli M, et al. Diagnostic utility of MS-MLPA in DNA methylation profiling of adenocarcinomas and neuroendocrine carcinomas of the colon-rectum. Virchows Arch. 2013;462:47-56.
62. Sahnane N, Furlan D, Monti M, Romualdi C, Vanoli A, Vicari E, et al. Microsatellite unstable gastrointestinal neuroendocrine carcinomas: a new clinicopathologic entity. Endocr Relat Cancer. 2014;22:35-45.
63. Furlan D, Sahnane N, Bernasconi B, Frattini M, Tibiletti MG, Molinari F, et al. APC alterations are frequently involved in the pathogenesis of acinar cell carcinoma of the pancreas, mainly through gene loss and promoter hypermethylation. Virchows Arch. 2014;464:553-64.
64. Schwarz G. Estimating the dimension of a model. Ann Stat. 1978;6:461-4.
65. Raftery CFaAE. Model-based clustering, discriminant analysis, and density estimation. J Am Stat Assoc. 2002;97:611-31.