Genome-scale analysis of DNA methylation in colorectal cancer using Infinium HumanMethylation450 BeadChips

Epigenetics

Volumn 8, Issue 9, 2013, Pages 921-934

  Naumov, Vladimir A ^a   Generozov, Edward V ^a   Zaharjevskaya, Natalya B ^a   Matushkina, Darya S ^a   Larin, Andrey K ^a   Chernyshov, Stanislav V ^b   Alekseev, Mikhail V ^b   Shelygin, Yuri A ^b   Govorun, Vadim M ^a  

^a FEDERAL RESEARCH AND CLINICAL CENTER OF PHYSICAL CHEMICAL MEDICINE OF FEDERAL MEDICAL BIOLOGICAL AGENCY   (Russian Federation)

^b State Research Center of Coloproctology   (Russian Federation)

Author keywords

450K BeadChip; Alterations; Colorectal cancer; DNA methylation; Genome wide

Indexed keywords

BETA CATENIN; CADHERIN; LIVER RECEPTOR HOMOLOG 1; NEUROGENIN 1; SEPTIN; SMAD3 PROTEIN; SOMATOMEDIN B RECEPTOR; SUPPRESSOR OF CYTOKINE SIGNALING 1; TRANSCRIPTION FACTOR RUNX3; VIMENTIN; WNT PROTEIN;

ADULT; AREA UNDER THE CURVE; ARTICLE; CELL ADHESION; CELL MIGRATION; CLINICAL ARTICLE; COLONOSCOPY; COLORECTAL CANCER; CONTROLLED STUDY; DNA METHYLATION; DNA MICROARRAY; FEMALE; GENE EXPRESSION; GENETIC HETEROGENEITY; GENETIC VARIABILITY; GENOMIC INSTABILITY; HUMAN; HUMAN TISSUE; HUMANMETHYLATION450 BEADCHIP MICROARRAY; MALE; PREVALENCE; SENSITIVITY AND SPECIFICITY; SIGNAL TRANSDUCTION;

450K BEADCHIP; ALTERATIONS; COLORECTAL CANCER; DNA METHYLATION; GENOME-WIDE;

CLUSTER ANALYSIS; COLORECTAL NEOPLASMS; CPG ISLANDS; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENETIC LOCI; GENETIC MARKERS; GENOME, HUMAN; GENOMICS; HUMANS; MALE; MIDDLE AGED; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RISK FACTORS; TUMOR CELLS, CULTURED;

EID: 84883520928     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/epi.25577     Document Type: Article

References (62)

1. Avksentyeva M. Colorectal cancer in Russia. Eur J Health Econ 2010; 10(Suppl 1):S91-8; PMID:20012132; http://dx.doi.org/10.1007/s10198-009-0195-9
2. Cancer Genome Atlas Research Network. Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 2008; 455:1061-8; PMID:18772890; http://dx.doi. org/10.1038/nature07385
3. Cancer Genome Atlas Research Network. Integrated genomic analyses of ovarian carcinoma. Nature 2011; 474:609-15; PMID:21720365; http://dx.doi. org/10.1038/nature10166
4. Cancer Genome Atlas Network. Comprehensive molecular characterization of human colon and rectal cancer. Nature 2012; 487:330-7; PMID:22810696; http://dx.doi.org/10.1038/nature11252
5. Fearon ER. Molecular genetics of colorectal cancer. Annu Rev Pathol 2011; 6:479-507; PMID:21090969; http:// dx.doi.org/10.1146/annurev-pathol-011110-130235
6. Pfeifer GP, Rauch TA. DNA methylation patterns in lung carcinomas. Semin Cancer Biol 2009; 19:181-7; PMID:19429482; http://dx.doi.org/10.1016/j.semcancer. 2009.02.008
7. Costello JF, Frühwald MC, Smiraglia DJ, Rush LJ, Robertson GP, Gao X, et al. Aberrant CpG-island methylation has non-random and tumour-type-specific patterns. Nat Genet 2000; 24:132-8; PMID:10655057; http://dx.doi.org/10.1038/72785
8. Irizarry RA, Ladd-Acosta C, Wen B, Wu Z, Montano C, Onyango P, 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; PMID:19151715; http://dx.doi. org/10.1038/ng.298
9. Bibikova M, Barnes B, Tsan C, Ho V, Klotzle B, Le JM, et al. High density DNA methylation array with single CpG site resolution. Genomics 2011; 98:288-95; PMID:21839163; http://dx.doi.org/10.1016/j. ygeno.2011.07.007
10. Dedeurwaerder S, Defrance M, Calonne E, Denis H, Sotiriou C, Fuks F. Evaluation of the Infinium Methylation 450K technology. Epigenomics 2011; 3:771-84; PMID:22126295; http://dx.doi. org/10.2217/epi.11.105
11. Touleimat N, Tost J. Complete pipeline for Infinium(®) Human Methylation 450K BeadChip data processing using subset quantile normalization for accurate DNA methylation estimation. Epigenomics 2012; 4:325-41; PMID:22690668; http://dx.doi. org/10.2217/epi.12.21
12. Wang D, Yan L, Hu Q, Sucheston LE, Higgins MJ, Ambrosone CB, et al. IMA: an R package for high-throughput analysis of Illumina's 450K Infinium methylation data. Bioinformatics 2012; 28:729-30; PMID:22253290; http://dx.doi.org/10.1093/bioinformatics/ bts013
13. Belshaw NJ, Elliott GO, Foxall RJ, Dainty JR, Pal N, Coupe A, et al. Profiling CpG island field methylation in both morphologically normal and neoplastic human colonic mucosa. Br J Cancer 2008; 99:136-42; PMID:18542073; http://dx.doi.org/10.1038/ sj.bjc.6604432
14. Nosho K, Kawasaki T, Ohnishi M, Suemoto Y, Kirkner GJ, Zepf D, et al. PIK3CA mutation in colorectal cancer: relationship with genetic and epigenetic alterations. Neoplasia 2008; 10:534-41; PMID:18516290
15. 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; 97:1330-8; PMID:16174854; http://dx.doi. org/10.1093/jnci/dji275
16. 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; 59:1516-26; PMID:20947886; http://dx.doi.org/10.1136/gut.2009.194787
17. Kibriya MG, Raza M, Jasmine F, Roy S, Paul-Brutus R, Rahaman R, et al. A genome-wide DNA methylation study in colorectal carcinoma. BMC Med Genomics 2011; 4:50; PMID:21699707; http:// dx.doi.org/10.1186/1755-8794-4-50
18. KimYH, LeeHC, KimSY, YeomYI, RyuKJ, MinBH, et al. Epigenomic analysis of aberrantly methylated genes in colorectal cancer identifies genes commonly affected by epigenetic alterations. Ann Surg Oncol 2011; 18:2338-47; PMID:21298349; http://dx.doi. org/10.1245/s10434-011-1573-y
19. Oster B, Thorsen K, Lamy P, Wojdacz TK, Hansen LL, Birkenkamp-Demtröder K, et al. Identification and validation of highly frequent CpG island hypermethylation in colorectal adenomas and carcinomas. Int J Cancer 2011; 129:2855-66; PMID:21400501; http:// dx.doi.org/10.1002/ijc.25951
20. Ausch C, Kim YH, Tsuchiya KD, Dzieciatkowski S, Washington MK, Paraskeva C, et al. Comparative analysis of PCR-based biomarker assay methods for colorectal polyp detection from fecal DNA. Clin Chem 2009; 55:1559-63; PMID:19541867; http://dx.doi. org/10.1373/clinchem.2008.122937
21. Issa JP, Vertino PM, Boehm CD, Newsham IF, Baylin SB. Switch from monoallelic to biallelic human IGF2 promoter methylation during aging and carcinogenesis. Proc Natl Acad Sci U S A 1996; 93:11757-62; PMID:8876210; http://dx.doi.org/10.1073/ pnas.93.21.11757
22. Jubb AM, Quirke P, Oates AJ. DNA methylation, a biomarker for colorectal cancer: implications for screening and pathological utility. Ann N Y Acad Sci 2003; 983:251-67; PMID:12724230; http://dx.doi. org/10.1111/j.1749-6632.2003.tb05980.x
23. 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; PMID:18089654; http://dx.doi. org/10.1373/clinchem.2007.095992
24. McLean CY, Bristor D, Hiller M, Clarke SL, Schaar BT, Lowe CB, et al. GREAT improves functional interpretation of cis-regulatory regions. Nat Biotechnol 2010; 28:495-501; PMID:20436461; http://dx.doi. org/10.1038/nbt.1630
25. Dexter D, Prodduturi N, Zhang B. WebGestalt2: an updated and expanded version of the Web-based Gene Set Analysis Toolkit. BMC Bioinformatics 2010; 11:1-10; PMID:20043860
26. Simmer F, Brinkman AB, Assenov Y, Matarese F, Kaan A, Sabatino L, et al. Comparative genome-wide DNA methylation analysis of colorectal tumor and matched normal tissues. Epigenetics 2012; 7:1355-67; PMID:23079744; http://dx.doi.org/10.4161/ epi.22562
27. Lascorz J, Hemminki K, Försti A. Systematic enrichment analysis of gene expression profiling studies identifies consensus pathways implicated in colorectal cancer development. J Carcinog 2011; 10:7; PMID:21483658; http://dx.doi.org/10.4103/1477-3163.78268
28. Kongkham PN, Northcott PA, Croul SE, Smith CA, Taylor MD, Rutka JT. The SFRP family of WNT inhibitors function as novel tumor suppressor genes epigenetically silenced in medulloblastoma. Oncogene2010; 29:3017-24; PMID:20208569; http://dx.doi.org/10.1038/onc.2010.32
29. Vincent A, Omura N, Hong SM, Jaffe A, Eshleman J, Goggins M. Genome-wide analysis of promoter methylation associated with gene expression profile in pancreatic adenocarcinoma. Clin Cancer Res 2011; 17:4341-54; PMID:21610144; http://dx.doi. org/10.1158/1078-0432.CCR-10-3431
30. Suzuki H, Gabrielson E, Chen W, Anbazhagan R, van Engeland M, Weijenberg MP, et al. A genomic screen for genes upregulated by demethylation and histone deacetylase inhibition in human colorectal cancer. Nat Genet 2002; 31:141-9; PMID:11992124; http:// dx.doi.org/10.1038/ng892
31. Wheeler JM, Kim HC, Efstathiou JA, Ilyas M, Mortensen NJ, Bodmer WF. Hypermethylation of the promoter region of the E-cadherin gene (CDH1) in sporadic and ulcerative colitis associated colorectal cancer. Gut 2001; 48:367-71; PMID:11171827; http:// dx.doi.org/10.1136/gut.48.3.367
32. Nanjo S, Asada K, Yamashita S, Nakajima T, Nakazawa K, Maekita T, et al. Identification of gastric cancer risk markers that are informative in individuals with past H. pylori infection. Gastric Cancer 2012; 15:382-8; PMID:22237657; http://dx.doi.org/10.1007/s10120-011-0126-1
33. 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; PMID:10411935; http://dx.doi. org/10.1073/pnas.96.15.8681
34. 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; PMID:16804544; http://dx.doi.org/10.1038/ng1834
35. Curtin K, Slattery ML, Samowitz WS. CpG island methylation in colorectal cancer: past, present and future. Patholog Res Int 2011; 2011:902674; PMID:21559209
36. Slattery ML, Wolff RK, Curtin K, Fitzpatrick F, Herrick J, Potter JD, et al. Colon tumor mutations and epigenetic changes associated with genetic polymorphism: insight into disease pathways. Mutat Res 2009; 660:12-21; PMID:18992263; http://dx.doi. org/10.1016/j.mrfmmm.2008.10.001
37. Barault L, Charon-Barra C, Jooste V, de la Vega MF, Martin L, Roignot P, et al. Hypermethylator phenotype in sporadic colon cancer: study on a population-based series of 582 cases. Cancer Res 2008; 68:8541-6; PMID:18922929; http://dx.doi.org/10.1158/0008-5472.CAN-08-1171
38. Shen L, Toyota M, Kondo Y, Lin E, Zhang L, Guo Y, et al. Integrated genetic and epigenetic analysis identifies three different subclasses of colon cancer. Proc Natl Acad Sci U S A 2007; 104:18654-9; PMID:18003927; http://dx.doi.org/10.1073/pnas.0704652104
39. Mikeska T, Bock C, Do H, Dobrovic A. DNA methylation biomarkers in cancer: progress towards clinical implementation. Expert Rev Mol Diagn 2012; 12:473-87; PMID:22702364; http://dx.doi.org/10.1586/ erm.12.45
40. 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; PMID:16077070; http://dx.doi.org/10.1093/jnci/ dji204
41. Tóth K, Sipos F, Kalmár A, Patai AV, Wichmann B, Stoehr R, et al. Detection of methylated SEPT9 in plasma is a reliable screening method for both left-and right-sided colon cancers. PLoS One 2012; 7:e46000; PMID:23049919; http://dx.doi.org/10.1371/journal. pone.0046000
42. Feinberg AP, Vogelstein B. Hypomethylation distinguishes genes of some human cancers from their normal counterparts. Nature 1983; 301:89-92; PMID:6185846; http://dx.doi.org/10.1038/301089a0
43. Bock C, Walter J, Paulsen M, Lengauer T. Interindividual variation of DNA methylation and its implications for large-scale epigenome mapping. Nucleic Acids Res 2008; 36:e55; PMID:18413340; http:// dx.doi.org/10.1093/nar/gkn122
44. Byun HM, Siegmund KD, Pan F, Weisenberger DJ, Kanel G, Laird PW, et al. Epigenetic profiling of somatic tissues from human autopsy specimens identifies tissue-and individual-specific DNA methylation patterns. Hum Mol Genet 2009; 18:4808-17; PMID:19776032; http://dx.doi.org/10.1093/hmg/ ddp445
45. Gervin K, Hammerø M, Akselsen HE, Moe R, Nygård H, Brandt I, et al. Extensive variation and low heritability of DNA methylation identified in a twin study. Genome Res 2011; 21:1813-21; PMID:21948560; http://dx.doi.org/10.1101/gr.119685.110
46. Krausz C, Sandoval J, Sayols S, Chianese C, Giachini C, Heyn H, et al. Novel insights into DNA methylation features in spermatozoa: stability and peculiarities. PLoS One 2012; 7:e44479; PMID:23071498; http:// dx.doi.org/10.1371/journal.pone.0044479
47. 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; PMID:21659424; http://dx.doi.org/10.1101/gr.117523.110
48. Sproul D, Nestor C, Culley J, Dickson JH, Dixon JM, Harrison DJ, et al. Transcriptionally repressed genes become aberrantly methylated and distinguish tumors of different lineages in breast cancer. Proc Natl Acad Sci U S A 2011; 108:4364-9; PMID:21368160; http:// dx.doi.org/10.1073/pnas.1013224108
49. Ying Z, Li J, Li M. Astrocyte elevated gene 1: biological functions and molecular mechanism in cancer and beyond. Cell Biosci 2011; 1:36; PMID:22060137; http://dx.doi.org/10.1186/2045-3701-1-36
50. Tsuchiya N, Nakagama H. MicroRNA, SND1, and alterations in translational regulation in colon carcinogenesis. Mutat Res 2010; 693:94-100; PMID:20883704; http://dx.doi.org/10.1016/j.mrfmmm. 2010.09.001
51. Kuruma H, Kamata Y, Takahashi H, Igarashi K, Kimura T, Miki K, et al. Staphylococcal nuclease domain-containing protein 1 as a potential tissue marker for prostate cancer. Am J Pathol 2009; 174:2044-50; PMID:19435788; http://dx.doi.org/10.2353/ ajpath.2009.080776
52. Wang N, Du X, Zang L, Song N, Yang T, Dong R, et al. Prognostic impact of Metadherin-SND1 interaction in colon cancer. Mol Biol Rep2012; 39:10497-504; PMID:23065261; http://dx.doi.org/10.1007/s11033-012-1933-0
53. Kardon T, Noël G, Vertommen D, Schaftingen EV. Identification of the gene encoding hydroxyacid-oxoacid transhydrogenase, an enzyme that metabolizes 4-hydroxybutyrate. FEBS Lett 2006; 580:2347-50; PMID:16616524; http://dx.doi.org/10.1016/j.febslet. 2006.02.082
54. Xu Y, Hu B, Choi AJ, Gopalan B, Lee BH, Kalady MF, et al. Unique DNA methylome profiles in CpG island methylator phenotype colon cancers. Genome Res 2012; 22:283-91; PMID:21990380; http://dx.doi. org/10.1101/gr.122788.111
55. Shen J, Wang S, Zhang YJ, Wu HC, Kibriya MG, Jasmine F, et al. Exploring genome-wide DNA methylation profiles altered in hepatocellular carcinoma using Infinium HumanMethylation 450 BeadChips. Epigenetics 2013; 8:34-43; PMID:23208076; http:// dx.doi.org/10.4161/epi.23062
56. Kaifi JT, Wagner M, Schurr PG, Wachowiak R, Reichelt U, Yekebas EF, et al. Allelic loss of Hox11L1 gene locus predicts outcome of gastrointestinal stromal tumors. Oncol Rep 2006; 16:915-9; PMID:16969514
57. Li SY, An P, Cai HY, Bai X, Zhang YN, Yu B, et al. Proteomic analysis of differentially expressed proteins involving in liver metastasis of human colorectal carcinoma. Hepatobiliary Pancreat Dis Int 2010; 9:149-53; PMID:20382585
58. Schoonjans K, Dubuquoy L, Mebis J, Fayard E, Wendling O, Haby C, et al. Liver receptor homolog 1 contributes to intestinal tumor formation through effects on cell cycle and inflammation. Proc Natl Acad Sci U S A 2005; 102:2058-62; PMID:15684064; http://dx.doi.org/10.1073/pnas.0409756102
59. Petersen GM, Amundadottir L, Fuchs CS, Kraft P, Stolzenberg-Solomon RZ, Jacobs KB, et al. A genome-wide association study identifies pancreatic cancer susceptibility loci on chromosomes 13q22.1, 1q32.1 and 5p15.33. Nat Genet 2010; 42:224-8; PMID:20101243; http://dx.doi.org/10.1038/ng.522
60. Minsky BD. Unique considerations in the patient with rectal cancer. Semin Oncol2011; 38:542-51; PMID:21810513; http://dx.doi.org/10.1053/j.seminoncol. 2011.05.008
61. Sandoval J, Heyn H, Moran S, Serra-Musach J, Pujana MA, Bibikova M, et al. Validation of a DNA methylation microarray for 450,000 CpG sites in the human genome. Epigenetics 2011; 6:692-702; PMID:21593595; http://dx.doi.org/10.4161/ epi.6.6.16196
62. DeLong ER, DeLong DM, Clarke-Pearson DL. Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics 1988; 44:837-45; PMID:3203132; http://dx.doi.org/10.2307/2531595