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Research Paper

Recurrent patterns of DNA methylation in the ZNF154,CASP8, and VHL promoters across a wide spectrum of human solid epithelial tumors and cancer cell lines

, , , , , , & show all
Pages 1355-1372 | Received 09 Aug 2013, Accepted 03 Oct 2013, Published online: 22 Oct 2013

References

  • Robertson KD. DNA methylation and human disease. Nat Rev Genet 2005; 6:597 - 610; http://dx.doi.org/10.1038/nrg1655; PMID: 16136652
  • Jaenisch R, Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 2003; 33:Suppl 245 - 54; http://dx.doi.org/10.1038/ng1089; PMID: 12610534
  • Portela A, Esteller M. Epigenetic modifications and human disease. Nat Biotechnol 2010; 28:1057 - 68; http://dx.doi.org/10.1038/nbt.1685; PMID: 20944598
  • Baylin SB, Jones PA. A decade of exploring the cancer epigenome - biological and translational implications. Nat Rev Cancer 2011; 11:726 - 34; http://dx.doi.org/10.1038/nrc3130; PMID: 21941284
  • Sproul D, Meehan RR. Genomic insights into cancer-associated aberrant CpG island hypermethylation. Brief Funct Genomics 2013; 12:174 - 90; http://dx.doi.org/10.1093/bfgp/els063; PMID: 23341493
  • Heichman KA, Warren JD. DNA methylation biomarkers and their utility for solid cancer diagnostics. Clin Chem Lab Med 2012; 50:1707 - 21; http://dx.doi.org/10.1515/cclm-2011-0935; PMID: 23089699
  • Jones PA, Baylin SB. The fundamental role of epigenetic events in cancer. Nat Rev Genet 2002; 3:415 - 28
  • Rodríguez-Paredes M, Esteller M. Cancer epigenetics reaches mainstream oncology. Nat Med 2011; 17:330 - 9; http://dx.doi.org/10.1038/nm.2305; PMID: 21386836
  • Esteller M. Epigenetic changes in cancer. F1000 Biol Rep 2011; 3:9; http://dx.doi.org/10.3410/B3-9; PMID: 21655338
  • Bock C. Analysing and interpreting DNA methylation data. Nat Rev Genet 2012; 13:705 - 19; http://dx.doi.org/10.1038/nrg3273; PMID: 22986265
  • Irizarry RA, Ladd-Acosta C, Wen B, Wu Z, Montano C, Onyango P, Cui H, Gabo K, Rongione M, Webster M, 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; http://dx.doi.org/10.1038/ng.298; PMID: 19151715
  • Jones PA. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet 2012; 13:484 - 92; http://dx.doi.org/10.1038/nrg3230; PMID: 22641018
  • Chi P, Allis CD, Wang GG. Covalent histone modifications--miswritten, misinterpreted and mis-erased in human cancers. Nat Rev Cancer 2010; 10:457 - 69; http://dx.doi.org/10.1038/nrc2876; PMID: 20574448
  • Cedar H, Bergman Y. Linking DNA methylation and histone modification: patterns and paradigms. Nat Rev Genet 2009; 10:295 - 304; http://dx.doi.org/10.1038/nrg2540; PMID: 19308066
  • Esteller M. Cancer epigenomics: DNA methylomes and histone-modification maps. Nat Rev Genet 2007; 8:286 - 98; http://dx.doi.org/10.1038/nrg2005; PMID: 17339880
  • Weisenberger DJ, Siegmund KD, Campan M, Young J, Long TI, Faasse MA, Kang GH, Widschwendter M, Weener D, Buchanan D, 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; http://dx.doi.org/10.1038/ng1834; PMID: 16804544
  • Ye D, Xiong Y, Guan K-L. The mechanisms of IDH mutations in tumorigenesis. Cell Res 2012; 22:1102 - 4; http://dx.doi.org/10.1038/cr.2012.51; PMID: 22453240
  • Reinert T, Borre M, Christiansen A, Hermann GG, Ørntoft TF, Dyrskjøt L. Diagnosis of bladder cancer recurrence based on urinary levels of EOMES, HOXA9, POU4F2, TWIST1, VIM, and ZNF154 hypermethylation. Christensen BC, ed. PLoS One 2012; 7(10):e46297;
  • Yin A, Zhang X, Wu J, Du L, He T, Zhang X. Screening significantly hypermethylated genes in fetal tissues compared with maternal blood using a methylated-CpG island recovery assay-based microarray. BMC Med Genomics 2012; 5:26; http://dx.doi.org/10.1186/1755-8794-5-26; PMID: 22709530
  • Lange CPE, Campan M, Hinoue T, et al. Genome-scale discovery of DNA-methylation biomarkers for blood-based detection of colorectal cancer. Marsit CJ, ed. PLoS One 2012; 7(11):e50266;
  • Carmona FJ, Azuara D, Berenguer-Llergo A, Fernández AF, Biondo S, de Oca J, Rodriguez-Moranta F, Salazar R, Villanueva A, Fraga MF, et al. DNA methylation biomarkers for noninvasive diagnosis of colorectal cancer. Cancer Prev Res (Phila) 2013; 6:656 - 65; http://dx.doi.org/10.1158/1940-6207.CAPR-12-0501; PMID: 23694962
  • Ma Y, Wang X, Jin H. Methylated DNA and microRNA in Body Fluids as Biomarkers for Cancer Detection. Int J Mol Sci 2013; 14:10307 - 31; http://dx.doi.org/10.3390/ijms140510307; PMID: 23681012
  • Heyn H, Esteller M. DNA methylation profiling in the clinic: applications and challenges. Nat Rev Genet 2012; 13:679 - 92; http://dx.doi.org/10.1038/nrg3270; PMID: 22945394
  • Herman JG, Latif F, Weng Y, Lerman MI, Zbar B, Liu S, Samid D, Duan DS, Gnarra JR, Linehan WM, et al. Silencing of the VHL tumor-suppressor gene by DNA methylation in renal carcinoma. Proc Natl Acad Sci U S A 1994; 91:9700 - 4; http://dx.doi.org/10.1073/pnas.91.21.9700; PMID: 7937876
  • Kolbe DL, DeLoia JA, Porter-Gill P, et al. Differential analysis of ovarian and endometrial cancers identifies a methylator phenotype. Califano J, ed. PLoS One 2012; 7(3):e32941;
  • Leek JT, Scharpf RB, Bravo HC, Simcha D, Langmead B, Johnson WE, Geman D, Baggerly K, Irizarry RA. Tackling the widespread and critical impact of batch effects in high-throughput data. Nat Rev Genet 2010; 11:733 - 9; http://dx.doi.org/10.1038/nrg2825; PMID: 20838408
  • Harper KN, Peters BA, Gamble MV. Batch effects and pathway analysis: two potential perils in cancer studies involving DNA methylation array analysis. Cancer Epidemiol Biomarkers Prev 2013; 22:1052 - 60; http://dx.doi.org/10.1158/1055-9965.EPI-13-0114; PMID: 23629520
  • Varley KE, Gertz J, Bowling KM, Parker SL, Reddy TE, Pauli-Behn F, Cross MK, Williams BA, Stamatoyannopoulos JA, Crawford GE, et al. Dynamic DNA methylation across diverse human cell lines and tissues. Genome Res 2013; 23:555 - 67; http://dx.doi.org/10.1101/gr.147942.112; PMID: 23325432
  • Cancer Genome Atlas Research Network. Comprehensive genomic characterization of squamous cell lung cancers. Nature 2012; 489:519 - 25; http://dx.doi.org/10.1038/nature11404; PMID: 22960745
  • Cancer Genome Atlas Research Network. Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 2008; 455:1061 - 8; http://dx.doi.org/10.1038/nature07385; PMID: 18772890
  • Cancer Genome Atlas Research Network. Integrated genomic analyses of ovarian carcinoma. Nature 2011; 474:609 - 15; http://dx.doi.org/10.1038/nature10166; PMID: 21720365
  • Cancer Genome Atlas Network. Comprehensive molecular characterization of human colon and rectal cancer. Nature 2012; 487:330 - 7; http://dx.doi.org/10.1038/nature11252; PMID: 22810696
  • Cancer Genome Atlas Network. Comprehensive molecular portraits of human breast tumours. Nature 2012; 490:61 - 70; http://dx.doi.org/10.1038/nature11412; PMID: 23000897
  • Kandoth C, Schultz N, Cherniack AD, Akbani R, Liu Y, Shen H, Robertson AG, Pashtan I, Shen R, Benz CC, et al, Cancer Genome Atlas Research Network. Integrated genomic characterization of endometrial carcinoma. Nature 2013; 497:67 - 73; http://dx.doi.org/10.1038/nature12113; PMID: 23636398
  • Bernstein BE, Birney E, Dunham I, Green ED, Gunter C, Snyder M, ENCODE Project Consortium. An integrated encyclopedia of DNA elements in the human genome. Nature 2012; 489:57 - 74; http://dx.doi.org/10.1038/nature11247; PMID: 22955616
  • Hansen KD, Timp W, Bravo HC, Sabunciyan S, Langmead B, McDonald OG, Wen B, Wu H, Liu Y, Diep D, et al. Increased methylation variation in epigenetic domains across cancer types. Nat Genet 2011; 43:768 - 75; http://dx.doi.org/10.1038/ng.865; PMID: 21706001
  • Zhuang J, Jones A, Lee S-H, et al. The dynamics and prognostic potential of DNA methylation changes at stem cell gene loci in women’s cancer. Absher D, ed. PLoS Genet 2012; 8(2):e1002517;
  • Sproul D, Kitchen RR, Nestor CE, Dixon JM, Sims AH, Harrison DJ, Ramsahoye BH, Meehan RR. Tissue of origin determines cancer-associated CpG island promoter hypermethylation patterns. Genome Biol 2012; 13:R84; http://dx.doi.org/10.1186/gb-2012-13-10-r84; PMID: 23034185
  • May T, Virtanen C, Sharma M, Milea A, Begley H, Rosen B, Murphy KJ, Brown TJ, Shaw PA. Low malignant potential tumors with micropapillary features are molecularly similar to low-grade serous carcinoma of the ovary. Gynecol Oncol 2010; 117:9 - 17; http://dx.doi.org/10.1016/j.ygyno.2010.01.006; PMID: 20117829
  • Ogino S, Kawasaki T, Kirkner GJ, Ohnishi M, Fuchs CS. 18q loss of heterozygosity in microsatellite stable colorectal cancer is correlated with CpG island methylator phenotype-negative (CIMP-0) and inversely with CIMP-low and CIMP-high. BMC Cancer 2007; 7:72; http://dx.doi.org/10.1186/1471-2407-7-72; PMID: 17474983
  • 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; http://dx.doi.org/10.2353/jmoldx.2006.060082; PMID: 17065427
  • Strathdee G, Appleton K, Illand M, Millan DW, Sargent J, Paul J, Brown R. Primary ovarian carcinomas display multiple methylator phenotypes involving known tumor suppressor genes. Am J Pathol 2001; 158:1121 - 7; http://dx.doi.org/10.1016/S0002-9440(10)64059-X; PMID: 11238060
  • Keshet I, Lieman-Hurwitz J, Cedar H. DNA methylation affects the formation of active chromatin. Cell 1986; 44:535 - 43; http://dx.doi.org/10.1016/0092-8674(86)90263-1; PMID: 3456276
  • Karlić R, Chung H-R, Lasserre J, Vlahovicek K, Vingron M. Histone modification levels are predictive for gene expression. Proc Natl Acad Sci U S A 2010; 107:2926 - 31; http://dx.doi.org/10.1073/pnas.0909344107; PMID: 20133639
  • Ooi SKT, Qiu C, Bernstein E, Li K, Jia D, Yang Z, Erdjument-Bromage H, Tempst P, Lin SP, Allis CD, et al. DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 2007; 448:714 - 7; http://dx.doi.org/10.1038/nature05987; PMID: 17687327
  • Okitsu CY, Hsieh C-L. DNA methylation dictates histone H3K4 methylation. Mol Cell Biol 2007; 27:2746 - 57; http://dx.doi.org/10.1128/MCB.02291-06; PMID: 17242185
  • Tommerup N, Vissing H. Isolation and fine mapping of 16 novel human zinc finger-encoding cDNAs identify putative candidate genes for developmental and malignant disorders. Genomics 1995; 27:259 - 64; http://dx.doi.org/10.1006/geno.1995.1040; PMID: 7557990
  • Laity JH, Lee BM, Wright PE. Zinc finger proteins: new insights into structural and functional diversity. Curr Opin Struct Biol 2001; 11:39 - 46; http://dx.doi.org/10.1016/S0959-440X(00)00167-6; PMID: 11179890
  • O’Geen H, Squazzo SL, Iyengar S, et al. Genome-wide analysis of KAP1 binding suggests autoregulation of KRAB-ZNFs. Ecker JR, ed. PLoS Genet 2007; 3(6):e89;
  • Long HK, Blackledge NP, Klose RJ. ZF-CxxC domain-containing proteins, CpG islands and the chromatin connection. Biochem Soc Trans 2013; 41:727 - 40; http://dx.doi.org/10.1042/BST20130028; PMID: 23697932
  • Abdollahi A, Roberts D, Godwin AK, Schultz DC, Sonoda G, Testa JR, Hamilton TC. Identification of a zinc-finger gene at 6q25: a chromosomal region implicated in development of many solid tumors. Oncogene 1997; 14:1973 - 9; http://dx.doi.org/10.1038/sj.onc.1201034; PMID: 9150364
  • Hajra KM, Chen DY-S, Fearon ER. The SLUG zinc-finger protein represses E-cadherin in breast cancer. Cancer Res 2002; 62:1613 - 8; PMID: 11912130
  • Zhang X, Jing Y, Qin Y, Hunsucker S, Meng H, Sui J, Jiang Y, Gao L, An G, Yang N, et al. The zinc finger transcription factor ZKSCAN3 promotes prostate cancer cell migration. Int J Biochem Cell Biol 2012; 44:1166 - 73; http://dx.doi.org/10.1016/j.biocel.2012.04.005; PMID: 22531714
  • Vanaja DK, Cheville JC, Iturria SJ, Young CYF. Transcriptional silencing of zinc finger protein 185 identified by expression profiling is associated with prostate cancer progression. Cancer Res 2003; 63:3877 - 82; PMID: 12873976
  • Yu Q, Zhang K, Wang X, Liu X, Zhang Z. Expression of transcription factors snail, slug, and twist in human bladder carcinoma. J Exp Clin Cancer Res 2010; 29:119; http://dx.doi.org/10.1186/1756-9966-29-119; PMID: 20809941
  • Reinert T, Modin C, Castano FM, Lamy P, Wojdacz TK, Hansen LL, Wiuf C, Borre M, Dyrskjøt L, Orntoft TF. Comprehensive genome methylation analysis in bladder cancer: identification and validation of novel methylated genes and application of these as urinary tumor markers. Clin Cancer Res 2011; 17:5582 - 92; http://dx.doi.org/10.1158/1078-0432.CCR-10-2659; PMID: 21788354
  • Hill VK, Ricketts C, Bieche I, Vacher S, Gentle D, Lewis C, Maher ER, Latif F. Genome-wide DNA methylation profiling of CpG islands in breast cancer identifies novel genes associated with tumorigenicity. Cancer Res 2011; 71:2988 - 99; http://dx.doi.org/10.1158/0008-5472.CAN-10-4026; PMID: 21363912
  • Poage GM, Butler RA, Houseman EA, McClean MD, Nelson HH, Christensen BC, Marsit CJ, Kelsey KT. Identification of an epigenetic profile classifier that is associated with survival in head and neck cancer. Cancer Res 2012; 72:2728 - 37; http://dx.doi.org/10.1158/0008-5472.CAN-11-4121-T; PMID: 22507853
  • Lleras RA, Smith RV, Adrien LR, Schlecht NF, Burk RD, Harris TM, Childs G, Prystowsky MB, Belbin TJ. Unique DNA Methylation Loci Distinguish Anatomic Site and HPV Status in Head and Neck Squamous Cell Carcinoma. Clin Cancer Res 2013; 19:5444 - 55; http://dx.doi.org/10.1158/1078-0432.CCR-12-3280; PMID: 23894057
  • Shen J, Wang S, Zhang Y-J, Kappil M, Wu HC, Kibriya MG, Wang Q, Jasmine F, Ahsan H, Lee PH, et al. Genome-wide DNA methylation profiles in hepatocellular carcinoma. Hepatology 2012; 55:1799 - 808; http://dx.doi.org/10.1002/hep.25569; PMID: 22234943
  • Okamoto T, Yamaguchi K, Huang Z, et al. Methylated-mediated repression of ZNF154 in ovarian cancer is associated with poor overall survival–[Abstract]. In: Proceedings of the 103rd Annual Meeting of the American Association for Cancer Research 2012; Available at: http://cancerres.aacrjournals.org/cgi/content/short/72/8_MeetingAbstracts/LB-87?rss=1. Accessed June 4, 2013.
  • Mahapatra S, Klee EW, Young CYF, Sun Z, Jimenez RE, Klee GG, Tindall DJ, Donkena KV. Global methylation profiling for risk prediction of prostate cancer. Clin Cancer Res 2012; 18:2882 - 95; http://dx.doi.org/10.1158/1078-0432.CCR-11-2090; PMID: 22589488
  • Arai E, Chiku S, Mori T, Gotoh M, Nakagawa T, Fujimoto H, Kanai Y. Single-CpG-resolution methylome analysis identifies clinicopathologically aggressive CpG island methylator phenotype clear cell renal cell carcinomas. Carcinogenesis 2012; 33:1487 - 93; http://dx.doi.org/10.1093/carcin/bgs177; PMID: 22610075
  • Mazumder S, Almasan A. Is caspase-8 a neuroendocrine lung tumor suppressor?. Cancer Biol Ther 2002; 1:70 - 1; http://dx.doi.org/10.4161/cbt.1.1.46; PMID: 12197486
  • Fulda S, Küfer MU, Meyer E, van Valen F, Dockhorn-Dworniczak B, Debatin K-M. Sensitization for death receptor- or drug-induced apoptosis by re-expression of caspase-8 through demethylation or gene transfer. Oncogene 2001; 20:5865 - 77; http://dx.doi.org/10.1038/sj.onc.1204750; PMID: 11593392
  • Shiao Y-H. The von Hippel-Lindau gene and protein in tumorigenesis and angiogenesis: a potential target for therapeutic designs. Curr Med Chem 2003; 10:2461 - 70; http://dx.doi.org/10.2174/0929867033456639; PMID: 14529485
  • Kondo K, Kaelin WG Jr.. The von Hippel-Lindau tumor suppressor gene. Exp Cell Res 2001; 264:117 - 25; http://dx.doi.org/10.1006/excr.2000.5139; PMID: 11237528
  • Miranda TB, Jones PA. DNA methylation: the nuts and bolts of repression. J Cell Physiol 2007; 213:384 - 90; http://dx.doi.org/10.1002/jcp.21224; PMID: 17708532
  • Jurkowska RZ, Jeltsch A. Silencing of gene expression by targeted DNA methylation: concepts and approaches. Methods Mol Biol 2010; 649:149 - 61; http://dx.doi.org/10.1007/978-1-60761-753-2_9; PMID: 20680833
  • Chen YA, Lemire M, Choufani S, Butcher DT, Grafodatskaya D, Zanke BW, Gallinger S, Hudson TJ, Weksberg R. Discovery of cross-reactive probes and polymorphic CpGs in the Illumina Infinium HumanMethylation450 microarray. Epigenetics 2013; 8:203 - 9; http://dx.doi.org/10.4161/epi.23470; PMID: 23314698
  • Rosenbloom KR, Dreszer TR, Long JC, Malladi VS, Sloan CA, Raney BJ, Cline MS, Karolchik D, Barber GP, Clawson H, et al. ENCODE whole-genome data in the UCSC Genome Browser: update 2012. Nucleic Acids Res 2012; 40:Database issue D912 - 7; http://dx.doi.org/10.1093/nar/gkr1012; PMID: 22075998
  • Krueger F, Andrews SR. Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics 2011; 27:1571 - 2; http://dx.doi.org/10.1093/bioinformatics/btr167; PMID: 21493656
  • Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods 2012; 9:357 - 9; http://dx.doi.org/10.1038/nmeth.1923; PMID: 22388286
  • Wang K, Singh D, Zeng Z, Coleman SJ, Huang Y, Savich GL, He X, Mieczkowski P, Grimm SA, Perou CM, et al. MapSplice: accurate mapping of RNA-seq reads for splice junction discovery. Nucleic Acids Res 2010; 38:e178; http://dx.doi.org/10.1093/nar/gkq622; PMID: 20802226
  • Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 2011; 12:323; http://dx.doi.org/10.1186/1471-2105-12-323; PMID: 21816040
  • Leek JT, Scharpf RB, Bravo HC, Simcha D, Langmead B, Johnson WE, Geman D, Baggerly K, Irizarry RA. Tackling the widespread and critical impact of batch effects in high-throughput data. Nat Rev Genet 2010; 11:733 - 9; http://dx.doi.org/10.1038/nrg2825; PMID: 20838408
  • Dy JG, Brodley CE. Feature Selection for Unsupervised Learning. J Mach Learn Res 2004; 5:845 - 89

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