High-frequency aberrantly methylated targets in pancreatic adenocarcinoma identified via global DNA methylation analysis using methylCap-seq

Clinical Epigenetics

Volumn 6, Issue 1, 2014, Pages

  Zhao, Yangxing ^a   Sun, Jinfeng ^b   Zhang, Hongyu ^c   Guo, Shicheng ^d   Gu, Jun ^a   Wang, Wei ^a   Tang, Ning ^c   Zhou, Xiaoyu ^e   Yu, Jian ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b FUDAN UNIVERSITY   (China)

^c SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^d FUDAN UNIVERSITY   (China)

^e SHANGHAI INSTITUTE OF PLANNED PARENTHOOD RESEARCH   (China)

Author keywords

CGI shore; DNA methylation; Genome wide; Methyl capture sequencing; Orphan CGI; Pancreatic adenocarcinoma

Indexed keywords

DNA; TUMOR MARKER;

ADULT; ARTICLE; CARCINOGENESIS; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; EXPRESSED SEQUENCE TAG; FEMALE; GENE EXPRESSION; GENE SEQUENCE; GENOMICS; HUMAN; HUMAN TISSUE; MALE; METHYL CAPTURE SEQUENCING; PANCREAS ADENOCARCINOMA; PANCREATIC CANCER CELL LINE; PRIORITY JOURNAL; PROMOTER REGION; TRANSCRIPTION INITIATION SITE;

EID: 84985009362     PISSN: 18687075     EISSN: 18687083     Source Type: Journal    
DOI: 10.1186/1868-7083-6-18     Document Type: Article

References (53)

1. Jemal A, Siegel R, Ward E, Murray T, Xu J, Thun MJ: Cancer statistics, 2007. CA Cancer J Clin 2007, 57(1): 43-66.
2. Ma C, Jiang YX, Liu SZ, Quan PL, Sun XB, Zheng RS, Zhang SW, Chen WQ: Trend and prediction on the incidence of pancreatic cancer in China. Zhonghua Liu Xing Bing Xue Za Zhi 2013, 34(2): 160-163.
3. Kanwal R, Gupta S: Epigenetic modifications in cancer. Clin Genet 2012, 81: 303-311.
4. Klump B, Hsieh CJ, Nehls O, Dette S, Holzmann K, Kiesslich R, Jung M, Sinn U, Ortner M, Porschen R, Gregor M: Methylation status of p14ARF and p16INK4a as detected in pancreatic secretions. Br J Cancer 2003, 88: 217-222.
5. Dammann R, Schagdarsurengin U, Liu L, Otto N, Gimm O, Dralle H, Boehm BO, Pfeifer GP, Hoang-Vu C: Frequent RASSF1A promoter hypermethylation and K-ras mutations in pancreatic carcinoma. Oncogene 2003, 22: 3806-3812.
6. Omura N, Li CP, Li A, Hong SM, Walter K, Jimeno A, Hidalgo M, Goggins M: Genome-wide profiling of methylated promoters in pancreatic adenocarcinoma. Cancer Biol Ther 2008, 7: 1146-1156.
7. 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(13): 4341-4354.
8. Bock C, Tomazou EM, Brinkman AB, Müller F, Simmer F, Gu H, Jäger N, Gnirke A, Stunnenberg HG, Meissner A: Quantitative comparison of genome-wide DNA methylation mapping technologies. Nat Biotechnol 2010, 28: 1106-1114.
9. Irizarry RA, Ladd-Acosta C, Wen B, Wu Z, Montano C, Onyango P, Cui H, Gabo K, Rongione M, Webster M, Ji H, Potash JB, Sabunciyan S, Feinberg AP: The human colon cancer methylome shows similar hypo- and hypermethylation at conserved tissue-specific CpG island shores. Nat Genet 2009, 41: 178-186.
10. Doi A, Park IH, Wen B, Murakami P, Aryee MJ, Irizarry R, Herb B, Ladd-Acosta C, Rho J, Loewer S, Miller J, Schlaeger T, Daley GQ, Feinberg AP: Differential methylation of tissue and cancer-specific CpG island shores distinguishes human induced pluripotent stem cells, embryonic stem cells and fibroblasts. Nat Genet 2009, 41: 1350-1353.
11. Serre D, Lee BH, Ting AH: MBD-isolated genome sequencing provides a high-throughput and comprehensive survey of DNA methylation in the human genome. Nucleic Acids Res 2010, 38: 391-399.
12. Li LM, Hu ZB, Zhou ZX, Chen X, Liu FY, Zhang JF, Shen HB, Zhang CY, Zen K: Serum microRNA profiles serve as novel biomarkers for HBV infection and diagnosis of HBV-positive hepatocarcinoma. Cancer Res 2010, 70(23): 9798-9807.
13. Deaton AM, Webb S, Kerr AR, Illingworth RS, Guy J, Andrews R, Bird A: Cell type-specific DNA methylation at intragenic CpG islands in the immune system. Genome Res 2011, 21(7): 1074-1086.
14. Helman E, Naxerova K, Kohane IS: DNA hypermethylation in lung cancer is targeted at differentiation-associated genes. Oncogene 2012, 31(9): 1181-1188.
15. Zhao M, Sun J, Zhao Z: TSGene: a web resource for tumor suppressor genes. Nucleic Acids Res 2013, 41(Database issue): D970-D976.
16. Cicek MS, Koestler DC, Fridley BL, Kalli KR, Armasu SM, Larson MC, Wang C, Winham SJ, Vierkant RA, Rider DN, Block MS, Klotzle B, Konecny G, Winterhoff BJ, Hamidi H, Shridhar V, Fan JB, Visscher DW, Olson JE, Hartmann LC, Bibikova M, Chien J, Cunningham JM, Goode EL: Epigenome-wide ovarian cancer analysis identifies a methylation profile differentiating clear-cell histology with epigenetic silencing of the HERG K+ channel. Hum Mol Genet 2013, 22(15): 3038-3047.
17. Sriraksa R, Zeller C, Dai W, Siddiq A, Walley AJ, Limpaiboon T, Brown R: Aberrant DNA methylation at genes associated with a stem cell-like phenotype in cholangiocarcinoma tumors. Cancer Prev Res (Phila) 2013, 6(12): 1348-1355.
18. Wei P, Tang H, Li D: Insights into pancreatic cancer etiology from pathway analysis of genome-wide association study data. PLoS One 2012, 7(10): e46887.
19. Keller A, Ludwig N, Backes C, Romeike BF, Comtesse N, Henn W, Steudel WI, Mawrin C, Lenhof HP, Meese E: Genome wide expression profiling identifies specific deregulated pathways in meningioma. Int J Cancer 2009, 124(2): 346-351.
20. Wang P, Chen L, Zhang J, Chen H, Fan J, Wang K, Luo J, Chen Z, Meng Z, Liu L: Methylation-mediated silencing of the miR-124 genes facilitates pancreatic cancer progression and metastasis by targeting Rac1. Oncogene 2014, 33(4): 514.
21. Gebauer K, Peters I, Dubrowinskaja N, Hennenlotter J, Abbas M, Scherer R, Tezval H, Merseburger AS, Stenzl A, Kuczyk MA, Serth J: Hsa-mir-124-3 CpG island methylation is associated with advanced tumours and disease recurrence of patients with clear cell renal cell carcinoma. Br J Cancer 2013, 108(1): 131-138.
22. Zhao G, Zhang JG, Shi Y, Qin Q, Liu Y, Wang B, Tian K, Deng SC, Li X, Zhu S, Gong Q, Niu Y, Wang CY: MiR-130b is a prognostic marker and inhibits cell proliferation and invasion in pancreatic cancer through targeting STAT3. PLoS One 2013, 8: e73803.
23. Takikawa T, Masamune A, Hamada S, Nakano E, Yoshida N, Shimosegawa T: miR-210 regulates the interaction between pancreatic cancer cells and stellate cells. Biochem Biophys Res Commun 2013, 437(3): 433-439.
24. Heller G, Weinzierl M, Noll C, Babinsky V, Ziegler B, Altenberger C, Minichsdorfer C, Lang G, Döme B, End-Pfützenreuter A, Arns BM, Grin Y, Klepetko W, Zielinski CC, Zöchbauer-Müller S: Genome-wide miRNA expression profiling identifies miR-9-3 and miR-193a as targets for DNA methylation in non-small cell lung cancers. Clin Cancer Res 2012, 18(6): 1619-1629.
25. Lehmann U, Hasemeier B, Christgen M, Müller M, Römermann D, Länger F, Kreipe H: Epigenetic inactivation of microRNA gene hsa-mir-9-1 in human breast cancer. J Pathol 2008, 214(1): 17-24.
26. Wilting SM, van Boerdonk RA, Henken FE, Meijer CJ, Diosdado B, Meijer GA, le Sage C, Agami R, Snijders PJ, Steenbergen RD: Methylation-mediated silencing and tumour suppressive function of hsa-miR-124 in cervical cancer. Mol Cancer 2010, 9: 167.
27. Chim CS, Wong KY, Leung CY, Chung LP, Hui PK, Chan SY, Yu L: Epigenetic inactivation of the hsa-miR-203 in haematological malignancies. J Cell Mol Med 2011, 15(12): 2760-2767.
28. Ma L, Reinhardt F, Pan E, Soutschek J, Bhat B, Marcusson EG, Teruya-Feldstein J, Bell GW, Weinberg RA: Therapeutic silencing of miR-10b inhibits metastasis in a mouse mammary tumor model. Nat Biotechnol 2010, 28: 341-347.
29. Nakata K, Ohuchida K, Mizumoto K, Kayashima T, Ikenaga N, Sakai H, Lin C, Fujita H, Otsuka T, Aishima S, Nagai E, Oda Y, Tanaka M: MicroRNA-10b is overexpressed in pancreatic cancer, promotes its invasiveness, and correlates with a poor prognosis. Surgery 2011, 150(5): 916-922.
30. Sato N, Fukushima N, Maitra A, Matsubayashi H, Yeo CJ, Cameron JL, Hruban RH, Goggins M: Discovery of novel targets for aberrant methylation in pancreatic carcinoma using high-throughput microarrays. Cancer Res 2003, 63: 3735-3742.
31. Kumagai T, Akagi T, Desmond JC, Kawamata N, Gery S, Imai Y, Song JH, Gui D, Said J, Koeffler HP: Epigenetic regulation and molecular characterization of C/EBPα in pancreatic cancer cells. Int J Cancer 2009, 124: 827-833.
32. Ueki T, Toyota M, Sohn T, Yeo CJ, Issa JP, Hruban RH, Goggins M: Hypermethylation of multiple genes in pancreatic adenocarcinoma. Cancer Res 2000, 60: 1835-1839.
33. Matsubayashi H, Sato N, Fukushima N, Yeo CJ, Walter KM, Brune K, Sahin F, Hruban RH, Goggins M: Methylation of cyclin D2 is observed frequently in pancreatic cancer but is also an age-related phenomenon in gastrointestinal tissues. Clin Cancer Res 2003, 9: 1446-1452.
34. Omura N, Goggins M: Epigenetics and epigenetic alterations in pancreatic cancer. Int J Clin Exp Pathol 2009, 2: 310-326.
35. Schutte M, Hruban RH, Geradts J, Maynard R, Hilgers W, Rabindran SK, Moskaluk CA, Hahn SA, Schwarte-Waldhoff I, Schmiegel W, Baylin SB, Kern SE, Herman JG: Abrogation of the Rb/p16 tumor-suppressive path way in virtually all pancreatic carcinomas. Cancer Res 1997, 57: 3126-3130.
36. Nourse C, Kazakoff S, Taylor D, Leonard C, Chang DK, Jones MD, Thomas M, Watson C, Pinese M, Cowley M, Rooman I, APGI, Pajic M, Butturini G, Malpaga A, Corbo V, Crippa S, Falconi M, Zamboni G, Castelli P, Lawlor RT, Gill AJ, Scarpa A, Pearson JV, Biankin AV, Grimmond SM: Genome-wide DNA methylation patterns in pancreatic ductal adenocarcinoma reveal epigenetic deregulation of SLIT-ROBO, ITGA2 and MET signaling. Int J Cancer 2014, 135: 1110-1118.
37. Tan AC, Jimeno A, Lin SH, Wheelhouse J, Chan F, Solomon A, Rajeshkumar NV, Rubio-Viqueira B, Hidalgo M: Characterizing DNA methylation patterns in pancreatic cancer genome. Mol Oncol 2009, 3: 425-438.
38. Deaton AM, Bird A: CpG islands and the regulation of transcription. Genes & Dev 2011, 25: 1010-1022.
39. Illingworth RS, Gruenewald-Schneider U, Webb S, Kerr AR, James KD, Turner DJ, Smith C, Harrison DJ, Andrews R, Bird AP: Orphan CpG islands identify numerous conserved promoters in mammalian genome. PLoS Genet 2010, 6: e1001134.
40. Yu W, Jin C, Lou X, Han X, Li L, He Y, Zhang H, Ma K, Zhu J, Cheng L, Lin B: Global analysis of DNA methylation by methyl-capture sequencing reveals epigenetic control of cisplatin resistance in ovarian cancer cell. PLoS One 2011, 6(12): e29450.
41. Greene FL, Page DL, Fleming ID, Fritz AG, Balch CM, Haller DG, Morrow M: AJCC cancer staging handbook: TNM classification of malignant tumors. 6th edition. New York: Springer-Verlag; 2002: 171-177.
42. Zhao Y, Guo S, Sun J, Huang Z, Zhu T, Zhang H, Gu J, He Y, Wang W, Ma K, Wang J, Yu J: Methylcap-Seq reveals novel DNA methylation markers for the diagnosis and recurrence prediction of bladder cancer in a Chinese population. PLoS One 2012, 7: e35175.
43. Li H, Durbin R: Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009, 25(14): 1754-1760.
44. Kuhn RM, Haussler D, Kent WJ: The UCSC genome browser and associated tools. Brief Bioinform 2012, 14(2): 144-161.
45. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R: The Sequence Alignment/Map format and SAMtools. Bioinformatics 2009, 25(16): 2078-2079.
46. Picard. [http://picard.sourceforge.net]
47. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nusbaum C, Myers RM, Brown M, Li W, Liu XS: Model-based analysis of ChIP-Seq (MACS). Genome Biol 2008, 9: R137.
48. Lan X, Adams C, Landers M, Dudas M, Krissinger D, Marnellos G, Bonneville R, Xu M, Wang J, Huang TH, Meredith G, Jin VX: High resolution detection and analysis of CpG dinucleotides methylation using MBD-Seq technology. PLoS One 2011, 6(7): e22226.
49. Quinlan AR, Hall IM: BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 2010, 26(6): 841-842.
50. David Bioinformatics Resources 6.7. [http://david.abcc.ncifcrf.gov/]
51. Huang ZH, Hu Y, Hua D, Wu YY, Song MX, Cheng ZH: Quantitative analysis of multiple methylated genes in plasma for the diagnosis and prognosis of hepatocellular carcinoma. Exp Mol Pathol 2011, 91(3): 702-707.
52. MethPrimer. [http://www.urogene.org/methprimer/]
53. Primer3. [http://www.embnet.sk/cgi-bin/primer3_www.cgi]