Systematic CpG islands methylation profiling of genes in the wnt pathway in epithelial ovarian cancer identifies biomarkers of progression-free survival

Clinical Cancer Research

Volumn 17, Issue 12, 2011, Pages 4052-4062

  Dai, Wei ^a   Teodoridis, Jens M ^a   Zeller, Constanze ^a   Graham, Janet ^a   Hersey, Jenny ^b   Flanagan, James M ^a   Stronach, Euan ^a   Millan, David W ^c   Siddiqui, Nadeem ^d   Paul, Jim ^c   Brown, Robert ^a,b  

^a HAMMERSMITH HOSPITAL   (United Kingdom)

^b INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^c BEATSON WEST OF SCOTLAND CANCER CENTRE   (United Kingdom)

^d GLASGOW ROYAL INFIRMARY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; DISHEVELLED 1; DNA; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 5; PLATINUM; PROTEIN AXIN1; PROTEIN CCND1; PROTEIN CCND3; PROTEIN CTBP1; PROTEIN FRAT1; PROTEIN FZD4; PROTEIN FZD9; PROTEIN NKD1; PROTEIN NKD2; PROTEIN PPP2R2B; PROTEIN ROCK1; PROTEIN RUVBL1; SECRETED FRIZZLED RELATED PROTEIN 5; TRANSCRIPTION FACTOR NFAT; TRANSCRIPTION FACTOR NFATC3; UNCLASSIFIED DRUG; WNT PROTEIN; WNT4 PROTEIN;

ARTICLE; AXIN1 GENE; CANCER GROWTH; CANCER RELAPSE; CCND1 GENE; CCND3 GENE; COHORT ANALYSIS; CONTROLLED STUDY; CPG ISLAND; CTBP1 GENE; CYTOREDUCTIVE SURGERY; DIFFERENTIAL METHYLATION HYBRIDIZATION; DNA METHYLATION; DVL1 GENE; EPIGENETICS; EPITHELIAL OVARY CANCER; FEMALE; FRAT1 GENE; FZD4 GENE; FZD9 GENE; GENE EXPRESSION PROFILING; GENE LOCUS; GENOME SIZE; HUMAN; HUMAN TISSUE; HYBRIDIZATION; LRP5 GENE; MAJOR CLINICAL STUDY; NFATC3 GENE; NKD1 GENE; NKD2 GENE; OVARY CANCER; OVERALL SURVIVAL; PPP2R2B GENE; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; PROMOTER REGION; PROSPECTIVE STUDY; PROTEIN EXPRESSION; ROCK1 GENE; RUVBL1 GENE; SFRP5 GENE; TREATMENT RESPONSE; TUMOR BIOPSY; WNT4 GENE;

ADULT; AGED; AGED, 80 AND OVER; CARRIER PROTEINS; COHORT STUDIES; CPG ISLANDS; DISEASE-FREE SURVIVAL; DNA METHYLATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MIDDLE AGED; NEOPLASM STAGING; NEOPLASMS, GLANDULAR AND EPITHELIAL; OVARIAN NEOPLASMS; REPRODUCIBILITY OF RESULTS; SIGNAL TRANSDUCTION; TUMOR MARKERS, BIOLOGICAL; WNT PROTEINS;

EID: 79959218200     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-10-3021     Document Type: Article

References (66)

1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ. Cancer statistics, 2009. CA Cancer J Clin 2009;59:225-49.
2. Agarwal R, Kaye SB. Ovarian cancer: strategies for overcoming resistance to chemotherapy. Nat Rev Cancer 2003;3:502-16. (Pubitemid 37328838)
3. Konstantinopoulos PA, Spentzos D, Cannistra SA. Gene-expression profiling in epithelial ovarian cancer. Nat Clin Pract Oncol 2008;5:577-87.
4. Kulasingam V, Pavlou MP, Diamandis EP. Integrating high-throughput technologies in the quest for effective biomarkers for ovarian cancer. Nat Rev Cancer 2010;10:371-8.
5. Cannistra SA. Cancer of the ovary. N Engl J Med 2004;351:2519-29.
6. Bristow RE, Tomacruz RS, Armstrong DK, Trimble EL, Montz FJ. Survival effect of maximal cytoreductive surgery for advanced ovarian carcinoma during the platinum era: a meta-analysis. J Clin Oncol 2002;20:1248-59. (Pubitemid 34177431)
7. Thigpen T, Brady MF, Omura GA, Creasman WT, McGuire WP, Hoskins WJ, et al. Age as a prognostic factor in ovarian carcinoma. The Gynecologic Oncology Group experience. Cancer 1993;71:606-14.
8. Havrilesky L, Darcy M, Hamdan H, Priore RL, Leon J, Bell J, et al. Prognostic significance of p53 mutation and p53 overexpression in advanced epithelial ovarian cancer: a Gynecologic Oncology Group Study. J Clin Oncol 2003;21:3814-25. (Pubitemid 46606237)
9. Berchuck A, Kamel A, Whitaker R, Kerns B, Olt G, Kinney R, et al. Overexpression of HER-2/neu is associated with poor survival in advanced epithelial ovarian cancer. Cancer Res 1990;50:4087-91. (Pubitemid 20225635)
10. Lee YK, Park NH. Prognostic value and clinicopathological significance of p53 and PTEN in epithelial ovarian cancers. Gynecol Oncol 2009;112:475-80.
11. Verri E, Guglielmini P, Puntoni M, Perdelli L, Papadia A, Lorenzi P, et al. HER2/neu oncoprotein overexpression in epithelial ovarian cancer: evaluation of its prevalence and prognostic significance. Clinical study.Oncology 2005;68:154-61. (Pubitemid 41158970)
12. Rustin GJ, van der Burg ME, Griffin CL, Guthrie D, Lamont A, Jayson GC, et al. Early versus delayed treatment of relapsed ovarian cancer (MRC OV05/EORTC 55955): a randomised trial. Lancet 2010;376:1155-63.
13. Havrilesky LJ, Whitehead CM, Rubatt JM, Cheek RL, Groelke J, He Q, et al. Evaluation of biomarker panels for early stage ovarian cancer detection and monitoring for disease recurrence. Gynecol Oncol 2008;110:374-82.
14. Anastasi E, Marchei GG, Viggiani V, Gennarini G, Frati L, Reale MG. HE4: a new potential early biomarker for the recurrence of ovarian cancer. Tumour Biol 2010;31:113-9.
15. Moore RG, MacLaughlan S, Bast RC Jr. Current state of biomarker development for clinical application in epithelial ovarian cancer. Gynecol Oncol 2010;116:240-5.
16. Illingworth RS, Bird AP. CpG islands-'a rough guide'. FEBS Lett 2009;583:1713-20.
17. Wei SH, Balch C, Paik HH, Kim YS, Baldwin RL, Liyanarachchi S, et al. Prognostic DNA methylation biomarkers in ovarian cancer. Clin Cancer Res 2006;12:2788-94.
18. Chou JL, Su HY, Chen LY, Liao YP, Hartman-Frey C, Lai YH, et al. Promoter hypermethylation of FBXO32, a novel TGF-beta/SMAD4 target gene and tumor suppressor, is associated with poor prognosis in human ovarian cancer. Lab Invest 2010;90:414-25.
19. Li M, Balch C, Montgomery JS, Jeong M, Chung JH, Yan P, et al. Integrated analysis of DNA methylation and gene expression reveals specific signaling pathways associated with platinum resistance in ovarian cancer. BMC Med Genomics 2009;2:34.
20. Boyer A, Goff AK, Boerboom D. WNT signaling in ovarian follicle biology and tumorigenesis. Trends Endocrinol Metab 2009;21:25-32.
21. McDonald SL, Silver A. The opposing roles of Wnt-5a in cancer. Br J Cancer 2009;101:209-14.
22. Ricken A, Lochhead P, Kontogiannea M, Farookhi R. Wnt signaling in the ovary: identification and compartmentalized expression of wnt-2, wnt-2b, and frizzled-4 mRNAs. Endocrinology 2002;143:2741-9. (Pubitemid 34701338)
23. van Amerongen R, Nawijn MC, Lambooij JP, Proost N, Jonkers J, Berns A. Frat oncoproteins act at the crossroad of canonical and noncanonical Wnt-signaling pathways. Oncogene 2010;29:93-104.
24. Gatcliffe TA, Monk BJ, Planutis K, Holcombe RF. Wnt signaling in ovarian tumorigenesis. Int J Gynecol Cancer 2008;18:954-62.
25. Vogelstein B, Fearon ER, Hamilton SR, Kern SE, Preisinger AC, Leppert M, et al. Genetic alterations during colorectal-tumor development. N Engl J Med 1988;319:525-32.
26. Sparks AB, Morin PJ, Vogelstein B, Kinzler KW. Mutational analysis of the APC/beta-catenin/Tcf pathway in colorectal cancer. Cancer Res 1998;58:1130-4. (Pubitemid 28183198)
27. Ueda M, Gemmill RM, West J, Winn R, Sugita M, Tanaka N, et al. Mutations of the beta- and gamma-catenin genes are uncommon in human lung, breast, kidney, cervical and ovarian carcinomas. Br J Cancer 2001;85:64-8. (Pubitemid 32695717)
28. Wu R, Hendrix-Lucas N, Kuick R, Zhai Y, Schwartz DR, Akyol A, et al. Mouse model of human ovarian endometrioid adenocarcinoma based on somatic defects in the Wnt/beta-catenin and PI3K/Pten signaling pathways. Cancer Cell 2007;11:321-33. (Pubitemid 46518315)
29. Miller JR, Hocking AM, Brown JD, Moon RT. Mechanism and function of signal transduction by the Wnt/beta-catenin and Wnt/Ca2+ pathways. Oncogene 1999;18:7860-72. (Pubitemid 30066232)
30. Wang Y. Wnt/Planar cell polarity signaling: a new paradigm for cancer therapy. Mol Cancer Ther 2009;8:2103-9.
31. Akira K, Hideki Y. Tumor formation due to abnormalities in the beta-catenin-independent pathway of Wnt signaling. Cancer Sci 2008;99:202-8.
32. Klarmann GJ, Decker A, Farrar WL. Epigenetic gene silencing in the Wnt pathway in breast cancer. Epigenetics 2008;3:59-63.
33. Valencia A, Román-Gómez J, Cervera J, Such E, Barragán E, Bolufer P, et al. Wnt signaling pathway is epigenetically regulated by methylation of Wnt antagonists in acute myeloid leukemia. Leukemia 2009;23:1658-66.
34. Ying Y, Tao Q. Epigenetic disruption of the WNT/beta-catenin signaling pathway in human cancers. Epigenetics 2009;4:307-12.
35. Bennett LB, Taylor KH, Arthur GL, Rahmatpanah FB, Hooshmand SI, Caldwell CW. Epigenetic regulation of WNT signaling in chronic lymphocytic leukemia. Epigenomics 2010;2:53-70.
36. Deng Y, Yu B, Cheng Q, Jin J, You H, Ke R, et al. Epigenetic silencing of WIF-1 in hepatocellular carcinomas. J Cancer Res Clin Oncol 2010;136:1161-7.
37. Yu J, Tao Q, Cheng YY, Lee KY, Ng SS, Cheung KF, et al. Promoter methylation of the Wnt/beta-catenin signaling antagonist Dkk-3 is associated with poor survival in gastric cancer. Cancer 2009;115:49-60.
38. Takada T, Yagi Y, Maekita T, Imura M, Nakagawa S, Tsao SW, et al. Methylation-associated silencing of the Wnt antagonist SFRP1 gene in human ovarian cancers. Cancer Sci 2004;95:741-4. (Pubitemid 39335094)
39. Veeck J, Niederacher D, An H, Klopocki E, Wiesmann F, Betz B, et al. Aberrant methylation of the Wnt antagonist SFRP1 in breast cancer is associated with unfavourable prognosis. Oncogene 2006;25:3479-88.
40. Su HY, Lai HC, Lin YW, Liu CY, Chen CK, Chou YC, et al. Epigenetic silencing of SFRP5 is related to malignant phenotype and chemoresistance of ovarian cancer through Wnt signaling pathway. Int J Cancer 2010;127:555-67.
41. Rosen DG, Yang G, Liu G, Mercado-Uribe I, Chang B, Xiao XS, et al. Ovarian cancer: pathology, biology, and disease models. Front Biosci 2009;14:2089-102.
42. Sugiyama T, Kamura T, Kigawa J, Terakawa N, Kikuchi Y, Kita T, et al. Clinical characteristics of clear cell carcinoma of the ovary: a distinct histologic type with poor prognosis and resistance to platinum-based chemotherapy. Cancer 2000;88:2584-9. (Pubitemid 30331967)
43. Strathdee G, MacKean MJ, Illand M, Brown R. A role for methylation of the hMLH1 promoter in loss of hMLH1 expression and drug resistance in ovarian cancer. Oncogene 1999;18:2335-41. (Pubitemid 29192710)
44. Nouzova M, Holtan N, Oshiro MM, Isett RB, Munoz-Rodriguez JL, List AF, et al. Epigenomic changes during leukemia cell differentiation: analysis of histone acetylation and cytosine methylation using CpG island microarrays. J Pharmacol Exp Ther 2004;311:968-81. (Pubitemid 39612701)
45. Stewart FJ, Raleigh EA. Dependence of McrBC cleavage on distance between recognition elements. Biol Chem 1998;379:611-6. (Pubitemid 28209945)
46. Sutherland E, Coe L, Raleigh EA. McrBC: a multisubunit GTP-dependent restriction endonuclease. J Mol Biol 1992;225:327-48.
47. Troyanskaya O, Cantor M, Sherlock G, Brown P, Hastie T, Tibshirani R, et al. Missing value estimation methods for DNA microarrays. Bioinformatics 2001;17:520-5. (Pubitemid 32600498)
48. Hastie T, Tibshirani R, Sherlock G, Eisen M, Brown P, Bostein D. Imputing missing data for gene expression arrays: Standord University Statistics Department Technical report 1999.
49. Dai W, Teodoridis JM, Graham J, Zeller C, Huang TH, Yan P, et al. Methylation Linear Discriminant Analysis (MLDA) for identifying differentially methylated CpG islands. BMC Bioinformatics 2008;9:337.
50. Kanehisa M, Goto S, Furumichi M, Tanabe M, Hirakawa M. KEGG for representation and analysis of molecular networks involving diseases and drugs. Nucleic Acids Res 2010;38:D355-60.
51. Rhead B, Karolchik D, Kuhn RM, Hinrichs AS, Zweig AS, Fujita PA, et al. The UCSC Genome Browser database: update 2010. Nucleic Acids Res 2010;38:D613-9.
52. Bock C, Walter J, Paulsen M, Lengauer T. CpG island mapping by epigenome prediction. PLoS Comput Biol 2007;3:e110.
53. Gardiner-Garden M, Frommer M. CpG islands in vertebrate genomes. J Mol Biol 1987;196:261-82. (Pubitemid 17122132)
54. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B Methodol 1995;57:289-300.
55. McShane LM, Altman DG, Sauerbrei W, Taube SE, Gion M, Clark GM. Reporting recommendations for tumor marker prognostic studies. J Clin Oncol 2005;23:9067-72.
56. Lee YN, Gao Y, Wang HY. Differential mediation of the Wnt canonical pathway by mammalian Dishevelleds-1, -2, and -3. Cell Signal 2008;20:443-52.
57. Cho KR, Shih Ie M. Ovarian cancer. Ann Rev Pathol 2009;4:287-313.
58. Bese T, Barbaros M, Baykara E, Guralp O, Cengiz S, Demirkiran F, et al. Comparison of total plasma lysophosphatidic acid and serum CA-125 as a tumor marker in the diagnosis and follow-up of patients with epithelial ovarian cancer. J Gynecol Oncol 2010;21:248-54.
59. Crijns AP, Fehrmann RS, de Jong S, Gerbens F, Meersma GJ, Klip HG, et al. Survival-related profile, pathways, and transcription factors in ovarian cancer. PLoS Med 2009;6:e24.
60. Tothill RW, Tinker AV, George J, Brown R, Fox SB, Lade S, et al. Novel molecular subtypes of serous and endometrioid ovarian cancer linked to clinical outcome. Clin Cancer Res 2008;14:5198-208.
61. van Jaarsveld MT, Helleman J, Berns EM, Wiemer EA. MicroRNAs in ovarian cancer biology and therapy resistance. Int J Biochem Cell Biol 2010;42:1282-90.
62. Anglim PP, Alonzo TA, Laird-Offringa IA. DNA methylation-based biomarkers for early detection of non-small cell lung cancer: an update. Mol Cancer 2008;7:81.
63. Laird PW. The power and the promise of DNA methylation markers. Nat Rev Cancer 2003;3:253-66. (Pubitemid 37328861)
64. Cottrell SE, Laird PW. Sensitive detection of DNA methylation. Ann N Y Acad Sci 2003;983:120-30. (Pubitemid 36399325)
65. Gifford G, Paul J, Vasey PA, Kaye SB, Brown R. The acquisition of hMLH1 methylation in plasma DNA after chemotherapy predicts poor survival for ovarian cancer patients. Clin Cancer Res 2004;10:4420-6. (Pubitemid 38878884)
66. Luu HH, Zhang R, Haydon RC, Rayburn E, Kang Q, Si W, et al. Wnt/beta-catenin signaling pathway as a novel cancer drug target. Curr Cancer Drug Targets 2004;4:653-71. (Pubitemid 40013572)