Methylomics analysis identifies epigenetically silenced genes and implies an activation of β-catenin signaling in cervical cancer

International Journal of Cancer

Volumn 135, Issue 1, 2014, Pages 117-127

  Chen, Yu Chih ^a,b   Huang, Rui Lan ^b,c   Huang, Yung Kai ^d   Liao, Yu Ping ^a,b   Su, Po Hsuan ^b,c   Wang, Hui Chen ^b   Chang, Cheng Chang ^a,b   Lin, Ya Wen ^a   Yu, Mu Hsien ^b   Chu, Tang Yuan ^e   Lai, Hung Cheng ^a,b,c,f  

^a NATIONAL DEFENSE MEDICAL CENTER   (Taiwan)

^b TRI SERVICE GENERAL HOSPITAL   (Taiwan)

^c TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^d TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^e TZU CHI UNIVERSITY   (Taiwan)

^f TAIPEI MEDICAL UNIVERSITY   (Taiwan)

Author keywords

biomarkers; cervical cancer; CIN; DNA methylation

Indexed keywords

BIOMARKERS; CERVICAL CANCER; CIN; DNA METHYLATION;

BETA CATENIN; CARCINOGENESIS; CPG ISLANDS; DNA METHYLATION; EARLY DETECTION OF CANCER; EPIGENESIS, GENETIC; FEMALE; HUMANS; PROMOTER REGIONS, GENETIC; SEQUENCE ANALYSIS, DNA; SIGNAL TRANSDUCTION; TUMOR MARKERS, BIOLOGICAL; UTERINE CERVICAL NEOPLASMS;

EID: 84899423384     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.28658     Document Type: Article

References (50)

1. Nanda K, McCrory DC, Myers ER, et al. Accuracy of the Papanicolaou test in screening for and follow-up of cervical cytologic abnormalities: a systematic review. Ann Intern Med 2000; 132: 810-19.
2. Schneider A, Hoyer H, Lotz B, et al. Screening for high-grade cervical intra-epithelial neoplasia and cancer by testing for high-risk HPV, routine cytology or colposcopy. Int J Cancer 2000; 89: 529-34.
3. Roden R, Wu TC,. How will HPV vaccines affect cervical cancer? Nat Rev Cancer 2006; 6: 753-63.
4. Kulasingam SL, Hughes JP, Kiviat NB, et al. Evaluation of human papillomavirus testing in primary screening for cervical abnormalities: comparison of sensitivity, specificity, and frequency of referral. JAMA 2002; 288: 1749-57.
5. Jones PA, Baylin SB,. The epigenomics of cancer. Cell 2007; 128: 683-92.
6. Nephew KP, Huang TH,. Epigenetic gene silencing in cancer initiation and progression. Cancer Lett 2003; 190: 125-33.
7. Garinis GA, Patrinos GP, Spanakis NE, et al. DNA hypermethylation: when tumour suppressor genes go silent. Hum Genet 2002; 111: 115-27.
8. Heyn H, Esteller M,. DNA methylation profiling in the clinic: applications and challenges. Nat Rev Genet 2012; 13: 679-92.
9. Dong SM, Kim HS, Rha SH, et al. Promoter hypermethylation of multiple genes in carcinoma of the uterine cervix. Clin Cancer Res 2001; 7: 1982-6.
10. Wentzensen N, Sherman ME, Schiffman M, et al. Utility of methylation markers in cervical cancer early detection: appraisal of the state-of-the-science. Gynecol Oncol 2009; 112: 293-9.
11. Feng Q, Balasubramanian A, Hawes SE, et al. Detection of hypermethylated genes in women with and without cervical neoplasia. J Natl Cancer Inst 2005; 97: 273-82.
12. Reesink-Peters N, Wisman GB, Jeronimo C, et al. Detecting cervical cancer by quantitative promoter hypermethylation assay on cervical scrapings: a feasibility study. Mol Cancer Res 2004; 2: 289-95.
13. Kim YI, Giuliano A, Hatch KD, et al. Global DNA hypomethylation increases progressively in cervical dysplasia and carcinoma. Cancer 1994; 74: 893-9.
14. Sova P, Feng Q, Geiss G, et al. Discovery of novel methylation biomarkers in cervical carcinoma by global demethylation and microarray analysis. Cancer Epidemiol Biomarkers Prev 2006; 15: 114-23.
15. Wang SS, Smiraglia DJ, Wu YZ, et al. Identification of novel methylation markers in cervical cancer using restriction landmark genomic scanning. Cancer Res 2008; 68: 2489-97.
16. Lai HC, Lin YW, Huang RL, et al. Quantitative DNA methylation analysis detects cervical intraepithelial neoplasms type 3 and worse. Cancer 2010; 116: 4266-74.
17. Huang RL, Chang CC, Su PH, et al. Methylomic analysis identifies frequent DNA methylation of zinc finger protein 582 (ZNF582) in cervical neoplasms. PLoS One 2012; 7: e41060.
18. Su PH, Lin YW, Huang RL, et al. Epigenetic silencing of PTPRR activates MAPK signaling, promotes metastasis and serves as a biomarker of invasive cervical cancer. Oncogene 2012; 32: 15-26.
19. Szklarczyk D, Franceschini A, Kuhn M, et al. The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored. Nucleic Acids Res 2011; 39: D561-8.
20. Zhai Y, Kuick R, Nan B, et al. Gene expression analysis of preinvasive and invasive cervical squamous cell carcinomas identifies HOXC10 as a key mediator of invasion. Cancer Res 2007; 67: 10163-72.
21. Chung MT, Sytwu HK, Yan MD, et al. Promoter methylation of SFRPs gene family in cervical cancer. Gynecol Oncol 2009; 112: 301-16.
22. Baylin SB, Ohm JE,. Epigenetic gene silencing in cancer- A mechanism for early oncogenic pathway addiction? Nat Rev Cancer 2006; 6: 107-16.
23. Coste J, Cochand-Priollet B, de Cremoux P, Le Gales C, Cartier I, Molinie V, Labbe S, Vacher-Lavenu MC, Vielh P,. Cross sectional study of conventional cervical smear, monolayer cytology, and human papillomavirus DNA testing for cervical cancer screening. BMJ 2003; 326: 733.
24. Clarke MA, Wentzensen N, Mirabello L, et al. Human papillomavirus DNA methylation as a potential biomarker for cervical cancer. Cancer Epidemiol Biomarkers Prev 2012; 21: 2125-37.
25. Mirabello L, Sun C, Ghosh A, et al. Methylation of human papillomavirus type 16 genome and risk of cervical precancer in a Costa Rican population. J Natl Cancer Inst 2012; 104: 556-65.
26. Lorincz AT, Brentnall AR, Vasiljevic N, Scibior-Bentkowska D, Castanon A, Fiander A, Powell N, Tristram A, Cuzick J, Sasieni P,. HPV16 L1 and L2 DNA methylation predicts high-grade cervical intraepithelial neoplasia in women with mildly abnormal cervical cytology. Int J Cancer 2013; 133: 637-44.
27. Hesselink AT, Heideman DA, Steenbergen RD, Coupe VM, Overmeer RM, Rijkaart D, Berkhof J, Meijer CJ, Snijders PJ,. Combined promoter methylation analysis of CADM1 and MAL: an objective triage tool for high-risk human papillomavirus DNA-positive women. Clin Cancer Res 2011; 17: 2459-65.
28. Steenbergen RD, Ongenaert M, Snellenberg S, et al. Methylation-specific digital karyotyping of HPV16E6E7-expressing human keratinocytes identifies novel methylation events in cervical carcinogenesis. J Pathol 2013; 231: 53-62.
29. Senchenko VN, Kisseljova NP, Ivanova TA, et al. Novel tumor suppressor candidates on chromosome 3 revealed by NotI-microarrays in cervical cancer. Epigenetics 2013; 8: 409-20.
30. Lendvai A, Johannes F, Grimm C, et al. Genome-wide methylation profiling identifies hypermethylated biomarkers in high-grade cervical intraepithelial neoplasia. Epigenetics 2012; 7: 1268-78.
31. Farkas SA, Milutin-Gasperov N, Grce M, et al. Genome-wide DNA methylation assay reveals novel candidate biomarker genes in cervical cancer. Epigenetics 2013; 8: 1141-52.
32. van der Meide WF, Snellenberg S, Meijer CJ, et al. Promoter methylation analysis of WNT/beta-catenin signaling pathway regulators to detect adenocarcinoma or its precursor lesion of the cervix. Gynecol Oncol 2011; 123: 116-22.
33. Weisenberger DJ, Siegmund KD, Campan M, 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.
34. Issa JP,. CpG island methylator phenotype in cancer. Nat Rev Cancer 2004; 4: 988-93.
35. Hughes LA, Melotte V, de Schrijver J, et al. The CpG island methylator phenotype: what's in a name? Cancer Res 2013; 73: 5858-68.
36. Holowaty P, Miller AB, Rohan T, To T,. Natural history of dysplasia of the uterine cervix. J Natl Cancer Inst 1999; 91: 252-8.
37. Zhang W, Glockner SC, Guo M, et al. Epigenetic inactivation of the canonical Wnt antagonist SRY-box containing gene 17 in colorectal cancer. Cancer Res 2008; 68: 2764-72.
38. Sinner D, Kordich JJ, Spence JR, et al. Sox17 and Sox4 differentially regulate beta-catenin/T-cell factor activity and proliferation of colon carcinoma cells. Mol Cell Biol 2007; 27: 7802-15.
39. Fu DY, Wang ZM, Li C, et al. Sox17, the canonical Wnt antagonist, is epigenetically inactivated by promoter methylation in human breast cancer. Breast Cancer Res Treat 2010; 119: 601-12.
40. Lin N, Di C, Bortoff K, et al. Deletion or epigenetic silencing of AJAP1 on 1p36 in glioblastoma. Mol Cancer Res 2012; 10: 208-17.
41. Matsusaka K, Kaneda A, Nagae G, et al. Classification of Epstein-Barr virus-positive gastric cancers by definition of DNA methylation epigenotypes. Cancer Res 2011; 71: 7187-97.
42. Bharti S, Handrow-Metzmacher H, Zickenheiner S, et al. Novel membrane protein shrew-1 targets to cadherin-mediated junctions in polarized epithelial cells. Mol Biol Cell 2004; 15: 397-406.
43. Subauste MC, Nalbant P, Adamson ED, et al. Vinculin controls PTEN protein level by maintaining the interaction of the adherens junction protein beta-catenin with the scaffolding protein MAGI-2. J Biol Chem 2005; 280: 5676-81.
44. Hu Y, Li Z, Guo L, et al. MAGI-2 Inhibits cell migration and proliferation via PTEN in human hepatocarcinoma cells. Arch Biochem Biophys 2007; 467: 1-9.
45. Hou L, Pavan WJ,. Transcriptional and signaling regulation in neural crest stem cell-derived melanocyte development: do all roads lead to Mitf? Cell Res 2008; 18: 1163-76.
46. Schwartz DR, Wu R, Kardia SL, et al. Novel candidate targets of beta-catenin/T-cell factor signaling identified by gene expression profiling of ovarian endometrioid adenocarcinomas. Cancer Res 2003; 63: 2913-22.
47. Chateauvieux S, Grigorakaki C, Morceau F, et al. Erythropoietin, erythropoiesis and beyond. Biochem Pharmacol 2011; 82: 1291-303.
48. Wang R, Lohr CV, Fischer K, et al. Epigenetic inactivation of endothelin-2 and endothelin-3 in colon cancer. Int J Cancer 2013; 132: 1004-12.
49. Steinmann K, Richter AM, Dammann RH,. Epigenetic silencing of erythropoietin in human cancers. Genes Cancer 2011; 2: 65-73.
50. Rodriguez-Sastre MA, Gonzalez-Maya L, Delgado R, et al. Abnormal distribution of E-cadherin and beta-catenin in different histologic types of cancer of the uterine cervix. Gynecol Oncol 2005; 97: 330-6.