Methylation-specific digital karyotyping of HPV16E6E7-expressing human keratinocytes identifies novel methylation events in cervical carcinogenesis

Journal of Pathology

Volumn 231, Issue 1, 2013, Pages 53-62

  Steenbergen, Renske D M ^a   Ongenaert, Maté ^b   Snellenberg, Suzanne ^a   Trooskens, Geert ^b   Van Der Meide, Wendy F ^a,d   Pandey, Deeksha ^a,e   Bloushtain Qimron, Noga ^c   Polyak, Kornelia ^c   Meijer, Chris J L M ^a   Snijders, Peter J F ^a   Van Criekinge, Wim ^b  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b GHENT UNIVERSITY   (Belgium)

^c HARVARD MEDICAL SCHOOL   (United States)

^d U Cytech Biosciences   (Netherlands)

^e KASTURBA MEDICAL COLLEGE   (India)

Author keywords

Biomarkers; Cervical cancer; DNA methylation; Epigenetic reprogramming; Human papillomavirus

Indexed keywords

GENOMIC DNA; PR DOMAIN ZINC FINGER PROTEIN 14; PROTEIN; PROTEIN CLIC3; PROTEIN CREB3L1; PROTEIN FAM19A4; PROTEIN LFNG; PROTEIN LHX1; PROTEIN MRC2; PROTEIN NPTX 1; PROTEIN PHACTR3; SCLEROSTIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NKX2; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN;

ARTICLE; CONTROLLED STUDY; CPG ISLAND; DISEASE COURSE; DNA METHYLATION; FEMALE; GENE EXPRESSION; GENE FREQUENCY; GENE IDENTIFICATION; HUMAN; HUMAN CELL; HUMAN PAPILLOMAVIRUS TYPE 16; HUMAN TISSUE; KARYOTYPING; KERATINOCYTE; MAJOR CLINICAL STUDY; METHYLATION SPECIFIC DIGITAL KARYOTYPING; PAPILLOMAVIRUS INFECTION; PRIORITY JOURNAL; UTERINE CERVIX CARCINOMA;

EID: 84885184476     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.4210     Document Type: Article

References (47)

1. Walboomers JM, Jacobs MV, Manos MM, et al. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol 1999; 189: 12-19.
2. Moody CA, Laimins LA. Human papillomavirus oncoproteins: pathways to transformation. Nat Rev Cancer 2010; 10: 550-560.
3. Wentzensen N, Sun C, Ghosh A, et al. Methylation of HPV18, HPV31, and HPV45 genomes and cervical intraepithelial neoplasia grade 3. J Natl Cancer Inst 2012; 104: 1738-1749.
4. Fernandez AF, Rosales C, Lopez-Nieva P, et al. The dynamic DNA methylomes of double-stranded DNA viruses associated with human cancer. Genome Res 2009; 19: 438-451.
5. Snellenberg S, Schutze DM, Claassen-Kramer D, et al. Methylation status of the E2 binding sites of HPV16 in cervical lesions determined with the LuminexxMAP system. Virology 2012; 422: 357-365.
6. 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: 2125-2137.
7. Mirabello L, Schiffman M, Ghosh A, et al. Elevated methylation of HPV16 DNA is associated with the development of high grade cervical intraepithelial neoplasia. Int J Cancer 2013; 132: 1412-1422.
8. Au Yeung CL, Tsang WP, Tsang TY, et al. HPV-16 E6 upregulation of DNMT1 through repression of tumor suppressor p53 . Oncol Rep 2010; 24: 1599-1604.
9. Burgers WA, Blanchon L, Pradhan S, et al. Viral oncoproteins target the DNA methyltransferases. Oncogene 2007; 26: 1650-1655.
10. Wilting SM, Snijders PJ, Meijer GA, et al. Increased gene copy numbers at chromosome 20q are frequent in both squamous cell carcinomas and adenocarcinomas of the cervix. J Pathol 2006; 209: 220-230.
11. Sawada M, Kanai Y, Arai E, et al. Increased expression of DNA methyltransferase 1 (DNMT1) protein in uterine cervix squamous cell carcinoma and its precursor lesion. Cancer Lett 2007; 251: 211-219.
12. Leonard SM, Wei W, Collins SI, et al. Oncogenic human papillomavirus imposes an instructive pattern of DNA methylation changes which parallel the natural history of cervical HPV infection in young women. Carcinogenesis 2012; 33: 1286-1293.
13. 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: 293-299.
14. Roossink F, de JS, Wisman GB, et al. DNA hypermethylation biomarkers to predict response to cisplatin treatment, radiotherapy or chemoradiation: the present state of art. Cell Oncol (Dordr) 2012; 35: 231-241.
15. Hanahan D and Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011; 144: 646-674.
16. Snijders PJ, Steenbergen RD, Heideman DA, et al. HPV-mediated cervical carcinogenesis: concepts and clinical implications. J Pathol 2006; 208: 152-164.
17. Hu M, Yao J, Polyak K. Methylation-specific digital karyotyping. Nat Protoc 2006; 1: 1621-1636.
18. Steenbergen RD, Walboomers JM, Meijer CJ, et al. Transition of human papillomavirus type 16 and 18 transfected human foreskin keratinocytes towards immortality: activation of telomerase and allele losses at 3p, 10p, 11q and/or 18q. Oncogene 1996; 13: 1249-1257.
19. Struijk L, van der Meijden E, Kazem S, et al. Specific betapapillomaviruses associated with squamous cell carcinoma of the skin inhibit UVB-induced apoptosis of primary human keratinocytes. J Gen Virol 2008; 89: 2303-2314.
20. Steenbergen RD, Kramer D, Braakhuis BJ, et al. TSLC1 gene silencing in cervical cancer cell lines and cervical neoplasia. J Natl Cancer Inst 2004; 96: 294-305.
21. Jacobs MV, Snijders PJ, Van den Brule AJ, et al. A general primer GP5+/GP6+-mediated PCR-enzyme immunoassay method for rapid detection of 14 high-risk and 6 low-risk human papillomavirus genotypes in cervical scrapings. J Clin Microbiol 1997; 35: 791-795.
22. Kent WJ. BLAT-the BLAST-like alignment tool. Genome Res 2002; 12: 656-664.
23. Stajich JE, Block D, Boulez K, et al. The Bioperl toolkit: Perl modules for the life sciences. Genome Res 2002; 12: 1611-1618.
24. Audic S and Claverie JM. The significance of digital gene expression profiles. Genome Res 1997; 7: 986-995.
25. Hinrichs AS, Karolchik D, Baertsch R, et al. The UCSC Genome Browser Database: update 2006. Nucleic Acids Res 2006; 34: D590-598.
26. Overmeer RM, Louwers JA, Meijer CJ, et al. Combined CADM1 and MAL promoter methylation analysis to detect (pre-)malignant cervical lesions in high-risk HPV-positive women. Int J Cancer 2011; 129: 2218-2225.
27. Hesselink AT, Heideman DA, Steenbergen RD, et al. 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: 2459-2465.
28. Bachtiary B, Boutros PC, Pintilie M, et al. Gene expression profiling in cervical cancer: an exploration of intratumor heterogeneity. Clin Cancer Res 2006; 12: 5632-5640.
29. Wilting SM, de WJ, Meijer CJ, et al. Integrated genomic and transcriptional profiling identifies chromosomal loci with altered gene expression in cervical cancer. Genes Chromosomes Cancer 2008; 47: 890-905.
30. Yang N, Eijsink JJ, Lendvai A, et al. Methylation markers for CCNA1 and C13ORF18 are strongly associated with high-grade cervical intraepithelial neoplasia and cervical cancer in cervical scrapings. Cancer Epidemiol Biomarkers Prev 2009; 18: 3000-3007.
31. Bosch LJ, Oort FA, Neerincx M, et al. DNA methylation of phosphatase and actin regulator 3 detects colorectal cancer in stool and complements FIT. Cancer Prev Res (Phila) 2012; 5: 464-472.
32. Hagihara A, Miyamoto K, Furuta J, et al. Identification of 27 5 CpG islands aberrantly methylated and 13 genes silenced in human pancreatic cancers. Oncogene 2004; 23: 8705-8710.
33. Worch S, Fiedler E, Hansmann I, et al. Genomic organization and expression pattern of scapinin (PHACTR3) in mouse and human. Cytogenet Genome Res 2006; 115: 23-29.
34. Wang RH, Liu CW, Avramis VI, et al. Protein phosphatase 1a- mediated stimulation of apoptosis is associated with dephosphorylation of the retinoblastoma protein. Oncogene 2001; 20: 6111-6122.
35. Bankovic J, Stojsic J, Jovanovic D, et al. Identification of genes associated with non-small-cell lung cancer promotion and progression. Lung Cancer 2010; 67: 151-159.
36. Bock C, Tomazou EM, Brinkman AB, et al. Quantitative comparison of genome-wide DNA methylation mapping technologies. Nat Biotechnol 2010; 28: 1106-1114.
37. Tom TY, Emtage P, Funk WD, et al. TAFA: a novel secreted family with conserved cysteine residues and restricted expression in the brain. Genomics 2004; 83: 727-734.
38. Nishikawa N, Toyota M, Suzuki H, et al. Gene amplification and overexpression of PRDM14 in breast cancers. Cancer Res 2007; 67: 9649-9657.
39. Chia NY, Chan YS, Feng B, et al. A genome-wide RNAi screen reveals determinants of human embryonic stem cell identity. Nature 2010; 468: 316-320.
40. Dettman EJ, Simko SJ, Ayanga B, et al. Prdm14 initiates lymphoblastic leukemia after expanding a population of cells resembling common lymphoid progenitors. Oncogene 2011; 30: 2859-2873.
41. Yu C, Zhang Z, Liao W, et al. The tumor-suppressor gene Nkx2.8 suppresses bladder cancer proliferation through upregulation of FOXO3a and inhibition of the MEK/ERK signaling pathway. Carcinogenesis 2012; 33: 678-686.
42. Harris T, Pan Q, Sironi J, et al. Both gene amplification and allelic loss occur at 14q13.3 in lung cancer. Clin Cancer Res 2011; 17: 690-699.
43. Tong WG, Wierda WG, Lin E, et al. Genome-wide DNA methylation profiling of chronic lymphocytic leukemia allows identification of epigenetically repressed molecular pathways with clinical impact. Epigenetics 2010; 5: 499-508.
44. Sato N, Fukushima N, Hruban RH, et al. CpG island methylation profile of pancreatic intraepithelial neoplasia. Mod Pathol 2008; 21: 238-244.
45. Naucler P, Ryd W, Tornberg S, et al. Human papillomavirus and Papanicolaou tests to screen for cervical cancer. N Engl J Med 2007; 357: 1589-1597.
46. Rijkaart DC, Berkhof J, Rozendaal L, et al. Human papillomavirus testing for the detection of high-grade cervical intraepithelial neoplasia and cancer: final results of the POBASCAM randomised controlled trial. Lancet Oncol 2012; 13: 78-88.
47. Ronco G, Giorgi-Rossi P, Carozzi F, et al. Results at recruitment from a randomized controlled trial comparing human papillomavirus testing alone with conventional cytology as the primary cervical cancer screening test. J Natl Cancer Inst 2008; 100: 492-501.