Characterization of HPV DNA methylation of contiguous CpG sites by bisulfite treatment and massively parallel sequencing-the FRAGMENT approach

Frontiers in Genetics

Volumn 5, Issue JUN, 2014, Pages

  Sun, Chang ^a   McAndrew, Thomas ^a   Smith, Benjamin C ^a   Chen, Zigui ^a   Frimer, Marina ^a   Burk, Robert D ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

CpG methylation; Human papillomavirus; Methylation; Methylation haplotypes; Next generation sequencing

Indexed keywords

BISULFITE; CPG OLIGODEOXYNUCLEOTIDE;

ARTICLE; DNA METHYLATION; GENE SEQUENCE; HAPLOTYPE; HUMAN; HUMAN PAPILLOMAVIRUS TYPE 16; METHYLATION RATIO ANALYSIS; MOLECULAR BIOLOGY; POLYMERASE CHAIN REACTION; PROTEIN PURIFICATION; PYROSEQUENCING; RISK ASSESSMENT; SEQUENCE ANALYSIS; SINGLE MOLECULE ANALYSIS; VIRUS GENOME;

EID: 84906261672     PISSN: None     EISSN: 16648021     Source Type: Journal    
DOI: 10.3389/fgene.2014.00150     Document Type: Article

References (45)

1. Badal, V., Chuang, L. S., Tan, E. H., Badal, S., Villa, L. L., Wheeler, C. M., et al. (2003). CpG methylation of human papillomavirus type 16 DNA in cervical cancer cell lines and in clinical specimens: genomic hypomethylation correlates with carcinogenic progression. J. Virol . 77, 6227-6234. doi: 10.1128/JVI.77.11.6227-6234.2003
2. Bhattacharjee, B., and Sengupta, S. (2006). CpG methylation of HPV 16 LCR at E2 binding site proximal to P97 is associated with cervical cancer in presence of intact E2. Virology 354, 280-285. doi: 10.1016/j.virol.2006.06.018
3. Bibikova, M., and Fan, J. B. (2010). Genome-wide DNA methylation profiling. Wiley Interdiscip. Rev. Syst. Biol. Med . 2, 210-223. doi: 10.1002/wsbm.35
4. Brandsma, J. L., Harigopal, M., Kiviat, N. B., Sun, Y., Deng, Y., Zelterman, D., et al. (2014). Methylation of twelve CpGs in human papillomavirus type 16 (HPV16) as an informative biomarker for the triage of women positive for HPV16 infection. Cancer Prev. Res. (Phila.) 7, 526-533. doi: 10.1158/1940-6207.CAPR-13-0354
5. Brandsma, J. L., Sun, Y., Lizardi, P. M., Tuck, D. P., Zelterman, D., Haines, G. K. 3rd., et al. (2009). Distinct human papillomavirus type 16 methylomes in cervical cells at different stages of premalignancy. Virology 389, 100-107. doi: 10.1016/j.virol.2009.03.029
6. Clarke, M. A., Wentzensen, N., Mirabello, L., Ghosh, A., Wacholder, S., Harari, A., et al. (2012). Human papillomavirus DNA methylation as a potential biomarker for cervical cancer. Cancer Epidemiol. Biomarkers Prev . 21, 2125-2137. doi: 10.1158/1055-9965.EPI-12-0905
7. Cock, P. J., Fields, C. J., Goto, N., Heuer, M. L., and Rice, P. M. (2010). The Sanger FASTQ file format for sequences with quality scores, and the Solexa/Illumina FASTQ variants. Nucleic Acids Res . 38, 1767-1771. doi: 10.1093/nar/gkp1137
8. Dejeux, E., Elabdalaoui, H., Gut, I. G., and Tost, J. (2009). Identification and quantification of differentially methylated loci by the pyrosequencing technology. Methods Mol. Biol . 507, 189-205. doi: 10.1007/978-1-59745-522-0_15
9. Ding, D. C., Chiang, M. H., Lai, H. C., Hsiung, C. A., Hsieh, C. Y., and Chu, T. Y. (2009). Methylation of the long control region of HPV16 is related to the severity of cervical neoplasia. Eur. J. Obstet. Gynecol. Reprod. Biol . 147, 215-220. doi: 10.1016/j.ejogrb.2009.08.023
10. Ehrich, M., Nelson, M. R., Stanssens, P., Zabeau, M., Liloglou, T., Xinarianos, G., et al. (2005). Quantitative high-throughput analysis of DNA methylation patterns by base-specific cleavage and mass spectrometry. Proc. Natl. Acad. Sci. U.S.A . 102, 15785-15790. doi: 10.1073/pnas.0507816102
11. Ewing, B., and Green, P. (1998). Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res . 8, 186-194. doi: 10.1101/gr.8.3.175
12. Feng, S., Rubbi, L., Jacobsen, S. E., and Pellegrini, M. (2011). Determining DNA methylation profiles using sequencing. Methods Mol. Biol . 733, 223-238. doi: 10.1007/978-1-61779-089-8_16
13. Fernandez, A. F., and Esteller, M. (2010). Viral epigenomes in human tumorigenesis. Oncogene 29, 1405-1420. doi: 10.1038/onc.2009.517
14. Fernandez, A. F., Rosales, C., Lopez-Nieva, P., Grana, O., Ballestar, E., Ropero, S., et al. (2009). The dynamic DNA methylomes of double-stranded DNA viruses associated with human cancer. Genome Res . 19, 438-451. doi: 10.1101/gr.083550.108
15. Hong, D., Ye, F., Lu, W., Hu, Y., Wan, X., Chen, Y., et al. (2008). Methylation status of the long control region of HPV 16 in clinical cervical specimens. Mol. Med. Rep . 1, 555-560. doi: 10.3892/mmr.1.4.555
16. Jemal, A., Bray, F., Center, M. M., Ferlay, J., Ward, E., and Forman D. (2011). Global cancer statistics. CA Cancer J. Clin . 61, 69-90. doi: 10.3322/caac.20107
17. Kalantari, M., Calleja-Macias, I. E., Tewari, D., Hagmar, B., Lie, K., Barrera-Saldana, H. A., et al. (2004). Conserved methylation patterns of human papillomavirus type 16 DNA in asymptomatic infection and cervical neoplasia. J. Virol . 78, 12762-12772. doi: 10.1128/JVI.78.23.12762-12772.2004
18. Kalantari, M., Chase, D. M., Tewari, K. S., and Bernard, H. U. (2010). Recombination of human papillomavirus-16 and host DNA in exfoliated cervical cells: a pilot study of L1 gene methylation and chromosomal integration as biomarkers of carcinogenic progression. J. Med. Virol . 82, 311-320. doi: 10.1002/jmv.21676
19. Kalantari, M., Garcia-Carranca, A., Morales-Vazquez, C. D., Zuna, R., Montiel, D. P., Calleja-Macias, I. E., et al. (2009). Laser capture microdissection of cervical human papillomavirus infections: copy number of the virus in cancerous and normal tissue and heterogeneous DNA methylation. Virology 390, 261-267. doi: 10.1016/j.virol.2009.05.006
20. Kalantari, M., Osann, K., Calleja-Macias, I. E., Kim, S., Yan, B., Jordan, S., et al. (2014). Methylation of human papillomavirus 16, 18, 31, and 45 L2 and L1 genes and the cellular DAPK gene: considerations for use as biomarkers of the progression of cervical neoplasia. Virology 448C, 314-321. doi: 10.1016/j.virol.2013.10.032
21. Kaminsky, Z., and Petronis, A. (2009). Methylation SNaPshot: a method for the quantification of site-specific DNA methylation levels. Methods Mol. Biol . 507, 241-255. doi: 10.1007/978-1-59745-522-0_18
22. Kim, J. H., Dhanasekaran, S. M., Prensner, J. R., Cao, X., Robinson, D., Kalyana-Sundaram, S., et al. (2011). Deep sequencing reveals distinct patterns of DNA methylation in prostate cancer. Genome Res . 21, 1028-1041. doi: 10.1101/gr.119347.110
23. Komori, H. K., Lamere, S. A., Torkamani, A., Hart, G. T., Kotsopoulos, S., Warner, J., et al. (2011). Application of microdroplet PCR for large-scale targeted bisulfite sequencing. Genome Res . 21, 1738-1745. doi: 10.1101/gr.116863.110
24. Krueger, F., and Andrews, S. R. (2011). Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics 27, 1571-1572 doi: 10.1093/bioinformatics/btr167
25. Ku, C. S., Naidoo, N., Wu, M., and Soong, R. (2011). Studying the epigenome using next generation sequencing. J. Med. Genet . 48, 721-730. doi: 10.1136/jmedgenet-2011-100242
26. Laird, P. W. (2010). Principles and challenges of genomewide DNA methylation analysis. Nat. Rev. Genet . 11, 191-203. doi: 10.1038/nrg2732
27. Langmead, B., Trapnell, C., Pop, M., and Salzberg, S. L. (2009). Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol . 10:R25. doi: 10.1186/gb-2009-10-3-r25
28. Li, L. C., and Dahiya, R. (2002). MethPrimer: designing primers for methylation PCRs. Bioinformatics 18, 1427-1431. doi: 10.1093/bioinformatics/18.11.1427
29. Li, N., Franceschi, S., Howell-Jones, R., Snijders, P. J., and Clifford, G. M. (2011). Human papillomavirus type distribution in 30,848 invasive cervical cancers worldwide: variation by geographical region, histological type and year of publication. Int. J. Cancer 128, 927-935. doi: 10.1002/ijc.25396
30. Lorincz, A. T., Brentnall, A. R., Vasiljevic, N., Scibior-Bentkowska, D., Castanon, A., Fiander, A., et al. (2013). HPV16 L1 and L2 DNA methylation predicts high grade cervical intraepithelial neoplasia in women with mildly abnormal cervical cytology. Int. J. Cancer . 133, 637-644. doi: 10.1002/ijc.28050
31. Mirabello, L., Schiffman, M., Ghosh, A., Rodriguez, A. C., Vasiljevic, N., Wentzensen, N., et al. (2013). Elevated methylation of HPV16 DNA is associated with the development of high grade cervical intraepithelial neoplasia. Int. J. Cancer 132, 1412-1422. doi: 10.1002/ijc.27750
32. Mirabello, L., Sun, C., Ghosh, A., Rodriguez, A. C., Schiffman, M., Wentzensen, N., et al. (2012). Methylation of human papillomavirus type 16 genome and risk of cervical precancer in a Costa Rican population. J. Natl. Cancer Inst . 104, 556-565. doi: 10.1093/jnci/djs135
33. Nejman, D., Straussman, R., Steinfeld, I., Ruvolo, M., Roberts, D., Yakhini, Z., et al. (2014). Molecular rules governing de novo methylation in cancer. Cancer Res . 74, 1475-1483. doi: 10.1158/0008-5472.CAN-13-3042
34. Oates, N. A., van Vliet, J., Duffy, D. L., Kroes, H. Y., Martin, N. G., Boomsma, D. I., et al. (2006). Increased DNA methylation at the AXIN1 gene in a monozygotic twin from a pair discordant for a caudal duplication anomaly. Am. J. Hum. Genet . 79, 155-162. doi: 10.1086/505031
35. Piyathilake, C. J., Macaluso, M., Alvarez, R. D., Chen, M., Badiga, S., Edberg, J. C., et al. (2011). A higher degree of methylation of the HPV 16 E6 gene is associated with a lower likelihood of being diagnosed with cervical intraepithelial neoplasia. Cancer 117, 957-963. doi: 10.1002/cncr.25511
36. Schiffman, M., Castle, P. E., Jeronimo, J., Rodriguez, A. C., and Wacholder S. (2007). Human papillomavirus and cervical cancer. Lancet 370, 890-907. doi: 10.1016/S0140-6736(07)61416-0
37. Schiffman, M., and Wentzensen, N. (2013). Human papillomavirus infection and the multistage carcinogenesis of cervical cancer. Cancer Epidemiol. Biomarkers Prev . 22, 553-560. doi: 10.1158/1055-9965.EPI-12-1406
38. Schmieder, R., and Edwards, R. (2011). Quality control and preprocessing of metagenomic datasets. Bioinformatics 27, 863-864. doi: 10.1093/bioinformatics/btr026
39. Sun, C., Reimers, L. L., and Burk, R. D. (2011). Methylation of HPV16 genome CpG sites is associated with cervix precancer and cancer. Gynecol. Oncol . 121, 59-63. doi: 10.1016/j.ygyno.2011.01.013
40. Taylor, K. H., Kramer, R. S., Davis, J. W., Guo, J., Duff, D. J., Xu, D., et al. (2007). Ultradeep bisulfite sequencing analysis of DNA methylation patterns in multiple gene promoters by 454 sequencing. Cancer Res . 67, 8511-8518. doi: 10.1158/0008-5472.CAN-07-1016
41. Tost, J., and Gut, I. G. (2007a). DNA methylation analysis by pyrosequencing. Nat. Protoc . 2, 2265-2275. doi: 10.1038/nprot.2007.314
42. Tost, J., and Gut, I. G. (2007b). Analysis of gene-specific DNA methylation patterns by pyrosequencing technology. Methods Mol. Biol . 373, 89-102. doi: 10.1038/nprot.2007.314
43. Turan, T., Kalantari, M., Calleja-Macias, I. E., Cubie, H. A., Cuschieri, K., Villa, L. L., et al. (2006). Methylation of the human papillomavirus-18 L1 gene: a biomarker of neoplastic progression? Virology 349, 175-183. doi: 10.1016/j.virol.2005.12.033
44. Turan, T., Kalantari, M., Cuschieri, K., Cubie, H. A., Skomedal, H., and Bernard, H. U. (2007). High-throughput detection of human papillomavirus-18 L1 gene methylation, a candidate biomarker for the progression of cervical neoplasia. Virology 361, 185-193. doi: 10.1016/j.virol.2006.11.010
45. Wentzensen, N., Sun, C., Ghosh, A., Kinney, W., Mirabello, L., Wacholder, S., et al. (2012). Methylation of HPV18, HPV31, and HPV45 genomes and cervical intraepithelial neoplasia grade 3. J. Natl. Cancer Inst . 104, 1738-1749. doi: 10.1093/jnci/djs425