Methylation of human papillomavirus type 16 CpG sites at E2-binding site 1 (E2BS1), E2BS2, and the Sp1-binding site in cervical cancer samples as determined by high-resolution melting analysis-PCR

Journal of Clinical Microbiology

Volumn 51, Issue 10, 2013, Pages 3207-3215

  Jacquin, Elise ^a,b   Baraquin, Alice ^c   Ramanah, Rajeev ^c   Carcopino, Xavier ^d,e   Morel, Adrien ^a,b   Valmary Degano, Séverine ^a,b,c   Bravo, Ignacio G ^f   De Sanjosé, Silvia ^f   Riethmuller, Didier ^a,b,c   Mougin, Christiane ^a,b,c   Prétet, Jean Luc ^a,b,c  

^a UNIVERSITÉ DE FRANCHE COMTÉ   (France)

^b EA 3181   (France)

^c UNIVERSITY HOSPITAL OF BESANÇON   (France)

^d HÔPITAL NORD   (France)

^e AIX MARSEILLE UNIVERSITY   (France)

^f CATALAN INSTITUTE OF ONCOLOGY   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR SP1; VIRUS PROTEIN;

ARTICLE; BINDING SITE; CANCER GRADING; CONTROLLED STUDY; CPG ISLAND; FEMALE; HIGH GRADE SQUAMOUS INTRAEPITHELIAL LESION; HIGH RESOLUTION MELTING ANALYSIS; HUMAN; HUMAN CELL; HUMAN PAPILLOMAVIRUS TYPE 16; HUMAN TISSUE; LOW GRADE SQUAMOUS INTRAEPITHELIAL LESION; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROGNOSIS; PROTEIN ANALYSIS; PROTEIN METHYLATION; PUBLIC HEALTH; PYROSEQUENCING; QUANTITATIVE ANALYSIS; RELIABILITY; UTERINE CERVIX CANCER; VIRUS DETECTION; VIRUS GENOME;

BINDING SITES; DNA METHYLATION; DNA, VIRAL; DNA-BINDING PROTEINS; FEMALE; GENE EXPRESSION REGULATION, VIRAL; HUMAN PAPILLOMAVIRUS 16; HUMANS; ONCOGENE PROTEINS, VIRAL; POLYMERASE CHAIN REACTION; TRANSITION TEMPERATURE; UTERINE CERVICAL NEOPLASMS;

EID: 84884788058     PISSN: 00951137     EISSN: 1098660X     Source Type: Journal    
DOI: 10.1128/JCM.01106-13     Document Type: Article

References (56)

1. Bosch FX, Manos MM, Muñoz N, Sherman M, Jansen AM, Peto J, Schiffman MH, Moreno V, Kurman R, Shah KV. 1995. Prevalence of human papillomavirus in cervical cancer: a worldwide perspective. International Biological Study on Cervical Cancer (IBSCC) Study Group. J. Natl. Cancer Inst. 87:796-802.
2. Walboomers JM, Jacobs MV, Manos MM, Bosch FX, Kummer JA, Shah KV, Snijders PJ, Peto J, Meijer CJ, Muñoz N. 1999. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J. Pathol. 189:12-19. (Pubitemid 29406813)
3. Richardson H, Kelsall G, Tellier P, Voyer H, Abrahamowicz M, Ferenczy A, Coutlée F, Franco EL. 2003. The natural history of type-specific human papillomavirus infections in female university students. Cancer Epidemiol. Biomarkers Prev. 12:485-490. (Pubitemid 36713640)
4. Ho GY, Burk RD, Klein S, Kadish AS, Chang CJ, Palan P, Basu J, Tachezy R, Lewis R, Romney S. 1995. Persistent genital human papillomavirus infection as a risk factor for persistent cervical dysplasia. J. Natl. Cancer Inst. 87:1365-1371.
5. Dalstein V, Riethmuller D, Prétet JL, Le Bail Carval K, Sautière JL, Carbillet JP, Kantelip B, Schaal JP, Mougin C. 2003. Persistence and load of high-risk HPV are predictors for development of high-grade cervical lesions: a longitudinal French cohort study. Int. J. Cancer 106:396-403. (Pubitemid 36870403)
6. Woodman CB, Collins S, Winter H, Bailey A, Ellis J, Prior P, Yates M, Rollason TP, Young LS. 2001. Natural history of cervical human papillomavirus infection in young women: a longitudinal cohort study. Lancet 357:1831-1836. (Pubitemid 32539115)
7. Moscicki AB, Schiffman M, Kjaer S, Villa LL. 2006. Chapter 5: updating the natural history of HPV and anogenital cancer. Vaccine 24(Suppl 3): S3/42-S3/51. doi:10.1016/j.vaccine.2012.05.089.
8. Bulkmans NW, Berkhof J, Bulk S, Bleeker MC, van Kemenade FJ, Rozendaal L, Snijders PJ, Meijer CJ, POBASCAM Study Group. 2007. High-risk HPV type-specific clearance rates in cervical screening. Br. J. Cancer 96:1419-1424. (Pubitemid 46685773)
9. Khan MJ, Castle PE, Lorincz AT, Wacholder S, Sherman M, Scott DR, Rush BB, Glass AG, Schiffman M. 2005. The elevated 10-year risk of cervical precancer and cancer in women with human papillomavirus (HPV) type 16 or 18 and the possible utility of type-specific HPV testing in clinical practice. J. Natl. Cancer Inst. 97:1072-1079. (Pubitemid 41417924)
10. Bouvard V, Baan R, Straif K, Grosse Y, Secretan B, El Ghissassi F, Benbrahim-Tallaa L, Guha N, Freeman C, Galichet L, Cogliano V, WHO International Agency for Research on Cancer Monograph Working Group. 2009. A review of human carcinogens-part B: biological agents. Lancet Oncol. 10:321-322.
11. Guan P, Howell-Jones R, Li N, Bruni L, de Sanjosé S, Franceschi S, Clifford GM. 2012. Human papillomavirus types in 115,789 HPVpositive women: a meta-analysis from cervical infection to cancer. Int. J. Cancer 131:2349-2359.
12. de Sanjose S, Quint WG, Alemany L, Geraets DT, Klaustermeier JE, Lloveras B, Tous S, Felix A, Bravo LE, Shin HR, Vallejos CS, de Ruiz PA, Lima MA, Guimera N, Clavero O, Alejo M, Llombart-Bosch A, Cheng-Yang C, Tatti SA, Kasamatsu E, Iljazovic E, Odida M, Prado R, Seoud M, Grce M, Usubutun A, Jain A, Suarez GA, Lombardi LE, Banjo A, Menéndez C, Domingo EJ, Velasco J, Nessa A, Chichareon SC, Qiao YL, Lerma E, Garland SM, Sasagawa T, Ferrera A, Hammouda D, Mariani L, Pelayo A, Steiner I, Oliva E, Meijer CJ, Al-Jassar WF, Cruz E, Wright TC, Puras A, et al. 2010. Human papillomavirus genotype attribution in invasive cervical cancer: a retrospective cross-sectional worldwide study. Lancet Oncol. 11:1048-1056.
13. McLaughlin-Drubin ME, Munger K. 2009. Oncogenic activities of human papillomaviruses. Virus Res. 143:195-208.
14. Phelps WC, Howley PM. 1987. Transcriptional trans-activation by the human papillomavirus type 16 E2 gene product. J. Virol. 61:1630-1638. (Pubitemid 17069742)
15. Romanczuk H, Thierry F, Howley PM. 1990. Mutational analysis of cis elements involved in E2 modulation of human papillomavirus type 16 P97 and type 18 P105 promoters. J. Virol. 64:2849-2859. (Pubitemid 20171275)
16. Thierry F. 2009. Transcriptional regulation of the papillomavirus oncogenes by cellular and viral transcription factors in cervical carcinoma. Virology 384:375-379.
17. Tan SH, Leong LE, Walker PA, Bernard HU. 1994. The human papillomavirus type 16 E2 transcription factor binds with low cooperativity to two flanking sites and represses the E6 promoter through displacement of Sp1 and TFIID. J. Virol. 68:6411-6420. (Pubitemid 24294891)
18. Bellanger S, Tan CL, Xue YZ, Teissier S, Thierry F. 2011. Tumor suppressor or oncogene? A critical role of the human papillomavirus (HPV) E2 protein in cervical cancer progression. Am. J. Cancer Res. 1:373-389.
19. Kalantari M, Karlsen F, Kristensen G, Holm R, Hagmar B, Johansson B. 1998. Disruption of the E1 and E2 reading frames of HPV 16 in cervical carcinoma is associated with poor prognosis. Int. J. Gynecol. Pathol. 17: 146-153. (Pubitemid 28151014)
20. Arias-Pulido H, Peyton CL, Joste NE, Vargas H, Wheeler CM. 2006. Human papillomavirus type 16 integration in cervical carcinoma in situ and in invasive cervical cancer. J. Clin. Microbiol. 44:1755-1762. (Pubitemid 43726265)
21. Leonard SM, Wei W, Collins SI, Pereira M, Diyaf A, Constandinou-Williams C, Young LS, Roberts S, Woodman CB. 2012. Oncogenic human papillomavirus imposes an instructive pattern of DNA methylation changes which parallel the natural history of cervical HPV infection in young women. Carcinogenesis 33:1286-1293.
22. Wentzensen N, Sherman ME, Schiffman M, Wang SS. 2009. Utility of methylation markers in cervical cancer early detection: appraisal of the state-of-the-science. Gynecol. Oncol. 112:293-299.
23. Danos O, Katinka M, Yaniv M. 1980. Molecular cloning, refined physical map and heterogeneity of methylation sites of papilloma virus type 1a DNA. Eur. J. Biochem. 109:457-461. (Pubitemid 11248610)
24. Fernandez AF, Esteller M. 2010. Viral epigenomes in human tumorigenesis. Oncogene 29:1405-1420.
25. Brandsma JL, Sun Y, Lizardi PM, Tuck DP, Zelterman D, Haines GK, III, Martel M, Harigopal M, Schofield K, Neapolitano M. 2009. Distinct human papillomavirus type 16 methylomes in cervical cells at different stages of premalignancy. Virology 389:100-107.
26. Fernandez AF, Rosales C, Lopez-Nieva P, Graña O, Ballestar E, Ropero S, Espada J, Melo SA, Lujambio A, Fraga MF, Pino I, Javierre B, Carmona FJ, Acquadro F, Steenbergen RD, Snijders PJ, Meijer CJ, Pineau P, Dejean A, Lloveras B, Capella G, Quer J, Buti M, Esteban JI, Allende H, Rodriguez-Frias F, Castellsague X, Minarovits J, Ponce J, Capello D, Gaidano G, Cigudosa JC, Gomez-Lopez G, Pisano DG, Valencia A, Piris MA, Bosch FX, Cahir-McFarland E, Kieff E, Esteller M. 2009. The dynamic DNA methylomes of double-stranded DNA viruses associated with human cancer. Genome Res. 19:438-451.
27. Mirabello L, Schiffman M, Ghosh A, Rodriguez AC, Vasiljevic N, Wentzensen N, Herrero R, Hildesheim A, Wacholder S, Scibior-Bentkowska D, Burk RD, Lorincz AT. 2013. Elevated methylation of HPV16 DNA is associated with the development of high grade cervical intraepithelial neoplasia. Int. J. Cancer 132:1412-1422.
28. Kalantari M, Calleja-Macias IE, Tewari D, Hagmar B, Lie K, Barrera-Saldana HA, Wiley DJ, Bernard HU. 2004. Conserved methylation patterns of human papillomavirus type 16 DNA in asymptomatic infection and cervical neoplasia. J. Virol. 78:12762-12772. (Pubitemid 39507784)
29. Sun C, Reimers LL, Burk RD. 2011. Methylation of HPV16 genome CpG sites is associated with cervix precancer and cancer. Gynecol. Oncol. 121: 59-63.
30. Badal V, Chuang LS, Tan EH, Badal S, Villa LL, Wheeler CM, Li BF, Bernard HU. 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. (Pubitemid 36588393)
31. Mazumder Indra D, Singh RK, Mitra S, Dutta S, Chakraborty C, Basu PS, Mondal RK, Roychoudhury S, Panda CK. 2011. Genetic and epigenetic changes of HPV16 in cervical cancer differentially regulate E6/E7 expression and associate with disease progression. Gynecol. Oncol. 123: 597-604.
32. Patel DA, Rozek LS, Colacino JA, Van Zomeren-Dohm A, Ruffin MT, Unger ER, Dolinoy DC, Swan DC, Onyekwuluje J, DeGraffinreid CR, Paskett ED. 2012. Patterns of cellular and HPV 16 methylation as biomarkers for cervical neoplasia. J. Virol. Methods 184:84-92.
33. Piyathilake CJ, Macaluso M, Alvarez RD, Chen M, Badiga S, Edberg JC, Partridge EE, Johanning GL. 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.
34. Xi LF, Jiang M, Shen Z, Hulbert A, Zhou XH, Lin YY, Kiviat NB, Koutsky LA. 2011. Inverse association between methylation of human papillomavirus type 16 DNA and risk of cervical intraepithelial neoplasia grades 2 or 3. PLoS One 6:e23897. doi:10.1371/journal.pone.0023897.
35. Bhattacharjee B, 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. (Pubitemid 44527961)
36. Ding DC, Chiang MH, Lai HC, Hsiung CA, Hsieh CY, Chu TY. 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.
37. Snellenberg S, Schütze DM, Claassen-Kramer D, Meijer CJ, Snijders PJ, Steenbergen RD. 2012. Methylation status of the E2 binding sites of HPV16 in cervical lesions determined with the Luminex xMAP system. Virology 422:357-365.
38. Vinokurova S, von Knebel Doeberitz M. 2011. Differential methylation of the HPV16 upstream regulatory region during epithelial differentiation and neoplastic transformation. PLoS One 6:e24451. doi:10.1371/journal. pone.0024451.
39. Hong D, Ye F, Lu W, Hu Y, Wan X, Chen Y, Xie X. 2008. Methylation status of the long control region of HPV 16 in clinical cervical specimens. Mol. Med. Rep. 1:555-560.
40. Saunier M, Monnier-Benoit S, Mauny F, Dalstein V, Briolat J, Riethmuller D, Kantelip B, Schwarz E, Mougin C, Prétet JL. 2008. Analysis of human papillomavirus type 16 (HPV16) DNA load and physical state for identification of HPV16-infected women with high-grade lesions or cervical carcinoma. J. Clin. Microbiol. 46:3678-3685.
41. Seedorf K, Krämmer G, Dürst M, Suhai S, Röwekamp WG. 1985. Human papillomavirus type 16 DNA sequence. Virology 145:181-185. (Pubitemid 15234421)
42. Tse MY, Ashbury JE, Zwingerman N, King WD, Taylor SAM, Pang SC. 2011. A refined, rapid and reproducible high resolution melt (HRM)- based method suitable for quantification of global LINE-1 repetitive element methylation. BMC Res. Notes 4:565. doi:10.1186/1756-0500-4-565.
43. Warnecke PM, Stirzaker C, Song J, Grunau C, Melki JR, Clark SJ. 2002. Identification and resolution of artifacts in bisulfite sequencing. Methods 27:101-107. (Pubitemid 34757119)
44. Clarke MA, Wentzensen N, Mirabello L, Ghosh A, Wacholder S, Harari A, Lorincz A, Schiffman M, Burk RD. 2012. Human papillomavirus DNA methylation as a potential biomarker for cervical cancer. Cancer Epidemiol. Biomarkers Prev. 21:2125-2137.
45. Sun LL, Cao DY, Yang JX, Li H, Zhou XR, Song ZQ, Cheng XM, Chen J, Shen K. 2012. Population-based case-control study on DAPK1, RAR-β2 and MGMT methylation in liquid-based cytology. Arch. Gynecol. Obstet. 285:1433-1439.
46. Turan T, Kalantari M, Calleja-Macias IE, Cubie HA, Cuschieri K, Villa LL, Skomedal H, Barrera-Saldaña HA, Bernard HU. 2006. Methylation of the human papillomavirus-18 L1 gene: a biomarker of neoplastic progression? Virology 349:175-183.
47. Liu Y, Mayo MW, Nagji AS, Smith PW, Ramsey CS, Li D, Jones DR. 2012. Phosphorylation of RelA/p65 promotes DNMT-1 recruitment to chromatin and represses transcription of the tumor metastasis suppressor gene BRMS1. Oncogene 31:1143-1154.
48. Kulmala SM, Syrjanen SM, Gyllensten UB, Shabalova IP, Petrovichev N, Tosi P, Syrjänen KJ, Johansson BC. 2006. Early integration of high copy HPV16 detectable in women with normal and low grade cervical cytology and histology. J. Clin. Pathol. 59:513-517.
49. Peitsaro P, Johansson B, Syrjanen S. 2002. Integrated human papillomavirus type 16 is frequently found in cervical cancer precursors as demonstrated by a novel quantitative real-time PCR technique. J. Clin. Microbiol. 40:886-891. (Pubitemid 34208640)
50. Tonon SA, Picconi MA, Bos PD, Zinovich JB, Galuppo J, Alonio LV, Teyssie AR. 2001. Physical status of the E2 human papilloma virus 16 viral gene in cervical preneoplastic and neoplastic lesions. J. Clin. Virol. 21: 129-134. (Pubitemid 32506923)
51. Cricca M, Morselli-Labate AM, Venturoli S, Ambretti S, Gentilomi GA, Gallinella G, Costa S, Musiani M, Zerbini M. 2007. Viral DNA load, physical status and E2/E6 ratio as markers to grade HPV16 positive women for high-grade cervical lesions. Gynecol. Oncol. 106:549-557. (Pubitemid 47302471)
52. Hudelist G, Manavi M, Pischinger KI, Watkins-Riedel T, Singer CF, Kubista E, Czerwenka KF. 2004. Physical state and expression of HPV DNA in benign and dysplastic cervical tissue: different levels of viral integration are correlated with lesion grade. Gynecol. Oncol. 92:873-880. (Pubitemid 38251391)
53. Fujii T, Masumoto N, Saito M, Hirao N, Niimi S, Mukai M, Ono A, Hayashi S, Kubushiro K, Sakai E, Tsukazaki K, Nozawa S. 2005. Comparison between in situ hybridization and real-time PCR technique as a means of detecting the integrated form of human papillomavirus 16 in cervical neoplasia. Diagn. Mol. Pathol. 14:103-108. (Pubitemid 40734078)
54. Schmitt M, Pawlita M. 2011. The HPV transcriptome in HPV16 positive cell lines. Mol. Cell. Probes 25:108-113.
55. Thain A, Jenkins O, Clarke AR, Gaston K. 1996. CpG methylation directly inhibits binding of the human papillomavirus type 16 E2 protein to specific DNA sequences. J. Virol. 70:7233-7235. (Pubitemid 26307443)
56. Kim K, Garner-Hamrick PA, Fisher C, Lee D, Lambert PF. 2003. Methylation patterns of papillomavirus DNA, its influence on E2 function, and implications in viral infection. J. Virol. 77:12450-12459. (Pubitemid 37430642)