HPV16 methyl-haplotypes determined by a novel next-generation sequencing method are associated with cervical precancer

International Journal of Cancer

Volumn 136, Issue 4, 2015, Pages E146-E153

  Mirabello, Lisa ^a   Frimer, Marina ^b   Harari, Ariana ^b   McAndrew, Thomas ^b   Smith, Benjamin ^b   Chen, Zigui ^b   Wentzensen, Nicolas ^a   Wacholder, Sholom ^a   Castle, Philip E ^c   Raine Bennett, Tina ^d   Schiffman, Mark ^a   Burk, Robert D ^b  

^a NATIONAL CANCER INSTITUTE   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c Global Cancer Initiative   (United States)

^d DIVISION OF RESEARCH   (United States)

Author keywords

Cervical precancer; HPV16; Methylation; Next generation sequencing; Pyrosequencing

Indexed keywords

BISULFITE; L1 PROTEIN; L2 PROTEIN; METHYL CPG BINDING PROTEIN; PROTEIN E6; UNCLASSIFIED DRUG; VIRUS DNA; VIRUS PROTEIN;

ADULT; AGED; ARTICLE; CANCER DIAGNOSIS; CANCER SCREENING; CONTROLLED STUDY; DIAGNOSTIC TEST ACCURACY STUDY; DISEASE ASSOCIATION; DNA ISOLATION; DNA METHYLATION; DNA METHYLATION ASSAY; FEMALE; GENE SEQUENCE; HAPLOTYPE; HUMAN; HUMAN CELL; HUMAN PAPILLOMAVIRUS TYPE 16; INTERMETHOD COMPARISON; MAJOR CLINICAL STUDY; METHYL HAPLOTYPE; NEXT GENERATION BISULFITE SEQUENCING; NONHUMAN; OPEN READING FRAME; PAPANICOLAOU TEST; PAPILLOMAVIRUS INFECTION; PYROSEQUENCING; SENSITIVITY AND SPECIFICITY; UTERINE CERVIX CARCINOMA IN SITU; VIRUS DETECTION; CASE CONTROL STUDY; DNA SEQUENCE; GENETICS; HIGH THROUGHPUT SEQUENCING; MIDDLE AGED; PRECANCER; UTERINE CERVIX TUMOR; VIROLOGY; YOUNG ADULT;

ADULT; AGED; CASE-CONTROL STUDIES; DNA METHYLATION; FEMALE; HAPLOTYPES; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMAN PAPILLOMAVIRUS 16; HUMANS; MIDDLE AGED; PAPILLOMAVIRUS INFECTIONS; PRECANCEROUS CONDITIONS; SEQUENCE ANALYSIS, DNA; UTERINE CERVICAL NEOPLASMS; YOUNG ADULT;

EID: 84918782714     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.29119     Document Type: Article

References (40)

1. de Sanjose S, Quint WGV, Alemany L, et al. Human papillomavirus genotype attribution in invasive cervical cancer: A retrospective crosssectional worldwide study. Lancet Oncol 2010;11: 1048-56
2. Guan P, Howell-Jones R, Li N, et al. Human papillomavirus types in 115,789 HPV-positive women: A meta-Analysis from cervical infection to cancer. Int J Cancer 2012;131:2349-59
3. Ho G, Bierman R, Beardsley L, et al. Natural history of cervicovaginal papillomavirus infection in young women. N Engl J Med 1998;338: 423-8
4. McCredie M, Sharples K, Paul C, et al. Natural history of cervical neoplasia and risk of invasive cancer in women with cervical intraepithelial neoplasia 3: A retrospective cohort study. Lancet Oncol 2008;9:425-34
5. Saslow D, Solomon D, Lawson HW, et al. American cancer society, american society for colposcopy and cervical pathology, and american society for clinical pathology screening guidelines for the prevention and early detec- tion of cervical cancer. Am J Clin Pathol 2012; 137:516-42
6. Schiffman M, Wentzensen N, Wacholder S, et al. Human papillomavirus testing in the prevention of cervical cancer. J Natl Cancer Inst 2011;103: 368-83
7. Katki H, Schiffman M, Castle P, et al. Fiveyear risks of CIN 31 and cervical cancer among women who test Pap-negative but are HPV-positive. J Low Genit Tract Dis 2013;17: S56-63
8. Schiffman M, Castle PE, Jeronimo J, et al. Human papillomavirus and cervical cancer. Lancet 2007;370:890-907
9. Dillner J, Rebolj M, Birembaut P, et al. Long term predictive values of cytology and human papillomavirus testing in cervical cancer screening: joint European cohort study. BMJ 2008;337
10. 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
11. Kalantari M, Garcia-Carranca A, Morales- Vazquez CD, et al. Laser capture microdissection of cervical human papillomavirus infections: Copy number of the virus in cancerous and normal tissue and heterogeneous DNA methylation. Virology 2009;390:261-7
12. Ding D, Chiang M, Lai H, et al. Methylation of the long control region of HPV16 is related to the severity of cervical neoplasia. Eur J Obstet Gynecol Reprod Biol 2009;147:215-20
13. Kalantari M, Calleja-Macias IE, Tewari D, et al. Conserved methylation patterns of human papillomavirus type 16 DNA in asymptomatic infection and cervical neoplasia. J Virol 2004;78: 12762-72
14. Bhattacharjee B, Sengupta S. CpG methylation of HPV 16 LCR at E2 binding site proximal to P97 is associated with cervical cancer in presence of intact E2. Virology 2006;354:280-5
15. Sun C, Reimers L, Burk R. Methylation of HPV16 genome CpG sites is associated with cervix precancer and cancer. Gynecol Oncol 2011; 121:59-63
16. Brandsma J, Sun Y, Lizardi PM, et al. Distinct human papillomavirus type 16 methylomes in cervical cells at different stages of premalignancy. Virology 2009;389:100-7
17. 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. JNCI 2012;104:556-65
18. Fernandez A, Rosales C, Lopez-Nieva P, et al. The dynamic DNA methylomes of doublestranded DNA viruses associated with human cancer. Genome Res 2009;19:438-51
19. Hong D, Ye F, Lu W, et al. Methylation status of the long control region of HPV 16 in clinical cervical specimens. Mol Med Report 2008;1:555-60
20. Snellenberg S, Schutze DM, Claassen-Kramer D, et al. Methylation status of the E2 binding sites of HPV16 in cervical lesions determined with the Luminex(R) xMAP system. Virology 2012;422: 357-65
21. Vinokurova S, von Knebel Doeberitz M. Differential methylation of the HPV 16 upstream regulatory region during epithelial differentiation and neoplastic transformation. PLoS One 2011;6: e24451
22. Mirabello L, Schiffman S, Ghosh S, et al. Elevated methylation of HPV16 DNA is associated with the development of high grade cervical intraepithelial neoplasia. Int J Cancer 2013;132:1412-22
23. Kalantari M, Chase DM, Tewari KS, et al. 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 2010;82:311-20
24. Bryant D, Tristram A, Liloglou T, et al. Quantitative measurement of Human Papillomavirus type 16 L1/L2 DNA methylation correlates with cervical disease grade. J Clin Virol 2014;59:24-9
25. 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;104:1738-49
26. Badal S, Badal V, Calleja-Macias IE, et al. The human papillomavirus-18 genome is efficiently targeted by cellular DNA methylation. Virology 2004;324:483-92
27. Turan T, Kalantari M, Calleja-Macias IE, et al. Methylation of the human papillomavirus-18 L1 gene: A biomarker of neoplastic progression? Virology 2006;349:175-83
28. Kalantari M, Osann K, Calleja-Macias IE, et al. 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 2014; 448:314-21
29. Castle P, Shaber R, LaMere B, et al. Human papillomavirus (HPV) genotypes in women with cervical precancer and cancer at Kaiser Permanente Northern California. Cancer Epidemiol Biomarkers Prev 2011;20:946-53
30. Burk RD, Ho GYF, Beardsley L, et al. Sexual behavior and partner characteristics are the predominant risk factors for genital human papillomavirus infection in young women. J Infect Dis 1996;174:679-89
31. Castle PE, Schiffman M, Gravitt PE, et al. Comparisons of HPV DNA detection by MY09/11 PCR methods. J Med Virol 2002;68:417-23
32. Sun C, Reimers LL, Burk RD. Methylation of HPV16 genome CpG sites is associated with cervix precancer and cancer. Gynecol Oncol 121:59-63
33. Tost J, Gut I. DNA methylation analysis by pyrosequencing. Nat Protoc 2007;2:2265-75
34. Smith BC, McAndrew T, Chen Z, et al. The cervical microbiome over 7 years and a comparison of methodologies for its characterization. PLoS One 7:e40425
35. Krueger F, Andrews S. Bismark: A flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics 2011;27:1571-2
36. Badal V, Chuang L, Tan E, et al. 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 2003;77:6227-34
37. Bland J, Altman D. Measuring agreement in method comparison studies. Stat Methods Med Res 1999;8:135-60
38. Bland J, Altman D. Statistical method for assessing agreement between two methods of clinical measurement. Lancet 1986;1:307-10
39. Passing H, Bablok W. A new biometrical procedure for testing the equality of measurements from two different analytical methods. Application of linear regression procedures for method comparison studies in clinical chemistry, Part I. J Clin Chem Clin Biochem 1983;21:709-20
40. Wentzensen N, Wacholder S. From differences in means between cases and controls to risk stratification: A business plan for biomarker development. Cancer Discov 2013;3:148-57.