Hostname: page-component-745bb68f8f-b6zl4 Total loading time: 0 Render date: 2025-01-31T10:59:54.333Z Has data issue: false hasContentIssue false
  • English
  • Français

Molecular approaches for HPV genotyping and HPV-DNA physical status

Published online by Cambridge University Press:  06 February 2017

D. Tsakogiannis ,
C. Gartzonika ,
S. Levidiotou-Stefanou  and
P. Markoulatos
D. Tsakogiannis*
Affiliation:
Department of Biochemistry & Biotechnology, Microbiology-Virology Laboratory, University of Thessaly, School of Health Sciences, Larissa, Greece
C. Gartzonika
Affiliation:
Department of Microbiology, University of Ioannina, Medical School, Ioannina, Greece
S. Levidiotou-Stefanou
Affiliation:
Department of Microbiology, University of Ioannina, Medical School, Ioannina, Greece
P. Markoulatos
Affiliation:
Department of Biochemistry & Biotechnology, Microbiology-Virology Laboratory, University of Thessaly, School of Health Sciences, Larissa, Greece
*
*Corresponding author: D. Tsakogiannis, Department of Biochemistry & Biotechnology, Microbiology-Virology Laboratory, University of Thessaly, School of Health Sciences, Ploutonos 26 & Aiolou str., 41221 Larissa, Greece. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Persistent infection with high-risk human papillomavirus (HPV) genotypes is the leading cause of cervical cancer development. To this end several studies have focused on designing molecular assays for HPV genotyping, which are considered as the gold standard for the early diagnosis of HPV infection. Moreover, the tendency of HPV DNA to be integrated into the host chromosome is a determining event for cervical oncogenesis. Thus, the establishment of molecular techniques was promoted in order to investigate the physical status of the HPV DNA and the locus of viral insertion into the host chromosome. The molecular approaches that have been developed recently facilitate the collection of a wide spectrum of valuable information specific to each individual patient and therefore can significantly contribute to the establishment of a personalised prognosis, diagnosis and treatment of HPV-positive patients. The present review focuses on state of the art molecular assays for HPV detection and genotyping for intra-lesion analyses, it examines molecular approaches for the determination of HPV-DNA physical status and it discusses the criteria for selecting the most appropriate regions of viral DNA to be incorporated in HPV genotyping and in the determination of HPV-DNA physical status.

Type
Review
Information
Expert Reviews in Molecular Medicine , Volume 19 , 2017 , e1
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1. zur Hausen, H. (1996) Papillomavirus infections – a major cause of human cancers. Biochimica et Biophysica Acta 1288, F55-F78 Google Scholar
2. Chen, Z., de Freitas, L.B. and Burk, R.D. (2015) Evolution and classification of oncogenic human papillomavirus types and variants associated with cervical cancer. Methods in Molecular Biology 1249, 3-26 Google Scholar
3. Tommasino, M. (2014) The human papillomavirus family and its role in carcinogenesis. Seminars in Cancer Biology 26, 13-21 CrossRefGoogle ScholarPubMed
4. Bernard, H.U. et al. (2010) Classification of papillomaviruses (PVs) based on 189 PV types and proposal of taxonomic amendments. Virology 401, 70-79 Google Scholar
5. Bernard, H.U., Calleja-Macias, I.E. and Dunn, S.T. (2006) Genome variation of human papillomavirus types: phylogenetic and medical implications. International Journal of Cancer 118, 1071-1076 Google Scholar
6. Doorbar, J. (2006) Molecular biology of human papillomavirus infection and cervical cancer. Clinical Science (London) 110, 525-541 Google Scholar
7. de Villiers, E.M. et al. (2004) Classification of papillomaviruses. Virology 324, 17-27 Google Scholar
8. Jemal, A. et al. (2011) Global cancer statistics. CA Cancer Journal for Clinicians 61, 69-90 Google Scholar
9. Forman, D. et al. (2012) Global burden of human papillomavirus and related diseases. Vaccine 5, F12-F23 Google Scholar
10. de Sanjose, S. et al. (2010) Human papillomavirus genotype attribution in invasive cervical cancer: a retrospective cross-sectional worldwide study. Lancet Oncology 11, 1048-1056 Google Scholar
11. Li, N. et al. (2011) Human papillomavirus type distribution in 30,848 invasive cervical cancers worldwide: variation by geographical region, histological type and year of publication. International Journal of Cancer 128, 927-935 CrossRefGoogle Scholar
12. Ronco, G. et al. (2013) Efficacy of HPV-based screening for prevention of invasive cervical cancer: follow-up of four European randomised controlled trials. Lancet 383, 524-532 CrossRefGoogle ScholarPubMed
13. Ikenberg, H. et al. (2013) Screening for cervical cancer precursors with p16/Ki-67 dual-stained cytology: results of the PALMS study. Journal of the National Cancer Institute 105, 1550-1557 Google Scholar
14. Snellenberg, S. et al. (2012) Development of a multiplex methylation-specific PCR as candidate triage test for women with an HPV-positive cervical scrape. BMC Cancer 12, 551 Google Scholar
15. Brentnall, A.R. et al. (2014) A DNA methylation classifier of cervical precancer based on human papillomavirus and human genes. International Journal of Cancer 135, 1425-1432 Google Scholar
16. Castle, P.E. et al. (2011) Performance of carcinogenic human papillomavirus (HPV) testing and HPV16 or HPV18 genotyping for cervical cancer screening of women aged 25 years and older: a subanalysis of the ATHENA study. Lancet Oncology 12, 880-890. 1CrossRefGoogle ScholarPubMed
17. Cox, J.T. et al. (2013) Comparison of cervical cancer screening strategies incorporating different combinations of cytology, HPV testing, and genotyping for HPV 16/18: results from the ATHENA HPV study. American Journal Obstetrics & Gynecology 208, 184. e1–84. e11Google Scholar
18. McLaughlin-Drubin, M.E. and Munger, K. (2009) The human papillomavirus E7 oncoprotein. Virology 384, 335-344 Google Scholar
19. Howie, H.L., Katzenellenbogen, R.A. and Galloway, D.A. (2009) Papillomavirus E6 proteins. Virology 384, 324-334 CrossRefGoogle ScholarPubMed
20. Moody, C.A. and Laimins, L.A. (2010) Human papillomavirus oncoproteins: pathways to transformation. Nature Reviews Cancer 10, 550-560 Google Scholar
21. Doorbar, J. et al. (2012) The biology and life-cycle of human papillomaviruses. Vaccine 30 (Suppl 5), F55-F70 CrossRefGoogle ScholarPubMed
22. Hudelist, G. et al. (2004) Physical state and expression of HPV DNA in benign and dysplastic cervical tissue: different levels of viral integration are correlated with lesion grade. Gynecologic Oncology 92, 873-880 Google Scholar
23. Cricca, M. et al. (2007) Viral DNA load, physical status and E2/E6 ratio as markers to grade HPV16 positive women for high-grade cervical lesions. Gynecologic Oncology 106, 549-557 Google Scholar
24. Li, W. et al. (2008) The physical state of HPV16 infection and its clinical significance in cancer precursor lesion and cervical carcinoma. Journal of Cancer Research and Clinical Oncology 134, 1355-1361 Google Scholar
25. Boulet, G.A. et al. (2009) Human papillomavirus 16 load and E2/E6 ratio in HPV16-positive women: biomarkers for cervical intraepithelial neoplasia >or=2 in a liquid-based cytology setting? Cancer Epidemiology Biomarkers and Prevention 18, 2992-2999 Google Scholar
26. Akagi, K. et al. (2014) Genome-wide analysis of HPV integration in human cancers reveals recurrent, focal genomic instability. Genome Research 24, 185-199 Google Scholar
27. Tsakogiannis, D. et al. (2016) Identification of rearranged sequences of HPV16 DNA in precancerous and cervical cancer cases. Molecular and Cellular Probes 30, 6-12 Google Scholar
28. Wentzensen, N., Vinokurova, S. and von Knebel Doeberitz, M. (2004) Systematic review of genomic integration sites of human papillomavirus genomes in epithelial dysplasia and invasive cancer of the female lower genital tract. Cancer Research 64, 3878-3884 Google Scholar
29. Xu, B. et al. (2013) Multiplex identification of human papillomavirus 16 DNA integration sites in cervical carcinomas. PLoS ONE 8, e66693 Google Scholar
30. Tsakogiannis, D. et al. (2014) Determination of human papillomavirus 16 physical status through E1/E6 and E2/E6 ratio analysis. Journal of Medical Microbiology 63, 1716-1723 Google Scholar
31. Theelen, W. et al. (2013) Human papillomavirus multiplex ligation-dependent probe amplification assay for the assessment of viral load, integration, and gain of telomerase-related genes in cervical malignancies. Human Pathology 44, 2410-2418 Google Scholar
32. Abreu, A.L. et al. (2012) A review of methods for detect human Papillomavirus infection. Virology Journal 9, 262 Google Scholar
33. Schiffman, M. and Wentzensen, N. (2016) A suggested approach to simplify and improve cervical screening in the United States. Journal of Lower Genital Tract Disease 20, 1-7 Google Scholar
34. Castle, P.E. et al. (2012) Introduction of human papillomavirus DNA screening in the world: 15 years of experience. Vaccine 5, F117-F122 CrossRefGoogle Scholar
35. Cuzick, J. et al. (2008) Longterm follow-up of cervical abnormalities among women screened by HPV testing and cytology-Results from the Hammersmith study. International Journal of Cancer 122, 2294-2300 Google Scholar
36. Bozzetti, M. et al. (2000) Comparison between hybrid capture II and polymerase chain reaction results among women at low risk for cervical cancer. Annals of Epidemiology 10, 466 Google Scholar
37. Ratnam, S. et al. (2011) Aptima HPV E6/E7 mRNA test is as sensitive as Hybrid Capture 2 Assay but more specific at detecting cervical precancer and cancer. Journal of Clinical Microbiology 49, 557-564 Google Scholar
38. Luu, H.N. et al. (2013) Comparison of the accuracy of Hybrid Capture II and polymerase chain reaction in detecting clinically important cervical dysplasia: a systematic review and meta-analysis. Cancer Medicine 2, 367-390 CrossRefGoogle ScholarPubMed
39. Meijer, C.J. et al. (2009) Guidelines for human papillomavirus DNA test requirements for primary cervical cancer screening in women 30 years and older. International Journal of Cancer 124, 516-520 Google Scholar
40. Castle, P.E. et al. (2004) Hybrid capture 2 viral load and the 2-year cumulative risk of cervical intraepithelial neoplasia grade 3 or cancer. American Journal of Obstetrics & Gynecology 191, 1590-1597 Google Scholar
41. Gravitt, P.E. et al. (2011) Looking ahead: a case for human papillomavirus testing of self-sampled vaginal specimens as a cervical cancer screening strategy. International Journal of Cancer 129, 517-527 Google Scholar
42. Fotiadis, D.I. (2016) HPV Detection Methods, Handbook of Research on Trends in the Diagnosis and Treatment of Chronic Conditions, IGI Global, Hershey, Pennsylvania, USA, pp. 99-132 Google Scholar
43. Day, S.P. et al. (2009) Analytical performance of the Investigational Use Only Cervista HPV HR test as determined by a multi-center study. Journal of Clinical Virology 45, S63-S72 Google Scholar
44. Einstein, M.H. et al. (2010) Clinical validation of the Cervista HPV HR and 16/18 genotyping tests for use in women with ASC-US cytology. Gynecologic Oncology 118, 116-122 Google Scholar
45. Belinson, J.L. et al. (2011) A population-based clinical trial comparing endocervical high-risk HPV testing using hybrid capture 2 and Cervista from the SHENCCAST II Study. Americal Journal of Clinical Pathology 135, 790-795 CrossRefGoogle ScholarPubMed
46. Tao, K. et al. (2014) Comparative study of the cervista and hybrid capture 2 methods in detecting high-risk human papillomavirus in cervical lesions. Diagnostic Cytopathology 42, 213-217 Google Scholar
47. Boehmer, G. et al. (2014) A population-based observational study comparing Cervista and Hybrid Capture 2 methods: improved relative specificity of the Cervista assay by increasing its cut-off. BMC Infectious Diseases 14, 674 Google Scholar
48. Rao, A. et al. (2013) Development and characterization of the cobas human papillomavirus test. Journal of Clinical Microbiology 51, 1478-1484 CrossRefGoogle ScholarPubMed
49. Heideman, D.A. et al. (2011) Clinical validation of the cobas 4800 HPV test for cervical screening purposes. Journal of Clinical Microbiology 49, 3983-3985 Google Scholar
50. Cui, M. et al. (2014) Clinical performance of Roche Cobas 4800 HPV Test. Journal of Clinical Microbiology 52, 2210-2211 Google Scholar
51. Castle, P.E. et al. (2015) Comparison of human papillomavirus detection by Aptima HPV and cobas HPV tests in a population of women referred for colposcopy following detection of atypical squamous cells of undetermined significance by Pap cytology. Journal of Clinical Microbiology 53, 1277-1281 Google Scholar
52. Castle, P.E. et al. (2015) The reliability of high-risk human papillomavirus detection by Aptima HPV assay in women with ASC-US cytology. Journal of Clinical Virology 69, 52-55 Google Scholar
53. Haedicke, J. and Iftner, T. (2016) A review of the clinical performance of the Aptima HPV assay. Journal of Clinical Virology 1, S40-S48 Google Scholar
54. Cuzick, J. et al. (2010) Performance of the Abbott RealTime high-risk HPV test in women with abnormal cervical cytology smears. Journal of Medical Virology 82, 1186-1191 CrossRefGoogle ScholarPubMed
55. Hwang, Y. and Lee, M. (2012) Comparison of the AdvanSure human papillomavirus screening real-time PCR, the Abbott RealTime high risk human papillomavirus test, and the hybrid capture human papillomavirus DNA test for the detection of human papillomavirus. Annals of Laboratory Medicine 32, 201-205 CrossRefGoogle ScholarPubMed
56. Poljak, M. and Oštrbenk, A. (2013) The Abbott RealTime High Risk HPV test is a clinically validated human papillomavirus assay for triage in the referral population and use in primary cervical cancer screening in women 30 years and older: a review of validation studies. Acta Dermatovenerol Alpina Pannonica et Adriatica 22, 43-47 Google Scholar
57. Park, S. et al. (2013) Comparison of the analytical and clinical performances of Abbott RealTime High Risk HPV, Hybrid Capture 2, and DNA Chip assays in gynecology patients. Diagnostic Microbiology and Infectious Disease 76, 432-436 CrossRefGoogle ScholarPubMed
58. Chung, H.S., Hahm, C. and Lee, M. (2014) Comparison of the clinical performances of the AdvanSure HPV Screening Real-Time PCR, the Abbott Real-Time High-Risk HPV test, and the Hybrid Capture High-Risk HPV DNA test for Cervical Cancer Screening. Journal of Virological Methods 205, 57-60 Google Scholar
59. Ngou, J. et al. (2015) Comparison of analytical and clinical performances of the digene HC2 HPV DNA assay and the INNO-LiPA HPV genotyping assay for detecting high-risk HPV infection and cervical neoplasia among HIV-positive African women. Journal of Acquired Immune Deficiency Syndromes 68, 162-168 CrossRefGoogle ScholarPubMed
60. Alberizzi, P. et al. (2014) Evaluation of the HPV typing INNO-LiPA EXTRA assay on formalin-fixed paraffin-embedded cervical biopsy samples. Journal of Clinical Virology 61, 535-539 Google Scholar
61. van Hamont, D. et al. (2006) Evaluation of the SPF10-INNO LiPA human papillomavirus (HPV) genotyping test and the roche linear array HPV genotyping test. Journal of Clinical Microbiology 44, 3122-3129 CrossRefGoogle ScholarPubMed
62. Gravitt, P.E. et al. (2008) A comparison of linear array and hybrid capture 2 for detection of carcinogenic human papillomavirus and cervical precancer in ASCUS-LSIL triage study. Cancer Epidemiology, Biomarkers & Prevention 17, 1248-1254 CrossRefGoogle ScholarPubMed
63. Ejegod, D.M., Rebolj, M. and Bonde, J. (2015) Comparison of analytical and clinical performance of CLART HPV2 genotyping assay to Linear Array and Hybrid Capture 2: a split-sample study. BMC Cancer 15, 216 Google Scholar
64. Roberts, C.C. et al. (2011) Comparison of real-time multiplex human papillomavirus (HPV) PCR assays with the linear array HPV genotyping PCR assay and influence of DNA extraction method on HPV detection. Journal of Clinical Microbiology 49, 1899-1906 Google Scholar
65. Pista, A., Verdasca, N. and Oliveira, A. (2011) Clinical performance of the CLART human papillomavirus 2 assay compared with the hybrid capture 2 test. Journal of Medical Virology 83, 272-276 CrossRefGoogle ScholarPubMed
66. Crosbie, E.J. et al. (2015) The PapilloCheck Assay for Detection of High-Grade Cervical Intraepithelial Neoplasia. Journal of Clinical Microbiology 53, 3553-3559 CrossRefGoogle ScholarPubMed
67. Heard, I. et al. (2016) Clinical and analytical performance of the PapilloCheck HPV-Screening assay using the VALGENT framework. Journal of Clinical Virology 81, 6-11 Google Scholar
68. Vieira, L. and Almeida, A. (2013) The cytology and DNA detection by the PapilloCheck® test in the diagnosis of human papillomavirus infection. European Journal of Microbiology and Immunology 3, 61-67 Google Scholar
69. Didelot, M.N. et al. (2011) Comparison of the PapilloCheck® assay with the digene HC2 HPV DNA assay for the detection of 13 high-risk human papillomaviruses in cervical and anal scrapes. Journal of Medical Virology 83, 1377-1382 Google Scholar
70. Guo, M. et al. (2008) Evaluation of a commercialized in situ hybridization assay for detecting human papillomavirus DNA in tissue specimens from patients with cervical intraepithelial neoplasia and cervical carcinoma. Journal of Clinical Microbiology 46, 274-280 Google Scholar
71. Sheng, Z. et al. (2013) Detection of high-risk human papillomavirus subtypes in cervical glandular neoplasia by in situ hybridization. International Journal of Clinical and Experimental Pathology 6, 2168-2177 Google Scholar
72. Kong, C.S. et al. (2007) p16INK4A immunohistochemistry is superior to HPV in situ hybridization for the detection of high-risk HPV in atypical squamous metaplasia. American Journal of Surgical Pathology 31, 33-43 Google Scholar
73. Sotlar, K. et al. (2004) Detection and typing of human papillomavirus by E6 nested multiplex PCR. Journal of Clinical Microbiology 42, 3176-3384 CrossRefGoogle ScholarPubMed
74. Tsakogiannis, D. et al. (2015) Multiplex PCR assay for the rapid identification of human papillomavirus genotypes 16, 18, 45, 35, 66, 33, 51, 58, and 31 in clinical samples. Archives of Virology 160, 207-214 Google Scholar
75. de-Roda, H.A. et al. (1995) The use of general primers GP5 and GP6 elongated at their 3_ ends with adjacent highly conserved sequences improves human papillomavirus detection by PCR. Journal of General Virology 76, 1057-1062 Google Scholar
76. Gravitt, P.E. et al. (2000) Improved amplification of genital human papillomaviruses. Journal of Clinical Microbiology 38, 357-361 Google Scholar
77. Karlsen, F. et al. (1996) Use of multiple PCR primer sets for optimal detection of human papillomavirus. Journal of Clinical Microbiology 34, 2095-2100 CrossRefGoogle ScholarPubMed
78. Kleter, B. et al. (1999) Development and clinical evaluation of a highly sensitive PCR-reverse hybridization line probe assay for detection and identification of anogenital human papillomavirus. Journal of Clinical Microbiology 37, 2508-2517 Google Scholar
79. Sasagawa, T. et al. (2000) A new PCR-based assay amplifies the E6–E7 genes of most mucosal human papillomaviruses (HPV). Virus Research 67, 127-139 Google Scholar
80. Lin, H. et al. (2005) A simple method for the detection and genotyping of high-risk human papillomavirus using seminested polymerase chain reaction and reverse hybridization. Gynecologic Oncology 96, 84-91 Google Scholar
81. Depuydt, C.E. et al. (2007) Comparison of MY09/11 consensus PCR and type-specific PCRs in the detection of oncogenic HPV types. Journal of Cellular and Molecular Medicine 11, 881-891 Google Scholar
82. Shen-Gunther, J. and Rebeles, J. (2013) Genotyping human papillomaviruses: development and evaluation of a comprehensive DNA microarray. Gynecologic Oncology 128, 433-441 Google Scholar
83. Maver, P.J. et al. (2010) Detection and typing of low-risk human papillomavirus genotypes HPV 6, HPV 11, HPV 42, HPV 43 and HPV 44 by polymerase chain reaction and restriction fragment length polymorphism. Journal of Virological Methods 169, 215-218 Google Scholar
84. Naqvi, S.H., Wajid, S. and Mitra, A.B. (2004) Restriction fragment length polymorphism of L1 amplicon using Rsa 1 detects five different human papillomavirus types and their co-infections among women attending a gynaecological outpatient department. Journal of Virological Methods 117, 91-95 CrossRefGoogle ScholarPubMed
85. Militello, V. et al. (2013) Accurate human papillomavirus genotyping by 454 pyrosequencing. Clinical Microbiology and Infection 19, E428-E434 Google Scholar
86. Romero-Pastrana, F. (2012) Detection and typing of human papilloma virus by multiplex PCR with type-specific primers. ISRN Microbiology 2012, 186915 Google Scholar
87. Gravitt, P.E. et al. (1998) Genotyping of 27 human papillomavirus types by using L1 consensus PCR products by a single-hybridization, reverse line blot detection method. Journal of Clinical Microbiology 36, 3020-3027 Google Scholar
88. Szarewski, A. et al. (2008) Comparison of predictors for high-grade cervical intraepithelial neoplasia in women with abnormal smears. Cancer Epidemiology, Biomarkers & Prevention 17, 3033-3042 Google Scholar
89. Schmitt, M. et al. (2006) Bead-based multiplex genotyping of human papillomaviruses. Journal of Clinical Microbiology 44, 504-512 Google Scholar
90. Zubach, V. et al. (2012) Novel microsphere-based method for detection and typing of 46 mucosal human papillomavirus types. Journal of Clinical Microbiology 50, 460-464 CrossRefGoogle ScholarPubMed
91. Oh, Y. et al. (2007) Polymerase chain reaction-based fluorescent Luminex assay to detect the presence of human papillomavirus types. Cancer Science 98, 549-554 Google Scholar
92. Jiang, H.L. et al. (2006) Genotyping of human papillomavirus in cervical lesions by L1 consensus PCR and the Luminex xMAP system. Journal of Medical Microbiology 55, 715-720 Google Scholar
93. Seme, K. et al. (2009) Digene HPV Genotyping RH Test RUO: comparative evaluation with INNO-LiPA HPV Genotyping Extra Test for detection of 18 high-risk and probable high-risk human papillomavirus genotypes. Journal of Clinical Virology 46, 176-179 Google Scholar
94. Chen, L. et al. (2013) Simple and rapid human papillomavirus genotyping method by restriction fragment length polymorphism analysis with two restriction enzymes. Journal of Medical Virology 85, 1229-1234 Google Scholar
95. Naqvi, S.H., Wajid, S. and Mitra, A.B. (2004) Restriction fragment length polymorphism of L1 amplificon using RSA 1 detects five different human papillomavirus types and their co-infections among women attending a gynaecological outpatient department. Journal of Virological Methods 117, 91-95 Google Scholar
96. Gimenes, F. et al. (2014) Sensitive simultaneous detection of seven sexually transmitted agents in semen by multiplex-PCR and of HPV by single PCR. PLoS ONE 9, e98862 CrossRefGoogle ScholarPubMed
97. Milutin Gasperov, N. et al. (2008) Detection and typing of human papillomaviruses combining different methods: polymerase chain reaction, restriction fragment length polymorphism, line probe assay and sequencing. Pathology and Oncology Research 14, 355-363 Google Scholar
98. Coser, J. et al. (2011) Human papillomavirus detection and typing using a nested-PCR-RFLP assay. Brazilian Journal of Infectious Diseases 15, 467-472 Google Scholar
99. Carvalho Nde, O. et al. (2010) Comparison of HPV genotyping by type-specific PCR and sequencing. Memórias do Instituto Oswaldo Cruz 105, 73-78 Google Scholar
100. Tardif, K.D. et al. (2013) Sequencing-based genotyping of mixed human papillomavirus infections by use of RipSeq software. Journal of Clinical Microbiology 51, 1278-1280 Google Scholar
101. Lee, S.H. et al. (2007) Routine human papillomavirus genotyping by DNA sequencing in community hospital laboratories. Infectious Agents and Cancer 2, 11 Google Scholar
102. Wang, L. et al. (2016) Prevalence of high-risk human papillomavirus (HR-HPV) genotypes and multiple infections in cervical abnormalities from Northern Xinjiang, China. PLoS ONE 11, e0160698 Google Scholar
103. Husnjak, K. et al. (2000) Comparison of five different polymerase chain reaction methods for detection of human papillomavirus in cervical cell specimens. Journal of Virological Methods 88, 125-134 Google Scholar
104. Giovannelli, L. et al. (2004) Detection of human papillomavirus DNA in cervical samples: analysis of the new PGMY-PCR compared to the hybrid capture II and MY-PCR assays and a two-step nested PCR assay. Journal of Clinical Microbiology 42, 3861-3864 Google Scholar
105. Lin, C.Y. et al. (2008) Human papillomavirus typing with a polymerase chain reaction-based genotyping array compared with type-specific PCR. Journal of Clinical Virology 42, 361-367 Google Scholar
106. Brestovac, B. et al. (2005) Multiplex nested PCR (MNP) assay for the detection of 15 high risk genotypes of human papillomavirus. Journal of Clinical Virology 33, 116-122 Google Scholar
107. Nishiwaki, M. et al. (2008) Genotyping of human papillomaviruses by a novel one-step typing method with multiplex PCR and clinical applications. Journal of Clinical Microbiology 46, 1161-1168 Google Scholar
108. Souho, T. and Bennani, B. (2014) Oncogenic human papillomavirus genotyping by multiplex PCR and fragment analysis. Journal of Virological Methods 196, 45-49 Google Scholar
109. Ozaki, S. et al. (2014) Analytical performance of newly developed multiplex human papillomavirus genotyping assay using Luminex xMAPTM technology (MebgenTM HPV Kit). Journal of Virological Methods 204, 73-80 Google Scholar
110. García-Vallve, S., Alonso, A. and Bravo, I.G. (2005) Papillomaviruses: different genes have different histories. Trends in Microbiology 13, 514-521 CrossRefGoogle ScholarPubMed
111. Shah, S.D., Doorbar, J. and Goldstein, R.A. (2010) Analysis of host-parasite incongruence in papillomavirus evolution using importance sampling. Molecular Biology and Evolution 27, 1301-1314 Google Scholar
112. Tsakogiannis, D. et al. (2015) Duplex Real-time PCR assay and SYBR green I melting curve analysis for molecular identification of HPV genotypes 16, 18, 31, 35, 51 and 66. Molecular and Cellular Probes 29, 13-18 Google Scholar
113. Tsakogiannis, D. et al. (2015) Sites of disruption within E1 and E2 genes of HPV16 and association with cervical dysplasia. Journal of Medical Virology 87, 1973-1980 Google Scholar
114. Li, H. et al. (2013) Preferential sites for the integration and disruption of human papillomavirus 16 in cervical lesions. Journal of Clinical Virology 56, 342-347 CrossRefGoogle ScholarPubMed
115. Espy, M.J. et al. (2006) Real-time PCR in clinical microbiology: applications for routine laboratory testing. Clinical Microbiology Reviews 19, 165-256 Google Scholar
116. Depuydt, C.E. et al. (2012) Clinical validation of a type-specific real-time quantitative human papillomavirus PCR against the performance of hybrid capture 2 for the purpose of cervical cancer screening. Journal of Clinical Microbiology 50, 4073-4077 Google Scholar
117. Micalessi, I.M. et al. (2011) High-throughput detection, genotyping and quantification of the human papillomavirus using real-time PCR. Clinical Chemistry and Laboratory Mediciny 50, 655-661 Google Scholar
118. Micalessi, M.I., Boulet, G.A. and Bogers, J. (2015) A real-time PCR approach based on SPF10 primers and the INNO-LiPA HPV genotyping extra assay for the detection and typing of human papillomavirus. Methods in Molecular Biology 1249, 27-35 Google Scholar
119. Wong, M.L. and Medrano, J.F. (2005) Real-time PCR for mRNA quantitation. Biotechniques 39, 75-85 Google Scholar
120. Dabic, M.M. et al. (2004) Comparison of polymerase chain reaction and catalyzed signal amplification in situ hybridization methods for human papillomavirus detection in paraffin-embedded cervical preneoplastic and neoplastic lesions. Archives of Medical Research 35, 511-516 Google Scholar
121. Kelesidis, T. et al. (2011) Human papillomavirus (HPV) detection using in situ hybridization in histologic samples: correlations with cytologic changes and polymerase chain reaction HPV detection. American Journal of Clinical Pathology 136, 119-127 Google Scholar
122. Larque, A.B. et al. (2014) High-risk human papillomavirus is transcriptionally active in a subset of sinonasal squamous cell carcinomas. Modern Pathology 27, 343-351 Google Scholar
123. Wang, H. et al. (2014) RNAscope for in situ detection of transcriptionally active human papillomavirus in head and neck squamous cell carcinoma. Journal of Visualized Experiments 85, 51426 Google Scholar
124. Evans, M.F. et al. (2014) HPV E6/E7 RNA in situ hybridization signal patterns as biomarkers of three-tier cervical intraepithelial neoplasia grade. PLoS ONE 9, e91142 Google Scholar
125. Nuovo, G.J. (2011) In situ detection of human papillomavirus DNA after PCR-amplification. Methods in Molecular Biology 688, 35-46 Google Scholar
126. Xiao, Y. (2001) High sensitivity of PCR in situ hybridization for the detection of human papillomavirus infection in uterine cervical neoplasias. Gynecologic Oncology 82, 350-354 Google Scholar
127. Venuti, A. and Paolini, F. (2012) HPV detection methods in head and neck cancer. Head and Neck Pathology 1, S63-S74 Google Scholar
128. McKinney, C.C., Hussmann, K.L. and McBride, A.A. (2015) The Role of the DNA Damage Response throughout the Papillomavirus life cycle. Viruses 21, 2450-2469 Google Scholar
129. Ziegert, C. et al. (2003) A comprehensive analysis of HPV integration loci in anogenital lesions combining transcript and genome-based amplification techniques. Oncogene 22, 3977-3984 Google Scholar
130. Jeon, S., Allen-Hoffmann, B.L. and Lambert, P.F. (1995) Integration of human papillomavirus type 16 into the human genome correlates with a selective growth advantage of cells. Journal of Virology 69, 2989-2997 Google Scholar
131. Peter, M. et al. (2010) Frequent genomic structural alterations at HPV insertion sites in cervical carcinoma. Journal of Pathology 221, 320-330 CrossRefGoogle ScholarPubMed
132. Matovina, M. et al. (2009) Identification of human papillomavirus type 16 integration sites in high-grade precancerous cervical lesions. Gynecologic Oncology 113, 120-127 CrossRefGoogle ScholarPubMed
133. Chandrani, P. et al. (2015) NGS-based approach to determine the presence of HPV and their sites of integration in human cancer genome. British Journal of Cancer 112, 1958-1965 Google Scholar
134. Hu, Z. et al. (2015) Genome-wide profiling of HPV integration in cervical cancer identifies clustered genomic hot spots and a potential microhomology-mediated integration mechanism. Nature Genetics 47, 158-163 Google Scholar
135. Ferber, M.J. et al. (2003) Preferential integration of human papillomavirus type 18 near the c-myc locus in cervical carcinoma. Oncogene 22, 7233-7242 Google Scholar
136. Thorland, E.C. et al. (2003) Common fragile sites are preferential targets for HPV16 integrations in cervical tumors. Oncogene 22, 1225-1237 Google Scholar
137. Thorland, E.C. et al. (2000) Human papillomavirus type 16 integrations in cervical tumors frequently occur in common fragile sites. Cancer Research 60, 5916-5921 Google Scholar
138. Schmitz, M. et al. (2012) Non-random integration of the HPV genome in cervical cancer. PLoS ONE 7, e39632 CrossRefGoogle ScholarPubMed
139. Andersson, S. et al. (2005) Type distribution, viral load and integration state of high-risk human papillomaviruses in pre-stages of cervical cancer (CIN). British Journal of Cancer 92, 2195-2200 Google Scholar
140. Huang, L.W. et al. (2008) Integration of human papillomavirus type-16 and type-18 is a very early event in cervical carcinogenesis. Journal of Clinical Pathology 61, 627-631 Google Scholar
141. Han, L. et al. (2015) Comparative study of HPV16 integration in cervical lesions between ethnicities with high and low rates of infection with high-risk HPV and the correlation between integration rate and cervical neoplasia. Experimental and Therapeutic Medicine 10, 2169-2174 Google Scholar
142. Das, P. et al. (2015) Human papillomavirus (HPV) genome status & cervical cancer outcome – a retrospective study. Indian Journal of Medical Research 142, 525-352Google Scholar
143. Pett, M. and Coleman, N. (2007) Integration of high-risk human papillomavirus: a key event in cervical carcinogenesis? The Journal of Pathology 212, 356-367 Google Scholar
144. Klaes, R. et al. (1999) Detection of high-risk cervical intraepithelial neoplasia and cervical cancer by amplification of transcripts derived from integrated papillomavirus oncogenes. Cancer Research 59, 6132-6136 Google Scholar
145. Vinokurova, S. et al. (2008) Type-dependent integration frequency of human papillomavirus genomes in cervical lesions. Cancer Research 68, 307-313 Google Scholar
146. Chaiwongkot, A. et al. (2013) Detection of the human papillomavirus 58 physical state using the amplification of papillomavirus oncogene transcripts assay. Journal of Virological Methods 189, 290-298 Google Scholar
147. Fehrmann, F. and Laimins, L.A. (2003) Human papillomaviruses: targeting differentiating epithelial cells for malignant transformation. Oncogene 22, 5201-5207 Google Scholar
148. Badaracco, G. et al. (2002) HPV16 and HPV18 in genital tumors: significantly different levels of viral integration and correlation to tumor invasiveness. Journal of Medical Virology 67, 574-582 CrossRefGoogle ScholarPubMed
149. Woodman, C.B. et al. (2003) Human papillomavirus type 18 and rapidly progressing cervical intraepithelial neoplasia. Lancet 361, 40-43 Google Scholar
150. Cullen, A.P. et al. (1991) Analysis of the physical state of different human papillomavirus DNAs in intraepithelial and invasive cervical neoplasms. Journal of Virology 65, 606-612 Google Scholar
151. Pirami, L., Giache, V. and Becciolini, A. (1997) Analysis of HPV16, 18, 31, and 35 DNA in pre-invasive and invasive lesions of the uterine cervix. Journal of Clinical Pathology 50, 600-604 Google Scholar
152. Bhat, S. et al. (2016) Biological implications and therapeutic significance of DNA methylation regulated genes in cervical cancer. Biochimie 121, 298-311 Google Scholar
153. Jiménez-Wences, H. et al. (2016) Methylation and expression of miRNAs in precancerous lesions and cervical cancer with HPV16 infection. Oncology Reports 35, 2297-2305 Google Scholar
154. Tsakogiannis, D. et al. (2012) Sequence variation analysis of the E2 gene of human papilloma virus type 16 in cervical lesions from women in Greece. Archives of Virology 157, 825-832 Google Scholar
155. Graham, D.A. and Herrington, C.S. (2000) HPV-16 E2 gene disruption and sequence variation in CIN 3 lesions and invasive squamous cell carcinomas of the cervix: relation to numerical chromosome abnormalities. Molecular Pathology 53, 201-206 Google Scholar
156. Tsakogiannis, D. et al. (2013) Molecular and evolutionary analysis of HPV16 E6 and E7 genes in Greek women. Journal of Medical Microbiology 62, 1688-1696 Google Scholar
157. Grodzki, M. et al. (2006) Increased risk for cervical disease progression of French women infected with the human papillomavirus type 16 E6-350G variant. Cancer Epidemiology, Biomarkers & Prevention 15, 820-822 Google Scholar
158. Andersson, S. et al. (2000) Uneven distribution of HPV 16 E6 prototype and variant (L83V) oncoprotein in cervical neoplastic lesions. British Journal of Cancer 83, 307-310 Google Scholar
159. Arias-Pulido, H. et al. (2006) Human papillomavirus type 16 integration in cervical carcinoma in situ and in invasive cervical cancer. Journal of Clinical Microbiology 44, 1755-1762 Google Scholar
160. Cricca, M. et al. (2009) Disruption of HPV16 E1 and E2 genes in precancerous cervical lesions. Journal of Virological Methods 158, 180-183 Google Scholar
161. Wang, L. et al. (2013) Integration sites and genotype distributions of human papillomavirus in cervical intraepithelial neoplasia. Asian Pacific Journal of Cancer Prevention 14, 3837-3841 Google Scholar
162. Khoury, J.D. et al. (2013) Landscape of DNA virus associations across human malignant cancers: analysis of 3,775 cases using RNA-Seq. Journal of Virology 87, 8916-8926 Google Scholar
163. McBride, A.A. (2013) The papillomavirus E2 proteins. Virology 445, 57-79 Google Scholar
164. Kraus, I. et al. (2008) The majority of viral-cellular fusion transcripts in cervical carcinomas cotranscribe cellular sequences of known or predicted genes. Cancer Research 68, 2514-2522 Google Scholar
165. D'Abramo, C.M. and Archambault, J. (2011) Small molecule inhibitors of human papillomavirus protein-protein interactions. The Open Virology Journal 5, 80-95 Google Scholar
166. Lehoux, M., Gagnon, D. and Archambault, J. (2014) E1-mediated recruitment of a UAF1-USP deubiquitinase complex facilitates human papillomavirus DNA replication. Journal of Virology 88, 8545-8555 Google Scholar
167. Kalantari, M. et al. (1998) Disruption of the E1 and E2 reading frames of HPV 16 in cervical carcinoma is associated with poor prognosis. International Journal of Gynecologic Pathology 17, 146-153 Google Scholar
168. Briolat, J. et al. (2007) HPV prevalence, viral load and physical state of HPV-16 in cervical smears of patients with different grades of CIN. International Journal of Cancer 121, 2198-2204 Google Scholar
169. Houldsworth, J. (2014) FHACT: the FISH-based HPV-associated cancer test that detects nonrandom gain at four genomic loci as biomarkers of disease progression. Expert Reviews in Molecular Diagnostics 14, 921-934 Google Scholar
170. Olthof, N.C. et al. (2015) Viral load, gene expression and mapping of viral integration sites in HPV16-associated HNSCC cell lines. International Journal of Cancer 136, 207-218 Google Scholar
171. Gimenes, F. et al. (2016) Simultaneous detection of human papillomavirus integration and c-MYC gene amplification in cervical lesions: an emerging marker for the risk to progression. Archives of Gynecology and Obstetrics 293, 857-863 Google Scholar
172. De Marchi Triglia, R. et al. (2009) HPV in situ hybridization signal patterns as a marker for cervical intraepithelialneoplasia progression. Gynecologic Oncology 112, 114-118 Google Scholar
173. Hopman, A.H.N. et al. (2005) HPV in situ hybridization: impact of different protocols on the detection of integrated HPV. International Journal of Cancer 115, 419-428 Google Scholar
174. Sokolova, I. et al. (2007) Chromosomal biomarkers for detection of human papillomavirus associated genomic instability in epithelial cells of cervical cytology specimens. Journal of Molecular Diagnostics 9, 604-611 Google Scholar
175. Luft, F. et al. (2001) Detection of integrated papillomavirus sequences by ligation-mediated PCR (DIPS-PCR) and molecular characterization in cervical cancer cells. International Journal of Cancer 92, 9-17 Google Scholar
176. Lu, X. et al. (2014) Multiple-integrations of HPV16 genome and altered transcription of viral oncogenes and cellular genes are associated with the development of cervical cancer. PLoS ONE 9, e97588 Google Scholar
177. Saunier, M. et al. (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. Journal of Clinical Microbiology 46, 3678-3685 Google Scholar
178. Jiang, M. et al. (2009) Sequence variation of human papillomavirus type 16 and measurement of viral integration by quantitative PCR. Journal of Clinical Microbiology 47, 521-526 Google Scholar
179. Peitsaro, P., Johansson, B. and Syrjänen, S. (2002) Integrated human papillomavirus type 16 is frequently found in cervical cancer precursors as demonstrated by a novel quantitative real-time PCR technique. Journal of Clinical Microbiology 40, 886-891 CrossRefGoogle ScholarPubMed
180. Sarkar, G., Turner, R.T. and Bolander, M.E. (1993) Restriction-site PCR: a direct method of unknown sequence retrieval adjacent to a known locus by using universal primers. PCR Methods and Applications 2, 318-322 Google Scholar
181. Chen, C.Y. (2014) DNA polymerases drive DNA sequencing-by-synthesis technologies: both past and present. Frontiers in Microbiology 5, 305 Google Scholar
182. Datta, S. et al. (2015) Next-generation sequencing in clinical virology: discovery of new viruses. World Journal of Virology 4, 265-276 Google Scholar
183. Soper, S.A. et al. (1998) Sanger DNA-sequencing reactions performed in a solid-phase nanoreactor directly coupled to capillary gel electrophoresis. Analytical Chemistry 70, 4036-4043 Google Scholar
184. Flores-Miramontes, M.G. et al. (2015) Human papillomavirus genotyping by Linear Array and Next-Generation Sequencing in cervical samples from Western Mexico. Virology Journal 12, 161 Google Scholar
185. Fonseca, D.J. et al. (2015) Next generation sequencing in women affected by nonsyndromic premature ovarian failure displays new potential causative genes and mutations. Fertility and Sterility 104, 154-162 Google Scholar
186. Liu, L. et al. (2012) Comparison of next-generation sequencing systems. Journal of Biomedicine and Biotechnology 2012, 251364 Google Scholar
187. Bahassi, E.M. and Stambrook, P.J. (2014) Next-generation sequencing technologies: breaking the sound barrier of human genetics. Mutagenesis 29, 303-310 Google Scholar
188. Buermans, H.P. and den Dunnen, J.T. (2014) Next generation sequencing technology: advances and applications. Biochimica et Biophysica Acta 1842, 1932-1941 Google Scholar
189. van Dijk, E.L. et al. (2014) Ten years of next-generation sequencing technology. Trends Genetics 30, 418-426 Google Scholar
190. Goodwin, S., McPherson, J.D. and McCombie, W.R. (2016) Coming of age: ten years of next-generation sequencing technologies. Nature Review Genetics 17, 333-351 Google Scholar
191. Mardis, E.R. (2008) The impact of next-generation sequencing technology on genetics. Trends in Genetics 24, 33-141 Google Scholar