{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,24]],"date-time":"2026-09-24T23:03:39Z","timestamp":1790291019314,"version":"4.1.0"},"reference-count":74,"publisher":"MDPI AG","issue":"10","license":[{"start":{"date-parts":[[2021,9,28]],"date-time":"2021-09-28T00:00:00Z","timestamp":1632787200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"National Institutes of Health","award":["HHSN261200800001E"],"award-info":[{"award-number":["HHSN261200800001E"]}]},{"name":"National Cancer Institute","award":["CA78527"],"award-info":[{"award-number":["CA78527"]}]},{"name":"Einstein Cancer Research Center","award":["P30CA013330"],"award-info":[{"award-number":["P30CA013330"]}]},{"DOI":"10.13039\/501100006364","name":"Institut National du Cancer","doi-asserted-by":"publisher","award":["SHSESP 16-006"],"award-info":[{"award-number":["SHSESP 16-006"]}],"id":[{"id":"10.13039\/501100006364","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Viruses"],"abstract":"<jats:p>Human papillomavirus (HPV) type 31 (HPV31) is closely related to the most carcinogenic type, HPV16, but only accounts for 4% of cervical cancer cases worldwide. Viral genetic and epigenetic variations have been associated with carcinogenesis for other high-risk HPV types, but little is known about HPV31. We sequenced 2093 HPV31 viral whole genomes from two large studies, one from the U.S. and one international. In addition, we investigated CpG methylation in a subset of 175 samples. We evaluated the association of HPV31 lineages\/sublineages, single nucleotide polymorphisms (SNPs) and viral methylation with cervical carcinogenesis. HPV31 A\/B clade was &gt;1.8-fold more associated with cervical intraepithelial neoplasia grade 3 and cancer (CIN3+) compared to the most common C lineage. Lineage\/sublineage distribution varied by race\/ethnicity and geographic region. A viral genome-wide association analysis identified SNPs within the A\/B clade associated with CIN3+, including H23Y (C626T) (odds ratio = 1.60, confidence intervals = 1.17\u20132.19) located in the pRb CR2 binding-site within the E7 oncogene. Viral CpG methylation was higher in lineage B, compared to the other lineages, and was most elevated in CIN3+. In conclusion, these data support the increased oncogenicity of the A\/B lineages and suggest variation of E7 as a contributing risk factor.<\/jats:p>","DOI":"10.3390\/v13101948","type":"journal-article","created":{"date-parts":[[2021,9,28]],"date-time":"2021-09-28T21:39:29Z","timestamp":1632865169000},"page":"1948","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":22,"title":["Phylogenomic Analysis of Human Papillomavirus Type 31 and Cervical Carcinogenesis: A Study of 2093 Viral Genomes"],"prefix":"10.3390","volume":"13","author":[{"given":"Maisa","family":"Pinheiro","sequence":"first","affiliation":[{"name":"Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Rockville, MD 20850, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ariana","family":"Harari","sequence":"additional","affiliation":[{"name":"Departments of Pediatrics and Microbiology & Immunology, Albert Einstein College of Medicine, Bronx, NY 10461, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mark","family":"Schiffman","sequence":"additional","affiliation":[{"name":"Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Rockville, MD 20850, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7534-333X","authenticated-orcid":false,"given":"Gary M.","family":"Clifford","sequence":"additional","affiliation":[{"name":"Early Detection, Prevention and Infections Branch, International Agency for Research on Cancer (IARC\/WHO), 150 cours Albert Thomas, CEDEX 08, 69372 Lyon, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8577-1298","authenticated-orcid":false,"given":"Zigui","family":"Chen","sequence":"additional","affiliation":[{"name":"Department of Microbiology, The Chinese University of Hong 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F.","family":"Boland","sequence":"additional","affiliation":[{"name":"Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Rockville, MD 20850, USA"},{"name":"Cancer Genomics Research Laboratory, Leidos Biomedical Research, Inc., Frederick, MD 21701, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tina","family":"Raine-Bennett","sequence":"additional","affiliation":[{"name":"Division of Research, Kaiser Permanente Northern California, Oakland, CA 94612, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mia","family":"Steinberg","sequence":"additional","affiliation":[{"name":"Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Rockville, MD 20850, USA"},{"name":"Cancer Genomics Research Laboratory, Leidos Biomedical Research, Inc., Frederick, MD 21701, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sara","family":"Bass","sequence":"additional","affiliation":[{"name":"Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Rockville, MD 20850, USA"},{"name":"Cancer Genomics Research Laboratory, Leidos Biomedical Research, Inc., Frederick, MD 21701, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yanzi","family":"Xiao","sequence":"additional","affiliation":[{"name":"Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Rockville, MD 20850, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vanessa","family":"Tenet","sequence":"additional","affiliation":[{"name":"Early Detection, Prevention and Infections Branch, International Agency for Research on Cancer (IARC\/WHO), 150 cours Albert Thomas, CEDEX 08, 69372 Lyon, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kai","family":"Yu","sequence":"additional","affiliation":[{"name":"Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Rockville, MD 20850, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bin","family":"Zhu","sequence":"additional","affiliation":[{"name":"Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Rockville, MD 20850, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Laurie","family":"Burdett","sequence":"additional","affiliation":[{"name":"Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Rockville, MD 20850, USA"},{"name":"Cancer Genomics Research Laboratory, Leidos Biomedical Research, Inc., Frederick, MD 21701, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sevilay","family":"Turan","sequence":"additional","affiliation":[{"name":"Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Rockville, MD 20850, USA"},{"name":"Cancer Genomics Research Laboratory, Leidos Biomedical Research, Inc., Frederick, MD 21701, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Thomas","family":"Lorey","sequence":"additional","affiliation":[{"name":"Regional Laboratory, Kaiser Permanente Northern California, Oakland, CA 94710, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Philip E.","family":"Castle","sequence":"additional","affiliation":[{"name":"Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Rockville, MD 20850, USA"},{"name":"Division of Cancer Prevention, National Cancer Institute, National Institutes of Health, Rockville, MD 20850, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nicolas","family":"Wentzensen","sequence":"additional","affiliation":[{"name":"Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Rockville, MD 20850, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8376-8458","authenticated-orcid":false,"given":"Robert D.","family":"Burk","sequence":"additional","affiliation":[{"name":"Departments of Pediatrics and Microbiology & Immunology, Albert Einstein College of Medicine, Bronx, NY 10461, USA"},{"name":"Department of Epidemiology & Population Health, and Obstetrics, Gynecology and Women\u2019s Health, Albert Einstein College of Medicine, Bronx, NY 10461, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lisa","family":"Mirabello","sequence":"additional","affiliation":[{"name":"Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Rockville, MD 20850, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,9,28]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"394","DOI":"10.3322\/caac.21492","article-title":"Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries","volume":"68","author":"Bray","year":"2018","journal-title":"CA Cancer J. Clin."},{"key":"ref_2","unstructured":"IARC Working Group (2005). IARC Handbooks of Cancer Prevention: Cervix Cancer Screening, IARC Press."},{"key":"ref_3","unstructured":"WHO (2014). Human papillomavirus vaccines: WHO position paper, October 2014. Wkly. Epidemiol. Rec., 89, 465\u2013491."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"70","DOI":"10.1016\/j.virol.2010.02.002","article-title":"Classification of papillomaviruses (PVs) based on 189 PV types and proposal of taxonomic amendments","volume":"401","author":"Bernard","year":"2010","journal-title":"Virology"},{"key":"ref_5","unstructured":"(2021, January 08). PapillomaVirus Episteme (PaVe), Available online: https:\/\/pave.niaid.nih.gov\/#home."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1048","DOI":"10.1016\/S1470-2045(10)70230-8","article-title":"Human papillomavirus genotype attribution in invasive cervical cancer: A retrospective cross-sectional worldwide study","volume":"11","author":"Quint","year":"2010","journal-title":"Lancet Oncol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"76","DOI":"10.1016\/j.virol.2005.04.002","article-title":"The carcinogenicity of human papillomavirus types reflects viral evolution","volume":"337","author":"Schiffman","year":"2005","journal-title":"Virology"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"321","DOI":"10.1016\/S1470-2045(09)70096-8","article-title":"A review of human carcinogens--Part B: Biological agents","volume":"10","author":"Bouvard","year":"2009","journal-title":"Lancet Oncol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"306","DOI":"10.1016\/0042-6822(89)90545-X","article-title":"Nucleotide sequence of human papillomavirus type 31: A cervical neoplasia-associated virus","volume":"171","author":"Goldsborough","year":"1989","journal-title":"Virology"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"431","DOI":"10.1002\/path.4424","article-title":"Are 20 human papillomavirus types causing cervical cancer?","volume":"234","author":"Arbyn","year":"2014","journal-title":"J. Pathol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"621","DOI":"10.1002\/ijc.22527","article-title":"Human papillomavirus type distribution in invasive cervical cancer and high-grade cervical lesions: A meta-analysis update","volume":"121","author":"Smith","year":"2007","journal-title":"Int. J. Cancer"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"2349","DOI":"10.1002\/ijc.27485","article-title":"Human papillomavirus types in 115,789 HPV-positive women: A meta-analysis from cervical infection to cancer","volume":"131","author":"Guan","year":"2012","journal-title":"Int. J. Cancer"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"513","DOI":"10.1093\/jnci\/djn044","article-title":"Rapid clearance of human papillomavirus and implications for clinical focus on persistent infections","volume":"100","author":"Rodriguez","year":"2008","journal-title":"J. Natl. Cancer Inst."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"486","DOI":"10.1093\/aje\/kwg171","article-title":"Determinants of clearance of human papillomavirus infections in Colombian women with normal cytology: A population-based, 5-year follow-up study","volume":"158","author":"Molano","year":"2003","journal-title":"Am. J. Epidemiol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"423","DOI":"10.1056\/NEJM199802123380703","article-title":"Natural history of cervicovaginal papillomavirus infection in young women","volume":"338","author":"Ho","year":"1998","journal-title":"N. Engl. J. Med."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"890","DOI":"10.1016\/S0140-6736(07)61416-0","article-title":"Human papillomavirus and cervical cancer","volume":"370","author":"Schiffman","year":"2007","journal-title":"Lancet"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"368","DOI":"10.1093\/jnci\/djq562","article-title":"Human papillomavirus testing in the prevention of cervical cancer","volume":"103","author":"Schiffman","year":"2011","journal-title":"J. Natl. Cancer Inst."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"2194","DOI":"10.1158\/1078-0432.CCR-17-3251","article-title":"Human Papillomavirus DNA Methylation as a Biomarker for Cervical Precancer: Consistency across 12 Genotypes and Potential Impact on Management of HPV-Positive Women","volume":"24","author":"Clarke","year":"2018","journal-title":"Clin. Cancer Res."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"3159","DOI":"10.1158\/0008-5472.CAN-09-4179","article-title":"A population-based prospective study of carcinogenic human papillomavirus variant lineages, viral persistence, and cervical neoplasia","volume":"70","author":"Schiffman","year":"2010","journal-title":"Cancer Res."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"232","DOI":"10.1016\/j.virol.2013.07.018","article-title":"Human papillomavirus genome variants","volume":"445","author":"Burk","year":"2013","journal-title":"Virology"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"djw100","DOI":"10.1093\/jnci\/djw100","article-title":"HPV16 Sublineage Associations with Histology-Specific Cancer Risk Using HPV Whole-Genome Sequences in 3200 Women","volume":"108","author":"Mirabello","year":"2016","journal-title":"J. Natl. Cancer Inst."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1098","DOI":"10.1002\/ijc.30164","article-title":"Variant-specific persistence of infections with human papillomavirus Types 31, 33, 45, 56 and 58 and risk of cervical intraepithelial neoplasia","volume":"139","author":"Xi","year":"2016","journal-title":"Int. J. Cancer"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"dju270","DOI":"10.1093\/jnci\/dju270","article-title":"Lineages of oncogenic human papillomavirus types other than type 16 and 18 and risk for cervical intraepithelial neoplasia","volume":"106","author":"Xi","year":"2014","journal-title":"J. Natl. Cancer Inst."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1164","DOI":"10.1016\/j.cell.2017.08.001","article-title":"HPV16 E7 Genetic Conservation Is Critical to Carcinogenesis","volume":"170","author":"Mirabello","year":"2017","journal-title":"Cell"},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Chen, Z., Schiffman, M., Herrero, R., Desalle, R., Anastos, K., Segondy, M., Sahasrabuddhe, V.V., Gravitt, P.E., Hsing, A.W., and Burk, R.D. (2011). Evolution and taxonomic classification of human papillomavirus 16 (HPV16)-related variant genomes: HPV31, HPV33, HPV35, HPV52, HPV58 and HPV67. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0020183"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1412","DOI":"10.1002\/ijc.27750","article-title":"Elevated methylation of HPV16 DNA is associated with the development of high grade cervical intraepithelial neoplasia","volume":"132","author":"Mirabello","year":"2013","journal-title":"Int. J. Cancer"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"314","DOI":"10.1016\/j.virol.2013.10.032","article-title":"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","volume":"448","author":"Kalantari","year":"2014","journal-title":"Virology"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"2745","DOI":"10.1002\/ijc.30008","article-title":"Validation of a DNA methylation HPV triage classifier in a screening sample","volume":"138","author":"Lorincz","year":"2016","journal-title":"Int. J. Cancer"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"2582","DOI":"10.1093\/cid\/ciz677","article-title":"Methylation in predicting progression of untreated high-grade cervical intraepithelial neoplasia","volume":"70","author":"Louvanto","year":"2019","journal-title":"Clin. Infect. Dis"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1738","DOI":"10.1093\/jnci\/djs425","article-title":"Methylation of HPV18, HPV31, and HPV45 genomes and cervical intraepithelial neoplasia grade 3","volume":"104","author":"Wentzensen","year":"2012","journal-title":"J. Natl. Cancer Inst."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1425","DOI":"10.1002\/ijc.28790","article-title":"A DNA methylation classifier of cervical precancer based on human papillomavirus and human genes","volume":"135","author":"Brentnall","year":"2014","journal-title":"Int. J. Cancer"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1016\/j.jcv.2013.12.014","article-title":"A comparison of methylation levels in HPV18, HPV31 and HPV33 genomes reveals similar associations with cervical precancers","volume":"59","author":"Vasiljevic","year":"2014","journal-title":"J. Clin. Virol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"946","DOI":"10.1158\/1055-9965.EPI-10-1267","article-title":"Human papillomavirus (HPV) genotypes in women with cervical precancer and cancer at Kaiser Permanente Northern California","volume":"20","author":"Castle","year":"2011","journal-title":"Cancer Epidemiol. Biomark. Prev."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"298","DOI":"10.1016\/j.jviromet.2008.05.017","article-title":"Impact of 6-month frozen storage of cervical specimens in alkaline buffer conditions on human papillomavirus genotyping","volume":"151","author":"LaMere","year":"2008","journal-title":"J. Virol. Methods"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"80","DOI":"10.1016\/j.jviromet.2007.06.001","article-title":"Human papillomavirus genotyping after denaturation of specimens for Hybrid Capture 2 testing: Feasibility study for the HPV persistence and progression cohort","volume":"146","author":"LaMere","year":"2007","journal-title":"J. Virol. Methods"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"796","DOI":"10.1093\/jnci\/87.11.796","article-title":"Prevalence of human papillomavirus in cervical cancer: A worldwide perspective. International biological study on cervical cancer (IBSCC) Study Group","volume":"87","author":"Bosch","year":"1995","journal-title":"J. Natl. Cancer Inst."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"991","DOI":"10.1016\/S0140-6736(05)67069-9","article-title":"Worldwide distribution of human papillomavirus types in cytologically normal women in the International Agency for Research on Cancer HPV prevalence surveys: A pooled analysis","volume":"366","author":"Clifford","year":"2005","journal-title":"Lancet"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"889","DOI":"10.1016\/S0140-6736(13)60022-7","article-title":"Human papillomavirus and cervical cancer","volume":"382","author":"Crosbie","year":"2013","journal-title":"Lancet"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"518","DOI":"10.1056\/NEJMoa021641","article-title":"Epidemiologic classification of human papillomavirus types associated with cervical cancer","volume":"348","author":"Bosch","year":"2003","journal-title":"N. Engl. J. Med."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"221","DOI":"10.1002\/1097-0215(20000715)87:2<221::AID-IJC11>3.0.CO;2-2","article-title":"Distribution of 37 mucosotropic HPV types in women with cytologically normal cervical smears: The age-related patterns for high-risk and low-risk types","volume":"87","author":"Jacobs","year":"2000","journal-title":"Int. J. Cancer"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"679","DOI":"10.1093\/infdis\/174.4.679","article-title":"Sexual behavior and partner characteristics are the predominant risk factors for genital human papillomavirus infection in young women","volume":"174","author":"Burk","year":"1996","journal-title":"J. Infect. Dis."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"6855","DOI":"10.1128\/JVI.00483-12","article-title":"Human papillomavirus type 16 genetic variants: Phylogeny and classification based on E6 and LCR","volume":"86","author":"Cornet","year":"2012","journal-title":"J. Virol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1016\/j.pvr.2015.05.004","article-title":"Deep sequencing of HPV16 genomes: A new high-throughput tool for exploring the carcinogenicity and natural history of HPV16 infection","volume":"1","author":"Cullen","year":"2015","journal-title":"Papillomavirus Res."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"80","DOI":"10.4161\/fly.19695","article-title":"A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3","volume":"6","author":"Cingolani","year":"2012","journal-title":"Fly"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"2520","DOI":"10.1093\/bioinformatics\/bts480","article-title":"Snakemake\u2014A scalable bioinformatics workflow engine","volume":"28","author":"Koster","year":"2012","journal-title":"Bioinformatics"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1038\/nmeth.1184","article-title":"Error-correcting barcoded primers for pyrosequencing hundreds of samples in multiplex","volume":"5","author":"Hamady","year":"2008","journal-title":"Nat. Methods"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"R25","DOI":"10.1186\/gb-2009-10-3-r25","article-title":"Ultrafast and memory-efficient alignment of short DNA sequences to the human genome","volume":"10","author":"Langmead","year":"2009","journal-title":"Genome Biol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"1571","DOI":"10.1093\/bioinformatics\/btr167","article-title":"Bismark: A flexible aligner and methylation caller for Bisulfite-Seq applications","volume":"27","author":"Krueger","year":"2011","journal-title":"Bioinformatics"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"2688","DOI":"10.1093\/bioinformatics\/btl446","article-title":"RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models","volume":"22","author":"Stamatakis","year":"2006","journal-title":"Bioinformatics"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1870","DOI":"10.1093\/molbev\/msw054","article-title":"MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets","volume":"33","author":"Kumar","year":"2016","journal-title":"Mol. Biol. Evol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"W256","DOI":"10.1093\/nar\/gkz239","article-title":"Interactive Tree Of Life (iTOL) v4: Recent updates and new developments","volume":"47","author":"Letunic","year":"2019","journal-title":"Nucleic Acids Res."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1038\/nbt.1754","article-title":"Integrative genomics viewer","volume":"29","author":"Robinson","year":"2011","journal-title":"Nat. Biotechnol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.meegid.2014.11.026","article-title":"Within-host nucleotide diversity of virus populations: Insights from next-generation sequencing","volume":"30","author":"Nelson","year":"2015","journal-title":"Infect. Genet. Evol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1038\/nrm3043","article-title":"Dedifferentiation, transdifferentiation and reprogramming: Three routes to regeneration","volume":"12","author":"Jopling","year":"2011","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"16086","DOI":"10.1038\/nrdp.2016.86","article-title":"Carcinogenic human papillomavirus infection","volume":"2","author":"Schiffman","year":"2016","journal-title":"Nat. Rev. Dis. Primers"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"e01285-17","DOI":"10.1128\/JVI.01285-17","article-title":"Ancient Evolution and Dispersion of Human Papillomavirus 58 Variants","volume":"91","author":"Chen","year":"2017","journal-title":"J. Virol."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1093\/molbev\/msw214","article-title":"Transmission between Archaic and Modern Human Ancestors during the Evolution of the Oncogenic Human Papillomavirus 16","volume":"34","author":"Pimenoff","year":"2017","journal-title":"Mol. Biol. Evol."},{"key":"ref_58","doi-asserted-by":"crossref","unstructured":"Chen, Z., DeSalle, R., Schiffman, M., Herrero, R., Wood, C.E., Ruiz, J.C., Clifford, G.M., Chan, P.K.S., and Burk, R.D. (2018). Niche adaptation and viral transmission of human papillomaviruses from archaic hominins to modern humans. PLoS Pathog., 14.","DOI":"10.1371\/journal.ppat.1007352"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"6339","DOI":"10.1128\/JVI.00233-07","article-title":"Characterization and experimental transmission of an oncogenic papillomavirus in female macaques","volume":"81","author":"Wood","year":"2007","journal-title":"J. Virol."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"3532","DOI":"10.1158\/0008-5472.CAN-07-6471","article-title":"Comprehensive analysis of HLA-A, HLA-B, HLA-C, HLA-DRB1, and HLA-DQB1 loci and squamous cell cervical cancer risk","volume":"68","author":"Madeleine","year":"2008","journal-title":"Cancer Res."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"E146","DOI":"10.1002\/ijc.29119","article-title":"HPV16 methyl-haplotypes determined by a novel next-generation sequencing method are associated with cervical precancer","volume":"136","author":"Mirabello","year":"2015","journal-title":"Int. J. Cancer"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"435","DOI":"10.1016\/j.arcmed.2009.06.002","article-title":"Host factors in HPV-related carcinogenesis: Cellular mechanisms controlling HPV infections","volume":"40","author":"Doeberitz","year":"2009","journal-title":"Arch. Med. Res."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1158\/1055-9965.EPI-06-0670","article-title":"Risk for high-grade cervical intraepithelial neoplasia associated with variants of human papillomavirus types 16 and 18","volume":"16","author":"Xi","year":"2007","journal-title":"Cancer Epidemiol. Biomark. Prev."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"2677","DOI":"10.1002\/ijc.33033","article-title":"Association of HPV35 with cervical carcinogenesis among women of African ancestry: Evidence of viral-host interaction with implications for disease intervention","volume":"147","author":"Pinheiro","year":"2020","journal-title":"Int. J. Cancer"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"138","DOI":"10.1016\/j.virol.2013.04.013","article-title":"The papillomavirus E7 proteins","volume":"445","author":"Roman","year":"2013","journal-title":"Virology"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"908","DOI":"10.1016\/S0021-9258(18)48370-6","article-title":"Specific N-methylations of HPV-16 E7 peptides alter binding to the retinoblastoma suppressor protein","volume":"267","author":"Jones","year":"1992","journal-title":"J. Biol. Chem."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"238","DOI":"10.1006\/viro.1997.8885","article-title":"The relative ability of human papillomavirus type 6 and human papillomavirus type 16 E7 proteins to transactivate E2F-responsive elements is promoter- and cell-dependent","volume":"239","author":"Armstrong","year":"1997","journal-title":"Virology"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"11197","DOI":"10.1093\/nar\/gkz961","article-title":"RB, p130 and p107 differentially repress G1\/S and G2\/M genes after p53 activation","volume":"47","author":"Schade","year":"2019","journal-title":"Nucleic Acids Res."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"572","DOI":"10.1136\/bmj.325.7364.572","article-title":"Type specific persistence of high risk human papillomavirus (HPV) as indicator of high grade cervical squamous intraepithelial lesions in young women: Population based prospective follow up study","volume":"325","author":"Kjaer","year":"2002","journal-title":"BMJ"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"182","DOI":"10.1086\/426867","article-title":"A longitudinal study of genital human papillomavirus infection in a cohort of closely followed adolescent women","volume":"191","author":"Brown","year":"2005","journal-title":"J. Infect. Dis."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1016\/j.virol.2013.07.020","article-title":"The E1 proteins","volume":"445","author":"Bergvall","year":"2013","journal-title":"Virology"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"681","DOI":"10.1038\/nrmicro2872","article-title":"Understanding and learning from the success of prophylactic human papillomavirus vaccines","volume":"10","author":"Schiller","year":"2012","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1016\/j.virol.2013.05.038","article-title":"The papillomavirus major capsid protein L1","volume":"445","author":"Buck","year":"2013","journal-title":"Virology"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"886","DOI":"10.1038\/s41467-020-14730-1","article-title":"Mutations in the HPV16 genome induced by APOBEC3 are associated with viral clearance","volume":"11","author":"Zhu","year":"2020","journal-title":"Nat. Commun."}],"container-title":["Viruses"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1999-4915\/13\/10\/1948\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T07:06:37Z","timestamp":1760166397000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1999-4915\/13\/10\/1948"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,9,28]]},"references-count":74,"journal-issue":{"issue":"10","published-online":{"date-parts":[[2021,10]]}},"alternative-id":["v13101948"],"URL":"https:\/\/doi.org\/10.3390\/v13101948","relation":{},"ISSN":["1999-4915"],"issn-type":[{"value":"1999-4915","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,9,28]]}}}