1887

Abstract

Human papillomavirus type 16 (HPV16) non-European variants have been associated with persistent infection and cervical cancer development, while the L83V variant of the E6 gene has been correlated with the progression of cervical malignancy. The present study investigated the presence of the HPV16 L83V variant in Greek women. Molecular evolutionary analysis of the HPV16 E6 and E7 oncogenes was conducted in order to estimate the evolution of the HPV16 genome in the Greek population. The E6 L83V variant was found in 78.2 % of high- and 64.28 % of low-grade specimens. Moreover, the prototype and E6 L83V variants were both prevalent in high- and low-grade malignancies in Greek women. Selective pressure analysis of the individual amino acid residues of HPV16 sequences from the Greek population indicates that codon 83 of the E6 protein, as well as codon 85 of the E7 protein, are undergoing positive selection. Novel sequence variations were recorded within the E6 and E7 genes in cervical samples, characterized as (T350G) European variants. However, no signal of intratypic recombination event was identified within the E6–E7 region. Molecular and evolutionary analyses of HPV16 genomes from distinct geographical locations might provide valuable information about viral evolution and oncogenecity.

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2013-11-01
2019-12-15
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References

  1. Andersson S., Alemi M., Rylander E., Strand A., Larsson B., Sällström J., Wilander E.. ( 2000;). Uneven distribution of HPV 16 E6 prototype and variant (L83V) oncoprotein in cervical neoplastic lesions. . Br J Cancer 83:, 307–310. [CrossRef][PubMed]
    [Google Scholar]
  2. Angulo M., Carvajal-Rodríguez A.. ( 2007;). Evidence of recombination within human alpha-papillomavirus. . Virol J 4:, 33. [CrossRef][PubMed]
    [Google Scholar]
  3. Bernard H. U., Calleja-Macias I. E., Dunn S. T.. ( 2006;). Genome variation of human papillomavirus types: phylogenetic and medical implications. . Int J Cancer 118:, 1071–1076. [CrossRef][PubMed]
    [Google Scholar]
  4. Bernard H. U., Burk R. D., Chen Z., van Doorslaer K., zur Hausen H., de Villiers E. M.. ( 2010;). Classification of papillomaviruses (PVs) based on 189 PV types and proposal of taxonomic amendments. . Virology 401:, 70–79. [CrossRef][PubMed]
    [Google Scholar]
  5. Boulet G., Horvath C., Vanden Broeck D., Sahebali S., Bogers J.. ( 2007;). Human papillomavirus: E6 and E7 oncogenes. . Int J Biochem Cell Biol 39:, 2006–2011. [CrossRef][PubMed]
    [Google Scholar]
  6. Carvajal-Rodríguez A.. ( 2008;). Detecting recombination and diversifying selection in human alpha-papillomavirus. . Infect Genet Evol 8:, 689–692. [CrossRef][PubMed]
    [Google Scholar]
  7. Casas I., Powell L., Klapper P. E., Cleator G. M.. ( 1995;). New method for the extraction of viral RNA and DNA from cerebrospinal fluid for use in the polymerase chain reaction assay. . J Virol Methods 53:, 25–36. [CrossRef][PubMed]
    [Google Scholar]
  8. Chan S. Y., Bernard H. U., Ratterree M., Birkebak T. A., Faras A. J., Ostrow R. S.. ( 1997;). Genomic diversity and evolution of papillomaviruses in rhesus monkeys. . J Virol 71:, 4938–4943.[PubMed]
    [Google Scholar]
  9. Chen Z., Terai M., Fu L., Herrero R., DeSalle R., Burk R. D.. ( 2005;). Diversifying selection in human papillomavirus type 16 lineages based on complete genome analyses. . J Virol 79:, 7014–7023. [CrossRef][PubMed]
    [Google Scholar]
  10. Chen Z., DeSalle R., Schiffman M., Herrero R., Burk R. D.. ( 2009;). Evolutionary dynamics of variant genomes of human papillomavirus types 18, 45, and 97. . J Virol 83:, 1443–1455. [CrossRef][PubMed]
    [Google Scholar]
  11. Cornet I., Gheit T., Franceschi S., Vignat J., Burk R. D., Sylla B. S., Tommasino M., Clifford G. M..IARC HPV Variant Study Group ( 2012;). Human papillomavirus type 16 genetic variants: phylogeny and classification based on E6 and LCR. . J Virol 86:, 6855–6861. [CrossRef][PubMed]
    [Google Scholar]
  12. de Boer M. A., Peters L. A., Aziz M. F., Siregar B., Cornain S., Vrede M. A., Jordanova E. S., Kolkman-Uljee S., Fleuren G. J.. ( 2004;). Human papillomavirus type 16 E6, E7, and L1 variants in cervical cancer in Indonesia, Suriname, and The Netherlands. . Gynecol Oncol 94:, 488–494. [CrossRef][PubMed]
    [Google Scholar]
  13. de Sanjose S., Quint W. G., Alemany L., Geraets D. T., Klaustermeier J. E., Lloveras B., Tous S., Felix A., Bravo L. E.. & other authors ( 2010;). Human papillomavirus genotype attribution in invasive cervical cancer: a retrospective cross-sectional worldwide study. . Lancet Oncol 11:, 1048–1056. [CrossRef][PubMed]
    [Google Scholar]
  14. DeFilippis V. R., Ayala F. J., Villarreal L. P.. ( 2002;). Evidence of diversifying selection in human papillomavirus type 16 E6 but not E7 oncogenes. . J Mol Evol 55:, 491–499. [CrossRef][PubMed]
    [Google Scholar]
  15. Drummond A. J., Rambaut A.. ( 2007;). beast: Bayesian evolutionary analysis by sampling trees. . BMC Evol Biol 7:, 214. [CrossRef][PubMed]
    [Google Scholar]
  16. Edgar R. C.. ( 2004;). muscle: multiple sequence alignment with high accuracy and high throughput. . Nucleic Acids Res 32:, 1792–1797. [CrossRef][PubMed]
    [Google Scholar]
  17. Eriksson A., Herron J. R., Yamada T., Wheeler C. M.. ( 1999;). Human papillomavirus type 16 variant lineages characterized by nucleotide sequence analysis of the E5 coding segment and the E2 hinge region. . J Gen Virol 80:, 595–600.[PubMed]
    [Google Scholar]
  18. Ghittoni R., Accardi R., Hasan U., Gheit T., Sylla B., Tommasino M.. ( 2010;). The biological properties of E6 and E7 oncoproteins from human papillomaviruses. . Virus Genes 40:, 1–13. [CrossRef][PubMed]
    [Google Scholar]
  19. Grodzki M., Besson G., Clavel C., Arslan A., Franceschi S., Birembaut P., Tommasino M., Zehbe I.. ( 2006;). Increased risk for cervical disease progression of French women infected with the human papillomavirus type 16 E6-350G variant. . Cancer Epidemiol Biomarkers Prev 15:, 820–822. [CrossRef][PubMed]
    [Google Scholar]
  20. Halpern A. L.. ( 2000;). Comparison of papillomavirus and immunodeficiency virus evolutionary patterns in the context of a papillomavirus vaccine. . J Clin Virol 19:, 43–56. [CrossRef][PubMed]
    [Google Scholar]
  21. Junes-Gill K., Sichero L., Maciag P. C., Mello W., Noronha V., Villa L. L.. ( 2008;). Human papillomavirus type 16 variants in cervical cancer from an admixtured population in Brazil. . J Med Virol 80:, 1639–1645. [CrossRef][PubMed]
    [Google Scholar]
  22. Kosakovsky Pond S. L., Frost S. D.. ( 2005;). Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. . Bioinformatics 21:, 2531–2533. [CrossRef][PubMed]
    [Google Scholar]
  23. Kosakovsky Pond S. L., Posada D., Gravenor M. B., Woelk C. H., Frost S. D.. ( 2006;). Automated phylogenetic detection of recombination using a genetic algorithm. . Mol Biol Evol 23:, 1891–1901. [CrossRef][PubMed]
    [Google Scholar]
  24. Lee K., Magalhaes I., Clavel C., Briolat J., Birembaut P., Tommasino M., Zehbe I.. ( 2008;). Human papillomavirus 16 E6, L1, L2 and E2 gene variants in cervical lesion progression. . Virus Res 131:, 106–110. [CrossRef][PubMed]
    [Google Scholar]
  25. Li W., Wang W., Si M., Han L., Gao Q., Luo A., Li Y., Lu Y., Wang S., Ma D.. ( 2008;). The physical state of HPV16 infection and its clinical significance in cancer precursor lesion and cervical carcinoma. . J Cancer Res Clin Oncol 134:, 1355–1361. [CrossRef][PubMed]
    [Google Scholar]
  26. Li N., Franceschi S., Howell-Jones R., Snijders P. J. F., Clifford G. M.. ( 2011;). Human papillomavirus type distribution in 30,848 invasive cervical cancers worldwide: variation by geographical region, histological type and year of publication. . Int J Cancer 128:, 927–935. [CrossRef][PubMed]
    [Google Scholar]
  27. Münger K., Baldwin A., Edwards K. M., Hayakawa H., Nguyen C. L., Owens M., Grace M., Huh K.. ( 2004;). Mechanisms of human papillomavirus-induced oncogenesis. . J Virol 78:, 11451–11460. [CrossRef][PubMed]
    [Google Scholar]
  28. Muñoz N.. ( 2000;). Human papillomavirus and cancer: the epidemiological evidence. . J Clin Virol 19:, 1–5. [CrossRef][PubMed]
    [Google Scholar]
  29. Pande S., Jain N., Prusty B. K., Bhambhani S., Gupta S., Sharma R., Batra S., Das B. C.. ( 2008;). Human papillomavirus type 16 variant analysis of E6, E7, and L1 genes and long control region in biopsy samples from cervical cancer patients in north India. . J Clin Microbiol 46:, 1060–1066. [CrossRef][PubMed]
    [Google Scholar]
  30. Puranen M., Saarikoski S., Syrjänen K., Syrjänen S.. ( 1996;). Polymerase chain reaction amplification of human papillomavirus DNA from archival, Papanicolaou-stained cervical smears. . Acta Cytol 40:, 391–395. [CrossRef][PubMed]
    [Google Scholar]
  31. Quint K. D., de Koning M. N., van Doorn L. J., Quint W. G., Pirog E. C.. ( 2010;). HPV genotyping and HPV16 variant analysis in glandular and squamous neoplastic lesions of the uterine cervix. . Gynecol Oncol 117:, 297–301. [CrossRef][PubMed]
    [Google Scholar]
  32. Sanchez G. I., Kleter B., Gheit T., van Doorn L. J., de Koning M. N., de Sanjosé S., Alemany L., Bosch X. F., Tommasino M.. & other authors ( 2011;). Clinical evaluation of polymerase chain reaction reverse hybridization assay for detection and identification of human papillomavirus type 16 variants. . J Clin Virol 51:, 165–169. [CrossRef][PubMed]
    [Google Scholar]
  33. Schiffman M., Rodriguez A. C., Chen Z., Wacholder S., Herrero R., Hildesheim A., Desalle R., Befano B., Yu K.. & other authors ( 2010;). A population-based prospective study of carcinogenic human papillomavirus variant lineages, viral persistence, and cervical neoplasia. . Cancer Res 70:, 3159–3169. [CrossRef][PubMed]
    [Google Scholar]
  34. Sotlar K., Diemer D., Dethleffs A., Hack Y., Stubner A., Vollmer N., Menton S., Menton M., Dietz K.. & other authors ( 2004;). Detection and typing of human papillomavirus by e6 nested multiplex PCR. . J Clin Microbiol 42:, 3176–3184. [CrossRef][PubMed]
    [Google Scholar]
  35. Stern A., Doron-Faigenboim A., Erez E., Martz E., Bacharach E., Pupko T.. ( 2007;). Selecton 2007: advanced models for detecting positive and purifying selection using a Bayesian inference approach. . Nucleic Acids Res 35: (Web Server issue), W506–W511. [CrossRef][PubMed]
    [Google Scholar]
  36. Sun M., Gao L., Liu Y., Zhao Y., Wang X., Pan Y., Ning T., Cai H., Yang H.. & other authors ( 2012;). Whole genome sequencing and evolutionary analysis of human papillomavirus type 16 in central China. . PLoS ONE 7:, e36577. [CrossRef][PubMed]
    [Google Scholar]
  37. Suzuki Y., Gojobori T.. ( 1999;). A method for detecting positive selection at single amino acid sites. . Mol Biol Evol 16:, 1315–1328. [CrossRef][PubMed]
    [Google Scholar]
  38. Swan D. C., Rajeevan M., Tortolero-Luna G., Follen M., Tucker R. A., Unger E. R.. ( 2005;). Human papillomavirus type 16 E2 and E6/E7 variants. . Gynecol Oncol 96:, 695–700. [CrossRef][PubMed]
    [Google Scholar]
  39. Tamura K., Dudley J., Nei M., Kumar S.. ( 2007;). mega4: Molecular Evolutionary Genetics Analysis (mega) software version 4.0. . Mol Biol Evol 24:, 1596–1599. [CrossRef][PubMed]
    [Google Scholar]
  40. Tornesello M. L., Losito S., Benincasa G., Fulciniti F., Botti G., Greggi S., Buonaguro L., Buonaguro F. M.. ( 2011;). Human papillomavirus (HPV) genotypes and HPV16 variants and risk of adenocarcinoma and squamous cell carcinoma of the cervix. . Gynecol Oncol 121:, 32–42. [CrossRef][PubMed]
    [Google Scholar]
  41. Tsakogiannis D., Ruether I. G., Kyriakopoulou Z., Pliaka V., Skordas V., Gartzonika C., Levidiotou-Stefanou S., Markoulatos P.. ( 2012;). Molecular and phylogenetic analysis of the HPV 16 E4 gene in cervical lesions from women in Greece. . Arch Virol 157:, 1729–1739. [CrossRef][PubMed]
    [Google Scholar]
  42. Wheeler C. M., Yamada T., Hildesheim A., Jenison S. A.. ( 1997;). Human papillomavirus type 16 sequence variants: identification by E6 and L1 lineage-specific hybridization. . J Clin Microbiol 35:, 11–19.[PubMed]
    [Google Scholar]
  43. Wu Y., Chen Y., Li L., Yu G., He Y., Zhang Y.. ( 2006;). Analysis of mutations in the E6/E7 oncogenes and L1 gene of human papillomavirus 16 cervical cancer isolates from China. . J Gen Virol 87:, 1181–1188. [CrossRef][PubMed]
    [Google Scholar]
  44. Yamada T., Wheeler C. M., Halpern A. L., Stewart A. C., Hildesheim A., Jenison S. A.. ( 1995;). Human papillomavirus type 16 variant lineages in United States populations characterized by nucleotide sequence analysis of the E6, L2, and L1 coding segments. . J Virol 69:, 7743–7753.[PubMed]
    [Google Scholar]
  45. Yamada T., Manos M. M., Peto J., Greer C. E., Munoz N., Bosch F. X., Wheeler C. M.. ( 1997;). Human papillomavirus type 16 sequence variation in cervical cancers: a worldwide perspective. . J Virol 71:, 2463–2472.[PubMed]
    [Google Scholar]
  46. Zuna R. E., Moore W. E., Shanesmith R. P., Dunn S. T., Wang S. S., Schiffman M., Blakey G. L., Teel T.. ( 2009;). Association of HPV16 E6 variants with diagnostic severity in cervical cytology samples of 354 women in a US population. . Int J Cancer 125:, 2609–2613. [CrossRef][PubMed]
    [Google Scholar]
  47. zur Hausen H.. ( 1996;). Papillomavirus infections–a major cause of human cancers. . Biochim Biophys Acta 1288:, F55–F78.[PubMed]
    [Google Scholar]
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