1887

Abstract

A modified pan-PV consensus-degenerate hybrid oligonucleotide primer (CODEHOP) PCR was developed for generic and sensitive detection of a broad-spectrum of human papillomaviruses (HPVs) infecting the cutaneous epithelium. To test the analytical sensitivity of the assay we examined 149 eyebrow hair follicle specimens from immunocompetent male patients. HPV DNA was detected in 60 % (89/149) of analysed eyebrow samples with a total of 48 different HPV sequences, representing 21 previously described HPVs and 27 putative novel HPV types. Evidence for ten novel HPV subtypes and seven viral variants, clustering to three out of five genera containing cutaneous HPVs, was also obtained. Thus, we have shown that the modified pan-PV CODEHOP PCR assay is able to identify multiple HPV types, even from different genera, in the same clinical sample. Overall, these results demonstrate that the pan-PV CODEHOP PCR is an excellent tool for screening and identification of novel cutaneous HPVs, even in samples with low viral loads.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000988
2017-12-15
2019-10-17
Loading full text...

Full text loading...

/deliver/fulltext/jgv/99/1/109.html?itemId=/content/journal/jgv/10.1099/jgv.0.000988&mimeType=html&fmt=ahah

References

  1. de Villiers EM, Fauquet C, Broker TR, Bernard HU, Zur Hausen H. Classification of papillomaviruses. Virology 2004;324:17–27 [CrossRef][PubMed]
    [Google Scholar]
  2. de Villiers EM. Cross-roads in the classification of papillomaviruses. Virology 2013;445:2–10 [CrossRef][PubMed]
    [Google Scholar]
  3. Cubie HA. Diseases associated with human papillomavirus infection. Virology 2013;445:21–34 [CrossRef][PubMed]
    [Google Scholar]
  4. Forman D, de Martel C, Lacey CJ, Soerjomataram I, Lortet-Tieulent J et al. Global burden of human papillomavirus and related diseases. Vaccine 2012;30:F12–F23 [CrossRef][PubMed]
    [Google Scholar]
  5. Forslund O, Iftner T, Andersson K, Lindelof B, Hradil E et al. Cutaneous human papillomaviruses found in sun-exposed skin: Beta-papillomavirus species 2 predominates in squamous cell carcinoma. J Infect Dis 2007;196:876–883 [CrossRef][PubMed]
    [Google Scholar]
  6. Arroyo Mühr LS, Hultin E, Bzhalava D, Eklund C, Lagheden C et al. Human papillomavirus type 197 is commonly present in skin tumors. Int J Cancer 2015;136:2546–2555 [CrossRef][PubMed]
    [Google Scholar]
  7. Hošnjak L, Kocjan BJ, Pirš B, Seme K, Poljak M. Characterization of two novel gammapapillomaviruses, HPV179 and HPV184, isolated from common warts of a renal-transplant recipient. PLoS One 2015;10:e0119154 [CrossRef][PubMed]
    [Google Scholar]
  8. Antonsson A, Erfurt C, Hazard K, Holmgren V, Simon M et al. Prevalence and type spectrum of human papillomaviruses in healthy skin samples collected in three continents. J Gen Virol 2003;84:1881–1886 [CrossRef][PubMed]
    [Google Scholar]
  9. Ekström J, Bzhalava D, Svenback D, Forslund O, Dillner J. High throughput sequencing reveals diversity of human papillomaviruses in cutaneous lesions. Int J Cancer 2011;129:2643–2650 [CrossRef][PubMed]
    [Google Scholar]
  10. Foulongne V, Sauvage V, Hebert C, Dereure O, Cheval J et al. Human skin microbiota: high diversity of DNA viruses identified on the human skin by high throughput sequencing. PLoS One 2012;7:e38499 [CrossRef][PubMed]
    [Google Scholar]
  11. Bolatti EM, Chouhy D, Hošnjak L, Casal PE, Kocjan BJ et al. Corrigendum: natural history of human papillomavirus infection of sun-exposed healthy skin of immunocompetent individuals over three climatic seasons and identification of HPV209, a novel betapapillomavirus. J Gen Virol 2017;98:2205–2206 [CrossRef][PubMed]
    [Google Scholar]
  12. Chouhy D, Bolatti EM, Pérez GR, Giri AA. Analysis of the genetic diversity and phylogenetic relationships of putative human papillomavirus types. J Gen Virol 2013;94:2480–2488 [CrossRef][PubMed]
    [Google Scholar]
  13. Boxman IL, Berkhout RJ, Mulder LH, Wolkers MC, Bouwes Bavinck JN et al. Detection of human papillomavirus DNA in plucked hairs from renal transplant recipients and healthy volunteers. J Invest Dermatol 1997;108:712–715 [CrossRef][PubMed]
    [Google Scholar]
  14. Forslund O, Ly H, Higgins G. Improved detection of cutaneous human papillomavirus DNA by single tube nested 'hanging droplet' PCR. J Virol Methods 2003;110:129–136 [CrossRef][PubMed]
    [Google Scholar]
  15. Chouhy D, Gorosito M, Sánchez A, Serra EC, Bergero A et al. New generic primer system targeting mucosal/genital and cutaneous human papillomaviruses leads to the characterization of HPV 115, a novel Beta-papillomavirus species 3. Virology 2010;397:205–216 [CrossRef][PubMed]
    [Google Scholar]
  16. Kocjan BJ, Bzhalava D, Forslund O, Dillner J, Poljak M. Molecular methods for identification and characterization of novel papillomaviruses. Clin Microbiol Infect 2015;21:808–816 [CrossRef][PubMed]
    [Google Scholar]
  17. Rose TM, Schultz ER, Henikoff JG, Pietrokovski S, McCallum CM et al. Consensus-degenerate hybrid oligonucleotide primers for amplification of distantly related sequences. Nucleic Acids Res 1998;26:1628–1635 [CrossRef][PubMed]
    [Google Scholar]
  18. Rose TM. CODEHOP-mediated PCR–a powerful technique for the identification and characterization of viral genomes. Virol J 2005;2:20 [CrossRef][PubMed]
    [Google Scholar]
  19. Staheli JP, Ryan JT, Bruce AG, Boyce R, Rose TM. Consensus-degenerate hybrid oligonucleotide primers (CODEHOPs) for the detection of novel viruses in non-human primates. Methods 2009;49:32–41 [CrossRef][PubMed]
    [Google Scholar]
  20. Walsh EE, Falsey AR, Swinburne IA, Formica MA. Reverse transcription polymerase chain reaction (RT-PCR) for diagnosis of respiratory syncytial virus infection in adults: use of a single-tube "hanging droplet" nested PCR. J Med Virol 2001;63:259–263 [CrossRef][PubMed]
    [Google Scholar]
  21. Chouhy D, Bolatti EM, Piccirilli G, Sánchez A, Fernandez Bussy R et al. Identification of human papillomavirus type 156, the prototype of a new human gammapapillomavirus species, by a generic and highly sensitive PCR strategy for long DNA fragments. J Gen Virol 2013;94:524–533 [CrossRef][PubMed]
    [Google Scholar]
  22. Kocjan BJ, Poljak M, Seme K, Potocnik M, Fujs K et al. Distribution of human papillomavirus genotypes in plucked eyebrow hairs from Slovenian males with genital warts. Infect Genet Evol 2005;5:255–259 [CrossRef][PubMed]
    [Google Scholar]
  23. van Duin M, Snijders PJ, Schrijnemakers HF, Voorhorst FJ, Rozendaal L et al. Human papillomavirus 16 load in normal and abnormal cervical scrapes: an indicator of CIN II/III and viral clearance. Int J Cancer 2002;98:590–595 [CrossRef][PubMed]
    [Google Scholar]
  24. Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 2016;33:1870–1874 [CrossRef][PubMed]
    [Google Scholar]
  25. Drummond AJ, Suchard MA, Xie D, Rambaut A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 2012;29:1969–1973 [CrossRef][PubMed]
    [Google Scholar]
  26. Hampras SS, Giuliano AR, Lin HY, Fisher KJ, Abrahamsen ME et al. Natural history of cutaneous human papillomavirus (HPV) infection in men: the HIM study. PLoS One 2014;9:e104843 [CrossRef][PubMed]
    [Google Scholar]
  27. Neale RE, Weissenborn S, Abeni D, Bavinck JN, Euvrard S et al. Human papillomavirus load in eyebrow hair follicles and risk of cutaneous squamous cell carcinoma. Cancer Epidemiol Biomarkers Prev 2013;22:719–727 [CrossRef][PubMed]
    [Google Scholar]
  28. Schneider I, Lehmann MD, Kogosov V, Stockfleth E, Nindl I. Eyebrow hairs from actinic keratosis patients harbor the highest number of cutaneous human papillomaviruses. BMC Infect Dis 2013;13:186 [CrossRef][PubMed]
    [Google Scholar]
  29. Iannacone MR, Gheit T, Pfister H, Giuliano AR, Messina JL et al. Case-control study of genus-beta human papillomaviruses in plucked eyebrow hairs and cutaneous squamous cell carcinoma. Int J Cancer 2014;134:2231–2244 [CrossRef][PubMed]
    [Google Scholar]
  30. Asgari MM, Kiviat NB, Critchlow CW, Stern JE, Argenyi ZB et al. Detection of human papillomavirus DNA in cutaneous squamous cell carcinoma among immunocompetent individuals. J Invest Dermatol 2008;128:1409–1417 [CrossRef][PubMed]
    [Google Scholar]
  31. de Koning MN, Weissenborn SJ, Abeni D, Bouwes Bavinck JN, Euvrard S et al. Prevalence and associated factors of betapapillomavirus infections in individuals without cutaneous squamous cell carcinoma. J Gen Virol 2009;90:1611–1621 [CrossRef][PubMed]
    [Google Scholar]
  32. Deng Q, Li J, Pan Y, Liu F, He Z et al. Prevalence and associated risk factors of human papillomavirus in healthy skin specimens collected from rural Anyang, China, 2006–2008. J Invest Dermatol 2016;136:1191–1198 [CrossRef][PubMed]
    [Google Scholar]
  33. Bzhalava D, Eklund C, Dillner J. International standardization and classification of human papillomavirus types. Virology 2015;476:341–344 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000988
Loading
/content/journal/jgv/10.1099/jgv.0.000988
Loading

Data & Media loading...

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error