1887

Abstract

Whereas the antibody response to the anogenital human papillomaviruses (HPVs) is known to be mainly type-specific, correlated with the presence of viral DNA and mainly directed to conformational epitopes of the virion, it is not known if this applies also to the antibody response to cutaneous HPVs. For 434 non-immunosuppressed patients with skin lesions (squamous cell carcinoma and basal cell carcinoma of the skin, actinic keratosis and benign skin lesions), we compared HPV DNA status with seroreactivity to HPV pseudovirions (PsV) and to GST-L1 fusion proteins from HPV types -5, -6, -15, -16, -32 and -38. Biopsies from the skin lesions were tested for the presence of HPV DNA using three different PCR methods, with typing by sequencing. Serum samples from subjects with HPV DNA-positive biopsies and randomly selected serum samples from subjects with HPV DNA-negative biopsies were also tested with neutralization assays with HPV5, -38 and -76 PsV. Agreement of the three serological methods varied from poor to moderate. Type-specific seroprevalences among patients positive for the same type of HPV DNA (sensitivity of serology) was improved with the PsV-based method (mean of 40 %, maximum 63 %) compared with the GST-L1 method (mean of 20 %, maximum of 25 %). Neutralization was the most sensitive assay for HPV38 (50 %). In summary, cutaneous HPVs also appear to induce a type-specific antibody response that correlates with the presence of HPV DNA and that can be detected with improved sensitivity using PsV-based serology.

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2013-05-01
2022-06-27
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References

  1. Andersson K., Waterboer T., Kirnbauer R., Slupetzky K., Iftner T., de Villiers E. M., Forslund O., Pawlita M., Dillner J. 2008; Seroreactivity to cutaneous human papillomaviruses among patients with nonmelanoma skin cancer or benign skin lesions. Cancer Epidemiol Biomarkers Prev 17:189–195 [View Article][PubMed]
    [Google Scholar]
  2. Antonsson A. 2012; Review: antibodies to cutaneous human papillomaviruses. J Med Virol 84:814–822 [View Article][PubMed]
    [Google Scholar]
  3. Buck C. B., Pastrana D. V., Lowy D. R., Schiller J. T. 2004; Efficient intracellular assembly of papillomaviral vectors. J Virol 78:751–757 [View Article][PubMed]
    [Google Scholar]
  4. de Roda Husman A. M., Snijders P. J., Stel H. V., van den Brule A. J., Meijer C. J., Walboomers J. M. 1995; Processing of long-stored archival cervical smears for human papillomavirus detection by the polymerase chain reaction. Br J Cancer 72:412–417 [View Article][PubMed]
    [Google Scholar]
  5. de Villiers E. M., Fauquet C., Broker T. R., Bernard H. U., zur Hausen H. 2004; Classification of papillomaviruses. Virology 324:17–27 [View Article][PubMed]
    [Google Scholar]
  6. Dessy F. J., Giannini S. L., Bougelet C. A., Kemp T. J., David M. P., Poncelet S. M., Pinto L. A., Wettendorff M. A. 2008; Correlation between direct ELISA, single epitope-based inhibition ELISA and pseudovirion-based neutralization assay for measuring anti-HPV-16 and anti-HPV-18 antibody response after vaccination with the AS04-adjuvanted HPV-16/18 cervical cancer vaccine. Hum Vaccin 4:425–434 [View Article][PubMed]
    [Google Scholar]
  7. Dias D., Van Doren J., Schlottmann S., Kelly S., Puchalski D., Ruiz W., Boerckel P., Kessler J., Antonello J. M.other authors 2005; Optimization and validation of a multiplexed luminex assay to quantify antibodies to neutralizing epitopes on human papillomaviruses 6, 11, 16, and 18. Clin Diagn Lab Immunol 12:959–969[PubMed]
    [Google Scholar]
  8. Dillner J. 1999; The serological response to papillomaviruses. Semin Cancer Biol 9:423–430 [View Article][PubMed]
    [Google Scholar]
  9. Eklund C., Unger E. R., Nardelli-Haefliger D., Zhou T., Dillner J. 2012; International collaborative proficiency study of human papillomavirus type 16 serology. Vaccine 30:294–299 [View Article][PubMed]
    [Google Scholar]
  10. Faust H., Knekt P., Forslund O., Dillner J. 2010; Validation of multiplexed human papillomavirus serology using pseudovirions bound to heparin-coated beads. J Gen Virol 91:1840–1848 [View Article][PubMed]
    [Google Scholar]
  11. Favre M., Majewski S., Noszczyk B., Maienfisch F., Pura A., Orth G., Jablonska S. 2000; Antibodies to human papillomavirus type 5 are generated in epidermal repair processes. J Invest Dermatol 114:403–407 [View Article][PubMed]
    [Google Scholar]
  12. Feltkamp M. C., de Koning M. N., Bavinck J. N., Ter Schegget J. 2008; Betapapillomaviruses: innocent bystanders or causes of skin cancer. J Clin Virol 43:353–360 [View Article][PubMed]
    [Google Scholar]
  13. Forslund O., Antonsson A., Nordin P., Stenquist B., Hansson B. G. 1999; A broad range of human papillomavirus types detected with a general PCR method suitable for analysis of cutaneous tumours and normal skin. J Gen Virol 80:2437–2443[PubMed]
    [Google Scholar]
  14. Forslund O., Antonsson A., Edlund K., van den Brule A. J., Hansson B. G., Meijer C. J., Ryd W., Rylander E., Strand A.other authors 2002; Population-based type-specific prevalence of high-risk human papillomavirus infection in middle-aged Swedish women. J Med Virol 66:535–541 [View Article][PubMed]
    [Google Scholar]
  15. Forslund O., Lindelöf B., Hradil E., Nordin P., Stenquist B., Kirnbauer R., Slupetzky K., Dillner J. 2004; High prevalence of cutaneous human papillomavirus DNA on the top of skin tumors but not in “Stripped” biopsies from the same tumors. J Invest Dermatol 123:388–394 [View Article][PubMed]
    [Google Scholar]
  16. Forslund O., Iftner T., Andersson K., Lindelof B., Hradil E., Nordin P., Stenquist B., Kirnbauer R., Dillner J., de Villiers E. M.Viraskin Study Group 2007; Cutaneous human papillomaviruses found in sun-exposed skin: beta-papillomavirus species 2 predominates in squamous cell carcinoma. J Infect Dis 196:876–883 [View Article][PubMed]
    [Google Scholar]
  17. Hagensee M. E., Yaegashi N., Galloway D. A. 1993; Self-assembly of human papillomavirus type 1 capsids by expression of the L1 protein alone or by coexpression of the L1 and L2 capsid proteins. J Virol 67:315–322[PubMed]
    [Google Scholar]
  18. Kirnbauer R., Booy F., Cheng N., Lowy D. R., Schiller J. T. 1992; Papillomavirus L1 major capsid protein self-assembles into virus-like particles that are highly immunogenic. Proc Natl Acad Sci U S A 89:12180–12184 [View Article][PubMed]
    [Google Scholar]
  19. Kirnbauer R., Hubbert N. L., Wheeler C. M., Becker T. M., Lowy D. R., Schiller J. T. 1994; A virus-like particle enzyme-linked immunosorbent assay detects serum antibodies in a majority of women infected with human papillomavirus type 16. J Natl Cancer Inst 86:494–499 [View Article][PubMed]
    [Google Scholar]
  20. Landis J. R., Koch G. G. 1977; An application of hierarchical kappa-type statistics in the assessment of majority agreement among multiple observers. Biometrics 33:363–374 [View Article][PubMed]
    [Google Scholar]
  21. Michael K. M., Waterboer T., Sehr P., Rother A., Reidel U., Boeing H., Bravo I. G., Schlehofer J., Gärtner B. C., Pawlita M. 2008; Seroprevalence of 34 human papillomavirus types in the German general population. PLoS Pathog 4:e1000091 [View Article][PubMed]
    [Google Scholar]
  22. Newall A. T., Brotherton J. M., Quinn H. E., McIntyre P. B., Backhouse J., Gilbert L., Esser M. T., Erick J., Bryan J.other authors 2008; Population seroprevalence of human papillomavirus types 6, 11, 16, and 18 in men, women, and children in Australia. Clin Infect Dis 46:1647–1655 [View Article][PubMed]
    [Google Scholar]
  23. Opalka D., Lachman C. E., MacMullen S. A., Jansen K. U., Smith J. F., Chirmule N., Esser M. T. 2003; Simultaneous quantitation of antibodies to neutralizing epitopes on virus-like particles for human papillomavirus types 6, 11, 16, and 18 by a multiplexed luminex assay. Clin Diagn Lab Immunol 10:108–115[PubMed]
    [Google Scholar]
  24. Opalka D., Matys K., Bojczuk P., Green T., Gesser R., Saah A., Haupt R., Dutko F., Esser M. T. 2010; Multiplexed serologic assay for nine anogenital human papillomavirus types. Clin Vaccine Immunol 17:818–827 [View Article][PubMed]
    [Google Scholar]
  25. Paaso A. E., Louvanto K., Syrjänen K. J., Waterboer T., Grénman S. E., Pawlita M., Syrjänen S. M. 2011; Lack of type-specific concordance between human papillomavirus (HPV) serology and HPV DNA detection in the uterine cervix and oral mucosa. J Gen Virol 92:2034–2046 [View Article][PubMed]
    [Google Scholar]
  26. Pastrana D. V., Buck C. B., Pang Y. Y., Thompson C. D., Castle P. E., FitzGerald P. C., Krüger Kjaer S., Lowy D. R., Schiller J. T. 2004; Reactivity of human sera in a sensitive, high-throughput pseudovirus-based papillomavirus neutralization assay for HPV16 and HPV18. Virology 321:205–216 [View Article][PubMed]
    [Google Scholar]
  27. Plasmeijer E. I., Neale R. E., O’Rourke P., Mallitt K. A., de Koning M. N., Quint W., Buettner P. G., Pawlita M., Waterboer T.other authors 2010; Lack of association between the presence and persistence of betapapillomavirus DNA in eyebrow hairs and betapapillomavirus L1 antibodies in serum. J Gen Virol 91:2073–2079 [View Article][PubMed]
    [Google Scholar]
  28. Rizk R. Z., Christensen N. D., Michael K. M., Müller M., Sehr P., Waterboer T., Pawlita M. 2008; Reactivity pattern of 92 monoclonal antibodies with 15 human papillomavirus types. J Gen Virol 89:117–129 [View Article][PubMed]
    [Google Scholar]
  29. Schiller J. T., Lowy D. R. 2009; Immunogenicity testing in human papillomavirus virus-like-particle vaccine trials. J Infect Dis 200:166–171 [View Article][PubMed]
    [Google Scholar]
  30. Sehr P., Zumbach K., Pawlita M. 2001; A generic capture ELISA for recombinant proteins fused to glutathione S-transferase: validation for HPV serology. J Immunol Methods 253:153–162 [View Article][PubMed]
    [Google Scholar]
  31. Villa L. L., Costa R. L., Petta C. A., Andrade R. P., Ault K. A., Giuliano A. R., Wheeler C. M., Koutsky L. A., Malm C.other authors 2005; Prophylactic quadrivalent human papillomavirus (types 6, 11, 16, and 18) L1 virus-like particle vaccine in young women: a randomised double-blind placebo-controlled multicentre phase II efficacy trial. Lancet Oncol 6:271–278 [View Article][PubMed]
    [Google Scholar]
  32. Waterboer T., Sehr P., Michael K. M., Franceschi S., Nieland J. D., Joos T. O., Templin M. F., Pawlita M. 2005; Multiplex human papillomavirus serology based on in situ-purified glutathione S-transferase fusion proteins. Clin Chem 51:1845–1853 [View Article][PubMed]
    [Google Scholar]
  33. Waterboer T., Sehr P., Pawlita M. 2006; Suppression of non-specific binding in serological Luminex assays. J Immunol Methods 309:200–204 [View Article][PubMed]
    [Google Scholar]
  34. zur Hausen H. 2002; Papillomaviruses and cancer: from basic studies to clinical application. Nat Rev Cancer 2:342–350 [View Article][PubMed]
    [Google Scholar]
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