Validation of multiplexed human papillomavirus serology using pseudovirions bound to heparin-coated beads

Journal of General Virology

Volumn 91, Issue 7, 2010, Pages 1840-1848

  Faust, Helena ^a   Knekt, Paul ^b   Forslund, Ola ^a   Dillner, Joakim ^a  

^a LUND UNIVERSITY HOSPITAL   (Sweden)

^b NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

HEPARIN; MONOCLONAL ANTIBODY; VIRUS DNA;

ADULT; AGED; ARTICLE; CHILD; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLUORESCENCE; HUMAN; NONHUMAN; PRIORITY JOURNAL; RISK FACTOR; SEROLOGY; TRANSMISSION ELECTRON MICROSCOPY; UTERINE CERVIX CANCER; VIRION; WART VIRUS; ALPHAPAPILLOMAVIRUS; ANIMAL; CELL LINE; CLASSIFICATION; IMMUNOASSAY; IMMUNOLOGY; INSTRUMENTATION; MALE; METHODOLOGY; MIDDLE AGED; REPRODUCIBILITY; SENSITIVITY AND SPECIFICITY; UTERINE CERVIX TUMOR; VIROLOGY;

HUMAN PAPILLOMAVIRUS; HUMAN PAPILLOMAVIRUS TYPE 16; MAMMALIA;

ADULT; ALPHAPAPILLOMAVIRUS; ANIMALS; CELL LINE; CHILD; DNA, VIRAL; FEMALE; HEPARIN; HUMANS; IMMUNOASSAY; MALE; MIDDLE AGED; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY; SEROLOGIC TESTS; UTERINE CERVICAL NEOPLASMS;

EID: 77954157567     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.019349-0     Document Type: Article

References (47)

1. af Geijersstam, V., Eklund, C., Wang, Z., Sapp, M., Schiller, J. T., Dillner, J. & Dillner, L. (1999). A survey of seroprevalence of human papillomavirus types 16, 18 and 33 among children. Int J Cancer 80, 489-493.
2. Antonsson, A., Karanfilovska, S., Lindqvist, P. G. & Hansson, B. G. (2003). General acquisition of human papillomavirus infections of skin occurs in early infancy. J Clin Microbiol 41, 2509-2514. (Pubitemid 36712461)
3. Arbyn, M. & Dillner, J. (2007). Review of current knowledge on HPV vaccination: an appendix to the European Guidelines for Quality Assurance in cervical cancer screening. J Clin Virol 38, 189-197.
4. Buck, C. B., Pastrana, D. V., Lowy, D. R. & Schiller, J. T. (2004). Efficient intracellular assembly of papillomaviral vectors. J Virol 78, 751-757.
5. Buck, C. B., Pastrana, D. V., Lowy, D. R. & Schiller, J. T. (2005). Generation of HPV pseudovirions using transfection and their use in neutralization assays. Methods Mol Med 119, 445-462.
6. Carter, J. J., Koutsky, L. A., Wipf, G. C., Christensen, N. D., Lee, S. K., Kuypers, J., Kiviat, N. & Galloway, D. A. (1996). The natural history of human papillomavirus type 16 capsid antibodies among a cohort of university women. J Infect Dis 174, 927-936. (Pubitemid 26357453)
7. Christensen, N. D., Dillner, J., Eklund, C., Carter, J. J., Wipf, G. C., Reed, C. A., Cladel, N. M. & Galloway, D. A. (1996a). Surface conformational and linear epitopes on HPV-16 and HPV-18 L1 virus-like particles as defined by monoclonal antibodies. Virology 223, 174-184.
8. Christensen, N. D., Reed, C. A., Cladel, N. M., Hall, K. & Leiserowitz, G. S. (1996b). Monoclonal antibodies to HPV-6 L1 virus-like particles identify conformational and linear neutralizing epitopes on HPV-11 in addition to type-specific epitopes on HPV-6. Virology 224, 477-486.
9. Christensen, N. D., Cladel, N. M., Reed, C. A., Budgeon, L. R., Embers, M. E., Skulsky, D. M., McClements, W. L., Ludmerer, S. W. & Jansen, K. U. (2001). Hybrid papillomavirus L1 molecules assemble into virus-like particles that reconstitute conformational epitopes and induce neutralizing antibodies to distinct HPV types. Virology 291, 324-334.
10. Combita, A. L., Touzé, A., Bousarghin, L., Sizaret, P. Y., Muñoz, N. & Coursaget, P. (2001). Gene transfer using human papillomavirus pseudovirions varies according to virus genotype and requires cell surface heparan sulfate. FEMS Microbiol Lett 204, 183-188.
11. 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.
12. Dillner, J., Wiklund, F., Lenner, P., Eklund, C., Frederiksson- Shanazarian, V., Schiller, J. T., Hibma, M., Hallmans, G. & Stendahl, U. (1995). Antibodies against linear and conformational epitopes of human papillomavirus type 16 that independently associate with incident cervical cancer. Int J Cancer 60, 377-382.
13. Dillner, J., Andersson-Ellstrom, A., Hagmar, B. & Schiller, J. (1999). High risk genital papillomavirus infections are not spread vertically. Rev Med Virol 9, 23-29. (Pubitemid 29088064)
14. Drobni, P., Mistry, N., McMillan, N. & Evander, M. (2003). Carboxyfluorescein diacetate, succinimidyl ester labeled papillomavirus viruslike particles fluoresce after internalization and interact with heparan sulfate for binding and entry. Virology 310, 163-172.
15. Ferguson, M., Heath, A., Johnes, S., Pagliusi, S. & Dillner, J. (2006). Results of the first WHO international collaborative study on the standardization of the detection of antibodies to human papillomaviruses. Int J Cancer 118, 1508-1514.
16. 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.
17. Forslund, O., Iftner, T., Andersson, K., Lindelof, B., Hradil, E., Nordin, P., Stenquist, B., Kirnbauer, R., Dillner, J. & de Villiers, E. M. (2007). Cutaneous human papillomaviruses found in sun-exposed skin: betapapillomavirus species 2 predominates in squamous cell carcinoma. J Infect Dis 196, 876-883.
18. Giroglou, T., Florin, L., Schafer, F., Streeck, R. E. & Sapp, M. (2001). Human papillomavirus infection requires cell surface heparan sulfate. J Virol 75, 1565-1570.
19. Grabowska, K., Wang, X., Jacobsson, A. & Dillner, J. (2002). Evaluation of cost-precision ratios of different strategies for ELISA measurement of serum antibody levels. J Immunol Methods 271, 1-15.
20. Hagensee, M. E., Yaegashi, N. & Galloway, D. A. (1993). Selfassembly 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. (Pubitemid 23002992)
21. Hakama, M., Lehtinen, M., Knekt, P., Aromaa, A., Leinikki, P., Miettinen, A., Paavonen, J., Peto, R. & Teppo, L. (1993). Serum antibodies and subsequent cervical neoplasms: a prospective study with 12 years of follow-up. Am J Epidemiol 137, 166-170.
22. Harper, D. M., Franco, E. L., Wheeler, C., Ferris, D. G., Jenkins, D., Schuind, A., Zahaf, T., Innis, B., Naud, P. & other authors (2004). Efficacy of a bivalent L1 virus-like particle vaccine in prevention of infection with human papillomavirus types 16 and 18 in young women: a randomised controlled trial. Lancet 364, 1757-1765.
23. Ho, G. Y., Burk, R. D., Klein, S., Kadish, A. S., Chang, C. J., Palan, P., Basu, J., Tachezy, R., Lewis, R. & Romney, S. (1995). Persistent genital human papillomavirus infection as a risk factor for persistent cervical dysplasia. J Natl Cancer Inst 87, 1365-1371.
24. Joyce, J. G., Tung, J. S., Przysiecki, C. T., Cook, J. C., Lehman, E. D., Sands, J. A., Jansen, K. U. & Keller, P. M. (1999). The L1 major capsid protein of human papillomavirus type 11 recombinant virus-like particles interacts with heparin and cell-surface glycosaminoglycans on human keratinocytes. J Biol Chem 274, 5810-5822.
25. 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.
26. Kjellberg, L., Wang, Z., Wiklund, F., Edlund, K., Angstrom, T., Lenner, P., Sjoberg, I., Hallmans, G., Wallin, K. L. & other authors (1999). Sexual behaviour and papillomavirus exposure in cervical intraepithelial neoplasia: a population-based case-control study. J Gen Virol 80, 391-398.
27. Koutsky, L. A., Ault, K. A., Wheeler, C. M., Brown, D. R., Barr, E., Alvarez, F. B., Chiacchierini, L. M. & Jansen, K. U. (2002). A controlled trial of a human papillomavirus type 16 vaccine. N Engl J Med 347, 1645-1651.
28. 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.
29. Le Cann, P., Coursaget, P., Iochmann, S. & Touze, A. (1994). Self-assembly of human papillomavirus type 16 capsids by expression of the L1 protein in insect cells. FEMS Microbiol Lett 117, 269-274.
30. Lehtinen, M., Dillner, J., Knekt, P., Luostarinen, T., Aromaa, A., Kirnbauer, R., Koskela, P., Paavonen, J., Peto, R. & other authors (1996). Serologically diagnosed infection with human papillomavirus type 16 and risk for subsequent development of cervical carcinoma: nested case-control study. BMJ 312, 537-539. (Pubitemid 26070265)
31. Marais, D. J., Sampson, C. C., Urban, M. I., Sitas, F. & Wiliamson, A. L. (2007). The seroprevalence of IgG antibodies to human papillomavirus (HPV) types HPV-16, HPV-18, and HPV-11 capsid-antigens in mothers and their children. J Med Virol 79, 1370-1374.
32. Michael, K.M., Waterboer, T., Sehr, P., Rother, A., Reidel, U., Boeing, H., Bravo, I. G., Schlehofer, J., Gartner, B. C. & Pawlita, M. (2008). Seroprevalence of 34 human papillomavirus types in the German general population. PLoS Pathog 4, e1000091.
33. Naucler, P., Da Costa, F. M., Ljungberg, O., Bugalho, A. & Dillner, J. (2004). Human papillomavirus genotypes in cervical cancers in Mozambique. J Gen Virol 85, 2189-2190.
34. 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.
35. Pagliusi, S. R., Dillner, J., Pawlita, M., Quint, W. G. V., Wheeler, C. M. & Ferguson, M. (2006). Chapter 23: International standard reagents for harmonization of HPV serology and DNA assays - an update. Vaccine 24 (Suppl. 3), S193-S200.
36. Pastrana, D. V., Buck, C. B., Pang, Y. Y., Thompson, C. D., Castle, P. E., FitzGerald, P. C., Kruger 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. HPV serology
37. Rizk, R. Z., Christensen, N. D., Michael, K. M., Muller, 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.
38. Rommel, O., Dillner, J., Fligge, C., Bergsdorf, C., Wang, X., Selinka, H. C. & Sapp, M. (2005). Heparan sulfate proteoglycans interact exclusively with conformationally intact HPV L1 assemblies: basis for a virus-like particle ELISA. J Med Virol 75, 114-121.
39. Sasagawa, T., Pushko, P., Steers, G., Gschmeissner, S. E., Hajibagheri, M. A., Finch, J., Crawford, L. & Tommasino, M. (1995). Synthesis and assembly of virus-like particles of human papillomaviruses type 6 and type 16 in fission yeast Schizosaccharomyces pombe. Virology 206, 126-135.
40. Schiffman, M. H., Bauer, H. M., Hoover, R. N., Glass, A. G., Cadell, D. M., Rush, B. B., Scott, D. R., Sherman, M. E., Kurman, R. J. & other authors (1993). Epidemiologic evidence showing that human papillomavirus infection causes most cervical intraepithelial neoplasia. J Natl Cancer Inst 85, 958-964.
41. Shafti-Keramat, S., Handisurya, A., Kriehuber, E., Meneguzzi, G., Slupetzky, K. & Kirnbauer, R. (2003). Different heparan sulfate proteoglycans serve as cellular receptors for human papillomaviruses. J Virol 77, 13125-13135.
42. Silins, I., Wang, X., Tadesse, A., Jansen, K. U., Schiller, J. T., Avall-Lundqvist, E., Frankendal, B. & Dillner, J. (2004). A population-based study of cervical carcinoma and HPV infection in Latvia. Gynecol Oncol 93, 484-492. (Pubitemid 38507623)
43. Sturegard, E., Johnsson, A., Gustafsson, E. & Dillner, J. (2008). Condyloma typing important for follow up ofHPV vaccination. A condyloma reporting project. Lakartidningen 105, 3648-3650 (in Swedish).
44. Walboomers, J. M., Jacobs, M. V., Manos, M. M., Bosch, F. X., Kummer, J. A., Shah, K. V., Snijders, P. J., Peto, J., Meijer, C. J. & Muñoz, N. (1999). Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol 189, 12-19.
45. Wang, Z., Hansson, B. G., Forslund, O., Dillner, L., Sapp, M., Schiller, J. T., Bjerre, B. & Dillner, J. (1996). Cervical mucus antibodies against human papillomavirus type 16, 18, and 33 capsids in relation to presence of viral DNA. J Clin Microbiol 34, 3056-3062. (Pubitemid 26389358)
46. Wang, X., Sapp, M., Christensen, N. D. & Dillner, J. (2005). Heparin-based ELISA reduces background reactivity in virus-like particle-based papillomavirus serology. J Gen Virol 86, 65-73.
47. 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.