1887

Abstract

Neutralization capsid epitopes are important determinants for antibody-mediated immune protection against papillomavirus (PV) infection and induced disease. Chimeric L1 major capsid proteins of the human PV type 16 (HPV-16) and the bovine PV type 1 (BPV-1) with a foreign peptide incorporated into several capsid surface loops self-assembled into pentamers or virus-like particles (VLP). Binding patterns of neutralizing monoclonal antibodies (MAb) and immunization of mice confirmed (i) that regions around aa 282–286 and 351–355 contribute to neutralization epitopes and identified the latter region as an immunodominant site and (ii) that placing a foreign peptide in the context of an assembled structure markedly enhanced its immunogenicity. Pentamers disassembled from wild-type HPV-16 and BPV-1 VLPs displayed some of the neutralization epitopes that were detected on fully assembled VLPs, but were deficient for binding a subset of neutralizing MAb that inhibit cell attachment.

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2001-11-01
2020-01-28
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References

  1. Baker, T. S., Newcomb, W. W., Olson, N. H., Cowsert, L. M., Olson, C. & Brown, J. C. ( 1991; ). Structures of bovine and human papillomaviruses. Analysis by cryoelectron microscopy and three-dimensional image reconstruction. Biophysical Journal 60, 1445-1456.[CrossRef]
    [Google Scholar]
  2. Bell, J. A., Sunberg, J. P., Ghim, S. J., Newsome, J., Jenson, A. B. & Schlegel, R. ( 1994; ). A formalin-inactivated vaccine protects against mucosal papillomavirus infection: a canine model. Pathobiology 62, 194-198.[CrossRef]
    [Google Scholar]
  3. Breitburd, F., Kirnbauer, R., Hubbert, N. L., Nonnenmacher, B., Trin-Dinh-Desmarquet, C., Orth, G., Schiller, J. T. & Lowy, D. R. ( 1995; ). Immunization with viruslike particles from cottontail rabbit papillomavirus (CRPV) can protect against experimental CRPV infection. Journal of Virology 69, 3959-3963.
    [Google Scholar]
  4. Chackerian, B., Lowy, D. R. & Schiller, J. T. ( 1999; ). Induction of autoantibodies to mouse CCR5 with recombinant papillomavirus particles. Proceedings of the National Academy of Sciences, USA 96, 2373-2378.[CrossRef]
    [Google Scholar]
  5. Chen, X. S., Garcea, R. L., Goldberg, I., Casini, G. & Harrison, S. C. ( 2000; ). Structure of small virus-like particles assembled from the L1 protein of human papillomavirus 16. Molecular Cell 5, 557-567.[CrossRef]
    [Google Scholar]
  6. Christensen, N., Reed, C., Cladel, N., Han, R. & Kreider, J. ( 1996; ). Immunization with viruslike particles induces long-term protection of rabbits against challenge with cottontail rabbit papillomavirus. Journal of Virology 70, 960-965.
    [Google Scholar]
  7. Day, P. M., Roden, R. B. S., Lowy, D. R. & Schiller, J. T. ( 1998; ). The papillomavirus minor capsid protein, L2, induces localization of the major capsid protein, L1, and the viral transcription/replication protein, E2, to PML oncogenic domains. Journal of Virology 72, 142-150.
    [Google Scholar]
  8. Dvoretzky, I., Shober, R., Chattopadhyay, S. K. & Lowy, D. R. ( 1980; ). Focus assay in mouse cells for bovine papillomavirus. Virology 103, 369-375.[CrossRef]
    [Google Scholar]
  9. Howley, P. M. (1991). Role of the human papillomaviruses in human cancer. Cancer Research (Suppl. 18) 51, S5019–S5022.
  10. Kerschbaumer, R. J., Hirschl, S., Schwager, C., Ibl, M. & Himmler, G. ( 1996; ). pDAP2: a vector for construction of alkaline phosphatase fusion proteins. Immunotechnology 2, 145-150.[CrossRef]
    [Google Scholar]
  11. Kirnbauer, R. ( 1996; ). Papillomavirus-like particles for serology and vaccine development. Intervirology 39, 54-61.
    [Google Scholar]
  12. 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. Proceedings of the National Academy of Sciences, USA 89, 12180-12184.[CrossRef]
    [Google Scholar]
  13. Kirnbauer, R., Taub, J., Greenstone, H., Roden, R., Durst, M., Gissmann, L., Lowy, D. R. & Schiller, J. T. ( 1993; ). Efficient self-assembly of human papillomavirus type 16 L1 and L1–L2 into virus-like particles. Journal of Virology 67, 6929-6936.
    [Google Scholar]
  14. Kirnbauer, R., Chandrachud, L., O’Neil, B., Wagner, E., Grindlay, G., Armstrong, A., McGarvie, G., Schiller, J., Lowy, D. & Campo, M. ( 1996; ). Virus-like particles of bovine papillomavirus type-4 in prophylactic and therapeutic immunization. Virology 219, 37-44.[CrossRef]
    [Google Scholar]
  15. Kreider, J. W., Howett, M. K., Leure, D. A., Zaino, R. J. & Weber, J. A. ( 1987; ). Laboratory production in vivo of infectious human papillomavirus type 11. Journal of Virology 61, 590-593.
    [Google Scholar]
  16. Lowy, D. R., Kirnbauer, R. & Schiller, J. T. ( 1994; ). Genital human papillomavirus infection. Proceedings of the National Academy of Sciences, USA 91, 2436-2440.[CrossRef]
    [Google Scholar]
  17. Ludmerer, S. W., Benincasa, D. & Mark, G. E. ( 1996; ). Two amino acid residues confer type specificity to a neutralizing, conformationally dependent epitope on human papillomavirus type 11. Journal of Virology 70, 4791-4794.
    [Google Scholar]
  18. Ludmerer, S. W., Benincasa, D., Mark, G. E. & Christensen, N. D. ( 1997; ). A neutralizing epitope of human papillomavirus type 11 is principally described by a continuous set of residues which overlap a distinct linear, surface-exposed epitope. Journal of Virology 71, 3834-3839.
    [Google Scholar]
  19. Ludmerer, S. W., McClements, W. L., Wang, X. M., Ling, J. C., Jansen, K. U. & Christensen, N. D. ( 2000; ). HPV11 mutant virus-like particles elicit immune responses that neutralize virus and delineate a novel neutralizing domain. Virology 266, 237-245.[CrossRef]
    [Google Scholar]
  20. McCarthy, M. P., White, W. I., Palmer Hill, F., Koenig, S. & Suzich, J. A. ( 1998; ). Quantitative disassembly and reassembly of human papillomavirus type 11 viruslike particles in vitro. Journal of Virology 72, 32-41.
    [Google Scholar]
  21. Meyers, C., Mayer, T. J. & Ozbun, M. A. ( 1997; ). Synthesis of infectious human papillomavirus type 18 in differentiating epithelium transfected with viral DNA. Journal of Virology 71, 7381-7386.
    [Google Scholar]
  22. Muster, T., Guinea, R., Trkola, A., Purtscher, M., Klima, A., Steindl, F., Palese, P. & Katinger, H. ( 1994; ). Cross-neutralizing activity against divergent human immunodeficiency virus type 1 isolates induced by the gp41 sequence ELDKWAS. Journal of Virology 68, 4031-4034.
    [Google Scholar]
  23. Ochman, H., Gerber, A. S. & Hartl, D. L. ( 1988; ). Genetic applications of an inverse polymerase chain reaction. Genetics 120, 621-623.
    [Google Scholar]
  24. Roden, R., Greenstone, H., Kirnbauer, R., Booy, F., Joel, J., Lowy, D. & Schiller, J. ( 1996a; ). In vitro generation and type-specific neutralization of a human papillomavirus type 16 virion pseudotype. Journal of Virology 70, 5875-5883.
    [Google Scholar]
  25. Roden, R., Hubbert, N., Kirnbauer, R., Christensen, N., Lowy, D. & Schiller, J. ( 1996b; ). Assessment of the serological relatedness of genital human papillomaviruses by hemagglutination inhibition. Journal of Virology 70, 3298-3301.
    [Google Scholar]
  26. Roden, R. B., Armstrong, A., Haderer, P., Christensen, N. D., Hubbert, N. L., Lowy, D. R., Schiller, J. T. & Kirnbauer, R. ( 1997; ). Characterization of a human papillomavirus type 16 variant-dependent neutralizing epitope. Journal of Virology 71, 6247-6252.
    [Google Scholar]
  27. Rose, R., White, W., Maolin, L., Suzich, J., Lane, C. & Garcea, R. ( 1998; ). Human papillomavirus type 11 recombinant L1 capsomeres induce virus-neutralizing antibodies. Journal of Virology 72, 6151-6154.
    [Google Scholar]
  28. Schiller, J. T. & Okun, M. ( 1996; ). Papillomavirus vaccines: current status and future prospects. Advances in Dermatology 11, 355-380.
    [Google Scholar]
  29. Suzich, J. A., Ghim, S., Palmer-Hill, F. J., White, W. I., Tamura, J. K., Bell, J., Newsome, J. A., Jenson, A. B. & Schlegel, R. ( 1995; ). Systemic immunization with papillomavirus L1 protein completely prevents the development of viral mucosal papillomas. Proceedings of the National Academy of Sciences, USA 92, 11553-11557.[CrossRef]
    [Google Scholar]
  30. Trus, B. L., Roden, R. B., Greenstone, H. L., Vrhel, M., Schiller, J. T. & Booy, F. P. ( 1997; ). Novel structural features of bovine papillomavirus capsid revealed by a three-dimensional reconstruction to 9 Å resolution. Nature Structural Biology 4, 413-420.[CrossRef]
    [Google Scholar]
  31. White, W. I., Wilson, S. D., Bonnez, W., Rose, R. C., Koenig, S. & Suzich, J. A. ( 1998; ). In vitro infection and type-restricted antibody-mediated neutralization of authentic human papillomavirus type 16. Journal of Virology 72, 959-964.
    [Google Scholar]
  32. Zinkernagel, R. M. & Hengartner, H. ( 1997; ). Antiviral immunity. Immunology Today 18, 258-260.
    [Google Scholar]
  33. zur Hausen, H. ( 1991; ). Human papillomaviruses in the pathogenesis of anogenital cancer. Virology 184, 9-13.[CrossRef]
    [Google Scholar]
  34. zur Hausen, H. ( 1994; ). Molecular pathogenesis of cancer of the cervix and its causation by specific human papillomavirus types. Current Topics in Microbiology and Immunology 186, 131-156.
    [Google Scholar]
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