A direct comparison of human papillomavirus type 16 L1 particles reveals a lower immunogenicity of capsomeres than viruslike particles with respect to the induced antibody response

Journal of Virology

Volumn 82, Issue 11, 2008, Pages 5472-5485

  Thönes, Nadja ^a   Herreiner, Anna ^a   Schädlich, Lysann ^a   Piuko, Konrad ^a   Müller, Martin ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; CALGRANULIN; CAPSOMERE ANTIGEN; DNA; EPITOPE; IMMUNOGLOBULIN M; TOLL LIKE RECEPTOR 4; VIRUS ANTIGEN; VIRUS LIKE PARTICLE ANTIGEN;

ANIMAL EXPERIMENT; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CORRELATION ANALYSIS; DNA IMMUNIZATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GENE SWITCHING; HUMAN PAPILLOMAVIRUS TYPE 16; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNIZATION; IMMUNOGENICITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SERODIAGNOSIS;

ANIMALS; ANTIBODY FORMATION; CAPSID; CAPSID PROTEINS; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE; DNA, VIRAL; EPITOPES; HUMAN PAPILLOMAVIRUS 16; HUMANS; IMMUNITY, MUCOSAL; IMMUNOGENETICS; IMMUNOGLOBULIN CLASS SWITCHING; MICE; ONCOGENE PROTEINS, VIRAL; TOLL-LIKE RECEPTORS;

HEXAPODA; HUMAN PAPILLOMAVIRUS TYPE 16; MUS; PROKARYOTA;

EID: 43949083734     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02482-07     Document Type: Article

References (62)

1. Akira, S., and K. Takeda. 2004. Toll-like receptor signalling. Nat. Rev. Immunol. 4:499-511.
2. Bachmann, M. F., and R. M. Zinkernagel. 1996. The influence of virus structure on antibody responses and virus serotype formation. Immunol. Today 17:553-558.
3. Bachmann, M. F., and R. M. Zinkernagel. 1997. Neutralizing antiviral B cell responses. Annu. Rev. Immunol. 15:235-270.
4. Bachmann, M. F., R. M. Zinkernagel, and A. Oxenius. 1998. Immune responses in the absence of costimulation: viruses know the trick. J. Immunol. 161:5791-5794.
5. Balmelli, C., R. Roden, A. Potts, J. Schiller, P. De Grandi, and D. Nardelli-Haefliger. 1998. Nasal immunization of mice with human papillomavirus type 16 virus-like particles elicits neutralizing antibodies in mucosal secretions. J. Virol. 72:8220-8229.
6. Baumgarth, N. 2000. A two-phase model of B-cell activation. Immunol. Rev. 176:171-180.
7. Bins, A. D., A. Jorritsma, M. C. Wolkers, C. F. Hung, T. C. Wu, T. N. Schumacher, and J. B. Haanen. 2005. A rapid and potent DNA vaccination strategy defined by in vivo monitoring of antigen expression. Nat. Med. 11:899-904.
8. Breitburd, F., R. Kirnbauer, N. L. Hubbert, B. Nonnenmacher, C. Trin-Dinh-Desmarquet, G. Orth, J. T. Schiller, and D. R. Lowy. 1995. Immunization with viruslike particles from cottontail rabbit papillomavirus (CRPV) can protect against experimental CRPV infection. J. Virol. 69:3959-3963.
9. Carter, J. J., G. C. Wipf, S. F. Benki, N. D. Christensen, and D. A. Galloway. 2003. Identification of a human papillomavirus type 16-specific epitope on the C-terminal arm of the major capsid protein L1. J. Virol. 77:11625-11632.
10. Christensen, N. D., N. M. Cladel, C. A. Reed, L. R. Budgeon, M. E. Embers, D. M. Skulsky, W. L. McClements, S. W. Ludmerer, and K. U. Jansen. 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.
11. Christensen, N. D., J. Dillner, C. Eklund, J. J. Carter, G. C. Wipf, C. A. Reed, N. M. Cladel, and D. A. Galloway. 1996. Surface conformational and linear epitopes on HPV-16 and HPV-18 L1 virus-like particles as defined by monoclonal antibodies. Virology 223:174-184.
12. Christensen, N. D., R. Hopfl, S. L. DiAngelo, N. M. Cladel, S. D. Patrick, P. A. Welsh, L. R. Budgeon, C. A. Reed, and J. W. Kreider. 1994. Assembled baculovirus-expressed human papillomavirus type 11 L1 capsid protein virus-like particles are recognized by neutralizing monoclonal antibodies and induce high titres of neutralizing antibodies. J. Gen. Virol. 75:2271-2276.
13. Da Silva, D. M., D. V. Pastrana, J. T. Schiller, and W. M. Kast. 2001. Effect of preexisting neutralizing antibodies on the anti-tumor immune response induced by chimeric human papillomavirus virus-like particle vaccines. Virology 290:350-360.
14. Da Silva, D. M., J. T. Schiller, and W. M. Kast. 2003. Heterologous boosting increases immunogenicity of chimeric papillomavirus virus-like particle vaccines. Vaccine 21:3219-3227.
15. Dell, K., R. Koesters, M. Linnebacher, C. Klein, and L. Gissmann. 2006. Intranasal immunization with human papillomavirus type 16 capsomeres in the presence of non-toxic cholera toxin-based adjuvants elicits increased vaginal immunoglobulin levels. Vaccine 24:2238-2247.
16. Dupuy, C., D. Buzoni-Gatel, A. Touze, D. Bout, and P. Coursaget. 1999. Nasal immunization of mice with human papillomavirus type 16 (HPV-16) virus-like particles or with the HPV-16 L1 gene elicits specific cytotoxic T lymphocytes in vaginal draining lymph nodes. J. Virol. 73:9063-9071.
17. Fligge, C., T. Giroglou, R. E. Streeck, and M. Sapp. 2001. Induction of type-specific neutralizing antibodies by capsomeres of human papillomavirus type 33. Virology 283:353-357.
18. Gasparic, M., I. Rubio, N. Thönes, L. Gissmann, and M. Müller. 2007. Prophylactic DNA immunization against multiple papillomavirus types. Vaccine 25:4540-4553.
19. Hagensee, M. E., J. J. Carter, G. C. Wipf, and D. A. Galloway. 1995. Immunization of mice with HPV vaccinia virus recombinants generates serum IgG, IgM, and mucosal IgA antibodies. Virology 206:174-182.
20. Hagensee, M. E., N. Yaegashi, and D. A. Galloway. 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.
21. Harper, D. M., E. L. Franco, C. Wheeler, D. G. Ferris, D. Jenkins, A. Schuind, T. Zahaf, B. Innis, P. Naud, N. S. De Carvalho, C. M. Roteli-Martins, J. Teixeira, M. M. Blatter, A. P. Korn, W. Quint, and G. Dubin. 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.
22. Heidari, S., A. Vlastos, T. Ramqvist, B. Clark, B. E. Griffin, M. I. Garcia, M. Perez, P. Amati, and T. Dalianis. 2002. Immunization of T-cell deficient mice against polyomavirus infection using viral pseudocapsids or temperature sensitive mutants. Vaccine 20:1571-1578.
23. Ishii, Y., K. Tanaka, and T. Kanda. 2003. Mutational analysis of human papillomavirus type 16 major capsid protein L1: the cysteines affecting the intermolecular bonding and structure of L1-capsids. Virology 308:128-136.
24. Jegerlehner, A., T. Storni, G. Lipowsky, M. Schmid, P. Pumpens, and M. F. Bachmann. 2002. Regulation of IgG antibody responses by epitope density and CD21-mediated costimulation. Eur. J. Immunol. 32:3305-3314.
25. Kirnbauer, R., F. Booy, N. Cheng, D. R. Lowy, and J. T. Schiller. 1992. Papillomavirus L1 major capsid protein self-assembles into virus-like particles that are highly immunogenic. Proc. Natl. Acad. Sci. USA 89:12180-12184.
26. Kirnbauer, R., L. M. Chandrachud, B. W. O'Neil, E. R. Wagner, G. J. Grindlay, A. Armstrong, G. M. McGarvie, J. T. Schiller, D. R. Lowy, and M. S. Campo. 1996. Virus-like particles of bovine papillomavirus type 4 in prophylactic and therapeutic immunization. Virology 219:37-44.
27. Kirnbauer, R., J. Taub, H. Greenstone, R. Roden, M. Dürst, L. Gissmann, D. R. Lowy, and J. T. Schiller. 1993. Efficient self-assembly of human papillomavirus type 16 L1 and L1-L2 into virus-like particles. J. Virol. 67:6929-6936.
28. Leder, C., J. A. Kleinschmidt, C. Wiethe, and M. Müller. 2001. Enhancement of capsid gene expression: preparing the human papillomavirus type 16 major structural gene L1 for DNA vaccination purposes. J. Virol. 75:9201-9209.
29. Li, M., P. Beard, P. A. Estes, M. K. Lyon, and R. L. Garcea. 1998. Intercapsomeric disulfide bonds in papillomavirus assembly and disassembly. J. Virol. 72:2160-2167.
30. McLean, C. S., M. J. Churcher, J. Meinke, G. L. Smith, G. Higgins, M. Stanley, and A. C. Minson. 1990. Production and characterisation of a monoclonal antibody to human papillomavirus rype 16 using recombinant vaccinia virus. J. Clin. Pathol. 43:488-492.
31. Müller, M., and L. Gissmann. 2007. A long way: history of the prophylactic papillomavirus vaccine. Dis. Markers 23:331-336.
32. Müller, M., J. Zhou, T. D. Reed, C. Rittmüller, A. Burger, J. Gabelsberger, J. Braspenning, and L. Gissmann. 1997. Chimeric papillomavirus-like particles. Virology 234:93-111.
33. Öhlschläger, P., W. Osen, K. Dell, S. Faath, R. L. Garcea, I. Jochmus, M. Müller, M. Pawlita, K. Schäfer, P. Sehr, C. Staib, G. Sutter, and L. Gissmann. 2003. Human papillomavirus type 16 L1 capsomeres induce L1-specific cytotoxic T lymphocytes and tumor regression in C57BL/6 mice. J. Virol. 77:4635-4645.
34. Parkin, D. M., and F. Bray. 2006. Chapter 2: the burden of HPV-related cancers. Vaccine 24(Suppl. 3):S11-S25.
35. Parkin, D. M., F. Bray, J. Ferlay, and P. Pisani. 2005. Global cancer statistics, 2002. CA Cancer J. Clin. 55:74-108.
36. Pastrana, D. V., C. B. Buck, Y. Y. Pang, C. D. Thompson, P. E. Castle, P. C. FitzGerald, S. Kruger Kjaer, D. R. Lowy, and J. T. Schiller. 2004. Reactivity of human sera in a sensitive, high-throughput pseudovirus-based papillomavirus neutralization assay for HPV16 and HPV18. Virology 321:205-216.
37. Poltorak, A., X. He, I. Smirnova, M. Y. Liu, C. Van Huffel, X. Du, D. Birdwell, E. Alejos, M. Silva, C. Galanos, M. Freudenberg, P. Ricciardi-Castagnoli, B. Layton, and B. Beutler. 1998. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282: 2085-2088.
38. Rizk, R. Z., R. D. Christensen, K. M. Michael, M. Müller, P. Sehr, T. Waterboer, and M. Pawlita. 2008. Reactivity pattern of 92 monoclonal antibodies with 15 human papillomavirus types. J. Gen. Virol. 89:117-129.
39. Roden, R. B., A. Armstrong, P. Haderer, N. D. Christensen, N. L. Hubbert, D. R. Lowy, J. T. Schiller, and R. Kirnbauer. 1997. Characterization of a human papillomavirus type 16 variant-dependent neutralizing epitope. J. Virol. 71:6247-6252.
40. Rose, R. C., W. Bonnez, R. C. Reichman, and R. L. Garcea. 1993. Expression of human papillomavirus type 11 L1 protein in insect cells: in vivo and in vitro assembly of viruslike particles. J. Virol. 67:1936-1944.
41. Rose, R. C., C. Lane, S. Wilson, J. A. Suzich, E. Rybicki, and A. L. Williamson. 1999. Oral vaccination of mice with human papillomavirus virus-like particles induces systemic virus-neutralizing antibodies. Vaccine 17:2129-2135.
42. Rose, R. C., R. C. Reichman, and W. Bonnez. 1994. Human papillomavirus (HPV) type 11 recombinant virus-like particles induce the formation of neutralizing antibodies and detect HPV-specific antibodies in human sera. J. Gen. Virol. 75:2075-2079.
43. Rose, R. C., W. I. White, M. Li, J. A. Suzich, C. Lane, and R. L. Garcea. 1998. Human papillomavirus type 11 recombinant L1 capsomeres induce virus-neutralizing antibodies. J. Virol. 72:6151-6154.
44. Rossi, M., and J. W. Young. 2005. Human dendritic cells: potent antigen-presenting cells at the crossroads of innate and adaptive immunity. J. Immunol. 175:1373-1381.
45. Rudolf, M. P., J. D. Nieland, D. M. DaSilva, M. P. Velders, M. Müller, H. L. Greenstone, J. T. Schiller, and W. M. Kast. 1999. Induction of HPV16 capsid protein-specific human T cell responses by virus-like particles. Biol. Chem. 380:335-340.
46. Ryding, J., L. Dahlberg, M. Wallen-Ohman, and J. Dillner. 2007. Deletion of a major neutralizing epitope of human papillomavirus type 16 virus-like particles. J. Gen. Virol. 88:792-802.
47. Sapp, M., C. Fligge, I. Petzak, J. R. Harris, and R. E. Streeck. 1998. Papillomavirus assembly requires trimerization of the major capsid protein by disulfides between two highly conserved cysteines. J. Virol. 72:6186-6189.
48. Sasagawa, T., P. Pushko, G. Steers, S. E. Gschmeissner, M. A. Hajibagheri, J. Finch, L. Crawford, and M. Tommasino. 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.
49. Sun, S., C. Beard, R. Jaenisch, P. Jones, and J. Sprent. 1997. Mitogenicity of DNA from different organisms for murine B cells. J. Immunol. 159:3119-3125.
50. Sun, S., H. Kishimoto, and J. Sprent. 1998. DNA as an adjuvant: capacity of insect DNA and synthetic oligodeoxynucleotides to augment T cell responses to specific antigen. J. Exp. Med. 187:1145-1150.
51. Suzich, J. A., S. J. Ghim, F. J. Palmer-Hill, W. I. White, J. K. Tamura, J. A. Bell, J. A. Newsome, A. B. Jenson, and R. Schlegel. 1995. Systemic immunization with papillomavirus L1 protein completely prevents the development of viral mucosal papillomas. Proc. Natl. Acad. Sci. USA 92:11553-11557.
52. Szomolanyi-Tsuda, E., and R. M. Welsh. 1998. T-cell-independent antiviral antibody responses. Curr. Opin. Immunol. 10:431-435.
53. Thönes, N., and M. Müller. 2007. Oral immunization with different assembly forms of the HPV 16 major capsid protein L1 induces neutralizing antibodies and cytotoxic T-lymphocytes. Virology 369:375-388.
54. Villa, L. L., R. L. Costa, C. A. Petta, R. P. Andrade, J. Paavonen, O. E. Iversen, S. E. Olsson, J. Hoye, M. Steinwall, G. Riis-Johannessen, A. Andersson-Ellstrom, K. Elfgren, G. Krogh, M. Lehtinen, C. Malm, G. M. Tamms, K. Giacoletti, L. Lupinacci, R. Railkar, F. J. Taddeo, J. Bryan, M. T. Esser, H. L. Sings, A. J. Saah, and E. Barr. 2006. High sustained efficacy of a prophylactic quadrivalent human papillomavirus types 6/11/16/18 L1 virus-like particle vaccine through 5 years of follow-up. Br. J. Cancer 95:1459-1466.
55. Vlastos, A., K. Andreasson, K. Tegerstedt, D. Hollanderova, S. Heidari, J. Forstova, T. Ramqvist, and T. Dalianis. 2003. VP1 pseudocapsids, but not a glutathione-S-transferase VP1 fusion protein, prevent polyomavirus infection in a T-cell immune deficient experimental mouse model. J. Med. Virol. 70:293-300.
56. Vos, Q., A. Lees, Z. Q. Wu, C. M. Snapper, and J. J. Mond. 2000. B-cell activation by T-cell-independent type 2 antigens as an integral part of the humoral immune response to pathogenic microorganisms. Immunol. Rev. 176:154-170.
57. White, W. I., S. D. Wilson, F. J. Palmer-Hill, R. M. Woods, S. J. Ghim, L. A. Hewitt, D. M. Goldman, S. J. Burke, A. B. Jenson, S. Koenig, and J. A. Suzich. 1999. Characterization of a major neutralizing epitope on human papillomavirus type 16 L1. J. Virol. 73:4882-4889.
58. Yang, R., F. M. Murillo, H. Cui, R. Blosser, S. Uematsu, K. Takeda, S. Akira, R. P. Viscidi, and R. B. Roden. 2004. Papillomavirus-like particles stimulate murine bone marrow-derived dendritic cells to produce alpha interferon and Th1 immune responses via MyD88. J. Virol. 78:11152-11160.
59. Yang, R., F. M. Murillo, M. J. Delannoy, R. L. Blosser, W. H. t. Yutzy, S. Uematsu, K. Takeda, S. Akira, R. P. Viscidi, and R. B. Roden. 2005. B lymphocyte activation by human papillomavirus-like particles directly induces Ig class switch recombination via TLR4-MyD88. J. Immunol. 174: 7912-7919.
60. Yuan, H., P. A. Estes, Y. Chen, J. Newsome, V. A. Olcese, R. L. Garcea, and R. Schlegel. 2001. Immunization with a pentameric L1 fusion protein protects against papillomavirus infection. J. Virol. 75:7848-7853.
61. Zinkernagel, R. M., and H. Hengartner. 2001. Regulation of the immune response by antigen. Science 293:251-253.
62. Zolotukhin, S., M. Potter, W. W. Hauswirth, J. Guy, and N. Muzyczka. 1996. A "humanized" green fluorescent protein cDNA adapted for high-level expression in mammalian cells. J. Virol. 70:4646-4654.