Chimeric L1-L2 virus-like particles as potential broad-spectrum human papillomavirus vaccines

Journal of Virology

Volumn 83, Issue 19, 2009, Pages 10085-10095

  Schellenbacher, Christina ^a   Roden, Richard ^b   Kirnbauer, Reinhard ^a  

^a Universitatsklinik fur Dermatologie   (Austria)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALUMINUM HYDROXIDE; AMINO ACID DERIVATIVE; CAPSID PROTEIN; CAPSID PROTEIN L1; CAPSID PROTEIN L2; DODECYL SULFATE SODIUM; EPITOPE; FREUND ADJUVANT; NEUTRALIZING ANTIBODY; PHOSPHORYL LIPID A; UNCLASSIFIED DRUG; VIRUS FUSION PROTEIN; WART VIRUS VACCINE;

ANIMAL EXPERIMENT; ANTIBODY SPECIFICITY; ANTIBODY TITER; ARTICLE; CHIMERA; CONTROLLED STUDY; GENETIC ENGINEERING; HUMAN PAPILLOMAVIRUS TYPE 11; HUMAN PAPILLOMAVIRUS TYPE 16; HUMAN PAPILLOMAVIRUS TYPE 18; HUMAN PAPILLOMAVIRUS TYPE 6; IMMUNIZATION; IMMUNOGENICITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; RABBIT; VACCINATION; VIRION; VIRUS LIKE AGENT;

ANIMALS; BACULOVIRIDAE; CAPSID; CAPSID PROTEINS; EPITOPES; MICE; MICE, INBRED BALB C; MICROSCOPY, ELECTRON, TRANSMISSION; ONCOGENE PROTEINS, VIRAL; PAPILLOMAVIRUS VACCINES; PEPTIDES; PROTEIN STRUCTURE, TERTIARY; RABBITS; RECOMBINANT FUSION PROTEINS; RISK;

BOVINE PAPILLOMAVIRUS TYPE 1; HUMAN PAPILLOMAVIRUS; MIRIDAE; MUS; ORYCTOLAGUS CUNICULUS;

EID: 70349299873     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01088-09     Document Type: Article

References (50)

1. Alphs, H. H., R. Gambhira, B. Karanam, J. N. Roberts, S. Jagu, J. T. Schiller, W. Zeng, D. C. Jackson, and R. B. Roden. 2008. Protection against heterologous human papillomavirus challenge by a synthetic lipopeptide vaccine containing a broadly cross-neutralizing epitope of L2. Proc. Natl. Acad. Sci. USA 105:5850-5855.
2. Bachmann, M. F., and R. M. Zinkernagel. 1997. Neutralizing antiviral B cell responses. Annu. Rev. Immunol. 15:235-270.
3. Brown, D. R., S. K. Kjaer, K. Sigurdsson, O. E. Iversen, M. Hernandez-Avila, C. M. Wheeler, G. Perez, L. A. Koutsky, E. H. Tay, P. Garcia, K. A. Ault, S. M. Garland, S. Leodolter, S. E. Olsson, G. W. Tang, D. G. Ferris, J. Paavonen, M. Steben, F. X. Bosch, J. Dillner, E. A. Joura, R. J. Kurman, S. Majewski, N. Munoz, E. R. Myers, L. L. Villa, F. J. Taddeo, C. Roberts, A. Tadesse, J. Bryan, L. C. Lupinacci, K. E. Giacoletti, H. L. Sings, M. James, T. M. Hesley, and E. Barr. 2009. The impact of quadrivalent human papillomavirus (HPV; types 6, 11, 16, and 18) L1 virus-like particle vaccine on infection and disease due to oncogenic nonvaccine HPV types in generally HPV-naive women aged 16-26 years. J. Infect. Dis. 199:926-935.
4. Buck, C. B., D. V. Pastrana, D. R. Lowy, and J. T. Schiller. 2005. Generation of HPV pseudovirions using transfection and their use in neutralization assays. Methods Mol. Med. 119:445-462.
5. Campo, M. S., B. W. O'Neil, G. J. Grindlay, F. Curtis, G. Knowles, and L. Chandrachud. 1997. A peptide encoding a B-cell epitope from the N-terminus of the capsid protein L2 of bovine papillomavirus-4 prevents disease. Virology 234:261-266.
6. Carter, J. J., M. B. Hagensee, S. K. Lee, B. McKnight, L. A. Koutsky, and D. A. Galloway. 1994. Use of HPV 1 capsids produced by recombinant vaccinia viruses in an ELISA to detect serum antibodies in people with foot warts. Virology 199:284-291.
7. Chackerian, B. 2007. Virus-like particles: flexible platforms for vaccine development. Expert Rev. Vaccines 6:381-390. (Pubitemid 46911601)
8. Chackerian, B., P. Lenz, D. R. Lowy, and J. T. Schiller. 2002. Determinants of autoantibody induction by conjugated papillomavirus virus-like particles. J. Immunol. 169:6120-6126. (Pubitemid 36903455)
9. Chandrachud, L. M., G. J. Grindlay, G. M. McGarvie, B. W. O'Neil, E. R. Wagner, W. F. Jarrett, and M. S. Campo. 1995. Vaccination of cattle with the N-terminus of L2 is necessary and sufficient for preventing infection by bovine papillomavirus-4. Virology 211:204-208.
10. Chen, X. S., R. L. Garcea, I. Goldberg, G. Casini, and S. C. Harrison. 2000. Structure of small virus-like particles assembled from the L1 protein of human papillomavirus 16. Mol. Cell 5:557-567. (Pubitemid 30950045)
11. 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.
12. Christensen, N. D., and J. W. Kreider. 1990. Antibody-mediated neutralization in vivo of infectious papillomaviruses. J. Virol. 64:3151-3156. (Pubitemid 20219515)
13. Culp, T. D., and N. D. Christensen. 2004. Kinetics of in vitro adsorption and entry of papillomavirus virions. Virology 319:152-161.
14. de Villiers, E. M., C. Fauquet, T. R. Broker, H. U. Bernard, and H. zur Hausen. 2004. Classification of papillomaviruses. Virology 324:17-27.
15. Embers, M. E., L. R. Budgeon, T. D. Culp, C. A. Reed, M. D. Pickel, and N. D. Christensen. 2004. Differential antibody responses to a distinct region of human papillomavirus minor capsid proteins. Vaccine 22:670-680.
16. Embers, M. E., L. R. Budgeon, M. Pickel, and N. D. Christensen. 2002. Protective immunity to rabbit oral and cutaneous papillomaviruses by immunization with short peptides of L2, the minor capsid protein. J. Virol. 76:9798-9805.
17. Gambhira, R., S. Jagu, B. Karanam, P. E. Gravitt, T. D. Culp, N. D. Christensen, and R. B. S. Roden. 2007. Protection of rabbits against challenge with rabbit papillomaviruses by immunization with the N terminus of human papillomavirus type 16 minor capsid antigen L2. J. Virol. 81:11585-11592. (Pubitemid 47623790)
18. Gambhira, R., B. Karanam, S. Jagu, J. N. Roberts, C. B. Buck, I. Bossis, H. Alphs, T. Culp, N. D. Christensen, and R. B. S. Roden. 2007. A protective and broadly cross-neutralizing epitope of human papillomavirus L2. J. Virol. 81:13927-13931. (Pubitemid 350247886)
19. Gaukroger, J. M., L. M. Chandrachud, B. W. O'Neil, G. J. Grindlay, G. Knowles, and M. S. Campo. 1996. Vaccination of cattle with bovine papillomavirus type 4 L2 elicits the production of virus-neutralizing antibodies. J. Gen. Virol. 77:1577-1583.
20. Giannini, S. L., E. Hanon, P. Moris, M. Van Mechelen, S. Morel, F. Dessy, M. A. Fourneau, B. Colau, J. Suzich, G. Losonksy, M. T. Martin, G. Dubin, and M. A. Wettendorff. 2006. Enhanced humoral and memory B cellular immunity using HPV16/18 L1 VLP vaccine formulated with the MPL/aluminium salt combination (AS04) compared to aluminium salt only. Vaccine 24:5937-5949.
21. Handisurya, A., S. Gilch, D. Winter, S. Shafti-Keramat, D. Maurer, H. M. Schatzl, and R. Kirnbauer. 2007. Vaccination with prion peptide-displaying papillomavirus-like particles induces autoantibodies to normal prion protein that interfere with pathologic prion protein production in infected cells. FEBS J. 274:1747-1758. (Pubitemid 46426909)
22. Harper, D. M., E. L. Franco, C. M. Wheeler, A. B. Moscicki, B. Romanowski, C. M. Roteli-Martins, D. Jenkins, A. Schuind, S. A. Costa Clemens, and G. Dubin. 2006. Sustained efficacy up to 4.5 years of a bivalent L1 virus-like particle vaccine against human papillomavirus types 16 and 18: follow-up from a randomised control trial. Lancet 367:1247-1255.
23. Hu, D., and S. Goldie. 2008. The economic burden of noncervical human papillomavirus disease in the United States. Am. J. Obstet. Gynecol. 198:500.e1-7
24. Kawana, K., K. Matsumoto, H. Yoshikawa, Y. Taketani, T. Kawana, K. Yoshiike, and T. Kanda. 1998. A surface immunodeterminant of human papillomavirus type 16 minor capsid protein L2. Virology 245:353-359. (Pubitemid 28394198)
25. Kawana, K., H. Yoshikawa, Y. Taketani, K. Yoshiike, and T. Kanda. 1999. Common neutralization epitope in minor capsid protein L2 of human papillomavirus types 16 and 6. J. Virol. 73:6188-6190. (Pubitemid 29274916)
26. 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.
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. (Pubitemid 23343814)
28. Kondo, K., Y. Ishii, H. Ochi, T. Matsumoto, H. Yoshikawa, and T. Kanda. 2007. Neutralization of HPV16, 18, 31, and 58 pseudovirions with antisera induced by immunizing rabbits with synthetic peptides representing segments of the HPV16 minor capsid protein L2 surface region. Virology 358:266-272.
29. Kondo, K., H. Ochi, T. Matsumoto, H. Yoshikawa, and T. Kanda. 2008. Modification of human papillomavirus-like particle vaccine by insertion of the cross-reactive L2-epitopes. J. Med. Virol. 80:841-846.
30. Lenz, P., P. M. Day, Y. Y. Pang, S. A. Frye, P. N. Jensen, D. R. Lowy, and J. T. Schiller. 2001. Papillomavirus-like particles induce acute activation of dendritic cells. J. Immunol. 166:5346-5355. (Pubitemid 32374153)
31. McCarthy, M. P., W. I. White, F. Palmer Hill, S. Koenig, and J. A. Suzich. 1998. Quantitative disassembly and reassembly of human papillomavirus type 11 viruslike particles in vitro. J. Virol. 72:32-41.
32. Munoz, N., F. X. Bosch, X. Castellsague, M. Diaz, S. de Sanjose, D. Hammouda, K. V. Shah, and C. J. Meijer. 2004. Against which human papillomavirus types shall we vaccinate and screen? The international perspective. Int. J. Cancer 111:278-285. (Pubitemid 38924707)
33. Pastrana, D. V., R. Gambhira, C. B. Buck, Y. Y. Pang, C. D. Thompson, T. D. Culp, N. D. Christensen, D. R. Lowy, J. T. Schiller, and R. B. Roden. 2005. Cross-neutralization of cutaneous and mucosal Papillomavirus types with anti-sera to the amino terminus of L2. Virology 337:365-372.
34. Pinto, L. A., J. Edwards, P. E. Castle, C. D. Harro, D. R. Lowy, J. T. Schiller, D. Wallace, W. Kopp, J. W. Adelsberger, M. W. Baseler, J. A. Berzofsky, and A. Hildesheim. 2003. Cellular immune responses to human papillomavirus (HPV)-16 L1 in healthy volunteers immunized with recombinant HPV-16 L1 virus-like particles. J. Infect. Dis. 188:327-338.
35. Richards, R. M., D. R. Lowy, J. T. Schiller, and P. M. Day. 2006. Cleavage of the papillomavirus minor capsid protein, L2, at a furin consensus site is necessary for infection. Proc. Natl. Acad. Sci. USA 103:1522-1527.
36. Roberts, J. N., C. B. Buck, C. D. Thompson, R. Kines, M. Bernardo, P. L. Choyke, D. R. Lowy, and J. T. Schiller. 2007. Genital transmission of HPV in a mouse model is potentiated by nonoxynol-9 and inhibited by carrageenan. Nat. Med. 13:857-861.
37. Roden, R. B. S., E. M. Weissinger, D. W. Henderson, F. Booy, R. Kirnbauer, J. F. Mushinski, D. R. Lowy, and J. T. Schiller. 1994. Neutralization of bovine papillomavirus by antibodies to L1 and L2 capsid proteins. J. Virol. 68:7570-7574.
38. Roden, R. B. S., W. H. Yutzy, R. Fallon, S. Inglis, D. R. Lowy, and J. T. Schiller. 2000. Minor capsid protein of human genital papillomaviruses contains subdominant, cross-neutralizing epitopes. Virology 270:254-257.
39. Rose, R. C., W. Bonnez, C. Da Rin, D. J. McCance, and R. C. Reichman. 1994. Serological differentiation of human papillomavirus types 11, 16 and 18 using recombinant virus-like particles. J. Gen. Virol. 75:2445-2449.
40. Rubio, I., A. Bolchi, N. Moretto, E. Canali, L. Gissmann, M. Tommasino, M. Muller, and S. Ottonello. 2009. Potent anti-HPV immune responses induced by tandem repeats of the HPV16 L2 (20-38) peptide displayed on bacterial thioredoxin. Vaccine 27:1949-1956.
41. Rudolf, M. P., S. C. Fausch, D. M. Da Silva, and W. M. Kast. 2001. Human dendritic cells are activated by chimeric human papillomavirus type-16 virus-like particles and induce epitope-specific human T cell responses in vitro. J. Immunol. 166:5917-5924.
42. Slupetzky, K., R. Gambhira, T. D. Culp, S. Shafti-Keramat, C. Schellenbacher, N. D. Christensen, R. B. Roden, and R. Kirnbauer. 2007. A papillomavirus-like particle (VLP) vaccine displaying HPV16 L2 epitopes induces cross-neutralizing antibodies to HPV11. Vaccine 25:2001-2010. (Pubitemid 46227679)
43. Slupetzky, K., S. Shafti-Keramat, P. Lenz, S. Brandt, A. Grassauer, M. Sara, and R. Kirnbauer. 2001. Chimeric papillomavirus-like particles expressing a foreign epitope on capsid surface loops. J. Gen. Virol. 82:2799-2804.
44. Suzich, J. A., S. Ghim, F. J. Palmer-Hill, W. I. White, J. K. Tamura, J. 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.
45. Thones, N., A. Herreiner, L. Schädlich, K. Piuko, and M. Müller. 2008. 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. J. Virol. 82:5472-5485. (Pubitemid 351705254)
46. Villa, L. L., R. L. Costa, C. A. Petta, R. P. Andrade, K. A. Ault, A. R. Giuliano, C. M. Wheeler, L. A. Koutsky, C. Malm, M. Lehtinen, F. E. Skjeldestad, S. E. Olsson, M. Steinwall, D. R. Brown, R. J. Kurman, B. M. Ronnett, M. H. Stoler, A. Ferenczy, D. M. Harper, G. M. Tamms, J. Yu, L. Lupinacci, R. Railkar, F. J. Taddeo, K. U. Jansen, M. T. Esser, H. L. Sings, A. J. Saah, and E. Barr. 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.
47. Wheeler, C. M., S. K. Kjaer, K. Sigurdsson, O. E. Iversen, M. Hernandez-Avila, G. Perez, D. R. Brown, L. A. Koutsky, E. H. Tay, P. Garcia, K. A. Ault, S. M. Garland, S. Leodolter, S. E. Olsson, G. W. Tang, D. G. Ferris, J. Paavonen, M. Steben, F. X. Bosch, J. Dillner, E. A. Joura, R. J. Kurman, S. Majewski, N. Munoz, E. R. Myers, L. L. Villa, F. J. Taddeo, C. Roberts, A. Tadesse, J. Bryan, L. C. Lupinacci, K. E. Giacoletti, M. James, S. Vuocolo, T. M. Hesley, and E. Barr. 2009. The impact of quadrivalent human papillomavirus (HPV; types 6, 11, 16, and 18) L1 virus-like particle vaccine on infection and disease due to oncogenic nonvaccine HPV types in sexually active women aged 16-26 years. J. Infect. Dis. 199:936-944.
48. Yang, R., P. M. Day, W. H. Yutzy IV, K.-Y. Lin, C.-F. Hung, and R. B. S. Roden. 2003. Cell surface-binding motifs of L2 that facilitate papillomavirus infection. J. Virol. 77:3531-3541. (Pubitemid 36297272)
49. Yang, R., F. M. Murillo, K. Y. Lin, W. H. Yutzy IV, S. Uematsu, K. Takeda, S. Akira, R. P. Viscidi, and R. B. Roden. 2004. Human papillomavirus type-16 virus-like particles activate complementary defense responses in key dendritic cell subpopulations. J. Immunol. 173:2624-2631. (Pubitemid 39063122)
50. Zamora, E., A. Handisurya, S. Shafti-Keramat, D. Borchelt, G. Rudow, K. Conant, C. Cox, J. C. Troncoso, and R. Kirnbauer. 2006. Papillomavirus-like particles are an effective platform for amyloid-beta immunization in rabbits and transgenic mice. J. Immunol. 177:2662-2670. (Pubitemid 44201025)