Protection of rabbits against challenge with rabbit papillomaviruses by immunization with the N terminus of human papillomavirus type 16 minor capsid antigen L2

Journal of Virology

Volumn 81, Issue 21, 2007, Pages 11585-11592

  Gambhira, Ratish ^a   Jagu, Subhashini ^a   Karanam, Balasubramanyam ^a   Gravitt, Patti E ^b   Culp, Timothy D ^c   Christensen, Neil D ^c   Roden, Richard B S ^a,b  

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

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC DNA; IMMUNOLOGICAL ADJUVANT; NEUTRALIZING ANTIBODY; VIRUS ANTIGEN; VIRUS PROTEIN;

ARTICLE; COTTONTAIL RABBIT PAPILLOMAVIRUS; GENE EXPRESSION; HUMAN PAPILLOMAVIRUS TYPE 16; IMMUNE RESPONSE; IMMUNIZATION; INFECTION PREVENTION; NONHUMAN; PAPILLOMA; PRIORITY JOURNAL; RABBIT; VACCINATION; VIRUS CAPSID;

ANIMALS; CAPSID PROTEINS; DNA, VIRAL; FEMALE; GENOTYPE; NEUTRALIZATION TESTS; ONCOGENE PROTEINS, VIRAL; PAPILLOMA; PAPILLOMAVIRIDAE; PEPTIDES; PROTEIN STRUCTURE, TERTIARY; RABBITS; SKIN; UTERINE CERVICAL NEOPLASMS; VIRAL VACCINES;

BOVINE PAPILLOMAVIRUS TYPE 1; COTTONTAIL RABBIT PAPILLOMAVIRUS; HUMAN PAPILLOMAVIRUS; HUMAN PAPILLOMAVIRUS TYPE 16; MIRIDAE; ORYCTOLAGUS CUNICULUS; PAPILLOMAVIRIDAE; RABBIT ORAL PAPILLOMAVIRUS;

EID: 35448929981     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01577-07     Document Type: Article

References (43)

1. Breitburd, F., R. Kirnbauer, N. L. Hubbert, B. Nonnenmacher, C. TrinDinh-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.
2. Campo, M. S. 1997. Vaccination against papillomavirus in cattle. Clin. Dermatol. 15:275-283.
3. 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.
4. 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.
5. Christensen, N. D., N. M. Cladel, C. A. Reed, L. R. Budgeon, P. A. Welsh, S. D. Patrick, and J. W. Kreiden 1996. Laboratory production of infectious stocks of rabbit oral papillomavirus. J. Gen. Virol. 77:1793-1798.
6. Christensen, N. D., and J. W. Kreider. 1990. Antibody-mediated neutralization in vivo of infectious papillomaviruses. J. Virol. 64:3151-3156.
7. Christensen, N. D., J. W. Kreider, N. C. Kan, and S. L. DiAngelo. 1991. The open reading frame L2 of cottontail rabbit papillomavirus contains antibody-inducing neutralizing epitopes. Virology 181:572-579.
8. Christensen, N. D., C. A. Reed, N. M. Cladel, K. Hall, and G. S. Leiserowitz. 1996. 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. de Villiers, E. M., C. Fauquet, T. R. Broker, H. U. Bernard, and H. zur Hausen. 2004. Classification of papillomaviruses. Virology 324:17-27.
10. 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 12, the minor capsid protein. J. Virol. 76:9798-9805.
11. Gambhira, R., P. E. Gravitt, I. Bossis, P. L. Stern, R. P. Viscidi, and R. B. Roden. 2006. Vaccination of healthy volunteers with human papillomavirus type 16 L2E7E6 fusion protein induces serum antibody that neutralizes across papillomavirus species. Cancer Res. 66:11120-11124.
12. 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.
13. 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. RoteliMartins, 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.
14. 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.
15. Hu, J., N. M. Cladel, L. R. Budgeon, C. A. Reed, M. D. Pickel, and N. D. Christensen. 2006. Protective cell-mediated immunity by DNA vaccination against Papillomavirus L1 capsid protein in the cottontail rabbit papillomavirus model. Viral Immunol. 19:492-507.
16. Kawana, K., Y. Kawana, H. Yoshikawa, Y. Taketani, K. Yoshiike, and T. Kanda. 2001. Nasal immunization of mice with peptide having a cross-neutralization epitope on minor capsid protein L2 of human papillomavirus type 16 elicit systemic and mucosal antibodies. Vaccine 19:1496-1502.
17. 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.
18. Kawana, Y., K. Kawana, H. Yoshikawa, Y. Taketani, K. Yoshiike, and T. Kanda. 2001. Human papillomavirus type 16 minor capsid protein L2 N-terminal region containing a common neutralization epitope binds to the cell surface and enters the cytoplasm. J. Virol. 75:2331-2336.
19. 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.
20. Knowles, G., G. J. Grindlay, M. S. Campo, L. M. Chandrachud, and B. W. O'Neil. 1997. Linear B-cell epitopes in the N terminus of L2 of bovine papillomavirus type 4. Res. Vet. Sci. 62:289-291.
21. Koutsky, L. A., K. A. Ault, C. M. Wheeler, D. R. Brown, E. Barr, F. B. Alvarez, L. M. Chiacchierini, and K. U. Jansen. 2002. A controlled trial of a human papillomavirus type 16 vaccine. N. Engl. J. Med. 347:1645-1651.
22. Lin, Y. L., L. A. Borenstein, R. Selvakumar, R. Ahmed, and F. O. Wettstein. 1992. Effective vaccination against papilloma development by immunization with L1 or L2 structural protein of cottontail rabbit papillomavirus. Virology 187:612-619.
23. Mao, C., L. A. Koutsky, K. A. Ault, C. M. Wheeler, D. R. Brown, D. J. Wiley, F. B. Alvarez, O. M. Bautista, K. U. Jansen, and E. Barr. 2006. Efficacy of human papillomavirus-16 vaccine to prevent cervical intraepithelial neoplasia: a randomized controlled trial. Obstet. Gynecol. 107:18-27.
24. 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.
25. Nardelli-Haefliger, D., R. Roden, C. Balmelli, A. Potts, J. Schiller, and P. De Grandi. 1999. Mucosal but not parenteral immunization with purified human papillomavirus type 16 virus-like particles induces neutralizing titers of antibodies throughout the estrous cycle of mice. J. Virol. 73:9609-9613.
26. Paavonen, J., D. Jenkins, F. X. Bosch, P. Naud, J. Salmeron, C. M. Wheeler, S. N. Chow, D. L. Apter, H. C. Kitchener, X. Castellsague, N. S. de Carvalho, S. R. Skinner, D. M. Harper, J. A. Hedrick, U. Jaisamrarn, G. A. Limson, M. Dionne, W. Quint, B. Spiessens, P. Peeters, F. Struyf, S. L. Wieting, M. O. Lehtinen, and G. Dubin. 2007. Efficacy of a prophylactic adjuvanted bivalent L1 virus-like-particle vaccine against infection with human papillomavirus types 16 and 18 in young women: an interim analysis of a phase III double-blind, randomised controlled trial. Lancet 369:2161-2170.
27. Palmer, K. E., A. Benko, S. A. Doucette, T. I. Cameron, T. Foster, K. M. Hanley, A. A. McCormick, M. McCulloch, G. P. Pogue, M. L. Smith, and N. D. Christensen. 2006. Protection of rabbits against cutaneous papillomavirus infection using recombinant tobacco mosaic virus containing L2 capsid epitopes. Vaccine 24:5516-5525.
28. 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.
29. 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.
30. 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.
31. Roden, R., and T. C. Wu. 2006. How will HPV vaccines affect cervical cancer? Nat. Rev. Cancer 6:753-763.
32. Roden, R. B., H. L. Greenstone, R. Kirnbauer, F. P. Booy, J. Jessie, D. R. Lowy, and J. T. Schiller. 1996. In vitro generation and type-specific neutralization of a human papillomavirus type 16 virion pseudotype. J. Virol. 70:5875-5883.
33. Roden, R. B., N. L. Hubbert, R. Kirnbauer, N. D. Christensen, D. R. Lowy, and J. T. Schiller. 1996. Assessment of the serological relatedness of genital human papillomaviruses by hemagglutination inhibition. J. Virol. 70:3298-3301.
34. Roden, R. B., W. I. 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.
35. 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.
36. 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.
37. 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.
38. 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.
39. 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.
40. Viscidi, R. P., B. Snyder, S. Cu-Uvin, J. W. Hogan, B. Clayman, R. S. Klein, J. Sobel, and K. V. Shah. 2005. Human papillomavirus capsid antibody response to natural infection and risk of subsequent HPV infection in HIV-positive and HIV-negative women. Cancer Epidemiol. Biomarkers Prev. 14:283-288.
41. Walboomers, J. M., M. V. Jacobs, M. M. Manos, F. X. Bosch, J. A. Kummer, K. V. Shah, P. J. Snijders, J. Peto, C. J. Meijer, and N. Munoz. 1999. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J. Pathol. 189:12-19.
42. Yang, R., P. M. Day, W. H. T. Yutzy, K. Y. Lin, C. F. Hung, and R. B. Roden. 2003. Cell surface-binding motifs of L2 that facilitate papillomavirus infection. J. Virol. 77:3531-3541.
43. Yang, R., W. H. T. Yutzy, R. P. Viscidi, and R. B. Roden. 2003. Interaction of L2 with beta-actin directs intracellular transport of papillomavirus and infection. J. Biol. Chem. 278:12546-12553.