Human papillomavirus type 16 L1 capsomeres induce L1-specific cytotoxic T lymphocytes and tumor regression in C57BL/6 mice

Journal of Virology

Volumn 77, Issue 8, 2003, Pages 4635-4645

  Öhischläger, Peter ^a   Osen, Wolfram ^a   Dell, Kerstin ^a   Faath, Stefan ^a,d   Garcea, Robert L ^c   Jochmus, Ingrid ^a,d   Müller, Martin ^a   Pawlita, Michael ^a   Schäfer, Klaus ^a,e   Sehr, Peter ^a   Staib, Caroline ^b   Sutter, Gerd ^b   Gissmann, Lutz ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

^c UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^d MediGene AG   (Germany)

^e SANOFI AVENTIS DEUTSCHLAND GMBH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALANYLGLYCYLVALYLASPARTYLASPARAGINYLARGINYLGLUTAMYLCYSTEINYLISOLEUCINE; BACTERIUM LIPOPOLYSACCHARIDE; ENDOTOXIN; EPITOPE; GLUTATHIONE TRANSFERASE; HYBRID PROTEIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PEPTIDE FRAGMENT; STRUCTURAL PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ANTIGEN BINDING; ARTICLE; CELLULAR IMMUNITY; CHROMIUM 51 RELEASE; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DOSE RESPONSE; ENZYME LINKED IMMUNOSPOT ASSAY; ESCHERICHIA COLI; IMMUNIZATION; IMMUNOASSAY; IMMUNOGENICITY; IMMUNOSTIMULATION; MOLECULAR WEIGHT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN PURIFICATION; SEDIMENTATION; SEQUENCE ANALYSIS; SPLEEN CELL; TUMOR REGRESSION; VIRUS PARTICLE; WART VIRUS;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, VIRAL; CAPSID PROTEINS; CELL LINE; EPITOPES, T-LYMPHOCYTE; HUMANS; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; NEOPLASMS, EXPERIMENTAL; ONCOGENE PROTEINS, VIRAL; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTIONS; PEPTIDES; T-LYMPHOCYTES, CYTOTOXIC; TUMOR VIRUS INFECTIONS; VACCINATION; VIRAL VACCINES;

EID: 0344406986     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.77.8.4635-4645.2003     Document Type: Article

References (51)

1. Balmelli, C., R. Roden, A. Potts, J. Schiller, P. De Grandi, and D. NardelliHaefliger. 1998. Nasal immunization of mice with human papillomavirus type 16 virus-like particles elicits neutralizing antibodies in mucosal secretions. J. Virol. 72:8220-8229.
2. Bousarghin, L., A. L. Combita-Rojas, A. Touze, S. El Mehdaoui, P. Y. Sizaret, M. M. Bravo, and P. Coursaget. 2002. Detection of neutralizing antibodies against human papillomaviruses (HPV) by inhibition of gene transfer mediated by HPV pseudovirions. J. Clin. Microbiol. 40:926-932.
3. Breitburd, F., and P. Coursaget. 1999. Human papillomavirus vaccines. Semin. Cancer Biol. 9:431-444.
4. 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 virus-like particles from cottontail rabbit papillomavirus (CRPV) can protect against experimental CRPV infection. J. Virol. 69:3959-3963.
5. Brown, D. R., J. T. Bryan, J. M. Schroeder, T. S. Robinson, K. H. Fife, C. M. Wheeler, E. Barr, P. R. Smith, L. Chiacchierini, A. DiCello, and K. U. Jansen. 2001. Neutralization of human papillomavirus type 11 (HPV-11) by serum from women vaccinated with yeast-derived HPV-11 L1 virus-like particles: correlation with competitive radioimmunoassay titer. J. Infect. Dis. 184:1183-1186.
6. Chen, Y., G. Casini, S. C. Harrison, and R. L. Garcea. 2001. Papiliomavirus capsid protein expression in Escherichia coli: purification and assembly of HPV11 and HPV16 L1. J. Mol. Biol. 307:173-182.
7. Chen, Y., 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.
8. Da Silva, D. M., G. L. Eiben, S. C. Fausch, M. T. Wakabayashi, M. P. Rudolf, M. P. Velders, and W. M. Kast. 2001. Cervical cancer vaccines: emerging concepts and developments. J. Cell. Physiol. 186:169-182.
9. De Bruijn, M. L., H. L. Greenstone, H. Vermeulen, C. J. Melief, D. R. Lowy, J. T. Schiller, and W. M. Kast. 1998. L1-specific protection from tumor challenge elicited by HPV16 virus-like particles. Virology 250:371-376.
10. 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.
11. Evans, S. W., T. Feizi, R. Childs, and N. R. Ling. 1983. Monoclonal antibody against a cross-reactive idiotypic determinant found on human autoantibodies with anti-I and -i specificities. Mol. Immunol. 20:1127-1131.
12. Feltkamp, M. C., H. L. Smits, M. P. Vierboom, R. P. Minnaar, B. M. de Jongh, J. W. Drijfhout, J. ter Schegget, C. J. Melief, and W. M. Kast. 1993. Vaccination with cytotoxic T lymphocyte epitope-containing peptide protects against a tumor induced by human papillomavirus type 16-transformed cells. Eur. J. Immunol. 23:2242-2249.
13. 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.
14. Gissmann, L., W. Osen, M. Mfiller, and 1. Jochmus. 2001. Therapeutic vaccines for human papillomaviruses, Intervirology 44:167-175.
15. Greenstone, H. L., J. D. Nieland, K. E. de Visser, M. L. De Bruijn, R. Kirnbauer, R. B. Roden, D. R. Lowy, W. M. Kast, and J. T. Schiller. 1998. Chimeric papillomavirus virus-like particles elicit antitumor immunity against the E7 oncoprotein in an HPV16 tumor model. Proc. Natl. Acad. Sci. USA 95:1800-1805.
16. Harro, C. D., Y. Y. Pang, R. B. Roden, A. Hildesheim, Z. Wang, M. J. Reynolds, T. C. Mast, R. Robinson, B. R. Murphy, R. A. Karron, J. Dillner, J. T. Schiller, and D. R. Lowy. 2001. Safety and immunogenicity trial in adult volunteers of a human papillomavirus 16 L1 virus-like particle vaccine. J. Natl. Cancer Inst. 93:284-292.
17. Jochmus, I., K. Schfifer, S. Faath, M. Muller, and L. Gissmann. 1999. Chimeric virus-like particles of the human papillomavirus type 16 (HPV 16) as a prophylactic and therapeutic vaccine. Arch. Med. Res. 30:269-274.
18. Kawana, K., Y. Kawana, H. Yoshikawa, Y. Taketani, K. Yoshiike, and T. Kanda. 2001. Nasal immunization of mice with peptide having a crossneutralization epitope on minor capsid protein L2 of human papillomavirus type 16 elicit systemic and mucosal antibodies. Vaccine 19:1496-1502.
19. 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.
20. Lemke, H., G. J. Hämmerling, and U. Hämmerling. 1979. Fine specificity analysis with monoclonal antibodies of antigens controlled by the major histocompatibility complex and by the Qa/TL region in mice. Immunol. Rev. 47:175-206.
21. 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.
22. Levin, J., and F. B. Bang. 1968. Clottable protein in Limulus: its localization and kinetics of its coagulation by endotoxin. Thromb. Diath. Haemorrh. 19:186-197.
23. Li, M., T. P. Cripe, P. A. Estes, M. K. Lyon, R. C. Rose, and R. L. Garcea. 1997. Expression of the human papillomavirus type 11 L1 capsid protein in Escherichia coli: characterization of protein domains involved in DNA binding and capsid assembly. J. Virol. 71:2988-2995.
24. Liu, X. S., W. J. Liu, K. N. Zhao, Y. H. Liu, G. Leggatt, and I. H. Frazer. 2002. Route of administration of chimeric BPV1 VLP determines the character of the induced immune responses. Immunol. Cell Biol. 80:21-29.
25. Ljunggren, H. G., and K. Kärre. 1985. Host resistance directed selectively against H-2-deficient lymphoma variants. Analysis of the mechanism. J. Exp. Med. 162:1745-1759.
26. Matsuguchi, T., T. Musikacharoen, T. Ogawa, and Y. Yoshikai. 2000. Gene expressions of Toll-like receptor 2, but not Toll-like receptor 4, is induced by LPS and inflammatory cytokines in mouse macrophages. J. Immunol. 165: 5767-5772.
27. McCarthy, M. P., W. I. White, F. Palmer-Hill, S. Koenig, and J. Suzich. 1998. Quantitative disassembly and reassembly of human papillomavirus type 11 virus-like particles in vitro. J. Virol. 72:32-41.
28. Michel, N., P. Öhlschläger, W. Osen, E.-J. Freyschmidt, H. Guthöhrlein, A. M. Kaufmann, M. Müller, and L. Gissmann. 2002. T cell response to human papillomavirus 16 E7 in mice: comparison of Cr release assay, intracellular IFN-gamma production, ELISPOT and tetramer staining. Intervirology 45:290-299.
29. Molvig, J., and L. Baek. 1987. Removal of endotoxin from culture media by a polymyxin B sepharose column. The activity of contaminating endotoxin in culture media measured by the interleukin 1 inducing effect on human monocyte cultures and by the Limulus test. Scand. J. Immunol. 26:611-619.
30. Müller, M., J. Zhou, T. D. Reed, C. Rittmuller, A. Burger, J. Gabelsberger, J. Braspenning, and L. Gissmann. 1997. Chimeric papillomavirus-like particles. Virology 234:93-111.
31. 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.
32. Nieland, J. D., D. M. Da Silva, M. P. Velders, K. E. de Visser, J. T. Schiller, M. Müller, and W. M. Kast. 1999. Chimeric papillomavirus virus-like particles induce a murine self-antigen-specific protective and therapeutic antitumor immune response. J. Cell. Biochem. 73:145-152.
33. Paintsil, J., M. Müller, M. Picken, L. Gissmann, and J. Zhou. 1998. Calcium is required in reassembly of bovine papillomavirus in vitro. J. Gen. Virol. 79:1133-1141.
34. Parkin, D. M., P. Pisani, and J. Ferlay. 1999. Estimates of the worldwide incidence of 25 major cancers in 1990. Int. J. Cancer 80:827-841.
35. Pastrana, D. V., W. C. Vass, D. R. Lowy, and J. T. Schiller. 2001. NHPV16 VLP vaccine induces human antibodies that neutralize divergent variants of HPV16. Virology 279:361-369.
36. Rammensee, H., J. Bachmann, N. P. Emmerich, O. A. Bachor, and S. Stevanovic. 1999, SYFPEITHI: database for MHC ligands and peptide motifs. Immunogenetics 50:213-219.
37. Rammensee, H., J. Bachmann, and S. Stevanovic. 1997. MHC ligands and peptide motifs. Landes, Austin, Tex.
38. 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.
39. 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.
40. Schäfer, K., M. Müller, S. Faath, A. Henn, W. Osen, H. Zentgraf, A. Benner, L. Gissmann, and I. Jochmus. 1999. Immune response to human papillomavirus 16 L1E7 chimeric virus-like particles: induction of cytotoxic T cells and specific tumor protection. Int. J. Cancer 81:881-888.
41. Schiller, J. T., and R. B. S. Roden. 1995. Papillomavirus-like particles. Papillomavirus Rep. 6:121-128.
42. Sehr, P., M. Müller, R. Höpfl, A. Widschwendter, and M. Pawlita. 2002. HPV antibody detection by ELISA with capsid protein L1 fused to glutathione S-transferase. J. Virol. Methods 106:61-70.
43. Sehr, P., K. Zumbach, and M. Pawlita. 2001. A generic capture ELISA for recombinant proteins fused to glutathione S-transferase: validation for HPV serology. J. Immunol. Methods 253:153-162.
44. Staib, C., I. Drexler, M. Ohlmann, S. Wintersperger, V. Erfle, and G. Sutter. 2000. Transient host range selection for genetic engineering of modified vaccinia virus Ankara. BioTechniques 28:1137-1142, 1144-1146, 1148.
45. Stern, P. L., R. Faulkner, E. C. Veranes, and E. J. Davidson. 2001. The role of human papillomavirus vaccines in cervical neoplasia. Best Pract. Res. Clin. Obstet. Gynaecol. 15:783-799.
46. 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.
47. Ulevitch, R. J., and P. S. Tobias. 1999. Recognition of gram-negative bacteria and endotoxin by the innate immune system. Curr. Opin. Immunol. 11:19-22.
48. Woodworth, C. D. 2002. HPV innate immunity. Front. Biosci. 7: d2058-d2071.
49. Yeager, M. D., M. Aste-Amezaga, D. R. Brown, M. M. Martin, M. J. Shah, J. C. Cook, N. D. Christensen, C. Ackerson, R. S. Lowe, J. F. Smith, P. Keller, and K. U. Jansen. 2000. Neutralization of human papillomavirus (HPV) pseudovirions: a novel and efficient approach to detect and characterize HPV neutralizing antibodies. Virology 278:570-577.
50. 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.
51. Zhang, W., J. Carmichael, J. Ferguson, S. Inglis, H. Ashrafian, and M. Stanley. 1998. Expression of human papillomavirus type 16 L1 protein in Escherichia coli: denaturation, renaturation, and self-assembly of virus-like particles in vitro. Virology 243:423-431.