Oral immunization with different assembly forms of the HPV 16 major capsid protein L1 induces neutralizing antibodies and cytotoxic T-lymphocytes

Virology

Volumn 369, Issue 2, 2007, Pages 375-388

  Thönes, Nadja ^a   Müller, Martin ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

Capsomere; CTL; Neutralizing antibodies; Oral immunization; Virus like particles

Indexed keywords

CAPSID PROTEIN; CPG OLIGODEOXYNUCLEOTIDE; L1 PROTEIN; NEUTRALIZING ANTIBODY; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANTIBODY PRODUCTION; ANTIBODY TITER; ARTICLE; CELLULAR IMMUNITY; CONFORMATION; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; ESCHERICHIA COLI; HUMAN PAPILLOMAVIRUS TYPE 16; HUMORAL IMMUNITY; IMMUNITY; IMMUNIZATION; IMMUNOGENICITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; VIRION; VIRUS LIKE AGENT; VIRUS PARTICLE;

ADMINISTRATION, ORAL; ANIMALS; ANTIBODIES, VIRAL; ANTIBODY SPECIFICITY; ANTIGENS, VIRAL; CAPSID PROTEINS; FEMALE; HUMAN PAPILLOMAVIRUS 16; HUMANS; IMMUNIZATION; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICROSCOPY, ELECTRON, TRANSMISSION; NEUTRALIZATION TESTS; ONCOGENE PROTEINS, VIRAL; PAPILLOMAVIRUS VACCINES; RECOMBINANT PROTEINS; T-LYMPHOCYTES, CYTOTOXIC; VIRION; VIRUS ASSEMBLY;

ESCHERICHIA COLI; HEXAPODA; HUMAN PAPILLOMAVIRUS TYPE 16; MIRIDAE; MUS; PAPILLOMAVIRIDAE;

EID: 36049000191     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2007.08.004     Document Type: Article

References (46)

1. Aziz M.A., Midha S., Waheed S.M., and Bhatnagar R. Oral vaccines: new needs, new possibilities. BioEssays 29 6 (2007) 591-604
2. Balmelli C., Roden R., Potts A., Schiller J., De Grandi P., and Nardelli-Haefliger D. Nasal immunization of mice with human papillomavirus type 16 virus-like particles elicits neutralizing antibodies in mucosal secretions. J. Virol. 72 10 (1998) 8220-8229
3. Biemelt S., Sonnewald U., Galmbacher P., Willmitzer L., and Muller M. Production of human papillomavirus type 16 virus-like particles in transgenic plants. J. Virol. 77 17 (2003) 9211-9220
4. Bosch F.X., Manos M.M., Munoz N., Sherman M., Jansen A.M., Peto J., Schiffman M.H., Moreno V., Kurman R., and Shah K.V. Prevalence of human papillomavirus in cervical cancer: a worldwide perspective. International biological study on cervical cancer (IBSCC) Study Group. J. Natl. Cancer Inst. 87 11 (1995) 796-802
5. Breitburd F., and Coursaget P. Human papillomavirus vaccines. Semin. Cancer Biol. 9 6 (1999) 431-444
6. Buck C.B., Pastrana D.V., Lowy D.R., and Schiller J.T. Efficient intracellular assembly of papillomaviral vectors. J. Virol. 78 2 (2004) 751-757
7. Clifford G.M., Smith J.S., Plummer M., Munoz N., and Franceschi S. Human papillomavirus types in invasive cervical cancer worldwide: a meta-analysis. Br. J. Cancer 88 1 (2003) 63-73
8. Dell K., Koesters R., Linnebacher M., Klein C., and Gissmann L. 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 13 (2006) 2238-2247
9. De Maio A., Mooney M.L., Matesic L.E., Paidas C.N., and Reeves R.H. Genetic component in the inflammatory response induced by bacterial lipopolysaccharide. Shock 10 5 (1998) 319-323
10. Dupuy C., Buzoni-Gatel D., Touze A., Bout D., and Coursaget P. 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 11 (1999) 9063-9071
11. Fligge C., Giroglou T., Streeck R.E., and Sapp M. Induction of type-specific neutralizing antibodies by capsomeres of human papillomavirus type 33. Virology 283 2 (2001) 353-357
12. Franco E.L., Rohan T.E., and Villa L.L. Epidemiologic evidence and human papillomavirus infection as a necessary cause of cervical cancer. J. Natl. Cancer Inst. 91 6 (1999) 506-511
13. Freytag L.C., and Clements J.D. Bacterial toxins as mucosal adjuvants. Curr. Top. Microbiol. Immunol. 236 (1999) 215-236
14. Gerber S., Lane C., Brown D.M., Lord E., DiLorenzo M., Clements J.D., Rybicki E., Williamson A.L., and Rose R.C. Human papillomavirus virus-like particles are efficient oral immunogens when coadministered with Escherichia coli heat-labile enterotoxin mutant R192G or CpG DNA. J. Virol. 75 10 (2001) 4752-4760
15. Gissmann L., Osen W., Muller M., and Jochmus I. Therapeutic vaccines for human papillomaviruses. Intervirology 44 2-3 (2001) 167-175
16. Harper D.M., Franco E.L., Wheeler C., Ferris D.G., Jenkins D., Schuind A., Zahaf T., Innis B., Naud P., De Carvalho N.S., Roteli-Martins C.M., Teixeira J., Blatter M.M., Korn A.P., Quint W., and Dubin G. 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 9447 (2004) 1757-1765
17. Holmgren J., and Czerkinsky C. Mucosal immunity and vaccines. Nat. Med. 11 4 Suppl. (2005) S45-S53
18. Kozlowski P.A., Cu-Uvin S., Neutra M.R., and Flanigan T.P. Mucosal vaccination strategies for women. J. Infect. Dis. 179 Suppl. 3 (1999) S493-S498
19. Lal P., Ramachandran V.G., Goyal R., and Sharma R. Edible vaccines: current status and future. Indian J. Med. Microbiol. 25 2 (2007) 93-102
20. Lauterslager T.G., Florack D.E., van der Wal T.J., Molthoff J.W., Langeveld J.P., Bosch D., Boersma W.J., and Hilgers L.A. Oral immunisation of naive and primed animals with transgenic potato tubers expressing LT-B. Vaccine 19 17-19 (2001) 2749-2755
21. Lauterslager T.G., Stok W., and Hilgers L.A. Improvement of the systemic prime/oral boost strategy for systemic and local responses. Vaccine 21 13-14 (2003) 1391-1399
22. Liu X.S., Abdul-Jabbar I., Qi Y.M., Frazer I.H., and Zhou J. Mucosal immunisation with papillomavirus virus-like particles elicits systemic and mucosal immunity in mice. Virology 252 1 (1998) 39-45
23. Lowy D.R., and Schiller J.T. Prophylactic human papillomavirus vaccines. J. Clin. Invest. 116 5 (2006) 1167-1173
24. Mestecky J., and Russell M.W. Induction of mucosal immune responses in the human genital tract. FEMS Immunol. Med. Microbiol. 27 4 (2000) 351-355
25. Mestecky J., Kutteh W.H., and Jackson S. Mucosal immunity in the female genital tract: relevance to vaccination efforts against the human immunodeficiency virus. AIDS Res. Hum. Retroviruses 10 Suppl. 2 (1994) S11-S20
26. Muller M., Zhou J., Reed T.D., Rittmuller C., Burger A., Gabelsberger J., Braspenning J., and Gissmann L. Chimeric papillomavirus-like particles. Virology 234 1 (1997) 93-111
27. Munoz N., Castellsague X., de Gonzalez A.B., and Gissmann L. Chapter 1: HPV in the etiology of human cancer. Vaccine 24S3 (2006) S1-S10
28. Nardelli-Haefliger D., Roden R., Balmelli C., Potts A., Schiller J., and De Grandi P. 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 11 (1999) 9609-9613
29. Neutra M.R., and Kozlowski P.A. Mucosal vaccines: the promise and the challenge. Nat. Rev., Immunol. 6 2 (2006) 148-158
30. O'Malley J., Matesic L.E., Zink M.C., Strandberg J.D., Mooney M.L., De Maio A., and Reeves R.H. Comparison of acute endotoxin-induced lesions in A/J and C57BL/6J mice. J. Heredity 89 6 (1998) 525-530
31. Ohlschlager P., Osen W., Dell K., Faath S., Garcea R.L., Jochmus I., Muller M., Pawlita M., Schafer K., Sehr P., Staib C., Sutter G., and Gissmann L. Human papillomavirus type 16 L1 capsomeres induce L1-specific cytotoxic T lymphocytes and tumor regression in C57BL/6 mice. J. Virol. 77 8 (2003) 4635-4645
32. Parkin D.M., Bray F., Ferlay J., and Pisani P. Global cancer statistics, 2002. CA Cancer J. Clin. 55 2 (2005) 74-108
33. Pastrana D.V., Buck C.B., Pang Y.Y., Thompson C.D., Castle P.E., FitzGerald P.C., Kruger Kjaer S., Lowy D.R., and Schiller J.T. Reactivity of human sera in a sensitive, high-throughput pseudovirus-based papillomavirus neutralization assay for HPV16 and HPV18. Virology 321 2 (2004) 205-216
34. Pickering R.J., Smith S.D., Strugnell R.A., Wesselingh S.L., and Webster D.E. Crude saponins improve the immune response to an oral plant-made measles vaccine. Vaccine 24 2 (2006) 144-150
35. Pisani P., Bray F., and Parkin D.M. Estimates of the world-wide prevalence of cancer for 25 sites in the adult population. Int. J. Cancer 97 1 (2002) 72-81
36. Rose R.C., White W.I., Li M., Suzich J.A., Lane C., and Garcea R.L. Human papillomavirus type 11 recombinant L1 capsomeres induce virus-neutralizing antibodies. J. Virol. 72 7 (1998) 6151-6154
37. Rose R.C., Lane C., Wilson S., Suzich J.A., Rybicki E., and Williamson A.L. Oral vaccination of mice with human papillomavirus virus-like particles induces systemic virus-neutralizing antibodies. Vaccine 17 17 (1999) 2129-2135
38. Sapp M., Fligge C., Petzak I., Harris J.R., and Streeck R.E. Papillomavirus assembly requires trimerization of the major capsid protein by disulfides between two highly conserved cysteines. J. Virol. 72 7 (1998) 6186-6189
39. Sasagawa T., Tani M., Basha W., Rose R.C., Tohda H., Giga-Hama Y., Azar K.K., Yasuda H., Sakai A., and Inoue M. A human papillomavirus type 16 vaccine by oral delivery of L1 protein. Virus Res. 110 1-2 (2005) 81-90
40. Schiller J.T., and Davies P. Delivering on the promise: HPV vaccines and cervical cancer. Nat. Rev., Microbiol. 2 4 (2004) 343-347
41. Schiller J.T., and Lowy D.R. Papillomavirus-like particle vaccines. J. Natl. Cancer Inst. Monogr. 28 (2001) 50-54
42. Stewart D., Fulton W.B., Wilson C., Monitto C.L., Paidas C.N., Reeves R.H., and De Maio A. Genetic contribution to the septic response in a mouse model. Shock 18 4 (2002) 342-347
43. Villa L.L., Costa R.L., Petta C.A., Andrade R.P., Paavonen J., Iversen O.E., Olsson S.E., Hoye J., Steinwall M., Riis-Johannessen G., Andersson-Ellstrom A., Elfgren K., Krogh G., Lehtinen M., Malm C., Tamms G.M., Giacoletti K., Lupinacci L., Railkar R., Taddeo F.J., Bryan J., Esser M.T., Sings H.L., Saah A.J., and Barr E. 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 11 (2006) 1459-1466
44. Walker P.S., Scharton-Kersten T., Krieg A.M., Love-Homan L., Rowton E.D., Udey M.C., and Vogel J.C. Immunostimulatory oligodeoxynucleotides promote protective immunity and provide systemic therapy for leishmaniasis via IL-12- and IFN-gamma-dependent mechanisms. Proc. Natl. Acad. Sci. U. S. A. 96 12 (1999) 6970-6975
45. Watson J.L., and McKay D.M. The immunophysiological impact of bacterial CpG DNA on the gut. Clin. Chim. Acta 364 1-2 (2006) 1-11
46. Yuan H., Estes P.A., Chen Y., Newsome J., Olcese V.A., Garcea R.L., and Schlegel R. Immunization with a pentameric L1 fusion protein protects against papillomavirus infection. J. Virol. 75 17 (2001) 7848-7853