A papillomavirus-like particle (VLP) vaccine displaying HPV16 L2 epitopes induces cross-neutralizing antibodies to HPV11

Vaccine

Volumn 25, Issue 11, 2007, Pages 2001-2010

  Slupetzky, Katharina ^a   Gambhira, Ratish ^b   Culp, Timothy D ^c   Shafti Keramat, Saeed ^a   Schellenbacher, Christina ^a   Christensen, Neil D ^c   Roden, Richard B S ^b   Kirnbauer, Reinhard ^a  

^a Division of Immunology Allergy and Infectious Diseases (DIAID)   (Austria)

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

^c PENN STATE CANCER INSTITUTE   (United States)

Author keywords

HPV; L2 peptide; VLP vaccine

Indexed keywords

CAPSID PROTEIN; GLUTATHIONE TRANSFERASE; HYBRID PROTEIN; L2 PROTEIN; NEUTRALIZING ANTIBODY; SYNTHETIC PEPTIDE; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS RNA; WART VIRUS VACCINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY TITER; ARTICLE; BACULOVIRUS; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN PAPILLOMAVIRUS TYPE 11; HUMAN PAPILLOMAVIRUS TYPE 16; HUMAN PAPILLOMAVIRUS TYPE 18; HUMAN PAPILLOMAVIRUS TYPE 6; IMMUNIZATION; MOUSE; NONHUMAN; PAPILLOMA VIRUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RABBIT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VACCINATION; VIRION; VIRUS CAPSID; VIRUS INFECTION; VIRUS LIKE AGENT; VIRUS NEUTRALIZATION; VIRUS RECOMBINANT; WART VIRUS;

ANIMALS; ANTIBODIES, VIRAL; BOVINE PAPILLOMAVIRUS 1; CAPSID PROTEINS; CROSS REACTIONS; EPITOPES; GENETIC VECTORS; HUMAN PAPILLOMAVIRUS 11; HUMAN PAPILLOMAVIRUS 16; HUMANS; MICE; MODELS, ANIMAL; NEUTRALIZATION TESTS; ONCOGENE PROTEINS, VIRAL; PAPILLOMAVIRUS VACCINES; RABBITS; VACCINES, VIROSOME;

EID: 33846875433     PISSN: 0264410X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vaccine.2006.11.049     Document Type: Article

References (60)

1. de Villiers E.M., Fauquet C., Broker T.R., Bernard H.U., and zur Hausen H. Classification of papillomaviruses. Virology 324 (2004) 17-27
2. Walboomers J.M., Jacobs M.V., Manos M.M., Bosch F.X., Kummer J.A., Shah K.V., et al. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol 189 (1999) 12-19
3. Pfister H. Chapter 8: human papillomavirus and skin cancer. J Natl Cancer Inst Monogr (2003) 52-56
4. The Papovaviridae. In: Salzman N.P., and Howley P.M. (Eds). The Papillomaviruses 2 (1987), Plenum Press, New York 392
5. zur Hausen H. Papillomavirus infection- a major cause of human cancers. Biochim Biophys Acta 1288 (1996) F55-F78
6. Kirnbauer R. Papillomavirus-like particles for serology and vaccine development. Intervirology 39 (1996) 54-61
7. Baker T.S., Newcomb W.W., Olson N.H., Cowsert L.M., Olson C., and Brown J.C. Structures of bovine and human papillomaviruses. Analysis by cryoelectron microscopy and three-dimensional image reconstruction. Biophys J 60 (1991) 1445-1456
8. Chen X.S., Garcea R.L., Goldberg I., Casini G., and Harrison S.C. Structure of small virus-like particles assembled from the L1 protein of human papillomavirus 16. Mol Cell 5 (2000) 557-567
9. Trus B.L., Roden R.B., Greenstone H.L., Vrhel M., Schiller J.T., and Booy F.P. Novel structural features of bovine papillomavirus capsid revealed by a three-dimensional reconstruction to 9 Å resolution. Nat Struct Biol 4 (1997) 413-420
10. Breitburd F., Kirnbauer R., Hubbert N.L., Nonnenmacher B., Trin-Dinh-Desmarquet C., Orth G., et al. Immunization with viruslike particles from cottontail rabbit papillomavirus (CRPV) can protect against experimental CRPV infection. J Virol 69 (1995) 3959-3963
11. Christensen N., Reed C., Cladel N., Han R., and Kreider J. Immunization with viruslike particles induces long-term protection of rabbits against challenge with cottontail rabbit papillomavirus. J Virol 70 (1996) 960-965
12. Jansen K., Rosolowsky M., Schultz L., Markus H., Cook J., Donnelly J., et al. Vaccination with yeast-expressed cottontail rabbit papillomavirus (CRPV) virus-like particles protects rabbits from CRPV-induced papilloma formation. Vaccine 13 (1995) 1509-1514
13. Kirnbauer R., Chandrachud L., O'Neil B., Wagner E., Grindlay G., Armstrong A., et al. Virus-like particles of bovine papillomavirus type-4 in prophylactic and therapeutic immunization. Virology 219 (1996) 37-44
14. Kirnbauer R., Booy F., Cheng N., Lowy D.R., and Schiller J.T. Papillomavirus L1 major capsid protein self-assembles into virus-like particles that are highly immunogenic. Proc Natl Acad Sci USA 89 (1992) 12180-12184
15. Suzich J.A., Ghim S., Palmer-Hill F.J., White W.I., Tamura J.K., Bell J., et al. Systemic immunization with papillomavirus L1 protein completely prevents the development of viral mucosal papillomas. Proc Natl Acad Sci USA 92 (1995) 11553-11557
16. Harper D.M., Franco E.L., Wheeler C.M., Moscicki A.B., Romanowski B., Roteli-Martins C.M., et al. 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 (2006) 1247-1255
17. Harper D.M., Franco E.L., Wheeler C., Ferris D.G., Jenkins D., Schuind A., et al. 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 (2004) 1757-1765
18. Harro C.D., Pang Y.Y., Roden R.B., Hildesheim A., Wang Z., Reynolds M.J., et al. Safety and immunogenicity trial in adult volunteers of a human papillomavirus 16 L1 virus-like particle vaccine. J Natl Cancer Inst 93 (2001) 284-292
19. Koutsky L.A., Ault K.A., Wheeler C.M., Brown D.R., Barr E., Alvarez F.B., et al. A controlled trial of a human papillomavirus type 16 vaccine. N Engl J Med 347 (2002) 1645-1651
20. Villa L.L., Costa R.L., Petta C.A., Andrade R.P., Ault K.A., Giuliano A.R., et al. 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 (2005) 271-278
21. Munoz N., Bosch F.X., de Sanjose S., Herrero R., Castellsague X., Shah K.V., et al. Epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med 348 (2003) 518-527
22. Roden R.B., Weissinger E.M., Henderson D.W., Booy F., Kirnbauer R., Mushinski J.F., et al. Neutralization of bovine papillomavirus by antibodies to L1 and L2 capsid proteins. J Virol 68 (1994) 7570-7574
23. Pastrana D.V., Gambhira R., Buck C.B., Pang Y.Y., Thompson C.D., Culp T.D., et al. Cross-neutralization of cutaneous and mucosal papillomavirus types with anti-sera to the amino terminus of L2. Virology 337 (2005) 365-372
24. Roden R.B.S., Yutzy W.H., Fallon R., Inglis S., Lowy D.R., and Schiller J.T. Minor capsid protein of human genital papillomaviruses contains subdominant, cross-neutralizing epitopes. Virology 270 (2000) 254-257
25. Kawana K., Yasugi T., Kanda T., Kino N., Oda K., Okada S., et al. Safety and immunogenicity of a peptide containing the cross-neutralization epitope of HPV16 L2 administered nasally in healthy volunteers. Vaccine 21 (2003) 4256-4260
26. Campo M.S. Animal models of papillomavirus pathogenesis. Virus Res 89 (2002) 249-261
27. Christensen N.D., Kreider J.W., Kan N.C., and DiAngelo S.L. The open reading frame L2 of cottontail rabbit papillomavirus contains antibody-inducing neutralizing epitopes. Virology 181 (1991) 572-579
28. Kawana K., Yoshikawa H., Taketani Y., Yoshiike K., and Kanda T. Common neutralization epitope in minor capsid protein L2 of human papillomavirus types 16 and 6. J Virol 73 (1999) 6188-6190
29. Bachmann M.F., Zinkernagel R.M., and Oxenius A. Immune responses in the absence of costimulation: viruses know the trick. J Immunol 161 (1998) 5791-5794
30. Yuan H., Estes P.A., Chen Y., Newsome J., Olcese V.A., Garcea R.L., et al. Immunization with a pentameric L1 fusion protein protects against papillomavirus infection. J Virol 75 (2001) 7848-7853
31. Rose R., White W., Maolin L., Suzich J., Lane C., and Garcea R. Human papillomavirus type 11 recombinant L1 capsomeres induce virus-neutralizing antibodies. J Virol 72 (1998) 6151-6154
32. 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 (2001) 353-357
33. Varsani A., Williamson A.L., de Villiers D., Becker I., Christensen N.D., and Rybicki E.P. Chimeric human papillomavirus type 16 (HPV-16) L1 particles presenting the common neutralizing epitope for the L2 minor capsid protein of HPV-6 and HPV-16. J Virol 77 (2003) 8386-8393
34. Slupetzky K., Shafti-Keramat S., Lenz P., Brandt S., Grassauer A., Sara M., et al. Chimeric papillomavirus-like particles expressing a foreign epitope on capsid surface loops. J Gen Virol 82 (2001) 2799-2804
35. Chackerian B., Lowy D.R., and Schiller J.T. Induction of autoantibodies to mouse CCR5 with recombinant papillomavirus particles. Proc Natl Acad Sci USA 96 (1999) 2373-2378
36. Ailenberg M., and Silverman M. Controlled hot start and improved specificity in carrying out PCR utilizing touch-up and loop incorporated primers (TULIPS). Biotechniques 29 5 (2000) 1018-1024
37. Sambrook J., Fritsch E.F., and Maniatis T. Molecular cloning. A laboratory manual (1989), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
38. Shafti-Keramat S., Handisurya A., Kriehuber E., Meneguzzi G., Slupetzky K., and Kirnbauer R. Different heparan sulfate proteoglycans serve as cellular receptors for human papillomaviruses. J Virol 77 (2003) 13125-13135
39. Smith L.H., Foster C., Hitchcock M.E., Leiserowitz G.S., Hall K., Isseroff R., et al. Titration of HPV-11 infectivity and antibody neutralization can be measured in vitro. J Invest Dermatol 105 (1995) 438-444
40. Culp T.D., Christensen N.D., and Quantitative. RT-PCR assay for HPV infection in cultured cells. J Virol Methods 111 (2003) 135-144
41. Buck C.B., Pastrana D.V., Lowy D.R., and Schiller J.T. Efficient intracellular assembly of papillomaviral vectors. J Virol 78 (2004) 751-757
42. Pastrana D.V., Buck C.B., Pang Y.Y., Thompson C.D., Castle P.E., FitzGerald P.C., et al. Reactivity of human sera in a sensitive, high-throughput pseudovirus-based papillomavirus neutralization assay for HPV16 and HPV18. Virology 321 (2004) 205-216
43. Kawana K., Matsumoto K., Yoshikawa H., Taketani Y., Kawana T., Yoshiike K., et al. A surface immunodeterminant of human papillomavirus type 16 minor capsid protein L2. Virology 245 (1998) 353-359
44. Kawana Y., Kawana K., Yoshikawa H., Taketani Y., Yoshiike K., and Kanda T. 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 (2001) 2331-2336
45. Rose R.C., Bonnez W., Da Rin C., McCance D.J., and Reichman R.C. Serological differentiation of human papillomavirus types 11, 16 and 18 using recombinant virus-like particles. J Gen Virol 75 (1994) 2445-2449
46. Buck C.B., Pastrana D.V., Lowy D.R., and Schiller J.T. Generation of HPV pseudovirions using transfection and their use in neutralization assays. Methods Mol Med 119 (2005) 445-462
47. Zamora E., Handisurya A., Shafti-Keramat S., Borchelt D., Rudow G., Conant K., et al. Papillomavirus-like particles are an effective platform for amyloid-β immunization in rabbits and transgenic mice. J Immunol 177 (2006) 2662-2670
48. Chandrachud L.M., Grindlay G.J., McGarvie G.M., O'Neil B.W., Wagner E.R., Jarrett W.F., et al. Vaccination of cattle with the N-terminus of L2 is necessary and sufficient for preventing infection by bovine papillomavirus-4. Virology 211 (1995) 204-208
49. Bachmann M.F., and Zinkernagel R.M. Neutralizing antiviral B cell responses. Annu Rev Immunol 15 (1997) 235-270
50. Lenz P., Day P.M., Pang Y.Y., Frye S.A., Jensen P.N., Lowy D.R., et al. Papillomavirus-like particles induce acute activation of dendritic cells. J Immunol 166 (2001) 5346-5355
51. Rudolf M.P., Fausch S.C., Da Silva D.M., and Kast W.M. 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 (2001) 5917-5924
52. Yang R., Murillo F.M., Delannoy M.J., Blosser R.L., Yutzy W.H.t., Uematsu S., et al. B lymphocyte activation by human papillomavirus-like particles directly induces Ig class switch recombination via TLR4-MyD88. J Immunol 174 (2005) 7912-7919
53. Pinto L.A., Castle P.E., Roden R.B., Harro C.D., Lowy D.R., Schiller J.T., et al. HPV-16 L1 VLP vaccine elicits a broad-spectrum of cytokine responses in whole blood. Vaccine 23 (2005) 3555-3564
54. Pinto L.A., Edwards J., Castle P.E., Harro C.D., Lowy D.R., Schiller J.T., et al. 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 (2003) 327-338
55. Yang R., Murillo F.M., Lin K.Y., Yutzy W.H.t., Uematsu S., Takeda K., et al. Human papillomavirus type-16 virus-like particles activate complementary defense responses in key dendritic cell subpopulations. J Immunol 173 (2004) 2624-2631
56. Chackerian B., Lowy D.R., and Schiller J.T. Conjugation of a self-antigen to papillomavirus-like particles allows for efficient induction of protective autoantibodies. J Clin Invest 108 (2001) 415-423
57. Chackerian B., Lenz P., Lowy D.R., and Schiller J.T. Determinants of autoantibody induction by conjugated papillomavirus virus-like particles. J Immunol (Baltimore Md.: 1950) 169 (2002) 6120-6126
58. Embers M.E., Budgeon L.R., Pickel M., and Christensen N.D. Protective immunity to rabbit oral and cutaneous papillomaviruses by immunization with short peptides of L2, the minor capsid protein. J Virol 76 (2002) 9798-9805
59. Culp T.D., and Christensen N.D. Kinetics of in vitro adsorption and entry of papillomavirus virions. Virology 319 (2004) 152-161
60. Day P.M., Lowy D.R., and Schiller J.T. Papillomaviruses infect cells via a clathrin-dependent pathway. Virology 307 (2003) 1-11