Development of human papillomavirus chimaeric L1/L2 candidate vaccines

Archives of Virology

Volumn 158, Issue 10, 2013, Pages 2079-2088

  McGrath, Marieta ^a   de Villiers, Gillian K ^a   Shephard, Enid ^a,b,c   Hitzeroth, Inga I ^a   Rybicki, Edward P ^a,b  

^a UNIVERSITY OF CAPE TOWN   (South Africa)

^b Institute of Infectious Disease and Molecular Medicine   (South Africa)

^c SOUTH AFRICAN MEDICAL RESEARCH COUNCIL   (South Africa)

Author keywords

[No Author keywords available]

Indexed keywords

NEUTRALIZING ANTIBODY; VIRUS ANTIBODY; WART VIRUS VACCINE;

ANIMAL; ARTICLE; BLOOD; C57BL MOUSE; FEMALE; HUMAN; HUMAN PAPILLOMAVIRUS TYPE 16; IMMUNOLOGY; METABOLISM; MOUSE; SF9 CELL;

ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; FEMALE; HUMAN PAPILLOMAVIRUS 16; HUMANS; MICE; MICE, INBRED C57BL; PAPILLOMAVIRUS VACCINES; SF9 CELLS;

BOVINE PAPILLOMAVIRUS TYPE 1; CHIMAERIFORMES; HEXAPODA; HUMAN PAPILLOMAVIRUS; HUMAN PAPILLOMAVIRUS TYPE 16; MIRIDAE; MUS;

EID: 84884814561     PISSN: 03048608     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00705-013-1713-8     Document Type: Article

References (57)

1. Alphs HH, Gambhira R, Karanam B, Roberts JN, Jagu S, Schiller JT, Zeng W, Jackson DC, Roden RBS (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. Bernard H-U, Burk RD, Chen Z, van Doorslaer K, Hausen Hz, De Villiers E-M (2010) Classification of papillomaviruses (PVs) based on 189 PV types and proposal of taxonomic amendments. Virology 401: 70-79.
3. Bishop B, Dasgupta J, Chen XS (2007) Structure-based engineering of papillomavirus major capsid L1: controlling particle assembly. Virol J 4: 3.
4. Bosch FX (2009) Broad-spectrum human papillomavirus vaccines: new horizons but one step at a time. J Natl Cancer Inst 101: 771-773.
5. Bosch FX, Burchell AN, Schiffman M, Giuliano AR, De Sanjose S, Bruni L, Tortolero-Luna G, Kjaer SK, Muñoz N (2008) Epidemiology and natural history of human papillomavirus infections and type-specific implications in cervical neoplasia. Vaccine 26(Suppl 10): K1-K16.
6. Breitburd F, Kirnbauer R, Hubbert NL, Nonnenmacher B, Trin-Dinh-Desmarquet C, Orth G, Schiller JT, Lowy DR (1995) Immunization with viruslike particles from cottontail rabbit papillomavirus (CRPV) can protect against experimental CRPV infection. J Virol 69: 3959-3963.
7. Buck CB, Cheng N, Thompson CD, Lowy DR, Steven AC, Schiller JT, Trus BL (2008) Arrangement of L2 within the papillomavirus capsid. J Virol 82: 5190-5197.
8. Buck CB, Pastrana DV, Lowy DR, Schiller JT (2005) Generation of HPV pseudovirions using transfection and their use in neutralization assays. Methods Mol Med 119: 445-462.
9. Cason J, Kambo PK, Jewers RJ, Best JM (1994) Detection of protein aggregates, but not virus-like particles, when the major (L1) coat protein of a wild-type human papillomavirus type 16 (HPV-16) is expressed in insect cells. Biochem Soc Trans 22: 335S.
10. Castellsagué X (2008) Natural history and epidemiology of HPV infection and cervical cancer. Gynecol Oncol 110: S4-S7.
11. Chackerian B, Lowy DR, Schiller JT (1999) Induction of autoantibodies to mouse CCR5 with recombinant papillomavirus particles. Proc Natl Acad Sci USA 96: 2373-2378.
12. Chen XS, Garcea RL, Goldberg I, Casini G, Harrison SC (2000) Structure of small virus-like particles assembled from the L1 protein of human papillomavirus 16. Mol Cell 5: 557-567.
13. Christensen ND, Dillner J, Eklund C, Carter JJ, Wipf GC, Reed CA, Cladel NM, Galloway DA (1996) Surface conformational and linear epitopes on HPV-16 and HPV-18 L1 virus-like particles as defined by monoclonal antibodies. Virology 223: 174-184.
14. Christensen ND, Kreider JW (1990) Antibody-mediated neutralization in vivo of infectious papillomaviruses. J Virol 64: 3151-3156.
15. Cutts FT, Franceschi S, Goldie S, Castellsague X, De Sanjose S, Garnett G, Edmunds WJ, Claeys P, Goldenthal KL, Harper DM, Markowitz L (2007) Human papillomavirus and HPV vaccines: a review. Bull World Health Organ 85: 719-726.
16. TM, the AS04-adjuvanted HPV-16 and -18 cervical cancer vaccine. Hum Vaccin 6: 407-419.
17. de Villiers E-M, Fauquet C, Broker TR, Bernard H-U, Zur Hausen H (2004) Classification of papillomaviruses. Virology 324: 17-27.
18. Embers ME, Budgeon LR, Pickel M, Christensen ND (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.
19. Fang NX, Frazer IH, Fernando GJ (2000) Differences in the post-translational modifications of human papillomavirus type 6b major capsid protein expressed from a baculovirus system compared with a vaccinia virus system. Biotechnol Appl Biochem 32(Pt 1): 27-33.
20. Gambhira R, Karanam B, Jagu S, Roberts JN, Buck CB, Bossis I, Alphs H, Culp T, Christensen ND, Roden RBS (2007) A protective and broadly cross-neutralizing epitope of human papillomavirus L2. J Virol 81: 13927-13931.
21. Huh WK, Roden RBS (2008) The future of vaccines for cervical cancer. Gynecol Oncol 109: S48-S56.
22. Kawana K, Matsumoto K, Yoshikawa H, Taketani Y, Kawana T, Yoshiike K, Kanda T (1998) A surface immunodeterminant of human papillomavirus type 16 minor capsid protein L2. Virology 245: 353-359.
23. Kawana K, Yasugi T, Kanda T, Kino N, Oda K, Okada S, Kawana Y, Nei T, Takada T, Toyoshima S, Tsuchiya A, Kondo K, Yoshikawa H, Tsutsumi O, Taketani Y (2003) Safety and immunogenicity of a peptide containing the cross-neutralization epitope of HPV16 L2 administered nasally in healthy volunteers. Vaccine 21: 4256-4260.
24. Kawana K, Yoshikawa H, Taketani Y, Yoshiike K, Kanda T (1999) Common neutralization epitope in minor capsid protein L2 of human papillomavirus types 16 and 6. J Virol 73: 6188-6190.
25. Kirnbauer R, Booy F, Cheng N, Lowy DR, Schiller JT (1992) Papillomavirus L1 major capsid protein self-assembles into virus-like particles that are highly immunogenic. Proc Natl Acad Sci USA 89: 12180-12184.
26. Koh YT, Higgins SA, Weber JS, Kast WM (2006) Immunological consequences of using three different clinical/laboratory techniques of emulsifying peptide-based vaccines in incomplete Freund's adjuvant. J Transl Med 4: 42.
27. Kohl TO, Hitzeroth II, Christensen ND, Rybicki EP (2007) Expression of HPV-11 L1 protein in transgenic Arabidopsis thaliana and Nicotiana tabacum. BMC Biotechnol 7: 56.
28. Kondo K, Ishii Y, Ochi H, Matsumoto T, Yoshikawa H, Kanda T (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, Ochi H, Matsumoto T, Yoshikawa H, Kanda T (2008) Modification of human papillomavirus-like particle vaccine by insertion of the cross-reactive L2-epitopes. J Med Virol 80: 841-846.
30. Kuck D, Leder C, Kern A, Müller M, Piuko K, Gissmann L, Kleinschmidt JA (2006) Efficiency of HPV 16 L1/E7 DNA immunization: influence of cellular localization and capsid assembly. Vaccine 24: 2952-2965.
31. Lenz P, Day PM, Pang YY, Frye SA, Jensen PN, Lowy DR, Schiller JT (2001) Papillomavirus-like particles induce acute activation of dendritic cells. J Immunol 166: 5346-5355.
32. Lenz P, Thompson CD, Day PM, Bacot SM, Lowy DR, Schiller JT (2003) Interaction of papillomavirus virus-like particles with human myeloid antigen-presenting cells. Clin Immunol 106: 231-237.
33. Liu XS, Liu WJ, Zhao KN, Liu YH, Leggatt G, Frazer IH (2002) Route of administration of chimeric BPV1 VLP determines the character of the induced immune responses. Immunol Cell Biol 80: 21-29.
34. Maclean J, Koekemoer M, Olivier AJ, Stewart D, Hitzeroth II, Rademacher T, Fischer R, Williamson A-L, Rybicki EP (2007) Optimization of human papillomavirus type 16 (HPV-16) L1 expression in plants: comparison of the suitability of different HPV-16 L1 gene variants and different cell-compartment localization. J Gen Virol 88: 1460-1469.
35. Murata Y, Lightfoote PM, Rose RC, Walsh EE (2009) Antigenic presentation of heterologous epitopes engineered into the outer surface-exposed helix 4 loop region of human papillomavirus L1 capsomeres. Virol J 6: 81.
36. Neeper MP, Hofmann KJ, Jansen KU (1996) Expression of the major capsid protein of human papillomavirus type 11 in Saccharomyces cerevisae. Gene 180: 1-6.
37. Ohlschläger P, Osen W, Dell K, Faath S, Garcea RL, Jochmus I, Müller M, Pawlita M, Schäfer K, Sehr P, Staib C, Sutter G, Gissmann L (2003) Human papillomavirus type 16 L1 capsomeres induce L1-specific cytotoxic T lymphocytes and tumor regression in C57BL/6 mice. J Virol 77: 4635-4645.
38. Pastrana DV, Buck CB, Pang Y-YS, Thompson CD, Castle PE, FitzGerald PC, Krüger Kjaer S, Lowy DR, Schiller JT (2004) Reactivity of human sera in a sensitive, high-throughput pseudovirus-based papillomavirus neutralization assay for HPV16 and HPV18. Virology 321: 205-216.
39. Pastrana DV, Gambhira R, Buck CB, Pang Y-YS, Thompson CD, Culp TD, Christensen ND, Lowy DR, Schiller JT, Roden RBS (2005) Cross-neutralization of cutaneous and mucosal Papillomavirus types with anti-sera to the amino terminus of L2. Virology 337: 365-372.
40. Pillay S, Meyers A, Williamson A-L, Rybicki EP (2009) Optimization of chimeric HIV-1 virus-like particle production in a baculovirus-insect cell expression system. Biotechnol Prog 25: 1153-1160.
41. Roden RB, Yutzy WH 4th, Fallon R, Inglis S, Lowy DR, Schiller JT (2000) Minor capsid protein of human genital papillomaviruses contains subdominant, cross-neutralizing epitopes. Virology 270: 254-257.
42. Rose RC, Bonnez W, Da Rin C, McCance DJ, Reichman RC (1994) Serological differentiation of human papillomavirus types 11, 16 and 18 using recombinant virus-like particles. J Gen Virol 75(Pt 9): 2445-2449.
43. Rubio I, Bolchi A, Moretto N, Canali E, Gissmann L, Tommasino M, Müller M, Ottonello S (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.
44. Rudolf MP, Fausch SC, Da Silva DM, Kast WM (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.
45. Schädlich L, Senger T, Gerlach B, Mücke N, Klein C, Bravo IG, Müller M, Gissmann L (2009) Analysis of modified human papillomavirus type 16 L1 capsomeres: the ability to assemble into larger particles correlates with higher immunogenicity. J Virol 83: 7690-7705.
46. Schellenbacher C, Roden R, Kirnbauer R (2009) Chimeric L1-L2 virus-like particles as potential broad-spectrum human papillomavirus vaccines. J Virol 83: 10085-10095.
47. Schiller JT, Castellsagué X, Villa LL, Hildesheim A (2008) An update of prophylactic human papillomavirus L1 virus-like particle vaccine clinical trial results. Vaccine 26(Suppl 10): K53-K61.
48. Senger T, Schädlich L, Gissmann L, Müller M (2009) Enhanced papillomavirus-like particle production in insect cells. Virology 388: 344-353.
49. Shi L, Sings HL, Bryan JT, Wang B, Wang Y, Mach H, Kosinski M, Washabaugh MW, Sitrin R, Barr E (2007) GARDASIL: prophylactic human papillomavirus vaccine development-from bench top to bed-side. Clin Pharmacol Ther 81: 259-264.
50. Slupetzky K, Shafti-Keramat S, Lenz P, Brandt S, Grassauer A, Sara M, Kirnbauer R (2001) Chimeric papillomavirus-like particles expressing a foreign epitope on capsid surface loops. J Gen Virol 82: 2799-2804.
51. Thönes N, Herreiner A, Schädlich L, Piuko K, Müller M (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.
52. Touze A, El Mehdaoui S, Sizaret PY, Mougin C, Muñoz N, Coursaget P (1998) The L1 major capsid protein of human papillomavirus type 16 variants affects yield of virus-like particles produced in an insect cell expression system. J Clin Microbiol 36: 2046-2051.
53. Varsani A, Williamson A-L, De Villiers D, Becker I, Christensen ND, Rybicki EP (2003) 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: 8386-8393.
54. Wakabayashi MT, Da Silva DM, Potkul RK, Kast WM (2002) Comparison of human papillomavirus type 16 L1 chimeric virus-like particles versus L1/L2 chimeric virus-like particles in tumor prevention. Intervirology 45: 300-307.
55. World Health Organization-International Agency for Research on Cancer (2007) Monograph on Human Papillomaviruses. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, vol 90.
56. Yuan H, Estes PA, Chen Y, Newsome J, Olcese VA, Garcea RL, Schlegel R (2001) Immunization with a pentameric L1 fusion protein protects against papillomavirus infection. J Virol 75: 7848-7853.
57. WHO {pipe} Immunization. http://www. who. int/topics/immunization/en/. Accessed 6 Sep 2011.