Second-generation prophylactic HPV vaccines: Successes and challenges

Expert Review of Vaccines

Volumn 13, Issue 2, 2014, Pages 247-255

  Tyler, Mitchell ^a   Tumban, Ebenezer ^a   Chackerian, Bryce ^a  

^a UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

Author keywords

cervical cancer; HPV; L2; vaccines; virus like particles

Indexed keywords

CANCER VACCINE; CAPSID PROTEIN; CAPSID PROTEIN L2; NEUTRALIZING ANTIBODY; UNCLASSIFIED DRUG; WART VIRUS VACCINE;

CANCER EPIDEMIOLOGY; CANCER IMMUNIZATION; CANCER PREVENTION; CLINICAL EFFECTIVENESS; CROSS PROTECTION; DEVELOPING COUNTRY; DRUG COST; DRUG MANUFACTURE; FEMALE; HUMAN; IMMUNE SYSTEM; IMMUNOGENICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN TARGETING; REVIEW; UTERINE CERVIX CANCER; WART VIRUS;

ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; ANTIGENS, VIRAL; CAPSID PROTEINS; CROSS REACTIONS; FEMALE; HUMANS; PAPILLOMAVIRUS INFECTIONS; PAPILLOMAVIRUS VACCINES; UTERINE CERVICAL NEOPLASMS; VACCINATION; VACCINES, VIRUS-LIKE PARTICLE;

EID: 84893061405     PISSN: 14760584     EISSN: 17448395     Source Type: Journal    
DOI: 10.1586/14760584.2014.865523     Document Type: Review

References (83)

1. Bruni L, Diaz M, Castellsague X, Ferrer E, Bosch FX, De Sanjose S. Cervical human papillomavirus prevalence in 5 continents: meta-analysis of 1 million women with normal cytological findings. J. Infect. Dis. 202(12), 1789-1799 (2010).
2. Stanley M. Pathology and epidemiology of HPV infection in females. Gynecol. Oncol. 117(2 Suppl.), S5-S10 (2010).
3. Smith JS, Lindsay L, Hoots B et al. Human papillomavirus type distribution in invasive cervical cancer and high-grade cervical lesions: a meta-analysis update. Int. J. Cancer 121(3), 621-632 (2007).
4. Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int. J. Cancer 127(12), 2893-2917 (2010).
5. Parkin DM, Bray F. Chapter 2: the burden of HPV-related cancers. Vaccine 24(Suppl. 3), S3/11-25 (2006).
6. Rampias T, Sasaki C, Psyrri A. Molecular mechanisms of HPV induced carcinogenesis in head and neck. Oral Oncol. doi:10.1016/j.oraloncology.2013.07. 011 (2013) (Epub ahead of print).
7. Marklund L, Hammarstedt L. Impact of HPV in Oropharyngeal Cancer. J. Oncol. 2011, 509036 (2011).
8. D'souza G, Kreimer AR, Viscidi R et al. Case-control study of human papillomavirus and oropharyngeal cancer. N. Engl. J. Med. 356(19), 1944-1956 (2007).
9. Moscicki AB, Schiffman M, Burchell A et al. Updating the natural history of human papillomavirus and anogenital cancers. Vaccine 30(Suppl. 5), F24-F33 (2012).
10. Skamperle M, Kocjan BJ, Maver PJ, Seme K, Poljak M. Human papillomavirus (HPV) prevalence and HPV type distribution in cervical, vulvar, and anal cancers in central and eastern Europe. Acta Dermatovenerol. Alp. Panonica Adriat. 22(1), 1-5 (2013).
11. De Martel C, Ferlay J, Franceschi S et al. Global burden of cancers attributable to infections in 2008: a review and synthetic analysis. Lancet Oncol. 13(6), 607-615 (2012).
12. Glaxosmithkline Vaccine HPVSG, Romanowski B, De Borba PC et al. Sustained efficacy and immunogenicity of the human papillomavirus (HPV)-16/AS04- adjuvanted vaccine: analysis of a randomised placebo-controlled trial up to 6.4 years. Lancet 374(9706), 1975-1985 (2009).
13. Brown DR, Kjaer SK, Sigurdsson K et al. The impact of quadrivalent human papillomavirus (HPV; types 6, 11, 16, and 18) L1 virus-like particle vaccine on infection and disease due to oncogenic nonvaccine HPV types in generally HPV-naive women aged 16-26 years. J. Infect. Dis. 199(7), 926-935 (2009).
14. Lehtinen M, Paavonen J, Wheeler CM et al. Overall efficacy of HPV-16/AS04-adjuvanted vaccine against grade or greater cervical intraepithelial neoplasia: 4-year end-of-study analysis of the randomised, double-blind PATRICIA trial. Lancet Oncol. 13(1), 89-99 (2012).
15. Munoz N, Kjaer SK, Sigurdsson K et al. Impact of human papillomavirus (HPV)-6/11/16/18 vaccine on all HPV-associated genital diseases in young women. J. Natl Cancer Inst. 102(5), 325-339 (2010).
16. Paavonen J, Naud P, Salmeron J et al. Efficacy of human papillomavirus (HPV)-16/18 AS04-adjuvanted vaccine against cervical infection and precancer caused by oncogenic HPV types (PATRICIA): final analysis of a double-blind, randomised study in young women. Lancet 374(9686), 301-314 (2009).
17. Doorbar J, Quint W, Banks L et al. The biology and life-cycle of human papillomaviruses. Vaccine 30 (Suppl. 5), F55-F70 (2012).
18. Buck CB, Cheng N, Thompson CD et al. Arrangement of L2 within the papillomavirus capsid. J. Virol. 82(11), 5190-5197 (2008).
19. Day PM, Kines RC, Thompson CD et al. In vivo mechanisms of vaccine-induced protection against HPV infection. Cell Host Microbe 8(3), 260-270 (2010).
20. Day PM, Gambhira R, Roden RB, Lowy DR, Schiller JT. Mechanisms of human papillomavirus type 16 neutralization by l2 cross-neutralizing and l1 type-specific antibodies. J. Virol. 82(9), 4638-4646 (2008).
21. Conway MJ, Cruz L, Alam S, Christensen ND, Meyers C. Cross-neutralization potential of native human papillomavirus N-terminal L2 epitopes. PLoS ONE 6(2), e16405 (2011).
22. Day PM, Schiller JT. The role of furin in papillomavirus infection. Future Microbiol. 4(10), 1255-1262 (2009).
23. Richards RM, Lowy DR, Schiller JT, Day PM. Cleavage of the papillomavirus minor capsid protein, L2, at a furin consensus site is necessary for infection. Proc. Natl Acad. Sci. USA 103(5), 1522-1527 (2006).
24. Kondo K, Ishii Y, Mori S, Shimabukuro S, Yoshikawa H, Kanda T. Nuclear location of minor capsid protein L2 is required for expression of a reporter plasmid packaged in HPV51 pseudovirions. Virology 394(2), 259-265 (2009).
25. Marusic MB, Ozbun MA, Campos SK, Myers MP, Banks L. Human papillomavirus L2 facilitates viral escape from late endosomes via sorting nexin 17. Traffic 13(3), 455-467 (2012).
26. Bronnimann MP, Chapman JA, Park CK, Campos SK. A transmembrane domain and GxxxG motifs within L2 are essential for papillomavirus infection. J. Virol. 87(1), 464-473 (2013).
27. Ishii Y, Ozaki S, Tanaka K, Kanda T. Human papillomavirus 16 minor capsid protein L2 helps capsomeres assemble independently of intercapsomeric disulfide bonding. Virus Genes 31(3), 321-328 (2005).
28. Tota JE, Chevarie-Davis M, Richardson LA, Devries M, Franco EL. Epidemiology and burden of HPV infection and related diseases: implications for prevention strategies. Prev. Med. 53 (Suppl. 1), S12-S21 (2011).
29. Guan P, Howell-Jones R, Li N et al. Human papillomavirus types in 115,789 HPV-positive women: a meta-analysis from cervical infection to cancer. Int. J. Cancer 131(10), 2349-2359 (2012).
30. Vinodhini K, Shanmughapriya S, Das BC, Natarajaseenivasan K. Prevalence and risk factors of HPV infection among women from various provinces of the world. Arch. Gynecol. Obstet. 285(3), 771-777 (2012).
31. Bosch FX, Burchell AN, Schiffman M et al. Epidemiology and natural history of human papillomavirus infections and type-specific implications in cervical neoplasia. Vaccine (Suppl. 10), K1-K16 (2008).
32. Quek SC, Lim BK, Domingo E et al. Human papillomavirus type distribution in invasive cervical cancer and high-grade cervical intraepithelial neoplasia across countries in Asia. Int. J. Gynecol. Cancer 23(1), 148-156 (2013).
33. De Oliveira CM, Fregnani JH, Carvalho JP, Longatto-Filho A, Levi JE. Human papillomavirus genotypes distribution in invasive cervical cancer cases from Brazil. BMC Cancer 13, 357 (2013).
34. De Sanjose S, Quint WG, Alemany L et al. Human papillomavirus genotype attribution in invasive cervical cancer: a retrospective cross-sectional worldwide study. Lancet Oncol. 11(11), 1048-1056 (2010).
35. Hagensee ME, Yaegashi N, Galloway DA. Self-assembly of human papillomavirus type 1 capsids by expression of the L1 protein alone or by coexpression of the L1 and L2 capsid proteins. J. Virol. 67(1), 315-322 (1993).
36. Kirnbauer R, Booy F, Cheng N, Lowy DR, Schiller JT. Papillomavirus L1 major capsid protein self-assembles into virus-like particles that are highly immunogenic. Proc. Natl Acad. Sci. USA 89(24), 12180-12184 (1992).
37. Rose RC, Bonnez W, Reichman RC, Garcea RL. Expression of human papillomavirus type 11 L1 protein in insect cells: in vivo and in vitro assembly of viruslike particles. J. Virol. 67(4), 1936-1944 (1993).
38. Tabrizi SN, Brotherton JM, Kaldor JM et al . Fall in human papillomavirus prevalence following a national vaccination program. J. Infect. Dis. 206(11), 1645-1651 (2012).
39. Markowitz LE, Hariri S, Lin C et al. Reduction in human papillomavirus (HPV) prevalence among young women following HPV vaccine introduction in the United States, National Health and Nutrition Examination Surveys, 2003-2010. J. Infect. Dis. 208(3), 385-393 (2013).
40. Einstein MH, Baron M, Levin MJ et al. Comparison of the immunogenicity and safety of Cervarix and Gardasil human papillomavirus (HPV) cervical cancer vaccines in healthy women aged 18-45 years. Human Vaccin. 5(10), 705-719 (2009).
41. Roberts JN, Buck CB, Thompson CD et al. Genital transmission of HPV in a mouse model is potentiated by nonoxynol-9 and inhibited by carrageenan. Nat. Med. 13(7), 857-861 (2007).
42. Pastrana DV, Buck CB, Pang YY et al. Reactivity of human sera in a sensitive, high-throughput pseudovirus-based papillomavirus neutralization assay for HPV16 and HPV18. Virology 321(2), 205-216 (2004).
43. Longet S, Schiller JT, Bobst M, Jichlinski P, Nardelli-Haefliger D. A murine genital-challenge model is a sensitive measure of protective antibodies against human papillomavirus infection. J.Virol. 85(24), 13253-13259 (2011).
44. Roteli-Martins CM, Naud P, De Borba P et al. Sustained immunogenicity and efficacy of the HPV-16/18 AS04-adjuvanted vaccine: up to 8.4 years of follow-up. Hum. Vaccin. Immunother. 8(3), 390-397 (2012).
45. Chackerian B. Virus-like particles: flexible platforms for vaccine development. Expert Rev. Vaccines 6(3), 381-390 (2007).
46. Grgacic EV, Anderson DA. Virus-like particles: passport to immune recognition. Methods 40(1), 60-65 (2006).
47. Harro CD, Pang YY, Roden RB et al. Safety and immunogenicity trial in adult volunteers of a human papillomavirus L1 virus-like particle vaccine. J. Natl Cancer Inst. 93(4), 284-292 (2001).
48. Schiller JT, Castellsague X, Garland SM. A review of clinical trials of human papillomavirus prophylactic vaccines. Vaccine 30 (Suppl. 5), F123-F138 (2012).
49. Einstein MH, Baron M, Levin MJ et al. Comparison of the immunogenicity of the human papillomavirus (HPV)-16/18 vaccine and the HPV-6/11/16/18 vaccine for oncogenic non-vaccine types HPV-31 and HPV-45 in healthy women aged 18-45 years. Hum. Vaccin. 7(12), 1359-1373 (2011).
50. Draper E, Bissett SL, Howell-Jones R et al. A randomized, observer-blinded immunogenicity trial of Cervarix((R)) and Gardasil((R)) Human Papillomavirus vaccines in 12-15 year old girls. PLoS ONE 8(5), e61825 (2013).
51. Kreimer AR, Rodriguez AC, Hildesheim A et al. Proof-of-principle evaluation of the efficacy of fewer than three doses of a bivalent HPV16/18 vaccine. J. Natl Cancer Inst. 103(19), 1444-1451 (2011).
52. Kiatpongsan S, Campos NG, Kim JJ. Potential benefits of second-generation human papillomavirus vaccines. PLoS ONE 7(11), e48426 (2012).
53. Tumban E, Peabody J, Peabody DS, Chackerian B. A pan-HPV vaccine based on bacteriophage PP7 VLPs displaying broadly cross-neutralizing epitopes from the HPV minor capsid protein, L2. PLoS ONE 6(8), e23310 (2011).
54. Campo MS, Grindlay GJ, O'neil BW, Chandrachud LM, Mcgarvie GM, Jarrett WF. Prophylactic and therapeutic vaccination against a mucosal papillomavirus. J. Gen. Virol. 74 (Pt 6), 945-953 (1993).
55. Christensen ND, Kreider JW, Kan NC, Diangelo SL. The open reading frame L2 of cottontail rabbit papillomavirus contains antibody-inducing neutralizing epitopes. Virology 181(2), 572-579 (1991).
56. Lin YL, Borenstein LA, Selvakumar R, Ahmed R, Wettstein FO. Effective vaccination against papilloma development by immunization with L1 or L2 structural protein of cottontail rabbit papillomavirus. Virology 187(2), 612-619 (1992).
57. Roden RB, Yutzy WHT, Fallon R, Inglis S, Lowy DR, Schiller JT. Minor capsid protein of human genital papillomaviruses contains subdominant, cross-neutralizing epitopes. Virology 270(2), 254-257 (2000).
58. Gambhira R, Karanam B, Jagu S et al. A protective and broadly cross-neutralizing epitope of human papillomavirus L2. J. Virol. 81(24), 13927-13931 (2007).
59. Campos SK, Ozbun MA. Two highly conserved cysteine residues in HPV16 L2 form an intramolecular disulfide bond and are critical for infectivity in human keratinocytes. PLoS ONE 4(2), e4463 (2009).
60. Seitz H, Dantheny T, Burkart F, Ottonello S, Muller M. Influence of oxidation and multimerization on the immunogenicity of a thioredoxin-l2 prophylactic papillomavirus vaccine. Clin.Vaccine Immunol. 20(7), 1061-1069 (2013).
61. Tumban E, Peabody J, Tyler M, Peabody DS, Chackerian B. VLPs displaying a single L2 epitope induce broadly cross-neutralizing antibodies against human papillomavirus. PLoS ONE 7(11), e49751 (2012).
62. Slupetzky K, Gambhira R, Culp TD et al. A papillomavirus-like particle (VLP) vaccine displaying HPV16 L2 epitopes induces cross-neutralizing antibodies to HPV11. Vaccine 25(11), 2001-2010 (2007).
63. Varsani A, Williamson AL, De Villiers D, Becker I, Christensen ND, Rybicki EP. 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(15), 8386-8393 (2003).
64. Kawana K, Yasugi T, Kanda T et al. Safety and immunogenicity of a peptide containing the cross-neutralization epitope of HPV16 L2 administered nasally in healthy volunteers. Vaccine 21(27-30), 4256-4260 (2003).
65. Jagu S, Karanam B, Gambhira R et al. Concatenated multitype L2 fusion proteins as candidate prophylactic pan-human papillomavirus vaccines. J. Natl Cancer Inst. 101(11), 782-792 (2009).
66. Jagu S, Kwak K, Garcea RL, Roden RB. Vaccination with multimeric L2 fusion protein and L1 VLP or capsomeres to broaden protection against HPV infection. Vaccine 28(28), 4478-4486 (2010).
67. Thones N, Herreiner A, Schadlich L, Piuko K, Muller M. 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(11), 5472-5485 (2008).
68. Jagu S, Kwak K, Karanam B et al. Optimization of multimeric human papillomavirus L2 vaccines. PLoS ONE 8(1), e55538 (2013).
69. Kondo K, Ochi H, Matsumoto T, Yoshikawa H, Kanda T. Modification of human papillomavirus-like particle vaccine by insertion of the cross-reactive L2-epitopes. J. Med. Virol. 80(5), 841-846 (2008).
70. Mcgrath M, De Villiers GK, Shephard E, Hitzeroth, Ii, Rybicki EP. Development of human papillomavirus chimaeric L1/L2 candidate vaccines. Arch. Virol. 158(10), 2079-2088 (2013).
71. Schellenbacher C, Roden R, Kirnbauer R. Chimeric L1-L2 virus-like particles as potential broad-spectrum human papillomavirus vaccines. J. Virol. 83(19), 10085-10095 (2009).
72. Schellenbacher C, Kwak K, Fink D et al. Efficacy of RG1-VLP Vaccination against Infections with Genital and Cutaneous Human Papillomaviruses. J. Invest. Dermatol. 133(12), 2706-2713 (2013).
73. Smith ML, Lindbo JA, Dillard-Telm S et al. Modified tobacco mosaic virus particles as scaffolds for display of protein antigens for vaccine applications. Virology 348(2), 475-488 (2006).
74. Cerovska N, Hoffmeisterova H, Moravec T et al. Transient expression of Human papillomavirus type 16 L2 epitope fused to N-and C-terminus of coat protein of Potato virus X in plants. J. Biosci. 37(1), 125-133 (2012).
75. Nieto K, Weghofer M, Sehr P et al. Development of AAVLP(HPV16/31L2) particles as broadly protective HPV vaccine candidate. PLoS ONE 7(6), e39741 (2012).
76. Caldeira Jdo C, Medford A, Kines RC et al. Immunogenic display of diverse peptides, including a broadly cross-type neutralizing human papillomavirus L2 epitope, on virus-like particles of the RNA bacteriophage PP7. Vaccine 28(27), 4384-4393 (2010).
77. Tumban E, Peabody J, Peabody DS, Chackerian B. A universal virus-like particlebased vaccine for human papillomavirus: Longevity of protection and role of endogenous and exogenous adjuvants. Vaccine 31(41), 4647-4654 (2013).
78. Day PM, Pang YY, Kines RC, Thompson CD, Lowy DR, Schiller JT. A human papillomavirus (HPV) in vitro neutralization assay that recapitulates the in vitro process of infection provides a sensitive measure of HPV L2 infection-inhibiting antibodies. Clin. Vaccine Immunol.19(7), 1075-1082 (2012).
79. Alphs HH, Gambhira R, Karanam B et al. 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(15), 5850-5855 (2008).
80. Rubio I, Bolchi A, Moretto N et al. Potent anti-HPV immune responses induced by tandem repeats of the HPV16 L2 (20 -38) peptide displayed on bacterial thioredoxin. Vaccine 27(13), 1949-1956 (2009).
81. Yoon SW, Lee TY, Kim SJ et al. Oral administration of HPV-16 L2 displayed on Lactobacillus casei induces systematic and mucosal cross-neutralizing effects in Balb/c mice. Vaccine 30(22), 3286-3294 (2012).
82. Jagu S, Malandro N, Kwak K et al. A multimeric L2 vaccine for prevention of animal papillomavirus infections. Virology 420(1), 43-50 (2011).
83. Broad spectrum HPV (human papillomavirus) vaccine study in 16-to 26-year-old women (V503-001 AM3). http://clinicaltrials.gov/ct2/show/NCT00543543