940
Views
89
CrossRef citations to date
0
Altmetric
Review

Virus-like particles for the prevention of human papillomavirus-associated malignancies

&
Pages 129-141 | Published online: 09 Jan 2014

References

  • 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).
  • Dillner J, Kjaer SK, Wheeler CM et al. Four year efficacy of prophylactic human papillomavirus quadrivalent vaccine against low grade cervical, vulvar, and vaginal intraepithelial neoplasia and anogenital warts: randomised controlled trial. BMJ 341, c3493 (2010).
  • Lehtinen M, Paavonen J, Wheeler CM et al.; HPV PATRICIA Study Group. Overall efficacy of HPV-16/18 AS04-adjuvanted vaccine against grade 3 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).
  • Kaufmann AM, Nitschmann S. [Vaccine against human papillomavirus: PATRICIA Study (Papilloma Trial Against Cancer In Young Adults)]. Der. Internist. 51(3), 412–413 (2010).
  • Kreimer AR, González P, Katki HA et al.; CVT Vaccine Group. Efficacy of a bivalent HPV 16/18 vaccine against anal HPV 16/18 infection among young women: a nested analysis within the Costa Rica Vaccine Trial. Lancet Oncol. 12(9), 862–870 (2011).
  • 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).
  • Romanowski B, de Borba PC, Naud PS et al.; GlaxoSmithKline Vaccine HPV-007 Study Group. Sustained efficacy and immunogenicity of the human papillomavirus (HPV)-16/18 AS04-adjuvanted vaccine: analysis of a randomised placebo-controlled trial up to 6.4 years. Lancet 374(9706), 1975–1985 (2009).
  • Harper DM, Franco EL, Wheeler CM et al.; HPV Vaccine Study group. 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(9518), 1247–1255 (2006).
  • Mao C, Koutsky LA, Ault KA et al. Efficacy of human papillomavirus-16 vaccine to prevent cervical intraepithelial neoplasia: a randomized controlled trial. Obstet. Gynecol. 107(1), 18–27 (2006).
  • Roldão A, Mellado MC, Castilho LR, Carrondo MJ, Alves PM. Virus-like particles in vaccine development. Expert Rev. Vaccines 9(10), 1149–1176 (2010).
  • Chackerian B, Lenz P, Lowy DR, Schiller JT. Determinants of autoantibody induction by conjugated papillomavirus virus-like particles. J. Immunol. 169(11), 6120–6126 (2002).
  • Lenz P, Day PM, Pang YY et al. Papillomavirus-like particles induce acute activation of dendritic cells. J. Immunol. 166(9), 5346–5355 (2001).
  • Lenz P, Thompson CD, Day PM, Bacot SM, Lowy DR, Schiller JT. Interaction of papillomavirus virus-like particles with human myeloid antigen-presenting cells. Clin. Immunol. 106(3), 231–237 (2003).
  • Buck CB, Trus BL. The papillomavirus virion: a machine built to hide molecular Achilles’ heels. Adv. Exp. Med. Biol. 726, 403–422 (2012).
  • Chen XS, Garcea RL, Goldberg I, Casini G, Harrison SC. Structure of small virus-like particles assembled from the L1 protein of human papillomavirus 16. Mol. Cell 5(3), 557–567 (2000).
  • Doorbar J. Molecular biology of human papillomavirus infection and cervical cancer. Clin. Sci. 110(5), 525–541 (2006).
  • de Villiers EM, Fauquet C, Broker TR, Bernard HU, zur Hausen H. Classification of papillomaviruses. Virology 324(1), 17–27 (2004).
  • de Sanjose S, Quint WG, Alemany L et al.; Retrospective International Survey and HPV Time Trends Study Group. Human papillomavirus genotype attribution in invasive cervical cancer: a retrospective cross-sectional worldwide study. Lancet Oncol. 11(11), 1048–1056 (2010).
  • Roden R, Wu TC. How will HPV vaccines affect cervical cancer? Nat. Rev. Cancer 6(10), 753–763 (2006).
  • Walboomers JM, Jacobs MV, Manos MM et al. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J. Pathol. 189(1), 12–19 (1999).
  • Donovan B, Franklin N, Guy R et al. Quadrivalent human papillomavirus vaccination and trends in genital warts in Australia: analysis of national sentinel surveillance data. Lancet Infect. Dis. 11(1), 39–44 (2011).
  • Rolando H, Quint W, Hildesheim A et al.; FTCV. Efficacy of an HPV16/18 vaccine against oral HPV infections: a randomized clinical trial. 12(9), 862–870 (2012).
  • Mcneil C. Who invented the VLP cervical cancer vaccines? J. Natl Cancer Institute 98(7), 433 (2006).
  • Einstein MH, Baron M, Levin MJ et al.; HPV-010 Study Group. Comparison of the immunogenicity and safety of Cervarix and Gardasil human papillomavirus (HPV) cervical cancer vaccines in healthy women aged 18–45 years. Hum. Vaccin. 5(10), 705–719 (2009).
  • Koutsky LA, Ault KA, Wheeler CM et al.; Proof of Principle Study Investigators. A controlled trial of a human papillomavirus type 16 vaccine. N. Engl. J. Med. 347(21), 1645–1651 (2002).
  • Poland GA, Jacobson RM, Koutsky LA et al. Immunogenicity and reactogenicity of a novel vaccine for human papillomavirus 16: a 2-year randomized controlled clinical trial. Mayo Clin. Proc. 80(5), 601–610 (2005).
  • Villa LL, Costa RL, Petta CA 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(5), 271–278 (2005).
  • Breitburd F, Kirnbauer R, Hubbert NL et al. Immunization with viruslike particles from cottontail rabbit papillomavirus (CRPV) can protect against experimental CRPV infection. J. Virol. 69(6), 3959–3963 (1995).
  • 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).
  • Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA. Cancer J. Clin. 61(2), 69–90 (2011).
  • Clemens JD, Jodar L. Translational research to assist policy decisions about introducing new vaccines in developing countries. J. Health. Popul. Nutr. 22(3), 223–231 (2004).
  • Schiffman M, Wacholder S. Success of HPV vaccination is now a matter of coverage. Lancet Oncol. 13(1), 10–12 (2012).
  • Lowy DR, Solomon D, Hildesheim A, Schiller JT, Schiffman M. Human papillomavirus infection and the primary and secondary prevention of cervical cancer. Cancer 113(Suppl. 7), 1980–1993 (2008).
  • Paavonen J, Jenkins D, Bosch FX et al.; HPV PATRICIA study group. Efficacy of a prophylactic adjuvanted bivalent L1 virus-like-particle vaccine against infection with human papillomavirus types 16 and 18 in young women: an interim analysis of a Phase III double-blind, randomised controlled trial. Lancet 369(9580), 2161–2170 (2007).
  • Wheeler CM, Castellsagué X, Garland SM et al.; HPV PATRICIA Study Group. Cross-protective efficacy of HPV-16/18 AS04-adjuvanted vaccine against cervical infection and precancer caused by non-vaccine oncogenic HPV types: 4-year end-of-study analysis of the randomised, double-blind PATRICIA trial. Lancet Oncol. 13(1), 100–110 (2012).
  • Lehtinen M, Paavonen J, Wheeler CM et al.; HPV PATRICIA Study Group. Overall efficacy of HPV-16/18 AS04-adjuvanted vaccine against grade 3 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).
  • Roden R, Monie A, Wu TC. The impact of preventive HPV vaccination. Discov. Med. 6(35), 175–181 (2006).
  • Schiller JT, Day PM, Kines RC. Current understanding of the mechanism of HPV infection. Gynecol. Oncol. 118(Suppl. 1), S12–S17 (2010).
  • Schiller JT, Lowy DR. Immunogenicity testing in human papillomavirus virus-like-particle vaccine trials. J. Infect. Dis. 200(2), 166–171 (2009).
  • 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).
  • Fay A, Yutzy WH 4th, Roden RB, Moroianu J. The positively charged termini of L2 minor capsid protein required for bovine papillomavirus infection function separately in nuclear import and DNA binding. J. Virol. 78(24), 13447–13454 (2004).
  • 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).
  • 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).
  • 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).
  • Embers ME, Budgeon LR, Pickel M, Christensen ND. Protective immunity to rabbit oral and cutaneous papillomaviruses by immunization with short peptides of L2, the minor capsid protein. J. Virol. 76(19), 9798–9805 (2002).
  • Campo MS, O’Neil BW, Grindlay GJ, Curtis F, Knowles G, Chandrachud L. A peptide encoding a B-cell epitope from the N-terminus of the capsid protein L2 of bovine papillomavirus-4 prevents disease. Virology 234(2), 261–266 (1997).
  • Chandrachud LM, Grindlay GJ, McGarvie GM et al. Vaccination of cattle with the N-terminus of L2 is necessary and sufficient for preventing infection by bovine papillomavirus-4. Virology 211(1), 204–208 (1995).
  • Gambhira R, Jagu S, Karanam B et al. Protection of rabbits against challenge with rabbit papillomaviruses by immunization with the N terminus of human papillomavirus type 16 minor capsid antigen L2. J. Virol. 81(21), 11585–11592 (2007).
  • 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).
  • Kawana K, Kawana Y, Yoshikawa H, Taketani Y, Yoshiike K, Kanda T. Nasal immunization of mice with peptide having a cross-neutralization epitope on minor capsid protein L2 of human papillomavirus type 16 elicit systemic and mucosal antibodies. Vaccine 19(11–12), 1496–1502 (2001).
  • Rubio I, Seitz H, Canali E et al. The N-terminal region of the human papillomavirus L2 protein contains overlapping binding sites for neutralizing, cross-neutralizing and non-neutralizing antibodies. Virology 409(2), 348–359 (2011).
  • Karanam B, Jagu S, Huh WK, Roden RB. Developing vaccines against minor capsid antigen L2 to prevent papillomavirus infection. Immunol. Cell Biol. 87(4), 287–299 (2009).
  • Buck CB, Pastrana DV, Lowy DR, Schiller JT. Generation of HPV pseudovirions using transfection and their use in neutralization assays. Methods Mol. Med. 119, 445–462 (2005).
  • 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).
  • 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).
  • Roden RB, Greenstone HL, Kirnbauer R et al. in vitro generation and type-specific neutralization of a human papillomavirus type 16 virion pseudotype. J. Virol. 70(9), 5875–5883 (1996).
  • 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).
  • 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).
  • 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).
  • Jagu S, Malandro N, Kwak K et al. A multimeric L2 vaccine for prevention of animal papillomavirus infections. Virology 420(1), 43–50 (2011).
  • Roden RB, Yutzy WH 4th, 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).
  • Buck CB, Cheng N, Thompson CD et al. Arrangement of L2 within the papillomavirus capsid. J. Virol. 82(11), 5190–5197 (2008).
  • 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).
  • Johnson KM, Kines RC, Roberts JN, Lowy DR, Schiller JT, Day PM. Role of heparan sulfate in attachment to and infection of the murine female genital tract by human papillomavirus. J. Virol. 83(5), 2067–2074 (2009).
  • Kines RC, Thompson CD, Lowy DR, Schiller JT, Day PM. The initial steps leading to papillomavirus infection occur on the basement membrane prior to cell surface binding. Proc. Natl Acad. Sci. USA 106(48), 20458–20463 (2009).
  • Selinka HC, Giroglou T, Nowak T, Christensen ND, Sapp M. Further evidence that papillomavirus capsids exist in two distinct conformations. J. Virol. 77(24), 12961–12967 (2003).
  • Roden RB, Day PM, Bronzo BK et al. Positively charged termini of the L2 minor capsid protein are necessary for papillomavirus infection. J. Virol. 75(21), 10493–10497 (2001).
  • 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).
  • 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).
  • 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).
  • 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).
  • Rose RC, White WI, Li M, Suzich JA, Lane C, Garcea RL. Human papillomavirus type 11 recombinant L1 capsomeres induce virus-neutralizing antibodies. J. Virol. 72(7), 6151–6154 (1998).
  • Wu WH, Gersch E, Kwak K et al. Capsomer vaccines protect mice from vaginal challenge with human papillomavirus. PLoS ONE 6(11), e27141 (2011).
  • Palmer KE, Benko A, Doucette SA et al. Protection of rabbits against cutaneous papillomavirus infection using recombinant tobacco mosaic virus containing L2 capsid epitopes. Vaccine 24(26), 5516–5525 (2006).
  • 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).
  • Cerovská N, Hoffmeisterová H, Pecenková T et al. Transient expression of HPV16 E7 peptide (aa 44–60) and HPV16 L2 peptide (aa 108–120) on chimeric potyvirus-like particles using potato virus X-based vector. Protein Expr. Purif. 58(1), 154–161 (2008).
  • 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).
  • 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).
  • 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).
  • Suba EJ, Raab SS. Lessons learned from successful Papanicolaou cytology cervical cancer prevention in the Socialist Republic of Vietnam. Diagn. Cytopathol. 40(4), 355–366 (2012).
  • Lin K, Doolan K, Hung CF, Wu TC. Perspectives for preventive and therapeutic HPV vaccines. J. Formos. Med. Assoc. 109(1), 4–24 (2010).
  • Hung CF, Ma B, Monie A, Tsen SW, Wu TC. Therapeutic human papillomavirus vaccines: current clinical trials and future directions. Expert Opin. Biol. Ther. 8(4), 421–439 (2008).
  • Wu CY, Monie A, Pang X, Hung CF, Wu TC. Improving therapeutic HPV peptide-based vaccine potency by enhancing CD4+ T help and dendritic cell activation. J. Biomed. Sci. 17, 88 (2010).
  • Barrios K, Celis E. TriVax-HPV: an improved peptide-based therapeutic vaccination strategy against human papillomavirus-induced cancers. Cancer Immunol. Immunother. 61(8), 1307–1317 (2012).
  • Rudolf MP, Fausch SC, Da Silva DM, Kast WM. 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(10), 5917–5924 (2001).
  • Wakabayashi MT, Da Silva DM, Potkul RK, Kast WM. Comparison of human papillomavirus type 16 L1 chimeric virus-like particles versus L1/L2 chimeric virus-like particles in tumor prevention. Intervirology 45(4–6), 300–307 (2002).
  • Paz De La Rosa G, Monroy-Garcia A, Mora-Garcia Mde L et al. An HPV 16 L1-based chimeric human papilloma virus-like particles containing a string of epitopes produced in plants is able to elicit humoral and cytotoxic T-cell activity in mice. Virol. J. 6, 2 (2009).
  • Bian T, Wang Y, Lu Z et al. Human papillomavirus type 16 L1E7 chimeric capsomeres have prophylactic and therapeutic efficacy against papillomavirus in mice. Mol. Cancer Ther. 7(5), 1329–1335 (2008).
  • Müller M, Zhou J, Reed TD et al. Chimeric papillomavirus-like particles. Virology 234(1), 93–111 (1997).
  • Schäfer K, Müller M, Faath S et al. Immune response to human papillomavirus 16 L1E7 chimeric virus-like particles: induction of cytotoxic T cells and specific tumor protection. Int. J. Cancer 81(6), 881–888 (1999).
  • Sharma C, Dey B, Wahiduzzaman M, Singh N. Human papillomavirus 16 L1-E7 chimeric virus like particles show prophylactic and therapeutic efficacy in murine model of cervical cancer. Vaccine 30(36), 5417–5424 (2012).
  • Kaufmann AM, Nieland J, Schinz M et al. HPV16 L1E7 chimeric virus-like particles induce specific HLA-restricted T cells in humans after in vitro vaccination. Int. J. Cancer 92(2), 285–293 (2001).
  • Kaufmann AM, Nieland JD, Jochmus I et al. Vaccination trial with HPV16 L1E7 chimeric virus-like particles in women suffering from high grade cervical intraepithelial neoplasia (CIN 2/3). Int. J. Cancer 121(12), 2794–2800 (2007).
  • Da Silva DM, Pastrana DV, Schiller JT, Kast WM. Effect of preexisting neutralizing antibodies on the anti-tumor immune response induced by chimeric human papillomavirus virus-like particle vaccines. Virology 290(2), 350–360 (2001).
  • Da Silva DM, Schiller JT, Kast WM. Heterologous boosting increases immunogenicity of chimeric papillomavirus virus-like particle vaccines. Vaccine 21(23), 3219–3227 (2003).
  • Trimble CL, Clark RA, Thoburn C et al. Human papillomavirus 16-associated cervical intraepithelial neoplasia in humans excludes CD8 T cells from dysplastic epithelium. J. Immunol. 185(11), 7107–7114 (2010).
  • Welters MJ, Kenter GG, de Vos van Steenwijk PJ et al. Success or failure of vaccination for HPV16-positive vulvar lesions correlates with kinetics and phenotype of induced T-cell responses. Proc. Natl Acad. Sci. USA 107(26), 11895–11899 (2010).
  • van der Burg SH, Piersma SJ, de Jong A et al. Association of cervical cancer with the presence of CD4+ regulatory T cells specific for human papillomavirus antigens. Proc. Natl Acad. Sci. USA 104(29), 12087–12092 (2007).
  • Chuang CM, Hoory T, Monie A, Wu A, Wang MC, Hung CF. Enhancing therapeutic HPV DNA vaccine potency through depletion of CD4+CD25+ T regulatory cells. Vaccine 27(5), 684–689 (2009).
  • Chuang CM, Monie A, Wu A, Hung CF. Combination of apigenin treatment with therapeutic HPV DNA vaccination generates enhanced therapeutic antitumor effects. J. Biomed. Sci. 16, 49 (2009).
  • Graham BS, Kines RC, Corbett KS et al. Mucosal delivery of human papillomavirus pseudovirus-encapsidated plasmids improves the potency of DNA vaccination. Mucosal Immunol. 3(5), 475–486 (2010).
  • Gordon SN, Kines RC, Kutsyna G et al. Targeting the vaginal mucosa with human papillomavirus pseudovirion vaccines delivering simian immunodeficiency virus DNA. J. Immunol. 188(2), 714–723 (2012).
  • Peng S, Monie A, Kang TH, Hung CF, Roden R, Wu TC. Efficient delivery of DNA vaccines using human papillomavirus pseudovirions. Gene Ther. 17(12), 1453–1464 (2010).

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.