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Research Paper

Displaying 31RG-1 peptide on the surface of HPV16 L1 by use of a human papillomavirus chimeric virus-like particle induces cross-neutralizing antibody responses in mice

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Pages 2025-2033 | Received 23 Jan 2018, Accepted 26 Mar 2018, Published online: 14 May 2018

References

  • de Martel C, Ferlay J, Franceschi S, Vignat J, Bray F, Forman D, Plummer M. Global burden of cancers attributable to infections in 2008: a review and synthetic analysis. Lancet Oncol [Internet]. 2012 [cited 2016 Aug 21];13:607–15. Available from: http://www.ncbi.nlm.nih.gov/pubmed/22575588 doi:10.1016/S1470-2045(12)70137-7.
  • Cubie HA. Diseases associated with human papillomavirus infection. Virology [Internet]. 2013;445:21–34. Available from: doi:10.1016/j.virol.2013.06.007.
  • Arbyn M, Tommasino M, Depuydt C, Dillner J. Are 20 human papillomavirus types causing cervical cancer? J Pathol. 2014;234:431–5. doi:10.1002/path.4424. PMID:25124771
  • Paavonen J, Jenkins D, Bosch FX, Naud P, Salmerón J, Wheeler CM, Chow SN, Apter DL, Kitchener HC, Castellsague X, et al. 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 2007;369:2161–70. doi:10.1016/S0140-6736(07)60946-5. PMID:17602732
  • Schiller JT, Castellsagué X, Garland SM. A review of clinical trials of human papillomavirus prophylactic vaccines. Vaccine [Internet]. 2012;30:F123–38. Available from: doi:10.1016/j.vaccine.2012.04.108.
  • Garland SM, Kjaer SK, Muñoz N, Block SL, Brown DR, Dinubile MJ, Lindsay BR, Kuter BJ, Perez G, Dominiak-Felden G, et al. Impact and effectiveness of the quadrivalent human papillomavirus vaccine: A systematic review of 10 years of real-world experience. Clin Infect Dis. 2016;63:519–27. doi:10.1093/cid/ciw354. PMID:27230391
  • Romanowski B, Schwarz TF, Ferguson L, Peters K, Dionne M, Behre U, Schulze K, Hillemanns P, Suryakiran P, Thomas F, et al. Sustained immunogenicity of the HPV-16/18 AS04-adjuvanted vaccine administered as a two-dose schedule in adolescent girls: Five-year clinical data and modeling predictions from a randomized study. Hum Vaccin Immunother [Internet]. 2016;12:20–9. Available from: http://www.ncbi.nlm.nih.gov/pubmed/26176261 doi:10.1080/21645515.2015.1065363.
  • Vesikari T, Brodszki N, van Damme P, Diez-Domingo J, Icardi G, Petersen LK, Tran C, Thomas S, Luxembourg A, Baudin M. A randomized, double-blind, phase III study of the immunogenicity and safety of a 9-valent human papillomavirus L1 virus-like particle vaccine (V503) Versus Gardasil® in 9–15-year-old girls. Pediatr Infect Dis J [Internet]. 2015;34:992–8. Available from: http://www.ncbi.nlm.nih.gov/pubmed/26090572 doi:10.1097/INF.0000000000000773.
  • Meta-analysis performed by IARC's Infections and Cancer Epidemiology Group [Internet]. ICO HPV Inf. Cent. [cited 2017 Aug 30]; Available from: http://www.hpvcentre.net/parser.php?xml=M1_Cervical cancer by histology_HPV type distribution&iso=XWX_CHN&title=M1. HPV prevalence estimates – Invasive cervical cancer – HPV type distribution (Country/Regions)
  • Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. CA Cancer J Clin [Internet]. 2015;65:87–108. Available from: doi:10.3322/caac.21262.
  • Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D, Bray F. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J cancer [Internet]. 2015;136:E359–86. Available from: http://www.ncbi.nlm.nih.gov/pubmed/25220842 doi:10.1002/ijc.29210.
  • Pastrana D V, Gambhira R, Buck CB, Pang YYS, Thompson CD, Culp TD, Christensen ND, Lowy DR, Schiller JT, Roden RBS. Cross-neutralization of cutaneous and mucosal Papillomavirus types with anti-sera to the amino terminus of L2. Virology. 2005;337:365–72. doi:10.1016/j.virol.2005.04.011. PMID:15885736
  • Jagu S, Karanam B, Gambhira R, Chivukula SV, Chaganti RJ, Lowy DR, Schiller JT, Roden RBS. Concatenated multitype L2 fusion proteins as candidate prophylactic pan-human papillomavirus vaccines. J Natl Cancer Inst. 2009;101:782–92. doi:10.1093/jnci/djp106. PMID:19470949
  • Chen X, Liu H, Wang Z, Wang S, Zhang T, Hu M, Qiao L, Xu X. Human papillomavirus 16L1-58L2 chimeric virus-like particles elicit durable neutralizing antibody responses against a broad-spectrum of human papillomavirus types. Oncotarget [Internet]. 2017;8:63333–44. Available from: http://www.oncotarget.com/fulltext/19327
  • Roden RBS, Yutzy WH, Fallon R, Inglis S, Lowy DR, Schiller JT. Minor capsid protein of human genital papillomaviruses contains subdominant, cross-neutralizing Epitopes. Virology [Internet]. 2000;270:254–7. Available from: http://linkinghub.elsevier.com/retrieve/pii/S0042682200902721 doi:10.1006/viro.2000.0272.
  • Gambhira R, Karanam B, Jagu S, Roberts JN, Buck CB, Bossis I, Alphs H, Culp T, Christensen ND, Roden RBS. A protective and broadly cross-neutralizing epitope of human papillomavirus L2. J Virol [Internet]. 2007;81:13927–31. Available from: doi:10.1128/JVI.00936-07.
  • Kawana Y, Kawana K, Yoshikawa H, Taketani Y, Yoshiike K, 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 [Internet]. 2001;75:2331–6. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=114816&tool=pmcentrez&rendertype=abstract doi:10.1128/JVI.75.5.2331-2336.2001.
  • Chen X, Liu H, Zhang T, Liu Y, Xie X, Wang Z, Xu X. A vaccine of L2 epitope repeats fused with a modified IgG1 Fc induced cross-neutralizing antibodies and protective immunity against divergent human papillomavirus types. PLoS One [Internet]. 2014;9:e95448. Available from: http://www.ncbi.nlm.nih.gov/pubmed/24802101 doi:10.1371/journal.pone.0095448.
  • Zhang T, Liu H, Chen X, Wang Z, Wang S, Qu C, Zhang J, Xu X. Lipidated L2 epitope repeats fused with a single-chain antibody fragment targeting human FcγRI elicited cross-neutralizing antibodies against a broad spectrum of human papillomavirus types. Vaccine [Internet]. 2016;34:5531–9. Available from: doi:10.1016/j.vaccine.2016.10.009.
  • Rubio I, Bolchi A, Moretto N, Canali E, Gissmann L, Tommasino M, M??ller M, Ottonello S. Potent anti-HPV immune responses induced by tandem repeats of the HPV16 L2 (20-38) peptide displayed on bacterial thioredoxin. Vaccine 2009;27:1949–56. doi:10.1016/j.vaccine.2009.01.102. PMID:19368776
  • Seitz H, Canali E, Ribeiro-Müller L, Pàlfi A, Bolchi A, Tommasino M, Ottonello S, Müller M. A three component mix of thioredoxin-L2 antigens elicits broadly neutralizing responses against oncogenic human papillomaviruses. Vaccine 2014;32:2610–7. doi:10.1016/j.vaccine.2014.03.033. PMID:24662712
  • Kalnin K, Tibbitts T, Yan Y, Stegalkina S, Shen L, Costa V, Sabharwal R, Anderson SF, Day PM, Christensen N, et al. Low doses of flagellin-L2 multimer vaccines protect against challenge with diverse papillomavirus genotypes. Vaccine 2014;32:3540–7. doi:10.1016/j.vaccine.2014.04.032. PMID:24780250
  • Kalnin K, Chivukula S, Tibbitts T, Yan Y, Stegalkina S, Shen L, Cieszynski J, Costa V, Sabharwal R, Anderson SF, et al. Incorporation of RG1 epitope concatemers into a self-adjuvanting Flagellin-L2 vaccine broaden durable protection against cutaneous challenge with diverse human papillomavirus genotypes. Vaccine [Internet]. 2017;35:4942–51. Available from: http://linkinghub.elsevier.com/retrieve/pii/S0264410X17310125 doi:10.1016/j.vaccine.2017.07.086.
  • Wheeler CM, Skinner SR, Del Rosario-Raymundo MR, Garland SM, Chatterjee A, Lazcano-Ponce E, Salmerón J, McNeil S, Stapleton JT, Bouchard C, et al. Efficacy, safety, and immunogenicity of the human papillomavirus 16/18 AS04-adjuvanted vaccine in women older than 25 years: 7-year follow-up of the phase 3, double-blind, randomised controlled VIVIANE study. Lancet Infect Dis [Internet]. 2016 [cited 2016 Jul 14];0:1048–56. Available from: http://linkinghub.elsevier.com/retrieve/pii/S1473309916301207
  • GlaxoSmithKline Vaccine HPV-007 Study Group, Romanowski B, de Borba PC, Naud PS, Roteli-Martins CM, De Carvalho NS, Teixeira JC, Aoki F, Ramjattan B, Shier RM, et al. 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 (London, England) [Internet]. 2009;374:1975–85. Available from: doi:10.1016/S0140-6736(09)61567-1.
  • De Carvalho N, Teixeira J, Roteli-Martins CM, Naud P, De Borba P, Zahaf T, Sanchez N, Schuind A. Sustained efficacy and immunogenicity of the HPV-16/18 AS04-adjuvanted vaccine up to 7.3 years in young adult women. Vaccine [Internet]. 2010;28:6247–55. Available from: doi:10.1016/j.vaccine.2010.07.007.
  • Einstein MH, Takacs P, Chatterjee A, Sperling RS, Chakhtoura N, Blatter MM, Lalezari J, David M-P, Lin L, Struyf F, et al. Comparison of long-term immunogenicity and safety of human papillomavirus (HPV)-16/18 AS04-adjuvanted vaccine and HPV-6/11/16/18 vaccine in healthy women aged 18–45 years: end-of-study analysis of a Phase III randomized trial. Hum Vaccin Immunother [Internet]. 2014;10:3435–45. Available from: http://www.ncbi.nlm.nih.gov/pubmed/25483701 doi:10.4161/hv.36121.
  • Nieto K, Weghofer M, Sehr P, Ritter M, Sedlmeier S, Karanam B, Seitz H, Müller M, Kellner M, Hörer M, et al. Development of AAVLP(HPV16/31L2) particles as broadly protective HPV vaccine candidate. PLoS One [Internet]. 2012;7:e39741. Available from: http://www.ncbi.nlm.nih.gov/pubmed/22761884 doi:10.1371/journal.pone.0039741.
  • Wang D, Li Z, Xiao J, Wang J, Zhang L, Liu Y, Fan F, Xin L, Wei M, Kong Z, et al. Identification of Broad-Genotype HPV L2 Neutralization Site for Pan-HPV Vaccine Development by a Cross-Neutralizing Antibody. PLoS One [Internet]. 2015;10:e0123944. Available from: doi:10.1371/journal.pone.0123944.
  • Boxus M, Fochesato M, Miseur A, Mertens E, Dendouga N, Brendle S, Balogh KK, Christensen ND, Giannini SL. Broad cross-protection is induced in preclinical models by a human papillomavirus vaccine composed of L1/L2 chimeric virus-like particles. J Virol [Internet]. 2016;90:6314–25. Available from: doi:10.1128/JVI.00449-16.
  • Huber B, Schellenbacher C, Jindra C, Fink D, Shafti-Keramat S, Kirnbauer R. A chimeric 18L1-45RG1 virus-like particle vaccine cross-protects against oncogenic alpha-7 human papillomavirus types. PLoS One 2015;10:1–18. doi:10.1371/journal.pone.0120152.
  • Schellenbacher C, Kwak K, Fink D, Shafti-Keramat S, Huber B, Jindra C, Faust H, Dillner J, Roden RBS, Kirnbauer R. Efficacy of RG1-VLP vaccination against infections with genital and cutaneous human papillomaviruses. J Invest Dermatol [Internet]. 2013;133:2706–13. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3826974&tool=pmcentrez&rendertype=abstract doi:10.1038/jid.2013.253.
  • Schellenbacher C, Roden R, Kirnbauer R. Chimeric L1-L2 virus-like particles as potential broad-spectrum human papillomavirus vaccines. J Virol [Internet]. 2009;83:10085–95. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2748020&tool=pmcentrez&rendertype=abstract doi:10.1128/JVI.01088-09.
  • 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. 2008;80:841–6. doi:10.1002/jmv.21124. PMID:18360909
  • Bruni L, Barrionuevo-Rosas L, Albero G, Aldea M, Serrano B, Valencia S, Brotons M, Mena M, Cosano R, Muñoz J, Bosch FX, de Sanjosé S CX. Human papillomavirus and related diseases in the world. ICO Inf Cent HPV Cancer [Internet]. 2016; Available from: www.hpvcentre.com
  • Zhang T, Chen X, Liu H, Zhou Y, Wang Z, Xu X. Conservative epitope of human papillomavirus type 31 L2 can induce broad-spectrum neutralizing antibodies. Basic Clin Med. 2017;37:1552–6.
  • Combita AL, Touze A, Bousarghin L, Christensen ND, Coursaget P. Identification of two cross-neutralizing linear epitopes within the L1 major capsid protein of human papillomaviruses. J Virol [Internet]. 2002;76:6480–6. Available from:http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=12050360 doi:10.1128/JVI.76.13.6480-6486.2002.
  • Conway MJ, Cruz L, Alam S, Christensen ND, Meyers C. Cross-neutralization potential of native human papillomavirus N-terminal L2 epitopes. PLoS One [Internet]. 2011 [cited 2016 Sep 26];6:e16405. Available from: doi:10.1371/journal.pone.0016405.
  • Rubio I, Seitz H, Canali E, Sehr P, Bolchi A, Tommasino M, Ottonello S, Müller M. The N-terminal region of the human papillomavirus L2 protein contains overlapping binding sites for neutralizing, cross-neutralizing and non-neutralizing antibodies. Virology [Internet]. 2011 [cited 2016 Sep 26];409:348–59. Available from: http://linkinghub.elsevier.com/retrieve/pii/S0042682210006641 doi:10.1016/j.virol.2010.10.017.
  • Day PM, Kines RC, Thompson CD, Jagu S, Roden RB, Lowy DR, Schiller JT. In vivo mechanisms of vaccine-induced protection against HPV infection. Cell Host Microbe [Internet]. 2010;8:260–70. Available from: doi:10.1016/j.chom.2010.08.003.
  • Day PM, Pang YYS, 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 [Internet]. 2012 [cited 2016 Sep 26];19:1075–82. Available from: http://www.ncbi.nlm.nih.gov/pubmed/22593236 doi:10.1128/CVI.00139-12.
  • Huber B, Schellenbacher C, Shafti-Keramat S, Jindra C, Christensen N, Kirnbauer R. Chimeric L2-based virus-like particle (VLP) vaccines targeting cutaneous human papillomaviruses (HPV). PLoS One [Internet]. 2017 [cited 2017 Feb 8];12:e0169533. Available from: doi:10.1371/journal.pone.0169533.
  • Breitburd F, Kirnbauer R, Hubbert NL, Nonnenmacher B, Trin-Dinh-Desmarquet C, Orth G, Schiller JT, Lowy DR. Immunization with viruslike particles from cottontail rabbit papillomavirus (CRPV) can protect against experimental CRPV infection. J Virol [Internet]. 1995 [cited 2017 Sep 8];69:3959–63. Available from: http://www.ncbi.nlm.nih.gov/pubmed/7745754
  • Suzich JA, Ghim SJ, Palmer-Hill FJ, White WI, Tamura JK, Bell JA, Newsome JA, Jenson AB, Schlegel R. Systemic immunization with papillomavirus L1 protein completely prevents the development of viral mucosal papillomas. Proc Natl Acad Sci [Internet]. 1995 [cited 2017 Sep 8];92:11553–7. Available from: http://www.ncbi.nlm.nih.gov/pubmed/8524802 doi:10.1073/pnas.92.25.11553.
  • Roberts JN, Buck CB, Thompson CD, Kines R, Bernardo M, Choyke PL, Lowy DR, Schiller JT. Genital transmission of HPV in a mouse model is potentiated by nonoxynol-9 and inhibited by carrageenan. Nat Med [Internet]. 2007 [cited 2017 Sep 8];13:857–61. Available from: doi:10.1038/nm1598.
  • 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 [Internet]. 2011;85:13253–9. Available from: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd = Retrieve&db=PubMed&dopt=Citation&list_uids=21976653 doi:10.1128/JVI.06093-11.
  • Seitz H, Ribeiro-Muller L, Canali E, Bolchi A, Tommasino M, Ottonello S, Muller M. Robust in vitro and in vivo neutralization against multiple high-risk HPV types induced by a thermostable thioredoxin-L2 vaccine. Cancer Prev Res [Internet]. 2015;8:932–41. Available from: doi:10.1158/1940-6207.CAPR-15-0164.
  • Dessy FJ, Giannini SL, Bougelet CA, Kemp TJ, David M-PM, Poncelet SM, Pinto LA, Wettendorff MA. Correlation between direct ELISA, single epitope-based inhibition ELISA and pseudovirion-based neutralization assay for measuring anti-HPV-16 and anti-HPV-18 antibody response after vaccination with the AS04-adjuvanted HPV-16/18 cervical cancer vaccine. Hum Vaccin [Internet]. 2008;4:425–34. Available from:http://www.ncbi.nlm.nih.gov/pubmed/18948732 doi:10.4161/hv.4.6.6912.
  • Villa LL, Costa RLR, Petta CA, Andrade RP, Ault KA, Giuliano AR, Wheeler CM, Koutsky LA, Malm C, Lehtinen M, 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. 2005;6:271–8. doi:10.1016/S1470-2045(05)70101-7. PMID:15863374
  • Einstein MH, Levin MJ, Chatterjee A, Chakhtoura N, Takacs P, Catteau G, Dessy FJ, Moris P, Lin L, Struyf F, et al. Comparative humoral and cellular immunogenicity and safety of human papillomavirus (HPV)-16/18 AS04-adjuvanted vaccine and HPV-6/11/16/18 vaccine in healthy women aged 18–45 years: follow-up through Month 48 in a Phase III randomized study. Hum Vaccin Immunother [Internet]. 2014;10:3455–65. Available from: doi:10.4161/hv.36117.
  • Zhang T, Xu Y, Qiao L, Wang Y, Wu X, Fan D, Peng Q, Xu X. Trivalent Human Papillomavirus (HPV) VLP vaccine covering HPV type 58 can elicit high level of humoral immunity but also induce immune interference among component types. Vaccine [Internet]. 2010;28:3479–87. Available from: http://www.ncbi.nlm.nih.gov/pubmed/20211219 doi:10.1016/j.vaccine.2010.02.057.
  • Buck CB, Pastrana D V, Lowy DR, Schiller JT. Generation of HPV pseudovirions using transfection and their use in neutralization assays. Methods Mol Med [Internet]. 2005 [cited 2016 Aug 15];119:445–62. Available from: http://www.ncbi.nlm.nih.gov/pubmed/16350417
  • Pastrana DV, Buck CB, Pang Y-YS, Thompson CD, Castle PE, FitzGerald PC, Krüger Kjaer S, Lowy DR, Schiller JT. Reactivity of human sera in a sensitive, high-throughput pseudovirus-based papillomavirus neutralization assay for HPV16 and HPV18. Virology [Internet]. 2004 [cited 2016 Aug 15];321:205–16. Available from: http://www.ncbi.nlm.nih.gov/pubmed/15051381 doi:10.1016/j.virol.2003.12.027.

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