Progress and prospects for L2-based human papillomavirus vaccines

References

• Bernard H-U, Burk RD, Chen Z, et al. Classification of papillomaviruses (PVs) based on 189 PV types and proposal of taxonomic amendments. Virology. 2010;401(1):70–79.
   PubMed Web of Science ®Google Scholar
• Mammas IN, Sourvinos G, Spandidos DA. The paediatric story of human papillomavirus (Review). Oncol Lett. 2014;8(2):502–506.
   PubMed Web of Science ®Google Scholar
• Munoz N, Bosch FX, de Sanjose S, et al. Epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med. 2003;348(6):518–527.
   PubMed Web of Science ®Google Scholar
• Walboomers JM, Jacobs MV, Manos MM, et al. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol. 1999;189(1):12–19.
   PubMed Web of Science ®Google Scholar
• Munoz N, Bosch FX, Castellsague X, et al. Against which human papillomavirus types shall we vaccinate and screen? The international perspective. Int J Cancer. 2004;111(2):278–285.
   PubMed Web of Science ®Google Scholar
• D’Souza G, Kreimer AR, Viscidi R, et al. Case-control study of human papillomavirus and oropharyngeal cancer. N Engl J Med. 2007;356(19):1944–1956.
   PubMed Web of Science ®Google Scholar
• Parkin DM, Bray F. Chapter 2: The burden of HPV-related cancers. Vaccine. 2006;24(Suppl 3):S11–25.
   Web of Science ®Google Scholar
• Grulich AE, Van Leeuwen MT, Falster MO, et al. Incidence of cancers in people with HIV/AIDS compared with immunosuppressed transplant recipients: a meta-analysis. Lancet. 2007;370(9581):59–67.
   PubMed Web of Science ®Google Scholar
• McLaughlin-Drubin ME. Human papillomaviruses and non-melanoma skin cancer. Semin Oncol. 2015;42(2):284–290.
   PubMed Web of Science ®Google Scholar
• Majewski S, Jablonska S. Human papillomavirus-associated tumors of the skin and mucosa. J Am Acad Dermatol. 1997;36(5 Pt 1):659-85; quiz 686-8.
   PubMed Web of Science ®Google Scholar
• Ulrich C, Kanitakis J, Stockfleth E, et al. Skin cancer in organ transplant recipients--where do we stand today? Am J Transplant. 2008;8(11):2192–2198.
   PubMed Web of Science ®Google Scholar
• Quint KD, Genders RE, de Koning MN, et al. Human Beta-papillomavirus infection and keratinocyte carcinomas. J Pathol. 2015;235(2):342–354.
   PubMed Web of Science ®Google Scholar
• Miller DJ, Strauch RJ. Management of Cutaneous Warts of the Hand. The Journal of Hand Surgery. 2015;40(11):2274–2276.
   PubMed Web of Science ®Google Scholar
• Bellew SG, Quartarolo N, Janniger CK. Childhood warts: an update. Cutis. 2004;73(6):379–384.
   PubMed Web of Science ®Google Scholar
• Zur Hausen H. Papillomaviruses in the causation of human cancers - a brief historical account. Virology. 2009;384(2):260–265.
   PubMed Web of Science ®Google Scholar
• Harper DM, Franco EL, Wheeler C, 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. 2004;364(9447):1757–1765.
   PubMed Web of Science ®Google Scholar
• 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. 2005;6(5):271–278.
   PubMed Web of Science ®Google Scholar
• Malagon T, Drolet M, Boily M-C, et al. Cross-protective efficacy of two human papillomavirus vaccines: a systematic review and meta-analysis. Lancet Infect Dis. 2012;12(10):781–789.
   PubMed Web of Science ®Google Scholar
• Vesikari T, Brodszki N, van Damme P, et al. 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(R) in 9-15-year-old girls. Pediatr Infect Dis J. 2015;34(9):992–998.
   PubMed Web of Science ®Google Scholar
• Kreimer AR, Struyf F, Del Rosario-Raymundo MR, et al. Efficacy of fewer than three doses of an HPV-16/18 AS04-adjuvanted vaccine: combined analysis of data from the Costa Rica Vaccine and PATRICIA trials. Lancet. Oncol. 2015;16(7):775–786.
   PubMed Web of Science ®Google Scholar
• Sankaranarayanan R, Prabhu PR, Pawlita M, et al. Immunogenicity and HPV infection after one, two, and three doses of quadrivalent HPV vaccine in girls in India: a multicentre prospective cohort study. Lancet. Oncol. 2016;17(1):67–77.
   PubMed Web of Science ®Google Scholar
• Jardine D, Lu J, Pang J, et al. A randomized trial of immunotherapy for persistent genital warts. Hum Vaccin Immunother. 2012;8(5):623–629.
   PubMed Web of Science ®Google Scholar
• Doorbar J, Quint W, Banks L, et al. The biology and life-cycle of human papillomaviruses. Vaccine. 2012;30(Suppl 5):F55–70.
   PubMed Web of Science ®Google Scholar
• Han R, Reed CA, Cladel NM, et al. Immunization of rabbits with cottontail rabbit papillomavirus E1 and E2 genes: protective immunity induced by gene gun-mediated intracutaneous delivery but not by intramuscular injection. Vaccine. 2000;18(26):2937–2944.
   PubMed Web of Science ®Google Scholar
• Kirnbauer R, Booy F, Cheng N, et al. Papillomavirus L1 major capsid protein self-assembles into virus-like particles that are highly immunogenic. Proc Natl Acad Sci U S A. 1992;89(24):12180–12184.
   PubMed Web of Science ®Google Scholar
• Campo MS, Roden RB. Papillomavirus prophylactic vaccines: established successes, new approaches. J Virol. 2010;84(3):1214–1220.
   PubMed Web of Science ®Google Scholar
• 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. 1995;211(1):204–208.
   PubMed Web of Science ®Google Scholar
• Christensen ND, Kreider JW, Kan NC, et al. The open reading frame L2 of cottontail rabbit papillomavirus contains antibody-inducing neutralizing epitopes. Virology. 1991;181(2):572–579.
   PubMed Web of Science ®Google Scholar
• Pilacinski WP, Glassman DL, Glassman KF, et al. Immunization against bovine papillomavirus infection. Ciba Found Symp. 1986;120:136–156.
   PubMedGoogle Scholar
• Jarrett WF, Smith KT, O’Neil BW, et al. Studies on vaccination against papillomaviruses: prophylactic and therapeutic vaccination with recombinant structural proteins. Virology. 1991;184(1):33–42.
   PubMed Web of Science ®Google Scholar
• Hitzeroth II, Passmore JA, Shephard E, et al. Immunogenicity of an HPV-16 L2 DNA vaccine. Vaccine. 2009;27(46):6432–6434.
   PubMed Web of Science ®Google Scholar
• Thompson HS, Davies ML, Holding FP, et al. Phase I safety and antigenicity of TA-GW: a recombinant HPV6 L2E7 vaccine for the treatment of genital warts. Vaccine. 1999;17(1):40–49.
   PubMed Web of Science ®Google Scholar
• Lacey CJ, Thompson HS, Monteiro EF, et al. Phase IIa safety and immunogenicity of a therapeutic vaccine, TA-GW, in persons with genital warts. J Infect Dis. 1999;179(3):612–618.
   PubMed Web of Science ®Google Scholar
• Vandepapeliere P, Barrasso R, Meijer CJ, et al. Randomized controlled trial of an adjuvanted human papillomavirus (HPV) type 6 L2E7 vaccine: infection of external anogenital warts with multiple HPV types and failure of therapeutic vaccination. J Infect Dis. 2005;192(12):2099–2107.
   PubMed Web of Science ®Google Scholar
• de Jong A, O’Neill T, Khan AY, et al. Enhancement of human papillomavirus (HPV) type 16 E6 and E7-specific T-cell immunity in healthy volunteers through vaccination with TA-CIN, an HPV16 L2E7E6 fusion protein vaccine. Vaccine. 2002;20(29–30):3456–3464.
   PubMed Web of Science ®Google Scholar
• Smyth LJ, Van Poelgeest MI, Davidson EJ, et al. Immunological responses in women with human papillomavirus type 16 (HPV-16)-associated anogenital intraepithelial neoplasia induced by heterologous prime-boost HPV-16 oncogene vaccination. Clin Cancer Res. 2004;10(9):2954–2961.
   PubMed Web of Science ®Google Scholar
• Fiander AN, Tristram AJ, Davidson EJ, et al. Prime-boost vaccination strategy in women with high-grade, noncervical anogenital intraepithelial neoplasia: clinical results from a multicenter phase II trial. Int J Gynecol Cancer. 2006;16(3):1075–1081.
   PubMed Web of Science ®Google Scholar
• Davidson EJ, Faulkner RL, Sehr P, et al. Effect of TA-CIN (HPV 16 L2E6E7) booster immunisation in vulval intraepithelial neoplasia patients previously vaccinated with TA-HPV (vaccinia virus encoding HPV 16/18 E6E7). Vaccine. 2004;22(21–22):2722–2729.
   PubMed Web of Science ®Google Scholar
• Daayana S, Elkord E, Winters U, et al. Phase II trial of imiquimod and HPV therapeutic vaccination in patients with vulval intraepithelial neoplasia. Br J Cancer. 2010;102(7):1129–1136.
   PubMed Web of Science ®Google Scholar
• Gambhira R, Gravitt PE, Bossis I, et al. Vaccination of healthy volunteers with human papillomavirus type 16 L2E7E6 fusion protein induces serum antibody that neutralizes across papillomavirus species. Cancer Res. 2006;66(23):11120–11124.
   PubMed Web of Science ®Google Scholar
• Wang JW, Jagu S, Wang C, et al. Measurement of neutralizing serum antibodies of patients vaccinated with human papillomavirus L1 or L2-based immunogens using furin-cleaved HPV Pseudovirions. PLoS ONE. 2014;9(7):e101576.
   PubMed Web of Science ®Google Scholar
• 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. 2003;21(27–30):4256–4260.
   PubMed Web of Science ®Google Scholar
• Kawana K, Yoshikawa H, Taketani Y, et al. Common neutralization epitope in minor capsid protein L2 of human papillomavirus types 16 and 6. J Virol. 1999;73(7):6188–6190.
   PubMed Web of Science ®Google Scholar
• Kawana K, Kawana Y, Yoshikawa H, et al. 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. 2001;19(11–12):1496–1502.
   PubMed Web of Science ®Google Scholar
• Lin YL, Borenstein LA, Selvakumar R, et al. Effective vaccination against papilloma development by immunization with L1 or L2 structural protein of cottontail rabbit papillomavirus. Virology. 1992;187(2):612–619.
   PubMed Web of Science ®Google Scholar
• Campo MS, O’Neil BW, Grindlay GJ, et al. A peptide encoding a B-cell epitope from the N-terminus of the capsid protein L2 of bovine papillomavirus-4 prevents disease. Virology. 1997;234(2):261–266.
   PubMed Web of Science ®Google Scholar
• Gambhira R, Jagu S, Karanam B, et al. Protection of rabbits against challenge with rabbit papillomaviruses by immunization with the N-terminus of HPV16 minor capsid antigen L2. J Virol. 2007;81(21):13927–13931.
   PubMed Web of Science ®Google Scholar
• Gaukroger JM, Chandrachud LM, O’Neil BW, et al. Vaccination of cattle with bovine papillomavirus type 4 L2 elicits the production of virus-neutralizing antibodies. J Gen Virol. 1996;77(Pt 7):1577–1583.
   PubMed Web of Science ®Google Scholar
• Kirnbauer R, Chandrachud LM, O’Neil BW, et al. Virus-like particles of bovine papillomavirus type 4 in prophylactic and therapeutic immunization. Virology. 1996;219(1):37–44.
   PubMed Web of Science ®Google Scholar
• Suzich JA, Ghim SJ, Palmer-Hill FJ, et al. Systemic immunization with papillomavirus L1 protein completely prevents the development of viral mucosal papillomas. Proc Natl Acad Sci U S A. 1995;92(25):11553–11557.
   PubMed Web of Science ®Google Scholar
• Gambhira R, Karanam B, Jagu S, et al. A protective and broadly cross-neutralizing epitope of Human Papillomavirus L2. J Virol. 2007;81(24):13927–13931.
   PubMed Web of Science ®Google Scholar
• Roden RB, Yutzy WHT, Fallon R, et al. Minor capsid protein of human genital papillomaviruses contains subdominant, cross-neutralizing epitopes. Virology. 2000;270(2):254–257.
   PubMed Web of Science ®Google Scholar
• 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. 2011;409(2):348–359.
   PubMed Web of Science ®Google Scholar
• 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. 1996;70(9):5875–5883.
   PubMed Web of Science ®Google Scholar
• Buck CB, Cheng N, Thompson CD, et al. Arrangement of L2 within the papillomavirus capsid. J Virol. 2008;82(11):5190–5197.
   PubMed Web of Science ®Google Scholar
• Chackerian B, Lenz P, Lowy DR, et al. Determinants of autoantibody induction by conjugated papillomavirus virus-like particles. J Immunol. 2002;169(11):6120–6126.
   PubMed Web of Science ®Google Scholar
• Bachmann MF, Rohrer UH, Kundig TM, et al. The influence of antigen organization on B cell responsiveness. Science. 1993;262(5138):1448–1451.
   PubMed Web of Science ®Google Scholar
• Roost HP, Bachmann MF, Haag A, et al. Early high-affinity neutralizing anti-viral IgG responses without further overall improvements of affinity [see comments]. Proc Natl Acad Sci U S A. 1995;92(5):1257–1261.
   PubMed Web of Science ®Google Scholar
• Varsani A, Williamson A-L, de Villiers D, et al. 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. 2003;77(15):8386–8393.
   PubMed Web of Science ®Google Scholar
• Pineo CB, Hitzeroth II, Rybicki EP. Immunogenic assessment of plant-produced human papillomavirus type 16 L1/L2 chimaeras. Plant Biotechnol J. 2013;11(8):964–975.
   PubMed Web of Science ®Google Scholar
• Kondo K, Ochi H, Matsumoto T, et al. Modification of human papillomavirus-like particle vaccine by insertion of the cross-reactive L2-epitopes. J Med Virol. 2008;80(5):841–846.
   PubMed Web of Science ®Google Scholar
• 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. 2007;25(11):2001–2010.
   PubMed Web of Science ®Google Scholar
• Schellenbacher C, Roden R, Kirnbauer R. Chimeric L1-L2 virus-like particles as potential broad-spectrum human papillomavirus vaccines. J Virol. 2009;83(19):10085–10095.
   PubMed Web of Science ®Google Scholar
• Schellenbacher C, Kwak K, Fink D, et al. Efficacy of RG1-VLP vaccination against infections with genital and cutaneous human papillomaviruses. J Invest Dermatol. 2013;133:2706–2713.
   PubMed Web of Science ®Google Scholar
• 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. 2006;24(26):5516–5525.
   PubMed Web of Science ®Google Scholar
• 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. 2010;28(27):4384–4393.
   PubMed Web of Science ®Google Scholar
• Tumban E, Peabody J, Peabody DS, et al. A pan-HPV vaccine based on bacteriophage PP7 VLPs displaying broadly cross-neutralizing epitopes from the HPV minor capsid protein, L2. PLoS ONE. 2011;6(8):e23310.
   PubMed Web of Science ®Google Scholar
• Tumban E, Peabody J, Tyler M, et al. VLPs displaying a single L2 epitope induce broadly cross-neutralizing antibodies against human papillomavirus. PLoS ONE. 2012;7(11):e49751.
   PubMed Web of Science ®Google Scholar
• Tyler M, Tumban E, Dziduszko A, et al. Immunization with a consensus epitope from human papillomavirus L2 induces antibodies that are broadly neutralizing. Vaccine. 2014;32(34):4267–4274.
   PubMed Web of Science ®Google Scholar
• Tumban E, Peabody J, Peabody DS, et al. A universal virus-like particle-based vaccine for human papillomavirus: longevity of protection and role of endogenous and exogenous adjuvants. Vaccine. 2013;31(41):4647–4654.
   PubMed Web of Science ®Google Scholar
• Tumban E, Muttil P, Escobar CA, et al. Preclinical refinements of a broadly protective VLP-based HPV vaccine targeting the minor capsid protein, L2. Vaccine. 2015;33(29):3346–3353.
   PubMed Web of Science ®Google Scholar
• Nieto K, Weghofer M, Sehr P, et al. Development of AAVLP(HPV16/31L2) particles as broadly protective HPV vaccine candidate. PLoS ONE. 2012;7(6):e39741.
   PubMed Web of Science ®Google Scholar
• Jagu S, Karanam B, Wang JW, et al. Durable immunity to oncogenic human papillomaviruses elicited by adjuvanted recombinant Adeno-associated virus-like particle immunogen displaying L2 17-36 epitopes. Vaccine. 2015;33(42):5553–5563.
   PubMed Web of Science ®Google Scholar
• Wu W-H, Alkutkar T, Karanam B, et al. Capsid display of a conserved human papillomavirus L2 peptide in the adenovirus 5 hexon protein: a candidate prophylactic HPV vaccine approach. Virol J. 2015;12:140.
   PubMed Web of Science ®Google Scholar
• Yoon S-W, Lee T-Y, Kim S-J, et al. Oral administration of HPV-16 L2 displayed on Lactobacillus casei induces systematic and mucosal cross-neutralizing effects in Balb/c mice. Vaccine. 2012;30(22):3286–3294.
   PubMed Web of Science ®Google Scholar
• Breitburd F, Kirnbauer R, Hubbert NL, et al. Immunization with virus like particles from cottontail rabbit papillomavirus (CRPV) can protect against experimental CRPV infection. J Virol. 1995;69(6):3959–3963.
   PubMed Web of Science ®Google Scholar
• Kirnbauer R, Taub J, Greenstone H, et al. Efficient self-assembly of human papillomavirus type 16 L1 and L1-L2 into virus-like particles. J Virol. 1993;67(12):6929–6936.
   PubMed Web of Science ®Google Scholar
• Jagu S, Karanam B, Gambhira R, et al. Concatenated multitype L2 fusion proteins as candidate prophylactic pan-human papillomavirus vaccines. J Natl Cancer Inst. 2009;101(11):782–792.
   PubMed Web of Science ®Google Scholar
• Jagu S, Kwak K, Schiller JT, et al. Phylogenetic considerations in designing a broadly protective multimeric L2 vaccine. J Virol. 2013;87(11):6127–6136.
   PubMed Web of Science ®Google Scholar
• Jagu S, Kwak K, Karanam B, et al. Optimization of multimeric human papillomavirus L2 vaccines. PLoS ONE. 2013;8(1):e55538.
   PubMed Web of Science ®Google Scholar
• 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. 2009;27(13):1949–1956.
   PubMed Web of Science ®Google Scholar
• Seitz H, Dantheny T, Burkart F, et al. Influence of oxidation and multimerization on the immunogenicity of a thioredoxin-l2 prophylactic papillomavirus vaccine. Clinical and Vaccine Immunology : CVI. 2013;20(7):1061–1069.
   PubMed Web of Science ®Google Scholar
• Canali E, Bolchi A, Spagnoli G, et al. A high-performance thioredoxin-based scaffold for peptide immunogen construction: proof-of-concept testing with a human papillomavirus epitope. Sci Rep. 2014;4:4729.
   PubMed Web of Science ®Google Scholar
• Seitz H, Ribeiro-Muller L, Canali E, et al. Robust in vitro and in vivo neutralization against multiple high-risk HPV types induced by a thermostable thioredoxin-L2 vaccine. Cancer Prevention Research. 2015;8(10):932–941.
   PubMed Web of Science ®Google Scholar
• Karanam B, Gambhira R, Peng S, et al. Vaccination with HPV16 L2E6E7 fusion protein in GPI-0100 adjuvant elicits protective humoral and cell-mediated immunity. Vaccine. 2009;27(7):1040–1049.
   PubMed Web of Science ®Google Scholar
• 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 U S A. 2008;105(15):5850–5855.
   PubMed Web of Science ®Google Scholar
• Kalnin K, Tibbitts T, Yan Y, et al. Low doses of flagellin-L2 multimer vaccines protect against challenge with diverse papillomavirus genotypes. Vaccine. 2014;32(28):3540–3547.
   PubMed Web of Science ®Google Scholar
• Greenstone HL, Nieland JD, de Visser KE, et al. Chimeric papillomavirus virus-like particles elicit antitumor immunity against the E7 oncoprotein in an HPV16 tumor model. Proc Natl Acad Sci U S A. 1998;95(4):1800–1805.
   PubMed Web of Science ®Google Scholar
• van der Burg SH, Kwappenberg KM, O’Neill T, et al. Pre-clinical safety and efficacy of TA-CIN, a recombinant HPV16 L2E6E7 fusion protein vaccine, in homologous and heterologous prime-boost regimens. Vaccine. 2001;19(27):3652–3660.
   PubMed Web of Science ®Google Scholar
• Peng S, Wang JW, Karanam B, et al. Sequential cisplatin therapy and vaccination with HPV16 E6E7L2 fusion protein in saponin adjuvant GPI-0100 for the treatment of a model HPV16+ cancer. PLoS One. 2015;10(1):e116389.
   PubMed Web of Science ®Google Scholar
• Cheng WF, Hung CF, Chai CY, et al. Tumor-specific immunity and antiangiogenesis generated by a DNA vaccine encoding calreticulin linked to a tumor antigen. J Clin Invest. 2001;108(5):669–678.
   PubMed Web of Science ®Google Scholar
• Kim D, Gambhira R, Karanam B, et al. Generation and characterization of a preventive and therapeutic HPV DNA vaccine. Vaccine. 2008;26(3):351–360.
   PubMed Web of Science ®Google Scholar
• Peng S, Song L, Knoff J, et al. Control of HPV-associated tumors by innovative therapeutic HPV DNA vaccine in the absence of CD4+ T cells. Cell Biosci. 2014;4(1):11.
   PubMed Web of Science ®Google Scholar
• Wang JW, Jiang R, Peng S, et al. Immunologic control of Mus musculus papillomavirus type 1. PLoS Pathog. 2015;11(10):e1005243.
   PubMed Web of Science ®Google Scholar
• Wang JW, Hung C-F, Huh WK, et al. Immunoprevention of human papillomavirus-associated malignancies. Cancer Prevention Research. 2015;8(2):95–104.
   PubMed Web of Science ®Google Scholar
• Balmelli C, Roden R, Potts A, et al. Nasal immunization of mice with human papillomavirus type 16 virus-like particles elicits neutralizing antibodies in mucosal secretions `In Process Citation]. J Virol. 1998;72(10):8220–8229.
   PubMed Web of Science ®Google Scholar
• Nardelli-Haefliger D, Lurati F, Wirthner D, et al. Immune responses induced by lower airway mucosal immunisation with a human papillomavirus type 16 virus-like particle vaccine. Vaccine. 2005;23(28):3634–3641.
   PubMed Web of Science ®Google Scholar
• Gerber S, Lane C, Brown DM, et al. Human papillomavirus virus-like particles are efficient oral immunogens when coadministered with Escherichia coli heat-labile enterotoxin mutant R192G or CpG DNA. J Virol. 2001;75(10):4752–4760.
   PubMed Web of Science ®Google Scholar
• Lin Z, Yemelyanova AV, Gambhira R, et al. Expression pattern and subcellular localization of human papillomavirus minor capsid protein L2. Am J Pathol. 2009;174(1):136–143.
   PubMed Web of Science ®Google Scholar
• Day PM, Kines RC, Thompson CD, et al. In vivo mechanisms of vaccine-induced protection against HPV infection. Cell Host Microbe. 2010;8(3):260–270.
   PubMed Web of Science ®Google Scholar
• Day PM, Pang YY, Kines RC, et al. An HPV in vitro neutralization assay that recapitulates the in vivo process of infection provides a sensitive measure of L2 infection-inhibiting antibodies. Clin Vaccine Immunol. 2012;19(7):1075–1082.
   Web of Science ®Google Scholar
• 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. 2007;13(7):857–861.
   PubMed Web of Science ®Google Scholar
• Wang JW, Jagu S, Kwak K, et al. Preparation and properties of a papillomavirus infectious intermediate and its utility for neutralization studies. Virology. 2014;449:304–316.
   PubMed Web of Science ®Google Scholar
• Wang JW, Matsui K, Pan Y, et al. Production of Furin-cleaved papillomavirus pseudovirions and their use for in vitro neutralization assays of L1- or L2-Specific Antibodies. Curr Protoc Microbiol. 2015;38:14B 5 1–14B 5 26.
   PubMedGoogle Scholar
• Wang JW, Jagu S, Wu W-H, et al. Seroepidemiology of Human Papillomavirus 16 (HPV16) L2 and generation of L2-specific human chimeric monoclonal antibodies. Clinical and Vaccine Immunology : CVI. 2015;22(7):806–816.
   PubMed Web of Science ®Google Scholar
• Kim TJ, Jin HT, Hur SY, et al. Clearance of persistent HPV infection and cervical lesion by therapeutic DNA vaccine in CIN3 patients. Nat Commun. 2014;5:5317.
   PubMed Web of Science ®Google Scholar