Neutralization sites of human papillomavirus-6 relate to virus attachment and entry phase in viral infection

References

• Roden RBS, Stern PL. Opportunities and challenges for human papillomavirus vaccination in cancer. Nat Rev Cancer. 2018 Apr;18(4):240–254. doi:10.1038/nrc.2018.13. PubMed PMID: 29497146; PubMed Central PMCID: PMCPMC6454884.
   PubMed Web of Science ®Google Scholar
• de Villiers EM. Cross-roads in the classification of papillomaviruses. Virology. 2013;445(1-2):2–10. doi:10.1016/j.virol.2013.04.023.
   PubMed Web of Science ®Google Scholar
• Wiley DJ, Douglas J, Beutner K, et al. External genital warts: Diagnosis, treatment, and prevention. Clin Infect Dis. 2002;35:S210–S224. doi:10.1086/342109.
   PubMed Web of Science ®Google Scholar
• Vandepapelière P, Barrasso R, Meijer CJLM, 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. doi:10.1086/498164.
   PubMed Web of Science ®Google Scholar
• Greer CE, Wheeler CM, Ladner MB, et al. Human papillomavirus (HPV) type distribution and serological response to HPV type 6 virus-like particles in patients with genital warts. J Clin Microbiol. 1995;33(8):2058–2063.
   PubMed Web of Science ®Google Scholar
• Rose RC, Reichman RC, Bonnez W. Human papillomavirus (HPV) type 11 recombinant virus-like particles induce the formation of neutralizing antibodies and detect HPV-specific antibodies in human sera. J Gen Virol. 1994;75(8):2075–2079. doi: 10.1099/0022-1317-75-8-2075
   PubMed Web of Science ®Google Scholar
• Brown DB, Shew ML, Qadadri B, et al. A longitudinal study of genital human papillomavirus infection in a cohort of closely followed adolescent women. J Infect Dis. 2005;191(2):182–192. doi:10.1086/426867.
   PubMed Web of Science ®Google Scholar
• Brown DR, Schroeder JM, Bryan JT, et al. Detection of multiple human papillomavirus types in condylomata acuminata lesions from otherwise healthy and immunosuppressed patients. J Clin Microbiol. 1999;37(10):3316–3322.
   PubMed Web of Science ®Google Scholar
• Ho GYF, Bierman R, Beardsley L, et al. Natural history of cervicovaginal papillomavirus infection in young women. N Engl J Med. 1998;338(7):423–428. doi:10.1056/NEJM199802123380703.
   PubMed Web of Science ®Google Scholar
• Herrero R, González P, Markowitz LE. Present status of human papillomavirus vaccine development and implementation. Lancet Oncol. 2015;16(5):e206–e216. doi:10.1016/S1470-2045(14)70481-4.
   PubMed Web of Science ®Google Scholar
• McCormack PL. Quadrivalent human papillomavirus (types 6, 11, 16, 18) recombinant vaccine (Gardasil®): A review of its use in the prevention of premalignant anogenital lesions, cervical and anal cancers, and genital warts. Drugs. 2014;74(11):1253–1283. doi:10.1007/s40265-014-0255-z.
   PubMed Web of Science ®Google Scholar
• Buck CB, Day PM, Trus BL. The papillomavirus major capsid protein L1. Virology. 2013;445(1-2):169–174. doi:10.1016/j.virol.2013.05.038.
   PubMed Web of Science ®Google Scholar
• Wang JW, Roden RBS. L2, the minor capsid protein of papillomavirus. Virology. 2013;445(1-2):175–186. doi:10.1016/j.virol.2013.04.017.
   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. doi: 10.1073/pnas.89.24.12180
   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
• Guan J, Bywaters SM, Brendle SA, et al. Cryoelectron microscopy maps of human papillomavirus 16 Reveal L2 densities and Heparin binding site. Structure. 2016 Dec 31. doi:10.1016/j.str.2016.12.001. PubMed PMID: 28065506.
   PubMed Web of Science ®Google Scholar
• Lee H, Brendle SA, Bywaters SM, et al. A cryo-electron microscopy study identifies the complete H16.V5 epitope and reveals global conformational changes initiated by binding of the neutralizing antibody fragment. J Virol. 2015 Jan 15;89(2):1428–1438. doi:10.1128/JVI.02898-14. PubMed PMID: 25392224; PubMed Central PMCID: PMCPMC4300654.
   PubMed Web of Science ®Google Scholar
• Bishop B, Dasgupta J, Klein M, et al. Crystal structures of four types of human papillomavirus L1 capsid proteins: Understanding the specificity of neutralizing monoclonal antibodies. J Biol Chem. 2007;282(43):31803–31811. doi:10.1074/jbc.M706380200.
   PubMed Web of Science ®Google Scholar
• Yeager MD, Aste-Amezaga M, Brown DR, et al. Neutralization of human papillomavirus (HPV) pseudovirions: A novel and efficient approach to detect and characterize HPV neutralizing antibodies. Virology. 2000;278(2):570–577. doi:10.1006/viro.2000.0674.
   PubMed Web of Science ®Google Scholar
• Orozco JJ, Carter JJ, Koutsky LA, et al. Humoral immune response recognizes a complex set of epitopes on human papillomavirus type 6 l1 capsomers. J Virol. 2005 Aug;79(15):9503–9514. doi:10.1128/JVI.79.15.9503-9514.2005. PubMed PMID: 16014913; PubMed Central PMCID: PMCPMC1181614.
   PubMed Web of Science ®Google Scholar
• Ozbun MA. Extracellular events impacting human papillomavirus infections: Epithelial wounding to cell signaling involved in virus entry. Papillomavirus Res. 2019 Jun;7:188–192. doi:10.1016/j.pvr.2019.04.009. PubMed PMID: 30981651; PubMed Central PMCID: PMCPMC6514438.
   PubMed Web of Science ®Google Scholar
• Day PM, Lowy DR, Schiller JT. Heparan sulfate-independent cell binding and infection with furin-precleaved papillomavirus capsids. J Virol. 2008;82(24):12565–12568. doi:10.1128/JVI.01631-08.
   PubMed Web of Science ®Google Scholar
• Richards KF, Bienkowska-Haba M, Dasgupta J, et al. Multiple heparan sulfate binding site Engagements Are Required for the Infectious entry of human papillomavirus type 16. J Virol. 2013 Nov;87(21):11426–11437. doi:10.1128/Jvi.01721-13. PubMed PMID: WOS:000325863400010; English.
   PubMed Web of Science ®Google Scholar
• Raff AB, Woodham AW, Raff LM, et al. The evolving field of human papillomavirus receptor research: a review of binding and entry. J Virol. 2013 Jun;87(11):6062–6072. doi:10.1128/JVI.00330-13. PubMed PMID: 23536685; PubMed Central PMCID: PMCPMC3648114.
   PubMed Web of Science ®Google Scholar
• Schafer G, Blumenthal MJ, Katz AA. Interaction of human tumor viruses with host cell surface receptors and cell entry. Viruses. 2015 May 22;7(5):2592–2617. doi:10.3390/v7052592. PubMed PMID: 26008702; PubMed Central PMCID: PMCPMC4452921.
   PubMed Web of Science ®Google Scholar
• Day PM, Thompson CD, Buck CB, et al. Neutralization of human papillomavirus with monoclonal antibodies reveals different mechanisms of inhibition. J Virol. 2007 Aug;81(16):8784–8792. doi:10.1128/JVI.00552-07. PubMed PMID: 17553881; PubMed Central PMCID: PMCPMC1951340.
   PubMed Web of Science ®Google Scholar
• Guan J, Bywaters SM, Brendle SA, et al. The U4 antibody epitope on human papillomavirus 16 identified by cryo-electron microscopy. J Virol. 2015 Dec;89(23):12108–12117. doi:10.1128/jvi.02020-15. PubMed PMID: WOS:000366896600032.
   PubMed Web of Science ®Google Scholar
• McClements WL, Wang XM, Ling JC, et al. A novel human papillomavirus type 6 neutralizing domain comprising two discrete regions of the major capsid protein L1. Virology. 2001 Oct 25;289(2):262–268. doi:10.1006/viro.2001.1146. PubMed PMID: 11689049.
   PubMed Web of Science ®Google Scholar
• Li M, Wang X, Cao L, et al. Quantitative and epitope-specific antigenicity analysis of the human papillomavirus 6 capsid protein in aqueous solution or when adsorbed on particulate adjuvants. Vaccine. 2016 Aug 17;34(37):4422–4428. doi:10.1016/j.vaccine.2016.07.012. PubMed PMID: 27426626.
   PubMed Web of Science ®Google Scholar
• Buck CB, Pastrana DV, Lowy DR, et al. Generation of HPV pseudovirions using transfection and their use in neutralization assays. Methods Mol Med. 2005;119:445–462.
   PubMedGoogle Scholar
• Chen Y, Li C, He D, et al. Antigenic analysis of divergent genotypes human Enterovirus 71 viruses by a panel of neutralizing monoclonal antibodies: current genotyping of EV71 does not reflect their antigenicity. Vaccine. 2013 Jan 2;31(2):425–430. doi:10.1016/j.vaccine.2012.10.032. PubMed PMID: 23088887.
   PubMed Web of Science ®Google Scholar
• Yan X, Sinkovits RS, Baker TS. AUTO3DEM-an automated and high throughput program for image reconstruction of icosahedral particles. J Struct Biol. 2007;157(1):73–82. doi:10.1016/j.jsb.2006.08.007.
   PubMed Web of Science ®Google Scholar
• Pettersen EF, Goddard TD, Huang CC, et al. UCSF Chimera–a visualization system for exploratory research and analysis. J Comput Chem. 2004 Oct;25(13):1605–1612. doi:10.1002/jcc.20084. PubMed PMID: 15264254.
   PubMed Web of Science ®Google Scholar
• Emsley P, Lohkamp B, Scott WG, et al. Features and development of Coot. Acta Crystallogr D Biol Crystallogr. 2010 Apr;66(Pt 4):486-501. doi:10.1107/S0907444910007493. PubMed PMID: 20383002; PubMed Central PMCID: PMCPMC2852313.
   PubMedGoogle Scholar
• Adams PD, Afonine PV, Bunkoczi G, et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr. 2010 Feb;66(Pt 2):213-221. doi:10.1107/S0907444909052925. PubMed PMID: 20124702; PubMed Central PMCID: PMCPMC2815670.
   PubMedGoogle Scholar
• Xiao C, Rossmann MG. Interpretation of electron density with stereographic roadmap projections. J Struct Biol. 2007 May;158(2):182–187. doi:10.1016/j.jsb.2006.10.013. PubMed PMID: 17116403; PubMed Central PMCID: PMC1978246.
   PubMed Web of Science ®Google Scholar
• Ludmerer SW, Benincasa D, Mark GE. Two amino acid residues confer type specificity to a neutralizing, conformationally dependent epitope on human papillomavirus type 11. J Virol. 1996 Jul;70(7):4791–4794. PubMed PMID: WOS:A1996UR13000072; English.
   PubMed Web of Science ®Google Scholar
• Li Z, Wang D, Gu Y, et al. Crystal structures of Two immune complexes identify determinants for viral infectivity and type-specific neutralization of human papillomavirus. MBio. 2017 Sep 26;8(5). doi:10.1128/mBio.00787-17. PubMed PMID: 28951471; PubMed Central PMCID: PMCPMC5615192.
   Web of Science ®Google Scholar
• Guan J, Bywaters SM, Brendle SA, et al. Structural comparison of four different antibodies interacting with human papillomavirus 16 and mechanisms of neutralization. Virology. 2015;483:253–263. doi:10.1016/j.virol.2015.04.016.
   PubMed Web of Science ®Google Scholar
• Day PM, Thompson CD, Buck CB, et al. Neutralization of human papillomavirus with monoclonal antibodies Reveals different mechanisms of inhibition▿. J Virol. 2007;81(16):8784–8792. doi:10.1128/JVI.00552-07.
   PubMed Web of Science ®Google Scholar
• Li Z, Wang D, Gu Y, et al. Crystal structures of two immune complexes identify determinants for viral infectivity and type-specific neutralization of human papillomavirus. mBio. 2017;8(5):17), doi:10.1128/mBio.00787-17.
   Web of Science ®Google Scholar
• Li Z, Yan X, Yu H, et al. The C-terminal arm of the human papillomavirus major capsid protein Is Immunogenic and involved in virus-host interaction. Structure. 2016;24(6):874–885. doi:10.1016/j.str.2016.04.008.
   PubMed Web of Science ®Google Scholar
• Xu L, Zheng Q, Li S, et al. Atomic structures of coxsackievirus A6 and its complex with a neutralizing antibody. Nat Commun. 2017 Sep 11;8(1):505), doi:10.1038/s41467-017-00477-9. PubMed PMID: 28894095; PubMed Central PMCID: PMCPMC5593947.
   PubMed Web of Science ®Google Scholar
• Xiao C, Rossmann MG. Interpretation of electron density with stereographic roadmap projections. J Struct Biol. 2007;158(2):182–187. doi:10.1016/j.jsb.2006.10.013.
   PubMed Web of Science ®Google Scholar
• Letian T, Tianyu Z. Cellular receptor binding and entry of human papillomavirus. Virol J. 2010;7:2, doi:10.1186/1743-422X-7-2. PubMed PMID: 20051141; PubMed Central PMCID: PMCPMC2820467.
   PubMed Web of Science ®Google Scholar