Functional epitopes on hepatitis E virions and recombinant capsids are highly conformation-dependent

References

• Wu X, Chen P, Lin H, Hao X, Liang Z. Hepatitis E virus: current epidemiology and vaccine. Hum Vaccin Immunother. 2016;12:2603–10. PMID:27184971. doi:10.1080/21645515.2016.1184806.
   PubMed Web of Science ®Google Scholar
• Rein DB, Stevens GA, Theaker J, Wittenborn JS, Wiersma ST. The global burden of hepatitis E virus genotypes 1 and 2 in 2005. Hepatology. 2012;55:988–97. PMID:22121109. doi:10.1002/hep.25505.
   PubMed Web of Science ®Google Scholar
• Nan Y, Zhang YJ. Molecular biology and infection of hepatitis E virus. Front Microbiol. 2016;7:1419. PMID:27656178. doi:10.3389/fmicb.2016.01419.
   PubMed Web of Science ®Google Scholar
• Navaneethan U, Al Mohajer M, Shata MT. Hepatitis E and pregnancy: understanding the pathogenesis. Liver Int. 2008;28:1190–99. PMID:18662274. doi:10.1111/j.1478-3231.2008.01840.x.
   PubMed Web of Science ®Google Scholar
• Dalton HR, Hazeldine S, Banks M, Ijaz S, Bendall R. Locally acquired hepatitis E in chronic liver disease. Lancet. 2007;369:1260. PMID:17434400. doi:10.1016/S0140-6736(07)60595-9.
   PubMed Web of Science ®Google Scholar
• Perez-Gracia MT, Suay-Garcia B, Mateos-Lindemann ML. Hepatitis E and pregnancy: current state. Rev Med Virol. 2017;27:e1929. PMID:28318080. doi:10.1002/rmv.1929.
   PubMed Web of Science ®Google Scholar
• Li SW, Zhao Q, Wu T, Chen S, Zhang J, Xia NS. The development of a recombinant hepatitis E vaccine HEV 239. Hum Vaccin Immunother. 2015;11:908–14. PMID:25714510. doi:10.1080/21645515.2015.1008870.
   PubMed Web of Science ®Google Scholar
• Rodriguez-Lázaro D, Hernandez M, Cook N. Hepatitis E virus: a new foodborne zoonotic concern. Adv Food Nutr Res. 2018;86:55–70. PMID:30077224. doi:10.1016/bs.afnr.2018.04.002.
   PubMedGoogle Scholar
• Emerson SU, Nguyen HT, Torian U, Burke D, Engle R, Purcell RH. Release of genotype 1 hepatitis E virus from cultured hepatoma and polarized intestinal cells depends on open reading frame 3 protein and requires an intact PXXP motif. J Virol. 2010;84:9059–69. PMID:20610720. doi:10.1128/JVI.00593-10.
   PubMed Web of Science ®Google Scholar
• Zhao Q, Zhang J, Wu T, Li SW, Ng MH, Xia NS, Shih JW. Antigenic determinants of hepatitis E virus and vaccine-induced immunogenicity and efficacy. J Gastroenterol. 2013;48:159–68. PMID:23149436. doi:10.1007/s00535-012-0701-1.
   PubMed Web of Science ®Google Scholar
• Li S, Tang X, Seetharaman J, Yang C, Gu Y, Zhang J, Du H, Shih JW, Hew CL, Sivaraman J, et al. Dimerization of hepatitis E virus capsid protein E2s domain is essential for virus-host interaction. PLoS Pathog. 2009;5:e1000537. PMID:19662165;. doi:10.1371/journal.ppat.1000537.
   PubMed Web of Science ®Google Scholar
• Li SW, Zhang J, Li YM, Ou SH, Huang GY, He ZQ, Ge SX, Xian YL, Pang SQ, Ng MH, et al. A bacterially expressed particulate hepatitis E vaccine: antigenicity, immunogenicity and protectivity on primates. Vaccine. 2005;23:2893–901. PMID:15780738. doi:10.1016/j.vaccine.2004.11.064.
   PubMed Web of Science ®Google Scholar
• Zhu FC, Zhang J, Zhang XF, Zhou C, Wang ZZ, Huang SJ, Wang H, Yang CL, Jiang HM, Cai JP, et al. Efficacy and safety of a recombinant hepatitis E vaccine in healthy adults: a large-scale, randomised, double-blind placebo-controlled, phase 3 trial. Lancet. 2010;376:895–902. PMID:20728932. doi:10.1016/S0140-6736(10)61030-6.
   PubMed Web of Science ®Google Scholar
• Zhang J, Shih JW, Xia NS. Long-term efficacy of a hepatitis E vaccine. N Engl J Med. 2015;372:2265–66. PMID:26039604. doi:10.1056/NEJMoa1406011.
   PubMed Web of Science ®Google Scholar
• Innis BL, Lynch JA. Immunization against Hepatitis E. Cold Spring Harb Perspect Med. 2018;8:a032573. PMID:29530951. doi:10.1101/cshperspect.a032573.
   PubMed Web of Science ®Google Scholar
• Zhao M, Li XJ, Tang ZM, Yang F, Wang SL, Cai W, Zhang K, Xia NS, Zheng ZZ. A comprehensive study of neutralizing antigenic sites on the Hepatitis E Virus (HEV) capsid by constructing, clustering, and characterizing a tool box. J Biol Chem. 2015;290:19910–22. PMID:26085097. doi:10.1074/jbc.M115.649764.
   PubMed Web of Science ®Google Scholar
• Tang X, Yang C, Gu Y, Song C, Zhang X, Wang Y, Zhang J, Hew CL, Li S, Xia N, et al. Structural basis for the neutralization and genotype specificity of hepatitis E virus. Proc Natl Acad Sci USA. 2011;108:10266–71. PMID:21642534. doi:10.1073/pnas.1101309108.
   PubMed Web of Science ®Google Scholar
• Wei M, Zhang X, Yu H, Tang ZM, Wang K, Li Z, Zheng Z, Li S, Zhang J, Xia N, et al. Bacteria expressed hepatitis E virus capsid proteins maintain virion-like epitopes. Vaccine. 2014;32:2859–65. PMID:24662711. doi:10.1016/j.vaccine.2014.02.025.
   PubMed Web of Science ®Google Scholar
• Gu Y, Tang X, Zhang X, Song C, Zheng M, Wang K, Zhang J, Ng MH, Hew CL, Li S, et al. Structural basis for the neutralization of hepatitis E virus by a cross-genotype antibody. Cell Res. 2015;25:604–20. PMID:25793314. doi:10.1038/cr.2015.34.
   PubMed Web of Science ®Google Scholar
• Li S, Zhang J, Xia N. Lessons from hepatitis E vaccine design. Curr Opin Virol. 2015;11:130–36. PMID:25913817. doi:10.1016/j.coviro.2015.04.003.
   PubMed Web of Science ®Google Scholar
• Riddell MA, Li F, Anderson DA. Identification of immunodominant and conformational epitopes in the capsid protein of hepatitis E virus by using monoclonal antibodies. J Virol. 2000;74:8011–17. PMID:10933710. doi:10.1128/jvi.74.17.8011-8017.2000.
   PubMed Web of Science ®Google Scholar
• Thönes N, Herreiner A, Schädlich L, Piuko K, Müller 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. 2008;82:5472–85. PMID:18385253. doi:10.1128/JVI.02482-07.
   PubMed Web of Science ®Google Scholar
• Cai W, Tang ZM, Wen GP, Wang SL, Ji WF, Yang M, Ying D, Zheng ZZ, Xia NS. A high-throughput neutralizing assay for antibodies and sera against hepatitis E virus. Sci Rep. 2016;6:25141. PMID:27122081. doi:10.1038/srep25141.
   PubMed Web of Science ®Google Scholar
• Zhang X, Xin L, Li S, Fang M, Zhang J, Xia N, Zhao Q. Lessons learned from successful human vaccines: delineating key epitopes by dissecting the capsid proteins. Hum Vaccin Immunother. 2015;11:1277–92. PMID:25751641. doi:10.1080/21645515.2015.1016675.
   PubMed Web of Science ®Google Scholar
• Zhang JZ, Im SW, Lau SH, Chau TN, Lai ST, Ng SP, Peiris M, Tse C, Ng TK, Ng MH. Occurrence of hepatitis E virus IgM, low avidity IgG serum antibodies, and viremia in sporadic cases of non-A, -B, and -C acute hepatitis. J Med Virol. 2002;66:40–48. PMID:11748657. doi:10.1002/jmv.2109.
   PubMed Web of Science ®Google Scholar
• Khudyakov Y, Kamili S. Serological diagnostics of hepatitis E virus infection. Virus Res. 2011;161:84–92. PMID:21704091. doi:10.1016/j.virusres.2011.06.006.
   PubMed Web of Science ®Google Scholar
• Yin XC, Wang X, Zhang ZG, Li Y, Lin Z, Pan H, Gu Y, Li S, Zhang J, Xia N, et al. Demonstration of real-time and accelerated stability of hepatitis E vaccine with a combination of different physicochemical and immunochemical methods. J Pharm Biomed Anal. 2019;177:112880. PMID:31546137. doi:10.1016/j.jpba.2019.112880.
   PubMed Web of Science ®Google Scholar
• Zhao Q, Modis Y, High K, Towne V, Meng Y, Wang Y, Alexandroff J, Brown M, Carragher B, Potter CS, et al. Disassembly and reassembly of human papillomavirus virus-like particles produces more virion-like antibody reactivity. Virol J. 2012;9:52. PMID:22356831. doi:10.1186/1743-422X-9-52.
   PubMed Web of Science ®Google Scholar
• Wang X, Li M, Lin Z, Pan H, Tang Z, Zheng Z, Li S, Zhang J, Xia N, Zhao Q, et al. Multifaceted characterization of recombinant protein-based vaccines: an immunochemical toolbox for epitope-specific analyses of the hepatitis E vaccine. Vaccine. 2018;36:7650–58. PMID:30396752. doi:10.1016/j.vaccine.2018.10.089.
   PubMed Web of Science ®Google Scholar
• Wu X, Chen P, Lin H, Su Y, Hao X, Cao Y, Li L, Zhu F, Liang Z. Dynamics of 8G12 competitive antibody in “prime-boost” vaccination of Hepatitis E vaccine. Hum Vaccin Immunother. 2017;13:1–6. PMID:28272983. doi:10.1080/21645515.2017.1291105.
   Web of Science ®Google Scholar
• Liu C, Cai W, Yin X, Tang Z, Wen G, Ambardekar C, Li X, Ying D, Feng Z, Zheng Z, et al. An optimized high-throughput neutralization assay for Hepatitis E Virus (HEV) involving detection of secreted porf2. Viruses. 2019;11:64. PMID: 30650547. doi:10.3390/v11010064.
   PubMed Web of Science ®Google Scholar
• Marasco WA, Sui J. The growth and potential of human antiviral monoclonal antibody therapeutics. Nat Biotechnol. 2007;25:1421–34. PMID:18066039. doi:10.1038/nbt1363.
   PubMed Web of Science ®Google Scholar
• Yin X, Ying D, Lhomme S, Tang Z, Walker CM, Xia N, Zheng Z, Feng Z. Origin, antigenicity, and function of a secreted form of ORF2 in hepatitis E virus infection. Proc Natl Acad Sci USA. 2018;115:4773–78. PMID:29669922. doi:10.1073/pnas.1721345115.
   PubMed Web of Science ®Google Scholar
• Geng Y, Zhao C, Huang W, Harrison TJ, Zhang H, Geng K, Wang Y. Detection and assessment of infectivity of hepatitis E virus in urine. J Hepatol. 2016;64:37–43. PMID:26362822. doi:10.1016/j.jhep.2015.08.034.
   PubMed Web of Science ®Google Scholar
• Wen GP, Tang ZM, Yang F, Zhang K, Ji WF, Cai W, Huang SJ, Wu T, Zhang J, Zheng ZZ, et al. A valuable antigen detection method for diagnosis of acute hepatitis E. J Clin Microbiol. 2015;53:782–88. PMID:25540394 https://jcm.asm.org/content/53/3/782.
   PubMed Web of Science ®Google Scholar
• Montpellier C, Wychowski C, Sayed IM, Meunier JC, Saliou JM, Ankavay M, Bull A, Pillez A, Abravanel F, Helle F, et al. Hepatitis E virus lifecycle and identification of 3 forms of the ORF2 capsid protein. Gastroenterology. 2018;154:211–23. PMID:28958858. doi:10.1053/j.gastro.2017.09.020.
   PubMed Web of Science ®Google Scholar