Antigenic determinants of hepatitis e virus and vaccine-induced immunogenicity and efficacy

Journal of Gastroenterology

Volumn 48, Issue 2, 2013, Pages 159-168

  Zhao, Qinjian ^a   Zhang, Jun ^a   Wu, Ting ^a   Li, Shao Wei ^a   Ng, Mun Hon ^a   Xia, Ning Shao ^a   Shih, James Wai Kuo ^a  

^a XIAMEN UNIVERSITY   (China)

Author keywords

Antigenic determinants; Hepatitis E; Hepatitis E virus; Immunogenicity; Vaccine; Vaccine efficacy

Indexed keywords

BIOLOGICAL MARKER; EPITOPE; HECOLIN; HEPATITIS E VACCINE; IMMUNOGLOBULIN G; UNCLASSIFIED DRUG; HEPATITIS ANTIGEN; HEPATITIS VACCINE;

ANTIBODY RESPONSE; BLOOD SAMPLING; CLINICAL EVALUATION; CRYSTAL STRUCTURE; GENOTYPE; HEPATITIS; HEPATITIS E; HEPATITIS E VIRUS; HUMAN; IMMUNOGENICITY; IMMUNOGLOBULIN BLOOD LEVEL; IMMUNOREACTIVITY; NONHUMAN; PREGNANT WOMAN; PRIORITY JOURNAL; PROTECTION; REINFECTION; REVIEW; SENSITIVITY AND SPECIFICITY; SEROCONVERSION; SERODIAGNOSIS; ANIMAL; BLOOD; DISEASE MODEL; IMMUNOLOGY;

ANIMALS; BIOLOGICAL MARKERS; DISEASE MODELS, ANIMAL; EPITOPES; HEPATITIS ANTIGENS; HEPATITIS E; HEPATITIS E VIRUS; HUMANS; VIRAL HEPATITIS VACCINES;

MLCS; MLOWN;

EID: 84879475483     PISSN: 09441174     EISSN: 14355922     Source Type: Journal    
DOI: 10.1007/s00535-012-0701-1     Document Type: Review

References (72)

1. Teshale EH, Hu DJ, Holmberg SD. The two faces of hepatitis E virus. Clin Infect Dis. 2010;51(3): 328-34.
2. Purcell RH, Emerson SU. Prevention. In: Thomas HC, Lemon S, Zuckerman AJ, editors. Viral hepatitis. 3rd ed. Malden: Blackwell; 2005. p. 635-45.
3. Aggarwal R. The global prevalence of hepatitis E virus infection and susceptibility: a systematic review. WHO/IVB/10.14. Viral hepatitis in the WHO South-East Asia region, 2011, SEA-CD- 232; 2010.
4. Nelson KE, Kmush B, Labrique AB. The epidemiology of hepatitis E virus infections in developed countries and among immunocompromised patients. Expert Rev Anti Infect Ther. 2011;9(12): 1133-48.
5. Dalton HR, Bendall RP, Keane FE, Tedder RS, Ijaz S. Persistent carriage of hepatitis E virus in patients with HIV infection. N Engl J Med. 2009;361(10): 1025-7.
6. Kamar N, Selves J, Mansuy JM, Ouezzani L, Peron JM, Guitard J, et al. Hepatitis E virus and chronic hepatitis in organ-transplant recipients. N Engl J Med. 2008;358(8): 811-7.
7. Kamar N, Garrouste C, Haagsma EB, Garrigue V, Pischke S, Chauvet C, et al. Factors associated with chronic hepatitis in patients with hepatitis E virus infection who have received solid organ transplants. Gastroenterology. 2011;140(5): 1481-9.
8. Wu T, Zhu FC, Huang SJ, Zhang XF, Wang ZZ, Zhang J, et al. Safety of the hepatitis E vaccine for pregnant women: a preliminary analysis. Hepatology. 2012;55(6):2038.
9. Labrique AB, Zaman K, Hossain Z, Saha P, Yunus M, Hossain A, et al. Epidemiology and risk factors of incident hepatitis E virus infections in rural Bangladesh. Am J Epidemiol. 2010;172(8): 952-61.
10. Koonin EV, Gorbalenya AE, Purdy MA, Rozanov MN, Reyes GR, Bradley DW. Computer-assisted assignment of functional domains in the nonstructural polyprotein of hepatitis E virus: delineation of an additional group of positive-strand RNA plant and animal viruses. Proc Natl Acad Sci U S A. 1992;89(17): 8259-63.
11. Zafrullah M, Ozdener MH, Panda SK, Jameel S. The ORF3 protein of hepatitis E virus is a phosphoprotein that associates with the cytoskeleton. J Virol. 1997;71(12): 9045-53.
12. Panda SK, Thakral D, Rehman S. Hepatitis E virus. Rev Med Virol. 2007;17(3): 151-80.
13. Tyagi S, Korkaya H, Zafrullah M, Jameel S, Lal SK. The phosphorylated form of the ORF3 protein of hepatitis E virus interacts with its non-glycosylated form of the major capsid protein, ORF2. J Biol Chem. 2002;277(25): 22759-67.
14. Tyagi S, Surjit M, Lal SK. The 41-amino-acid C-terminal region of the hepatitis E virus ORF3 protein interacts with bikunin, a kunitz-type serine protease inhibitor. J Virol. 2005;79(18): 12081-7.
15. Tyagi S, Surjit M, Roy AK, Jameel S, Lal SK. The ORF3 protein of hepatitis E virus interacts with liver-specific alpha1-microglobulin and its precursor alpha1-microglobulin/bikunin precursor (AMBP) and expedites their export from the hepatocyte. J Biol Chem. 2004;279(28): 29308-19.
16. Yamada K, Takahashi M, Hoshino Y, Takahashi H, Ichiyama K, Nagashima S, et al. ORF3 protein of hepatitis E virus is essential for virion release from infected cells. J General Virol. 2009;90(Pt 8): 1880-91.
17. Chandra V, Kalia M, Hajela K, Jameel S. The ORF3 protein of hepatitis E virus delays degradation of activated growth factor receptors by interacting with CIN85 and blocking formation of the Cbl-CIN85 complex. J Virol. 2010;84(8): 3857-67.
18. Takahashi M, Yamada K, Hoshino Y, Takahashi H, Ichiyama K, Tanaka T, et al. Monoclonal antibodies raised against the ORF3 protein of hepatitis E virus (HEV) can capture HEV particles in culture supernatant and serum but not those in feces. Arch Virol. 2008;153(9): 1703-13.
19. Zhang J, Li SW, Wu T, Zhao Q, Ng MH, Xia NS. Hepatitis E virus: neutralizing sites, diagnosis, and protective immunity. Rev Med Virol. 2012;22(5): 339-49.
20. Zhang J, Ge SX, Huang GY, Li SW, He ZQ, Wang YB, et al. Evaluation of antibody-based and nucleic acid-based assays for diagnosis of hepatitis E virus infection in a rhesus monkey model. J Med Virol. 2003;71(4): 518-26.
21. Bendall R, Ellis V, Ijaz S, Ali R, Dalton H. A comparison of two commercially available anti-HEV IgG kits and a re-evaluation of anti-HEV IgG seroprevalence data in developed countries. J Med Virol. 2010;82(5): 799-805.
22. Lee SD, Wang YJ, Lu RH, Chan CY, Lo KJ, Moeckli R. Seroprevalence of antibody to hepatitis E virus among Chinese subjects in Taiwan. Hepatology. 1994;19(4): 866-70.
23. Xing L, Kato K, Li T, Takeda N, Miyamura T, Hammar L, et al. Recombinant hepatitis E capsid protein self-assembles into a dual-domain T = 1 particle presenting native virus epitopes. Virology. 1999;265(1): 35-45.
24. Li TC, Takeda N, Miyamura T, Matsuura Y, Wang JC, Engvall H, et al. Essential elements of the capsid protein for self-assembly into empty virus-like particles of hepatitis E virus. J Virol. 2005;79(20): 12999-3006.
25. Xing L, Li TC, Mayazaki N, Simon MN, Wall JS, Moore M, et al. Structure of hepatitis E virion-sized particle reveals an RNAdependent viral assembly pathway. J Biol Chem. 2010;285(43): 33175-83.
26. Guu TS, Liu Z, Ye Q, Mata DA, Li K, Yin C, et al. Structure of the hepatitis E virus-like particle suggests mechanisms for virus assembly and receptor binding. Proc Natl Acad Sci U S A. 2009;106(31): 12992-7.
27. Yamashita T, Mori Y, Miyazaki N, Cheng RH, Yoshimura M, Unno H, et al. Biological and immunological characteristics of hepatitis E virus-like particles based on the crystal structure. Proc Natl Acad Sci U S A. 2009;106(31): 12986-91.
28. Mast EE, Alter MJ, Holland PV, Purcell RH. Evaluation of assays for antibody to hepatitis E virus by a serum panel. Hepatitis E Virus Antibody Serum Panel Evaluation Group. Hepatology. 1998;27(3): 857-61.
29. Ghabrah TM, Tsarev S, Yarbough PO, Emerson SU, Strickland GT, Purcell RH. Comparison of tests for antibody to hepatitis E virus. J Med Virol. 1998;55(2): 134-7.
30. Khudyakov Y, Kamili S. Serological diagnostics of hepatitis E virus infection. Virus Res. 2011;161(1): 84-92.
31. Huang W, Zhang H, Harrison TJ, Lang S, Huang G, Wang Y. Cross-protection of hepatitis E virus genotypes 1 and 4 in Rhesus macaques. J Med Virol. 2008;80(5): 824-32.
32. Zhang JZ, Im SW, Lau SH, Chau TN, Lai ST, Ng SP, et al. 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(1): 40-8.
33. Bendall R, Ellis V, Ijaz S, Thurairajah P, Dalton HR. Serological response to hepatitis E virus genotype 3 infection: IgG quantitation, avidity, and IgM response. J Med Virol. 2008;80(1): 95-101.
34. Bigaillon C, Tesse S, Lagathu G, Nicand E. Use of hepatitis E IgG avidity for diagnosis of hepatitis E infection. J Virol Methods. 2010;164(1-2): 127-30.
35. Huang S, Zhang X, Jiang H, Yan Q, Ai X, Wang Y, et al. Profile of acute infectious markers in sporadic hepatitis E. PLoS One. 2010;5(10):e13560.
36. Seriwatana J, Shrestha MP, Scott RM, Tsarev SA, Vaughn DW, Myint KS, et al. Clinical and epidemiological relevance of quantitating hepatitis E virus-specific immunoglobulin M. Clin Diagn Lab Immunol. 2002;9(5): 1072-8.
37. Takahashi M, Kusakai S, Mizuo H, Suzuki K, Fujimura K, Masuko K, et al. Simultaneous detection of immunoglobulin A (IgA) and IgM antibodies against hepatitis E virus (HEV) is highly specific for diagnosis of acute HEV infection. J Clin Microbiol. 2005;43(1): 49-56.
38. Elkady A, Tanaka Y, Kurbanov F, Hirashima N, Sugiyama M, Khan A, et al. Evaluation of anti-hepatitis E virus (HEV) immunoglobulin A in a serological screening for HEV infection. J Gastroenterol. 2007;42(11): 911-7.
39. Herremans M, Duizer E, Jusic E, Koopmans MP. Detection of hepatitis E virus-specific immunoglobulin A in patients infected with hepatitis E virus genotype 1 or 3. Clin Vaccine Immunol. 2007;14(3): 276-80.
40. Zhang JZ, Ng MH, Xia NS, Lau SH, Che XY, Chau TN, et al. Conformational antigenic determinants generated by interactions between a bacterially expressed recombinant peptide of the hepatitis E virus structural protein. J Med Virol. 2001;64(2): 125-32.
41. Im SW, Zhang JZ, Zhuang H, Che XY, Zhu WF, Xu GM, et al. A bacterially expressed peptide prevents experimental infection of primates by the hepatitis E virus. Vaccine. 2001;19(27): 3726-32.
42. Li SW, Zhang J, He ZQ, Gu Y, Liu RS, Lin J, et al. Mutational analysis of essential interactions involved in the assembly of hepatitis E virus capsid. J Biol Chem. 2005;280(5): 3400-6.
43. Li SW, Zhang J, Li YM, Ou SH, Huang GY, He ZQ, et al. A bacterially expressed particulate hepatitis E vaccine: antigenicity, immunogenicity and protectivity on primates. Vaccine. 2005;23 (22): 2893-901.
44. Tang X, Yang C, Gu Y, Song C, Zhang X, Wang Y, et al. Structural basis for the neutralization and genotype specificity of hepatitis E virus. Proc Natl Acad Sci U S A. 2011;108(25): 10266-71.
45. Bryan JP, Tsarev SA, Iqbal M, Ticehurst J, Emerson S, Ahmed A, et al. Epidemic hepatitis E in Pakistan: patterns of serologic response and evidence that antibody to hepatitis E virus protects against disease. J Infect Dis. 1994;170(3): 517-21.
46. Tsarev SA, Tsareva TS, Emerson SU, Govindarajan S, Shapiro M, Gerin JL, et al. Successful passive and active immunization of cynomolgus monkeys against hepatitis E. Proc Natl Acad Sci U S A. 1994;91(21): 10198-202.
47. Prasad BV, Hardy ME, Dokland T, Bella J, Rossmann MG, Estes MK. X-ray crystallographic structure of the Norwalk virus capsid. Science. 1999;286(5438): 287-90.
48. Dong J, Dong L, Mendez E, Tao Y. Crystal structure of the human astrovirus capsid spike. Proc Natl Acad Sci U S A. 2011; 108(31): 12681-6.
49. Pokidysheva E, Zhang Y, Battisti AJ, Bator-Kelly CM, Chipman PR, Xiao C, et al. Cryo-EM reconstruction of dengue virus in complex with the carbohydrate recognition domain of DC-SIGN. Cell. 2006;124(3): 485-93.
50. Kwong PD, Wyatt R, Robinson J, Sweet RW, Sodroski J, Hendrickson WA. Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature. 1998;393(6686): 648-59.
51. Bullough PA, Hughson FM, Skehel JJ, Wiley DC. Structure of influenza haemagglutinin at the pH of membrane fusion. Nature. 1994;371(6492): 37-43.
52. Wu L, Gerard NP, Wyatt R, Choe H, Parolin C, Ruffing N, et al. CD4-induced interaction of primary HIV-1 gp120 glycoproteins with the chemokine receptor CCR-5. Nature. 1996;384(6605): 179-83.
53. Wyatt R, Kwong PD, Desjardins E, Sweet RW, Robinson J, Hendrickson WA, et al. The antigenic structure of the HIV gp120 envelope glycoprotein. Nature. 1998;393(6686): 705-11.
54. Li S, Tang X, Seetharaman J, Yang C, Gu Y, Zhang J, et al. Dimerization of hepatitis E virus capsid protein E2s domain is essential for virus-host interaction. PLoS Pathog. 2009;5(8): e1000537.
55. Li F, Torresi J, Locarnini SA, Zhuang H, Zhu W, Guo X, et al. Amino-terminal epitopes are exposed when full-length open reading frame 2 of hepatitis E virus is expressed in Escherichia coli, but carboxy-terminal epitopes are masked. J Med Virol. 1997;52(3): 289-300.
56. Robinson RA, Burgess WH, Emerson SU, Leibowitz RS, Sosnovtseva SA, Tsarev S, et al. Structural characterization of recombinant hepatitis E virus ORF2 proteins in baculovirusinfected insect cells. Protein Expr Purif. 1998;12(1): 75-84.
57. Zhang M, Emerson SU, Nguyen H, Engle RE, Govindarajan S, Gerin JL, et al. Immunogenicity and protective efficacy of a vaccine prepared from 53 kDa truncated hepatitis E virus capsid protein expressed in insect cells. Vaccine. 2001;20(5-6): 853-7.
58. Shrestha MP, Scott RM, Joshi DM, Mammen MP Jr, Thapa GB, Thapa N, et al. Safety and efficacy of a recombinant hepatitis E vaccine. N Engl J Med. 2007;356(9): 895-903.
59. Zhu FC, Zhang J, Zhang XF, Zhou C, Wang ZZ, Huang SJ, et al. Efficacy and safety of a recombinant hepatitis E vaccine in healthy adults: a large-scale, randomised, double-blind placebocontrolled, phase 3 trial. Lancet. 2010;376(9744): 895-902.
60. Purdy MA, McCaustland KA, Krawczynski K, Tam A, Beach MJ, Tassopoulos NC, et al. Expression of a hepatitis E virus (HEV)-trpE fusion protein containing epitopes recognized by antibodies in sera from human cases and experimentally infected primates. Arch Virol. 1992;123(3-4): 335-49.
61. Schofield DJ, Glamann J, Emerson SU, Purcell RH. Identification by phage display and characterization of two neutralizing chimpanzee monoclonal antibodies to the hepatitis E virus capsid protein. J Virol. 2000;74(12): 5548-55.
62. Meng J, Dai X, Chang JC, Lopareva E, Pillot J, Fields HA, et al. Identification and characterization of the neutralization epitope (s) of the hepatitis E virus. Virology. 2001;288(2): 203-11.
63. Zhang J, Gu Y, Ge SX, Li SW, He ZQ, Huang GY, et al. Analysis of hepatitis E virus neutralization sites using monoclonal antibodies directed against a virus capsid protein. Vaccine. 2005;23 (22): 2881-92.
64. He J, Kuschner RA, Dewar V, Voet P, Asher LV, Vaughn DW. Characterization of monoclonal antibodies to hepatitis E virus (HEV) capsid protein and identification of binding activity. J Biomed Sci. 2007;14(5): 555-63.
65. Zhang H, Dai X, Shan X, Meng J. The Leu477 and Leu613 of ORF2-encoded protein are critical in forming neutralization antigenic epitope of hepatitis E virus genotype 4. Cell Mol Immunol. 2008;5(6): 447-56.
66. Takahashi M, Hoshino Y, Tanaka T, Takahashi H, Nishizawa T, Okamoto H. Production of monoclonal antibodies against hepatitis E virus capsid protein and evaluation of their neutralizing activity in a cell culture system. Arch Virol. 2008;153(4): 657-66.
67. Xing L, Wang JC, Li TC, Yasutomi Y, Lara J, Khudyakov Y, et al. Spatial configuration of hepatitis E virus antigenic domain. J Virol. 2011;85(2): 1117-24.
68. Guthmann JP, Klovstad H, Boccia D, Hamid N, Pinoges L, Nizou JY, et al. A large outbreak of hepatitis E among a displaced population in Darfur, Sudan, 2004: the role of water treatment methods. Clin Infect Dis. 2006;42(12): 1685-91.
69. Bryan JP, Iqbal M, Tsarev S, Malik IA, Duncan JF, Ahmed A, et al. Epidemic of hepatitis E in a military unit in Abbotrabad, Pakistan. Am J Trop Med Hyg. 2002;67(6): 662-8.
70. Clayson ET, Vaughn DW, Innis BL, Shrestha MP, Pandey R, Malla DB. Association of hepatitis E virus with an outbreak of hepatitis at a military training camp in Nepal. J Med Virol. 1998; 54(3): 178-82.
71. 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(4): 988-97.
72. Goel A, Aggarwal R. Prevention of hepatitis E: another step forward. Future Microbiol. 2011;6(1): 23-7.