Development of the Hepatitis E Vaccine: From Bench to Field

Jun Zhang; James WaiKuo Shih; Ting Wu; Shao-Wei Li; Ning-Shao Xia

doi:10.1055/s-0033-1338116

Seminars in Liver Disease, Inhaltsverzeichnis

Semin Liver Dis 2013; 33(01): 079-088
DOI: 10.1055/s-0033-1338116

Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Development of the Hepatitis E Vaccine: From Bench to Field

Jun Zhang

¹National Institute of Diagnostics and Vaccine Development in Infectious Diseases, Xiamen University, Xiamen, People's Republic of China

,

James WaiKuo Shih

¹National Institute of Diagnostics and Vaccine Development in Infectious Diseases, Xiamen University, Xiamen, People's Republic of China

,

Ting Wu

¹National Institute of Diagnostics and Vaccine Development in Infectious Diseases, Xiamen University, Xiamen, People's Republic of China

,

Shao-Wei Li

¹National Institute of Diagnostics and Vaccine Development in Infectious Diseases, Xiamen University, Xiamen, People's Republic of China

,

Ning-Shao Xia Prof.

¹National Institute of Diagnostics and Vaccine Development in Infectious Diseases, Xiamen University, Xiamen, People's Republic of China

› Institutsangaben

Abstract

Along with the improvement of diagnostic techniques, hepatitis E has attracted increasing awareness in recent years. Hepatitis E virus infection leads to high mortality in pregnant women and patients with underlying liver disease. Several hepatitis E vaccine candidates have been designed and have proved their efficacy in animal models; two candidates have successfully undergone clinical trials. Having proved safe and effective in a large phase III trials, an Escherichia coli expressed particulate protein, HEV 239, has been registered in China and is now available for use in China.

Keywords

hepatitis E virus - HEV - antigenic determinants - vaccine - immunogenicity - vaccine efficacy

Volltext

Referenzen

References
1 Wedemeyer H, Pischke S, Manns MP. Pathogenesis and treatment of hepatitis e virus infection. Gastroenterology 2012; 142 (6) 1388-1397 , e1
2 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) 988-997
3 Kamar N, Bendall R, Legrand-Abravanel F , et al. Hepatitis E. Lancet 2012; 379 (9835) 2477-2488
4 Hoofnagle JH, Nelson KE, Purcell RH. Hepatitis E. N Engl J Med 2012; 367 (13) 1237-1244
5 Kamar N, Bendall RP, Peron JM , et al. Hepatitis E virus and neurologic disorders. Emerg Infect Dis 2011; 17 (2) 173-179
6 Boccia D, Guthmann JP, Klovstad H , et al. High mortality associated with an outbreak of hepatitis E among displaced persons in Darfur, Sudan. Clin Infect Dis 2006; 42 (12) 1679-1684
7 Teshale EH, Howard CM, Grytdal SP , et al. Hepatitis E epidemic, Uganda. Emerg Infect Dis 2010; 16 (1) 126-129
8 Corwin AL, Khiem HB, Clayson ET , et al. A waterborne outbreak of hepatitis E virus transmission in southwestern Vietnam. Am J Trop Med Hyg 1996; 54 (6) 559-562
9 Khuroo MS. Study of an epidemic of non-A, non-B hepatitis. Possibility of another human hepatitis virus distinct from post-transfusion non-A, non-B type. Am J Med 1980; 68 (6) 818-824
10 Naik SR, Aggarwal R, Salunke PN, Mehrotra NN. A large waterborne viral hepatitis E epidemic in Kanpur, India. Bull World Health Organ 1992; 70 (5) 597-604
11 Velázquez O, Stetler HC, Avila C , et al. Epidemic transmission of enterically transmitted non-A, non-B hepatitis in Mexico, 1986–1987. JAMA 1990; 263 (24) 3281-3285
12 Meng XJ, Wiseman B, Elvinger F , et al. Prevalence of antibodies to hepatitis E virus in veterinarians working with swine and in normal blood donors in the United States and other countries. J Clin Microbiol 2002; 40 (1) 117-122
13 Abe K, Li TC, Ding X , et al. International collaborative survey on epidemiology of hepatitis E virus in 11 countries. Southeast Asian J Trop Med Public Health 2006; 37 (1) 90-95
14 Kuniholm MH, Purcell RH, McQuillan GM, Engle RE, Wasley A, Nelson KE. Epidemiology of hepatitis E virus in the United States: results from the Third National Health and Nutrition Examination Survey, 1988-1994. J Infect Dis 2009; 200 (1) 48-56
15 Mansuy JM, Bendall R, Legrand-Abravanel F , et al. Hepatitis E virus antibodies in blood donors, France. Emerg Infect Dis 2011; 17 (12) 2309-2312
16 Boutrouille A, Bakkali-Kassimi L, Crucière C, Pavio N. Prevalence of anti-hepatitis E virus antibodies in French blood donors. J Clin Microbiol 2007; 45 (6) 2009-2010
17 Buti M, Domínguez A, Plans P , et al. Community-based seroepidemiological survey of hepatitis E virus infection in Catalonia, Spain. Clin Vaccine Immunol 2006; 13 (12) 1328-1332
18 Ijaz S, Vyse AJ, Morgan D, Pebody RG, Tedder RS, Brown D. Indigenous hepatitis E virus infection in England: more common than it seems. J Clin Virol 2009; 44 (4) 272-276
19 Taniguchi M, Kim SR, Mishiro S , et al. Epidemiology of hepatitis E in Northeastern China, South Korea and Japan. J Infect 2009; 58 (3) 232-237
20 Christensen PB, Engle RE, Hjort C , et al. Time trend of the prevalence of hepatitis E antibodies among farmers and blood donors: a potential zoonosis in Denmark. Clin Infect Dis 2008; 47 (8) 1026-1031
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 Mansuy JM, Legrand-Abravanel F, Calot JP , et al. High prevalence of anti-hepatitis E virus antibodies in blood donors from South West France. J Med Virol 2008; 80 (2) 289-293
23 Dalton HR, Fellows HJ, Stableforth W , et al. The role of hepatitis E virus testing in drug-induced liver injury. Aliment Pharmacol Ther 2007; 26 (10) 1429-1435
24 Davern TJ, Chalasani N, Fontana RJ , et al; Drug-Induced Liver Injury Network (DILIN). Acute hepatitis E infection accounts for some cases of suspected drug-induced liver injury. Gastroenterology 2011; 141 (5) 1665-1672 , e1–e9
25 Zhao Q, Zhang J, Wu T , et al. Antigenic determinants of hepatitis E virus and vaccine-induced immunogenicity and efficacy. J Gastroenterol 2012;
26 FitzSimons D, Hendrickx G, Vorsters A, Van Damme P. Hepatitis A and E: update on prevention and epidemiology. Vaccine 2010; 28 (3) 583-588
27 Bryan JP, Tsarev SA, Iqbal M , 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) 517-521
28 Krawczynski K, Meng XJ, Rybczynska J. Pathogenetic elements of hepatitis E and animal models of HEV infection. Virus Res 2011; 161 (1) 78-83
29 Arankalle VA, Chadha MS, Chobe LP. Long-term serological follow up and cross-challenge studies in rhesus monkeys experimentally infected with hepatitis E virus. J Hepatol 1999; 30 (2) 199-204
30 Arankalle VA, Chadha MS, Chobe LP, Nair R, Banerjee K. Cross-challenge studies in rhesus monkeys employing different Indian isolates of hepatitis E virus. J Med Virol 1995; 46 (4) 358-363
31 Arankalle VA, Favorov MO, Chadha MS, Phule DM, Banerjee K. Rhesus monkeys infected with hepatitis E virus (HEV) from the former USSR are immune to subsequent challenge with an Indian strain of HEV. Acta Virol 1993; 37 (6) 515-518
32 Tsarev SA, Tsareva TS, Emerson SU , et al. Successful passive and active immunization of cynomolgus monkeys against hepatitis E. Proc Natl Acad Sci U S A 1994; 91 (21) 10198-10202
33 Zhang J, Gu Y, Ge SX , et al. Analysis of hepatitis E virus neutralization sites using monoclonal antibodies directed against a virus capsid protein. Vaccine 2005; 23 (22) 2881-2892
34 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) 5548-5555
35 Engle RE, Yu C, Emerson SU, Meng XJ, Purcell RH. Hepatitis E virus (HEV) capsid antigens derived from viruses of human and swine origin are equally efficient for detecting anti-HEV by enzyme immunoassay. J Clin Microbiol 2002; 40 (12) 4576-4580
36 Zhang J, Ge SX, Huang GY , 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) 518-526
37 Meng J, Pillot J, Dai X, Fields HA, Khudyakov YE. Neutralization of different geographic strains of the hepatitis E virus with anti-hepatitis E virus-positive serum samples obtained from different sources. Virology 1998; 249 (2) 316-324
38 Emerson SU, Clemente-Casares P, Moiduddin N, Arankalle VA, Torian U, Purcell RH. Putative neutralization epitopes and broad cross-genotype neutralization of Hepatitis E virus confirmed by a quantitative cell-culture assay. J Gen Virol 2006; 87 (Pt 3) 697-704
39 Purcell RH, Nguyen H, Shapiro M , et al. Pre-clinical immunogenicity and efficacy trial of a recombinant hepatitis E vaccine. Vaccine 2003; 21 (19–20) 2607-2615
40 Li SW, Zhang J, Li YM , et al. A bacterially expressed particulate hepatitis E vaccine: antigenicity, immunogenicity and protectivity on primates. Vaccine 2005; 23 (22) 2893-2901
41 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) 824-832
42 Sanford BJ, Dryman BA, Huang YW, Feagins AR, Leroith T, Meng XJ. Prior infection of pigs with a genotype 3 swine hepatitis E virus (HEV) protects against subsequent challenges with homologous and heterologous genotypes 3 and 4 human HEV. Virus Res 2011; 159 (1) 17-22
43 Tang X, Yang C, Gu 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) 10266-10271
44 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) 339-349
45 Li S, Tang X, Seetharaman J , et al. Dimerization of hepatitis E virus capsid protein E2s domain is essential for virus-host interaction. PLoS Pathog 2009; 5 (8) e1000537
46 Xing L, Wang JC, Li TC , et al. Spatial configuration of hepatitis E virus antigenic domain. J Virol 2011; 85 (2) 1117-1124
47 Meng J, Dai X, Chang JC , et al. Identification and characterization of the neutralization epitope(s) of the hepatitis E virus. Virology 2001; 288 (2) 203-211
48 Li SW, Zhang J, He ZQ , et al. Mutational analysis of essential interactions involved in the assembly of hepatitis E virus capsid. J Biol Chem 2005; 280 (5) 3400-3406
49 Yamashita T, Mori Y, Miyazaki N , 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) 12986-12991
50 Amini-Bavil-Olyaee Samad, Trautwein Christian, Tacke Frank. Hepatitis E vaccine: current status and future prospects. Future virology 2009; 4 (2) 143-154
51 Purdy MA, McCaustland KA, Krawczynski K, Spelbring J, Reyes GR, Bradley DW. Preliminary evidence that a trpE-HEV fusion protein protects cynomolgus macaques against challenge with wild-type hepatitis E virus (HEV). J Med Virol 1993; 41 (1) 90-94
52 Purdy MA, McCaustland KA, Krawczynski K , 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) 335-349
53 Robinson RA, Burgess WH, Emerson SU , et al. Structural characterization of recombinant hepatitis E virus ORF2 proteins in baculovirus-infected insect cells. Protein Expr Purif 1998; 12 (1) 75-84
54 Tsarev SA, Tsareva TS, Emerson SU , et al. ELISA for antibody to hepatitis E virus (HEV) based on complete open-reading frame-2 protein expressed in insect cells: identification of HEV infection in primates. J Infect Dis 1993; 168 (2) 369-378
55 Zhang M, Emerson SU, Nguyen H , 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) 853-857
56 Tsarev SA, Tsareva TS, Emerson SU , et al. Recombinant vaccine against hepatitis E: dose response and protection against heterologous challenge. Vaccine 1997; 15 (17–18) 1834-1838
57 Zhang M, Emerson SU, Nguyen H , et al. Recombinant vaccine against hepatitis E: duration of protective immunity in rhesus macaques. Vaccine 2002; 20 (27–28) 3285-3291
58 Huang WJ, Zhang HY, Harrison TJ, Lan HY, Huang GY, Wang YC. Immunogenicity and protective efficacy in rhesus monkeys of a recombinant ORF2 protein from hepatitis E virus genotype 4. Arch Virol 2009; 154 (3) 481-488
59 Li TC, Yamakawa Y, Suzuki K , et al. Expression and self-assembly of empty virus-like particles of hepatitis E virus. J Virol 1997; 71 (10) 7207-7213
60 Li TC, Takeda N, Miyamura T , 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) 12999-13006
61 Li TC, Suzaki Y, Ami Y, Dhole TN, Miyamura T, Takeda N. Protection of cynomolgus monkeys against HEV infection by oral administration of recombinant hepatitis E virus-like particles. Vaccine 2004; 22 (3–4) 370-377
62 Zhang JZ, Ng MH, Xia NS , 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) 125-132
63 Guu TS, Liu Z, Ye Q , 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) 12992-12997
64 Ge S, Zhang J, Huang G, Pang S, Zhou K, Xia N. [The immuno-protect study of a hepatitis E virus ORF2 peptide expressed in E. coli]. Wei Sheng Wu Xue Bao 2003; 43 (1) 35-42
65 Wu T, Wu XL, Ou SH , et al. Difference of T cell and B cell activation in two homologous proteins with similar antigenicity but great distinct immunogenicity. Mol Immunol 2007; 44 (12) 3261-3266
66 Wu T, Zhang J, Su ZJ , et al. Specific cellular immune response in hepatitis E patients. Intervirology 2008; 51 (5) 322-327
67 Proffitt A. First HEV vaccine approved. Nat Biotechnol 2012; 30: 300
68 Park SB. Hepatitis E vaccine debuts. Nature 2012; 491 (7422) 21-22
69 Safary A. Perspectives of vaccination against hepatitis E. Intervirology 2001; 44 (2–3) 162-166
70 Shrestha MP, Scott RM, Joshi DM , et al. Safety and efficacy of a recombinant hepatitis E vaccine. N Engl J Med 2007; 356 (9) 895-903
71 Wu T, Li SW, Zhang J, Ng MH, Xia NS, Zhao Q. Hepatitis E vaccine development: a 14. year odyssey. Hum Vaccin Immunother 2012; 8 (6) 823-827
72 Zhang J, Liu CB, Li RC , et al. Randomized-controlled phase II clinical trial of a bacterially expressed recombinant hepatitis E vaccine. Vaccine 2009; 27 (12) 1869-1874
73 Zhu FC, Zhang J, Zhang XF , 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 (9744) 895-902
74 Wu T, Zhu FC, Huang SJ , et al. Safety of the hepatitis E vaccine for pregnant women: a preliminary analysis. Hepatology 2012; 55 (6) 2038
75 News Stories. Stretched UNHCR faces difficulties containing hepatitis E outbreak in South Sudan. The UN Refugee Agency. 2012. Available at: http://www.unhcr.org/509d084d9.html . Accessed November 9, 2012
76 Im SW, Zhang JZ, Zhuang H , et al. A bacterially expressed peptide prevents experimental infection of primates by the hepatitis E virus. Vaccine 2001; 19 (27) 3726-3732
77 Yarbough PO. Hepatitis E virus. Advances in HEV biology and HEV vaccine approaches. Intervirology 1999; 42 (2–3) 179-184
78 Kamili S, Spelbring J, Carson D, Krawczynski K. Protective efficacy of hepatitis E virus DNA vaccine administered by gene gun in the cynomolgus macaque model of infection. J Infect Dis 2004; 189 (2) 258-264
79 Arankalle VA, Lole KS, Deshmukh TM, Srivastava S, Shaligram US. Challenge studies in Rhesus monkeys immunized with candidate hepatitis E vaccines: DNA, DNA-prime-protein-boost and DNA-protein encapsulated in liposomes. Vaccine 2009; 27 (7) 1032-1039