Characterization of two novel linear B-cell epitopes in the capsid protein of avian hepatitis E virus (HEV) that are common to avian, swine, and human HEVs

Journal of Virology

Volumn 89, Issue 10, 2015, Pages 5491-5501

  Wang, Xinjie ^a,b   Zhao, Qin ^a,b   Dang, Lu ^a,c   Sun, Yani ^a,b   Gao, Jiming ^a,b   Liu, Baoyuan ^a,b   Syed, Shahid Faraz ^a,b   Tao, Hu ^a   Zhang, Gaiping ^a,c   Luo, Jianxun ^d   Zhou, En Min ^a,b  

^a NORTHWEST A F UNIVERSITY   (China)

^b Agriculture Ministry of China   (China)

^c HENAN AGRICULTURAL UNIVERSITY   (China)

^d INSTITUTE OF PLANT PROTECTION   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; EPITOPE; MONOCLONAL ANTIBODY; HEPATITIS ANTIGEN; VIRUS ANTIBODY;

AMINO ACID SEQUENCE; ANTIGEN BINDING; ANTIGEN DETECTION; ANTIGEN FUNCTION; ARTICLE; BINDING AFFINITY; BINDING SITE; BIRD; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CROSS REACTION; ENZYME LINKED IMMUNOSORBENT ASSAY; HEPATITIS E VIRUS; HUMAN; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; SWINE; VIRUS CELL INTERACTION; VIRUS IDENTIFICATION; WESTERN BLOTTING; ANIMAL; ANIMAL HEPATITIS; BLOOD; CHEMICAL STRUCTURE; CHEMISTRY; CHICKEN; GENETICS; HEPATITIS E; HEPEVIRUS; HOST RANGE; IMMUNOLOGY; MOLECULAR GENETICS; PIG; PROTEIN CONFORMATION; PROTEIN MOTIF; PROTEIN QUATERNARY STRUCTURE; RABBIT; RAT; RNA VIRUS INFECTION; SEQUENCE HOMOLOGY; VIROLOGY;

ANIMALIA; AVES; AVIAN HEPATITIS E VIRUS; CAMELIDAE; CERVIDAE; GALLUS GALLUS; HERPESTIDAE; MIRIDAE; MUSTELA; ORYCTOLAGUS CUNICULUS; RATTUS; SUIDAE;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, VIRAL; BIRDS; CAPSID PROTEINS; CHICKENS; CROSS REACTIONS; EPITOPES, B-LYMPHOCYTE; HEPATITIS ANTIGENS; HEPATITIS E; HEPATITIS E VIRUS; HEPATITIS, VIRAL, ANIMAL; HEPEVIRUS; HOST SPECIFICITY; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; PROTEIN STRUCTURE, QUATERNARY; RABBITS; RATS; RNA VIRUS INFECTIONS; SEQUENCE HOMOLOGY, AMINO ACID; SWINE;

EID: 84928530380     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00107-15     Document Type: Article

References (44)

1. Arankalle VA, Chadha MS, Tsarev SA, Emerson SU, Risbud AR, Banerjee K, Purcell RH. 1994. Seroepidemiology of water-borne hepatitis in India and evidence for a third enterically-transmitted hepatitis agent. Proc Natl Acad Sci U S A 91:3428-3432. http://dx.doi.org/10.1073/pnas.91.8.3428.
2. Tam AW, Smith MM, Guerra ME, Huang CC, Bradley DW, Fry KE, Reyes GR. 1991. Hepatitis E virus (HEV): molecular cloning and sequencing of the full-length viral genome. Virology 185:120-131. http://dx.doi.org/10.1016/0042-6822(91)90760-9.
3. Wang Y, Zhang H, Ling R, Li H, Harrison TJ. 2000. The complete sequence of hepatitis E virus genotype 4 reveals an alternative strategy for translation of open reading frames 2 and 3. J Gen Virol 81:1675-1686.
4. Amon JJ, Drobeniuc J, Bower WA, Magana JC, Escobedo MA, Williams IT, Bell BP, Armstrong GL. 2006. Locally acquired hepatitis E virus infection, El Paso, Texas. J Med Virol 78:741-746. http://dx.doi.org/10.1002/jmv.20617.
5. Erker JC, Desai SM, Schlauder GG, Dawson GJ, Mushahwar IK. 1999. A hepatitis E virus variant from the United States: molecular characterization and transmission in cynomolgus macaques. J Gen Virol 80:681-690.
6. Takahashi K, Kang JH, Ohnishi S, Hino K, Miyakawa H, Miyakawa Y, Maekubo H, Mishiro S. 2003. Full-length sequences of six hepatitis E virus isolates of genotypes III and IV from patients with sporadic acute or fulminant hepatitis in Japan. Intervirology 46:308-318. http://dx.doi.org/10.1159/000073210.
7. Emerson SU, Purcell RH. 2003. Hepatitis E virus. Rev Med Virol 13:145-154. http://dx.doi.org/10.1002/rmv.384.
8. Huang YW, Opriessnig T, Halbur PG, Meng XJ. 2007. Initiation at the third in-frameAUGcodon of open reading frame 3 of the hepatitis E virus is essential for viral infectivity in vivo. J Virol 81:3018-3026. http://dx.doi.org/10.1128/JVI.02259-06.
9. Graff J, Torian U, Nguyen H, Emerson SU. 2006. A bicistronic subgenomic mRNA encodes both the ORF2 and ORF3 proteins of hepatitis E virus. J Virol 80:5919-5926. http://dx.doi.org/10.1128/JVI.00046-06.
10. Meng XJ, Purcell RH, Halbur PG, Lehman JR, Webb DM, Tsareva TS, Haynes JS, Thacker BJ, Emerson SU. 1997. A novel virus in swine is closely related to the human hepatitis E virus. Proc Natl Acad Sci U S A 94:9860-9865. http://dx.doi.org/10.1073/pnas.94.18.9860.
11. Haqshenas G, Shivaprasad HL, Woolcock PR, Read DH, Meng XJ. 2001. Genetic identification and characterization of a novel virus related to human hepatitis E virus from chickens with hepatitis-splenomegaly syndrome in the United States. J Gen Virol 82:2449-2462.
12. Zhao Q, Zhou EM, Dong SW, Qiu HK, Zhang L, Hu SB, Zhao FF, Jiang SJ, Sun YN. 2010. Analysis of avian hepatitis E virus from chickens, China. Emerg Infect Dis 16:1469-1472. http://dx.doi.org/10.3201/eid1609.100626.
13. Zhao C, Ma Z, Harrison TJ, Feng R, Zhang C, Qiao Z, Fan J, Ma H, Li M, Song A, Wang Y. 2009. A novel genotype of hepatitis E virus prevalent among farmed rabbits in China. J Med Virol 81:1371-1379. http://dx.doi.org/10.1002/jmv.21536.
14. Takahashi K, Kitajima N, Abe N, Mishiro S. 2004. Complete or nearcomplete nucleotide sequences of hepatitis E virus genome recovered from a wild boar, a deer, and four patients who ate the deer. Virology 330:501-505. http://dx.doi.org/10.1016/j.virol.2004.10.006.
15. Nakamura M, Takahashi K, Taira K, Taira M, Ohno A, Sakugawa H, Arai M, Mishiro S. 2006. Hepatitis E virus infection in wild mongooses of Okinawa, Japan: demonstration of anti-HEV antibodies and a fullgenome nucleotide sequence. Hepatol Res 34:137-140. http://dx.doi.org/10.1016/j.hepres.2005.10.010.
16. Johne R, Heckel G, Plenge-Bonig A, Kindler E, Maresch C, Reetz J, Schielke A, Ulrich RG. 2010. Novel hepatitis E virus genotype in Norway rats, Germany. Emerg Infect Dis 16:1452-1455. http://dx.doi.org/10.3201/eid1609.100444.
17. Purcell RH, Engle RE, Rood MP, Kabrane-Lazizi Y, Nguyen HT, Govindarajan S, St Claire M, Emerson SU. 2011. Hepatitis E virus in rats, Los Angeles, California, USA. Emerg Infect Dis 17:2216-2222. http://dx.doi.org/10.3201/eid1712.110482.
18. Drexler JF, Seelen A, Corman VM, Fumie Tateno A, Cottontail V, Melim Zerbinati R, Gloza-Rausch F, Klose SM, Adu-Sarkodie Y, Oppong SK, Kalko EK, Osterman A, Rasche A, Adam A, Muller MA, Ulrich RG, Leroy EM, Lukashev AN, Drosten C. 2012. Bats worldwide carry hepatitis E virus-related viruses that form a putative novel genus within the family Hepeviridae. J Virol 86:9134-9147. http://dx.doi.org/10.1128/JVI.00800-12.
19. Raj VS, Smits SL, Pas SD, Provacia LB, Moorman-Roest H, Osterhaus AD, Haagmans BL. 2012. Novel hepatitis E virus in ferrets, the Netherlands. Emerg Infect Dis 18:1369-1370. http://dx.doi.org/10.3201/eid1808.111659.
20. Meng XJ. 2006. Hepatitis E as a zoonotic disease, p 611-623. In Thomas H, Zuckermann A, Lemon S (ed), Viral hepatitis, 3rd ed. Blackwell Publishing Ltd, Oxford, United Kingdom.
21. Hirano M, Ding X, Li TC, Takeda N, Kawabata H, Koizumi N, Kadosaka T, Goto I, Masuzawa T, Nakamura M, Taira K, Kuroki T, Tanikawa T, Watanabe H, Abe K. 2003. Evidence for widespread infection of hepatitis E virus among wild rats in Japan. Hepatol Res 27:1-5. http://dx.doi.org/10.1016/S1386-6346(03)00192-X.
22. Meng XJ. 2010. Hepatitis E virus: animal reservoirs and zoonotic risk. Vet Microbiol 140:256-265. http://dx.doi.org/10.1016/j.vetmic.2009.03.017.
23. Meng XJ. 2011. From barnyard to food table: the omnipresence of hepatitis E virus and risk for zoonotic infection and food safety. Virus Res 161:23-30. http://dx.doi.org/10.1016/j.virusres.2011.01.016.
24. Mizuo H, Yazaki Y, Sugawara K, Tsuda F, Takahashi M, Nishizawa T, Okamoto H. 2005. Possible risk factors for the transmission of hepatitis E virus and for the severe form of hepatitis E acquired locally in Hokkaido, Japan. J Med Virol 76:341-349. http://dx.doi.org/10.1002/jmv.20364.
25. Huang FF, Sun ZF, Emerson SU, Purcell RH, Shivaprasad HL, Pierson FW, Toth TE, Meng XJ. 2004. Determination and analysis of the complete genomic sequence of avian hepatitis E virus (avian HEV) and attempts to infect rhesus monkeys with avian HEV. J Gen Virol 85:1609-1618. http://dx.doi.org/10.1099/vir.0.79841-0.
26. Haqshenas G, Huang FF, Fenaux M, Guenette DK, Pierson FW, Larsen CT, Shivaprasad HL, Toth TE, Meng XJ. 2002. The putative capsid protein of the newly identified avian hepatitis E virus shares antigenic epitopes with that of swine and human hepatitis E viruses and chicken big liver and spleen disease virus. J Gen Virol 83:2201-2209.
27. Purdy MA, McCaustland KA, Krawczynski K, Spelbring J, Reyes GR, Bradley DW. 1993. Preliminary evidence that a trpE-HEV fusion protein protects cynomolgus macaques against challenge with wild-type hepatitis E virus (HEV). J Med Virol 41:90-94. http://dx.doi.org/10.1002/jmv.1890410118.
28. Tsarev SA, Tsareva TS, Emerson SU, Govindarajan S, Shapiro M, Gerin JL, Purcell RH. 1994. Successful passive and active immunization of cynomolgus monkeys against hepatitis E. Proc Natl Acad Sci U S A 91: 10198-10202. http://dx.doi.org/10.1073/pnas.91.21.10198.
29. Krawczynski K, Meng XJ, Rybczynska J. 2011. Pathogenetic elements of hepatitis E and animal models of HEV infection. Virus Res 161:78-83. http://dx.doi.org/10.1016/j.virusres.2011.03.007.
30. Guo H, Zhou EM, Sun ZF, Meng XJ, Halbur PG. 2006. Identification of B-cell epitopes in the capsid protein of avian hepatitis E virus (avian HEV) that are common to human and swine HEVs or unique to avian HEV. J Gen Virol 87:217-223. http://dx.doi.org/10.1099/vir.0.81393-0.
31. Zhao Q, Sun Y, Zhao J, Hu S, Zhao F, Chen F, Clavijo A, Zhou EM, Xiao Y. 2013. Development and application of an indirect ELISA for detection of antibodies against avian hepatitis E virus. J Virol Methods 187:32-36. http://dx.doi.org/10.1016/j.jviromet.2012.08.026.
32. Huang FF, Haqshenas G, Guenette DK, Halbur PG, Schommer SK, Pierson FW, Toth TE, Meng XJ. 2002. Detection by reverse transcription-PCR and genetic characterization of field isolates of swine hepatitis E virus from pigs in different geographic regions of the United States. J Clin Microbiol 40:1326-1332. http://dx.doi.org/10.1128/JCM.40.4.1326-1332.2002.
33. Zhang H, Jing S, Zhou EM, Sun P, Dong S, Li Y. 2009. Detection and characterization of human serum antibodies against avian hepatitis E virus. Chin J Health Lab Technol 19:1741-1744.
34. Wang XJ, Zhao Q, Jiang FL, Liu BY, Zhao JN, Dang L, Sun YN, Mu Y, Xiao SQ, Wang CB, Hsu WH, Liu L, Widen F, Zhou EM. 2014. Genetic characterization and serological prevalence of swine hepatitis E virus in Shandong Province, China. Vet Microbiol 172:415-424. http://dx.doi.org/10.1016/j.vetmic.2014.06.006.
35. Dong S, Zhao Q, Lu M, Sun P, Qiu H, Zhang L, Lv J, Zhou EM. 2011. Analysis of epitopes in the capsid protein of avian hepatitis E virus by using monoclonal antibodies. J Virol Methods 171:374-380. http://dx.doi.org/10.1016/j.jviromet.2010.11.025.
36. Zhao Q, Sun YN, Hu SB, Wang XJ, Xiao YH, Hsu WH, Xiao SQ, Wang CB, Mu Y, Hiscox JA, Zhou EM. 2013. Characterization of antigenic domains and epitopes in the ORF3 protein of a Chinese isolate of avian hepatitis E virus. Vet Microbiol 167:242-249. http://dx.doi.org/10.1016/j.vetmic.2013.08.006.
37. Sun EC, Ma JN, Liu NH, Yang T, Zhao J, Geng HW, Wang LF, Qin YL, Bu ZG, Yang YH, Lunt RA, Wang LF, Wu DL. 2011. Identification of two linear B-cell epitopes from West Nile virus NS1 by screening a phagedisplayed random peptide library. BMC Microbiol 11:160. http://dx.doi.org/10.1186/1471-2180-11-160.
38. Wang C, Zhao Q, Liang C, Dang L, Ma Y, Gao J, Li Q, Huang B, Kong N, Zhang C, Zhou EM. 2012. Complete genome sequence of a highly pathogenic porcine reproductive and respiratory syndrome virus variant. J Virol 86:8906. http://dx.doi.org/10.1128/JVI.01281-12.
39. Yamashita T, Mori Y, Miyazaki N, Cheng RH, Yoshimura M, Unno H, Shima R, Moriishi K, Tsukihara T, Li TC, Takeda N, Miyamura T, Matsuura Y. 2009. Biological and immunological characteristics of hepatitis E virus-like particles based on the crystal structure. Proc Natl Acad Sci U S A 106:12986-12991. http://dx.doi.org/10.1073/pnas.0903699106.
40. Troxler S, Marek A, Prokofieva I, Bilic I, Hess M. 2011. TaqMan real-time reverse transcription-PCR assay for universal detection and quantification of avian hepatitis E virus from clinical samples in the presence of a heterologous internal control RNA. J Clin Microbiol 49:1339-1346. http://dx.doi.org/10.1128/JCM.01626-10.
41. Guo H, Zhou EM, Sun ZF, Meng XJ. 2008. Immunodominant epitopes mapped by synthetic peptides on the capsid protein of avian hepatitis E virus are non-protective. Viral Immunol 21:61-67. http://dx.doi.org/10.1089/vim.2007.0082.
42. Smith DB, Simmonds P, International Committee on Taxonomy of Viruses Hepeviridae Study Group, Jameel S, Emerson SU, Harrison TJ, Meng XJ, Okamoto H, Van der Poel WH, Purdy MA. 2014. Consensus proposals for classification of the family Hepeviridae. J Gen Virol 95: 2223-2232. http://dx.doi.org/10.1099/vir.0.068429-0.
43. Meng XJ, Anderson DA, Arankalle VA, Emerson SU, Harrison TJ, Jameel S, Okamoto H. 2012. Hepeviridae, p 1021-1028. In King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (ed), Virus taxonomy: ninth report of the International Committee on Taxonomy of Viruses. Academic Press, London, United Kingdom.
44. Guo H, Zhou EM, Sun ZF, Meng XJ. 2007. Protection of chickens against avian hepatitis E virus (avian HEV) infection by immunization with recombinant avian HEV capsid protein. Vaccine 25:2892-2899. http://dx.doi.org/10.1016/j.vaccine.2006.09.038.