Construction of an infectious cDNA clone of avian hepatitis E virus (avian HEV) recovered from a clinically healthy chicken in the United States and characterization of its pathogenicity in specific-pathogen-free chickens

Veterinary Microbiology

Volumn 147, Issue 3-4, 2011, Pages 310-319

  Kwon, Hyuk Moo ^a,b   LeRoith, Tanya ^a   Pudupakam, R S ^a   Pierson, F William ^a   Huang, Yao Wei ^a   Dryman, Barbara A ^a   Meng, Xiang Jin ^a  

^a CENTER FOR MOLECULAR MEDICINE AND INFECTIOUS DISEASES   (United States)

^b Kangwon National University   (South Korea)

Author keywords

Avian hepatitis E virus; Avian HEV; Infectious clone

Indexed keywords

VIRUS RNA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CHICKEN; CONTROLLED STUDY; HEPATITIS E; HEPATITIS E VIRUS; HEPATOMEGALY; INOCULATION; LIVER CELL; LIVER WEIGHT; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENICITY; RNA TRANSCRIPTION; SEROCONVERSION; UNITED STATES; VIREMIA; VIRUS INFECTIVITY; VIRUS SHEDDING; VIRUS STRAIN;

ANIMALS; CELLS, CULTURED; CHICKENS; CLONING, MOLECULAR; DNA, COMPLEMENTARY; HEPATITIS E; HEPATITIS, VIRAL, ANIMAL; HEPEVIRUS; LIVER; POULTRY DISEASES; RNA CAPS; SPECIFIC PATHOGEN-FREE ORGANISMS; VIRGINIA; VIRUS SHEDDING;

ANIMALIA; AVES; AVIAN HEPATITIS E VIRUS; GALLUS GALLUS;

EID: 78650572593     PISSN: 03781135     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vetmic.2010.07.016     Document Type: Article

References (48)

1. Agunos A.C., Yoo D., Youssef S.A., Ran D., Binnington B., Hunter D.B. Avian hepatitis E virus in an outbreak of Hepatitis-Splenomegaly syndrome and fatty liver haemorrhage syndrome in two flaxseed-fed layer flocks in Ontario. Avian Pathol. 2006, 35:404-412.
2. Arankalle V.A., Chadha M.S., Tsarev S.A., Emerson S.U., Risbud A.R., Banerjee K., Purcell R.H. Seroepidemiology of water-borne hepatitis in India and evidence for a third enterically-transmitted hepatitis agent. Proc. Natl. Acad. Sci. U.S.A. 1994, 91:3428-3432.
3. Arankalle V.A., Chobe L.P., Chadha M.S. Type-IV Indian swine HEV infects rhesus monkeys. J. Viral Hepat. 2006, 13:742-745.
4. Billam P., Huang F.F., Sun Z.F., Pierson F.W., Duncan R.B., Elvinger F., Guenette D.K., Toth T.E., Meng X.J. Systematic pathogenesis and replication of avian hepatitis E virus in specific-pathogen-free adult chickens. J. Virol. 2005, 79:3429-3437.
5. Billam P., Sun Z.F., Meng X.J. Analysis of the complete genomic sequence of an apparently avirulent strain of avian hepatitis E virus (avian HEV) identified major genetic differences compared with the prototype pathogenic strain of avian HEV. J. Gen. Virol. 2007, 88:1538-1544.
6. Billam P., LeRoith T., Pudupakam R.S., Pierson F.W., Duncan R.B., Meng X.J. Comparative pathogenesis in specific-pathogen-free chickens of two strains of avian hepatitis E virus recovered from a chicken with Hepatitis-Splenomegaly syndrome and from a clinically healthy chicken. Vet. Microbiol. 2009, 139:253-261.
7. Bilic I., Jaskulska B., Basic A., Morrow C.J., Hess M. Sequence analysis and comparison of avian hepatitis E viruses from Australia and Europe indicate the existence of different genotypes. J. Gen. Virol. 2009, 90:863-873.
8. Chandra V., Taneja S., Kalia M., Jameel S. Molecular biology and pathogenesis of hepatitis E virus. J. Biosci. 2008, 33:451-464.
9. Chandra V., Kar-Roy A., Kumari S., Mayor S., Jameel S. The hepatitis E virus ORF3 protein modulates epidermal growth factor receptor trafficking, STAT3 translocation, and the acute-phase response. J. Virol. 2008, 82:7100-7110.
10. 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, 84:3857-3867.
11. Emerson S.U., Purcell R.H. Hepatitis E virus. Rev. Med. Virol. 2003, 13:145-154.
12. Emerson, S.U., Anderson, D., Arankalle, A., Meng, X.J., Purdy, M., Schlauder, G.G., Tsarev, S.A., 2004. Hepevirus. In: Fauquet, C.M., Mayo, M.A., Maniloff, J., Desselberger, U., Ball, L.A. (Eds.), Virus Taxonomy. Eighth Report of the International Committee on Taxonomy of Viruses. Elsevier/Academic Press, London, pp. 853-857.
13. Emerson S.U., Zhang M., Meng X.J., Nguyen H., St Claire M., Govindarajan S., Huang Y.K., Purcell R.H. Recombinant hepatitis E virus genomes infectious for primates: importance of capping and discovery of a cis-reactive element. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:15270-15275.
14. Feagins A.R., Opriessnig T., Huang Y.W., Halbur P.G., Meng X.J. Cross-species infection of specific-pathogen-free pigs by a genotype 4 strain of human hepatitis E virus. J. Med. Virol. 2008, 80:1379-1386.
15. Graff J., Nguyen H., Yu C., Elkins W.R., St Claire M., Purcell R.H., Emerson S.U. The open reading frame 3 gene of hepatitis E virus contains a cis-reactive element and encodes a protein required for infection of macaques. J. Virol. 2005, 79:6680-6689.
16. Graff J., Torian U., Nguyen H., Emerson S.U. A bicistronic subgenomic mRNA encodes both the ORF2 and ORF3 proteins of hepatitis E virus. J. Virol. 2006, 80:5919-5926.
17. Graff J., Zhou Y.H., Torian U., Nguyen H., St Claire M., Yu C., Purcell R.H., Emerson S.U. Mutations within potential glycosylation sites in the capsid protein of hepatitis E virus prevent the formation of infectious virus particles. J. Virol. 2008, 82:1185-1194.
18. Guo H., Zho E.M., Sun Z.F., Meng X.J., Halbur P.G. 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. 2006, 87:217-223.
19. Halbur P.G., Kasorndorkbua C., Gilbert C., Guenette D., Potters M.B., Purcell R.H., Emerson S.U., Toth T.E., Meng X.J. Comparative pathogenesis of infection of pigs with hepatitis E viruses recovered from a pig and a human. J. Clin. Microbiol. 2001, 39:918-923.
20. Haqshenas G., Shivaprasad H.L., Woolcock P.R., Read D.H., Meng X.J. 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. 2001, 82:2449-2462.
21. Haqshenas G., Huang F.F., Fenaux M., Guenette D.K., Pierson F.W., Larsen C.T., Shivaprasad H.L., Toth T.E., Meng X.J. 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. 2002, 83:2201-2209.
22. Huang F.F., Haqshenas G., Shivaprasad H.L., Guenette D.K., Woolcock P.R., Larsen C.T., Pierson F.W., Elvinger F., Toth T.E., Meng X.J. Heterogeneity and seroprevalence of a newly identified avian hepatitis e virus from chickens in the United States. J. Clin. Microbiol. 2002, 40:4197-4202.
23. Huang F.F., Sun Z.F., Emerson S.U., Purcell R.H., Shivaprasad H.L., Pierson F.W., Toth T.E., Meng X.J. 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. 2004, 85:1609-1618.
24. Huang F.F., Pierson F.W., Toth T.E., Meng X.J. Construction and characterization of infectious cDNA clones of a chicken strain of hepatitis E virus (HEV), avian HEV. J. Gen. Virol. 2005, 86:2585-2593.
25. Huang Y.W., Haqshenas G., Kasorndorkbua C., Halbur P.G., Emerson S.U., Meng X.J. Capped RNA transcripts of full-length cDNA clones of swine hepatitis E virus are replication competent when transfected into Huh7 cells and infectious when intrahepatically inoculated into pigs. J. Virol. 2005, 79:1552-1558.
26. Huang Y.W., Opriessnig T., Halbur P.G., Meng X.J. Initiation at the third in-frame AUG codon of open reading frame 3 of the hepatitis E virus is essential for viral infectivity in vivo. J. Virol. 2007, 81:3018-3026.
27. Johne R., Plenge-Bönig A., Hess M., Ulrich R.G., Reetz J., Schielke A. Detection of a novel hepatitis E-like virus in faeces of wild rats using a nested broad-spectrum RT-PCR. J. Gen. Virol. 2010, 91:750-758.
28. Kalia M., Chandra V., Rahman S.A., Sehgal D., Jameel S. Heparan sulfate proteoglycans are required for cellular binding of the hepatitis E virus ORF2 capsid protein and for viral infection. J. Virol. 2009, 83:12714-12724.
29. Marek, A., Bilic, I., Prokofieva, I., Hess, M., 2010. Phylogenetic analysis of avian hepatitis E virus samples from European and Australian chicken flocks supports the existence of a different genus within the Hepeviridae comprising at least three different genotypes. Vet. Microbiol. (Epub ahead of print).
30. Meng X.J., Purcell R.H., Halbur P.G., Lehman J.R., Webb D.M., Tsareva T.S., Haynes J.S., Thacker B.J., Emerson S.U. A novel virus in swine is closely related to the human hepatitis E virus. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:9860-9865.
31. Meng X.J., Halbur P.G., Shapiro M.S., Govindarajan S., Bruna J.D., Mushahwar I.K., Purcell R.H., Emerson S.U. Genetic and experimental evidence for cross-species infection by swine hepatitis E virus. J. Virol. 1998, 72:9714-9721.
32. Meng X.J. Hepatitis E virus: animal reservoirs and zoonotic risk. Vet. Microbiol. 2010, 140:256-265.
33. Meng X.J. Recent advances in hepatitis E virus. J. Viral Hepatitis 2010, 17:153-161.
34. Morrow C.J., Samu G., Mátrai E., Klausz A., Wood A.M., Richter S., Jaskulska B., Hess M. Avian hepatitis E virus infection and possible associated clinical disease in broiler breeder flocks in Hungary. Avian Pathol. 2008, 37:527-535.
35. Nishizawa T., Takahashi M., Mizuo H., Miyajima H., Gotanda Y., Okamoto H. Characterization of Japanese swine and human hepatitis E virus isolates of genotype IV with 99% identity over the entire genome. J. Gen. Virol. 2003, 84:1245-1251.
36. Okamoto H. Genetic variability and evolution of hepatitis E virus. Virus Res. 2007, 127:216-228.
37. Panda S.K., Ansari I.H., Durgapal H., Agrawal S., Jameel S. The in vitro-synthesized RNA from a cDNA clone of hepatitis E virus is infectious. J. Virol. 2000, 74:2430-2437.
38. Payne C.J., Ellis T.M., Plant S.L., Gregory A.R., Wilcox G.E. Sequence data suggests big liver and spleen disease virus (BLSV) is genetically related to hepatitis E virus. Vet. Microbiol. 1999, 68:119-125.
39. Pudupakam R.S., Huang Y.W., Opriessnig T., Halbur P.G., Pierson F.W., Meng X.J. Deletions of the hypervariable region (HVR) in open reading frame 1 of hepatitis E virus do not abolish virus infectivity: evidence for attenuation of HVR deletion mutants in vivo. J. Virol. 2009, 83:384-395.
40. Riddell M.A., Li F., Anderson D.A. Identification of immunodominant and conformational epitopes in the capsid protein of hepatitis E virus by using monoclonal antibodies. J. Virol. 2000, 74:8011-8017.
41. Sun Z.F., Larsen C.T., Dunlop A., Huang F.F., Pierson F.W., Toth T.E., Meng X.J. Genetic identification of avian hepatitis E virus (HEV) from healthy chicken flocks and characterization of the capsid gene of 14 avian HEV isolates from chickens with Hepatitis-Splenomegaly syndrome in different geographical regions of the United States. J. Gen. Virol. 2004, 85:693-700.
42. Takahashi K., Kitajima N., Abe N., Mishiro S. Complete or near-complete nucleotide sequences of hepatitis E virus genome recovered from a wild boar, a deer, and four patients who ate the deer. Virology 2004, 330:501-505.
43. Tei S., Kitajima N., Takahashi K., Mishiro S. Zoonotic transmission of hepatitis E virus from deer to human beings. Lancet 2003, 362:371-373.
44. Wang Y., Ling R., Erker J.C., Zhang H., Li H., Desai S., Mushahwar I.K., Harrison T.J. A divergent genotype of hepatitis E virus in Chinese patients with acute hepatitis. J. Gen. Virol. 1999, 80:169-177.
45. Wang Y., Zhang H., Ling R., Li H., Harrison T.J. 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. 2000, 81:1675-1686.
46. Wang Y., Levine D.F., Bendall R.P., Teo C.G., Harrison T.J. Partial sequence analysis of indigenous hepatitis E virus isolated in the United Kingdom. J. Med. Virol. 2001, 65:706-709.
47. Yamada K., Takahashi M., Hoshino Y., Takahashi H., Ichiyama K., Tanaka T., Okamoto H. Construction of an infectious cDNA clone of hepatitis E virus strain JE03-1760F that can propagate efficiently in cultured cells. J. Gen. Virol. 2009, 90:457-462.
48. Yamada K., Takahashi M., Hoshino Y., Takahashi H., Ichiyama K., Nagashima S., Tanaka T., Okamoto H. ORF3 protein of hepatitis E virus is essential for virion release from infected cells. J. Gen. Virol. 2009, 90:1880-1891.