1887

Abstract

Hepatitis E virus (HEV) is an important human pathogen. In addition to humans, HEV has also been identified in pig, chicken, mongoose, deer, rat, rabbit and fish. There are four recognized and two putative genotypes of mammalian HEV. Genotypes 1 and 2 are restricted to humans, while genotypes 3 and 4 are zoonotic. The recently identified rabbit HEV is a distant member of genotype 3. Here, we first expressed and purified the recombinant capsid protein of rabbit HEV and showed that the capsid protein of rabbit HEV cross-reacted with antibodies raised against avian, rat, swine and human HEV. Conversely, we showed that antibodies against rabbit HEV cross-reacted with capsid proteins derived from chicken, rat, swine and human HEV. Since pigs are the natural host of genotype 3 HEV, we then determined if rabbit HEV infects pigs. Twenty pigs were divided into five groups of four each and intravenously inoculated with PBS, US rabbit HEV, Chinese rabbit HEV, US rat HEV and swine HEV, respectively. Results showed that only half of the pigs inoculated with rabbit HEV had low levels of viraemia and faecal virus shedding, indicative of active but not robust HEV infection. Infection of pigs by rabbit HEV was further verified by transmission of the virus recovered from pig faeces to naïve rabbits. Pigs inoculated with rat HEV showed no evidence of infection. Preliminary results suggest that rabbit HEV is antigenically related to other HEV strains and infects pigs and that rat HEV failed to infect pigs.

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2012-08-01
2021-10-17
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References

  1. Aggarwal R., Jameel S. 2011; Hepatitis E. Hepatology 54:2218–2226 [View Article][PubMed]
    [Google Scholar]
  2. Ahmad I., Holla R. P., Jameel S. 2011; Molecular virology of hepatitis E virus. Virus Res 161:47–58 [View Article][PubMed]
    [Google Scholar]
  3. Arankalle V. A., Chobe L. P., Chadha M. S. 2006; Type-IV Indian swine HEV infects rhesus monkeys. J Viral Hepat 13:742–745 [View Article][PubMed]
    [Google Scholar]
  4. Batts W., Yun S., Hedrick R., Winton J. 2011; A novel member of the family Hepeviridae from cutthroat trout (Oncorhynchus clarkii). Virus Res 158:116–123 [View Article][PubMed]
    [Google Scholar]
  5. Bilic I., Jaskulska B., Basic A., Morrow C. J., Hess M. 2009; Sequence analysis and comparison of avian hepatitis E viruses from Australia and Europe indicate the existence of different genotypes. J Gen Virol 90:863–873 [View Article][PubMed]
    [Google Scholar]
  6. Bouquet J., Tessé S., Lunazzi A., Eloit M., Rose N., Nicand E., Pavio N. 2011; Close similarity between sequences of hepatitis E virus recovered from humans and swine, France, 2008-2009. Emerg Infect Dis 17:2018–2025 [View Article][PubMed]
    [Google Scholar]
  7. Cooper K., Huang F. F., Batista L., Rayo C. D., Bezanilla J. C., Toth T. E., Meng X. J. 2005; Identification of genotype 3 hepatitis E virus (HEV) in serum and fecal samples from pigs in Thailand and Mexico, where genotype 1 and 2 HEV strains are prevalent in the respective human populations. J Clin Microbiol 43:1684–1688 [View Article][PubMed]
    [Google Scholar]
  8. Córdoba L., Huang Y. W., Opriessnig T., Harral K. K., Beach N. M., Finkielstein C. V., Emerson S. U., Meng X. J. 2011; Three amino acid mutations (F51L, T59A, and S390L) in the capsid protein of the hepatitis E virus collectively contribute to virus attenuation. J Virol 85:5338–5349 [View Article][PubMed]
    [Google Scholar]
  9. Cossaboom C. M., Córdoba L., Dryman B. A., Meng X. J. 2011; Hepatitis E virus in rabbits, Virginia, USA. Emerg Infect Dis 17:2047–2049 [View Article][PubMed]
    [Google Scholar]
  10. Emerson S. U., Purcell R. H. 2003; Hepatitis E virus. Rev Med Virol 13:145–154 [View Article][PubMed]
    [Google Scholar]
  11. Emerson S. U., Purcell R. H. 2007; Hepatitis E virus. In Fields Virology, 5th edn. Edited by Knipe D. M., Howley P. M. Philadelphia, PA: Lippincott Williams & Wilkins;
    [Google Scholar]
  12. Feagins A. R., Opriessnig T., Huang Y. W., Halbur P. G., Meng X. J. 2008; Cross-species infection of specific-pathogen-free pigs by a genotype 4 strain of human hepatitis E virus. J Med Virol 80:1379–1386 [View Article][PubMed]
    [Google Scholar]
  13. Geng J., Wang L., Wang X., Fu H., Bu Q., Zhu Y., Zhuang H. 2011; Study on prevalence and genotype of hepatitis E virus isolated from Rex rabbits in Beijing, China. J Viral Hepat 18:661–667 [View Article][PubMed]
    [Google Scholar]
  14. Hakze-van der Honing R. W., van Coillie E., Antonis A. F., van der Poel W. H. 2011; First isolation of hepatitis E virus genotype 4 in Europe through swine surveillance in the Netherlands and Belgium. PLoS ONE 6:e22673 [View Article][PubMed]
    [Google Scholar]
  15. Halbur P. G., Kasorndorkbua C., Gilbert C., Guenette D., Potters M. B., Purcell R. H., Emerson S. U., Toth T. E., Meng X. J. 2001; Comparative pathogenesis of infection of pigs with hepatitis E viruses recovered from a pig and a human. J Clin Microbiol 39:918–923 [View Article][PubMed]
    [Google Scholar]
  16. Haqshenas G., Shivaprasad H. L., Woolcock P. R., Read D. H., Meng X. J. 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[PubMed]
    [Google Scholar]
  17. 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. 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[PubMed]
    [Google Scholar]
  18. Huang F. F., Haqshenas G., Guenette D. K., Halbur P. G., Schommer S. K., Pierson F. W., Toth T. E., Meng X. J. 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 [View Article][PubMed]
    [Google Scholar]
  19. Huang Y. W., Opriessnig T., Halbur P. G., Meng X. J. 2007; 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 81:3018–3026 [View Article][PubMed]
    [Google Scholar]
  20. Johne R., Plenge-Bönig A., Hess M., Ulrich R. G., Reetz J., Schielke A. 2010; Detection of a novel hepatitis E-like virus in faeces of wild rats using a nested broad-spectrum RT-PCR. J Gen Virol 91:750–758 [View Article][PubMed]
    [Google Scholar]
  21. Kasorndorkbua C., Halbur P. G., Thomas P. J., Guenette D. K., Toth T. E., Meng X. J. 2002; Use of a swine bioassay and a RT-PCR assay to assess the risk of transmission of swine hepatitis E virus in pigs. J Virol Methods 101:71–78 [View Article][PubMed]
    [Google Scholar]
  22. Ma H., Zheng L., Liu Y., Zhao C., Harrison T. J., Ma Y., Sun S., Zhang J., Wang Y. 2010; Experimental infection of rabbits with rabbit and genotypes 1 and 4 hepatitis E viruses. PLoS ONE 5:e9160 [View Article][PubMed]
    [Google Scholar]
  23. Meng X. J. 2010a; Hepatitis E virus: animal reservoirs and zoonotic risk. Vet Microbiol 140:256–265 [View Article][PubMed]
    [Google Scholar]
  24. Meng X. J. 2010b; Recent advances in hepatitis E virus. J Viral Hepat 17:153–161 [View Article][PubMed]
    [Google Scholar]
  25. Meng X. J. 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 [View Article][PubMed]
    [Google Scholar]
  26. Meng X. J., Anderson D. A., Arankalle V. A., Emerson S. U., Harrison T. J., Jameel S., Okamoto H. 2012; Hepeviridae. In Virus Taxonomy, 9th Report of the International Committee on Taxonomy of Viruses pp. 1021–1028 Edited by King A. M. Q., Carstens E., Adams M., Lefkowitz E. London: Elsevier/Academic Press;
    [Google Scholar]
  27. 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. 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 [View Article][PubMed]
    [Google Scholar]
  28. Meng X. J., Halbur P. G., Haynes J. S., Tsareva T. S., Bruna J. D., Royer R. L., Purcell R. H., Emerson S. U. 1998a; Experimental infection of pigs with the newly identified swine hepatitis E virus (swine HEV), but not with human strains of HEV. Arch Virol 143:1405–1415 [View Article][PubMed]
    [Google Scholar]
  29. Meng X. J., Halbur P. G., Shapiro M. S., Govindarajan S., Bruna J. D., Mushahwar I. K., Purcell R. H., Emerson S. U. 1998b; Genetic and experimental evidence for cross-species infection by swine hepatitis E virus. J Virol 72:9714–9721[PubMed]
    [Google Scholar]
  30. 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 full-genome nucleotide sequence. Hepatol Res 34:137–140 [View Article][PubMed]
    [Google Scholar]
  31. Okamoto H. 2007; Genetic variability and evolution of hepatitis E virus. Virus Res 127:216–228 [View Article][PubMed]
    [Google Scholar]
  32. Okamoto H. 2011a; Efficient cell culture systems for hepatitis E virus strains in feces and circulating blood. Rev Med Virol 21:18–31 [View Article][PubMed]
    [Google Scholar]
  33. Okamoto H. 2011b; Hepatitis E virus cell culture models. Virus Res 161:65–77 [View Article][PubMed]
    [Google Scholar]
  34. Pavio N., Meng X. J., Renou C. 2010; Zoonotic hepatitis E: animal reservoirs and emerging risks. Vet Res 41:46 [View Article][PubMed]
    [Google Scholar]
  35. Pudupakam R. S., Huang Y. W., Opriessnig T., Halbur P. G., Pierson F. W., Meng X. J. 2009; 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 83:384–395 [View Article][PubMed]
    [Google Scholar]
  36. Purcell R. H., Engle R. E., Rood M. P., Kabrane-Lazizi Y., Nguyen H. T., Govindarajan S., St Claire M., Emerson S. U. 2011; Hepatitis E virus in rats, Los Angeles, California, USA. Emerg Infect Dis 17:2216–2222 [View Article][PubMed]
    [Google Scholar]
  37. Purdy M. A., Khudyakov Y. E. 2010; Evolutionary history and population dynamics of hepatitis E virus. PLoS ONE 5:e14376 [View Article][PubMed]
    [Google Scholar]
  38. Saad M. D., Hussein H. A., Bashandy M. M., Kamel H. H., Earhart K. C., Fryauff D. J., Younan M., Mohamed A. H. 2007; Hepatitis E virus infection in work horses in Egypt. Infect Genet Evol 7:368–373 [View Article][PubMed]
    [Google Scholar]
  39. Sanford B. J., Dryman B. A., Huang Y. W., Feagins A. R., Leroith T., Meng X. J. 2011; 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 159:17–22 [View Article][PubMed]
    [Google Scholar]
  40. Sato Y., Sato H., Naka K., Furuya S., Tsukiji H., Kitagawa K., Sonoda Y., Usui T., Sakamoto H.other authors 2011; A nationwide survey of hepatitis E virus (HEV) infection in wild boars in Japan: identification of boar HEV strains of genotypes 3 and 4 and unrecognized genotypes. Arch Virol 156:1345–1358 [View Article][PubMed]
    [Google Scholar]
  41. Shukla P., Nguyen H. T., Torian U., Engle R. E., Faulk K., Dalton H. R., Bendall R. P., Keane F. E., Purcell R. H., Emerson S. U. 2011; Cross-species infections of cultured cells by hepatitis E virus and discovery of an infectious virus-host recombinant. Proc Natl Acad Sci U S A 108:2438–2443 [View Article][PubMed]
    [Google Scholar]
  42. Sonoda H., Abe M., Sugimoto T., Sato Y., Bando M., Fukui E., Mizuo H., Takahashi M., Nishizawa T., Okamoto H. 2004; Prevalence of hepatitis E virus (HEV) infection in wild boars and deer and genetic identification of a genotype 3 HEV from a boar in Japan. J Clin Microbiol 42:5371–5374 [View Article][PubMed]
    [Google Scholar]
  43. Studier F. W. 2005; Protein production by auto-induction in high density shaking cultures. Protein Expr Purif 41:207–234 [View Article][PubMed]
    [Google Scholar]
  44. Surjit M., Jameel S., Lal S. K. 2004; The ORF2 protein of hepatitis E virus binds the 5′ region of viral RNA. J Virol 78:320–328 [View Article][PubMed]
    [Google Scholar]
  45. Takahashi K., Kitajima N., Abe N., Mishiro S. 2004; 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 330:501–505 [View Article][PubMed]
    [Google Scholar]
  46. Takahashi M., Nishizawa T., Sato H., Sato Y., Jirintai, Nagashima S., Okamoto H. 2011; Analysis of the full-length genome of a hepatitis E virus isolate obtained from a wild boar in Japan that is classifiable into a novel genotype. J Gen Virol 92:902–908 [View Article][PubMed]
    [Google Scholar]
  47. Tsarev S. A., Emerson S. U., Tsareva T. S., Yarbough P. O., Lewis M., Govindarajan S., Reyes G. R., Shapiro M., Purcell R. H. 1993; Variation in course of hepatitis E in experimentally infected cynomolgus monkeys. J Infect Dis 167:1302–1306 [View Article][PubMed]
    [Google Scholar]
  48. Tsarev S. A., Tsareva T. S., Emerson S. U., Yarbough P. O., Legters L. J., Moskal T., Purcell R. H. 1994; Infectivity titration of a prototype strain of hepatitis E virus in cynomolgus monkeys. J Med Virol 43:135–142 [View Article][PubMed]
    [Google Scholar]
  49. Wang Y., Zhang H., Ling R., Li H., Harrison T. J. 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[PubMed]
    [Google Scholar]
  50. Yazaki Y., Mizuo H., Takahashi M., Nishizawa T., Sasaki N., Gotanda Y., Okamoto H. 2003; Sporadic acute or fulminant hepatitis E in Hokkaido, Japan, may be food-borne, as suggested by the presence of hepatitis E virus in pig liver as food. J Gen Virol 84:2351–2357 [View Article][PubMed]
    [Google Scholar]
  51. Zafrullah M., Ozdener M. H., Panda S. K., Jameel S. 1997; The ORF3 protein of hepatitis E virus is a phosphoprotein that associates with the cytoskeleton. J Virol 71:9045–9053[PubMed]
    [Google Scholar]
  52. Zhao C., Ma Z., Harrison T. J., Feng R., Zhang C., Qiao Z., Fan J., Ma H., Li M.other authors 2009; A novel genotype of hepatitis E virus prevalent among farmed rabbits in China. J Med Virol 81:1371–1379 [View Article][PubMed]
    [Google Scholar]
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