1887

Abstract

We recently identified a novel virus, designated avian hepatitis E virus (avian HEV), from chickens with hepatitis–splenomegaly (HS) syndrome in the USA. We showed that avian HEV is genetically related to swine and human HEVs. Here we report the antigenic cross-reactivity of the putative open reading frame 2 (ORF2) capsid protein of avian HEV with those of swine and human HEVs and the Australian chicken big liver and spleen disease virus (BLSV). The region encoding the C-terminal 268 amino acid residues of avian HEV ORF2 was cloned into expression vector pRSET-C. The truncated ORF2 protein was expressed in as a fusion protein and purified by affinity chromatography. Western blot analysis revealed that the avian HEV ORF2 protein reacted with antisera against the Sar-55 strain of human HEV and with convalescent antisera against swine HEV and the US2 strain of human HEV, as well as with antiserum against BLSV. Convalescent sera from specific-pathogen-free chickens experimentally infected with avian HEV also reacted with the recombinant capsid proteins of swine HEV and Sar-55 human HEV. Antisera against the US2 human HEV also reacted with recombinant ORF2 proteins of both swine HEV and Sar-55 human HEV. The antigenic cross-reactivity of the avian HEV putative capsid protein with those of swine and human HEVs was further confirmed, for the most part, by ELISA assays. The data indicate that avian HEV shares certain antigenic epitopes in its putative capsid protein with swine and human HEVs, as well as with BLSV. The results have implications for HEV diagnosis and taxonomy.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-83-9-2201
2002-09-01
2019-10-21
Loading full text...

Full text loading...

/deliver/fulltext/jgv/83/9/0832201a.html?itemId=/content/journal/jgv/10.1099/0022-1317-83-9-2201&mimeType=html&fmt=ahah

References

  1. Anderson, D. A., Li, F., Riddell, M., Howard, T., Seow, H. F., Torresi, J., Perry, G., Sumarsidi, D., Shrestha, S. M. & Shrestha, I. L. ( 1999; ). ELISA for IgG-class antibody to hepatitis E virus based on a highly conserved, conformational epitope expressed in Escherichia coli. Journal of Virological Methods 81, 131-142.[CrossRef]
    [Google Scholar]
  2. Arankalle, V. A., Chadha, M. S., Tsarev, S. A., Emerson, S. U., Risbud, A. R., Banerjee, K. & Purcell, R. H. ( 1994; ). Seroepidemiology of water-borne hepatitis in India and evidence for a third enterically-transmitted hepatitis agent. Proceedings of the National Academy of Sciences, USA 91, 3428-3432.[CrossRef]
    [Google Scholar]
  3. Arankalle, V. A., Tsarev, S. A., Chadha, M. S., Alling, D. W., Emerson, S. U., Banerjee, K. & Purcell, R. H. ( 1995; ). Age-specific prevalence of antibodies to hepatitis A and E viruses in Pune, India, 1982 and 1992. Journal of Infectious Diseases 171, 447-450.[CrossRef]
    [Google Scholar]
  4. Arankalle, V. A., Paranjape, S., Emerson, S. U., Purcell, R. H. & Walimbe, A. M. ( 1999; ). Phylogenetic analysis of hepatitis E virus isolates from India (1976–1993). Journal of General Virology 80, 1691-1700.
    [Google Scholar]
  5. Chandler, J. D., Riddell, M. A., Li, F., Love, R. J. & Anderson, D. A. ( 1999; ). Serological evidence for swine hepatitis E virus infection in Australian pig herds. Veterinary Microbiology 68, 95-105.[CrossRef]
    [Google Scholar]
  6. Emerson, S. U., Zhang, M., Meng, X. J., Nguyen, H., Huang, Y. & Purcell, R. H. ( 2001; ). Recombinant hepatitis E virus genomes infectious for primates: importance of capping and discovery of a cis-reactive element. Proceedings of the National Academy of Sciences, USA 98, 15270-15275.[CrossRef]
    [Google Scholar]
  7. Erker, J. C., Desai, S. M., Schlauder, G. G., Dawson, G. J. & Mushahwar, I. K. ( 1999; ). A hepatitis E virus variant from the United States: molecular characterization and transmission in cynomolgus macaques. Journal of General Virology 80, 681-690.
    [Google Scholar]
  8. Garkavenko, O., Obriadina, A., Meng, J., Anderson, D. A., Benard, H. J., Schroeder, B. A., Khudyakov, Y. E., Fields, H. A. & Croxson, M. C. ( 2001; ). Detection and characterization of swine hepatitis E virus in New Zealand. Journal of Medical Virology 65, 525-529.[CrossRef]
    [Google Scholar]
  9. 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. Journal of Clinical Microbiology 39, 918-923.[CrossRef]
    [Google Scholar]
  10. Haqshenas, G. & Meng, X. J. ( 2001; ). Determination of the nucleotide sequences at the extreme 5′ and 3′ ends of swine hepatitis E virus genome. Archives of Virology 146, 2461-2467.[CrossRef]
    [Google Scholar]
  11. 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. Journal of General Virology 82, 2449-2462.
    [Google Scholar]
  12. Hsieh, S. Y., Meng, X. J., Wu, Y. H., Liu, S. T., Tam, A. W., Lin, D. Y. & Liaw, Y. F. ( 1999; ). Identity of a novel swine hepatitis E virus in Taiwan forming a monophyletic group with Taiwan isolates of human hepatitis E virus. Journal of Clinical Microbiology 37, 3828-3834.
    [Google Scholar]
  13. Huang, F. F., Haqshenas, G., Guenette, D. K., Halbur, P. G., Schommer, S., Pierson, F. W., Toth, T. E. & Meng, X. J. ( 2002; ). Detection by RT-PCR and genetic characterization of field isolates of swine hepatitis E virus from pigs in different geographic regions of the U. S. Journal of Clinical Microbiology 40, 1326–1332.[CrossRef]
    [Google Scholar]
  14. Hussaini, S. H., Skidmore, S. J., Richardson, P., Sherratt, L. M., Cooper, B. T. & O′Grady, J. G. ( 1997; ). Severe hepatitis E infection during pregnancy. Journal of Viral Hepatitis 4, 51-54.
    [Google Scholar]
  15. Im, S. W., Zhang, J. Z., Zhuang , H., Che, X. Y., Zhu, W. F., Xu, G. M., Li, K., Xia, N. S. & Ng, M. H. ( 2001; ). A bacterially expressed peptide prevents experimental infection of primates by the hepatitis E virus. Vaccine 19, 3726-3732.[CrossRef]
    [Google Scholar]
  16. Julian, R. J. (1995). Hepatitis–liver hemorrhage syndrome in laying hens. In Proceedings of 67th North East Conference of Avian Diseases, p. 17. Mystic, CT, USA.
  17. Kasorndorkbua, C., Halbur, P. G., 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. Journal of Virological Methods 101, 71-78.[CrossRef]
    [Google Scholar]
  18. Kyte, J. & Doolittle, R. F. ( 1982; ). A simple method for displaying the hydropathic character of a protein. Journal of Molecular Biology 157, 105-132.[CrossRef]
    [Google Scholar]
  19. Li, F., Torresi, J., Locarnini, S. A., Zhuang, H., Zhu, W., Guo, X. & Anderson, D. A. ( 1997; ). 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. Journal of Medical Virology 52, 289-230.[CrossRef]
    [Google Scholar]
  20. Li, T. C., Yamakawa, Y., Suzuki, K., Tatsumi, M., Razak, M. A., Uchida, T., Takeda, N. & Miyamura, T. ( 1997; ). Expression and self-assembly of empty virus-like particles of hepatitis E virus. Journal of Virology 71, 7207-7213.
    [Google Scholar]
  21. McCrudden, R., O′Connell, S., Farrant, T., Beaton, S., Iredale, J. P. & Fine, D. ( 2000; ). Sporadic acute hepatitis E in the United Kingdom: an underdiagnosed phenomenon? Gut 46, 732–733.[CrossRef]
    [Google Scholar]
  22. Mast, E. E., Kuramoto, I. K., Favorov, M. O., Schoening, V. R., Burkholder, B. T., Shapiro, C. N. & Holland, P. V. ( 1997; ). Prevalence of and risk factors for antibody to hepatitis E virus seroreactivity among blood donors in Northern California. Journal of Infectious Diseases 176, 34-40.[CrossRef]
    [Google Scholar]
  23. Meng, X. J. ( 2000a; ). Novel strains of hepatitis E virus identified from humans and other animal species: is hepatitis E a zoonosis? Journal of Hepatology 33, 842-845.[CrossRef]
    [Google Scholar]
  24. Meng, X. J. ( 2000b; ). Zoonotic and xenozoonotic risks of hepatitis E virus. Infectious Disease Reviews 2, 35-41.
    [Google Scholar]
  25. Meng, X. J. (2002). Swine hepatitis E virus: cross-species infection and risk in xenotransplantation. Current Topics in Microbiology and Immunology (in press).
  26. 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. Proceedings of the National Academy of Sciences, USA 94, 9860-9865.[CrossRef]
    [Google Scholar]
  27. Meng, X. J., Halbur, P. G., Haynes, J. S., Tsareva, T. S., Bruna, J. D., Royer, R., 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. Archives of Virology 143, 1405-1415.[CrossRef]
    [Google Scholar]
  28. 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 the swine hepatitis E virus. Journal of Virology 72, 9714-9721.
    [Google Scholar]
  29. Meng, X. J., Dea, S., Engle, R. E., Friendship, R., Lyoo, Y. S., Sirinarumitr, T., Urairong, K., Wang, D., Wong, D., Yoo, D., Zhang, Y., Purcell, R. H. & Emerson, S. U. ( 1999; ). Prevalence of antibodies to the hepatitis E virus in pigs from countries where hepatitis E is common or is rare in the human population. Journal of Medical Virology 58, 297-302.
    [Google Scholar]
  30. Meng, X. J., Wiseman, B., Elvinger, F., Guenette, D. K., Toth, T. E., Engle, R., Emerson, S. U. & Purcell, R. H. ( 2002; ). Prevalence of antibodies to hepatitis E virus in veterinarians working with swine and in normal blood donors in the United States and other countries. Journal of Clinical Microbiology 40, 117-122.[CrossRef]
    [Google Scholar]
  31. Payne, C. J., Ellis, T. M., Plant, S. L., Gregory, A. R. & Wilcox, G. E. ( 1999; ). Sequence data suggests big liver and spleen disease virus (BLSV) is genetically related to hepatitis E virus. Veterinary Microbiology 68, 119-125.[CrossRef]
    [Google Scholar]
  32. Pina, S., Buti, M., Cotrina, M., Piella, J. & Girones, R. ( 2000; ). HEV identified in serum from humans with acute hepatitis and in sewage of animal origin in Spain. Journal of Hepatology 33, 826-833.[CrossRef]
    [Google Scholar]
  33. Purcell, R. H. ( 1996; ). Hepatitis E virus. In Fields Virology , pp. 2831-2843. Edited by B. N. Fields, D. M. Knipe & P. M. Howley. Philadelphia: Lippincott–Raven.
  34. Reyes, G. R. ( 1997; ). Overview of the epidemiology and biology of the hepatitis E virus. In Viral Hepatitis , pp. 239-258. Edited by R. A. Willson. New York: Marcel Dekker.
  35. Riddell, C. ( 1997; ). Hepatitis–splenomegaly syndrome. In Disease of Poultry , pp. 1041. Edited by B. W. Calnek, H. J. Barnes, C. W. Beard, L. R. McDougald & Y. M. Saif. Ames, IA: Iowa State University Press.
  36. Riddell, M. A., Li, F. & Anderson, D. A. ( 2000; ). Identification of immunodominant and conformational epitopes in the capsid protein of hepatitis E virus by using monoclonal antibodies. Journal of Virology 74, 8011-8017.[CrossRef]
    [Google Scholar]
  37. Ritchie, S. J. & Riddell, C. ( 1991; ). ‘‘Hepatitis–splenomegaly’’ syndrome in commercial egg laying hens. Canadian Veterinary Journal 32, 500-501.
    [Google Scholar]
  38. Robinson, R. A., Burgess, W. H., Emerson, S. U., Leibowitz, R. S., Sosnovtseva, S. A., Tsarev, S. & Purcell, R. H. ( 1998; ). Structural characterization of recombinant hepatitis E virus ORF2 proteins in baculovirus-infected insect cells. Protein Expression and Purification 12, 75-84.[CrossRef]
    [Google Scholar]
  39. Schlauder, G. G. & Mushahwar, I. K. ( 2001; ). Genetic heterogeneity of hepatitis E virus. Journal of Medical Virology 65, 282-292.[CrossRef]
    [Google Scholar]
  40. Schlauder, G. G., Dawson, G., Erker, J., Kwo, P., Knigge, M., Smalley, D., Rosenblatt, J., Desai, S. & Mushahwar, I. K. ( 1998; ). The sequence and phylogenetic analysis of a novel hepatitis E virus isolated from a patient with acute hepatitis reported in the United States. Journal of General Virology 79, 447-456.
    [Google Scholar]
  41. Schlauder, G. G., Desai, S. M., Zanetti, A. R., Tassopoulos, N. C. & Mushahwar, I. K. ( 1999; ). Novel hepatitis E virus (HEV) isolates from Europe: evidence for additional genotypes of HEV. Journal of Medical Virology 57, 243-251.[CrossRef]
    [Google Scholar]
  42. Schofield, D. J., Glamann, J., Emerson, S. U. & Purcell, R. H. ( 2000; ). Identification by phage display and characterization of two neutralizing chimpanzee monoclonal antibodies to the hepatitis E virus capsid protein. Journal of Virology 74, 5548-5555.[CrossRef]
    [Google Scholar]
  43. Shivaprasad, H. L. & Woolcock, P. R. (1995). Necrohemorrhagic hepatitis in broiler breeders. In Proceedings of Western Poultry Diseases Conference, p. 6. Sacramento, CA, USA.
  44. Tablante, N. L. & Vaillancourt, J. P. (1994). Hepatitis–liver hemorrhage syndrome in commercial laying hens: a survey of Ontario egg producers. In Proceedings of American Avian Practitioners Meeting, p. 132. San Francisco, CA, USA.
  45. Tablante, N. L., Vaillancourt, J. P. & Julian, R. J. ( 1994; ). Necrotic, haemorrhagic, hepatomegalic hepatitis associated with vasculitis and amyloidosis in commercial laying hens. Avian Pathology 23, 725-732.[CrossRef]
    [Google Scholar]
  46. Takahashi, K., Iwata, K., Watanabe, N., Hatahara, T., Ohta, Y., Baba, K. & Mishiro, S. ( 2001; ). Full-genome nucleotide sequence of a hepatitis E virus strain that may be indigenous to Japan. Virology 287, 9-12.[CrossRef]
    [Google Scholar]
  47. Thomas, D. L., Yarbough, P. O., Vlahov, D., Tsarev, S. A., Nelson, K. E., Saah, A. J. & Purcell, R. H. ( 1997; ). Seroreactivity to hepatitis E virus in areas where the disease is not endemic. Journal of Clinical Microbiology 35, 1244-1247.
    [Google Scholar]
  48. Tien, N. T., Clayson, H. T., Khiem, H. B., Sac, P. K., Corwin, A. L., Myint, K. S. & Vaughn, D. W. ( 1997; ). Detection of immunoglobulin G to the hepatitis E virus among several animal species in Vietnam. American Journal of Tropical Medicine and Hygiene 57, 211 (abstract).
    [Google Scholar]
  49. Tsarev, S. A., Tsareva, T. S., Emerson, S. U., Kapikian, A. Z., Ticehurst, J., London, W. & Purcell, R. H. ( 1993; ). 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. Journal of Infectious Diseases 168, 369-378.[CrossRef]
    [Google Scholar]
  50. Van Cuyck-Gandre, H., Zhang, H. Y., Tsarev, S. A., Clements, N. J., Cohen, S. J., Caudill, J. D., Buisson, Y., Coursaget, P., Warren, R. L. & Longer, C. F. ( 1997; ). Characterization of hepatitis E virus (HEV) from Algeria and Chad by partial genome sequence. Journal of Medical Virology 53, 340-347.[CrossRef]
    [Google Scholar]
  51. van der Poel, W., Verschoor, F., van der Heide, R., Herrera, M.-I., Vivo, A., Kooreman, M. & de Roda Husman, A. ( 2001; ). Hepatitis E virus sequences in swine related to sequences in humans, the Netherlands. Emerging Infectious Diseases 7, 970-976.[CrossRef]
    [Google Scholar]
  52. Wang, Y., Ling, R., Erker, J., Zhang, H., Li, H., Desai, S., Mushahwar, I. & Harrison, T. J. ( 1999; ). A divergent genotype of hepatitis E virus in Chinese patients with acute hepatitis. Journal of General Virology 80, 169-177.
    [Google Scholar]
  53. 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. Journal of General Virology 81, 1675-1686.
    [Google Scholar]
  54. Welling, G. W., Weijer, W. J., van der Zee, R. & Welling-Wester, S. ( 1985; ). Prediction of sequential antigenic regions in proteins. FEBS Letters 188, 215-218.[CrossRef]
    [Google Scholar]
  55. Williams, T. P., Kasorndorkbua, C., Halbur, P. G., Haqshenas, G., Guenette, D. K., Toth, T. E. & Meng, X. J. ( 2001; ). Evidence of extrahepatic sites of replication of the hepatitis E virus in a swine model. Journal of Clinical Microbiology 39, 3040-3046.[CrossRef]
    [Google Scholar]
  56. Wu, J. C., Chen, C., Chiang, T., Tsai, W., Jeng, W., Sheen, I., Chen, J., Lin, C. & Meng, X. J. ( 2002; ). Subclinical spread of HEV among swine, swine handlers and different countries: a longitudinal study. Journal of Medical Virology 66, 488-492.[CrossRef]
    [Google Scholar]
  57. Zanetti, A. R., Schlauder, G. G., Romano, L., Tanzi, E., Fabris, P., Dawson, G. J. & Mushahwar, I. K. ( 1999; ). Identification of a novel variant of hepatitis E virus in Italy. Journal of Medical Virology 57, 356-360.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-83-9-2201
Loading
/content/journal/jgv/10.1099/0022-1317-83-9-2201
Loading

Data & Media loading...

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error