1887

Journal of General Virology header logo

Volume 82, Issue 10

Genetic identification and characterization of a novel virus related to human hepatitis E virus from chickens with hepatitis–splenomegaly syndrome in the United States Free

Abstract

Hepatitis–splenomegaly (HS) syndrome is an emerging disease in chickens in North America; the cause of this disease is unknown. In this study, the genetic identification and characterization of a novel virus related to human hepatitis E virus (HEV) isolated from bile samples of chickens with HS syndrome is reported. Based upon the similar genomic organization and significant sequence identity of this virus with HEV, the virus has been tentatively named avian HEV in order to distinguish it from human and swine HEV. Electron microscopy revealed that avian HEV is a non-enveloped virus particle of 30–35 nm in diameter. The sequence of the 3′ half of the viral genome (∼4 kb) was determined. Sequence analyses revealed that this genomic region contains the complete 3′ non-coding region, the complete genes from open reading frames (ORFs) 2 and 3, the complete RNA-dependent RNA polymerase (RdRp) gene and a partial helicase gene from ORF 1. The helicase gene is the most conserved gene between avian HEV and other HEV strains, displaying 58–61% aa and 57–60% nt sequence identities. The RdRp gene of avian HEV shares 47–50% aa and 52–53% nt sequence identities and the putative capsid gene (ORF 2) of avian HEV shares 48–49% aa and 48–51% nt sequence identities with the corresponding regions of other known HEV strains. Phylogenetic analysis indicates that avian HEV is genetically related to, but distinct from, other known HEV strains. This discovery has important implications for HEV animal models, nomenclature and natural history.

  • Received:
  • Accepted:
  • Published Online:
© Microbiology Society
Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-82-10-2449
2001-10-01
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/jgv/82/10/0822449a.html?itemId=/content/journal/jgv/10.1099/0022-1317-82-10-2449&mimeType=html&fmt=ahah

References

  1. 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]
  2. Aye T. T., Uchida T., Ma X. Z., Iida F., Shikata T., Zhuang H., Win K. M. 1992; Complete nucleotide sequence of a hepatitis E virus isolated from the Xinjiang epidemic (1986–1988) of China. Nucleic Acids Research 20:3512
     [Google Scholar]
  3. Buisson Y., Grandadam M., Nicand E., Cheval P., van Cuyck-Gandre H., Innis B., Rehel P., Coursaget P., Teyssou R., Tsarev S. 2000; Identification of a novel hepatitis E virus in Nigeria. Journal of General Virology 81:903–909
     [Google Scholar]
  4. 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
     [Google Scholar]
  5. Clayson E. T., Innis B. L., Myint K. S., Narupiti S., Vaughn D. W., Giri S., Ranabhat P., Shrestha M. P. 1995; Detection of hepatitis E virus infections among domestic swine in the Kathmandu Valley of Nepal. American Journal of Tropical Medicine and Hygiene 53:228–232
     [Google Scholar]
  6. Donati M. C., Fagan E. A., Harrison T. J. 1997; Sequence analysis of full-length HEV clones derived directly from human liver in fulminant hepatitis E. In Viral Hepatitis and Liver Disease pp 313–316 Edited by Rizzetto M., Purcell R. H., Gerin J. L., Verme G. Torino, Italy: Edizioni Minerva Medica;
     [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. Favorov M. O., Nazarova O., Margolis H. S. 1998; Is hepatitis E an emerging zoonotic disease?. American Journal of Tropical Medicine and Hygiene 59:242
     [Google Scholar]
  9. Favorov M. O., Kosoy M. Y., Tsarev S. A., Childs J. E., Margolis H. S. 2000; Prevalence of antibody to hepatitis E virus among rodents in the United States. Journal of Infectious Diseases 181:449–455
     [Google Scholar]
  10. Gouvea V., Snellings N., Cohen S. J., Warren R. L., Myint K. S., Shrestha M. P., Vaughn D. W., Hoke C. H. Jr, Innis B. L. 1997; Hepatitis E virus in Nepal: similarities with the Burmese and Indian variants. Virus Research 52:87–96
     [Google Scholar]
  11. Halbur P. G., Kasorndorkbua C., Gilbert C., Guenette D. K., Potters M. B., Purcell R. H., Emerson S. U., Toth T. E., Meng X. J. 2000; Comparative pathogenesis of infection of pigs with hepatitis E viruses recovered from a pig and a human. Journal of Clinical Microbiology 39:918–923
     [Google Scholar]
  12. Handlinger J. H., Williams W. 1988; An egg drop associated with splenomegaly in broiler breeders. Avian Diseases 32:773–778
     [Google Scholar]
  13. Harrison T. J. 1999; Hepatitis E virus – an update. Liver 19:171–176
     [Google Scholar]
  14. Hsieh S. Y., Yang P. Y., Ho Y. P., Chu C. M., Liaw Y. F. 1998; Identification of a novel strain of hepatitis E virus responsible for sporadic acute hepatitis in Taiwan. Journal of Medical Virology 55:300–304
     [Google Scholar]
  15. 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]
  16. Huang C. C., Nguyen D., Fernandez J., Yun K. Y., Fry K. E., Bradley D. W., Tam A. W., Reyes G. R. 1992; Molecular cloning and sequencing of the Mexico isolate of hepatitis E virus (HEV). Virology 191:550–558
     [Google Scholar]
  17. Jeffrey J. S., Shivaprasad H. L. 1998; Investigation of hemorrhagic hepatosplenomegaly syndrome in broiler breeder hens. Proceedings of Western Poultry Disease Conference pp 46–48
     [Google Scholar]
  18. Julian R. J. 1995; Hepatitis-liver hemorrhage syndrome in laying hens. Proceedings of 67th North East Conference of Avian Disease Mystic, CT, USA:p– 17
     [Google Scholar]
  19. Kabrane-Lazizi Y., Meng X. J., Purcell R. H., Emerson S. U. 1999a; Evidence that the genomic RNA of hepatitis E virus is capped. Journal of Virology 73:8848–8850
     [Google Scholar]
  20. Kabrane-Lazizi Y., Fine J. B., Elm J., Glass G. E., Higa H., Diwan A., Gibbs C. J. Jr, Meng X. J., Emerson S. U., Purcell R. H. 1999b; Evidence for wide-spread infection of wild rats with hepatitis E virus in the United States. American Journal of Tropical Medicine and Hygiene 61:331–335
     [Google Scholar]
  21. Kamer G., Argos P. 1984; Primary structural comparison of RNA-dependent polymerases from plant, animal and bacterial viruses. Nucleic Acids Research 12:7269–7282
     [Google Scholar]
  22. Karetnyi Y. V., Gilchrist M. J., Naides S. J. 1999; Hepatitis E virus infection prevalence among selected populations in Iowa. Journal of Clinical Virology 14:51–55
     [Google Scholar]
  23. Koonin E. V., Gorbalenya A. E., Purdy M. A., Rozanov M. N., Reyes G. R., Bradley D. W. 1992; Computer-assisted assignment of functional domains in the nonstructural polyprotein of hepatitis E virus: delineation of an additional group of positive-strand RNA plant and animal viruses. Proceedings of the National Academy of Sciences, USA 89:8259–8263
     [Google Scholar]
  24. Li T. C., Yamakava Y., Suzuki K., Tatsumi M., Azeez 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]
  25. McCrudden R., O’Connell S., Farrant T., Beaton S., Iredale J. P., Fine D. 2000; Sporadic acute hepatitis E in the United Kingdom: an under diagnosed phenomenon?. Gut 46:732–733
     [Google Scholar]
  26. 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
     [Google Scholar]
  27. Meng J., Cong M., Dai X., Pillot J., Purdy M. A., Fields H. A., Khudyakov Y. E. 1999; Primary structure of open reading frame 2 and 3 of the hepatitis E virus isolated from Morocco. Journal of Medical Virology 57:126–133
     [Google Scholar]
  28. Meng X. J. 2000a; Zoonotic and xenozoonotic risks of hepatitis E virus. Infectious Disease Reviews 2:35–41
     [Google Scholar]
  29. Meng X. J. 2000b; Novel strains of hepatitis E virus identified from humans and other animal species: is hepatitis E a zoonosis?. Journal of Hepatology 33:842–845
     [Google Scholar]
  30. Meng X. J. 2001; Swine hepatitis E virus: cross-species infection and risk in xenotransplantation. Current Topics in Microbiology and Immunology (in press
    [Google Scholar]
  31. 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
     [Google Scholar]
  32. 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. Archives of Virology 143:1405–1415
     [Google Scholar]
  33. 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]
  34. 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]
  35. Panda S. K., Nanda S. K., Zafrullah M., Ansari I. H., Ozdener M. H., Jameel S. 1995; An Indian strain of hepatitis E virus (HEV): cloning, sequence, and expression of structural region and antibody responses in sera from individuals from an area of high-level HEV endemicity. Journal of Clinical Microbiology 33:2653–2659
     [Google Scholar]
  36. Panda S. K., Ansari I. H., Durgapal H., Agrawal S., Jameel S. 2000; The in vitro -synthesized RNA from a cDNA clone of hepatitis E virus is infectious. Journal of Virology 74:2430–2437
     [Google Scholar]
  37. 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
     [Google Scholar]
  38. 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
     [Google Scholar]
  39. Pringle C. 1998; Virus taxonomy – San Diego 1998. Archives of Virology 143:1449–1459
     [Google Scholar]
  40. Purcell R. H. 1996; Hepatitis E virus. In Fields Virology pp 2831–2843 Edited by Fields B. N., Knipe D. M., Howley P. M. Philadelphia: Lippincott–Raven;
     [Google Scholar]
  41. Ray R., Jameel S., Manivel V., Ray R. 1992; Indian hepatitis E virus shows a major deletion in the small open reading frame. Virology 189:359–362
     [Google Scholar]
  42. Reyes G. R., Purdy M. A., Kim J. P., Luk K. C., Young L. M., Fry K. E., Bradley D. W. 1990; Isolation of a cDNA from the virus responsible for enterically transmitted non-A, non-B hepatitis. Science 247:1335–1339
     [Google Scholar]
  43. Riddell C. 1997; Hepatitis-splenomegaly syndrome. In Diseases of Poultry pp 1041 Edited by Calnek B. W., Barnes H. J., Beard C. W., McDougald L. R., Saif Y. M. Iowa: Iowa State University Press;
     [Google Scholar]
  44. Ritchie S. J., Riddell C. 1991; Hepatitis-splenomegaly syndrome in commercial egg-laying hens. Canadian Veterinary Journal 32:500–501
     [Google Scholar]
  45. Schlauder G. G., Dawson G. J., Erker J. C., Kwo P. Y., Knigge M. F., Smalley D. L., Rosenblatt J. E., Desai S. M., 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]
  46. 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
     [Google Scholar]
  47. Schlauder G. G., Frider B., Sookoian S., Castano G. C., Mushahwar I. K. 2000; Identification of two novel isolates of hepatitis E virus in Argentina. Journal of Infectious Diseases 182:294–297
     [Google Scholar]
  48. Shivaprasad H. L., Woolcock P. R. 1995; Necrohemorrhagic hepatitis in broiler breeders. Proceedings of Western Poultry Diseases Conference Sacramento, CA, USA:p– 6
     [Google Scholar]
  49. 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
     [Google Scholar]
  50. Tam A. W., Smith M. M., Guerra M. E., Huang C. C., Bradley D. W., Fry K. E., Reyes G. R. 1991; Hepatitis E virus (HEV): molecular cloning and sequencing of the full-length viral genome. Virology 185:120–131
     [Google Scholar]
  51. 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]
  52. Tien N. T., Clayson E. 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
     [Google Scholar]
  53. Tsarev S. A., Emerson S. U., Reyes G. R., Tsareva T. S., Legters L. J., Malik I. A., Iqbal M., Purcell R. H. 1992; Characterization of a prototype strain of hepatitis E virus. Proceedings of the National Academy of Sciences, USA 89:559–563
     [Google Scholar]
  54. Tsarev S. A., Tsareva T. S., Emerson S. U., Rippy M. K., Zack P., Shapiro M., Purcell R. H. 1995; Experimental hepatitis E in pregnant rhesus monkeys: failure to transmit hepatitis E virus (HEV) to offspring and evidence of naturally acquired antibodies to HEV. Journal of Infectious Diseases 172:31–37
     [Google Scholar]
  55. Tsarev S. A., Shrestha M. P., He J., Scott R. M., Vaughn D. W., Clayson E. T., Gigliotti S., Longer C. F., Innis B. L. 1998; Naturally acquired hepatitis E virus (HEV) infection in Nepalese rodents. American Journal of Tropical Medicine and Hygiene 59:242
     [Google Scholar]
  56. Tsarev S. A., Binn L. N., Gomatos P. J., Arthur R. R., Monier M. K., van Cuyck-Gandre H., Longer C. F., Innis B. L. 1999; Phylogenetic analysis of hepatitis E virus isolates from Egypt. Journal of Medical Virology 57:68–74
     [Google Scholar]
  57. Uchida T., Suzuki K., Hayashi N., Iida F., Hara T., Oo S. S., Wang C. K., Shikata T., Ichikawa M., Rikihisa T., Mizuno K., Win K. M. 1992; Hepatitis E virus: cDNA cloning and expression. Microbiology and Immunology 36:67–79
     [Google Scholar]
  58. van Cuyck-Gandre H., Zhang H. Y., Tsarev S. A., Warren R. L., Caudill J. D., Snellings N. J., Begot L., Innis B. L., Longer C. F. 2000; Phylogenetically distinct hepatitis E viruses in Pakistan. American Journal of Tropical Medicine and Hygiene 62:187–189
     [Google Scholar]
  59. Wang Y., Ling R., Erker J. C., Zhang H., Li H., Desai S., Mushahwar I. K., 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]
  60. 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]
  61. Wu J. C., Sheen I. J., Chiang T. Y., Sheng W. Y., Wang Y. J., Chan C. Y., Lee S. D. 1998; The impact of traveling to endemic areas on the spread of hepatitis E virus infection: epidemiological and molecular analyses. Hepatology 27:1415–1420
     [Google Scholar]
  62. Yin S., Purcell R. H., Emerson S. U. 1994; A new Chinese isolate of hepatitis E virus: comparison with strains recovered from different geographical regions. Virus Genes 9:23–32
     [Google Scholar]
  63. Zafrullah M., Ozdener M. H., Kumar R., Panda S. K., Jameel S. 1999; Mutational analysis of glycosylation, membrane translocation, and cell surface expression of the hepatitis E virus ORF2 protein. Journal of Virology 73:4074–4082
     [Google Scholar]
  64. 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
     [Google Scholar]
  65. Zhang Y., McAtee P., Yarbough P. O., Tam A. W., Fuerst T. 1997; Expression, characterization, and immunoreactivities of a soluble hepatitis E virus putative capsid protein species expressed in insect cells. Clinical and Diagnostic Laboratory Immunology 4:423–428
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-82-10-2449
Loading
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 (2001); https://doi.org/10.1099/0022-1317-82-10-2449
/content/journal/jgv/10.1099/0022-1317-82-10-2449
/content/journal/jgv/10.1099/0022-1317-82-10-2449
Loading

Data & Media loading...

Most cited Most Cited RSS feed

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