1887

Abstract

A novel virus was detected in a sample collected from a Swedish moose (). The virus was suggested as a member of the family, although it was found to be highly divergent from the known four genotypes (gt1–4) of hepatitis E virus (HEV). Moose are regularly hunted for consumption in the whole of Scandinavia. Thus, the finding of this virus may be important from several aspects: (a) as a new diverged HEV in a new animal species, and (b) potential unexplored HEV transmission pathways for human infections. Considering these aspects, we have started the molecular characterization of this virus. A 5.1 kb amplicon was sequenced, and corresponded to the partial ORF1, followed by complete ORF2, ORF3 and poly(A) sequence. In comparison with existing HEVs, the moose HEV genome showed a general nucleotide sequence similarity of 37–63 % and an extensively divergent putative ORF3 sequence. The junction region between the ORFs was also highly divergent; however, two putative secondary stem–loop structures were retained when compared to gt1–4, but with altered structural appearance. In the phylogenetic analysis, the moose HEV deviated and formed its own branch between the gt1–4 and other divergent animal HEVs. The characterization of this highly divergent genome provides important information regarding the diversity of HEV infecting various mammalian species. However, further studies are needed to investigate its prevalence in the moose populations and possibly in other host species, including the risk for human infection.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.059238-0
2014-03-01
2019-09-21
Loading full text...

Full text loading...

/deliver/fulltext/jgv/95/3/557.html?itemId=/content/journal/jgv/10.1099/vir.0.059238-0&mimeType=html&fmt=ahah

References

  1. Abdelwahab S. , Rewisha E. , Hashem M. , Sobhy M. , Galal I. , Allam W. R. , Mikhail N. , Galal G. , El-Tabbakh M. . & other authors ( 2012; ). Risk factors for hepatitis C virus infection among Egyptian healthcare workers in a national liver diseases referral centre. . Trans R Soc Trop Med Hyg 106:, 98–103. [CrossRef] [PubMed]
    [Google Scholar]
  2. Aggarwal R. . ( 2011; ). Clinical presentation of hepatitis E. . Virus Res 161:, 15–22. [CrossRef] [PubMed]
    [Google Scholar]
  3. Aggarwal R. , Jameel S. . ( 2008; ). Hepatitis E vaccine. . Hepatol Int 2:, 308–315. [CrossRef] [PubMed]
    [Google Scholar]
  4. Ahmad I. , Holla R. P. , Jameel S. . ( 2011; ). Molecular virology of hepatitis E virus. . Virus Res 161:, 47–58. [CrossRef] [PubMed]
    [Google Scholar]
  5. Bányai K. , Tóth A. G. , Ivanics E. , Glávits R. , Szentpáli-Gavallér K. , Dán A. . ( 2012; ). Putative novel genotype of avian hepatitis E virus, Hungary, 2010. . Emerg Infect Dis 18:, 1365–1368. [CrossRef] [PubMed]
    [Google Scholar]
  6. 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. [CrossRef] [PubMed]
    [Google Scholar]
  7. Cao D. , Huang Y. W. , Meng X. J. . ( 2010; ). The nucleotides on the stem-loop RNA structure in the junction region of the hepatitis E virus genome are critical for virus replication. . J Virol 84:, 13040–13044. [CrossRef] [PubMed]
    [Google Scholar]
  8. Christensen P. B. , Engle R. E. , Hjort C. , Homburg K. M. , Vach W. , Georgsen J. , Purcell R. H. . ( 2008; ). Time trend of the prevalence of hepatitis E antibodies among farmers and blood donors: a potential zoonosis in Denmark. . Clin Infect Dis 47:, 1026–1031. [CrossRef] [PubMed]
    [Google Scholar]
  9. Colson P. , Borentain P. , Queyriaux B. , Kaba M. , Moal V. , Gallian P. , Heyries L. , Raoult D. , Gerolami R. . ( 2010; ). Pig liver sausage as a source of hepatitis E virus transmission to humans. . J Infect Dis 202:, 825–834. [CrossRef] [PubMed]
    [Google Scholar]
  10. Cossaboom C. M. , Córdoba L. , Sanford B. J. , Piñeyro P. , Kenney S. P. , Dryman B. A. , Wang Y. , Meng X. J. . ( 2012; ). Cross-species infection of pigs with a novel rabbit, but not rat, strain of hepatitis E virus isolated in the United States. . J Gen Virol 93:, 1687–1695. [CrossRef] [PubMed]
    [Google Scholar]
  11. Dalton H. R. , Thurairajah P. H. , Fellows H. J. , Hussaini H. S. , Mitchell J. , Bendall R. , Banks M. , Ijaz S. , Teo C. G. , Levine D. F. . ( 2007; ). Autochthonous hepatitis E in southwest England. . J Viral Hepat 14:, 304–309. [CrossRef] [PubMed]
    [Google Scholar]
  12. Drexler J. F. , Seelen A. , Corman V. M. , Fumie Tateno A. , Cottontail V. , Melim Zerbinati R. , Gloza-Rausch F. , Klose S. M. . & other authors ( 2012; ). Bats worldwide carry hepatitis E virus-related viruses that form a putative novel genus within the family Hepeviridae. . J Virol 86:, 9134–9147.[CrossRef]
    [Google Scholar]
  13. Egloff M. P. , Malet H. , Putics A. , Heinonen M. , Dutartre H. , Frangeul A. , Gruez A. , Campanacci V. , Cambillau C. . & other authors ( 2006; ). Structural and functional basis for ADP-ribose and poly(ADP-ribose) binding by viral macro domains. . J Virol 80:, 8493–8502. [CrossRef] [PubMed]
    [Google Scholar]
  14. Feagins A. R. , Córdoba L. , Sanford B. J. , Dryman B. A. , Huang Y. W. , LeRoith T. , Emerson S. U. , Meng X. J. . ( 2011; ). Intergenotypic chimeric hepatitis E viruses (HEVs) with the genotype 4 human HEV capsid gene in the backbone of genotype 3 swine HEV are infectious in pigs. . Virus Res 156:, 141–146. [CrossRef] [PubMed]
    [Google Scholar]
  15. Gorbalenya A. E. , Blinov V. M. , Donchenko A. P. , Koonin E. V. . ( 1989; ). An NTP-binding motif is the most conserved sequence in a highly diverged monophyletic group of proteins involved in positive strand RNA viral replication. . J Mol Evol 28:, 256–268. [CrossRef] [PubMed]
    [Google Scholar]
  16. Graff J. , Nguyen H. , Yu C. , Elkins W. R. , St Claire M. , Purcell R. H. , Emerson S. U. . ( 2005; ). 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 79:, 6680–6689. [CrossRef] [PubMed]
    [Google Scholar]
  17. Graff J. , Torian U. , Nguyen H. , Emerson S. U. . ( 2006; ). A bicistronic subgenomic mRNA encodes both the ORF2 and ORF3 proteins of hepatitis E virus. . J Virol 80:, 5919–5926. [CrossRef] [PubMed]
    [Google Scholar]
  18. Gyarmati P. , Mohammed N. , Norder H. , Blomberg J. , Belák S. , Widén F. . ( 2007; ). Universal detection of hepatitis E virus by two real-time PCR assays: TaqMan and Primer-Probe Energy Transfer. . J Virol Methods 146:, 226–235. [CrossRef] [PubMed]
    [Google Scholar]
  19. Huang F. F. , Sun Z. F. , Emerson S. U. , Purcell R. H. , Shivaprasad H. L. , Pierson F. W. , Toth T. E. , Meng X. J. . ( 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. [CrossRef] [PubMed]
    [Google Scholar]
  20. 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. [CrossRef] [PubMed]
    [Google Scholar]
  21. Johne R. , Heckel G. , Plenge-Bönig A. , Kindler E. , Maresch C. , Reetz J. , Schielke A. , Ulrich R. G. . ( 2010; ). Novel hepatitis E virus genotype in Norway rats, Germany. . Emerg Infect Dis 16:, 1452–1455. [CrossRef] [PubMed]
    [Google Scholar]
  22. Johne R. , Dremsek P. , Kindler E. , Schielke A. , Plenge-Bönig A. , Gregersen H. , Wessels U. , Schmidt K. , Rietschel W. . & other authors ( 2012; ). Rat hepatitis E virus: geographical clustering within Germany and serological detection in wild Norway rats (Rattus norvegicus). . Infect Genet Evol 12:, 947–956. [CrossRef] [PubMed]
    [Google Scholar]
  23. Jothikumar N. , Cromeans T. L. , Robertson B. H. , Meng X. J. , Hill V. R. . ( 2006; ). A broadly reactive one-step real-time RT-PCR assay for rapid and sensitive detection of hepatitis E virus. . J Virol Methods 131:, 65–71. [CrossRef] [PubMed]
    [Google Scholar]
  24. Kamar N. , Bendall R. , Legrand-Abravanel F. , Xia N. S. , Ijaz S. , Izopet J. , Dalton H. R. . ( 2012; ). Hepatitis E. . Lancet 379:, 2477–2488. [CrossRef] [PubMed]
    [Google Scholar]
  25. Kannan H. , Fan S. , Patel D. , Bossis I. , Zhang Y. J. . ( 2009; ). The hepatitis E virus open reading frame 3 product interacts with microtubules and interferes with their dynamics. . J Virol 83:, 6375–6382. [CrossRef] [PubMed]
    [Google Scholar]
  26. Kar-Roy A. , Korkaya H. , Oberoi R. , Lal S. K. , Jameel S. . ( 2004; ). The hepatitis E virus open reading frame 3 protein activates ERK through binding and inhibition of the MAPK phosphatase. . J Biol Chem 279:, 28345–28357. [CrossRef] [PubMed]
    [Google Scholar]
  27. Karpe Y. A. , Lole K. S. . ( 2010a; ). RNA 5′-triphosphatase activity of the hepatitis E virus helicase domain. . J Virol 84:, 9637–9641. [CrossRef] [PubMed]
    [Google Scholar]
  28. Karpe Y. A. , Lole K. S. . ( 2010b; ). NTPase and 5′ to 3′ RNA duplex-unwinding activities of the hepatitis E virus helicase domain. . J Virol 84:, 3595–3602. [CrossRef] [PubMed]
    [Google Scholar]
  29. Knowles N. J. , Hovi T. , Hyypiä T. , King A. M. Q. , Lindberg A. M. , Pallansch M. A. , Palmenberg A. C. , Simmonds P. , Skern T. . & other authors ( 2012; ). Picornaviridae. . In Virus Taxonomy, Ninth Report of the International Committee on Taxonomy of Viruses, pp 855–880. Edited by King A. M. Q. et al. . San Diego:: Elsevier;.
    [Google Scholar]
  30. 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. . Proc Natl Acad Sci U S A 89:, 8259–8263. [CrossRef] [PubMed]
    [Google Scholar]
  31. Korkaya H. , Jameel S. , Gupta D. , Tyagi S. , Kumar R. , Zafrullah M. , Mazumdar M. , Lal S. K. , Xiaofang L. . & other authors ( 2001; ). The ORF3 protein of hepatitis E virus binds to Src homology 3 domains and activates MAPK. . J Biol Chem 276:, 42389–42400. [CrossRef] [PubMed]
    [Google Scholar]
  32. Lack J. B. , Volk K. , Van Den Bussche R. A. . ( 2012; ). Hepatitis E virus genotype 3 in wild rats, United States. . Emerg Infect Dis 18:, 1268–1273. [CrossRef] [PubMed]
    [Google Scholar]
  33. Li T. C. , Chijiwa K. , Sera N. , Ishibashi T. , Etoh Y. , Shinohara Y. , Kurata Y. , Ishida M. , Sakamoto S. . & other authors ( 2005; ). Hepatitis E virus transmission from wild boar meat. . Emerg Infect Dis 11:, 1958–1960. [CrossRef] [PubMed]
    [Google Scholar]
  34. Li T. C. , Ami Y. , Suzaki Y. , Yasuda S. P. , Yoshimatsu K. , Arikawa J. , Takeda N. , Takaji W. . ( 2013; ). Characterization of full genome of rat hepatitis E virus strain from Vietnam. . Emerg Infect Dis 19:, 115–118. [CrossRef] [PubMed]
    [Google Scholar]
  35. Mansuy J. M. , Abravanel F. , Miedouge M. , Mengelle C. , Merviel C. , Dubois M. , Kamar N. , Rostaing L. , Alric L. . & other authors ( 2009; ). Acute hepatitis E in south-west France over a 5-year period. . J Clin Virol 44:, 74–77. [CrossRef] [PubMed]
    [Google Scholar]
  36. 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. [CrossRef] [PubMed]
    [Google Scholar]
  37. Mizuo H. , Suzuki K. , Takikawa Y. , Sugai Y. , Tokita H. , Akahane Y. , Itoh K. , Gotanda Y. , Takahashi M. . & other authors ( 2002; ). Polyphyletic strains of hepatitis E virus are responsible for sporadic cases of acute hepatitis in Japan. . J Clin Microbiol 40:, 3209–3218. [CrossRef] [PubMed]
    [Google Scholar]
  38. Mori Y. , Matsuura Y. . ( 2011; ). Structure of hepatitis E viral particle. . Virus Res 161:, 59–64. [CrossRef] [PubMed]
    [Google Scholar]
  39. Navaneethan U. , Al Mohajer M. , Shata M. T. . ( 2008; ). Hepatitis E and pregnancy: understanding the pathogenesis. . Liver Int 28:, 1190–1199. [CrossRef] [PubMed]
    [Google Scholar]
  40. Neuvonen M. , Ahola T. . ( 2009; ). Differential activities of cellular and viral macro domain proteins in binding of ADP-ribose metabolites. . J Mol Biol 385:, 212–225. [CrossRef] [PubMed]
    [Google Scholar]
  41. Norder H. , Sundqvist L. , Magnusson L. , Østergaard Breum S. , Löfdahl M. , Larsen L. E. , Hjulsager C. K. , Magnius L. , Böttiger B. E. , Widén F. . ( 2009; ). Endemic hepatitis E in two Nordic countries. . Euro Surveill 14:, 19211.[PubMed]
    [Google Scholar]
  42. Okamoto H. . ( 2007; ). Genetic variability and evolution of hepatitis E virus. . Virus Res 127:, 216–228. [CrossRef] [PubMed]
    [Google Scholar]
  43. Olsen B. , Axelsson-Olsson D. , Thelin A. , Weiland O. . ( 2006; ). Unexpected high prevalence of IgG-antibodies to hepatitis E virus in Swedish pig farmers and controls. . Scand J Infect Dis 38:, 55–58. [CrossRef] [PubMed]
    [Google Scholar]
  44. Pavio N. , Meng X. J. , Renou C. . ( 2010; ). Zoonotic hepatitis E: animal reservoirs and emerging risks. . Vet Res 41:, 46. [CrossRef] [PubMed]
    [Google Scholar]
  45. Purdy M. A. , Khudyakov Y. E. . ( 2011; ). The molecular epidemiology of hepatitis E virus infection. . Virus Res 161:, 31–39. [CrossRef] [PubMed]
    [Google Scholar]
  46. Purdy M. A. , Lara J. , Khudyakov Y. E. . ( 2012; ). The hepatitis E virus polyproline region is involved in viral adaptation. . PLoS ONE 7:, e35974. [CrossRef] [PubMed]
    [Google Scholar]
  47. Raj V. S. , Smits S. L. , Pas S. D. , Provacia L. B. , Moorman-Roest H. , Osterhaus A. D. , Haagmans B. L. . ( 2012; ). Novel hepatitis E virus in ferrets, the Netherlands. . Emerg Infect Dis 18:, 1369–1370. [CrossRef] [PubMed]
    [Google Scholar]
  48. Ratra R. , Kar-Roy A. , Lal S. K. . ( 2008; ). The ORF3 protein of hepatitis E virus interacts with hemopexin by means of its 26 amino acid N-terminal hydrophobic domain II. . Biochemistry 47:, 1957–1969. [CrossRef] [PubMed]
    [Google Scholar]
  49. Rikihisa Y. . ( 2011; ). Mechanisms of obligatory intracellular infection with Anaplasma phagocytophilum . . Clin Microbiol Rev 24:, 469–489. [CrossRef] [PubMed]
    [Google Scholar]
  50. 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. [CrossRef] [PubMed]
    [Google Scholar]
  51. Smith D. B. , Purdy M. A. , Simmonds P. . ( 2013; ). Genetic variability and the classification of hepatitis E virus. . J Virol 87:, 4161–4169. [CrossRef] [PubMed]
    [Google Scholar]
  52. Sprygin A. V. , Nikonova Z. B. , Zinyakov N. G. . ( 2012; ). Avian hepatitis E virus identified in Russian chicken flocks exhibits high genetic divergence based on the ORF2 capsid gene. . Avian Pathol 41:, 459–463. [CrossRef] [PubMed]
    [Google Scholar]
  53. Stuen S. . ( 2007; ). Anaplasma phagocytophilum - the most widespread tick-borne infection in animals in Europe. . Vet Res Commun 31: (Suppl 1), 79–84. [CrossRef] [PubMed]
    [Google Scholar]
  54. 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. [CrossRef] [PubMed]
    [Google Scholar]
  55. 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. [CrossRef] [PubMed]
    [Google Scholar]
  56. Tamura K. , Peterson D. , Peterson N. , Stecher G. , Nei M. , Kumar S. . ( 2011; ). mega 5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. . Mol Biol Evol 28:, 2731–2739. [CrossRef] [PubMed]
    [Google Scholar]
  57. Tei S. , Kitajima N. , Takahashi K. , Mishiro S. . ( 2003; ). Zoonotic transmission of hepatitis E virus from deer to human beings. . Lancet 362:, 371–373. [CrossRef] [PubMed]
    [Google Scholar]
  58. Tomiyama D. , Inoue E. , Osawa Y. , Okazaki K. . ( 2009; ). Serological evidence of infection with hepatitis E virus among wild Yezo-deer, Cervus nippon yesoensis, in Hokkaido, Japan. . J Viral Hepat 16:, 524–528. [CrossRef] [PubMed]
    [Google Scholar]
  59. Vasickova P. , Kralik P. , Slana I. , Pavlik I. . ( 2012; ). Optimisation of a triplex real time RT-PCR for detection of hepatitis E virus RNA and validation on biological samples. . J Virol Methods 180:, 38–42. [CrossRef] [PubMed]
    [Google Scholar]
  60. Wang H. , Zhang W. , Ni B. , Shen H. , Song Y. , Wang X. , Shao S. , Hua X. , Cui L. . ( 2010; ). Recombination analysis reveals a double recombination event in hepatitis E virus. . Virol J 7:, 129. [CrossRef] [PubMed]
    [Google Scholar]
  61. Widén F. , Sundqvist L. , Matyi-Toth A. , Metreveli G. , Belák S. , Hallgren G. , Norder H. . ( 2011; ). Molecular epidemiology of hepatitis E virus in humans, pigs and wild boars in Sweden. . Epidemiol Infect 139:, 361–371. [CrossRef] [PubMed]
    [Google Scholar]
  62. Xia H. , Liu L. , Linde A. M. , Belák S. , Norder H. , Widén F. . ( 2008; ). Molecular characterization and phylogenetic analysis of the complete genome of a hepatitis E virus from European swine. . Virus Genes 37:, 39–48. [CrossRef] [PubMed]
    [Google Scholar]
  63. Xing L. , Li T. C. , Mayazaki N. , Simon M. N. , Wall J. S. , Moore M. , Wang C. Y. , Takeda N. , Wakita T. . & other authors ( 2010; ). Structure of hepatitis E virion-sized particle reveals an RNA-dependent viral assembly pathway. . J Biol Chem 285:, 33175–33183. [CrossRef] [PubMed]
    [Google Scholar]
  64. Yamashita T. , Mori Y. , Miyazaki N. , Cheng R. H. , Yoshimura M. , Unno H. , Shima R. , Moriishi K. , Tsukihara T. . & other authors ( 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. [CrossRef] [PubMed]
    [Google Scholar]
  65. 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]
  66. 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. . J Virol 73:, 4074–4082.[PubMed]
    [Google Scholar]
  67. Zhai L. , Dai X. , Meng J. . ( 2006; ). Hepatitis E virus genotyping based on full-length genome and partial genomic regions. . Virus Res 120:, 57–69. [CrossRef] [PubMed]
    [Google Scholar]
  68. Zhao Q. , Zhou E. M. , Dong S. W. , Qiu H. K. , Zhang L. , Hu S. B. , Zhao F. F. , Jiang S. J. , Sun Y. N. . ( 2010; ). Analysis of avian hepatitis E virus from chickens, China. . Emerg Infect Dis 16:, 1469–1472. [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.059238-0
Loading
/content/journal/jgv/10.1099/vir.0.059238-0
Loading

Data & Media loading...

Supplementary material 

PDF

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