Hepatitis E virus cell culture models

Virus Research

Volumn 161, Issue 1, 2011, Pages 65-77

  Okamoto, Hiroaki ^a  

^a JICHI MEDICAL UNIVERSITY   (Japan)

Author keywords

Cell culture; Genotype; Hepatitis E virus; Infectious clone

Indexed keywords

COMPLEMENTARY DNA; LIPID;

CELL CULTURE; HEPATITIS E VIRUS; HUMAN; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; REVIEW; VIRION; VIRUS CULTURE; VIRUS LOAD; VIRUS PARTICLE; VIRUS REPLICATION;

ANIMALS; CELL LINE; HEPATITIS E; HEPATITIS E VIRUS; HUMANS; MODELS, BIOLOGICAL; VIRUS CULTIVATION;

HEPATITIS E VIRUS;

EID: 79957599046     PISSN: 01681702     EISSN: 18727492     Source Type: Journal    
DOI: 10.1016/j.virusres.2011.01.015     Document Type: Review

References (81)

1. Agrawal S., Gupta D., Panda S.K. The 3' end of hepatitis E virus (HEV) genome binds specifically to the viral RNA-dependent RNA polymerase (RdRp). Virology 2001, 282(1):87-101.
2. Arankalle V.A., Chobe L.P. Retrospective analysis of blood transfusion recipients: evidence for post-transfusion hepatitis E. Vox Sang. 2000, 79(2):72-74.
3. Arankalle V.A., Ticehurst J., Sreenivasan M.A., Kapikian A.Z., Popper H., Pavri K.M., Purcell R.H. Aetiological association of a virus-like particle with enterically transmitted non-A, non-B hepatitis. Lancet 1988, 1(8585):550-554.
4. Balayan M.S., Andjaparidze A.G., Savinskaya S.S., Ketiladze E.S., Braginsky D.M., Savinov A.P., Poleschuk V.F. Evidence for a virus in non-A, non-B hepatitis transmitted via the fecal-oral route. Intervirology 1983, 20(1):23-31.
5. Chandra V., Taneja S., Kalia M., Jameel S. Molecular biology and pathogenesis of hepatitis E virus. J. Biosci. 2008, 33(4):451-464.
6. Colson P., Borentain P., Queyriaux B., Kaba M., Moal V., Gallian P., Heyries L., Raoult D., Gerolami R. Pig liver sausage as a source of hepatitis E virus transmission to humans. J. Infect. Dis. 2010, 202(6):825-834.
7. Dalton H.R., Bendall R., Ijaz S., Banks M. Hepatitis E: an emerging infection in developed countries. Lancet Infect. Dis. 2008, 8(11):698-709.
8. Emerson S.U., Anderson D., Arankalle A., Meng X.J., Purdy M., Schlauder G.G., Tsarev S.A. Hepevirus. Virus Taxonomy, VIIIth Report of the ICTV 2005, 853-857. Elsevier/Academic Press, London. C.M. Fauquet, M.A. Mayo, J. Maniloff, U. Desselberger, L.A. Ball (Eds.).
9. Emerson S.U., Arankalle V.A., Purcell R.H. Thermal stability of hepatitis E virus. J. Infect. Dis. 2005, 192(5):930-933.
10. Emerson S.U., Clemente-Casares P., Moiduddin N., Arankalle V.A., Torian U., Purcell R.H. Putative neutralization epitopes and broad cross-genotype neutralization of Hepatitis E virus confirmed by a quantitative cell-culture assay. J. Gen. Virol. 2006, 87(Pt 3):697-704.
11. Emerson S.U., Nguyen H., Torian U., Purcell R.H. ORF3 protein of hepatitis E virus is not required for replication, virion assembly, or infection of hepatoma cells in vitro. J. Virol. 2006, 80(21):10457-10464.
12. Emerson S.U., Nguyen H.T., Torian U., Burke D., Engle R., Purcell R.H. Release of genotype 1 hepatitis E virus from cultured hepatoma and polarized intestinal cells depends on open reading frame 3 protein and requires an intact PXXP motif. J. Virol. 2010, 84(18):9059-9069.
13. Emerson S.U., Purcell R.H. Hepatitis E virus. Fields Virology 2007, 3047-3058. Lippincott Williams & Wilkins, Philadelphia. fifth ed. D.M. Knipe, P.M. Howley, D.E. Griffin, R.A. Lamb, M.A. Martin, B. Roizman, S.E. Straus (Eds.).
14. Garrus J.E., von Schwedler U.K., Pornillos O.W., Morham S.G., Zavitz K.H., Wang H.E., Wettstein D.A., Stray K.M., Cote M., Rich R.L., Myszka D.G., Sundquist W.I. Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding. Cell 2001, 107(1):55-65.
15. Graff J., Kasang C., Normann A., Pfisterer-Hunt M., Feinstone S.M., Flehmig B. Mutational events in consecutive passages of hepatitis A virus strain GBM during cell culture adaptation. Virology 1994, 204(1):60-68.
16. Graff J., Nguyen H., Kasorndorkbua C., Halbur P.G., St Claire M., Purcell R.H., Emerson S.U. In vitro and in vivo mutational analysis of the 3'-terminal regions of hepatitis e virus genomes and replicons. J. Virol. 2005, 79(2):1017-1026.
17. 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(11):6680-6689.
18. 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(12):5919-5926.
19. 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(3):1185-1194.
20. Guu T.S., Liu Z., Ye Q., Mata D.A., Li K., Yin C., Zhang J., Tao Y.J. Structure of the hepatitis E virus-like particle suggests mechanisms for virus assembly and receptor binding. Proc. Natl. Acad. Sci. U.S.A. 2009, 106(31):12992-12997.
21. Hu N.Z., Hu Y.Z., Shi H.J., Liu G.D., Qu S. Mutational characteristics in consecutive passage of rapidly replicating variants of hepatitis A virus strain H2 during cell culture adaptation. World J. Gastroenterol. 2002, 8(5):872-878.
22. Huang R., Li D., Wei S., Li Q., Yuan X., Geng L., Li X., Liu M. Cell culture of sporadic hepatitis E virus in China. Clin. Diagn. Lab. Immunol. 1999, 6(5):729-733.
23. Huang R., Nakazono N., Ishii K., Li D., Kawamata O., Kawaguchi R., Tsukada Y. Hepatitis E virus (87A strain) propagated in A549 cells. J. Med. Virol. 1995, 47(4):299-302.
24. Huang R.T., Li D.R., Wei J., Huang X.R., Yuan X.T., Tian X. Isolation and identification of hepatitis E virus in Xinjiang, China. J. Gen. Virol. 1992, 73(Pt 5):1143-1148.
25. 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(6):3018-3026.
26. Ichiyama K., Yamada K., Tanaka T., Nagashima S., Jirintai, Takahashi M., Okamoto H. Determination of the 5'-terminal sequence of subgenomic RNA of hepatitis E virus strains in cultured cells. Arch. Virol. 2009, 154(12):1945-1951.
27. Jansen R.W., Newbold J.E., Lemon S.M. Complete nucleotide sequence of a cell culture-adapted variant of hepatitis A virus: comparison with wild-type virus with restricted capacity for in vitro replication. Virology 1988, 163(2):299-307.
28. Kabrane-Lazizi Y., Meng X.J., Purcell R.H., Emerson S.U. Evidence that the genomic RNA of hepatitis E virus is capped. J. Virol. 1999, 73(10):8848-8850.
29. Kane M.A., Bradley D.W., Shrestha S.M., Maynard J.E., Cook E.H., Mishra R.P., Joshi D.D. Epidemic non-A, non-B hepatitis in Nepal. Recovery of a possible etiologic agent and transmission studies in marmosets. JAMA 1984, 252(22):3140-3145.
30. Kazachkov Yu A., Balayan M.S., Ivannikova T.A., Panina L.I., Orlova T.M., Zamyatina N.A., Kusov Y. Hepatitis E virus in cultivated cells. Arch. Virol. 1992, 127(1-4):399-402.
31. Koonin E.V., Gorbalenya A.E., Purdy M.A., Rozanov M.N., Reyes G.R., Bradley D.W. 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. 1992, 89(17):8259-8263.
32. Korkaya H., Jameel S., Gupta D., Tyagi S., Kumar R., Zafrullah M., Mazumdar M., Lal S.K., Xiaofang L., Sehgal D., Das S.R., Sahal D. The ORF3 protein of hepatitis E virus binds to Src homology 3 domains and activates MAPK. J. Biol. Chem. 2001, 276(45):42389-42400.
33. Lemon S.M., Binn L.N. Incomplete neutralization of hepatitis A virus in vitro due to lipid-associated virions. J. Gen. Virol. 1985, 66(Pt 11):2501-2505.
34. Lewis H.C., Wichmann O., Duizer E. Transmission routes and risk factors for autochthonous hepatitis E virus infection in Europe: a systematic review. Epidemiol. Infect. 2010, 138(2):145-166.
35. Li D.R., Huang R.T., Pang J.J., Yuan X.T., Li X.Y. Biological feature and genome analysis of HEV isolated by cell-culture. Enterically-Transmitted Hepatitis Viruses 1996, 349-361. La Simarre, Joue-les-Tours, France. Y. Buisson, P. Coursaget, M. Kane (Eds.).
36. Lorenzo F.R., Tanaka T., Takahashi H., Ichiyama K., Hoshino Y., Yamada K., Inoue J., Takahashi M., Okamoto H. Mutational events during the primary propagation and consecutive passages of hepatitis E virus strain JE03-1760F in cell culture. Virus Res. 2008, 137(1):86-96.
37. Lu L., Li C., Hagedorn C.H. Phylogenetic analysis of global hepatitis E virus sequences: genetic diversity, subtypes and zoonosis. Rev. Med. Virol. 2006, 16(1):5-36.
38. Martin-Serrano J., Zang T., Bieniasz P.D. HIV-1 and Ebola virus encode small peptide motifs that recruit Tsg101 to sites of particle assembly to facilitate egress. Nat. Med. 2001, 7(12):1313-1319.
39. Matsubayashi K., Kang J.H., Sakata H., Takahashi K., Shindo M., Kato M., Sato S., Kato T., Nishimori H., Tsuji K., Maguchi H., Yoshida J., Maekubo H., Mishiro S., Ikeda H. A case of transfusion-transmitted hepatitis E caused by blood from a donor infected with hepatitis E virus via zoonotic food-borne route. Transfusion 2008, 48(7):1368-1375.
40. Meng J., Dubreuil P., Pillot J. A new PCR-based seroneutralization assay in cell culture for diagnosis of hepatitis E. J. Clin. Microbiol. 1997, 35(6):1373-1377.
41. Meng J., Guinet R., Pillot J. Infection of PLC/PRF-5 cells with the hepatitis E virus. Enterically-transmitted hepatitis viruses 1996, 336-345. La Simarre, Joue-les-Tours, France. Y. Buisson, P. Coursaget, M. Kane (Eds.).
42. Meng X.J. Hepatitis E virus: animal reservoirs and zoonotic risk. Vet. Microbiol. 2010, 140(3-4):256-265.
43. 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(18):9860-9865.
44. Mitsui T., Tsukamoto Y., Yamazaki C., Masuko K., Tsuda F., Takahashi M., Nishizawa T., Okamoto H. Prevalence of hepatitis E virus infection among hemodialysis patients in Japan: evidence for infection with a genotype 3 HEV by blood transfusion. J. Med. Virol. 2004, 74(4):563-572.
45. Okamoto H. Genetic variability and evolution of hepatitis E virus. Virus Res. 2007, 127(2):216-228.
46. Okamoto H., Takahashi M., Nishizawa T. Features of hepatitis E virus infection in Japan. Intern. Med. 2003, 42(11):1065-1071.
47. Pavio N., Meng X.J., Renou C. Zoonotic hepatitis E: animal reservoirs and emerging risks. Vet. Res. 2010, 41(6):46.
48. Pillot J., Sharma M.D., Lazizi Y., Budkowska A., Dauguet C., Galimand M., Sarthou J.L. Immunological characterization of a viral agent involved in epidemic and sporadic non A non B hepatitis. Am. Inst. Pasteur/Virologie 1987, 138:145-158.
49. Provost P.J., Wolanski B.S., Miller W.J., Ittensohn O.L., McAleer W.J., Hilleman M.R. Physical, chemical and morphologic dimensions of human hepatitis A virus strain CR326 (38578). Proc. Soc. Exp. Biol. Med. 1975, 148(2):532-539.
50. Purcell R.H., Emerson S.U. Animal models of hepatitis A and E. ILAR J. 2001, 42(2):161-177.
51. Purcell R.H., Emerson S.U. Hepatitis E: an emerging awareness of an old disease. J. Hepatol. 2008, 48(3):494-503.
52. Purcell R.H., Feinstone S.M., Ticehurst J.R., Daemer R.J., Baroudy B.M. Hepatitis A virus. Viral Hepatitis and Liver Diseases 1984, 9-22. Grune & Stratton, Orland, FL. G.N. Vyas, J.L. Dienstag, J.H. Hoofnagle (Eds.).
53. Reuter G., Fodor D., Forgach P., Katai A., Szucs G. Characterization and zoonotic potential of endemic hepatitis E virus (HEV) strains in humans and animals in Hungary. J. Clin. Virol. 2009, 44(4):277-281.
54. Reyes G.R., Purdy M.A., Kim J.P., Luk K.C., Young L.M., Fry K.E., Bradley D.W. Isolation of a cDNA from the virus responsible for enterically transmitted non-A, non-B hepatitis. Science 1990, 247(4948):1335-1339.
55. Rueckert R. On the structure and morphogenesis of picornaviruses. Comprehensive Virology 1976, vol. 6:131-213. Plenum Press, New Yor, NY.
56. Sonoda H., Abe M., Sugimoto T., Sato Y., Bando M., Fukui E., Mizuo H., Takahashi M., Nishizawa T., Okamoto H. 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. 2004, 42(11):5371-5374.
57. Surjit M., Jameel S., Lal S.K. Cytoplasmic localization of the ORF2 protein of hepatitis E virus is dependent on its ability to undergo retrotranslocation from the endoplasmic reticulum. J. Virol. 2007, 81(7):3339-3345.
58. Surjit M., Oberoi R., Kumar R., Lal S.K. Enhanced alpha1 microglobulin secretion from Hepatitis E virus ORF3-expressing human hepatoma cells is mediated by the tumor susceptibility gene 101. J. Biol. Chem. 2006, 281(12):8135-8142.
59. 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(2):501-505.
60. Takahashi K., Toyota J., Karino Y., Kang J.H., Maekubo H., Abe N., Mishiro S. Estimation of the mutation rate of hepatitis E virus based on a set of closely related 7.5-year-apart isolates from Sapporo, Japan. Hepatol. Res. 2004, 29(4):212-215.
61. Takahashi M., Hoshino Y., Tanaka T., Takahashi H., Nishizawa T., Okamoto H. Production of monoclonal antibodies against hepatitis E virus capsid protein and evaluation of their neutralizing activity in a cell culture system. Arch. Virol. 2008, 153(4):657-666.
62. Takahashi M., Nishizawa T., Miyajima H., Gotanda Y., Iita T., Tsuda F., Okamoto H. Swine hepatitis E virus strains in Japan form four phylogenetic clusters comparable with those of Japanese isolates of human hepatitis E virus. J. Gen. Virol. 2003, 84(Pt 4):851-862.
63. Takahashi M., Tanaka T., Azuma M., Kusano E., Aikawa T., Shibayama T., Yazaki Y., Mizuo H., Inoue J., Okamoto H. Prolonged fecal shedding of hepatitis E virus (HEV) during sporadic acute hepatitis E: evaluation of infectivity of HEV in fecal specimens in a cell culture system. J. Clin. Microbiol. 2007, 45(11):3671-3679.
64. Takahashi M., Tanaka T., Takahashi H., Hoshino Y., Nagashima S., Jirintai, Mizuo H., Yazaki Y., Takagi T., Azuma M., Kusano E., Isoda N., Sugano K., Okamoto H. Hepatitis E Virus (HEV) strains in serum samples can replicate efficiently in cultured cells despite the coexistence of HEV antibodies: characterization of HEV virions in blood circulation. J. Clin. Microbiol. 2010, 48(4):1112-1125.
65. Takahashi M., Yamada K., Hoshino Y., Takahashi H., Ichiyama K., Tanaka T., Okamoto H. Monoclonal antibodies raised against the ORF3 protein of hepatitis E virus (HEV) can capture HEV particles in culture supernatant and serum but not those in feces. Arch. Virol. 2008, 153(9):1703-1713.
66. Tam A.W., Smith M.M., Guerra M.E., Huang C.C., Bradley D.W., Fry K.E., Reyes G.R. Hepatitis E virus (HEV): molecular cloning and sequencing of the full-length viral genome. Virology 1991, 185(1):120-131.
67. Tam A.W., White R., Reed E., Short M., Zhang Y., Fuerst T.R., Lanford R.E. In vitro propagation and production of hepatitis E virus from in vivo-infected primary macaque hepatocytes. Virology 1996, 215(1):1-9.
68. Tam A.W., White R., Yarbough P.O., Murphy B.J., McAtee C.P., Lanford R.E., Fuerst T.R. In vitro infection and replication of hepatitis E virus in primary cynomolgus macaque hepatocytes. Virology 1997, 238(1):94-102.
69. Tanaka T., Takahashi M., Kusano E., Okamoto H. Development and evaluation of an efficient cell-culture system for Hepatitis E virus. J. Gen. Virol. 2007, 88(Pt 3):903-911.
70. Tanaka T., Takahashi M., Takahashi H., Ichiyama K., Hoshino Y., Nagashima S., Mizuo H., Okamoto H. Development and characterization of a genotype 4 hepatitis E virus cell culture system using a HE-JF5/15F strain recovered from a fulminant hepatitis patient. J. Clin. Microbiol. 2009, 47(6):1906-1910.
71. Tei S., Kitajima N., Takahashi K., Mishiro S. Zoonotic transmission of hepatitis E virus from deer to human beings. Lancet 2003, 362(9381):371-373.
72. Torresi J., Li F., Locarnini S.A., Anderson D.A. Only the non-glycosylated fraction of hepatitis E virus capsid (open reading frame 2) protein is stable in mammalian cells. J. Gen. Virol. 1999, 80(Pt 5):1185-1188.
73. Tyagi S., Korkaya H., Zafrullah M., Jameel S., Lal S.K. The phosphorylated form of the ORF3 protein of hepatitis E virus interacts with its non-glycosylated form of the major capsid protein, ORF2. J. Biol. Chem. 2002, 277(25):22759-22767.
74. Tyagi S., Surjit M., Roy A.K., Jameel S., Lal S.K. The ORF3 protein of hepatitis E virus interacts with liver-specific alpha1-microglobulin and its precursor alpha1-microglobulin/bikunin precursor (AMBP) and expedites their export from the hepatocyte. J. Biol. Chem. 2004, 279(28):29308-29319.
75. Wei S., Walsh P., Huang R., To S.S. 93G, a novel sporadic strain of hepatitis E virus in South China isolated by cell culture. J. Med. Virol. 2000, 61(3):311-318.
76. Williams T.P., Kasorndorkbua C., Halbur P.G., Haqshenas G., Guenette D.K., Toth T.E., Meng X.J. Evidence of extrahepatic sites of replication of the hepatitis E virus in a swine model. J. Clin. Microbiol. 2001, 39(9):3040-3046.
77. 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(Pt 8):1880-1891.
78. 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(Pt 2):457-462.
79. Yamashita T., Mori Y., Miyazaki N., Cheng R.H., Yoshimura M., Unno H., Shima R., Moriishi K., Tsukihara T., Li T.C., Takeda N., Miyamura T., Matsuura Y. Biological and immunological characteristics of hepatitis E virus-like particles based on the crystal structure. Proc. Natl. Acad. Sci. U.S.A. 2009, 106(31):12986-12991.
80. Yazaki Y., Mizuo H., Takahashi M., Nishizawa T., Sasaki N., Gotanda Y., Okamoto H. 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. 2003, 84(Pt 9):2351-2357.
81. Zafrullah M., Ozdener M.H., Panda S.K., Jameel S. The ORF3 protein of hepatitis E virus is a phosphoprotein that associates with the cytoskeleton. J. Virol. 1997, 71(12):9045-9053.