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

Journal of Virology

Volumn 84, Issue 18, 2010, Pages 9059-9069

  Emerson, Suzanne U ^a   Nguyen, Hanh T ^a   Torian, Udana ^a   Burke, Danielle ^a   Engle, Ronald ^a   Purcell, Robert H ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; EPITOPE; OPEN READING FRAME 3 PROTEIN; UNCLASSIFIED DRUG; ORF3 PROTEIN, HEPATITIS E VIRUS; VIRUS PROTEIN;

APICAL MEMBRANE; ARTICLE; CELL CULTURE; CELL STRAIN CACO 2; CONFOCAL MICROSCOPY; CONTROLLED STUDY; COPY NUMBER VARIATION; GENETIC TRANSFECTION; GENOTYPE; HEPATITIS E VIRUS; HEPATOMA CELL; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN MOTIF; RNA REPLICATION; SEQUENCE HOMOLOGY; VIRION; VIRUS PARTICLE; VIRUS REPLICATION; ANIMAL; CELL LINE; EPITHELIUM CELL; GENETICS; HEPATITIS E; LIVER CELL; MONKEY DISEASE; PATHOGENICITY; PHYSIOLOGY; RHESUS MONKEY; VIROLOGY; VIRUS RELEASE;

ANIMALS; CELL LINE; EPITHELIAL CELLS; HEPATITIS E; HEPATITIS E VIRUS; HEPATOCYTES; HUMANS; MACACA MULATTA; MONKEY DISEASES; VIRAL PROTEINS; VIRUS RELEASE;

EID: 77956033632     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00593-10     Document Type: Article

References (32)

1. Billam, P., F. W. Pierson, W. Li, T. LeRoith, R. B. Duncan, and X. J. Meng. 2008. Development and validation of a negative-strand-specific reverse transcription-PCR assay for detection of a chicken strain of hepatitis E virus: identification of nonliver replication sites. J. Clin. Microbiol. 46:2630-2634.
2. Blank, C. A., D. A. Anderson, M. Beard, and S. M. Lemon. 2000. Infection of polarized cultures of human intestinal epithelial cells with hepatitis A virus: vectorial release of progeny virions through apical cellular membranes. J. Virol. 74:6476-6484.
3. Chandra, V., A. Kar-Roy, S. Kumari, S. Mayor, and S. Jameel. 2008. The hepatitis E virus ORF3 protein modulates epidermal growth factor receptor trafficking, STAT3 translocation, and the acute-phase response. J. Virol. 82:7100-7110. (Pubitemid 351977728)
4. Emerson, S. U., D. Anderson, V. Arankalle, X. J. Meng, M. Purdy, G. G. Schlauder, and S. A. Tsarev. 2004. Hepevirus, p. 853-857. In C. M. Fauquet, M. A. Mayo, J. Maniloff, U. Desselberger, and L. A. Ball (ed.), Virus taxonomy: classification and nomenclature of viruses. Eighth report of the International Committee on Taxonomy of Viruses. Elsevier/Academic Press, London, United Kingdom.
5. Emerson, S. U., H. Nguyen, J. Graff, D. Stephany, A. Brockington, and R. H. Purcell. 2004. In vitro replication of hepatitis E virus (HEV) genomes and of an HEV replicon expressing green fluorescent protein. J. Virol. 78:4838-4846.
6. Emerson, S. U., H. Nguyen, U. Torian, and R. H. Purcell. 2006. ORF3 protein of hepatitis E virus is not required for replication, virion assembly, or infection of hepatoma cells in vitro. J. Virol. 80:10457-10464.
7. Emerson, S. U., and R. H. Purcell. 2007. Hepatitis E virus, P. 3047-3058. In D. M. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman, and S. E. Straus (ed.), Fields virology, 5th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
8. Emerson, S. U., M. Zhang, X. J. Meng, H. Nguyen, M. St. Claire, S. Govindarajan, Y. K. Huang, and R. H. Purcell. 2001. Recombinant hepatitis E virus genomes infectious for primates: importance of capping and discovery of a cis-reactive element. Proc. Natl. Acad. Sci. U. S. A. 98:15270-15275.
9. Graff, J., H. Nguyen, C. Yu, W. R. Elkins, M. St. Claire, R. H. Purcell, and S. U. Emerson. 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.
10. Graff, J., U. Torian, H. Nguyen, and S. U. Emerson. 2006. A bicistronic subgenomic mRNA encodes both the ORF2 and ORF3 proteins of hepatitis E virus. J. Virol. 80:5919-5926.
11. Guu, T. S., Z. Liu, Q. Ye, D. A. Mata, K. Li, C. Yin, J. Zhang, and Y. J. Tao. 2009. Structure of the hepatitis E virus-like particle suggests mechanisms for virus assembly and receptor binding. Proc. Natl. Acad. Sci. U. S. A. 106:12992-12997.
12. Huang, Y. W., T. Opressnig, P. G. Halbur, and X. J. Meng. 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.
13. Kannan, H., S. Fan, D. Patel, I. Bossis, and Y.-J. Zhang. 2009. The hepatitis E virus open reading frame 3 product interacts with microtubules and interferes with their dynamics. J. Virol. 83:6375-6382.
14. Korkaya, H., S. Jameel, D. Gupta, S. Tyagi, R. Kumar, M. Zafrullah, M. Mazumdar, S. K. Lal, L. Xiaofang, D. Sehgal, S. R. Das, and D. Sahal. 2001. The ORF3 protein of hepatitis E virus binds to Src homology 3 domains and activates MAPK. J. Biol. Chem. 276:42389-42400.
15. Li, S., X. Tang, J. Seetharaman, C. Yang, Y. Gu, J. Zhang, H. Du, J. W. Shih, C. L. Hew, J. X. Sivaraman, and N. Xia. 2009. Dimerization of hepatitis E virus capsid protein E2s domain is essential for virus-host interaction. PLoS Pathog. 5:e1000537.
16. Meng, X. J. 2010. Recent advances in hepatitis E virus. J. Viral Hepat. 17:153-161.
17. Moin, S. M., V. Chandra, R. Arya, and S. Jameel. 2009. The hepatitis E virus ORF3 protein stabilizes HIF-1α and enhances HIF-1-mediated transcriptional activity through p300/CBP. Cell. Microbiol. 11:1409-1421.
18. Moin, S. M., M. Panteva, and S. Jameel. 2007. The hepatitis E virus ORF3 protein protects cells from mitochondrial depolarization and death. J. Biol. Chem. 282:21124-21133.
19. Nakabayashi, H., K. Taketa, K. Miyano, T. Yamane, and J. Sato. 1982. Growth of human hepatoma cell lines with differentiated functions in chemically defined medium. Cancer Res. 42:3858-38563.
20. National Research Council. 1996. Guide for the care and use of laboratory animals. National Academy Press, Washington, DC.
21. Ratra, R., A. Kar-Roy, and S. K. Lal. 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.
22. Takahashi, M., K. Yamada, Y. Hoshino, H. Takahashi, K. Ichiyama, T. Tanaka, and H. Okamoto. 2008. 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. 153:1703-1713.
23. Tanaka, T., M. Takahashi, E. Kusano, and H. Okamoto. 2007. Development and evaluation of an efficient cell-culture system for hepatitis E virus. J. Gen. Virol. 88:903-911.
24. Tanaka, T., M. Takahashi, H. Takahashi, K. Ichiyama, Y. Hoshino, S. Nagashima, H. Mizuo, and H. Okamoto. 2009. 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. 47:1906-1910.
25. Tei, S., N. Kitajima, K. Takahashi, and S. Mishiro. 2003. Zoonotic transmission of hepatitis E virus from deer to human beings. Lancet 362:371-373.
26. Tyagi, S., H. Korkaya, M. Zafrullah, S. Jameel, and S. K. Lal. 2002. 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. 277:22759-22767.
27. Tyagi, S., M. Surjit, and S. K. Lal. 2005. The 41-amino-acid C-terminal region of the hepatitis E. virus ORF3 protein interacts with bikunin, a Kunitz-type serine protease inhibitor. J. Virol. 79:12081-12087.
28. Wang, C. Y., N. Miyazaki, T. Yamashita, A. Higashiura, A. Nakagawa, T. C. Li, L. Xing, E. Hjalmarsson, C. Friberg, D. M. Liou, Y. J. Sung, T. Tsukihara, Y. Matsuura, T. Miyamura, and R. H. Cheng. 2008. Crystallization and preliminary X-ray diffraction analysis of recombinant hepatitis E virus-like particle. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 64:318-322.
29. Williams, T. P., C. Kasorndorkbua, P. G. Halbur, G. Haqshenas, D. K. Guenette, T. E. Toth, and X. J. Meng. 2001. Evidence of extrahepatic sites of replication of the hepatitis E virus in a swine model. J. Clin. Microbiol. 39:3040-3046.
30. Yamada, K., M. Takahashi, Y. Hoshino, H. Takahashi, K. Ichiyama, S. Nagashima, T. Tanaka, and H. Okamoto. 2009. ORF3 protein of hepatitis E virus is essential for virion release from infected cells. J. Gen. Virol. 90:1880-1891.
31. Yamashita, T., Y. Mori, N. Miyazaki, R. H. Cheng, M. Yoshimura, H. Unno, R. Shima, K. Moriishi, T. Tsukihara, T. C. Li, N. Takeda, T. Miyamura, and Y. Matsuura. 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.
32. Zhao, C., Z. Ma, T. J. Harrison, R. Feng, C. Zhang, Z. Qiao, J. Fan, H. Ma, M. Li, A. Song, and Y. Wang. 2009. A novel genotype of hepatitis E virus prevalent among farmed rabbits in China. J. Med. Virol. 81:1371-1379.