Tumour susceptibility gene 101 and the vacuolar protein sorting pathway are required for the release of hepatitis E virions

Journal of General Virology

Volumn 92, Issue 12, 2011, Pages 2838-2848

  Nagashima, Shigeo ^a   Takahashi, Masaharu ^a   Jirintai, Suljid ^a   Tanaka, Toshinori ^a   Nishizawa, Tsutomu ^a   Yasuda, Jiro ^b   Okamoto, Hiroaki ^a  

^a JICHI MEDICAL UNIVERSITY   (Japan)

^b NAGASAKI UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN ORF3; SMALL INTERFERING RNA; TUMOR SUSCEPTIBILITY GENE 101 PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; GENE EXPRESSION; GENETIC TRANSFECTION; HEPATITIS E VIRUS; IMMUNOPRECIPITATION; MULTIVESICULAR BODY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; VIRION; VIRUS RELEASE; WILD TYPE;

BLOTTING, WESTERN; CELLS, CULTURED; DNA-BINDING PROTEINS; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; HEPATITIS E VIRUS; HUMANS; IMMUNOPRECIPITATION; PROTEIN TRANSPORT; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; VACUOLAR PROTON-TRANSLOCATING ATPASES; VACUOLES; VIRAL PROTEINS; VIRION; VIRUS RELEASE;

HEPATITIS E VIRUS;

EID: 81255211998     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.035378-0     Document Type: Article

References (67)

1. Agrawal, S., Gupta, D. & Panda, S. K. (2001). The 39 end of hepatitis E virus (HEV) genome binds specifically to the viral RNA-dependent RNA polymerase (RdRp). Virology 282, 87-101.
2. Ahmad, I., Holla, R. P. & Jameel, S. (2011). Molecular virology of hepatitis E virus. Virus Res 161, 47-58.
3. Ariumi, Y., Kuroki, M., Maki, M., Ikeda, M., Dansako, H., Wakita, T. & Kato, N. (2011). The ESCRT system is required for hepatitis C virus production. PLoS ONE 6, e14517.
4. Babst, M., Wendland, B., Estepa, E. J. & Emr, S. D. (1998). The Vps4p AAA ATPase regulates membrane association of a Vps protein complex required for normal endosome function. EMBO J 17, 2982-2993.
5. Babst, M., Katzmann, D. J., Estepa-Sabal, E. J., Meerloo, T. & Emr, S. D. (2002a). Escrt-III: an endosome-associated heterooligomeric protein complex required for mvb sorting. Dev Cell 3, 271-282.
6. Babst, M., Katzmann, D. J., Snyder, W. B., Wendland, B. & Emr, S. D. (2002b). Endosome-associated complex, ESCRT-II, recruits transport machinery for protein sorting at the multivesicular body. Dev Cell 3, 283-289.
7. Bishop, N. & Woodman, P. (2001). TSG101/mammalian VPS23 and mammalian VPS28 interact directly and are recruited to VPS4- induced endosomes. J Biol Chem 276, 11735-11742.
8. Chandra, V., Taneja, S., Kalia, M. & Jameel, S. (2008). Molecular biology and pathogenesis of hepatitis E virus. J Biosci 33, 451-464.
9. Chen, B. J. & Lamb, R. A. (2008). Mechanisms for enveloped virus budding: can some viruses do without an ESCRT? Virology 372, 221-232.
10. 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.
11. Corless, L., Crump, C. M., Griffin, S. D. & Harris, M. (2010). Vps4 and the ESCRT-III complex are required for the release of infectious hepatitis C virus particles. J Gen Virol 91, 362-372.
12. Crump, C. M., Yates, C. & Minson, T. (2007). Herpes simplex virus type 1 cytoplasmic envelopment requires functional Vps4. J Virol 81, 7380-7387.
13. Dalton, H. R., Bendall, R., Ijaz, S. & Banks, M. (2008). Hepatitis E: an emerging infection in developed countries. Lancet Infect Dis 8, 698-709.
14. Demirov, D. G., Ono, A., Orenstein, J. M. & Freed, E. O. (2002). Overexpression of the N-terminal domain of TSG101 inhibits HIV-1 budding by blocking late domain function. Proc Natl Acad Sci U S A 99, 955-960.
15. Emerson, S. U. & Purcell, R. H. (2007). Hepatitis E virus. In Fields Virology, 5th edn, pp. 3047-3058. Edited by D. M. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman & S. E. Straus. Philadelphia: Lippincott Williams & Wilkins.
16. Emerson, S. U., Nguyen, H. T., Torian, U., Burke, D., Engle, R. & Purcell, R. H. (2010). 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 84, 9059-9069.
17. Fraile-Ramos, A., Pelchen-Matthews, A., Risco, C., Rejas, M. T., Emery, V. C., Hassan-Walker, A. F., Esteban, M. & Marsh, M. (2007). The ESCRT machinery is not required for human cytomegalovirus envelopment. Cell Microbiol 9, 2955-2967.
18. 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., Côté, M. & other authors (2001). Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding. Cell 107, 55-65.
19. Göttlinger, H. G., Dorfman, T., Sodroski, J. G. & Haseltine, W. A. (1991). Effect of mutations affecting the p6 gag protein on human immunodeficiency virus particle release. Proc Natl Acad Sci U S A 88, 3195-3199.
20. 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.
21. Haagsma, E. B., Riezebos-Brilman, A., van den Berg, A. P., Porte, R. J. & Niesters, H. G. (2010). Treatment of chronic hepatitis E in liver transplant recipients with pegylated interferon alpha-2b. Liver Transpl 16, 474-477.
22. Hartlieb, B. & Weissenhorn, W. (2006). Filovirus assembly and budding. Virology 344, 64-70.
23. Huang, M., Orenstein, J. M., Martin, M. A. & Freed, E. O. (1995). p6Gag is required for particle production from full-length human immunodeficiency virus type 1 molecular clones expressing protease. J Virol 69, 6810-6818.
24. Ichiyama, K., Yamada, K., Tanaka, T., Nagashima, S., Jirintai Takahashi, M. & Okamoto, H. (2009). Determination of the 59- terminal sequence of subgenomic RNA of hepatitis E virus strains in cultured cells. Arch Virol 154, 1945-1951.
25. Jayakar, H. R., Jeetendra, E. & Whitt, M. A. (2004). Rhabdovirus assembly and budding. Virus Res 106, 117-132.
26. Jouvenet, N., Neil, S. J., Zhadina, M., Zang, T., Kratovac, Z., Lee, Y., McNatt, M., Hatziioannou, T. & Bieniasz, P. D. (2009). Broadspectrum inhibition of retroviral and filoviral particle release by tetherin. J Virol 83, 1837-1844.
27. Kabrane-Lazizi, Y., Meng, X. J., Purcell, R. H. & Emerson, S. U. (1999). Evidence that the genomic RNA of hepatitis E virus is capped. J Virol 73, 8848-8850.
28. Kaletsky, R. L., Francica, J. R., Agrawal-Gamse, C. & Bates, P. (2009). Tetherin-mediated restriction of filovirus budding is antagonized by the Ebola glycoprotein. Proc Natl Acad Sci U S A 106, 2886-2891.
29. Kamar, N., Rostaing, L., Abravanel, F., Garrouste, C., Lhomme, S., Esposito, L., Basse, G., Cointault, O., Ribes, D. &other authors (2010). Ribavirin therapy inhibits viral replication on patients with chronic hepatitis e virus infection. Gastroenterology 139, 1612-1618.
30. Katzmann, D. J., Babst, M. & Emr, S. D. (2001). Ubiquitin-dependent sorting into the multivesicular body pathway requires the function of a conserved endosomal protein sorting complex, ESCRT-I. Cell 106, 145-155.
31. Katzmann, D. J., Odorizzi, G. & Emr, S. D. (2002). Receptor downregulation and multivesicular-body sorting. Nat Rev Mol Cell Biol 3, 893-905.
32. 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.
33. Lai, C. K., Jeng, K. S., Machida, K. & Lai, M. M. (2010). Hepatitis C virus egress and release depend on endosomal trafficking of core protein. J Virol 84, 11590-11598.
34. Lambert, C., Döring, T. & Prange, R. (2007). Hepatitis B virus maturation is sensitive to functional inhibition of ESCRT-III, Vps4, and gamma 2-adaptin. J Virol 81, 9050-9060.
35. Mansouri, M., Viswanathan, K., Douglas, J. L., Hines, J., Gustin, J., Moses, A. V. & Früh, K. (2009). Molecular mechanism of BST2/ tetherin downregulation by K5/MIR2 of Kaposi's sarcoma-associated herpesvirus. J Virol 83, 9672-9681.
36. Martin-Serrano, J., Zang, T. & Bieniasz, P. D. (2001). HIV-1 and Ebola virus encode small peptide motifs that recruit Tsg101 to sites of particle assembly to facilitate egress. Nat Med 7, 1313-1319.
37. Martin-Serrano, J., Yarovoy, A., Perez-Caballero, D. & Bieniasz, P. D. (2003a). Divergent retroviral late-budding domains recruit vacuolar protein sorting factors by using alternative adaptor proteins. Proc Natl Acad Sci U S A 100, 12414-12419.
38. Martin-Serrano, J., Zang, T. & Bieniasz, P. D. (2003b). Role of ESCRT-I in retroviral budding. J Virol 77, 4794-4804.
39. 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.
40. Nagashima, S., Takahashi, M., Jirintai Tanaka, T., Yamada, K., Nishizawa, T. & Okamoto, H. (2011). A PSAP motif in the ORF3 protein of hepatitis E virus is necessary for virion release from infected cells. J Gen Virol 92, 269-278.
41. Neil, S. J., Zang, T. & Bieniasz, P. D. (2008). Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451, 425-430.
42. Okamoto, H. (2007). Genetic variability and evolution of hepatitis E virus. Virus Res 127, 216-228.
43. Pincetic, A., Medina, G., Carter, C. & Leis, J. (2008). Avian sarcoma virus and human immunodeficiency virus, type 1 use different subsets of ESCRT proteins to facilitate the budding process. J Biol Chem 283, 29822-29830.
44. Pornillos, O., Alam, S. L., Davis, D. R. & Sundquist, W. I. (2002). Structure of the Tsg101 UEV domain in complex with the PTAP motif of the HIV-1 p6 protein. Nat Struct Biol 9, 812-817.
45. Purcell, R. H. & Emerson, S. U. (2008). Hepatitis E: an emerging awareness of an old disease. J Hepatol 48, 494-503.
46. Sakuma, T., Noda, T., Urata, S., Kawaoka, Y. & Yasuda, J. (2009). Inhibition of Lassa and Marburg virus production by tetherin. J Virol 83, 2382-2385.
47. Strack, B., Calistri, A., Craig, S., Popova, E. & Göttlinger, H. G. (2003). AIP1/ALIX is a binding partner for HIV-1 p6 and EIAV p9 functioning in virus budding. Cell 114, 689-699.
48. Surjit, M., Oberoi, R., Kumar, R. & Lal, S. K. (2006). Enhanced alpha1 microglobulin secretion from hepatitis E virus ORF3-expressing human hepatoma cells is mediated by the tumor susceptibility gene 101. J Biol Chem 281, 8135-8142.
49. Takahashi, M., Hoshino, Y., Tanaka, T., Takahashi, H., Nishizawa, T. & Okamoto, H. (2008a). Production of monoclonal antibodies against hepatitis E virus capsid protein and evaluation of their neutralizing activity in a cell culture system. Arch Virol 153, 657-666.
50. Takahashi, M., Yamada, K., Hoshino, Y., Takahashi, H., Ichiyama, K., Tanaka, T. & Okamoto, H. (2008b). 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.
51. Takahashi, M., Tanaka, T., Takahashi, H., Hoshino, Y., Nagashima, S., Jirintai Mizuo, H., Yazaki, Y., Takagi, T. & other authors (2010). 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 48, 1112-1125.
52. 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.
53. Tanaka, T., Takahashi, M., Kusano, E. & Okamoto, H. (2007). Development and evaluation of an efficient cell-culture system for hepatitis E virus. J Gen Virol 88, 903-911.
54. Tanzi, G. O., Piefer, A. J. & Bates, P. (2003). Equine infectious anemia virus utilizes host vesicular protein sorting machinery during particle release. J Virol 77, 8440-8447.
55. Tei, S., Kitajima, N., Takahashi, K. & Mishiro, S. (2003). Zoonotic transmission of hepatitis E virus from deer to human beings. Lancet 362, 371-373.
56. Urata, S., Noda, T., Kawaoka, Y., Yokosawa, H. & Yasuda, J. (2006). Cellular factors required for Lassa virus budding. J Virol 80, 4191-4195.
57. Urata, S., Yokosawa, H. & Yasuda, J. (2007). Regulation of HTLV-1 Gag budding by Vps4A, Vps4B, and AIP1/Alix. Virol J 4, 66.
58. Van Damme, N., Goff, D., Katsura, C., Jorgenson, R. L., Mitchell, R., Johnson, M. C., Stephens, E. B. & Guatelli, J. (2008). The interferoninduced protein BST-2 restricts HIV-1 release and is downregulated from the cell surface by the viral Vpu protein. Cell Host Microbe 3, 245-252.
59. VerPlank, L., Bouamr, F., LaGrassa, T. J., Agresta, B., Kikonyogo, A., Leis, J. & Carter, C. A. (2001). Tsg101, a homologue of ubiquitinconjugating (E2) enzymes, binds the L domain in HIV type 1 Pr55(Gag). Proc Natl Acad Sci U S A 98, 7724-7729.
60. von Schwedler, U. K., Stuchell, M., Müller, B., Ward, D. M., Chung, H. Y., Morita, E., Wang, H. E., Davis, T., He, G. P. & other authors (2003). The protein network of HIV budding. Cell 114, 701-713.
61. Watanabe, T., Sorensen, E. M., Naito, A., Schott, M., Kim, S. & Ahlquist, P. (2007). Involvement of host cellular multivesicular body functions in hepatitis B virus budding. Proc Natl Acad Sci U S A 104, 10205-10210.
62. Wills, J. W. & Craven, R. C. (1991). Form, function, and use of retroviral gag proteins. AIDS 5, 639-654.
63. Yamada, K., Takahashi, M., Hoshino, Y., Takahashi, H., Ichiyama, K., Nagashima, S., Tanaka, T. & Okamoto, H. (2009a). ORF3 protein of hepatitis E virus is essential for virion release from infected cells. J Gen Virol 90, 1880-1891.
64. Yamada, K., Takahashi, M., Hoshino, Y., Takahashi, H., Ichiyama, K., Tanaka, T. & Okamoto, H. (2009b). Construction of an infectious cDNA clone of hepatitis E virus strain JE03-1760F that can propagate efficiently in cultured cells. J Gen Virol 90, 457-462.
65. Yasuda, J. & Hunter, E. (1998). A proline-rich motif (PPPY) in the Gag polyprotein of Mason-Pfizer monkey virus plays a maturationindependent role in virion release. J Virol 72, 4095-4103.
66. Yasuda, J., Nakao, M., Kawaoka, Y. & Shida, H. (2003). Nedd4 regulates egress of Ebola virus-like particles from host cells. J Virol 77, 9987-9992.
67. Yazaki, Y., Mizuo, H., Takahashi, M., Nishizawa, T., Sasaki, N., Gotanda, Y. & Okamoto, H. (2003). 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 84, 2351-2357.