Expression of hepatitis C virus (HCV) structural proteins in trans facilitates encapsidation and transmission of HCV subgenomic RNA

Journal of General Virology

Volumn 90, Issue 4, 2009, Pages 833-842

  Adair, Richard ^a   Patel, Arvind H ^a   Corless, Lynsey ^b   Griffin, Stephen ^b   Rowlands, David J ^b   McCormick, Christopher J ^c  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b UNIVERSITY OF LEEDS   (United Kingdom)

^c UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACULOVIRUS VECTOR; GENOMIC RNA; GLYCOPROTEIN E2; NEUTRALIZING ANTIBODY; VIRUS RNA; VIRUS PROTEIN;

ARTICLE; CELL STRAIN; DENSITY GRADIENT; ENCAPSULATION; GENE CONSTRUCT; GENE EXPRESSION; GENETIC TRANSFECTION; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; PROTEIN TARGETING; REPLICON; TISSUE CULTURE; VIROGENESIS; VIRUS ISOLATION; VIRUS NEUTRALIZATION; VIRUS PARTICLE; VIRUS REPLICATION; VIRUS TRANSENCAPSIDATION; VIRUS TRANSMISSION; ANIMAL; ARMYWORM; BACULOVIRUS; CELL CULTURE; GENETIC TRANSDUCTION; GENETICS; METABOLISM; PATHOGENICITY; PHYSIOLOGY; TUMOR CELL LINE; VIRION; VIRUS ASSEMBLY;

HEPATITIS C VIRUS; RNA VIRUSES;

ANIMALS; BACULOVIRIDAE; CELL LINE, TUMOR; CELLS, CULTURED; HEPACIVIRUS; HUMANS; REPLICON; RNA, VIRAL; SPODOPTERA; TRANSDUCTION, GENETIC; VIRAL STRUCTURAL PROTEINS; VIRION; VIRUS ASSEMBLY;

EID: 65549147626     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.2008.006049-0     Document Type: Article

References (43)

1. + T-cell immunity. J Virol 76, 3791-3799.
2. Appel, N., Herian, U. & Bartenschlager, R. (2005). Efficient rescue of hepatitis C virus RNA replication by trans-complementation with nonstructural protein 5A. J Virol 79, 896-909.
3. Appel, N., Zayas, M., Miller, S., Krijnse-Locker, J., Schaller, T., Friebe, P., Kallis, S., Engel, U. & Bartenschlager, R. (2008). Essential role of domain III of nonstructural protein 5A for hepatitis C virus infectious particle assembly. PLoS Pathog 4, e1000035.
4. Blight, K. J., Kolykhalov, A. A. & Rice, C. M. (2000). Efficient initiation of HCV RNA replication in cell culture. Science 290, 1972-1974.
5. Bukh, J., Pietschmann, T., Lohmann, V., Krieger, N., Faulk, K., Engle, R. E., Govindarajan, S., Shapiro, M., St Claire, M. & Bartenschlager, R. (2002). Mutations that permit efficient replication of hepatitis C virus RNA in Huh-7 cells prevent productive replication in chimpanzees. Proc Natl Acad Sci U S A 99, 14416-14421.
6. Clayton, R. F., Owsianka, A., Aitken, J., Graham, S., Bhella, D. & Patel, A. H. (2002). Analysis of antigenicity and topology of E2 glycoprotein present on recombinant hepatitis C virus-like particles. J Virol 76, 7672-7682.
7. Date, T., Kato, T., Miyamoto, M., Zhao, Z., Yasui, K., Mizokami, M. & Wakita, T. (2004). Genotype 2a hepatitis C virus subgenomic replicon can replicate in HepG2 and IMY-N9 cells. J Biol Chem 279, 22371-22376.
8. Day, C. L., Seth, N. P., Lucas, M., Appel, H., Gauthier, L., Lauer, G. M., Robbins, G. K., Szczepiorkowski, Z. M., Casson, D. R. & other authors (2003). Ex vivo analysis of human memory CD4 T cells specific for hepatitis C virus using MHC class II tetramers. J Clin Invest 112, 831-842.
9. Delgrange, D., Pillez, A., Castelain, S., Cocquerel, L., Rouille, Y., Dubuisson, J., Wakita, T., Duverlie, G. & Wychowski, C. (2007). Robust production of infectious viral particles in Huh-7 cells by introducing mutations in hepatitis C virus structural proteins. J Gen Virol 88, 2495-2503.
10. Deutsch, M. & Hadziyannis, S. J. (2008). Old and emerging therapies in chronic hepatitis C: An update. J Viral Hepat 15, 2-11.
11. Fipaldini, C., Bellei, B. & La, M. N. (1999). Expression of hepatitis C virus cDNA in human hepatoma cell line mediated by a hybrid baculovirus-HCV vector. Virology 255, 302-311.
12. Gehrke, R., Ecker, M., Aberle, S. W., Allison, S. L., Heinz, F. X. & Mandl, C. W. (2003). Incorporation of tick-borne encephalitis virus replicons into virus-like particles by a packaging cell line. J Virol 77, 8924-8933.
13. Guiltinan, A. M., Kaidarova, Z., Custer, B., Orland, J., Strollo, A., Cyrus, S., Busch, M. P. & Murphy, E. L. (2008). Increased all-cause, liver, and cardiac mortality among hepatitis C virus-seropositive blood donors. Am J Epidemiol 167, 743-750.
14. Ishii, K., Murakami, K., Hmwe, S. S., Zhang, B., Li, J., Shirakura, M., Morikawa, K., Suzuki, R., Miyamura, T. & other authors (2008). Trans-encapsidation of hepatitis C virus subgenomic replicon RNA with viral structure proteins. Biochem Biophys Res Commun 371, 446-450.
15. Jones, C. T., Patkar, C. G. & Kuhn, R. J. (2005). Construction and applications of yellow fever virus replicons. Virology 331, 247-259.
16. Jones, C. T., Murray, C. L., Eastman, D. K., Tassello, J. & Rice, C. M. (2007). Hepatitis C virus p7 and NS2 proteins are essential for production of infectious virus. J Virol 81, 8374-8383.
17. Kato, T., Date, T., Miyamoto, M., Furusaka, A., Tokushige, K., Mizokami, M. & Wakita, T. (2003). Efficient replication of the genotype 2a hepatitis C virus subgenomic replicon. Gastroenterology 125, 1808-1817.
18. Khromykh, A. A., Varnavski, A. N. & Westaway, E. G. (1998). Encapsidation of the flavivirus Kunjin replicon RNA by using a complementation system providing Kunjin virus structural proteins in trans. J Virol 72, 5967-5977.
19. Koch, J. O. & Bartenschlager, R. (1999). Modulation of hepatitis C virus NS5A hyperphosphorylation by nonstructural proteins NS3, NS4A, and NS4B. J Virol 73, 7138-7146.
20. Krieger, N., Lohmann, V. & Bartenschlager, R. (2001). Enhancement of hepatitis C virus RNA replication by cell culture-adaptive mutations. J Virol 75, 4614-4624.
21. Lauer, G. M., Barnes, E., Lucas, M., Timm, J., Ouchi, K., Kim, A. Y., Day, C. L., Robbins, G. K., Casson, D. R. & other authors (2004). High resolution analysis of cellular immune responses in resolved and persistent hepatitis C virus infection. Gastroenterology 127, 924-936.
22. Lindenbach, B. D., Evans, M. J., Syder, A. J., Wolk, B., Tellinghuisen, T. L., Liu, C. C., Maruyama, T., Hynes, R. O., Burton, D. R. & other authors (2005). Complete replication of hepatitis C virus in cell culture. Science 309, 623-626.
23. Lindenbach, B. D., Meuleman, P., Ploss, A., Vanwolleghem, T., Syder, A. J., McKeating, J. A., Lanford, R. E., Feinstone, S. M., Major, M. E. & other authors (2006). Cell culture-grown hepatitis C virus is infectious in vivo and can be recultured in vitro. Proc Natl Acad Sci U S A 103, 3805-3809.
24. Lohmann, V., Korner, F., Koch, J., Herian, U., Theilmann, L. & Bartenschlager, R. (1999). Replication of subgenomic hepatitis C virus RNAs in a hepatoma cell line. Science 285, 110-113.
25. Lohmann, V., Korner, F., Dobierzewska, A. & Bartenschlager, R. (2001). Mutations in hepatitis C virus RNAs conferring cell culture adaptation. J Virol 75, 1437-1449.
26. Masaki, T., Suzuki, R., Murakami, K., Aizaki, H., Ishii, K., Murayama, A., Date, T., Matsuura, Y., Miyamura, T. & other authors (2008). Interaction of hepatitis C virus nonstructural protein 5A with core protein is critical for the production of infectious virus particles. J Virol 82, 7964-7976.
27. McCormick, C. J., Rowlands, D. J. & Harris, M. (2002). Efficient delivery and regulable expression of hepatitis C virus full-length and minigenome constructs in hepatocyte-derived cell lines using baculovirus vectors. J Gen Virol 83, 383-394.
28. McCormick, C. J., Challinor, L., Macdonald, A., Rowlands, D. J. & Harris, M. (2004). Introduction of replication-competent hepatitis C virus transcripts using a tetracycline-regulable baculovirus delivery system. J Gen Virol 85, 429-439.
29. McCormick, C. J., Brown, D., Griffin, S., Challinor, L., Rowlands, D. J. & Harris, M. (2006). A link between translation of the hepatitis C virus polyprotein and polymerase function; possible consequences for hyperphosphorylation of NS5A. J Gen Virol 87, 93-102.
30. Miyanari, Y., Atsuzawa, K., Usuda, N., Watashi, K., Hishiki, T., Zayas, M., Bartenschlager, R.,Wakita, T., Hijikata,M. & Shimotohno, K. (2007). The lipid droplet is an important organelle for hepatitis C virus production. Nat Cell Biol 9, 1089-1097.
31. Neddermann, P., Clementi, A. & De, F. R. (1999). Hyperphosphorylation of the hepatitis C virus NS5A protein requires an active NS3 protease, NS4A, NS4B, and NS5A encoded on the same polyprotein. J Virol 73, 9984-9991.
32. Owsianka, A., Tarr, A. W., Juttla, V. S., Lavillette, D., Bartosch, B., Cosset, F. L., Ball, J. K. & Patel, A. H. (2005). Monoclonal antibody AP33 defines a broadly neutralizing epitope on the hepatitis C virus E2 envelope glycoprotein. J Virol 79, 11095-11104.
33. Pietschmann, T., Lohmann, V., Kaul, A., Krieger, N., Rinck, G., Rutter, G., Strand, D. & Bartenschlager, R. (2002). Persistent and transient replication of full-length hepatitis C virus genomes in cell culture. J Virol 76, 4008-4021.
34. Pietschmann, T., Kaul, A., Koutsoudakis, G., Shavinskaya, A., Kallis, S., Steinmann, E., Abid, K., Negro, F., Dreux, M. & other authors (2006). Construction and characterization of infectious intragenotypic and intergenotypic hepatitis C virus chimeras. Proc Natl Acad Sci U S A 103, 7408-7413.
35. Pushko, P., Parker, M., Ludwig, G. V., Davis, N. L., Johnston, R. E. & Smith, J. F. (1997). Replicon-helper systems from attenuated Venezuelan equine encephalitis virus: Expression of heterologous genes in vitro and immunization against heterologous pathogens in vivo. Virology 239, 389-401.
36. Steinmann, E., Brohm, C., Kallis, S., Bartenschlager, R. & Pietschmann, T. (2008). Efficient trans-encapsidation of hepatitis C virus RNAs into infectious virus-like particles. J Virol 82, 7034-7046.
37. Stone, A. B. (1974). A simplified method for preparing sucrose gradients. Biochem J 137, 117-118.
38. Suzuki, T., Aizaki, H., Murakami, K., Shoji, I. & Wakita, T. (2007). Molecular biology of hepatitis C virus. J Gastroenterol 42, 411-423.
39. Tarr, A. W., Owsianka, A. M., Timms, J. M., McClure, C. P., Brown, R. J., Hickling, T. P., Pietschmann, T., Bartenschlager, R., Patel, A. H. & Ball, J. K. (2006). Characterization of the hepatitis C virus E2 epitope defined by the broadly neutralizing monoclonal antibody AP33. Hepatology 43, 592-601.
40. Wakita, T., Pietschmann, T., Kato, T., Date, T., Miyamoto, M., Zhao, Z., Murthy, K., Habermann, A., Krausslich, H. G. & other authors (2005). Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat Med 11, 791-796.
41. Yi, M., Ma, Y., Yates, J. & Lemon, S.M. (2007). Compensatory mutations in E1, p7, NS2, and NS3 enhance yields of cell culture-infectious intergenotypic chimeric hepatitis C virus. J Virol 81, 629-638.
42. Zhong, J., Gastaminza, P., Cheng, G., Kapadia, S., Kato, T., Burton, D. R., Wieland, S. F., Uprichard, S. L., Wakita, T. & Chisari, F. V. (2005). Robust hepatitis C virus infection in vitro. Proc Natl Acad Sci U S A 102, 9294-9299.
43. Zhou, X., Berglund, P., Rhodes, G., Parker, S. E., Jondal, M. & Liljestrom, P. (1994). Self-replicating Semliki Forest virus RNA as recombinant vaccine. Vaccine 12, 1510-1514.