Direct visualization of hepatitis C virus-infected Huh7.5 cells with a high titre of infectious chimeric JFH1-EGFP reporter virus in three-dimensional Matrigel cell cultures

Journal of General Virology

Volumn 95, Issue PART 2, 2014, Pages 423-433

  Liu, Shuanghu ^a   Chen, Ren ^a   Hagedorn, Curt H ^a,b  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRUS AGENT; ENHANCED GREEN FLUORESCENT PROTEIN; MATRIGEL; NONSTRUCTURAL PROTEIN 4B; NONSTRUCTURAL PROTEIN 5A; PROTEIN E2; PROTEIN P7; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANTIVIRAL ACTIVITY; ARTICLE; CELL CULTURE; CONTROLLED STUDY; EVOLUTIONARY ADAPTATION; HEPATITIS C VIRUS; HEPATOMA CELL; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; MUTANT; PRIORITY JOURNAL; PROTEIN EXPRESSION; THREE DIMENSIONAL IMAGING; VIRUS ASSEMBLY; VIRUS CULTURE; VIRUS PARTICLE; VIRUS RELEASE; VIRUS REPLICATION; VIRUS TITRATION;

CELL CULTURE TECHNIQUES; CELL LINE; COLLAGEN; DRUG COMBINATIONS; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; HEPACIVIRUS; HEPATOCYTES; HUMANS; LAMININ; MOLECULAR SEQUENCE DATA; PROTEOGLYCANS; RECOMBINANT FUSION PROTEINS; RNA, VIRAL; SEQUENCE ANALYSIS, DNA; STAINING AND LABELING; VIRAL LOAD; VIRAL NONSTRUCTURAL PROTEINS; VIROLOGY;

EID: 84892572200     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.055772-0     Document Type: Article

References (42)

1. Aizaki, H., Morikawa, K., Fukasawa, M., Hara, H., Inoue, Y., Tani, H., Saito, K., Nishijima, M., Hanada, K. & other authors (2008). Critical role of virion-associated cholesterol and sphingolipid in hepatitis C virus infection. J Virol 82, 5715-5724.
2. Alter, H. J. & Seeff, L. B. (2000). Recovery, persistence, and sequelae in hepatitis C virus infection: a perspective on long-term outcome. Semin Liver Dis 20, 17-35.
3. Appel, N., Pietschmann, T. & Bartenschlager, R. (2005). Mutational analysis of hepatitis C virus nonstructural protein 5A: potential role of differential phosphorylation in RNA replication and identification of a genetically flexible domain. J Virol 79, 3187-3194.
4. Bialek, S. R. & Terrault, N. A. (2006). The changing epidemiology and natural history of hepatitis C virus infection. Clin Liver Dis 10, 697-715.
5. Blight, K. J., McKeating, J. A. & Rice, C. M. (2002). Highly permissive cell lines for subgenomic and genomic hepatitis C virus RNA replication. J Virol 76, 13001-13014.
6. Bowen, D. G. & Walker, C. M. (2005). Adaptive immune responses in acute and chronic hepatitis C virus infection. Nature 436, 946-952.
7. Brass, V., Bieck, E., Montserret, R., Wölk, B., Hellings, J. A., Blum, H. E., Penin, F. & Moradpour, D. (2002). An amino-terminal amphipathic alpha-helix mediates membrane association of the hepatitis C virus nonstructural protein 5A. J Biol Chem 277, 8130-8139.
8. Cai, Z., Zhang, C., Chang, K. S., Jiang, J., Ahn, B. C., Wakita, T., Liang, T. J. & Luo, G. (2005). Robust production of infectious hepatitis C virus (HCV) from stably HCV cDNA-transfected human hepatoma cells. J Virol 79, 13963-13973.
9. Eldrup, A. B., Allerson, C. R., Bennett, C. F., Bera, S., Bhat, B., Bhat, N., Bosserman, M. R., Brooks, J., Burlein, C. & other authors (2004). Structure-activity relationship of purine ribonucleosides for inhibition of hepatitis C virus RNA-dependent RNA polymerase. J Med Chem 47, 2283-2295.
10. Evans, M. J., Rice, C. M. & Goff, S. P. (2004). Phosphorylation of hepatitis C virus nonstructural protein 5A modulates its protein interactions and viral RNA replication. Proc Natl Acad Sci U S A 101, 13038-13043.
11. Fried, M. W., Shiffman, M. L., Reddy, K. R., Smith, C., Marinos, G., Gonçales, F. L., Jr, Häussinger, D., Diago, M., Carosi, G. & other authors (2002). Peginterferon alfa-2a plus ribavirin for chronic hepatitis C virus infection. N Engl J Med 347, 975-982.
12. Guo, J. T., Bichko, V. V. & Seeger, C. (2001). Effect of alpha interferon on the hepatitis C virus replicon. J Virol 75, 8516-8523.
13. Härmä, V., Virtanen, J., Mäkelä, R., Happonen, A., Mpindi, J. P., Knuuttila, M., Kohonen, P., Lötjönen, J., Kallioniemi, O. & Nees, M. (2010). A comprehensive panel of three-dimensional models for studies of prostate cancer growth, invasion and drug responses. PLoS ONE 5, e10431.
14. Houghton, M. & Abrignani, S. (2005). Prospects for a vaccine against the hepatitis C virus. Nature 436, 961-966.
15. Inchauspe, G., Zebedee, S., Lee, D. H., Sugitani, M., Nasoff, M. & Prince, A. M. (1991). Genomic structure of the human prototype strain H of hepatitis C virus: comparison with American and Japanese isolates. Proc Natl Acad Sci U S A 88, 10292-10296.
16. Jiang, J. & Luo, G. (2012). Cell culture-adaptive mutations promote viral protein-protein interactions and morphogenesis of infectious hepatitis C virus. J Virol 86, 8987-8997.
17. 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.
18. Kato, T., Furusaka, A., Miyamoto, M., Date, T., Yasui, K., Hiramoto, J., Nagayama, K., Tanaka, T. & Wakita, T. (2001). Sequence analysis of hepatitis C virus isolated from a fulminant hepatitis patient. J Med Virol 64, 334-339.
19. Kaul, A., Woerz, I., Meuleman, P., Leroux-Roels, G. & Bartenschlager, R. (2007). Cell culture adaptation of hepatitis C virus and in vivo viability of an adapted variant. J Virol 81, 13168-13179.
20. Kim, C. S., Jung, J. H., Wakita, T., Yoon, S. K. & Jang, S. K. (2007). Monitoring the antiviral effect of alpha interferon on individual cells. J Virol 81, 8814-8820.
21. Kim, C. S., Keum, S. J. & Jang, S. K. (2011). Generation of a cell culture-adapted hepatitis C virus with longer half life at physiological temperature. PLoS ONE 6, e22808.
22. Kleinman, H. K. & Martin, G. R. (2005). Matrigel: basement membrane matrix with biological activity. Semin Cancer Biol 15, 378-386.
23. Koutsoudakis, G., Kaul, A., Steinmann, E., Kallis, S., Lohmann, V., Pietschmann, T. & Bartenschlager, R. (2006). Characterization of the early steps of hepatitis C virus infection by using luciferase reporter viruses. J Virol 80, 5308-5320.
24. Krieger, N., Lohmann, V. & Bartenschlager, R. (2001). Enhancement of hepatitis C virus RNA replication by cell culture-adaptive mutations. J Virol 75, 4614-4624.
25. Li, Y. P., Ramirez, S., Jensen, S. B., Purcell, R. H., Gottwein, J. M. & Bukh, J. (2012). Highly efficient full-length hepatitis C virus genotype 1 (strain TN) infectious culture system. Proc Natl Acad Sci U S A 109, 19757-19762.
26. Lindenbach, B. D., Evans, M. J., Syder, A. J., Wölk, 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.
27. Liu, S., Nelson, C. A., Xiao, L., Lu, L., Seth, P. P., Davis, D. R. & Hagedorn, C. H. (2011). Measuring antiviral activity of benzimidazole molecules that alter IRES RNA structure with an infectious hepatitis C virus chimera expressing Renilla luciferase. Antiviral Res 89, 54-63.
28. Liu, S., Xiao, L., Nelson, C. & Hagedorn, C. H. (2012). A cell culture adapted HCV JFH1 variant that increases viral titers and permits the production of high titer infectious chimeric reporter viruses. PLoS ONE 7, e44965.
29. 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.
30. Molina-Jimenez, F., Benedicto, I., Dao Thi, V. L., Gondar, V., Lavillette, D., Marin, J. J., Briz, O., Moreno-Otero, R., Aldabe, R. & other authors (2012). Matrigel-embedded 3D culture of Huh-7 cells as a hepatocytelike polarized systemto study hepatitis C virus cycle. Virology 425, 31-39.
31. Moradpour, D., Penin, F. & Rice, C. M. (2007). Replication of hepatitis C virus. Nat Rev Microbiol 5, 453-463.
32. Papic, N., Maxwell, C. I., Delker, D. A., Liu, S., Heale, B. S. & Hagedorn, C. H. (2012). RNA-sequencing analysis of 59 capped RNAs identifies many new differentially expressed genes in acute hepatitis C virus infection. Viruses 4, 581-612.
33. Penin, F., Dubuisson, J., Rey, F. A., Moradpour, D. & Pawlotsky, J. M. (2004). Structural biology of hepatitis C virus. Hepatology 39, 5-19.
34. Phan, T., Beran, R. K., Peters, C., Lorenz, I. C. & Lindenbach, B. D. (2009). Hepatitis C virus NS2 protein contributes to virus particle assembly via opposing epistatic interactions with the E1-E2 glycoprotein and NS3-NS4A enzyme complexes. J Virol 83, 8379-8395.
35. Reed, K. E. & Rice, C. M. (2000). Overview of hepatitis C virus genome structure, polyprotein processing, and protein properties. Curr Top Microbiol Immunol 242, 55-84.
36. Sainz, B., Jr, TenCate, V. & Uprichard, S. L. (2009). Threedimensional Huh7 cell culture system for the study of Hepatitis C virus infection. Virol J 6, 103.
37. Tellinghuisen, T. L., Marcotrigiano, J., Gorbalenya, A. E. & Rice, C. M. (2004). The NS5A protein of hepatitis C virus is a zinc metalloprotein. J Biol Chem 279, 48576-48587.
38. Tellinghuisen, T. L., Marcotrigiano, J. & Rice, C. M. (2005). Structure of the zinc-binding domain of an essential component of the hepatitis C virus replicase. Nature 435, 374-379.
39. Tscherne, D. M., Jones, C. T., Evans, M. J., Lindenbach, B. D., McKeating, J. A. & Rice, C. M. (2006). Time-and temperaturedependent activation of hepatitis C virus for low-pH-triggered entry. J Virol 80, 1734-1741.
40. Wakita, T., Pietschmann, T., Kato, T., Date, T., Miyamoto, M., Zhao, Z., Murthy, K., Habermann, A., Kräusslich, 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 cultureinfectious 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.