Replication of the hepatitis C virus in cell culture

Antiviral Research

Volumn 60, Issue 2, 2003, Pages 91-102

  Bartenschlager, Ralf ^a   Kaul, Artur ^a   Sparacio, Sandra ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Adaptation; Antiviral therapy; Cell culture; Flaviviridae; HCV; Hepatitis C virus; Interferon alpha; Positive strand RNA virus; Replicons; RNA replication

Indexed keywords

ALPHA INTERFERON; ANTIVIRUS AGENT; GENOMIC RNA; STRUCTURAL PROTEIN;

CELL CULTURE; CELL LINE; CONFERENCE PAPER; FLAVIVIRUS; GENE IDENTIFICATION; GENETIC ENGINEERING; HEPATITIS C; HEPATITIS C VIRUS; HEPATOMA CELL; HOST CELL; HUMAN; PRIORITY JOURNAL; REPLICON; RNA REPLICATION; VIRUS MUTATION; VIRUS REPLICATION;

FLAVIVIRIDAE; HEPATITIS C VIRUS; RNA VIRUSES;

EID: 0344443242     PISSN: 01663542     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.antiviral.2003.08.016     Document Type: Conference Paper

References (95)

1. Ali N., Tardif K.D., Siddiqui A. Cell-free replication of the hepatitis C virus subgenomic replicon. J. Virol. 76:2002;12001-12007.
2. Asabe S.I., Tanji Y., Satoh S., Kaneko T., Kimura K., Shimotohno K. The N-terminal region of hepatitis C virus-encoded NS5A is important for NS4A-dependent phosphorylation. J. Virol. 71:1997;790-796.
3. Bartenschlager R., Lohmann V. Replication of hepatitis C virus. J. Gen. Virol. 81:2000;1631-1648.
4. Bartenschlager R., Ahlborn-Laake L., Mous J., Jacobsen H. Kinetic and structural analyses of hepatitis C virus polyprotein processing. J. Virol. 68:1994;5045-5055.
5. Bartenschlager R., Lohmann V., Wilkinson T., Koch J.O. Complex formation between the NS3 serine-type proteinase of the hepatitis C virus and NS4A and its importance for polyprotein maturation. J. Virol. 69:1995;7519-7528.
6. Beard M.R., Abell G., Honda M., Carroll A., Gartland M., Clarke B., Suzuki K., Lanford R., Sangar D.V., Lemon S.M. An infectious molecular clone of a Japanese genotype 1b hepatitis C virus. Hepatology. 30:1999;316-324.
7. Behrens S.E., Tomei L., De Francesco R. Identification and properties of the RNA-dependent RNA polymerase of hepatitis C virus. EMBO J. 15:1996;12-22.
8. Bienz K., Egger D., Pfister T., Troxler M. Structural and functional characterization of the poliovirus replication complex. J. Virol. 66:1992;2740-2747.
9. Blajchman M.A., Bull S.B., Feinman S.V. Post-transfusion hepatitis: impact of non-A, non-B hepatitis surrogate tests. Canadian Post-Transfusion Hepatitis Prevention Study Group. Lancet. 345:1995;21-25.
10. Blight K.J., Kolykhalov A.A., Rice C.M. Efficient initiation of HCV RNA replication in cell culture. Science. 290:2000;1972-1974.
11. Blight K.J., McKeating J.A., Rice C.M. Highly permissive cell lines for subgenomic and genomic hepatitis C virus RNA replication. J. Virol. 76:2002;13001-13014.
12. Blight K.J., McKeating J.A., Marcotrigiano J., Rice C.M. Efficient replication of hepatitis C virus genotype 1a RNAs in cell culture. J. Virol. 77:2003;3181-3190.
13. Bost A.G., Venable D., Liu L., Heinz B.A. Cytoskeletal requirements for hepatitis C virus (HCV) RNA synthesis in the HCV replicon cell culture system. J. Virol. 77:2003;4401-4408.
14. Bukh J., Pietschmann T., Lohmann V., Krieger N., Faulk K., Engle R.E., Govindarajan S., Shapiro M., St. Claire M., Bartenschlager R. 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. 99:2002;14416-14421.
15. Choo Q.L., Kuo G., Weiner A.J., Overby L.R., Bradley D.W., Houghton M. Isolation of a cDNA clone derived from a blood-borne non-A, non-B viral hepatitis genome. Science. 244:1989;359-362.
16. Chu P.W., Westaway E.G. Molecular and ultrastructural analysis of heavy membrane fractions associated with the replication of Kunjin virus RNA. Arch. Virol. 125:1992;177-191.
17. De Tomassi A., Pizzuti M., Graziani R., Sbardellati A., Altamura S., Paonessa G., Traboni C. Cell clones selected from the Huh7 human hepatoma cell line support efficient replication of a subgenomic GB virus B replicon. J. Virol. 76:2002;7736-7746.
18. Donahue J.G., Munoz A., Ness P.M., Brown D.E. Jr., Yawn D.H., McAllister H.A. Jr., Reitz B.A., Nelson K.E. The declining risk of post-transfusion hepatitis C virus infection. N. Engl. J. Med. 327:1992;369-373.
19. Egger D., Wolk B., Gosert R., Bianchi L., Blum H.E., Moradpour D., Bienz K. Expression of hepatitis C virus proteins induces distinct membrane alterations including a candidate viral replication complex. J. Virol. 76:2002;5974-5984.
20. Failla C., Tomei L., De Francesco R. Both NS3 and NS4A are required for proteolytic processing of hepatitis C virus nonstructural proteins. J. Virol. 68:1994;3753-3760.
21. Frese M., Pietschmann T., Moradpour D., Haller O., Bartenschlager R. Interferon-alpha inhibits hepatitis C virus subgenomic RNA replication by an MxA-independent pathway. J. Gen. Virol. 82:2001;723-733.
22. Frese M., Schwarzle V., Barth K., Krieger N., Lohmann V., Mihm S., Haller O., Bartenschlager R. Interferon-gamma inhibits replication of subgenomic and genomic hepatitis C virus RNAs. Hepatology. 35:2002;694-703.
23. Friebe P., Bartenschlager R. Genetic analysis of sequences in the 3′ nontranslated region of hepatitis C virus that are important for RNA replication. J. Virol. 76:2002;5326-5338.
24. Friebe P., Lohmann V., Krieger N., Bartenschlager R. Sequences in the 5′ nontranslated region of hepatitis C virus required for RNA replication. J. Virol. 75:2001;12047-12057.
25. Gale M. Jr., Korth M.J., Tang N.M., Tan S.L., Hopkins D.A., Dever T.E., Polyak S.J., Gretch D.R., Katze M.G. Evidence that hepatitis C virus resistance to interferon is mediated through repression of the PKR protein kinase by the nonstructural 5A protein. Virology. 230:1997;217-227.
26. Gale M. Jr., Blakely C.M., Kwieciszewski B., Tan S.L., Dossett M., Tang N.M., Korth M.J., Polyak S.J., Gretch D.R., Katze M.G. Control of PKR protein kinase by hepatitis C virus nonstructural 5A protein: molecular mechanisms of kinase regulation. Mol. Cell. Biol. 18:1998;5208-5218.
27. Giannini C., Brechot C. Hepatitis C virus biology. Cell Death Differ. 10(Suppl. 1):2003;S27-S38.
28. Gosert R., Egger D., Lohmann V., Bartenschlager R., Blum H.E., Bienz K., Moradpour D. Identification of the hepatitis C virus RNA replication complex in huh-7 cells harboring subgenomic replicons. J. Virol. 77:2003;5487-5492.
29. Grakoui A., McCourt D.W., Wychowski C., Feinstone S.M., Rice C.M. A second hepatitis C virus-encoded proteinase. Proc. Natl. Acad. Sci. U.S.A. 90:1993;10583-10587.
30. Griffin S.D., Beales L.P., Clarke D.S., Worsfold O., Evans S.D., Jaeger J., Harris M.P., Rowlands D.J. The p7 protein of hepatitis C virus forms an ion channel that is blocked by the antiviral drug, Amantadine. FEBS Lett. 535:2003;34-38.
31. Guo J.T., Bichko V.V., Seeger C. Effect of alpha interferon on the hepatitis C virus replicon. J. Virol. 75:2001;8516-8523.
32. Gwack Y., Kim D.W., Han J.H., Choe J. Characterization of RNA binding activity and RNA helicase activity of the hepatitis C virus NS3 protein. Biochem. Biophys. Res. Commun. 225:1996;654-659.
33. Hardy R.W., Marcotrigiano J., Blight K.J., Majors J.E., Rice C.M. Hepatitis C virus RNA synthesis in a cell-free system isolated from replicon-containing hepatoma cells. J. Virol. 77:2003;2029-2037.
34. He Y., Katze M.G. To interfere and to anti-interfere: the interplay between hepatitis C virus and interferon. Viral Immunol. 15:2002;95-119.
35. Hijikata M., Mizushima H., Akagi T., Mori S., Kakiuchi N., Kato N., Tanaka T., Kimura K., Shimotohno K. Two distinct proteinase activities required for the processing of a putative nonstructural precursor protein of hepatitis C virus. J. Virol. 67:1993;4665-4675.
36. Hugle T., Fehrmann F., Bieck E., Kohara M., Krausslich H.G., Rice C.M., Blum H.E., Moradpour D. The hepatitis C virus nonstructural protein 4B is an integral endoplasmic reticulum membrane protein. Virology. 284:2001;70-81.
37. Ikeda M., Yi M., Li K., Lemon S.M. Selectable subgenomic and genome-length dicistronic RNAs derived from an infectious molecular clone of the HCV-N strain of hepatitis C virus replicate efficiently in cultured Huh7 cells. J. Virol. 76:2002;2997-3006.
38. Kaito M., Watanabe S., Tsukiyama-Kohara K., Yamaguchi K., Kobayashi Y., Konishi M., Yokoi M., Ishida S., Suzuki S., Kohara M. Hepatitis C virus particle detected by immunoelectron microscopic study. J. Gen. Virol. 75:1994;1755-1760.
39. Kaneko T., Tanji Y., Satoh S., Hijikata M., Asabe S., Kimura K., Shimotohno K. Production of two phosphoproteins from the NS5A region of the hepatitis C viral genome. Biochem. Biophys. Res. Commun. 205:1994;320-326.
40. Kao C.C., Yang X., Kline A., Wang Q.M., Barket D., Heinz B.A. Template requirements for RNA synthesis by a recombinant hepatitis C virus RNA-dependent RNA polymerase. J. Virol. 74:2000;11121-11128.
41. Kim D.W., Gwack Y., Han J.H., Choe J. C-terminal domain of the hepatitis C virus NS3 protein contains an RNA helicase activity. Biochem. Biophys. Res. Commun. 215:1995;160-166.
42. Kishine H., Sugiyama K., Hijikata M., Kato N., Takahashi H., Noshi T., Nio Y., Hosaka M., Miyanari Y., Shimotohno K. Subgenomic replicon derived from a cell line infected with the hepatitis C virus. Biochem. Biophys. Res. Commun. 293:2002;993-999.
43. Koch J.O., Bartenschlager R. Modulation of hepatitis C virus NS5A hyperphosphorylation by nonstructural proteins NS3, NS4A, and NS4B. J. Virol. 73:1999;7138-7146.
44. Kolykhalov A.A., Agapov E.V., Blight K.J., Mihalik K., Feinstone S.M., Rice C.M. Transmission of hepatitis C by intrahepatic inoculation with transcribed RNA. Science. 277:1997;570-574.
45. Kolykhalov A.A., Mihalik K., Feinstone S.M., Rice C.M. Hepatitis C virus-encoded enzymatic activities and conserved RNA elements in the 3′ nontranslated region are essential for virus replication in vivo. J. Virol. 74:2000;2046-2051.
46. Krieger N., Lohmann V., Bartenschlager R. Enhancement of hepatitis C virus RNA replication by cell culture- adaptive mutations. J. Virol. 75:2001;4614-4624.
47. Lai V.C., Dempsey S., Lau J.Y., Hong Z., Zhong W. In vitro RNA replication directed by replicase complexes isolated from the subgenomic replicon cells of hepatitis C virus. J. Virol. 77:2003;2295-2300.
48. Lanford R.E., Guerra B., Lee H., Averett D.R., Pfeiffer B., Chavez D., Notvall L., Bigger C. Antiviral effect and virus-host interactions in response to alpha interferon, gamma interferon, poly(i)-poly(c), tumor necrosis factor alpha, and ribavirin in hepatitis C virus subgenomic replicons. J. Virol. 77:2003;1092-1104.
49. Lin C., Pragai B.M., Grakoui A., Xu J., Rice C.M. Hepatitis C virus NS3 serine proteinase: trans-cleavage requirements and processing kinetics. J. Virol. 68:1994;8147-8157.
50. Lohmann V., Körner F., Herian U., Bartenschlager R. Biochemical properties of hepatitis C virus NS5B RNA-dependent RNA polymerase and identification of amino acid sequence motifs essential for enzymatic activity. J. Virol. 71:1997;8416-8428.
51. Lohmann V., Körner F., Koch J.O., Herian U., Theilmann L., Bartenschlager R. Replication of subgenomic hepatitis C virus RNAs in a hepatoma cell line. Science. 285:1999;110-113.
52. Lohmann V., Körner F., Dobierzewska A., Bartenschlager R. Mutations in hepatitis C virus RNAs conferring cell culture adaptation. J. Virol. 75:2001;1437-1449.
53. Lohmann V., Hoffmann S., Herian U., Penin F., Bartenschlager R. Viral and cellular determinants of hepatitis C virus RNA replication in cell culture. J. Virol. 77:2003;3007-3019.
54. Lundin M., Monne M., Widell A., Von Heijne G., Persson M.A. Topology of the membrane-associated hepatitis C virus protein NS4B. J. Virol. 77:2003;5428-5438.
55. Luo G., Hamatake R.K., Mathis D.M., Racela J., Rigat K.L., Lemm J., Colonno R.J. De novo initiation of RNA synthesis by the RNA-dependent RNA polymerase (NS5B) of hepatitis C virus. J. Virol. 74:2000;851-863.
56. Luo G., Xin S., Cai Z. Role of the 5′-proximal stem-loop structure of the 5′ untranslated region in replication and translation of hepatitis C virus RNA. J. Virol. 77:2003;3312-3318.
57. Mackenzie J.M., Jones M.K., Young P.R. Immunolocalization of the dengue virus nonstructural glycoprotein NS1 suggests a role in viral RNA replication. Virology. 220:1996;232-240.
58. Manns M.P., Cornberg M., Wedemeyer H. Current and future treatment of hepatitis C. Indian J. Gastroenterol. 20(Suppl. 1):2001;C47-C51.
59. Mehta S.H., Cox A., Hoover D.R., Wang X.H., Mao Q., Ray S., Strathdee S.A., Vlahov D., Thomas D.L. Protection against persistence of hepatitis C. Lancet. 359:2002;1478-1483.
60. Mottola G., Cardinali G., Ceccacci A., Trozzi C., Bartholomew L., Torrisi M.R., Pedrazzini E., Bonatti S., Migliaccio G. Hepatitis C virus nonstructural proteins are localized in a modified endoplasmic reticulum of cells expressing viral subgenomic replicons. Virology. 293:2002;31-43.
61. Murray E.M., Grobler J.A., Markel E.J., Pagnoni M.F., Paonessa G., Simon A.J., Flores O.A. Persistent replication of hepatitis C virus replicons expressing the beta-lactamase reporter in subpopulations of highly permissive Huh7 cells. J. Virol. 77:2003;2928-2935.
62. Neumann A.U., Lam N.P., Dahari H., Gretch D.R., Wiley T.E., Layden T.J., Perelson A.S. Hepatitis C viral dynamics in vivo and the antiviral efficacy of interferon-alpha therapy. Science. 282:1998;103-107.
63. O'Farrell D., Trowbridge R., Rowlands D., Jager J. Substrate complexes of hepatitis C virus RNA polymerase (HC-J4): structural evidence for nucleotide import and de novo initiation. J. Mol. Biol. 326:2003;1025-1035.
64. Op De Beek A., Cocquerel L., Dubuisson J. Biogenesis of hepatitis C virus envelope glycoproteins. J. Gen. Virol. 82:2001;2589-2595.
65. Pallaoro M., Lahm A., Biasiol G., Brunetti M., Nardella C., Orsatti L., Bonelli F., Orru S., Narjes F., Steinkuhler C. Characterization of the hepatitis C virus NS2/3 processing reaction by using a purified precursor protein. J. Virol. 75:2001;9939-9946.
66. Pawlotsky J.M. Hepatitis C virus infection: virus/host interactions. J. Viral Hepatol. 5(Suppl. 1):1998;3-8.
67. Pestova T.V., Shatsky I.N., Fletcher S.P., Jackson R.J., Hellen C.U. A prokaryotic-like mode of cytoplasmic eukaryotic ribosome binding to the initiation codon during internal translation initiation of hepatitis C and classical swine fever virus RNAs. Genes Dev. 12:1998;67-83.
68. Pieroni L., Santolini E., Fipaldini C., Pacini L., Migliaccio G., La Monica N. In vitro study of the NS2-3 protease of hepatitis C virus. J. Virol. 71:1997;6373-6380.
69. Pietschmann T., Lohmann V., Rutter G., Kurpanek K., Bartenschlager R. Characterization of cell lines carrying self-replicating hepatitis C virus RNAs. J. Virol. 75:2001;1252-1264.
70. Pietschmann T., Lohmann V., Kaul A., Krieger N., Rinck G., Rutter G., Strand D., Bartenschlager R. Persistent and transient replication of full-length hepatitis C virus genomes in cell culture. J. Virol. 76:2002;4008-4021.
71. Poynard T., Bedossa P., Opolon P. Natural history of liver fibrosis progression in patients with chronic hepatitis C. The OBSVIRC, METAVIR, CLINIVIR, and DOSVIRC groups. Lancet. 349:1997;825-832.
72. Rosen H.R., Ribeiro R.R., Weinberger L., Wolf S., Chung M., Gretch D.R., Perelson A.S. Early hepatitis C viral kinetics correlate with long-term outcome in patients receiving high dose induction followed by combination interferon and ribavirin therapy. J. Hepatol. 37:2002;124-130.
73. Shi S.T., Lee K.J., Aizaki H., Hwang S.B., Lai M.M. Hepatitis C virus RNA replication occurs on a detergent-resistant membrane that cofractionates with caveolin-2. J. Virol. 77:2003;4160-4168.
74. Sugiyama K., Kato N., Mizutani T., Ikeda M., Tanaka T., Shimotohno K. Genetic analysis of the hepatitis C virus (HCV) genome from HCV-infected human T cells. J. Gen. Virol. 78:1997;329-336.
75. Sun X.L., Johnson R.B., Hockman M.A., Wang Q.M. De novo RNA synthesis catalyzed by HCV RNA-dependent RNA polymerase. Biochem. Biophys. Res. Commun. 268:2000;798-803.
76. Suzich J.A., Tamura J.K., Palmer-Hill F., Warrener P., Grakoui A., Rice C.M., Feinstone S.M., Collett M.S. Hepatitis C virus NS3 protein polynucleotide-stimulated nucleoside triphosphatase and comparison with the related pestivirus and flavivirus enzymes. J. Virol. 67:1993;6152-6158.
77. Tan S.L., Pause A., Shi Y., Sonenberg N. Hepatitis C therapeutics: current status and emerging strategies. Nat. Rev. Drug Discov. 1:2002;867-881.
78. Tanji Y., Kaneko T., Satoh S., Shimotohno K. Phosphorylation of hepatitis C virus-encoded nonstructural protein NS5A. J. Virol. 69:1995;3980-3986.
79. Thibeault D., Maurice R., Pilote L., Lamarre D., Pause A. In vitro characterization of a purified NS2/3 protease variant of hepatitis C virus. J. Biol. Chem. 276:2001;46678-46684.
80. Trozzi C., Bartholomew L., Ceccacci A., Biasiol G., Pacini L., Altamura S., Narjes F., Muraglia E., Paonessa G., Koch U., De Francesco R., Steinkuhler C., Migliaccio G. In vitro selection and characterization of hepatitis C virus serine protease variants resistant to an active-site peptide inhibitor. J. Virol. 77:2003;3669-3679.
81. Tsukiyama-Kohara K., Iizuka N., Kohara M., Nomoto A. Internal ribosome entry site within hepatitis C virus RNA. J. Virol. 66:1992;1476-1483.
82. van Regenmortel, M.H.V., Fauquet, C.M., Bishop, D.H.L., Carstens, E.B., Estes, M.K., Lemon, S.M., Maniloff, J., Mayo, M.A., McGeoch, D.J., Pringle, C.R., Wickner, R.B., 2000. Virus Taxonomy: The Seventh Report of the International Committee on Taxonomy of Viruses. Academic Press, San Diego.
83. Varaklioti A., Vassilaki N., Georgopoulou U., Mavromara P. Alternate translation occurs within the core coding region of the hepatitis C viral genome. J. Biol. Chem. 277:2002;17713-17721.
84. Vrolijk J.M., Kaul A., Hansen B.E., Lohmann V., Haagmans B.L., Schalm S.W., Bartenschlager R. A replicon-based bioassay for the measurement of interferons in patients with chronic hepatitis C. J. Virol. Methods. 110(2):2003;201-209.
85. Wang C., Sarnow P., Siddiqui A. Translation of human hepatitis C virus RNA in cultured cells is mediated by an internal ribosome-binding mechanism. J. Virol. 67:1993;3338-3344.
86. Wang C., Pflugheber J., Sumpter R. Jr., Sodora D.L., Hui D., Sen G.C., Gale M. Jr. Alpha interferon induces distinct translational control programs to suppress hepatitis C virus RNA replication. J. Virol. 77:2003;3898-3912.
87. Waxman L., Whitney M., Pollok B.A., Kuo L.C., Darke P.L. Host cell factor requirement for hepatitis C virus enzyme maturation. Proc. Natl. Acad. Sci. U.S.A. 98:2001;13931-13935.
88. Xu Z., Choi J., Yen T.S., Lu W., Strohecker A., Govindarajan S., Chien D., Selby M.J., Ou J. Synthesis of a novel hepatitis C virus protein by ribosomal frameshift. EMBO J. 20:2001;3840-3848.
89. Yanagi M., St. Claire M., Emerson S.U., Purcell R.H., Bukh J. In vivo analysis of the 3′ untranslated region of the hepatitis C virus after in vitro mutagenesis of an infectious cDNA clone. Proc. Natl. Acad. Sci. U.S.A. 96:1999;2291-2295.
90. Yasui K., Wakita T., Tsukiyama-Kohara K., Funahashi S.I., Ichikawa M., Kajita T., Moradpour D., Wands J.R., Kohara M. The native form and maturation process of hepatitis C virus core protein. J. Virol. 72:1998;6048-6055.
91. Yi M., Lemon S.M. Replication of subgenomic hepatitis A virus RNAs expressing firefly luciferase is enhanced by mutations associated with adaptation of virus to growth in cultured cells. J. Virol. 76:2002;1171-1180.
92. Yi M., Lemon S.M. 3′ nontranslated RNA signals required for replication of hepatitis C virus RNA. J. Virol. 77:2003a;3557-3568.
93. Yi M., Lemon S.M. Structure-function analysis of the 3′ stem-loop of hepatitis C virus genomic RNA and its role in viral RNA replication. RNA. 9:2003b;331-345.
94. Zhong W., Uss A.S., Ferrari E., Lau J.Y., Hong Z. De novo initiation of RNA synthesis by hepatitis C virus nonstructural protein 5B polymerase. J. Virol. 74:2000;2017-2022.
95. Zhu Q., Guo J.T., Seeger C. Replication of hepatitis C virus subgenomes in nonhepatic epithelial and mouse hepatoma cells. J. Virol. 77:2003;9204-9210.