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Science 25 July 1997:
Vol. 277. no. 5325, pp. 570 - 574
DOI: 10.1126/science.277.5325.570
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Reports

Transmission of Hepatitis C by Intrahepatic Inoculation with Transcribed RNA

Alexander A. Kolykhalov, Eugene V. Agapov, Keril J. Blight, Kathleen Mihalik, Stephen M. Feinstone, Charles M. Rice *

More than 1% of the world's population is chronically infected with hepatitis C virus (HCV). HCV infection can result in acute hepatitis, chronic hepatitis, and cirrhosis, which is strongly associated with development of hepatocellular carcinoma. Genetic studies of HCV replication have been hampered by lack of a bona fide infectious molecular clone. Full-length functional clones of HCV complementary DNA were constructed. RNA transcripts from the clones were found to be infectious and to cause disease in chimpanzees after direct intrahepatic inoculation. This work defines the structure of a functional HCV genome RNA and proves that HCV alone is sufficient to cause disease.

A. A. Kolykhalov, E. V. Agapov, K. J. Blight, C. M. Rice, Department of Molecular Microbiology, Washington University School of Medicine, 660 South Euclid Avenue, St. Louis, MO 63110-1093, USA
K. Mihalik and S. M. Feinstone, Division of Virology, Center for Biologics Evaluation and Research, Food and Drug Administration, Bethesda, MD 20892, USA
*   To whom correspondence should be addressed.

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J. Virol. 78, 9093-9104
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Phosphorylation of hepatitis C virus nonstructural protein 5A modulates its protein interactions and viral RNA replication.
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Diverse Hepatitis C Virus Glycoproteins Mediate Viral Infection in a CD81-Dependent Manner.
J. A. McKeating, L. Q. Zhang, C. Logvinoff, M. Flint, J. Zhang, J. Yu, D. Butera, D. D. Ho, L. B. Dustin, C. M. Rice, et al. (2004)
J. Virol. 78, 8496-8505
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Neutralizing antibody response during acute and chronic hepatitis C virus infection.
C. Logvinoff, M. E. Major, D. Oldach, S. Heyward, A. Talal, P. Balfe, S. M. Feinstone, H. Alter, C. M. Rice, and J. A. McKeating (2004)
PNAS 101, 10149-10154
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CD81 is an entry coreceptor for hepatitis C virus.
E. G. Cormier, F. Tsamis, F. Kajumo, R. J. Durso, J. P. Gardner, and T. Dragic (2004)
PNAS 101, 7270-7274
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Uncleaved NS2-3 Is Required for Production of Infectious Bovine Viral Diarrhea Virus.
E. V. Agapov, C. L. Murray, I. Frolov, L. Qu, T. M. Myers, and C. M. Rice (2004)
J. Virol. 78, 2414-2425
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Hepatitis C Genotyping by Denaturing High-Performance Liquid Chromatography.
M. Liew, M. Erali, S. Page, D. Hillyard, and C. Wittwer (2004)
J. Clin. Microbiol. 42, 158-163
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Expression of Unmodified Hepatitis C Virus Envelope Glycoprotein-Coding Sequences Leads to Cryptic Intron Excision and Cell Surface Expression of E1/E2 Heterodimers Comprising Full-Length and Partially Deleted E1.
J. Dumonceaux, E. G. Cormier, F. Kajumo, G. P. Donovan, J. Roy-Chowdhury, I. J. Fox, J. P. Gardner, and T. Dragic (2003)
J. Virol. 77, 13418-13424
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In vitro assay for neutralizing antibody to hepatitis C virus: Evidence for broadly conserved neutralization epitopes.
B. Bartosch, J. Bukh, J.-C. Meunier, C. Granier, R. E. Engle, W. C. Blackwelder, S. U. Emerson, F.-L. Cosset, and R. H. Purcell (2003)
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Significance in Replication of the Terminal Nucleotides of the Flavivirus Genome.
A. A Khromykh, N. Kondratieva, J.-Y. Sgro, A. Palmenberg, and E. G Westaway (2003)
J. Virol. 77, 10623-10629
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Hepatitis C Virus-Like Particle Budding: Role of the Core Protein and Importance of Its Asp111.
E. Blanchard, C. Hourioux, D. Brand, M. Ait-Goughoulte, A. Moreau, S. Trassard, P.-Y. Sizaret, F. Dubois, and P. Roingeard (2003)
J. Virol. 77, 10131-10138
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Chronic hepatitis associated with GB virus B persistence in a tamarin after intrahepatic inoculation of synthetic viral RNA.
A. Martin, F. Bodola, D. V. Sangar, K. Goettge, V. Popov, R. Rijnbrand, R. E. Lanford, and S. M. Lemon (2003)
PNAS 100, 9962-9967
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Hepatitis C virus IRES efficiency is unaffected by the genomic RNA 3'NTR even in the presence of viral structural or non-structural proteins.
I. Imbert, M. Dimitrova, F. Kien, M. P. Kieny, and C. Schuster (2003)
J. Gen. Virol. 84, 1549-1557
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The Hepatitis C Virus Core Protein Modulates T Cell Responses by Inducing Spontaneous and Altering T-cell Receptor-triggered Ca2+ Oscillations.
A. Bergqvist, S. Sundstrom, L. Y. Dimberg, E. Gylfe, and M. G. Masucci (2003)
J. Biol. Chem. 278, 18877-18883
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Identification of a Key Determinant of Hepatitis C Virus Cell Culture Adaptation in Domain II of NS3 Helicase.
J. A. Grobler, E. J. Markel, J. F. Fay, D. J. Graham, A. L. Simcoe, S. W. Ludmerer, E. M. Murray, G. Migliaccio, and O. A. Flores (2003)
J. Biol. Chem. 278, 16741-16746
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Protein-Protein Interactions between Hepatitis C Virus Nonstructural Proteins.
M. Dimitrova, I. Imbert, M. P. Kieny, and C. Schuster (2003)
J. Virol. 77, 5401-5414
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Kinetics of CD4+ and CD8+ Memory T-Cell Responses during Hepatitis C Virus Rechallenge of Previously Recovered Chimpanzees.
M. Nascimbeni, E. Mizukoshi, M. Bosmann, M. E. Major, K. Mihalik, C. M. Rice, S. M. Feinstone, and B. Rehermann (2003)
J. Virol. 77, 4781-4793
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Hepatitis C Virus Glycoproteins Interact with DC-SIGN and DC-SIGNR.
S. Pohlmann, J. Zhang, F. Baribaud, Z. Chen, G. J. Leslie, G. Lin, A. Granelli-Piperno, R. W. Doms, C. M. Rice, and J. A. McKeating (2003)
J. Virol. 77, 4070-4080
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RNA interference blocks gene expression and RNA synthesis from hepatitis C replicons propagated in human liver cells.
J. A. Wilson, S. Jayasena, A. Khvorova, S. Sabatinos, I. G. Rodrigue-Gervais, S. Arya, F. Sarangi, M. Harris-Brandts, S. Beaulieu, and C. D. Richardson (2003)
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Analysis of the subcellular localization of hepatitis C virus E2 glycoprotein in live cells using EGFP fusion proteins.
F. Kien, J.-D. Abraham, C. Schuster, and M. P. Kieny (2003)
J. Gen. Virol. 84, 561-566
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Efficient Replication of Hepatitis C Virus Genotype 1a RNAs in Cell Culture.
K. J. Blight, J. A. McKeating, J. Marcotrigiano, and C. M. Rice (2003)
J. Virol. 77, 3181-3190
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A promoter activity is present in the DNA sequence corresponding to the hepatitis C virus 5' UTR.
E. Dumas, C. Staedel, M. Colombat, S. Reigadas, S. Chabas, T. Astier-Gin, A. Cahour, S. Litvak, and M. Ventura (2003)
Nucleic Acids Res. 31, 1275-1281
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The Clearance of Hepatitis C Virus Infection in Chimpanzees May Not Necessarily Correlate with the Appearance of Acquired Immunity.
M. Thomson, M. Nascimbeni, M. B. Havert, M. Major, S. Gonzales, H. Alter, S. M. Feinstone, K. K. Murthy, B. Rehermann, and T. J. Liang (2002)
J. Virol. 77, 862-870
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Role of the Asialoglycoprotein Receptor in Binding and Entry of Hepatitis C Virus Structural Proteins in Cultured Human Hepatocytes.
B. Saunier, M. Triyatni, L. Ulianich, P. Maruvada, P. Yen, and L. D. Kohn (2002)
J. Virol. 77, 546-559
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The Hepatitis C Virus RNA-Dependent RNA Polymerase Membrane Insertion Sequence Is a Transmembrane Segment.
N. Ivashkina, B. Wolk, V. Lohmann, R. Bartenschlager, H. E. Blum, F. Penin, and D. Moradpour (2002)
J. Virol. 76, 13088-13093
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Mutations that permit efficient replication of hepatitis C virus RNA in Huh-7 cells prevent productive replication in chimpanzees.
J. Bukh, T. Pietschmann, V. Lohmann, N. Krieger, K. Faulk, R. E. Engle, S. Govindarajan, M. Shapiro, M. St. Claire, and R. Bartenschlager (2002)
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Secondary Structure and Hybridization Accessibility of Hepatitis C Virus 3'-Terminal Sequences.
R. M. Smith, C. M. Walton, C. H. Wu, and G. Y. Wu (2002)
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M. Triyatni, B. Saunier, P. Maruvada, A. R. Davis, L. Ulianich, T. Heller, A. Patel, L. D. Kohn, and T. J. Liang (2002)
J. Virol. 76, 9335-9344
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Characterization of Vesicular Stomatitis Virus Recombinants That Express and Incorporate High Levels of Hepatitis C Virus Glycoproteins.
L. Buonocore, K. J. Blight, C. M. Rice, and J. K. Rose (2002)
J. Virol. 76, 6865-6872
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Previously Infected and Recovered Chimpanzees Exhibit Rapid Responses That Control Hepatitis C Virus Replication upon Rechallenge.
M. E. Major, K. Mihalik, M. Puig, B. Rehermann, M. Nascimbeni, C. M. Rice, and S. M. Feinstone (2002)
J. Virol. 76, 6586-6595
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Expression of Hepatitis C Virus Proteins Induces Distinct Membrane Alterations Including a Candidate Viral Replication Complex.
D. Egger, B. Wolk, R. Gosert, L. Bianchi, H. E. Blum, D. Moradpour, and K. Bienz (2002)
J. Virol. 76, 5974-5984
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Molecular and Immunological Significance of Chimpanzee Major Histocompatibility Complex Haplotypes for Hepatitis C Virus Immune Response and Vaccination Studies.
E. Mizukoshi, M. Nascimbeni, J. B. Blaustein, K. Mihalik, C. M. Rice, T. J. Liang, S. M. Feinstone, and B. Rehermann (2002)
J. Virol. 76, 6093-6103
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Subcellular Localization and Topology of the p7 Polypeptide of Hepatitis C Virus.
S. Carrere-Kremer, C. Montpellier-Pala, L. Cocquerel, C. Wychowski, F. Penin, and J. Dubuisson (2002)
J. Virol. 76, 3720-3730
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An Amino-terminal Amphipathic alpha -Helix Mediates Membrane Association of the Hepatitis C Virus Nonstructural Protein 5A.
V. Brass, E. Bieck, R. Montserret, B. Wolk, J. A. Hellings, H. E. Blum, F. Penin, and D. Moradpour (2002)
J. Biol. Chem. 277, 8130-8139
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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.
M. Ikeda, M. Yi, K. Li, and S. M. Lemon (2002)
J. Virol. 76, 2997-3006
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Binding of Hepatitis C Virus-Like Particles Derived from Infectious Clone H77C to Defined Human Cell Lines.
S. Wellnitz, B. Klumpp, H. Barth, S. Ito, E. Depla, J. Dubuisson, H. E. Blum, and T. F. Baumert (2002)
J. Virol. 76, 1181-1193
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Functional Properties of a Monoclonal Antibody Inhibiting the Hepatitis C Virus RNA-dependent RNA Polymerase.
D. Moradpour, E. Bieck, T. Hugle, W. Wels, J. Z. Wu, Z. Hong, H. E. Blum, and R. Bartenschlager (2002)
J. Biol. Chem. 277, 593-601
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Determinants for Membrane Association of the Hepatitis C Virus RNA-dependent RNA Polymerase.
J. Schmidt-Mende, E. Bieck, T. Hugle, F. Penin, C. M. Rice, H. E. Blum, and D. Moradpour (2001)
J. Biol. Chem. 276, 44052-44063
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Identification of a Hepatic Factor Capable of Supporting Hepatitis C Virus Replication in a Nonpermissive Cell Line.
C.-T. Yeh, H.-Y. Lai, T.-C. Chen, C.-M. Chu, and Y.-F. Liaw (2001)
J. Virol. 75, 11017-11024
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Generation of infectious and transmissible virions from a GB virus B full-length consensus clone in tamarins.
A. Sbardellati, E. Scarselli, E. Verschoor, A. De Tomassi, D. Lazzaro, and C. Traboni (2001)
J. Gen. Virol. 82, 2437-2448
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Effect of Alpha Interferon on the Hepatitis C Virus Replicon.
J.-T. Guo, V. V. Bichko, and C. Seeger (2001)
J. Virol. 75, 8516-8523
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Intrahepatic Genetic Inoculation of Hepatitis C Virus RNA Confers Cross-Protective Immunity.
A. J. Weiner, X. Paliard, M. J. Selby, A. Medina-Selby, D. Coit, S. Nguyen, J. Kansopon, C. L. Arian, P. Ng, J. Tucker, et al. (2001)
J. Virol. 75, 7142-7148
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Human hepatitis C virus NS5A protein alters intracellular calcium levels, induces oxidative stress, and activates STAT-3 and NF-kappa B.
G. Gong, G. Waris, R. Tanveer, and A. Siddiqui (2001)
PNAS
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Hepatitis C Virus Infection.
G. M. Lauer and B. D. Walker (2001)
N. Engl. J. Med. 345, 41-52
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Infectious cDNA clone of the hepatitis C virus genotype 1 prototype sequence.
R. E. Lanford, H. Lee, D. Chavez, B. Guerra, and K. M. Brasky (2001)
J. Gen. Virol. 82, 1291-1297
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Antigenicity and Immunogenicity of Novel Chimeric Hepatitis B Surface Antigen Particles with Exposed Hepatitis C Virus Epitopes.
H. J. Netter, T. B. Macnaughton, W.-P. Woo, R. Tindle, and E. J. Gowans (2001)
J. Virol. 75, 2130-2141
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Specific Interaction of Hepatitis C Virus Protease/Helicase NS3 with the 3'-Terminal Sequences of Viral Positive- and Negative-Strand RNA.
R. Banerjee and A. Dasgupta (2001)
J. Virol. 75, 1708-1721
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Enhanced Expression of Interferon-Regulated Genes in the Liver of Patients with Chronic Hepatitis C Virus Infection: Detection by Suppression-Subtractive Hybridization.
R. Patzwahl, V. Meier, G. Ramadori, and S. Mihm (2001)
J. Virol. 75, 1332-1338
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Hepatitis C Virus 3'X Region Interacts with Human Ribosomal Proteins.
J. Wood, R. M. Frederickson, S. Fields, and A. H. Patel (2001)
J. Virol. 75, 1348-1358
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Mutations in Hepatitis C Virus RNAs Conferring Cell Culture Adaptation.
V. Lohmann, F. Körner, A. Dobierzewska, and R. Bartenschlager (2001)
J. Virol. 75, 1437-1449
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