Turning hepatitis C into a real virus

Annual Review of Microbiology

Volumn 65, Issue , 2011, Pages 307-327

  Murray, Catherine L ^a   Rice, Charles M ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

Adaptive mutation; Cell culture; HCV; Infectious clone; Replicon

Indexed keywords

ANTIVIRUS AGENT; PEGINTERFERON ALPHA; RIBAVIRIN;

CELL CULTURE; CHIMERA; GENETIC VARIABILITY; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; NONHUMAN; PRIORITY JOURNAL; REPLICON; REVIEW; VIRUS INHIBITION; VIRUS ISOLATION; VIRUS MUTATION; VIRUS REPLICATION; VIRUS STRAIN;

ANIMALS; ANTIVIRAL AGENTS; DRUG DISCOVERY; HEPACIVIRUS; HEPATITIS C; HUMANS;

HEPATITIS C VIRUS;

EID: 80053264773     PISSN: 00664227     EISSN: 15453251     Source Type: Book Series    
DOI: 10.1146/annurev-micro-090110-102954     Document Type: Review

References (150)

1. Abe K, Ikeda M, Dansako H, Naka K, Kato N. 2007. Cell culture-adaptive NS3 mutations required for the robust replication of genome-length hepatitis C virus RNA. Virus Res. 125:88-97 (Pubitemid 46413392)
2. Ahn J, Chung KS, Kim DU, Won M, Kim L, et al. 2004. Systematic identification of hepatocellular proteins interacting with NS5A of the hepatitis C virus. J. Biochem. Mol. Biol. 37:741-48 (Pubitemid 40221537)
3. Ali S, Pellerin C, Lamarre D, Kukolj G. 2004. Hepatitis C virus subgenomic replicons in the human embryonic kidney 293 cell line. J. Virol. 78:491-501 (Pubitemid 37549759)
4. Alter H. 1999. Discovery of non-A, non-B hepatitis and identification of its etiology. Am. J. Med. 107:16S-20S
5. Alter HJ, Houghton M. 2000. Clinical medical research award Hepatitis C virus and eliminating posttransfusion hepatitis. Nat. Med. 6:1082-86
6. Alter HJ, Purcell RH, Holland PV, Popper H. 1978. Transmissible agent in non-A, non-B hepatitis. Lancet 1:459-63 (Pubitemid 8286033)
7. Aly HH, Watashi K, Hijikata M, Kaneko H, Takada Y, et al. 2007. Serum-derived hepatitis C virus infectivity in interferon regulatory factor-7-suppressed human primary hepatocytes. J. Hepatol. 46:26-36 (Pubitemid 44827421)
8. Andre P, Komurian-Pradel F, Deforges S, Perret M, Berland JL, et al. 2002. Characterization of lowand very-low-density hepatitis C virus RNA-containing particles. J. Virol. 76:6919-28 (Pubitemid 41246207)
9. 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. 79:3187-94 (Pubitemid 40270599)
10. Appel N, Zayas M, Miller S, Krijnse-Locker J, Schaller T, et al. 2008. Essential role of domain III of nonstructural protein 5A for hepatitis C virus infectious particle assembly. PLoS Pathog. 4:e1000035
11. Banaudha K, Orenstein JM, Korolnek T, St. Laurent GC 3rd, Wakita T, Kumar A. 2010. Primary hepatocyte culture supports hepatitis C virus replication: a model for infection-associated hepatocarcinogenesis. Hepatology 51:1922-32
12. Bartenschlager R, Kaul A, Sparacio S. 2003. Replication of the hepatitis C virus in cell culture. Antiviral. Res. 60:91-102 (Pubitemid 37452452)
13. Bartosch B, Vitelli A, Granier C, Goujon C, Dubuisson J, et al. 2003. Cell entry of hepatitis C virus requires a set of coreceptors that include the CD81 tetraspanin and the SR-B1 scavenger receptor. J. Biol. Chem. 278:41624-30 (Pubitemid 37310418)
14. Beard MR, Abell G, Honda M, Carroll A, Gartland M, et al. 1999. An infectious molecular clone of a Japanese genotype 1b hepatitis C virus. Hepatology 30:316-24 (Pubitemid 29300603)
15. Binder M, Kochs G, Bartenschlager R, Lohmann V. 2007. Hepatitis C virus escape from the interferon regulatory factor 3 pathway by a passive and active evasion strategy. Hepatology 46:1365-74 (Pubitemid 350155518)
16. Binder M, Quinkert D, Bochkarova O, Klein R, Kezmic N, et al. 2007. Identification of determinants involved in initiation of hepatitis C virus RNA synthesis by using intergenotypic replicase chimeras. J. Virol. 81:5270-83 (Pubitemid 46744436)
17. Bissig KD, Wieland SF, Tran P, Isogawa M, Le TT, et al. 2010. Human liver chimeric mice provide a model for hepatitis B and C virus infection and treatment. J. Clin. Investig. 120:924-30
18. Blight KJ, Kolykhalov AA, Rice CM. 2000. Efficient initiation of HCV RNA replication in cell culture. Science 290:1972-74
19. Blight KJ, McKeating JA, Marcotrigiano J, Rice CM. 2003. Efficient replication of hepatitis C virus genotype 1a RNAs in cell culture. J. Virol. 77:3181-90 (Pubitemid 36228102)
20. Blight KJ, McKeating JA, Rice CM. 2002. Highly permissive cell lines for subgenomic and genomic hepatitis C virus RNA replication. J. Virol. 76:13001-14 (Pubitemid 35386984)
21. Blight KJ, Rice CM. 1997. Secondary structure determination of the conserved 98-base sequence at the 3- terminus of hepatitis C virus genome RNA. J. Virol. 71:7345-52
22. Bradley DW, Maynard JE, Popper H, Cook EH, Ebert JW, et al. 1983. Posttransfusion non-A, non-B hepatitis: physicochemical properties of two distinct agents. J. Infect. Dis. 148:254-65 (Pubitemid 13002460)
23. Buck M. 2008. Direct infection and replication of naturally occurring hepatitis C virus genotypes 1, 2, 3 and 4 in normal human hepatocyte cultures. PLoS One 3:e2660
24. Bukh J, Meuleman P, Tellier R, Engle RE, Feinstone SM, et al. 2010. Challenge pools of hepatitis C virus genotypes 1-6 prototype strains: replication fitness and pathogenicity in chimpanzees and human liver-chimeric mouse models. J. Infect. Dis. 201:1381-89
25. Bukh J, Miller RH, Purcell RH. 1995. Genetic heterogeneity of hepatitis C virus: quasispecies and genotypes. Semin. Liver Dis. 15:41-63
26. Bukh J, Pietschmann T, Lohmann V, Krieger N, Faulk K, et al. 2002. Mutations that permit efficient replication of hepatitis C virus RNA in Huh-7 cells prevent productive replication in chimpanzees. Proc. Natl. Acad. Sci. USA 99:14416-21 (Pubitemid 35257686)
27. Bungyoku Y, Shoji I, Makine T, Adachi T, Hayashida K, et al. 2009. Efficient production of infectious hepatitis C virus with adaptive mutations in cultured hepatoma cells. J. Gen. Virol. 90:1681-91
28. Carloni G, Iacovacci S, Sargiacomo M, Ravagnan G, Ponzetto A, et al. 1993. Susceptibility of human liver cell cultures to hepatitis C virus infection. Arch. Virol. Suppl. 8:31-39
29. Chang KS, Cai Z, Zhang C, Sen GC, Williams BR, Luo G. 2006. Replication of hepatitis C virus (HCV) RNA in mouse embryonic fibroblasts: protein kinase R (PKR)-dependent and PKR-independent mechanisms for controllingHCV RNA replication and mediating interferon activities. J. Virol. 80:7364-74 (Pubitemid 44092559)
30. Choo Q-L, KuoG,Weiner AJ, Overby LR, Bradley DW, HoughtonM. 1989. Isolation of a cDNA clone derived from a blood-borne non-A, non-B viral hepatitis genome. Science 244:359-62 (Pubitemid 19117877)
31. Choo Q-L, Richman KH, Han JH, Berger K, Lee C, et al. 1991. Genetic organization and diversity of the hepatitis C virus. Proc. Natl. Acad. Sci. USA 88:2451-55 (Pubitemid 21916435)
32. Conley AJ, McKenna PM,Murthy KK, Migliaccio G, Paonessa G, DeFrancesco R. 1998. Isolation of in vivo replication-competent hepatitisCvirusBKstrain from molecular clones. Hepatology 28(Suppl.):560A
33. Date T, Kato T, Miyamoto M, Zhao Z, Yasui K, et al. 2004. Genotype 2a hepatitis C virus subgenomic replicon can replicate in HepG2 and IMY-N9 cells. J. Biol. Chem. 279:22371-76 (Pubitemid 38679434)
34. Delgrange D, Pillez A, Castelain S, Cocquerel L, Rouille Y, et al. 2007. Robust production of infectious viral particles in Huh-7 cells by introducing mutations in hepatitis C virus structural proteins. J. Gen. Virol. 88:2495-503 (Pubitemid 47323895)
35. Egger D,Wolk B, Gosert R, Bianchi L, Blum HE, et al. 2002. Expression of hepatitis C virus proteins induces distinct membrane alterations including a candidate viral replication complex. J. Virol. 76:5974-84 (Pubitemid 34556292)
36. Evans MJ, Rice CM, Goff SP. 2004. Phosphorylation of hepatitis C virus nonstructural protein 5A modulates its protein interactions and viral RNA replication. Proc. Natl. Acad. Sci. USA 101:13038-43 (Pubitemid 39167579)
37. Feinstone S, Alter HJ, Dienes HP, Shimizu Y, Popper H, et al. 1981. Non-A, non-B hepatitis in chimpanzees and marmosets. J. Infect. Dis. 144:588-98 (Pubitemid 12194465)
38. Feinstone SM, Kapikian AZ, Purcell RH, Alter HJ, Holland PV. 1975. Transfusion-associated hepatitis not due to viral hepatitis type A or B. N. Engl. J. Med. 292:767-70
39. Feinstone SM, Mihalik KB, Kamimura T, Alter HJ, London WT, Purcell RH. 1983. Inactivation of hepatitis B virus and non-A, non-B hepatitis by chloroform. Infect. Immun. 41:816-21 (Pubitemid 13074641)
40. Gale MJ Jr, Korth MJ, Tang NM, Tan SL, Hopkins DA, et al. 1997. Evidence that hepatitis C virus resistance to interferon is mediated through repression of the PKR protein kinase by the nonstructural 5A protein. Virology 230:217-27 (Pubitemid 27211852)
41. Gottwein JM, Scheel TK, Callendret B, Li YP, Eccleston HB, et al. 2010. Novel infectious cDNA clones of hepatitis C virus genotype 3a (strain S52) and 4a (strain ED43): genetic analyses and in vivo pathogenesis studies. J. Virol. 84:5277-93
42. Gottwein JM, Scheel TK, Hoegh AM, Lademann JB, Eugen-Olsen J, et al. 2007. Robust hepatitis C genotype 3a cell culture releasing adapted intergenotypic 3a/2a (S52/JFH1) viruses. Gastroenterology 133:1614-26 (Pubitemid 350029736)
43. Gottwein JM, Scheel TK, Jensen TB, Lademann JB, Prentoe JC, et al. 2009. Development and characterization of hepatitis C virus genotype 1-7 cell culture systems: role of CD81 and scavenger receptor class B type I and effect of antiviral drugs. Hepatology 49:364-77
44. Grobler JA, Markel EJ, Fay JF, Graham DJ, Simcoe AL, et al. 2003. Identification of a key determinant of hepatitis C virus cell culture adaptation in domain II of NS3 helicase. J. Biol. Chem. 278:16741-46 (Pubitemid 36799540)
45. Gu B, Gates AT, Isken O, Behrens SE, Sarisky RT. 2003. Replication studies using genotype 1a subgenomic hepatitis C virus replicons. J. Virol. 77:5352-59 (Pubitemid 36460949)
46. Guo JT, Bichko VV, Seeger C. 2001. Effect of alpha interferon on the hepatitis C virus replicon. J. Virol. 75:8516-23 (Pubitemid 32768956)
47. Hamamoto I, Nishimura Y, Okamoto T, Aizaki H, Liu M, et al. 2005. Human VAP-B is involved in hepatitis C virus replication through interaction with NS5A and NS5B. J. Virol. 79:13473-82 (Pubitemid 41508160)
48. Hanoulle X, Badillo A, Wieruszeski JM, Verdegem D, Landrieu I, et al. 2009. Hepatitis C virus NS5A protein is a substrate for the peptidyl-prolyl cis/trans isomerase activity of cyclophilins A and B. J. Biol. Chem. 284:13589-601
49. He LF, Alling D, Popkin T, Shapiro M, Alter HJ, Purcell RH. 1987. Determining the size of non-A, non-B hepatitis virus by filtration. J. Infect. Dis. 156:636-40 (Pubitemid 17154674)
50. Heller T, Saito S, Auerbach J, Williams T, Moreen TR, et al. 2005. An in vitro model of hepatitis C virion production. Proc. Natl. Acad. Sci. USA 102:2579-83 (Pubitemid 40279419)
51. Hong Z, Beaudet-Miller M, Lanford RE, Guerra B, Wright-Minogue J, et al. 1999. Generation of transmissible hepatitis C virions from a molecular clone in chimpanzees. Virology 256:36-44 (Pubitemid 29391824)
52. Houghton M. 2009. The long and winding road leading to the identification of the hepatitis C virus. J. Hepatol. 51:939-48
53. Huang Y, Staschke K, De Francesco R, Tan SL. 2007. Phosphorylation of hepatitis C virus NS5A nonstructural protein: a new paradigm for phosphorylation-dependent viral RNA replication? Virology 364:1-9 (Pubitemid 46829271)
54. Iacovacci S, Manzin A, Barca S, Sargiacomo M, Serafino A, et al. 1997. Molecular characterization and dynamics of hepatitis C virus replication in human fetal hepatocytes infected in vitro. Hepatology 26:1328-37 (Pubitemid 27509321)
55. Iacovacci S, Sargiacomo M, Parolini I, Ponzetto A, Peschle C, Carloni G. 1993. Replication and multiplication of hepatitis C virus genome in human foetal liver cells. Res. Virol. 144:275-79 (Pubitemid 23247315)
56. Ikeda M, Abe K, Dansako H, Nakamura T, Naka K, Kato N. 2005. Efficient replication of a full-length hepatitis C virus genome, strain O, in cell culture, and development of a luciferase reporter system. Biochem. Biophys. Res. Commun. 329:1350-59 (Pubitemid 40568718)
57. IkedaM, KatoN,Mizutani T, Sugiyama K, Tanaka K, Shimotohno K. 1997. Analysis of the cell tropism of HCV by using in vitro HCV-infected human lymphocytes and hepatocytes. J. Hepatol. 27:445-54 (Pubitemid 27390890)
58. Ikeda M, Yi M, Li K, Lemon SM. 2002. 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. 76:2997-3006 (Pubitemid 34184884)
59. Ishii N, Watashi K, Hishiki T, Goto K, Inoue D, et al. 2006. Diverse effects of cyclosporine on hepatitis C virus strain replication. J. Virol. 80:4510-20
60. Ito T, Mukaigawa J, Zuo J, Hirabayashi Y, Mitamura K, Yasui K. 1996. Cultivation of hepatitis C virus in primary hepatocyte culture from patients with chronic hepatitis C results in release of high titre infectious virus. J. Gen. Virol. 77:1043-54 (Pubitemid 26142340)
61. Jensen TB, Gottwein JM, Scheel TK, Hoegh AM, Eugen-Olsen J, Bukh J. 2008. Highly efficient JFH1- based cell-culture system for hepatitis C virus genotype 5a: failure of homologous neutralizing-antibody treatment to control infection. J. Infect. Dis. 198:1756-65
62. Jones CT, Catanese MT, Law LM, Khetani SR, Syder AJ, et al. 2010. Real-time imaging of hepatitis C virus infection using a fluorescent cell-based reporter system. Nat. Biotechnol. 28:167-71
63. Kang JI, Kim JP, Wakita T, Ahn BY. 2009. Cell culture-adaptive mutations in the NS5B gene of hepatitis C virus with delayed replication and reduced cytotoxicity. Virus Res. 144:107-16
64. Kato N, Ikeda M, Mizutani T, Sugiyama K, Noguchi M, et al. 1996. Replication of hepatitis C virus in cultured non-neoplastic human hepatocytes. Jpn. J. Cancer Res. 87:787-92 (Pubitemid 26335804)
65. Kato N, Sugiyama K, Namba K, Dansako H, Nakamura T, et al. 2003. Establishment of a hepatitis C virus subgenomic replicon derived from human hepatocytes infected in vitro. Biochem. Biophys. Res. Commun. 306:756-66 (Pubitemid 37323827)
66. Kato T, Choi Y, Elmowalid G, Sapp RK, Barth H, et al. 2008. Hepatitis C virus JFH-1 strain infection in chimpanzees is associated with low pathogenicity and emergence of an adaptive mutation. Hepatology 48:732-40
67. Kato T, Date T, Miyamoto M, Furusaka A, TokushigeK, et al. 2003. Efficient replication of the genotype 2a hepatitis C virus subgenomic replicon. Gastroenterology 125:1808-17 (Pubitemid 37500445)
68. Kato T, Date T, Miyamoto M, Zhao Z, Mizokami M, Wakita T. 2005. Nonhepatic cell lines HeLa and 293 support efficient replication of the hepatitis C virus genotype 2a subgenomic replicon. J. Virol. 79:592-96 (Pubitemid 39648411)
69. Kato T, Furusaka A, Miyamoto M, Date T, Yasui K, et al. 2001. Sequence analysis of hepatitis C virus isolated from a fulminant hepatitis patient. J. Med. Virol. 64:334-39 (Pubitemid 32565130)
70. Kato T, Matsumura T, Heller T, Saito S, Sapp RK, et al. 2007. Production of infectious hepatitis C virus of various genotypes in cell cultures. J. Virol. 81:4405-11 (Pubitemid 46668637)
71. Kaul A, Stauffer S, Berger C, Pertel T, Schmitt J, et al. 2009. Essential role of cyclophilin A for hepatitis C virus replication and virus production and possible link to polyprotein cleavage kinetics. PLoS Pathog. 5:e1000546
72. 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. 81:13168-79 (Pubitemid 350156954)
73. Kolykhalov AA, Agapov EV, Blight KJ, Mihalik K, Feinstone SM, Rice CM. 1997. Transmission of hepatitis C by intrahepatic inoculation with transcribed RNA. Science 277:570-74 (Pubitemid 27369006)
74. Kolykhalov AA, Feinstone SM, Rice CM. 1996. Identification of a highly conserved sequence element at the 3- terminus of hepatitis C virus genome RNA. J. Virol. 70:3363-71
75. KoutsoudakisG,Herrmann E, Kallis S, Bartenschlager R, Pietschmann T. 2007. The level of CD81 cell surface expression is a key determinant for productive entry of hepatitis C virus into host cells. J. Virol. 81:588-98 (Pubitemid 46067886)
76. Krieger N, Lohmann V, Bartenschlager R. 2001. Enhancement of hepatitis C virus RNA replication by cell culture-adaptive mutations. J. Virol. 75:4614-24 (Pubitemid 32381503)
77. Kuo G, Choo QL, Alter HJ, Gitnick GL, Redeker AG, et al. 1989. An assay for circulating antibodies to a major etiologic virus of human non-A, non-B hepatitis. Science 244:362-64 (Pubitemid 19117878)
78. Lanford RE, Guerra B, Lee H. 2006. Hepatitis C virus genotype 1b chimeric replicon containing genotype 3 NS5A domain. Virology 355:192-202 (Pubitemid 44692777)
79. Lanford RE, Guerra B, Lee H, Averett DR, Pfeiffer B, et al. 2003. 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. 77:1092-104 (Pubitemid 36055531)
80. Lanford RE, Lee H, Chavez D, Guerra B, Brasky KM. 2001. Infectious cDNA clone of the hepatitis C virus genotype 1 prototype sequence. J. Gen. Virol. 82:1291-97 (Pubitemid 32536635)
81. Lanford RE, Sureau C, Jacob JR, White R, Fuerst TR. 1994. Demonstration of in vitro infection of chimpanzee hepatocytes with hepatitis C virus using strand-specific RT/PCR. Virology 202:606-14 (Pubitemid 24254873)
82. Liang C, Rieder E, Hahm B, Jang SK, Paul A, Wimmer E. 2005. Replication of a novel subgenomic HCV genotype 1a replicon expressing a puromycin resistance gene in Huh-7 cells. Virology 333:41-53 (Pubitemid 40222189)
83. Liang Y, Shilagard T, Xiao SY, Snyder N, Lau D, et al. 2009. Visualizing hepatitis C virus infections in human liver by two-photon microscopy. Gastroenterology 137:1448-58
84. Lindenbach BD, Evans MJ, Syder AJ, Wolk B, Tellinghuisen TL, et al. 2005. Complete replication of hepatitis C virus in cell culture. Science 309:623-26 (Pubitemid 41033648)
85. Lindenbach BD, Meuleman P, Ploss A, Vanwolleghem T, Syder AJ, et al. 2006. Cell culture-grown hepatitis C virus is infectious in vivo and can be recultured in vitro. Proc. Natl. Acad. Sci. USA 103:3805-9 (Pubitemid 43376636)
86. Lindenbach BD, Rice CM. 2001. Flaviviridae: the viruses and their replication. In Fields Virology, ed. DM Knipe, PM Howley, pp. 991-1041. Philadelphia: Lippincott-Raven
87. Lohmann V, Hoffmann S, Herian U, Penin F, Bartenschlager R. 2003. Viral and cellular determinants of hepatitis C virus RNA replication in cell culture. J. Virol. 77:3007-19 (Pubitemid 36228086)
88. Lohmann V, Korner F, Dobierzewska A, Bartenschlager R. 2001. Mutations in hepatitis C virus RNAs conferring cell culture adaptation. J. Virol. 75:1437-49 (Pubitemid 32094702)
89. Lohmann V, Korner F, Koch JO, Herian U, Theilmann L, Bartenschlager R. 1999. Replication of subgenomic hepatitis C virus RNAs in a hepatoma cell line. Science 285:110-13 (Pubitemid 29307577)
90. Maekawa S, Enomoto N, Sakamoto N, Kurosaki M, Ueda E, et al. 2004. Introduction of NS5A mutations enables subgenomic HCV replicon derived from chimpanzee-infectious HC-J4 isolate to replicate efficiently in Huh-7 cells. J. Viral Hepat. 11:394-403 (Pubitemid 39336220)
91. Marukian S, Jones CT, Andrus L, Evans MJ, Ritola KD, et al. 2008. Cell culture-produced hepatitis C virus does not infect peripheral blood mononuclear cells. Hepatology 48:1843-50
92. Mateu G, Donis RO, Wakita T, Bukh J, Grakoui A. 2008. Intragenotypic JFH1 based recombinant hepatitis C virus produces high levels of infectious particles but causes increased cell death. Virology 376:397-407
93. McMullan LK, Grakoui A, Evans MJ, Mihalik K, Puig M, et al. 2007. Evidence for a functional RNA element in the hepatitis C virus core gene. Proc. Natl. Acad. Sci. USA 104:2879-84 (Pubitemid 46327973)
94. Mercer DF, Schiller DE, Elliott JF, Douglas DN, Hao C, et al. 2001. Hepatitis C virus replication in mice with chimeric human livers. Nat. Med. 7:927-33 (Pubitemid 32756430)
95. Meuleman P, Libbrecht L, De Vos R, de Hemptinne B, Gevaert K, et al. 2005. Morphological and biochemical characterization of a human liver in a uPA-SCID mouse chimera. Hepatology 41:847-56 (Pubitemid 40462948)
96. Miyamoto M, Kato T, Date T, Mizokami M, Wakita T. 2006. Comparison between subgenomic replicons of hepatitis C virus genotypes 2a ( JFH-1) and 1b (Con1 NK5.1). Intervirology 49:37-43 (Pubitemid 41318174)
97. Mori K, Abe K, Dansako H, Ariumi Y, Ikeda M, Kato N. 2008. New efficient replication system with hepatitis C virus genome derived from a patient with acute hepatitis C. Biochem. Biophys. Res. Commun. 371:104-9
98. Murayama A, Date T, Morikawa K, Akazawa D, Miyamoto M, et al. 2007. The NS3 helicase and NS5B-to-3-X regions are important for efficient hepatitis C virus strain JFH-1 replication inHuh7 cells. J. Virol. 81:8030-40
99. Murayama A, Weng L, Date T, Akazawa D, Tian X, et al. 2010. RNA polymerase activity and specific RNA structure are required for efficient HCV replication in cultured cells. PLoS Pathog. 6:e1000885
100. MurrayCL, JonesCT, RiceCM.2008. Architects of assembly: roles of Flaviviridae nonstructural proteins in virion morphogenesis. Nat. Rev. Microbiol. 6:699-708
101. Murray EM, Grobler JA, Markel EJ, Pagnoni MF, Paonessa G, et al. 2003. Persistent replication of hepatitis C virus replicons expressing the beta-lactamase reporter in subpopulations of highly permissive Huh7 cells. J. Virol. 77:2928-35 (Pubitemid 36228077)
102. Neddermann P, Quintavalle M, Di Pietro C, Clementi A, Cerretani M, et al. 2004. Reduction of hepatitis C virus NS5A hyperphosphorylation by selective inhibition of cellular kinases activates viral RNA replication in cell culture. J. Virol. 78:13306-14 (Pubitemid 39507835)
103. OgataN, Alter HJ,Miller RH, Purcell RH. 1991. Nucleotide sequence and mutation rate of theHstrain of hepatitis C virus. Proc. Natl. Acad. Sci. USA 88:3392-96 (Pubitemid 21916627)
104. Pflugheber J, Fredericksen B, Sumpter R Jr, Wang C, Ware F, et al. 2002. Regulation of PKR and IRF-1 during hepatitis C virus RNA replication. Proc. Natl. Acad. Sci. USA 99:4650-55 (Pubitemid 34286039)
105. Pietschmann T, Kaul A, Koutsoudakis G, Shavinskaya A, Kallis S, et al. 2006. Construction and characterization of infectious intragenotypic and intergenotypic hepatitis C virus chimeras. Proc. Natl. Acad. Sci. USA 103:7408-13 (Pubitemid 43727846)
106. Pietschmann T, Lohmann V, Kaul A, Krieger N,Rinck G, et al. 2002. Persistent and transient replication of full-length hepatitis C virus genomes in cell culture. J. Virol. 76:4008-21 (Pubitemid 34250565)
107. Pietschmann T, Lohmann V, Rutter G, Kurpanek K, Bartenschlager R. 2001. Characterization of cell lines carrying self-replicating hepatitis C virus RNAs. J. Virol. 75:1252-64 (Pubitemid 32094684)
108. Pietschmann T, Zayas M, Meuleman P, Long G, Appel N, et al. 2009. Production of infectious genotype 1b virus particles in cell culture and impairment by replication enhancing mutations. PLoS Pathog. 5:e1000475
109. Ploss A, Evans MJ, Gaysinskaya VA, Panis M, You H, et al. 2009. Human occludin is a hepatitis C virus entry factor required for infection of mouse cells. Nature 457:882-86
110. Ploss A, Khetani SR, Jones CT, Syder AJ, Trehan K, et al. 2010. Persistent hepatitis C virus infection in microscale primary human hepatocyte cultures. Proc. Natl. Acad. Sci. USA 107:3141-45
111. Russell RS, Kawaguchi K, Meunier JC, Takikawa S, Faulk K, et al. 2009. Mutational analysis of the hepatitis C virus E1 glycoprotein in retroviral pseudoparticles and cell-culture-derived H77/JFH1 chimeric infectious virus particles. J. Viral Hepat. 16:621-32
112. Russell RS, Meunier JC, Takikawa S, Faulk K, Engle RE, et al. 2008. Advantages of a single-cycle production assay to study cell culture-adaptive mutations of hepatitis C virus. Proc. Natl. Acad. Sci. USA 105:4370-75 (Pubitemid 351754387)
113. Sainz B Jr, Barretto N, Uprichard SL. 2009. Hepatitis C virus infection in phenotypically distinct Huh7 cell lines. PLoS One 4:e6561
114. Saito I, Miyamura T, Ohbayashi A, Harada H, Katayama T, et al. 1990. Hepatitis C virus infection is associated with the development of hepatocellular carcinoma. Proc. Natl. Acad. Sci. USA 87:6547-49
115. Sakai A, Takikawa S, Thimme R, Meunier JC, Spangenberg HC, et al. 2007. In vivo study of the HCTN strain of hepatitis C virus recovered from a patient with fulminant hepatitis: RNA transcripts of a molecular clone (pHC-TN) are infectious in chimpanzees but not in Huh7.5 cells. J. Virol. 81:7208-19 (Pubitemid 46986657)
116. Sarrazin C, Mihm U, Herrmann E,Welsch C, Albrecht M, et al. 2005. Clinical significance of in vitro replication-enhancing mutations of the hepatitis C virus (HCV) replicon in patients with chronic HCV infection. J. Infect. Dis. 192:1710-19 (Pubitemid 41587820)
117. Scheel TK, Gottwein JM, Jensen TB, Prentoe JC, Hoegh AM, et al. 2008. Development of JFH1-based cell culture systems for hepatitis C virus genotype 4a and evidence for cross-genotype neutralization. Proc. Natl. Acad. Sci. USA 105:997-1002 (Pubitemid 351282070)
118. Seipp S,Mueller HM, Pfaff E, StremmelW, Theilmann L, Goeser T. 1997. Establishment of persistent hepatitis C virus infection and replication in vitro. J. Gen. Virol. 78:2467-76 (Pubitemid 27469988)
119. Shepard CW, Finelli L, AlterMJ. 2005. Global epidemiology of hepatitis C virus infection. Lancet Infect. Dis. 5:558-67 (Pubitemid 41196755)
120. Shindo M, Di Bisceglie AM, Akatsuka T, Fong TL, Scaglione L, et al. 1994. The physical state of the negative strand of hepatitis C virus RNA in serum of patients with chronic hepatitis C. Proc. Natl. Acad. Sci. USA 91:8719-23 (Pubitemid 24273736)
121. Silberstein E,Mihalik K, Ulitzky L, Plant EP, Puig M, et al. 2010. Persistent growth of a human plasmaderived hepatitis C virus genotype 1b isolate in cell culture. PLoS Pathog. 6:e1000910
122. Simister P, Schmitt M, Geitmann M, Wicht O, Danielson UH, et al. 2009. Structural and functional analysis of hepatitis C virus strain JFH1 polymerase. J. Virol. 83:11926-39
123. Simmonds P. 2004. Genetic diversity and evolution of hepatitis C virus-15 years on. J. Gen. Virol. 85:3173-88 (Pubitemid 39445434)
124. Sumpter R Jr, Loo YM, Foy E, Li K, Yoneyama M, et al. 2005. Regulating intracellular antiviral defense and permissiveness to hepatitis C virus RNA replication through a cellular RNA helicase, RIG-I. J. Virol. 79:2689-99 (Pubitemid 40270547)
125. Sumpter R Jr, Wang C, Foy E, Loo YM, Gale M Jr. 2004. Viral evolution and interferon resistance of hepatitis C virus RNA replication in a cell culture model. J. Virol. 78:11591-604 (Pubitemid 39390745)
126. Tabor E, Garety RJ, Drucker JA, Seeff LB, Hoofnagle JF, et al. 1978. Transmission of non-A, non-B hepatitis from man to chimpanzee. Lancet 1:463-66 (Pubitemid 8286034)
127. Tagawa M, Kato N, Yokosuka O, Ishikawa T, OhtoM, Omata M. 1995. Infection of human hepatocyte cell lines with hepatitis C virus in vitro. J. Gastroenterol. Hepatol. 10:523-27
128. Tanaka T, Kato N, ChoM-J, Shimotohno K. 1995. A novel sequence found at the 3- terminus of hepatitis C virus genome. Biochem. Biophys. Res. Commun. 215:744-49
129. Tellinghuisen TL, Foss KL, Treadaway J. 2008. Regulation of hepatitis C virion production via phosphorylation of the NS5A protein. PLoS Pathog. 4:e1000032
130. Thomson M, Nascimbeni M, Gonzales S, Murthy KK, Rehermann B, Liang TJ. 2001. Emergence of a distinct pattern of viral mutations in chimpanzees infected with a homogeneous inoculum of hepatitis C virus. Gastroenterology 121:1226-33 (Pubitemid 33022104)
131. Tscherne DM, Evans MJ, von Hahn T, Jones CT, Stamataki Z, et al. 2007. Superinfection exclusion in cells infected with hepatitis C virus. J. Virol. 81:3693-703 (Pubitemid 46586866)
132. Tsuboi S, Nagamori S, Miyazaki M, Mihara K, Fukaya K, et al. 1996. Persistence of hepatitis C virus RNA in established human hepatocellular carcinoma cell lines. J. Med. Virol. 48:133-40 (Pubitemid 26063465)
133. Tu H, Gao L, Shi ST, Taylor DR, Yang T, et al. 1999. Hepatitis C virus RNA polymerase and NS5A complex with a SNARE-like protein. Virology 263:30-41 (Pubitemid 29493616)
134. Uprichard SL, Chung J, Chisari FV, Wakita T. 2006. Replication of a hepatitis C virus replicon clone in mouse cells. Virol. J. 3:89
135. Wakita T, Pietschmann T, Kato T, Date T, Miyamoto M, et al. 2005. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat. Med. 11:791-96 (Pubitemid 41021213)
136. Watashi K, Ishii N, Hijikata M, Inoue D, Murata T, et al. 2005. Cyclophilin B is a functional regulator of hepatitis C virus RNA polymerase. Mol. Cell 19:111-22 (Pubitemid 40884662)
137. Weng L, Du J, Zhou J, Ding J, Wakita T, et al. 2009. Modification of hepatitis C virus 1b RNA polymerase to make a highly active JFH1-type polymerase by mutation of the thumb domain. Arch. Virol. 154:765-73
138. Windisch MP, Frese M, Kaul A, Trippler M, Lohmann V, Bartenschlager R. 2005. Dissecting the interferon-induced inhibition of hepatitis C virus replication by using a novel host cell line. J. Virol. 79:13778-93 (Pubitemid 41508189)
139. Yanagi M, Purcell RH, Emerson SU, Bukh J. 1997. Transcripts from a single full-length cDNA clone of hepatitis C virus are infectious when directly transfected into the liver of a chimpanzee. Proc. Natl. Acad. Sci. USA 94:8738-43 (Pubitemid 27335109)
140. Yanagi M, Purcell RH, Emerson SU, Bukh J. 1999. Hepatitis C virus: an infectious molecular clone of a second major genotype (2a) and lack of viability of intertypic 1a and 2a chimeras. Virology 262:250-63 (Pubitemid 29455022)
141. Yanagi M, St. Claire M, Shapiro M, Emerson SU, Purcell RH, Bukh J. 1998. Transcripts of a chimeric cDNA clone of hepatitis C virus genotype 1b are infectious in vivo. Virology 244:161-72 (Pubitemid 28384135)
142. Yi M, Bodola F, Lemon SM. 2002. Subgenomic hepatitis C virus replicons inducing expression of a secreted enzymatic reporter protein. Virology 304:197-210 (Pubitemid 36069163)
143. Yi M, Lemon SM. 2004. Adaptive mutations producing efficient replication of genotype 1a hepatitis C virus RNA in normal Huh7 cells. J. Virol. 78:7904-15 (Pubitemid 38944276)
144. Yi M, Ma Y, Yates J, Lemon SM. 2007. Compensatory mutations in E1, p7, NS2, and NS3 enhance yields of cell culture-infectious intergenotypic chimeric hepatitis C virus. J. Virol. 81:629-38 (Pubitemid 46067890)
145. Yi M, Villanueva RA, Thomas DL, Wakita T, Lemon SM. 2006. Production of infectious genotype 1a hepatitis C virus (Hutchinson strain) in cultured human hepatoma cells. Proc. Natl. Acad. Sci. USA 103:2310-15 (Pubitemid 43271666)
146. Zhang Y,Weady P, Duggal R, Hao W. 2008. Novel chimeric genotype 1b/2a hepatitis C virus suitable for high-throughput screening. Antimicrob. Agents Chemother. 52:666-74 (Pubitemid 351170843)
147. Zhong J, Gastaminza P, Cheng G, Kapadia S, Kato T, et al. 2005. Robust hepatitis C virus infection in vitro. Proc. Natl. Acad. Sci. USA 102:9294-99 (Pubitemid 40923557)
148. Zhong J, Gastaminza P, Chung J, Stamataki Z, Isogawa M, et al. 2006. Persistent hepatitis C virus infection in vitro: coevolution of virus and host. J. Virol. 80:11082-93 (Pubitemid 44706549)
149. Zhu H, Dong H, Eksioglu E, Hemming A, Cao M, et al. 2007. Hepatitis C virus triggers apoptosis of a newly developed hepatoma cell line through antiviral defense system. Gastroenterology 133:1649-59 (Pubitemid 350029762)
150. Zhu Q, Guo JT, Seeger C. 2003. Replication of hepatitis C virus subgenomes in nonhepatic epithelial and mouse hepatoma cells. J. Virol. 77:9204-10 (Pubitemid 37011017)