Assays for RNA synthesis and replication by the hepatitis C virus
C. Cheng KAO, Baochang FAN, Sreedhar CHINNASWAMY, Hui CAI, C.T. RANJITH-KUMAR, Jerome DEVAL
Assays for RNA synthesis and replication by the hepatitis C virus
At least six major genotypes of Hepatitis C virus (HCV) cause liver diseases worldwide. The efficacy rates with current standard of care are about 50% against genotype 1, the most prevalent strain in the United States, Europe and Japan. Therefore more effective pan-genotypic therapies are needed. HCV RNA replication provides a number of validated targets for virus-specific and potentially pan-genotypic inhibitors. In vitro assays capturing the different steps of RNA synthesis are needed not only to identify new inhibitors, but also to examine their mechanisms of action. This review attempts to provide a comprehensive summary of the biochemical, cell-based and animal model systems to assess HCV polymerase activity and HCV RNA replication that should be useful for both basic research and applied studies.
assay / RNA synthesis and replication / hepatitis C virus
[1] |
AmakoY, Tsukiyama-KoharaK, KatsumeA, HirataY, SekiguchiS, TobitaY, HayashiY, HishimaT, FunataN, YonekawaH, KoharaM (2010). Pathogenesis of hepatitis C virus infection in Tupaia belangeri.J Virol, 84(1): 303-311
CrossRef
Pubmed
Google scholar
|
[2] |
AntonysamyS S, AubolB, BlaneyJ, BrownerM F, GiannettiA M, HarrisS F, HébertN, HendleJ, HopkinsS, JeffersonE, KissingerC, LevequeV, MarcianoD, McGeeE, NájeraI, NolanB, TomimotoM, TorresE, WrightT (2008). Fragment-based discovery of hepatitis C virus NS5b RNA polymerase inhibitors.Bioorg Med Chem Lett, 18(9): 2990-2995
CrossRef
Pubmed
Google scholar
|
[3] |
AriumiY, KurokiM, MakiM, IkedaM, DansakoH, WakitaT, KatoN (2011). The ESCRT system is required for hepatitis C virus production.PLoS ONE, 6(1): e14517
CrossRef
Pubmed
Google scholar
|
[4] |
BaconB R, GordonS C, LawitzE, MarcellinP, VierlingJ M, ZeuzemS, PoordadF,GoodmanZ D, SingsH L ,BoparaiN, BurroughsM, BrassC A, AlbrechtJ K ,EstebanR ,and the HCV RESPOND-2 Investigators (2011). Boceprevir for previously treated chronic HCV genotype 1 infection.N Engl J Med, 364(13): 1207-1217
CrossRef
Pubmed
Google scholar
|
[5] |
BartenschlagerR, SparacioS (2007). Hepatitis C virus molecular clones and their replication capacity in vivo and in cell culture.Virus Res, 127(2): 195-207
CrossRef
Pubmed
Google scholar
|
[6] |
BehrensS E, TomeiL, De FrancescoR (1996). Identification and properties of the RNA-dependent RNA polymerase of hepatitis C virus.EMBO J, 15(1): 12-22
Pubmed
|
[7] |
BensadounP, RodriguezC, SoulierA, HiggsM, ChevaliezS, PawlotskyJ M (2011). Genetic background of hepatocyte cell lines: are in vitro hepatitis C virus research data reliable?Hepatology, 54(2): 748
CrossRef
Pubmed
Google scholar
|
[8] |
BiswalB K, CherneyM M, WangM, ChanL, YannopoulosC G, BilimoriaD, NicolasO, BedardJ, JamesM N (2004). Crystal structures of the RNA-dependent RNA polymerase genotype 2a of hepatitis C virus reveal two conformations and suggest mechanisms of inhibition by non-nucleoside inhibitors.J Biol Chem, 280(18): 18202-18210
CrossRef
Pubmed
Google scholar
|
[9] |
BlightK J, McKeatingJ A, MarcotrigianoJ, RiceC M (2003). Efficient replication of hepatitis C virus genotype 1a RNAs in cell culture.J Virol, 77(5): 3181-3190
CrossRef
Pubmed
Google scholar
|
[10] |
BoonstraA, van der LaanL J, VanwolleghemT, JanssenH L (2009). Experimental models for hepatitis C viral infection.Hepatology, 50(5): 1646-1655
CrossRef
Pubmed
Google scholar
|
[11] |
BrassV, GouttenoireJ, WahlA, PalZ, BlumH E, PeninF, MoradpourD (2010). Hepatitis C virus RNA replication requires a conserved structural motif within the transmembrane domain of the NS5B RNA-dependent RNA polymerase.J Virol, 84(21): 11580-11584
CrossRef
Pubmed
Google scholar
|
[12] |
BressanelliS, TomeiL, RousselA, IncittiI, VitaleR L, MathieuM, De FrancescoR, ReyF A (1999). Crystal structure of the RNA-dependent RNA polymerase of hepatitis C virus.Proc Natl Acad Sci USA, 96(23): 13034-13039
CrossRef
Pubmed
Google scholar
|
[13] |
BuckM (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(7): e2660
CrossRef
Pubmed
Google scholar
|
[14] |
BukhJ (2004). A critical role for the chimpanzee model in the study of hepatitis C.Hepatology, 39(6): 1469-1475
CrossRef
Pubmed
Google scholar
|
[15] |
BurtonJ R Jr, EversonG T (2009). HCV NS5B polymerase inhibitors.Clin Liver Dis, 13(3): 453-465
CrossRef
Pubmed
Google scholar
|
[16] |
CarrollS S, TomassiniJ E, BossermanM, GettyK, StahlhutM W, EldrupA B, BhatB, HallD, SimcoeA L, LaFeminaR, RutkowskiC A, WolanskiB, YangZ, MigliaccioG, De FrancescoR, KuoL C, MacCossM, OlsenD B (2003). Inhibition of hepatitis C virus RNA replication by 2′-modified nucleoside analogs.J Biol Chem, 278(14): 11979-11984
CrossRef
Pubmed
Google scholar
|
[17] |
ChatterjiU, BobardtM, SelvarajahS, YangF, TangH, SakamotoN, VuagniauxG, ParkinsonT, GallayP (2009). The isomerase active site of cyclophilin A is critical for hepatitis C virus replication.J Biol Chem, 284(25): 16998-17005
CrossRef
Pubmed
Google scholar
|
[18] |
ChinnaswamyS, CaiH, KaoC (2010a). An update on small molecule inhibitors of the HCV NS5B polymerase: effects on RNA synthesis in vitro and in cultured cells, and potential resistance in viral quasispecies.Virus Adaptation and Treatment, 2: 73-89
|
[19] |
ChinnaswamyS, MuraliA, CaiH, YiG, PalaninathanS, KaoC C (2010b). Conformations of the monomeric Hepatitis C Virus RNA-dependent RNA Polymerase.Virus Treatments and Adaptation, 2: 21-39
|
[20] |
ChinnaswamyS, MuraliA, LiP, FujisakiK, KaoC C (2010c). Regulation of de novo-initiated RNA synthesis in hepatitis C virus RNA-dependent RNA polymerase by intermolecular interactions.J Virol, 84(12): 5923-5935
CrossRef
Pubmed
Google scholar
|
[21] |
ChinnaswamyS, YarbroughI, PalaninathanS, KumarC T, VijayaraghavanV, DemelerB, LemonS M, SacchettiniJ C, KaoC C (2008). A locking mechanism regulates RNA synthesis and host protein interaction by the hepatitis C virus polymerase.J Biol Chem, 283(29): 20535-20546
CrossRef
Pubmed
Google scholar
|
[22] |
ChooQ L, KuoG, WeinerA J, OverbyL R, BradleyD W, HoughtonM (1989). Isolation of a cDNA clone derived from a blood-borne non-A, non-B viral hepatitis genome.Science, 244(4902): 359-362
CrossRef
Pubmed
Google scholar
|
[23] |
Clemente-CasaresP, López-JiménezA J, Bellón-EcheverríaI, EncinarJ A, Martínez-AlfaroE, Pérez-FloresR, MasA (2011). De novo polymerase activity and oligomerization of hepatitis C virus RNA-dependent RNA-polymerases from genotypes 1 to 5.PLoS ONE, 6(4): e18515
CrossRef
Pubmed
Google scholar
|
[24] |
DevalJ, PowdrillM H, D’AbramoC M, CellaiL, GötteM (2007). Pyrophosphorolytic excision of nonobligate chain terminators by hepatitis C virus NS5B polymerase.Antimicrob Agents Chemother, 51(8): 2920-2928
CrossRef
Pubmed
Google scholar
|
[25] |
Di MarcoS, VolpariC, TomeiL, AltamuraS, HarperS, NarjesF, KochU, RowleyM, De FrancescoR, MigliaccioG, CarfíA (2005). Interdomain communication in hepatitis C virus polymerase abolished by small molecule inhibitors bound to a novel allosteric site.J Biol Chem, 280(33): 29765-29770
CrossRef
Pubmed
Google scholar
|
[26] |
DingC B, HangJ P, ZhaoY, PengZ G, SongD Q, JiangJ D (2011). Zebrafish as a potential model organism for drug test against hepatitis C virus. PLoS One, epub ahead of print: 6(8): e22921
|
[27] |
DivineyS, TuplinA, StruthersM, ArmstrongV, ElliottR M, SimmondsP, EvansD J (2008). A hepatitis C virus cis-acting replication element forms a long-range RNA-RNA interaction with upstream RNA sequences in NS5B.J Virol, 82(18): 9008-9022
CrossRef
Pubmed
Google scholar
|
[28] |
DornerM, HorwitzJ A, RobbinsJ B, BarryW T, FengQ, MuK, JonesC T, SchogginsJ W, CataneseM T, BurtonD R, LawM, RiceC M, PlossA (2011). A genetically humanized mouse model for hepatitis C virus infection.Nature, 474(7350): 208-211
CrossRef
Pubmed
Google scholar
|
[29] |
DouglasD N, KawaharaT, SisB, BondD, FischerK P, TyrrellD L, LewisJ T, KnetemanN M (2010). Therapeutic efficacy of human hepatocyte transplantation in a SCID/uPA mouse model with inducible liver disease.PLoS ONE, 5(2): e9209
CrossRef
Pubmed
Google scholar
|
[30] |
DutartreH, BussettaC, BorettoJ, CanardB (2006). General catalytic deficiency of hepatitis C virus RNA polymerase with an S282T mutation and mutually exclusive resistance towards 2′-modified nucleotide analogues.Antimicrob Agents Chemother, 50(12): 4161-4169
CrossRef
Pubmed
Google scholar
|
[31] |
EggerD, WölkB, GosertR, BianchiL, BlumH E, MoradpourD, BienzK (2002). Expression of hepatitis C virus proteins induces distinct membrane alterations including a candidate viral replication complex.J Virol, 76(12): 5974-5984
CrossRef
Pubmed
Google scholar
|
[32] |
EI-SeragH B (2004). Hepatocellular carcinoma: recent trends in the United States.Gastroenterology, 127(5 Suppl 1): S27-S34
CrossRef
Pubmed
Google scholar
|
[33] |
FreseM, SchwärzleV, BarthK, KriegerN, LohmannV, MihmS, HallerO, BartenschlagerR (2002). Interferon-gamma inhibits replication of subgenomic and genomic hepatitis C virus RNAs.Hepatology, 35(3): 694-703
CrossRef
Pubmed
Google scholar
|
[34] |
GaleM Jr, FoyE M (2005). Evasion of intracellular host defence by hepatitis C virus.Nature, 436(7053): 939-945
CrossRef
Pubmed
Google scholar
|
[35] |
GaleM Jr, SenG C (2009). Viral evasion of the interferon system.J Interferon Cytokine Res, 29(9): 475-476
CrossRef
Pubmed
Google scholar
|
[36] |
GeD, FellayJ, ThompsonA J, SimonJ S, ShiannaK V, UrbanT J, HeinzenE L, QiuP, BertelsenA H, MuirA J, SulkowskiM, McHutchisonJ G, GoldsteinD B (2009). Genetic variation in IL28B predicts hepatitis C treatment-induced viral clearance.Nature, 461(7262): 399-401
CrossRef
Pubmed
Google scholar
|
[37] |
MoH, HebnerC, HarrisJBaeA,WongK, DelaneyW, OldachD, MillerMD (2011). Characterization of viral resistance mutations in genotype 1 HCV patients receiving combination therapy with a protease inhibitor and a polymerase inhibitor with or without Ribavirin Gilead. EASL 46th Annual Meeting. Apr 3rd2011
|
[38] |
GrakouiA, HansonH L, RiceC M (2001). Bad time for Bonzo? Experimental models of hepatitis C virus infection, replication, and pathogenesis.Hepatology, 33(3): 489-495
CrossRef
Pubmed
Google scholar
|
[39] |
HangJ Q, YangY, HarrisS F, LevequeV, WhittingtonH J, RajyaguruS, Ao-IeongG, McCownM F, WongA, GiannettiA M, Le PogamS, TalamásF, CammackN, NájeraI, KlumppK (2009). Slow binding inhibition and mechanism of resistance of non-nucleoside polymerase inhibitors of hepatitis C virus.J Biol Chem, 284(23): 15517-15529
CrossRef
Pubmed
Google scholar
|
[40] |
HardyR W, MarcotrigianoJ, BlightK J, MajorsJ E, RiceC M (2003). Hepatitis C virus RNA synthesis in a cell-free system isolated from replicon-containing hepatoma cells.J Virol, 77(3): 2029-2037
CrossRef
Pubmed
Google scholar
|
[41] |
HarrusD, Ahmed-El-SayedN, SimisterP C, MillerS, TriconnetM, HagedornC H, MahiasK, ReyF A, Astier-GinT, BressanelliS (2010). Further insights into the roles of GTP and the C terminus of the hepatitis C virus polymerase in the initiation of RNA synthesis.J Biol Chem, 285(43): 32906-32918
CrossRef
Pubmed
Google scholar
|
[42] |
HeckJ A, LamA M, NarayananN, FrickD N (2008). Effects of mutagenic and chain-terminating nucleotide analogs on enzymes isolated from hepatitis C virus strains of various genotypes.Antimicrob Agents Chemother, 52(6): 1901-1911
CrossRef
Pubmed
Google scholar
|
[43] |
HorscroftN, LaiV C, CheneyW, YaoN, WuJ Z, HongZ, ZhongW (2005). Replicon cell culture system as a valuable tool in antiviral drug discovery against hepatitis C virus.Antivir Chem Chemother, 16(1): 1-12
Pubmed
|
[44] |
HsuM, ZhangJ, FlintM, LogvinoffC, Cheng-MayerC, RiceC M, McKeatingJ A (2003). Hepatitis C virus glycoproteins mediate pH-dependent cell entry of pseudotyped retroviral particles.Proc Natl Acad Sci USA, 100(12): 7271-7276
CrossRef
Pubmed
Google scholar
|
[45] |
HsuN Y, IlnytskaO, BelovG, SantianaM, ChenY H, TakvorianP M, PauC, van der SchaarH, Kaushik-BasuN, BallaT, CameronC E, EhrenfeldE, van KuppeveldF J, Altan-BonnetN (2010). Viral reorganization of the secretory pathway generates distinct organelles for RNA replication.Cell, 141(5): 799-811
CrossRef
Pubmed
Google scholar
|
[46] |
HuangH, SunF, OwenD M, LiW, ChenY, GaleM Jr, YeJ (2007). Hepatitis C virus production by human hepatocytes dependent on assembly and secretion of very low-density lipoproteins.Proc Natl Acad Sci USA, 104(14): 5848-5853
CrossRef
Pubmed
Google scholar
|
[47] |
IlanE, AraziJ, NussbaumO, ZaubermanA, ErenR, LubinI, NevilleL, Ben-MosheO, KischitzkyA, LitchiA, MargalitI, GopherJ, MounirS, CaiW, DaudiN, EidA, JurimO, CzerniakA, GalunE, DaganS (2002). The hepatitis C virus (HCV)-Trimera mouse: a model for evaluation of agents against HCV.J Infect Dis, 185(2): 153-161
CrossRef
Pubmed
Google scholar
|
[48] |
JoplingC L, YiM, LancasterA M, LemonS M, SarnowP (2005). Modulation of hepatitis C virus RNA abundance by a liver-specific MicroRNA.Science, 309(5740): 1577-1581
CrossRef
Pubmed
Google scholar
|
[49] |
KaoC C, YangX, KlineA, WangQ M, BarketD, HeinzB A (2000). Template requirements for RNA synthesis by a recombinant hepatitis C virus RNA-dependent RNA polymerase.J Virol, 74(23): 11121-11128
CrossRef
Pubmed
Google scholar
|
[50] |
KatoN, MoriK, AbeK, DansakoH, KurokiM, AriumiY, WakitaT, IkedaM (2009). Efficient replication systems for hepatitis C virus using a new human hepatoma cell line.Virus Res, 146(1-2): 41-50
CrossRef
Pubmed
Google scholar
|
[51] |
KhromykhA A, WestawayE G (1997). Subgenomic replicons of the flavivirus Kunjin: construction and applications.J Virol, 71(2): 1497-1505
Pubmed
|
[52] |
KlumppK, LévêqueV, Le PogamS, MaH, JiangW R, KangH, GranycomeC, SingerM, LaxtonC, HangJ Q, SarmaK, SmithD B, HeindlD, HobbsC J, MerrettJ H, SymonsJ, CammackN, MartinJ A, DevosR, NájeraI (2006). The novel nucleoside analog R1479 (4′-azidocytidine) is a potent inhibitor of NS5B-dependent RNA synthesis and hepatitis C virus replication in cell culture.J Biol Chem, 281(7): 3793-3799
CrossRef
Pubmed
Google scholar
|
[53] |
KoutsoudakisG, HerrmannE, KallisS, BartenschlagerR, PietschmannT (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(2): 588-598
CrossRef
Pubmed
Google scholar
|
[54] |
KriegerN, LohmannV, BartenschlagerR (2001). Enhancement of hepatitis C virus RNA replication by cell culture-adaptive mutations.J Virol, 75(10): 4614-4624
CrossRef
Pubmed
Google scholar
|
[55] |
LeeJ C, TsengC K, ChenK J, HuangK J, LinC K, LinY T (2010). A cell-based reporter assay for inhibitor screening of hepatitis C virus RNA-dependent RNA polymerase.Anal Biochem, 403(1-2): 52-62
CrossRef
Pubmed
Google scholar
|
[56] |
LesburgC A, CableM B, FerrariE, HongZ, MannarinoA F, WeberP C (1999). Crystal structure of the RNA-dependent RNA polymerase from hepatitis C virus reveals a fully encircled active site.Nat Struct Biol, 6(10): 937-943
CrossRef
Pubmed
Google scholar
|
[57] |
LindenbachB D, EvansM J, SyderA J, WölkB, TellinghuisenT L, LiuC C, MaruyamaT, HynesR O, BurtonD R, McKeatingJ A, RiceC M (2005). Complete replication of hepatitis C virus in cell culture.Science, 309(5734): 623-626
CrossRef
Pubmed
Google scholar
|
[58] |
LindenbachB D, MeulemanP, PlossA, VanwolleghemT, SyderA J, McKeatingJ A, LanfordR E, FeinstoneS M, MajorM E, Leroux-RoelsG, RiceC M (2006). Cell culture-grown hepatitis C virus is infectious in vivo and can be recultured in vitro.Proc Natl Acad Sci USA, 103(10): 3805-3809
CrossRef
Pubmed
Google scholar
|
[59] |
LohmannV, KörnerF, DobierzewskaA, BartenschlagerR (2001). Mutations in hepatitis C virus RNAs conferring cell culture adaptation.J Virol, 75(3): 1437-1449
CrossRef
Pubmed
Google scholar
|
[60] |
LohmannV, KörnerF, HerianU, BartenschlagerR (1997). 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(11): 8416-8428
Pubmed
|
[61] |
LohmannV, KörnerF, KochJ, HerianU, TheilmannL, BartenschlagerR (1999). Replication of subgenomic hepatitis C virus RNAs in a hepatoma cell line.Science, 285(5424): 110-113
CrossRef
Pubmed
Google scholar
|
[62] |
LoveR A, PargeH E, YuX, HickeyM J, DiehlW, GaoJ, WriggersH, EkkerA, WangL, ThomsonJ A, DragovichP S, FuhrmanS A (2003). Crystallographic identification of a noncompetitive inhibitor binding site on the hepatitis C virus NS5B RNA polymerase enzyme.J Virol, 77(13): 7575-7581
CrossRef
Pubmed
Google scholar
|
[63] |
LuC, XuH, Ranjith-KumarC T, BrooksM T, HouT Y, HuF, HerrA B, StrongR K, KaoC C, LiP (2010). The structural basis of 5′ triphosphate double-stranded RNA recognition by RIG-I C-terminal domain.Structure, 18(8): 1032-1043
CrossRef
Pubmed
Google scholar
|
[64] |
LuoG, HamatakeR K, MathisD M, RacelaJ, RigatK L, LemmJ, ColonnoR J (2000). De novo initiation of RNA synthesis by the RNA-dependent RNA polymerase (NS5B) of hepatitis C virus.J Virol, 74(2): 851-863
CrossRef
Pubmed
Google scholar
|
[65] |
MaH, LevequeV, De WitteA, LiW, HendricksT, ClausenS M, CammackN, KlumppK (2005). Inhibition of native hepatitis C virus replicase by nucleotide and non-nucleoside inhibitors.Virology, 332(1): 8-15
CrossRef
Pubmed
Google scholar
|
[66] |
McLauchlanJ (2009). Hepatitis C virus: viral proteins on the move.Biochem Soc Trans, 37(5): 986-990
CrossRef
Pubmed
Google scholar
|
[67] |
MeanwellN A, KadowJ F, ScolaP M (2009). Chapter 20, Progress towards the discovery and development of specifically targeted inhibitors of hepatitis C virus. Ann Reports in Med Chem,44:397-440
|
[68] |
MercerD F, SchillerD E, ElliottJ F, DouglasD N, HaoC, RinfretA, AddisonW R, FischerK P, ChurchillT A, LakeyJ R, TyrrellD L, KnetemanN M (2001). Hepatitis C virus replication in mice with chimeric human livers.Nat Med, 7(8): 927-933
CrossRef
Pubmed
Google scholar
|
[69] |
MicallefJ M, KaldorJ M, DoreG J (2006). Spontaneous viral clearance following acute hepatitis C infection: a systematic review of longitudinal studies.J Viral Hepat, 13(1): 34-41
CrossRef
Pubmed
Google scholar
|
[70] |
MoradpourD, EvansM J, GosertR, YuanZ, BlumH E, GoffS P, LindenbachB D, RiceC M (2004). Insertion of green fluorescent protein into nonstructural protein 5A allows direct visualization of functional hepatitis C virus replication complexes.J Virol, 78(14): 7400-7409
CrossRef
Pubmed
Google scholar
|
[71] |
MoradpourD, PeninF, RiceC M (2007). Replication of hepatitis C virus.Nat Rev Microbiol, 5(6): 453-463
CrossRef
Pubmed
Google scholar
|
[72] |
MoriishiK, MatsuuraY (2007). Host factors involved in the replication of hepatitis C virus.Rev Med Virol, 17(5): 343-354
CrossRef
Pubmed
Google scholar
|
[73] |
MunakataT, LiangY, KimS, McGivernD R, HuibregtseJ, NomotoA, LemonS M (2007). Hepatitis C virus induces E6AP-dependent degradation of the retinoblastoma protein.PLoS Pathog, 3(9): 1335-1347
CrossRef
Pubmed
Google scholar
|
[74] |
MurakamiE, NiuC, BaoH, Micolochick SteuerH M, WhitakerT, NachmanT, SofiaM A, WangP, OttoM J, FurmanP A (2008). The mechanism of action of beta-D-2′-deoxy-2′-fluoro-2′-C-methylcytidine involves a second metabolic pathway leading to beta-D-2′-deoxy-2′-fluoro-2′-C-methyluridine 5′-triphosphate, a potent inhibitor of the hepatitis C virus RNA-dependent RNA polymerase.Antimicrob Agents Chemother, 52(2): 458-464
CrossRef
Pubmed
Google scholar
|
[75] |
NyanguileO, DevogelaereB, VijgenL, Van den BroeckW, PauwelsF, CummingsM D, De BondtH L, VosA M, BerkeJ M, LenzO, VandercruyssenG, VermeirenK, MostmansW, DehertoghP, DelouvroyF, VendevilleS, VanDyckK, DockxK, CleirenE, RaboissonP, SimmenK A, FanningG C (2010). 1a/1b subtype profiling of nonnucleoside polymerase inhibitors of hepatitis C virus.J Virol, 84(6): 2923-2934
CrossRef
Pubmed
Google scholar
|
[76] |
O’FarrellD, TrowbridgeR, RowlandsD, JägerJ (2003). Substrate complexes of hepatitis C virus RNA polymerase (HC-J4): structural evidence for nucleotide import and de-novo initiation.J Mol Biol, 326(4): 1025-1035
CrossRef
Pubmed
Google scholar
|
[77] |
OhJ W, ItoT, LaiM M (1999). A recombinant hepatitis C virus RNA-dependent RNA polymerase capable of copying the full-length viral RNA.J Virol, 73(9): 7694-7702
Pubmed
|
[78] |
OlsenD B, EldrupA B, BartholomewL, BhatB, BossermanM R, CeccacciA, ColwellL F, FayJ F, FloresO A, GettyK L, GroblerJ A, LaFeminaR L, MarkelE J, MigliaccioG, PrhavcM, StahlhutM W, TomassiniJ E, MacCossM, HazudaD J, CarrollS S (2004). A 7-deaza-adenosine analog is a potent and selective inhibitor of hepatitis C virus replication with excellent pharmacokinetic properties.Antimicrob Agents Chemother, 48(10): 3944-3953
CrossRef
Pubmed
Google scholar
|
[79] |
PangP S, PlanetP J, GlennJ S (2009). The evolution of the major hepatitis C genotypes correlates with clinical response to interferon therapy.PLoS ONE, 4(8): e6579
CrossRef
Pubmed
Google scholar
|
[80] |
PauwelsF, MostmansW, QuirynenL M, Mm van derHelmL, BouttonC W, RueffA, CleirenE, RaboissonP, SurlerauxD, NyanguileO, SimmonK A (2007). Binding-site identification and genotypic profiling of hepatitis C virus polymerase inhibitors. J Virol. 81:6909-6919Pichlmair A, Schulz O, Tan CP, Näslund TI, Liljeström P, Weber F, Reis e Sousa C (2006). RIG-I-mediated antiviral responses to single-stranded RNA bearing 5′-phosphates.Science, 314(5801): 997-1001
|
[81] |
PichlmairASchulzO, TanCP, NäslundTL, LiljeströmP, WeberF,
|
[82] |
PietschmannT, KaulA, KoutsoudakisG, ShavinskayaA, KallisS, SteinmannE, AbidK, NegroF, DreuxM, CossetF L, BartenschlagerR (2006). Construction and characterization of infectious intragenotypic and intergenotypic hepatitis C virus chimeras.Proc Natl Acad Sci USA, 103(19): 7408-7413
CrossRef
Pubmed
Google scholar
|
[83] |
PietschmannT, LohmannV, RutterG, KurpanekK, BartenschlagerR (2001). Characterization of cell lines carrying self-replicating hepatitis C virus RNAs.J Virol, 75(3): 1252-1264
CrossRef
Pubmed
Google scholar
|
[84] |
PrinceA M, BrotmanB, LeeD H, RenL, MooreB S, ScheffelJ W (1999). Significance of the anti-E2 response in self-limited and chronic hepatitis C virus infections in chimpanzees and in humans.J Infect Dis, 180(4): 987-991
CrossRef
Pubmed
Google scholar
|
[85] |
Ranjith-KumarC T, GutshallL, KimM J, SariskyR T, KaoC C (2002). Requirements for de novo initiation of RNA synthesis by recombinant flaviviral RNA-dependent RNA polymerases.J Virol, 76(24): 12526-12536
CrossRef
Pubmed
Google scholar
|
[86] |
Ranjith-KumarC T, WenY, BaxterN, BhardwajK, Cheng KaoC (2011). A cell-based assay for RNA synthesis by the HCV polymerase reveals new insights on mechanism of polymerase inhibitors and modulation by NS5A.PLoS ONE, 6(7): e22575
CrossRef
Pubmed
Google scholar
|
[87] |
RhimJ A, SandgrenE P, DegenJ L, PalmiterR D, BrinsterR L (1994). Replacement of diseased mouse liver by hepatic cell transplantation.Science, 263(5150): 1149-1152
CrossRef
Pubmed
Google scholar
|
[88] |
SaitoT, OwenD M, JiangF, MarcotrigianoJ, GaleM Jr (2008). Innate immunity induced by composition-dependent RIG-I recognition of hepatitis C virus RNA.Nature, 454(7203): 523-527
CrossRef
Pubmed
Google scholar
|
[89] |
SarrazinC, KiefferT L, BartelsD, HanzelkaB, MühU, WelkerM, WincheringerD, ZhouY, ChuH M, LinC, WeeginkC, ReesinkH, ZeuzemS, KwongA D (2007). Dynamic hepatitis C virus genotypic and phenotypic changes in patients treated with the protease inhibitor telaprevir.Gastroenterology, 132(5): 1767-1777
CrossRef
Pubmed
Google scholar
|
[90] |
ShiS T, HerlihyK J, GrahamJ P, FuhrmanS A, DoanC, PargeH, HickeyM, GaoJ, YuX, ChauF, GonzalezJ, LiH, LewisC, PatickA K, DuggalR (2008). In vitro resistance study of AG-021541, a novel nonnucleoside inhibitor of the hepatitis C virus RNA-dependent RNA polymerase.Antimicrob Agents Chemother, 52(2): 675-683
CrossRef
Pubmed
Google scholar
|
[91] |
ShimakamiT, HondaM, KusakawaT, MurataT, ShimotohnoK, KanekoS, MurakamiS (2006). Effect of hepatitis C virus (HCV) NS5B-nucleolin interaction on HCV replication with HCV subgenomic replicon.J Virol, 80(7): 3332-3340
CrossRef
Pubmed
Google scholar
|
[92] |
ShimakamiT, LanfordR E, LemonS M (2009). Hepatitis C: recent successes and continuing challenges in the development of improved treatment modalities.Curr Opin Pharmacol, 9(5): 537-544
CrossRef
Pubmed
Google scholar
|
[93] |
SimmondsP, BukhJ, CombetC, DeléageG, EnomotoN, FeinstoneS, HalfonP, InchauspéG, KuikenC, MaertensG, MizokamiM, MurphyD G, OkamotoH, PawlotskyJ M, PeninF, SablonE, Shin-IT, StuyverL J, ThielH J, ViazovS, WeinerA J, WidellA (2005). Consensus proposals for a unified system of nomenclature of hepatitis C virus genotypes.Hepatology, 42(4): 962-973
CrossRef
Pubmed
Google scholar
|
[94] |
SteitzT A (1999). DNA polymerases: structural diversity and common mechanisms.J Biol Chem, 274(25): 17395-17398
CrossRef
Pubmed
Google scholar
|
[95] |
SumpterR Jr, LooY M, FoyE, LiK, YoneyamaM, FujitaT, LemonS M, GaleM Jr (2005). Regulating intracellular antiviral defense and permissiveness to hepatitis C virus RNA replication through a cellular RNA helicase, RIG-I.J Virol, 79(5): 2689-2699
CrossRef
Pubmed
Google scholar
|
[96] |
SunX L, JohnsonR B, HockmanM A, WangQ M (2000). De novo RNA synthesis catalyzed by HCV RNA-dependent RNA polymerase.Biochem Biophys Res Commun, 268(3): 798-803
CrossRef
Pubmed
Google scholar
|
[97] |
TatenoC, YoshizaneY, SaitoN, KataokaM, UtohR, YamasakiC, TachibanaA, SoenoY, AsahinaK, HinoH, AsaharaT, YokoiT, FurukawaT, YoshizatoK (2004). Near completely humanized liver in mice shows human-type metabolic responses to drugs.Am J Pathol, 165(3): 901-912
CrossRef
Pubmed
Google scholar
|
[98] |
TheofilopoulosA N, BaccalaR, BeutlerB, KonoD H (2005). Type I interferons (alpha/beta) in immunity and autoimmunity.Annu Rev Immunol, 23(1): 307-335
CrossRef
Pubmed
Google scholar
|
[99] |
ThomasD L, ThioC L, MartinM P, QiY, GeD, O’HuiginC, KiddJ, KiddK, KhakooS I, AlexanderG, GoedertJ J, KirkG D, DonfieldS M, RosenH R, ToblerL H, BuschM P, McHutchisonJ G, GoldsteinD B, CarringtonM (2009). Genetic variation in IL28B and spontaneous clearance of hepatitis C virus.Nature, 461(7265): 798-801
CrossRef
Pubmed
Google scholar
|
[100] |
TomassiniJ E, BootsE, GanL, GrahamP, MunshiV, WolanskiB, FayJ F, GettyK, LaFeminaR (2003). An in vitro Flaviviridae replicase system capable of authentic RNA replication.Virology, 313(1): 274-285
CrossRef
Pubmed
Google scholar
|
[101] |
TomeiL, AltamuraS, BartholomewL, BiroccioA, CeccacciA, PaciniL, NarjesF, GennariN, BisbocciM, IncittiI, OrsattiL, HarperS, StansfieldI, RowleyM, De FrancescoR, MigliaccioG (2003). Mechanism of action and antiviral activity of benzimidazole-based allosteric inhibitors of the hepatitis C virus RNA-dependent RNA polymerase.J Virol, 77(24): 13225-13231
CrossRef
Pubmed
Google scholar
|
[102] |
TomeiL, VitaleR L, IncittiI, SerafiniS, AltamuraS, VitelliA, De FrancescoR (2000). Biochemical characterization of a hepatitis C virus RNA-dependent RNA polymerase mutant lacking the C-terminal hydrophobic sequence.J Gen Virol, 81(Pt 3): 759-767
Pubmed
|
[103] |
TriyatniM, BergerE A, SaunierB (2011). A new model to produce infectious hepatitis C virus without the replication requirement.PLoS Pathog, 7(4): e1001333
CrossRef
Pubmed
Google scholar
|
[104] |
van DijkA A, MakeyevE V, BamfordD H (2004). Initiation of viral RNA-dependent RNA polymerization.J Gen Virol, 85(5): 1077-1093
CrossRef
Pubmed
Google scholar
|
[105] |
VrolijkJ M, KaulA, HansenB E, LohmannV, HaagmansB L, SchalmS W, BartenschlagerR (2003). A replicon-based bioassay for the measurement of interferons in patients with chronic hepatitis C.J Virol Methods, 110(2): 201-209
CrossRef
Pubmed
Google scholar
|
[106] |
WakitaT, PietschmannT, KatoT, DateT, MiyamotoM, ZhaoZ, MurthyK, HabermannA, KräusslichH G, MizokamiM, BartenschlagerR, LiangT J (2005). Production of infectious hepatitis C virus in tissue culture from a cloned viral genome.Nat Med, 11(7): 791-796
CrossRef
Pubmed
Google scholar
|
[107] |
WakitaT, TayaC, KatsumeA, KatoJ, YonekawaH, KanegaeY, SaitoI, HayashiY, KoikeM, KoharaM (1998). Efficient conditional transgene expression in hepatitis C virus cDNA transgenic mice mediated by the Cre/loxP system.J Biol Chem, 273(15): 9001-9006
CrossRef
Pubmed
Google scholar
|
[108] |
WangQ M, HockmanM A, StaschkeK, JohnsonR B, CaseK A, LuJ, ParsonsS, ZhangF, RathnachalamR, KirkegaardK, ColacinoJ M (2002). Oligomerization and cooperative RNA synthesis activity of hepatitis C virus RNA-dependent RNA polymerase.J Virol, 76(8): 3865-3872
CrossRef
Pubmed
Google scholar
|
[109] |
WangQ M, JohnsonR B, ChenD, LévêqueV J, RenJ, HockmanM A, AbeK, HachisuT, KondoY, IsakaY, SatoA, FujiwaraT (2004). Expression and purification of untagged full-length HCV NS5B RNA-dependent RNA polymerase.Protein Expr Purif, 35(2): 304-312
CrossRef
Pubmed
Google scholar
|
[110] |
WasleyA, AlterM J (2000). Epidemiology of hepatitis C: geographic differences and temporal trends.Semin Liver Dis, 20(1): 1-16
CrossRef
Pubmed
Google scholar
|
[111] |
WengL, HirataY, AraiM, KoharaM, WakitaT, WatashiK, ShimotohnoK, HeY, ZhongJ, ToyodaT (2010). Sphingomyelin activates hepatitis C virus RNA polymerase in a genotype-specific manner.J Virol, 84(22): 11761-11770
CrossRef
Pubmed
Google scholar
|
[112] |
YiM, BodolaF, LemonS M (2002). Subgenomic hepatitis C virus replicons inducing expression of a secreted enzymatic reporter protein.Virology, 304(2): 197-210
CrossRef
Pubmed
Google scholar
|
[113] |
YiM, VillanuevaR A, ThomasD L, WakitaT, LemonS M (2006). Production of infectious genotype 1a hepatitis C virus (Hutchinson strain) in cultured human hepatoma cells.Proc Natl Acad Sci USA, 103(7): 2310-2315
CrossRef
Pubmed
Google scholar
|
[114] |
ZeuzemS, AndreoneP, PolS, LawitzE, DiagoM, RobertsS, FocacciaR, YounossiZ, FosterG R, HorbanA, FerenciP, NevensF, MüllhauptB, PockrosP, TergR, ShouvalD, van HoekB, WeilandO, Van HeeswijkR, De MeyerS, LuoD, BoogaertsG, PoloR, PicchioG, BeumontM, and the REALIZE Study Team (2011). Telaprevir for retreatment of HCV infection.N Engl J Med, 364(25): 2417-2428
CrossRef
Pubmed
Google scholar
|
[115] |
ZhongJ, GastaminzaP, ChengG, KapadiaS, KatoT, BurtonD R, WielandS F, UprichardS L, WakitaT, ChisariF V (2005). Robust hepatitis C virus infection in vitro.Proc Natl Acad Sci USA, 102(26): 9294-9299
CrossRef
Pubmed
Google scholar
|
[116] |
ZhongW, UssA S, FerrariE, LauJ Y, HongZ (2000). De novo initiation of RNA synthesis by hepatitis C virus nonstructural protein 5B polymerase.J Virol, 74(4): 2017-2022
CrossRef
Pubmed
Google scholar
|
[117] |
ZonL I, PetersonR T (2005). In vivo drug discovery in the zebrafish.Nat Rev Drug Discov, 4(1): 35-44
CrossRef
Pubmed
Google scholar
|
/
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