New hepatitis C virus drug discovery strategies and model systems

Expert Opinion on Drug Discovery

Volumn 7, Issue 9, 2012, Pages 849-859

  Hussain, Snawar ^a   Barretto, Naina ^a   Uprichard, Susan L ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

antivirals; experimental model systems; HCV pseudoparticles (HCVpp); hepatitis C virus (HCV); high throughput screening (HTS); replicons

Indexed keywords

ANTIVIRUS AGENT; BOCEPREVIR; NONSTRUCTURAL PROTEIN 3; PEGINTERFERON ALPHA; RIBAVIRIN; SMALL INTERFERING RNA; TELAPREVIR;

CELL ASSAY; CHEMICAL ANALYSIS; DECOMPENSATED LIVER CIRRHOSIS; DRUG EFFICACY; DRUG TOLERABILITY; GENOTYPE; HEPATITIS C; HEPATITIS C VIRUS; HIGH THROUGHPUT SCREENING; HUMAN; LIVER CELL CARCINOMA; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; PSEUDOTYPING; REPLICON; REPORTER GENE; REVIEW; VIRUS CULTURE; VIRUS ENTRY; VIRUS GENOME; VIRUS PARTICLE;

ANIMALS; ANTIVIRAL AGENTS; DRUG DISCOVERY; HEPACIVIRUS; HEPATITIS C, CHRONIC; HUMANS; MODELS, BIOLOGICAL; REPLICON;

EID: 84865447874     PISSN: 17460441     EISSN: 1746045X     Source Type: Journal    
DOI: 10.1517/17460441.2012.711312     Document Type: Review

References (109)

1. Alter MJ Epidemiology of hepatitis C virus infection. World J Gastroenterol 2007;13(17):2436-41
2. Hoofnagle JH Course and outcome of hepatitis C. Hepatology 2002;36(5 Suppl 1):S21-9
3. Seeff LB Natural history of chronic hepatitis C. Hepatology 2002;36(5 Suppl 1):S35-46
4. Willems M, Metselaar HJ, Tilanus HW, et al. Liver transplantation and hepatitis C. Transpl Int 2002;15(2-3):61-72
5. McHutchison JG Understanding hepatitis C. Am J Manag Care 2004;10(2 Suppl):S21-9
6. Ghany MG, Nelson DR, Strader DB, et al. An update on treatment of genotype 1 chronic hepatitis C virus infection: 2011 practice guideline by the American Association for the Study of Liver Diseases. Hepatology 2011;54(4):1433-44
7. Tencate V, Sainz B Jr, Cotler SJ, Uprichard SL Potential treatment options and future research to increase hepatitis C virus treatment response rate. Hepat Med 2010;2010(2):125-45
8. Suzuki T, Aizaki H, Murakami K, et al. Molecular biology of hepatitis C virus. J Gastroenterol 2007;42(6):411-23
9. Suzuki T, Ishii K, Aizaki H, Wakita T Hepatitis C viral life cycle. Adv Drug Deliv Rev 2007;59(12):1200-12
10. Poenisch M, Bartenschlager R New insights into structure and replication of the hepatitis C virus and clinical implications. Semin Liver Dis 2012;30(4):333-47
11. Popescu CI, Dubuisson J Role of lipid metabolism in hepatitis C virus assembly and entry. Biol Cell 2009;102(1):63-74
12. Bartenschlager R, Penin F, Lohmann V, Andre P Assembly of infectious hepatitis C virus particles. Trends Microbiol 2011;19(2):95-103
13. Lindenbach BD, Evans MJ, Syder AJ, et al. Complete replication of hepatitis C virus in cell culture. Science 2005;309(5734):623-6
14. Zhong J, Gastaminza P, Chung J, et al. Persistent hepatitis C virus infection in vitro: coevolution of virus and host. J Virol 2006;80(22):11082-93
15. Haid S, Pietschmann T, Pecheur EI Low pH-dependent hepatitis C virus membrane fusion depends on E2 integrity, target lipid composition, and density of virus particles. J Biol Chem 2009;284(26):17657-67
16. Zeisel MB, Fofana I, Fafi-Kremer S, Baumert TF Hepatitis C virus entry into hepatocytes: molecular mechanisms and targets for antiviral therapies. J Hepatol 2011;54(3):566-76
17. Sainz B Jr, Barretto N, Martin DN, et al. Identification of the Niemann-Pick C1-like 1 cholesterol absorption receptor as a new hepatitis C virus entry factor. Nat Med 2012;18(2):281-5
18. Meertens L, Bertaux C, Dragic T Hepatitis C virus entry requires a critical postinternalization step and delivery to early endosomes via clathrin-coated vesicles. J Virol 2006;80(23):11571-8
19. Lavillette D, Bartosch B, Nourrisson D, et al. Hepatitis C virus glycoproteins mediate low pH-dependent membrane fusion with liposomes. J Biol Chem 2006;281(7):3909-17
20. Blanchard E, Belouzard S, Goueslain L, et al. Hepatitis C virus entry depends on clathrin-mediated endocytosis. J Virol 2006;80(14):6964-72
21. Hsu M, Zhang J, Flint M, et al. Hepatitis C virus glycoproteins mediate pH-dependent cell entry of pseudotyped retroviral particles. Proc Natl Acad Sci USA 2003;100(12):7271-6
22. Tscherne DM, Jones CT, Evans MJ, et al. Time- and temperature-dependent activation of hepatitis C virus for low-pH-triggered entry. J Virol 2006;80(4):1734-41
23. Tang H, Grise H Cellular and molecular biology of HCV infection and hepatitis. Clin Sci (Lond) 2009;117(2):49-65
24. Lohmann V, Korner F, Koch J, et al. Replication of subgenomic hepatitis C virus RNAs in a hepatoma cell line. Science 1999;285(5424):110-13
25. Lindenbach BD, Tellinghuisen TL, Raney KD, et al. Hepatitis C virus genome replication. Springer; US: 2009. p. 61-88
26. Gastaminza P, Cheng G, Wieland S, et al. Cellular determinants of hepatitis C virus assembly, maturation, degradation, and secretion. J Virol 2008;82(5):2120-9
27. Piver E, Roingeard P, Pages JC The cell biology of hepatitis C virus (HCV) lipid addiction: molecular mechanisms and its potential importance in the clinic. Int J Biochem Cell Biol 2010;42(6):869-79
28. Choo QL, Kuo G, Weiner AJ, et al. Isolation of a cDNA clone derived from a blood-borne non-A, non-B viral hepatitis genome. Science 1989;244(4902):359-62
29. Taliani M, Bianchi E, Narjes F, et al. A continuous assay of hepatitis C virus protease based on resonance energy transfer depsipeptide substrates. Anal Biochem 1996;240(1):60-7
30. Zhang R, Beyer BM, Durkin J, et al. A continuous spectrophotometric assay for the hepatitis C virus serine protease. Anal Biochem 1999;270(2):268-75
31. Kyono K, Miyashiro M, Taguchi I Detection of hepatitis C virus helicase activity using the scintillation proximity assay system. Anal Biochem 1998;257(2):120-6
32. Kyono K, Miyashiro M, Taguchi I Expression and purification of a hepatitis C virus NS3/4A complex, and characterization of its helicase activity with the scintillation proximity assay system. J Biochem 2004;135(2):245-52
33. Hagedorn CH, van Beers EH, De Staercke C Hepatitis C virus RNA-dependent RNA polymerase (NS5B polymerase). Curr Top Microbiol Immunol 2000;242:225-60
34. Leveque VJ, Wang QM RNA-dependent RNA polymerase encoded by hepatitis C virus: biomedical applications. Cell Mol Life Sci 2002;59(6):909-19
35. Bartenschlager R Hepatitis C virus molecular clones: from cDNA to infectious virus particles in cell culture. Curr Opin Microbiol 2006;9(4):416-22
36. Neyts J Selective inhibitors of hepatitis C virus replication. Antiviral Res 2006;71(2-3):363-71
37. Horscroft N, Lai VC, Cheney W, et al. Replicon cell culture system as a valuable tool in antiviral drug discovery against hepatitis C virus. Antivir Chem Chemother 2005;16(1):1-12
38. Bartosch B, Dubuisson J, Cosset FL Infectious hepatitis C virus pseudo-particles containing functional E1-E2 envelope protein complexes. J Exp Med 2003;197(5):633-42
39. McKeating JA, Zhang LQ, Logvinoff C, et al. Diverse hepatitis C virus glycoproteins mediate viral infection in a CD81-dependent manner. J Virol 2004;78(16):8496-505
40. Zhong J, Gastaminza P, Cheng G, et al. Robust hepatitis C virus infection in vitro. Proc Natl Acad Sci USA 2005;102(26):9294-9
41. Wakita T, Pietschmann T, Kato T, et al. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat Med 2005;11(7):791-6
42. Ikeda M, Abe K, Dansako H, et al. 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 2005;329(4):1350-9
43. Maekawa S, Enomoto N, Sakamoto N, et al. 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 2004;11(5):394-403
44. Kato T, Date T, Miyamoto M, et al. Efficient replication of the genotype 2a hepatitis C virus subgenomic replicon. Gastroenterology 2003;125(6):1808-17
45. Kishine H, Sugiyama K, Hijikata M, et al. Subgenomic replicon derived from a cell line infected with the hepatitis C virus. Biochem Biophys Res Commun 2002;293(3):993-9
46. Blight KJ, McKeating JA, Marcotrigiano J, Rice CM Efficient replication of hepatitis C virus genotype 1a RNAs in cell culture. J Virol 2003;77(5):3181-90
47. Ikeda M, Yi M, Li K, Lemon SM 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 2002;76(6):2997-3006
48. Guo JT, Bichko VV, Seeger C Effect of alpha interferon on the hepatitis C virus replicon. J Virol 2001;75(18):8516-23
49. Date T, Kato T, Miyamoto M, et al. Genotype 2a hepatitis C virus subgenomic replicon can replicate in HepG2 and IMY-N9 cells. J Biol Chem 2004;279(21):22371-6
50. Kato T, Date T, Miyamoto M, et al. Nonhepatic cell lines HeLa and 293 support efficient replication of the hepatitis C virus genotype 2a subgenomic replicon. J Virol 2005;79(1):592-6
51. Ali S, Pellerin C, Lamarre D, Kukolj G Hepatitis C virus subgenomic replicons in the human embryonic kidney 293 cell line. J Virol 2004;78(1):491-501
52. Zhu Q, Guo JT, Seeger C Replication of hepatitis C virus subgenomes in nonhepatic epithelial and mouse hepatoma cells. J Virol 2003;77(17):9204-10
53. Uprichard SL, Chung J, Chisari FV, Wakita T Replication of a hepatitis C virus replicon clone in mouse cells. Virol J 2006;3:89
54. Bukh J, Pietschmann T, Lohmann V, et al. Mutations that permit efficient replication of hepatitis C virus RNA in Huh-7 cells prevent productive replication in chimpanzees. Proc Natl Acad Sci USA 2002;99(22):14416-21
55. Ploss A, Evans MJ, Gaysinskaya VA, et al. Human occludin is a hepatitis C virus entry factor required for infection of mouse cells. Nature 2009;457(7231):882-6
56. Evans MJ, von Hahn T, Tscherne DM, et al. Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry. Nature 2007;446(7137):801-5
57. Owsianka A, Tarr AW, Juttla VS, et al. Monoclonal antibody AP33 defines a broadly neutralizing epitope on the hepatitis C virus E2 envelope glycoprotein. J Virol 2005;79(17):11095-104
58. Tong Y, Zhu Y, Xia X, et al. Tupaia CD81, SR-BI, claudin-1, and occludin support hepatitis C virus infection. J Virol 2011;85(6):2793-802
59. Brown KS, Keogh MJ, Owsianka AM, et al. Specific interaction of hepatitis C virus glycoproteins with mannan binding lectin inhibits virus entry. Protein Cell 2010;1(7):664-74
60. Meuleman P, Albecka A, Belouzard S, et al. Griffithsin has antiviral activity against hepatitis C virus. Antimicrob Agents Chemother 2011;55(11):5159-67
61. Wong-Staal F, Syder AJ, McKelvy JF Targeting HCV entry for development of therapeutics. Viruses 2010;2(8):1718-33
62. Yang JP, Zhou D, Wong-Staal F Screening of small-molecule compounds as inhibitors of HCV entry. Methods Mol Biol 2009;510:295-304
63. Molina S, Castet V, Fournier-Wirth C, et al. The low-density lipoprotein receptor plays a role in the infection of primary human hepatocytes by hepatitis C virus. J Hepatol 2007;46(3):411-19
64. Kato T, Furusaka A, Miyamoto M, et al. Sequence analysis of hepatitis C virus isolated from a fulminant hepatitis patient. J Med Virol 2001;64(3):334-9
65. Lindenbach BD, Meuleman P, Ploss A, et al. Cell culture-grown hepatitis C virus is infectious in vivo and can be recultured in vitro. Proc Natl Acad Sci USA 2006;103(10):3805-9
66. Cai Z, Zhang C, Chang KS, et al. Robust production of infectious hepatitis C virus (HCV) from stably HCV cDNA-transfected human hepatoma cells. J Virol 2005;79(22):13963-73
67. Scheel TK, Gottwein JM, Mikkelsen LS, et al. Recombinant HCV variants with NS5A from genotypes 1-7 have different sensitivities to an NS5A inhibitor but not interferon-alpha. Gastroenterology 2011;140(3):1032-42
68. Li YP, Ramirez S, Gottwein JM, Bukh J Non-genotype-specific role of the hepatitis C virus 5' untranslated region in virus production and in inhibition by interferon. Virology 2011;421(2):222-34
69. Gottwein JM, Scheel TK, Jensen TB, et al. 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 2009;49(2):364-77
70. Gottwein JM, Jensen TB, Mathiesen CK, et al. Development and application of hepatitis C reporter viruses with genotype 1 to 7 core-nonstructural protein 2 (NS2) expressing fluorescent proteins or luciferase in modified JFH1 NS5A. J Virol 2011;85(17):8913-28
71. Pietschmann T, Kaul A, Koutsoudakis G, et al. Construction and characterization of infectious intragenotypic and intergenotypic hepatitis C virus chimeras. Proc Natl Acad Sci USA 2006;103(19):7408-13
72. Kato T, Matsumura T, Heller T, et al. Production of infectious hepatitis C virus of various genotypes in cell cultures. J Virol 2007;81(9):4405-11
73. Pietschmann T, Zayas M, Meuleman P, et al. Production of infectious genotype 1b virus particles in cell culture and impairment by replication enhancing mutations. PLoS Pathog 2009;5(6):e1000475
74. Yi M, Villanueva RA, Thomas DL, et al. Production of infectious genotype 1a hepatitis C virus (Hutchinson strain) in cultured human hepatoma cells. Proc Natl Acad Sci USA 2006;103(7):2310-15
75. Ploss A, Khetani SR, Jones CT, et al. Persistent hepatitis C virus infection in microscale primary human hepatocyte cultures. Proc Natl Acad Sci USA 2010;107(7):3141-5
76. Molina S, Castet V, Pichard-Garcia L, et al. Serum-derived hepatitis C virus infection of primary human hepatocytes is tetraspanin CD81 dependent. J Virol 2008;82(1):569-74
77. Buck M Direct infection and replication of naturally occurring hepatitis C virus genotypes 1, 2, 3 and 4 in normal human hepatocyte cultures. PLoS One 2008;3(7):e2660
78. Sheahan T, Jones CT, Ploss A Advances and challenges in studying hepatitis C virus in its native environment. Expert Rev Gastroenterol Hepatol 2010;4(5):541-50
79. Ploss A, Rice CM Towards a small animal model for hepatitis C. EMBO Rep 2009;10(11):1220-7
80. Dandri M, Burda MR, Torok E, et al. Repopulation of mouse liver with human hepatocytes and in vivo infection with hepatitis B virus. Hepatology 2001;33(4):981-8
81. Mercer DF, Schiller DE, Elliott JF, et al. Hepatitis C virus replication in mice with chimeric human livers. Nat Med 2001;7(8):927-33
82. Meuleman P, Hesselgesser J, Paulson M, et al. Anti-CD81 antibodies can prevent a hepatitis C virus infection in vivo. Hepatology 2008;48(6):1761-8
83. Vanwolleghem T, Bukh J, Meuleman P, et al. Polyclonal immunoglobulins from a chronic hepatitis C virus patient protect human liver-chimeric mice from infection with a homologous hepatitis C virus strain. Hepatology 2008;47(6):1846-55
84. Kneteman NM, Mercer DF Mice with chimeric human livers: who says supermodels have to be tall?. Hepatology 2005;41(4):703-6
85. Lupberger J, Zeisel MB, Xiao F, et al. EGFR and EphA2 are host factors for hepatitis C virus entry and possible targets for antiviral therapy. Nat Med 2011;17(5):589-95
86. Lacek K, Vercauteren K, Grzyb K, et al. Novel human SR-BI antibodies prevent infection and dissemination of HCV in vitro and in humanized mice. J Hepatol 2012; Epub ahead of print
87. Dorner M, Horwitz JA, Robbins JB, et al. A genetically humanized mouse model for hepatitis C virus infection. Nature 2011;474(7350):208-11
88. Lin LT, Noyce RS, Pham TN, et al. Replication of subgenomic hepatitis C virus replicons in mouse fibroblasts is facilitated by deletion of interferon regulatory factor 3 and expression of liver-specific microRNA 122. J Virol 2010;84(18):9170-80
89. Krieger N, Lohmann V, Bartenschlager R Enhancement of hepatitis C virus RNA replication by cell culture-adaptive mutations. J Virol 2001;75(10):4614-24
90. Lohmann V, Korner F, Dobierzewska A, Bartenschlager R Mutations in hepatitis C virus RNAs conferring cell culture adaptation. J Virol 2001;75(3):1437-49
91. Blight KJ, McKeating JA, Rice CM Highly permissive cell lines for subgenomic and genomic hepatitis C virus RNA replication. J Virol 2002;76(24):13001-14
92. Bartenschlager R Hepatitis C virus replicons: potential role for drug development. Nat Rev Drug Discov 2002;1(11):911-16
93. Murray EM, Grobler JA, Markel EJ, et al. Persistent replication of hepatitis C virus replicons expressing the beta-lactamase reporter in subpopulations of highly permissive Huh7 cells. J Virol 2003;77(5):2928-35
94. Zuck P, Murray EM, Stec E, et al. A cell-based beta-lactamase reporter gene assay for the identification of inhibitors of hepatitis C virus replication. Anal Biochem 2004;334(2):344-55
95. Moradpour D, Evans MJ, Gosert R, et al. Insertion of green fluorescent protein into nonstructural protein 5A allows direct visualization of functional hepatitis C virus replication complexes. J Virol 2004;78(14):7400-9
96. Yi M, Bodola F, Lemon SM Subgenomic hepatitis C virus replicons inducing expression of a secreted enzymatic reporter protein. Virology 2002;304(2):197-210
97. Kamada K, Shoji I, Deng L, et al. Generation of a recombinant reporter hepatitis C virus useful for the analyses of virus entry, intra-cellular replication and virion production. Microbes Infect 2011;14(1):69-78
98. Wu Y, Liao Q, Yang R, et al. A novel luciferase and GFP dual reporter virus for rapid and convenient evaluation of hepatitis C virus replication. Virus Res 2011;155(2):406-14
99. Jones CT, Murray CL, Eastman DK, et al. Hepatitis C virus p7 and NS2 proteins are essential for production of infectious virus. J Virol 2007;81(16):8374-83
100. Koutsoudakis G, Kaul A, Steinmann E, et al. Characterization of the early steps of hepatitis C virus infection by using luciferase reporter viruses. J Virol 2006;80(11):5308-20
101. Iro M, Witteveldt J, Angus AG, et al. A reporter cell line for rapid and sensitive evaluation of hepatitis C virus infectivity and replication. Antiviral Res 2009;83(2):148-55
102. Chen Z, Simeon RL, Chockalingam K, Rice CM Creation and characterization of a cell-death reporter cell line for hepatitis C virus infection. Antiviral Res 2010;86(2):220-3
103. Chockalingam K, Simeon RL, Rice CM, Chen Z A cell protection screen reveals potent inhibitors of multiple stages of the hepatitis C virus life cycle. Proc Natl Acad Sci USA 2009;107(8):3764-9
104. Jones CT, Catanese MT, Law LM, et al. Real-time imaging of hepatitis C virus infection using a fluorescent cell-based reporter system. Nat Biotechnol 2010;28(2):167-71
105. Coburn GA, Fisch DN, Moorji SM, et al. Novel small-molecule inhibitors of hepatitis C virus entry block viral spread and promote viral clearance in cell culture. PLoS ONE 2012;7(4):e35351
106. Mondal R, Koev G, Pilot-Matias T, et al. Development of a cell-based assay for high-throughput screening of inhibitors against HCV genotypes 1a and 1b in a single well. Antiviral Res 2009;82(1):82-8
107. Robinson M, Yang H, Sun SC, et al. Novel hepatitis C virus reporter replicon cell lines enable efficient antiviral screening against genotype 1a. Antimicrob Agents Chemother 2010;54(8):3099-106
108. O'Boyle DR II, Nower PT, Lemm JA, et al. Development of a cell-based high-throughput specificity screen using a hepatitis C virus-bovine viral diarrhea virus dual replicon assay. Antimicrob Agents Chemother 2005;49(4):1346-53
109. Yu X, Sainz B Jr, Uprichard SL Development of a cell-based hepatitis C virus infection fluorescent resonance energy transfer assay for high-throughput antiviral compound screening. Antimicrob Agents Chemother 2009;53(10):4311-19