Development of a cell-based hepatitis C virus infection fluorescent resonance energy transfer assay for high-throughput antiviral compound screening

Antimicrobial Agents and Chemotherapy

Volumn 53, Issue 10, 2009, Pages 4311-4319

  Yu, Xuemei ^a   Sainz Jr , Bruno ^a   Uprichard, Susan L ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA E2 GLYCOPROTEIN ANTIBODY; ALPHA2A INTERFERON; ANTIVIRUS AGENT; BETA INTERFERON; CD81 MONOCLONAL ANTIBODY; CYCLOSPORIN A; ENZYME INHIBITOR; MIGLUSTAT; MONOCLONAL ANTIBODY; NARINGENIN; NM 107; NONSTRUCTURAL PROTEIN 3; UNCLASSIFIED DRUG;

ACCURACY; AMINO ACID SEQUENCE; ARTICLE; CANCER CELL CULTURE; CELL ASSAY; CONTROLLED STUDY; CULTURE TECHNIQUE; FLUORESCENCE RESONANCE ENERGY TRANSFER; HEPATITIS C; HEPATITIS C VIRUS; HEPATOMA CELL; HIGH THROUGHPUT SCREENING; HUMAN; HUMAN CELL; LIFE CYCLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN CONTENT; REAL TIME POLYMERASE CHAIN REACTION; REPRODUCIBILITY; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ANTIVIRAL AGENTS; BLOTTING, WESTERN; CELL LINE, TUMOR; CELL SURVIVAL; FLUORESCENCE RESONANCE ENERGY TRANSFER; HEPACIVIRUS; HEPATITIS C; HUMANS; KINETICS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; VIRAL NONSTRUCTURAL PROTEINS;

EID: 70349345813     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00495-09     Document Type: Article

References (58)

1. Ahmed, A., and E. B. Keeffe. 1999. Treatment strategies for chronic hepatitis C: update since the 1997 National Institutes of Health Consensus Development Conference. J. Gastroenterol. Hepatol. 14(Suppl.):S12-S8.
2. Alter, H. J., and L. B. Seeff. 2000. Recovery, persistence, and sequelae in hepatitis C virus infection: a perspective on long-term outcome. Semin. Liver Dis. 20:17-35.
3. Bartosch, B., J. Dubuisson, and F. L. Cosset. 2003. Infectious hepatitis C virus pseudo-particles containing functional E1-E2 envelope protein complexes. J. Exp. Med. 197:633-642.
4. Beames, B., D. Chavez, and R. E. Lanford. 2001. GB virus B as a model for hepatitis C virus. ILAR J. 42:152-160.
5. Bianchi, E., C. Steinkuhler, M. Taliani, A. Urbani, R. D. Francesco, and A. Pessi. 1996. Synthetic depsipeptide substrates for the assay of human hepatitis C virus protease. Anal. Biochem. 237:239-244.
6. Blight, K. J., A. A. Kolykhalov, and C. M. Rice. 2000. Efficient initiation of HCV RNA replication in cell culture. Science 290:1972-1975.
7. Blight, K. J., J. A. McKeating, J. Marcotrigiano, and C. M. Rice. 2003. Efficient replication of hepatitis C virus genotype 1a RNAs in cell culture. J. Virol. 77:3181-3190. (Pubitemid 36228102)
8. Bourne, N., R. B. Pyles, M. Yi, R. L. Veselenak, M. M. Davis, and S. M. Lemon. 2005. Screening for hepatitis C virus antiviral activity with a cell-based secreted alkaline phosphatase reporter replicon system. Antivir. Res. 67:76-82.
9. Choi, S., B. Sainz, Jr., P. Corcoran, S. L. Uprichard, and H. Jeong. 2009. Characterization of increased drug metabolism activity in dimethyl sulfoxide (DMSO)-treated Huh7 hepatoma cells. Xenobiotica 39:205-217.
10. Choo, Q.-L., G. Kuo, A. J. Weiner, L. R. Overby, D. W. Bradley, and M. Houghton. 1989. Isolation of a cDNA clone derived from a blood-borne non-A, non-B viral hepatitis genome. Science 244:359-362.
11. Dansako, H., M. Ikeda, K. Abe, K. Mori, K. Takemoto, Y. Ariumi, and N. Kato. 2008. A new living cell-based assay system for monitoring genomelength hepatitis C virus RNA replication. Virus Res. 137:72-79.
12. Fattori, D., A. Urbani, M. Brunetti, R. Ingenito, A. Pessi, K. Prendergast, F. Narjes, V. G. Matassa, R. De Francesco, and C. Steinkuhler. 2000. Probing the active site of the hepatitis C virus serine protease by fluorescence resonance energy transfer. J. Biol. Chem. 275:15106-15113.
13. Gastaminza, P., S. B. Kapadia, and F. V. Chisari. 2006. Differential biophysical properties of infectious intracellular and secreted hepatitis C virus particles. J. Virol. 80:11074-11081. (Pubitemid 44706548)
14. Goergen, B., S. Jakobs, P. Symmons, E. Hornes, K. H. Meyer zum Buschenfelde, and G. Gerken. 1994. Quantitation of HCV-replication using one-step competitive reverse transcription-polymerase chain reaction and a solid phase, colorimetric detection method. J. Hepatol. 21:678-682.
15. Gosert, R., D. Egger, V. Lohmann, R. Bartenschlager, H. E. Blum, K. Bienz, and D. Moradpour. 2003. Identification of the hepatitis C virus RNA replication complex in Huh-7 cells harboring subgenomic replicons. J. Virol. 77:5487-5492. (Pubitemid 36460961)
16. Hao, W., K. J. Herlihy, N. J. Zhang, S. A. Fuhrman, C. Doan, A. K. Patick, and R. Duggal. 2007. Development of a novel dicistronic reporter-selectable hepatitis C virus replicon suitable for high-throughput inhibitor screening. Antimicrob. Agents Chemother. 51:95-102.
17. Henry, S. D., H. J. Metselaar, R. C. Lonsdale, A. Kok, B. L. Haagmans, H. W. Tilanus, and L. J. van der Laan. 2006. Mycophenolic acid inhibits hepatitis C virus replication and acts in synergy with cyclosporin A and interferon-alpha. Gastroenterology 131:1452-1462. (Pubitemid 44708933)
18. Hirowatari, Y., M. Hijikata, and K. Shimotohno. 1995. A novel method for analysis of viral proteinase activity encoded by hepatitis C virus in cultured cells. Anal. Biochem. 225:113-120.
19. Huang, P., D. A. Goff, Q. Huang, A. Martinez, X. Xu, S. Crowder, S. D. Issakani, E. Anderson, N. Sheng, P. Achacoso, A. Yen, T. Kinsella, I. S. Darwish, R. Kolluri, H. Hong, K. Qu, E. Stauffer, E. Goldstein, R. Singh, D. G. Payan, and H. H. Lu. 2008. Discovery and characterization of substituted diphenyl heterocyclic compounds as potent and selective inhibitors of hepatitis C virus replication. Antimicrob. Agents Chemother. 52:1419-1429.
20. Ikeda, M., M. Yi, K. Li, and S. M. Lemon. 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)
21. Kakiuchi, N., S. Nishikawa, M. Hattori, and K. Shimotohno. 1999. A high throughput assay of the hepatitis C virus nonstructural protein 3 serine proteinase. J. Virol. Methods 80:77-84. (Pubitemid 29248905)
22. Kato, T., T. Date, M. Miyamoto, A. Furusaka, K. Tokushige, M. Mizokami, and T. Wakita. 2003. Efficient replication of the genotype 2a hepatitis C virus subgenomic replicon. Gastroenterology 125:1808-1817. (Pubitemid 37500445)
23. Kato, T., A. Furusaka, M. Miyamoto, T. Date, K. Yasui, J. Hiramoto, K. Nagayama, T. Tanaka, and T. Wakita. 2001. Sequence analysis of hepatitis C virus isolated from a fulminant hepatitis patient. J. Med. Virol. 64:334-339.
24. Kim, S. S., L. F. Peng, W. Lin, W. H. Choe, N. Sakamoto, N. Kato, M. Ikeda, S. L. Schreiber, and R. T. Chung. 2007. A cell-based, high-throughput screen for small molecule regulators of hepatitis C virus replication. Gastroenterology 132:311-320. (Pubitemid 46108745)
25. Konstantinidis, A. K., P. L. Richardson, K. A. Kurtz, R. Tripathi, C. M. Chen, P. Huang, J. Randolph, D. Towne, J. Donnelly, U. Warrior, T. Middleton, and W. M. Kati. 2007. Longer wavelength fluorescence resonance energy transfer depsipeptide substrates for hepatitis C virus NS3 protease. Anal. Biochem. 368:156-167.
26. Koutsoudakis, G., A. Kaul, E. Steinmann, S. Kallis, V. Lohmann, T. Pietschmann, and R. Bartenschlager. 2006. Characterization of the early steps of hepatitis C virus infection by using luciferase reporter viruses. J. Virol. 80:5308-5320. (Pubitemid 43752776)
27. Krieger, N., V. Lohmann, and R. Bartenschlager. 2001. Enhancement of hepatitis C virus RNA replication by cell culture-adaptive mutations. J. Virol. 75:4614-4624. (Pubitemid 32381503)
28. Law, M., T. Maruyama, J. Lewis, E. Giang, A. W. Tarr, Z. Stamataki, P. Gastaminza, F. V. Chisari, I. M. Jones, R. I. Fox, J. K. Ball, J. A. McKeating, N. M. Kneteman, and D. R. Burton. 2008. Broadly neutralizing antibodies protect against hepatitis C virus quasispecies challenge. Nat. Med. 14:25-27.
29. Lee, J. C., Y. F. Shih, S. P. Hsu, T. Y. Chang, L. H. Chen, and J. T. Hsu. 2003. Development of a cell-based assay for monitoring specific hepatitis C virus NS3/4A protease activity in mammalian cells. Anal. Biochem. 316:162-170.
30. Lee, J. C., M. C. Yu, T. W. Lien, C. F. Chang, and J. T. Hsu. 2005. High-throughput cell-based screening for hepatitis C virus NS3/4A protease inhibitors. Assay Drug Dev. Technol. 3:385-392.
31. Lindenbach, B. D., M. J. Evans, A. J. Syder, B. Wolk, T. L. Tellinghuisen, C. C. Liu, T. Maruyama, R. O. Hynes, D. R. Burton, J. A. McKeating, and C. M. Rice. 2005. Complete replication of hepatitis C virus in cell culture. Science 309:623-626. (Pubitemid 41033648)
32. Lindenbach, B. D., and C. M. Rice. 2005. Unravelling hepatitis C virus replication from genome to function. Nature 436:933-938. (Pubitemid 41191668)
33. Lohmann, V., F. Korner, J. Koch, U. Herian, L. Theilmann, and R. Bartenschlager. 1999. Replication of subgenomic hepatitis C virus RNAs in a hepatoma cell line. Science 285:110-113. (Pubitemid 29307577)
34. Mao, H. X., S. Y. Lan, Y. W. Hu, L. Xiang, and Z. H. Yuan. 2003. Establishment of a cell-based assay system for hepatitis C virus serine protease and its primary applications. World J. Gastroenterol. 9:2474-2479.
35. Mao, S. S., J. DiMuzio, C. McHale, C. Burlein, D. Olsen, and S. S. Carroll. 2008. A time-resolved, internally quenched fluorescence assay to characterize inhibition of hepatitis C virus nonstructural protein 3-4A protease at low enzyme concentrations. Anal. Biochem. 373:1-8.
36. Mathy, J. E., S. Ma, T. Compton, and K. Lin. 2008. Combinations of cyclophilin inhibitor NIM811 with hepatitis C Virus NS3-4A Protease or NS5B polymerase inhibitors enhance antiviral activity and suppress the emergence of resistance. Antimicrob. Agents Chemother. 52:3267-3275.
37. McCown, M. F., S. Rajyaguru, S. Le Pogam, S. Ali, W. R. Jiang, H. Kang, J. Symons, N. Cammack, and I. Najera. 2008. The hepatitis C virus replicon presents a higher barrier to resistance to nucleoside analogs than to non-nucleoside polymerase or protease inhibitors. Antimicrob. Agents Chemother. 52:1604-1612.
38. Mondal, R., G. Koev, T. Pilot-Matias, Y. He, T. Ng, W. Kati, and A. Molla. 2009. Development of a cell-based assay for high-throughput screening of inhibitors against HCV genotypes 1a and 1b in a single well. Antivir. Res. 82:82-88.
39. Murray, E. M., J. A. Grobler, E. J. Markel, M. F. Pagnoni, G. Paonessa, A. J. Simon, and O. A. Flores. 2003. Persistent replication of hepatitis C virus replicons expressing the beta-lactamase reporter in subpopulations of highly permissive Huh7 cells. J. Virol. 77:2928-2935.
40. Nahmias, Y., J. Goldwasser, M. Casali, D. van Poll, T. Wakita, R. T. Chung, and M. L. Yarmush. 2008. Apolipoprotein B-dependent hepatitis C virus secretion is inhibited by the grapefruit flavonoid naringenin. Hepatology 47:1437-1445. (Pubitemid 351702727)
41. Nakagawa, M., N. Sakamoto, N. Enomoto, Y. Tanabe, N. Kanazawa, T. Koyama, M. Kurosaki, S. Maekawa, T. Yamashiro, C. H. Chen, Y. Itsui, S. Kakinuma, and M. Watanabe. 2004. Specific inhibition of hepatitis C virus replication by cyclosporin A. Biochem. Biophys. Res. Commun. 313:42-47.
42. Nelson, H. B., and H. Tang. 2006. Effect of cell growth on hepatitis C virus (HCV) replication and a mechanism of cell confluence-based inhibition of HCV RNA and protein expression. J. Virol. 80:1181-1190.
43. O'Boyle, D. R., II, P. T. Nower, J. A. Lemm, L. Valera, J. H. Sun, K. Rigat, R. Colonno, and M. Gao. 2005. Development of a cell-based high-throughput specificity screen using a hepatitis C virus-bovine viral diarrhea virus dual replicon assay. Antimicrob. Agents Chemother. 49:1346-1353.
44. Phuong do, T., C. M. Ma, M. Hattori, and J. S. Jin. 2009. Inhibitory effects of antrodins A-E from Antrodia cinnamomea and their metabolites on hepatitis C virus protease. Phytother Res. 23:582-584.
45. Pietschmann, T., V. Lohmann, G. Rutter, K. Kurpanek, and R. Bartenschlager. 2001. Characterization of cell lines carrying self-replicating hepatitis C virus RNAs. J. Virol. 75:1252-1264. (Pubitemid 32094684)
46. Sainz, B., Jr., and F. V. Chisari. 2006. Production of infectious hepatitis C virus by well-differentiated, growth-arrested human hepatoma-derived cells. J. Virol. 80:10253-10257. (Pubitemid 44522619)
47. Steinmann, E., T. Whitfield, S. Kallis, R. A. Dwek, N. Zitzmann, T. Pietschmann, and R. Bartenschlager. 2007. Antiviral effects of amantadine and iminosugar derivatives against hepatitis C virus. Hepatology 46:330-338. (Pubitemid 47344767)
48. Tscherne, D. M., C. T. Jones, M. J. Evans, B. D. Lindenbach, J. A. Mc-Keating, and C. M. Rice. 2006. Time- and temperature-dependent activation of hepatitis C virus for low-pH-triggered entry. J. Virol. 80:1734-1741.
49. Uprichard, S. L., J. Chung, F. V. Chisari, and T. Wakita. 2006. Replication of a hepatitis C virus replicon clone in mouse cells. Virol. J. 3:89.
50. Wakita, T., T. Pietschmann, T. Kato, T. Date, M. Miyamoto, Z. Zhao, K. Murthy, A. Habermann, H. G. Krausslich, M. Mizokami, R. Bartenschlager, and T. J. Liang. 2005. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat. Med. 11:791-796.
51. Windisch, M. P., M. Frese, A. Kaul, M. Trippler, V. Lohmann, and R. Bartenschlager. 2005. Dissecting the interferon-induced inhibition of hepatitis C virus replication by using a novel host cell line. J. Virol. 79:13778-13793.
52. Yi, M., F. Bodola, and S. M. Lemon. 2002. Subgenomic hepatitis C virus replicons inducing expression of a secreted enzymatic reporter protein. Virology 304:197-210. (Pubitemid 36069163)
53. Yi, M., and S. Lemon. 2002. Replication of subgenomic hepatitis A virus RNAs expressing firefly luciferase is enhanced by mutations associated with adaptation of virus to growth in cultured cells. J. Virol. 76:1171-1180. (Pubitemid 34066421)
54. Zhang, J. H., T. D. Chung, and K. R. Oldenburg. 1999. A simple statistical parameter for use in evaluation and validation of high throughput screening assays. J. Biomol. Screen. 4:67-73.
55. Zhang, Y., P. Weady, R. Duggal, and W. Hao. 2008. Novel chimeric genotype 1b/2a hepatitis C virus suitable for high-throughput screening. Antimicrob. Agents Chemother. 52:666-674.
56. Zhong, J., P. Gastaminza, G. Cheng, S. Kapadia, T. Kato, D. R. Burton, S. F. Wieland, S. L. Uprichard, T. Wakita, and F. V. Chisari. 2005. Robust hepatitis C virus infection in vitro. Proc. Natl. Acad. Sci. USA 102:9294-9299.
57. Zhong, J., P. Gastaminza, J. Chung, Z. Stamataki, M. Isogawa, G. Cheng, J. A. McKeating, and F. V. Chisari. 2006. Persistent hepatitis C virus infection in vitro: coevolution of virus and host. J. Virol. 80:11082-11093. (Pubitemid 44706549)
58. Zuck, P., E. M. Murray, E. Stec, J. A. Grobler, A. J. Simon, B. Strulovici, J. Inglese, O. A. Flores, and M. Ferrer. 2004. A cell-based beta-lactamase reporter gene assay for the identification of inhibitors of hepatitis C virus replication. Anal. Biochem. 334:344-355.