Alternative Approaches for Efficient Inhibition of Hepatitis C Virus RNA Replication by Small Interfering RNAs

Journal of Virology

Volumn 78, Issue 7, 2004, Pages 3436-3446

  Krönke, Jan ^a   Kittler, Ralf ^b   Buchholz, Frank ^b   Windisch, Marc P ^a   Pietschmann, Thomas ^a   Bartenschlager, Ralf ^a   Frese, Michael ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

RIBONUCLEASE; SHORT HAIRPIN RNA; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VIRUS RNA; ANTIVIRUS AGENT;

5' UNTRANSLATED REGION; ANTIVIRAL ACTIVITY; ARTICLE; CHRONIC HEPATITIS; CONTROLLED STUDY; EVOLUTION; GENE EXPRESSION; GENE TARGETING; GENE THERAPY; GENETIC VARIABILITY; GENOTYPE; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; LIVER CELL CARCINOMA; LIVER CIRRHOSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REPLICON; RETROVIRUS; RNA INTERFERENCE; RNA REPLICATION; RNA SEQUENCE; VIRUS GENOME; VIRUS REPLICATION; BIOSYNTHESIS; CHEMISTRY; CONFORMATION; ENZYME SPECIFICITY; GENETICS; METABOLISM; METHODOLOGY; MOLECULAR EVOLUTION; MOLECULAR GENETICS; PHYSIOLOGY; TUMOR CELL LINE;

ANTIVIRAL AGENTS; BASE SEQUENCE; CELL LINE, TUMOR; EVOLUTION, MOLECULAR; GENE THERAPY; GENOME, VIRAL; GENOTYPE; HEPACIVIRUS; HUMANS; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; REPLICON; RNA INTERFERENCE; RNA, SMALL INTERFERING; RNA, VIRAL; SUBSTRATE SPECIFICITY; VIRUS REPLICATION;

EID: 12144289381     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.78.7.3436-3446.2004     Document Type: Article

References (74)

1. Alt, M., R. Renz, P. H. Hofschneider, G. Paumgartner, and W. H. Caselmann. 1995. Specific inhibition of hepatitis C viral gene expression by antisense phosphorothioate oligodeoxynucleotides. Hepatology 22:707-717.
2. Amarzguioui, M., T. Holen, E. Babaie, and H. Prydz. 2003. Tolerance for mutations and chemical modifications in a siRNA. Nucleic Acids Res. 31:589-595.
3. Amhros, V. 2003. MicroRNA pathways in flies and worms: growth, death, fat, stress, and timing. Cell 113:673-676.
4. Bartenschlager, R., M. Frese, and T. Pietschmann. Novel insights into hepatitis C virus replication and persistence. Adv. Virus Res., in press.
5. Berberich-Siebelt, F., S. Klein-Hessling, N. Hepping, B. Santner-Nanan, D. Lindemann, A. Schimpl, I. Berberich, and E. Serfling. 2000. C/EBPbeta enhances IL-4 but impairs IL-2 and IFN-gamma induction in T cells. Eur. J. Immunol. 30:2576-2585.
6. Brummelkamp, T. R., R. Bernards, and R. Agami. 2002. A system for stable expression of short interfering RNAs in mammalian cells. Science 296:550-553.
7. Buchholz, F., L. Ringrose, P. O. Angrand, F. Rossi, and A. F. Stewart. 1996. Different thermostabilities of FLP and Cre recombinases: implications for applied site-specific recombination. Nucleic Acids Res. 24:4256-4262.
8. Calegari, F., W. Haubensak, D. Yang, W. B. Huttner, and F. Buchholz. 2002. Tissue-specific RNA interference in postimplantation mouse embryos with endoribonuclease-prepared short interfering RNA. Proc. Natl. Acad. Sci. USA 99:14236-14240.
9. Caplen, N. J. 2003. RNAi as a gene therapy approach. Expert Opin. Biol. Ther. 3:575-586.
10. Capodici, J., K. Kariko, and D. Weissman. 2002. Inhibition of HIV-1 infection by small interfering RNA-mediated RNA interference. J. Immunol. 169:5196-5201.
11. Carrington, J. C., and V. Ambros. 2003. Role of microRNAs in plant and animal development. Science 301:336-338.
12. Chiu, Y. L., and T. M. Rana. 2002. RNAi in human cells: basic structural and functional features of small interfering RNA. Mol. Cell 10:549-561.
13. Coburn, G. A., and B. R. Cullen. 2002. Potent and specific inhibition of human immunodeficiency virus type 1 replication by RNA interference. J. Virol. 76:9225-9231.
14. DuBridge, R. B., P. Tang, H. C. Hsia, P. M. Leong, J. H. Miller, and M. P. Calos. 1987. Analysis of mutation in human cells by using an Epstein-Barr virus shuttle system. Mol. Cell. Biol. 7:379-387.
15. Elbashir, S. M., J. Harborth, W. Lendeckel, A. Yalcin, K. Weber, and T. Tuschl. 2001. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411:494-498.
16. Elbashir, S. M., J. Harborth, K. Weber, and T. Tuschl. 2002. Analysis of gene function in somatic mammalian cells using small interfering RNAs. Methods 26:199-213.
17. Fan, Z., Q. R. Yang, J. S. Twu, and A. H. Sherker. 1999. Specific in vitro association between the hepatitis C viral genome and core protein. J. Med. Virol. 59:131-134.
18. Frese, M., K. Barth, A. Kaul, V. Lohmann, V. Schwärzle, and R. Bartenschlager. 2003. Hepatis C virus RNA replication is resistant to tumor necrosis factor-α. J. Gen. Virol. 84:1253-1259.
19. Goodbourn, S., L. Didcock, and R. E. Randall. 2000. Interferons: cell signalling, immune modulation, antiviral response and virus countermeasures. J. Gen. Virol. 81:2341-2364.
20. Grishok, A., A. E. Pasquinelli, D. Conte, N. Li, S. Parrish, I. Ha, D. L. Baillie, A. Fire, G. Ruvkun, and C. C. Mello. 2001. Genes and mechanisms related to RNA interference regulate expression of the small temporal RNAs that control C. elegans developmental timing. Cell 106:23-34.
21. Hamada, M., T. Ohtsuka, R. Kawaida, M. Koizumi, K. Morita, H. Furukawa, T. Imanishi, M. Miyagishi, and K. Taira. 2002. Effects on RNA interference in gene expression (RNAi) in cultured mammalian cells of mismatches and the introduction of chemical modifications at the Y-ends of siRNAs. Antisense Nucleic Acid Drug Dev. 12:301-309.
22. Hammond, S. M., E. Bernstein, D. Beach, and G. J. Hannon. 2000. An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells. Nature 404:293-296.
23. Hannon, G. J. 2002. RNA interference. Nature 418:244-251.
24. Ho, S. N., H. D. Hunt, R. M. Horton, J. K. Pullen, and L. R. Pease. 1989. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77:51-59.
25. a. Holen, T., M. Amarzguioui, M. T. Wiiger, E. Babaie, and H. Prydz. 2002. Positional effects of short interfering RNAs targeting the human coagulation trigger tissue factor. Nucleic Acids Res. 30:1757-1766.
26. Honda, M., M. R. Beard, L. H. Ping, and S. M. Lemon. 1999. A phylogenetically conserved stem-loop structure at the 5′ border of the internal ribosome entry site of hepatitis C virus is required for cap-independent viral translation. J. Virol. 73:1165-1174.
27. Hoofnagle, J. H. 1997. Hepatitis C: the clinical spectrum of disease. Hepatology 26(Suppl. 1):15S-20S.
28. Jacque, J. M., K. Triques, and M. Stevenson. 2002. Modulation of HIV-1 replication by RNA interference. Nature 418:435-438.
29. Kalajzic, I., M. L. Stover, P. Liu, Z. Kalajzic, D. W. Rowe, and A. C. Lichtler. 2001. Use of VSV-G pseudotyped retroviral vectors to target murine osteoprogenitor cells. Virology 284:37-45.
30. Kapadia, S. B., A. Brideau-Andersen, and F. V. Chisari. 2003. Interference of hepatitis C virus RNA replication by short interfering RNAs. Proc. Natl. Acad. Sci. USA 100:2014-2018.
31. Khvorova, A., A. Reynolds, and S. D. Jayasena. 2003. Functional siRNAs and miRNAs exhibit strand bias. Cell 115:209-216.
32. Kim, Y. K., S. H. Lee, C. S. Kim, S. K. Seol, and S. K. Jang. 2003. Long-range RNA-RNA interaction between the 5′ nontranslated region and the core-coding sequences of hepatitis C virus modulates the IRES-dependent translation. RNA 9:599-606.
33. Kretschmer-Kazemi, F. R., and G. Sczakiel. 2003. The activity of siRNA in mammalian cells is related to structural target accessibility: a comparison with antisense oligonucleotides. Nucleic Acids Res. 31:4417-4424.
34. 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.
35. Lee, N. S., T. Dohjima, G. Bauer, H. Li, M. J. Li, A. Ehsani, P. Salvaterra, and J. Rossi. 2002. Expression of small interfering RNAs targeted against HIV-1 rev transcripts in human cells. Nat. Biotechnol. 20:500-505.
36. Li, H., W. X. Li, and S. W. Ding. 2002. Induction and suppression of RNA silencing by an animal virus. Science 296:1319-1321.
37. Li, W. X., and S. W. Ding. 2001. Viral suppressors of RNA silencing. Curr. Opin. Biotechnol. 12:150-154.
38. Lichner, Z., D. Silhavy, and J. Burgyan. 2003. Double-stranded RNA-binding proteins could suppress RNA interference-mediated antiviral defences. J. Gen. Virol. 84:975-980.
39. Lieber, A., C. Y. He, S. J. Polyak, D. R. Gretch, D. Barr, and M. A. Kay. 1996. Elimination of hepatitis C virus RNA in infected human hepatocytes by adenovirus-mediated expression of ribozymes. J. Virol. 70:8782-8791.
40. Lohmann, V., S. Hoffmann, U. Herian, F. Penin, and R. Bartenschlager. 2003. Viral and cellular determinants of hepatitis C virus RNA replication in cell culture. J. Virol. 77:3007-3019.
41. Lohmann, V., J. O. 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.
42. Lohmann, V., F. Körner, A. Dobierzewska, and R. Bartenschlager. 2001. Mutations in hepatitis C virus RNAs conferring cell culture adaptation. J. Virol. 75:1437-1449.
43. Lohmann, V., A. Roos, F. Körner, J. O. Koch, and R. Bartenschlager. 2000. Biochemical and structural analysis of the NS5B RNA-dependent RNA polymerase of the hepatitis C virus. J. Viral Hepat. 7:167-174.
44. McHutchison, J. G., and M. W. Fried. 2003. Current therapy for hepatitis C: pegylated interferon and ribavirin. Clin. Liver Dis. 7:149-161.
45. Morgenstern, J. P., and H. Land. 1990. Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids Res. 18:3587-3596.
46. Novina, C. D., M. F. Murray, D. M. Dykxhoorn, P. J. Beresford, J. Riess, S. K. Lee, R. G. Collman, J. Lieberman, P. Shankar, and P. A. Sharp. 2002. siRNA-directed inhibition of HIV-1 infection. Nat. Med. 8:681-686.
47. Nykanen, A., B. Haley, and P. D. Zamore. 2001. ATP requirements and small interfering RNA structure in the RNA interference pathway. Cell 107:309-321.
48. Ogata, N., H. J. Alter, R. H. Miller, and R. H. Purcell. 1991. Nucleotide sequence and mutation rate of the H strain of hepatitis C virus. Proc. Natl. Acad. Sci. USA 88:3392-3396.
49. Okamoto, H., M. Kojima, S. Okada, H. Yoshizawa, H. Iizuka, T. Tanaka, E. E. Muchmore, D. A. Peterson, Y. Ito, and S. Mishiro. 1992. Genetic drift of hepatitis C virus during an 8.2-year infection in a chimpanzee: variability and stability. Virology 190:894-899.
50. Park, W. S., N. Miyano-Kurosaki, M. Hayafune, E. Nakajima, T. Matsuzaki, F. Shimada, and H. Takaku. 2002. Prevention of HIV-1 infection in human peripheral blood mononuclear cells by specific RNA interference. Nucleic Acids Res. 30:4830-4835.
51. Pietschmann, T., V. Lohmann, A. Kaul, N. Krieger, G. Rinck, G. Rutter, D. Strand, and R. Bartenschlager. 2002. Persistent and transient replication of full-length hepatitis C virus genomes in cell culture. J. Virol. 76:4008-4021.
52. Randall, G., A. Grakoui, and C. M. Rice. 2003. Clearance of replicating hepatitis C virus replicon RNAs in cell culture by small interfering RNAs. Proc. Natl. Acad. Sci. USA 100:235-240.
53. Samuel, C. E. 2001. Antiviral actions of interferons. Clin. Microbiol. Rev. 14:778-809.
54. Santolini, E., G. Migliaccio, and N. La Monica. 1994. Biosynthesis and biochemical properties of the hepatitis C virus core protein. J. Virol. 68:3631-3641.
55. Sarnow, P. 2003. Viral internal ribosome entry site elements: novel ribosome-RNA complexes and roles in viral pathogenesis. J. Virol. 77:2801-2806.
56. Schwarz, D. S., G. Hutvagner, T. Du, Z. Xu, N. Aronin, and P. D. Zamore. 2003. Asymmetry in the assembly of the RNAi enzyme complex. Cell 115:199-208.
57. Shimoike, T., S. Mimori, H. Tani, Y. Matsuura, and T. Miyamura. 1999. Interaction of hepatitis C virus core protein with viral sense RNA and suppression of its translation. J. Virol. 73:9718-9725.
58. Silhavy, D., A. Molnar, A. Lucioli, G. Szittya, C. Hornyik, M. Tavazza, and J. Burgyan. 2002. A viral protein suppresses RNA silencing and binds silencing-generated, 21- to 25-nucleotide double-stranded RNAs. EMBO J. 21:3070-3080.
59. Soneoka, Y., P. M. Cannon, E. E. Ramsdale, J. C. Griffiths, G. Romano, S. M. Kingsman, and A. J. Kingsman. 1995. A transient three-plasmid expression system for the production of high titer retroviral vectors. Nucleic Acids Res. 23:628-633.
60. Spahn, C. M., J. S. Kieft, R. A. Grassucci, P. A. Penczek, K. Zhou, J. A. Doudna, and J. Frank. 2001. Hepatitis C virus IRES RNA-induced changes in the conformation of the 40s ribosomal subunit. Science 291:1959-1962.
61. Theodore, D., and M. W. Fried. 2000. Natural history and disease manifestations of hepatitis C infection. Curr. Top. Microbiol. Immunol. 242:44-54.
62. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
63. Van Regenmortel, M. H. V., C. M. Fauquet, D. H. L Bishop, E. B. Carstens, M. K. Estes, S. M. Lemon, J. Maniloff, M. A. Mayo, D. J. McGeoch, C. R. Pringle, and R. B. Wickner. 2000. Virus taxonomy: the VIIth report of the International Committee on Taxonomy of Viruses. Academic Press, San Diego, Calif.
64. Vidalin, O., M. E. Major, B. Rayner, J. L. Imbach, C. Trepo, and G. Inchauspe. 1996. In vitro inhibition of hepatitis C virus gene expression by chemically modified antisense oligodeoxynucleotides. Antimicrob. Agents Chemother. 40:2337-2344.
65. Vrolijk, J. M., A. Kaul, B. E. Hansen, V. Lohmann, B. L. Haagmans, S. W. Schalm, and R. Bartenschlager. 2003. A replicon-based bioassay for the measurement of interferons in patients with chronic hepatitis C. J. Virol. Methods 110:201-209.
66. Wakita, T., aud J. R. Wands. 1994. Specific inhibition of hepatitis C virus expression by antisense oligodeoxynucleotides. In vitro model for selection of target sequence. J. Biol. Chem. 269:.14205-14210.
67. Walewski, J. L., T. R. Keller, D. D. Stump, and A. D. Branch. 2001. Evidence for a new hepatitis C virus antigen encoded in an overlapping reading frame. RNA 7:710-721.
68. Wilson, J. A., S. Jayasena, A. Khvorova, S. Sabatinos, I. G. Rodrigue-Gervais, S. Arya, F. Sarangi, M. Harris-Brandts, S. Beaulieu, and C. D. Richardson. 2003. RNA interference blocks gene expression and RNA synthesis from hepatitis C replicons propagated in human liver cells. Proc. Natl. Acad. Sci. USA 100:.2783-2788.
69. World Health Organization. 2000. Hepatitis C: global prevalence (update). Wkly. Epidemiol. Rec. 75:18-19.
70. Xu, Z., J. Choi, T. S. Yen, W. Lu, A. Strohecker, S. Govindarajan, D. Chien, M. J. Selby, and J. Ou. 2001. Synthesis of a novel hepatitis C virus protein by ribosomal frameshift. EMBO J. 20:3840-3848.
71. Yanagi, M., R. H. Purcell, S. U. Emerson, and J. Bukh. 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 94:8738-8743.
72. Yanagi, M., R. H. Purcell, S. U. Emerson, and J. Bukh. 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 262:250-263.
73. Yang, D., F. Buchholz, Z. Huang, A. Goga, C. Y. Chen, F. M. Brodsky, and J. M. Bishop. 2002. Short RNA duplexes produced by hydrolysis with Escherichia coli RNase III mediate effective RNA interference in mammalian cells. Proc. Natl. Acad. Sci. USA 99:9942-9947.
74. Yokota, T., N. Sakamoto, N. Enomoto, Y. Tanabe, M. Miyagishi, S. Maekawa, L. Yi, M. Kurosaki, K. Taira, M. Watanabe, and H. Mizusawa. 2003. Inhibition of intracellular hepatitis C virus replication by synthetic and vector-derived small interfering RNAs. EMBO Rep. 4:602-608.