Potential role of RNAi in the treatment of HCV infection

Expert Review of Anti-Infective Therapy

Volumn 5, Issue 5, 2007, Pages 823-831

  Volarevic, Martina ^a   Smolic, Robert ^a   Wu, Catherine H ^a   Wu, George Y ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

Double stranded RNA; Hepatitis C virus; Japanese fulminant hepatitis 1; RNAi; shRNA; Subgenomic replicon system

Indexed keywords

DICER; DNA; DOUBLE STRANDED RNA; MICRORNA; RNA DIRECTED RNA POLYMERASE; RNA INDUCED SILENCING COMPLEX; SHORT HAIRPIN RNA; SINGLE STRANDED RNA; SMALL INTERFERING RNA; VIRUS RNA; VIRUS VECTOR;

5' UNTRANSLATED REGION; CELL CULTURE; CELL IMMORTALIZATION; DNA METHYLATION; DRUG RESEARCH; ELECTROPORATION; GENE DELETION; GENE EXPRESSION; GENE FUNCTION; GENE SILENCING; GENETIC ANALYSIS; GENETIC TRANSFECTION; HEPATITIS C; HEPATITIS C VIRUS; HETEROCHROMATIN; HUMAN; INHIBITION KINETICS; LIVER CELL CARCINOMA; LIVER CIRRHOSIS; MAMMAL CELL; MEDICAL DECISION MAKING; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; REPLICON; REVIEW; RNA CLEAVAGE; RNA INTERFERENCE; RNA SYNTHESIS; VIRAL GENE DELIVERY SYSTEM; VIRUS REPLICATION; VIRUS RESISTANCE;

GENE EXPRESSION REGULATION, VIRAL; HEPACIVIRUS; HEPATITIS C, CHRONIC; REPLICON; RNA INTERFERENCE; RNA, SMALL INTERFERING; VIRUS REPLICATION;

EID: 35348945357     PISSN: 14787210     EISSN: 17448336     Source Type: Journal    
DOI: 10.1586/14787210.5.5.823     Document Type: Review

References (94)

1. Hoofnagle JH. Course and outcome of hepatitis C. Hepatalogy 36 (5 Suppl. 1), S21-S29 (2002).
2. Fishman JA, Rubin RH, Koziel MJ, Periera BJ. Hepatitis C virus and organ transplantation. Transplantation 62(2), 147-154 (1996).
3. Alter MJ. Epidemiology of hepatitis C virus infection. World J. Gastroenterol. 13(17), 2436-2441 (2007).
4. Alter HJ, Seeff LB. Recovery, persistence, and sequelae in hepatitis C virus infection: a perspective on long-term outcome. Semin. Liver Dis. 20(1), 17-35 (2000).
5. Bowen DG, Walker CM. The origin of quasispecies: cause or consequence of chronic hepatitis C viral infection? J. Hepatol. 42 (3), 408-417 (2005).
6. Lohmann V, Koch JO, Bartenschlager R. Processing pathways of the hepatitis C virus proteins. J. Hepatol. 24 (Suppl. 2), 11-19 (1996).
7. Penin F, Dubuisson J, Rey FA, Moradpour D, Pawlotsky JM. Structural biology of hepatitis C virus. Hepatology 39(1), 5-19 (2004).
8. Moradpour D, Brass V, Bieck E et al. Membrane association of the RNA-dependent RNA polymerase is essential for hepatitis C virus RNA replication. J. Virol. 78(23), 13278-13284 (2004).
9. Lohmann V, Korner F, Koch J, Herian U, Theilmann L, Bartenschlager R. Replication of subgenomic hepatitis C virus RNAs in a hepatoma cell line. Science 285(5424), 110-113 (1999).
10. Krieger N, Lohmann V, Bartenschlager R. Enhancement of hepatitis C virus RNA replication by cell culture-adaptive mutations. J Virol. 75(10), 4614-4624 (2001).
11. Blight KJ, Kolykhalov AA, Rice CM. Efficient initiation of HCV RNA replication in cell culture. Science 290(5498), 1972-1974 (2000).
12. Blight KJ, McKeating JA, Rice CM. Highly permissive cell lines for subgenomic and genomic hepatitis C virus RNA replication. J. Virol. 76(24), 13001-13014 (2002).
13. Lindenbach BD, Evans MJ, Syder AJ et al. Complete replication of hepatitis C virus in cell culture. Science 309(5734), 623-626 (2005).
14. Wakita. T, Pietschmann T, Kato T et al. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat. Med. 11 (7), 791-796 (2005).
15. Zhong J, Gastaminza P, Cheng G et al. Robust hepatitis C virus infection [ in vitro. Proc. Natl. Acad. Sci. USA 102(26), 9294-9299 (2005).
16. 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. 79, 13963-13973 (2005).
17. Kanda T, Basu A, Steele R et al. Generation of infectious hepatitis C virus in immortalized human hepatocytes. J. Virol. 80(9), 4633-4639 (2006).
18. Lazaro CA, Chang M, Tang W et al. Hepatitis C virus replication In transfected and serum-infected cultured human fetal hepatocytes. Am. J. Pathol. 170(2), 478-489 (2007).
19. Elbashir SM, Lendeckel W, Tuschl T. RNA interference is mediated by 21- and 22-nucleotide RNAs. Genes Dev. 15(2), 188-200 (2001).
20. Elbashir SM, Martinez J, Patkaniowska A, Lendeckel W, Tuschl T. Functional anatomy of siRNAs for mediating efficient RNAi in Drasophila melanogaster embryo lysate. EMBO J. 20(23), 6877-6888 (2001).
21. Hamilton AJ, Baulcombe DC. A species of small antisense RNA in posttransriptional gene silencing in plants. Science 286, 950-952 (1999).
22. Napoli C, Lemieux C, Jorgensen R. Introduction of a chimeric chalcone synthase gene into petunia results in reversible co-suppression of homologous genes in trans. Plant Cell 2, 279-289 (1990).
23. Eire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC. Potent and specific genetic interference by double-stranded RNA in Caenarhabditis elegans. Nature 391(6669), 806-811 (1998).
24. Kennerdell JR, Carthew RW. Use of dsRNA-mediated genetic interference to demonstrate that frizzled and frizzled 2 act in the wingless pathway Cell 95(7), 1017-1026 (1998).
25. Misquitta L, Paterson BM. Targeted disruption of gene function in Drosophila by RNA interference (RNA-i), a role for nautilus in embryonic somatic muscle formation. Proc. Natl. Acad. Sci. USA 96 (4), 1451-1456 (1999).
26. Ngo H, Tschudi C, Gull K, Ullu E. Double-stranded RNA induces mRNA degradation in Trypanosoma brucei. Proc. Natl. Acad. Sci. USA. 95 (25), 14687-14692 (1998).
27. Elbashir SM, Harborth J, Weber K, Tuschl T. Analysis of gene function in somatic mammalian cells using small interfering RNAs. Methods 26(2), 199-213 (2002).
28. Wianny F, Zernicka-Goetz M. Specific interference with gene function by double-stranded RNA in early mouse development. Nat. Cell. Biol. 2(2), 70-75 (2000).
29. Yang S, Tutton S, Pierce E, Yoon K. Specific double-stranded RNA interference in undifferentisted mouse embryonic stem cells. Mol. Cell. Biol. 21(22), 7807-7816 (2001).
30. Zamore PD, Tuschi T, Sharp PA, Bartel DP. RNAi: doule-stranded RNA directs the ATP-dependent cleavage of mRNA at 21 to 23 nucleotide intervals. Cell 101 (1), 25-33 (2000).
31. Olsen PH, Ambros V. The lin-4 regulatory RNA controls developmental timing in Caenorhabditis elegans by blocking LIN- 14 protein synthesis after the initiation of translation. Dev Biol. 216(2), 671-680 (1999).
32. Tang G, Reinhart BJ, Bartel DP, Zamore PD. A biochemical framework for RNA silencing in plants. Genes Dev. 17(1), 49-63 (2003).
33. Hamilton A, Voinnet O, Chappell L, Baulcombe D. Two classes of short interfering RNA in RNA silencing. EMBO J. 21(17), 4671-4679 (2002).
34. Volpe TA, Kidner C, Hall IM, Teng G, Grewal SI, Martienssen RA. Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 297(5588), 1833-1837 (2002).
35. Hall IM, Shankaranarayana GD, Noma K, Ayoub N, Cohen A, Grewal SI. Establishment and maintenance of a heterochromatin domain. Science 297(5590), 2232-2237 (2002).
36. Mochizuki K, Fine NA, Fujisawa T, Gorovsky MA. Analysis of a piwi-related gene implicates small RNAs in genome rearrangement in tetrahymena. Cell 110(6). 689-699 (2002).
37. Bosher JM, Labouesse M. RNA interference: genetic wand and genetic watchdog. Nat. Cell Biol. 2(2), E31-E36 (2000).
38. Hannon GJ. RNA interference. Nature 418(6894), 244-251 (2002).
39. Bernstein E, Caudy AA, Hammond SM, Hannon GJ. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409 (6818), 363-366 (2001).
40. Nykanen A, Haley B, Zamore PD. ATP requirements and small interfering RNA structure in the RNA interference pathway. Cell 107(3), 309-321 (2001).
41. Hammond SM, Bernstein E, Beach D, Hannon GJ. An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells. Nature 404 (6775), 293-296 (2000).
42. Elbashir SM, Harborth J, Lendeckel W, Yalcin A, Weber K, Tuschl T. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411, 494-498 (2001).
43. Caplen NJ, Parrish S, Imani F, Fire A, Morgan RA. Specific inhibition of gene expression by small double-stranded RNAs in invertebrate and vertebrate systems. Proc. Natl. Acad Sci. USA. 98(17), 9742-9747 (2001).
44. Billy E, Brondani V, Zhang H, Muller U, Filipowicz W. Specific interference with gene expression induced by long, double-stranded RNA in mouse embryonal teratocarcinoma cell lines. Proc. Natl. Acad. Sci. USA 98(25), 14428-14433 (2001).
45. Sledz CA, Holko M, de Veer MJ, Silverman RH, Williams BR. Activation of the interferon system by short-interfering RNAs. Natl. Cell Biol. 5(9), 834-839 (2003).
46. Persengiev SP, Zhu X, Green MR. Nonspecific, concentration-dependent stimulation and repression of mammalian gene expression by small interfering RNAs (siRNAs). RNA 10(1), 12-18 (2004).
47. Almeida R, Allshire RC. RNA silencing and genome regulation. Trends Cell Biol. 15(5), 251-258 (2005).
48. Zamore PD, Haley B. Ribo-gnome: the big world of small RNAs. Science 309(5740), 1519-1524 (2005).
49. Simeoni F, Morris MC, Heitz F, Divita G. Insight into the mechanism of the peptide-based gene delivery system MPG: implications for delivery of siRNA into mammalian cells. Nucleic Acids Res. 31(11), 2717-2724 (2003).
50. Kronke J, Kittler R, Buchholz F et al. Alternative approaches for efficient inhibition of hepatitis C virus RNA replication by small interfering RNAs. J. Virol. 78, 3436-3446 (2004).
51. Kapadia SB, Brideau-Andersen A, Chisari FV. Interference of hepatitis C virus RNA replication by short interfering RNAs. Proc. Natl Acad. Sci. USA 100, 2014-2018 (2003).
52. Yokota T, Sakamoto N, Enomoto N et al. Inhibition of intracellular hepatitis C virus replication by synthetic and vector-derived small interfering RNAs. EMBO Rep. 4, 602-608 (2003).
53. Wilson JA, Jayasena S, Khvorova A et al. 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 (2003).
54. Randall G, Grakoui A, Rice CM. Clearance of replicating hepatitis C virus replicon RNAs in cell culture by small interfering RNAs. Proc. Natl Acad. Sci. USA 100, 235-240 (2003).
55. Seo MY, Abrignani S, Houghton M, Han JH. Small interfering RNA-mediated inhibition of hepatitis C virus replication in the human hepatoma cell line Huh-7. J. Virol. 77(1), 810-812 (2003).
56. Korf M, Meyer A, Jarczak D, Beger C, Manns MP, Kruger M. Inhibition of HCV subgenomic replicons by siRNAs derived from plasmids with opposing U6 and H1 promoters. J. Viral. Hepat. 14 (2), 122-132 (2007).
57. Smith RM, Smolic R, Volarevic M, Wu GY. Positional effects and strand preference of RNA interference against hepatitis C virus target sequences. J. Viral. Hepat. 14(3), 194-212 (2007).
58. Kanda T, Steele R, Ray R, Ray RB. Small interfering RNA targeted to hepatitis C virus 5′ nontranslated region exerts potent antiviral effect. J. Virol. 81(2), 669-676 (2007).
59. Prabhu R, Garry RF, Dash S. Small interfering RNA targeted to stem-loop II of the 5′ untranslated region effectively inhibits expression of six HCV genotypes. Virol. J. 27(3), 100 (2006).
60. Prabhu R, Vittal P, Yin Q et al. Small interfering RNA effectively inhibits protein expression and negative strand RNA synthesis from a full-length hepatitis C virus clone, J. Med. Virol. 76(4), 511-519 (2005).
61. Domitrovich AM, Diebei KW, Ali N, Sarker S, Siddiqui A. Role of La autoantigen and polypyrimidine tract-binding protein in HCV replication. Virology 335(1), 72-86 (2005).
62. Chang KS, Luo G. The polypyrimidine tract-binding protein (PTB) is required for efficient replication of hepatitis C virus (HCV) RNA. Virus Res. 115 (1), 1-8 (2005).
63. Hamamoto I, Nishimura Y, Okamoto T et al. Human VAP-B is involved in hepatitis C virus replication through interaction with NS5A and NS5B. J. Virol. 79(21), 13473-13482 (2005).
64. Lan S, Wang H, Jiang H et al. Direct interaction between α-actinin and hepatitis C virus NS5B. FEBS Lett. 554(3), 289-294 (2003).
65. Mannova P, Beretta L. Activation of the N-Ras-PI3K-Akt-mTOR pathway by hepatitis C virus: control of cell survival and viral replication. J. Virol. 79 (14), 8742-8749 (2005).
66. Wilson, JA, Richardson CD. Hepatitis C virus repilcons escape RNA interference induced by a short interfering RNA directed against the NS5b coding region. J. Virol. 79, 7050-7058 (2005).
67. Harris D, Zhang Z, Chaubey B, Pandey VN. Identification of cellular factors associated with the 3′-nontranslated region of the hepatitis C virus genome. Mol. Cell Proteomics 5(6), 1006-1018 (2006).
68. Konishi M, Wu CH, Kaito M et al. siRNA-resistance in treated HCV replicon cells is correlated with the development of specific HCV mutations. J. Viral. Hepat. 13(11), 756-761 (2006).
69. De Francesco R, Migliaccic, G. Challenges and successes in developing new therapies for hepatitis C. Nature 436(7053), 953-960 (2005).
70. Wang Y, Kato N, Jazag A et al. Hepatitis C virus core protein is a potent inhibitor of RNA silencing-based antiviral response. Gastroenterology 130(3), 883-892 (2006).
71. Korf M. Jarczak D, Beger C, Manns MP, Kruger M. Inhibition of hepatitis C virus translation and subgenomic replication by siRNAs directed against highly conserved HCV sequence and cellular HCV cofactors. J. Hepatol. 43(2), 225-234 (2005).
72. Jarczak D, Korf M, Beger C, Manns MP, Kruger M. Hairpin ribozymes in combination with siRNAs against highly conserved hepatitis C virus sequence inhibit RNA replication and protein translation from hepatitis C virus subgenomic replicons. FEBS J. 272(22), 5910-5922 (2005).
73. Jackson AL, Linsley PS. Noise amidst the silence: off-target effects of siRNAs? Trends Genet. 20(11), 521-524 (2004).
74. Grimm D, Streetz KL, Jopling CL et al. Fatality In mice due to oversaturation of cellular microRNA/short hairpin RNA pathways. Nature 441(7092), 537-541 (2006).
75. Judge AD, Sood V, Shaw JR, Fang D, McClintock K, MacLachlan I. Sequence-dependent stimulation of the mammalian innate immune response by synthetic siRNA. Nat. Biotechnol. 23(4), 457-462 (2005).
76. Braaseh DA, Paroo Z, Constantinescu A et al. Biodistribution of phosphodiester and phosphorothioate siRNA. Bioorg. Med. Chem. Lett. 14, 1139-1143 (2004).
77. Kakizawa Y, Furukawa S, Kataoka K. Block copolymer-coated calcium phosphate nanoparticles sensing intracellular environment for oligodeoxynucleotide and siRNA delivery. J. Control. Release 97(2), 345-356 (2004).
78. Simeoni F, Morris MC, Heitz F, Divita G. Insight into the mechanism of the peptide-based gene delivery system MPG: implications for delivery of siRNA into mammalian cells. Nucleic Acids Res. 31(11), 2717-2724 (2003).
79. Song E, Lee SK, Wang J et al. RNA interference targeting Fas protects mice from fulminant hepatitis. Nat. Med. 9, 347-351 (2003).
80. McCaffrey AP, Meuse L, Pham TT, Conklin DS, Hannon GJ, Kay MA. RNA interference in adult mice. Nature 418, 38-39 (2002).
81. Lewis DL, Wolff JA. Delivery of siRNA and siRNA expression constructs to adult mammals by hydrodynamic intravascular injection. Meth. Enzymol. 392, 336-350 (2005).
82. Uprichard SL, Boyd B, Althage A, Chisari FV. Clearance of hepatitis B virus from the liver of transgenic mice by short hairpin RNAs. Proc. Natl Acad Sci. USA 102, 773-718 (2005).
83. Morrissey DV, Lockridge JA, Shaw L et al. Potent and persistent in vivo anti-HBV activity of chemically modified siRNAs. Nat. Biotechnol. 23(8), 1002-1007 (2005).
84. Landen CN Jr, Chavez-Reyes A. Bucana C et al. Therapeutic EphA2 gene targeting in vivo using neutral liposomal small interfering RNA delivery. Cancer Res. 65(15), 6910-6918 (2005).
85. Sorensen DR, Leirdal M, Sloud M. Gene silencing by systemic delivery of synthetic siRNAs in adult mice. J. Mol. Biol. 327(4), 761-766 (2003).
86. Urban-Klein B, Werth S, Abuharbeld S, Czubayko F, Aigner A. RNAi-mediated gene-targeting through systemic application of polyethylenimine (PEI)-complexed siRNA in vivo. Gene Ther. 12(5), 461-466 (2005).
87. Song E, Zhu P, Lee SK et al. Antibody mediated in vivo delivery of small interfering RNAs via cell-surface receptors. Nat. Biotechnol. 23(6), 709-717 (2005).
88. Kim SI, Shin D, Choi TH et al. Systemic and specific delivery of small interfering RNAs to the liver mediated by apolipoprotein A-I. Mol. Ther. 15 (6), 1145-1152 (2007).
89. Wen WH, Liu JY, Qin WJ et al. Targeted inhibition of HBV gene expression by single-chain antibody mediated small interfering RNA delivery. Hepatalogy 46(1), 84-94 (2007).
90. Soutschek J, Akinc A, Bramlage B et al. Therapeutic silencing of an endogenous gene by systemic administration of modified siRNAs. Nature 432, 173-178 (2004).
91. Morrissey DV, Blanchard K, Shaw L et al. Activity of stabilized short interfering RNA in a mouse model of hepatitis B virus replication. Hepatology 41(6), 130-1356 (2005).
92. Randall G. Progress toward the therapy of hepatitis with RNA interference. Hepatology 41, 1220-1222 (2005).
93. Zimmermann TS, Lee AC, Akinc A et al. RNAi-mediated gene silencing in non-human primates. Nature 4, 441(7089), 111-114 (2006).
94. Feld JJ, Hoofnagle JH. Mechanism of action of interferon and ribavirin in treatment of hepatitis C. Nature 436(7053), 967-972 (2005).