Progress in the use of RNA interference as a therapy for chronic hepatitis B virus infection

Genome Medicine

Volumn 2, Issue 4, 2010, Pages

  Weinberg, Marc S ^a   Arbuthnot, Patrick ^a  

^a UNIVERSITY OF THE WITWATERSRAND MEDICAL SCHOOL   (South Africa)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; HEPATITIS B CORE ANTIBODY; NUCLEOSIDE ANALOG; RIBONUCLEASE; VIRUS VECTOR;

CANCER RISK; CHEMICAL MODIFICATION; DRUG SAFETY; ENZYME BLOOD LEVEL; GENE ACTIVATION; GENE EXPRESSION; GENE SILENCING; GENE THERAPY; GENETIC SUSCEPTIBILITY; HEPATITIS B; HUMAN; NONHUMAN; PRIORITY JOURNAL; REVIEW; RNA INTERFERENCE; RNA TRANSCRIPTION; VIRUS REPLICATION;

EID: 78751693009     PISSN: None     EISSN: 1756994X     Source Type: Journal    
DOI: 10.1186/gm149     Document Type: Review

References (69)

1. Arbuthnot P, Kew M. Hepatitis B virus and hepatocellular carcinoma. Int J Exp Pathol 2001, 82:77-100. 10.1111/j.1365-2613.2001.iep178.x, 11454100.
2. Chisari FV, Ferrari C. Hepatitis B virus immunopathogenesis. Annu Rev Immunol 1995, 13:29-60. 10.1146/annurev.iy.13.040195.000333, 7612225.
3. Keeffe EB, Dieterich DT, Pawlotsky JM, Benhamou Y. Chronic hepatitis B: preventing, detecting, and managing viral resistance. Clin Gastroenterol Hepatol 2008, 6:268-274. 10.1016/j.cgh.2007.12.043, 18328434.
4. Allen MI, Deslauriers M, Andrews CW, Tipples GA, Walters KA, Tyrrell DL, Brown N, Condreay LD. Identification and characterization of mutations in hepatitis B virus resistant to lamivudine. Lamivudine Clinical Investigation Group. Hepatology 1998, 27:1670-1677. 10.1002/hep.510270628, 9620341.
5. Terrault NA. Benefits and risks of combination therapy for hepatitis B. Hepatology 2009, 49(Suppl 5):S122-S128.
6. Greenberg HB, Pollard RB, Lutwick LI, Gregory PB, Robinson WS, Merigan TC. Effect of human leukocyte interferon on hepatitis B virus infection in patients with chronic active hepatitis. N Engl J Med 1976, 295:517-522.
7. Weimar W, Heijtink RA, Schalm SW, van Blankenstein M, Schellekens H, Masurel N, Edy VG, Billiau A, De Somer P. Fibroblast interferon in HBsAg-positive chronic active hepatitis. Lancet 1977, 2:1282. 10.1016/S0140-6736(77)92682-4, 73970.
8. Loomba R, Liang TJ. Treatment of chronic hepatitis B. Antivir Ther 2007, 12(Suppl 3):H33-H41.
9. Ganem D, Prince AM. Hepatitis B virus infection--natural history and clinical consequences. N Engl J Med 2004, 350:1118-1129. 10.1056/NEJMra031087, 15014185.
10. Elbashir SM, Lendeckel W, Tuschl T. RNA interference is mediated by 21- and 22-nucleotide RNAs. Genes Dev 2001, 15:188-200. 10.1101/gad.862301, 312613, 11157775.
11. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans . Nature 1998, 391:806-811. 10.1038/35888, 9486653.
12. Siomi H, Siomi MC. On the road to reading the RNA-interference code. Nature 2009, 457:396-404. 10.1038/nature07754, 19158785.
13. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136:215-233. 10.1016/j.cell.2009.01.002, 19167326.
14. Carmona S, Ely A, Crowther C, Moolla N, Salazar FH, Marion PL, Ferry N, Weinberg MS, Arbuthnot P. Effective inhibition of HBV replication in vivo by anti-HBx short hairpin RNAs. Mol Ther 2006, 13:411-421. 10.1016/j.ymthe.2005.10.013, 16337206.
15. Giladi H, Ketzinel-Gilad M, Rivkin L, Felig Y, Nussbaum O, Galun E. Small interfering RNA inhibits hepatitis B virus replication in mice. Mol Ther 2003, 8:769-776. 10.1016/S1525-0016(03)00244-2, 14599810.
16. Klein C, Bock CT, Wedemeyer H, Wustefeld T, Locarnini S, Dienes HP, Kubicka S, Manns MP, Trautwein C. Inhibition of hepatitis B virus replication in vivo by nucleoside analogues and siRNA. Gastroenterology 2003, 125:9-18. 10.1016/S0016-5085(03)00720-0, 12851866.
17. McCaffrey AP, Nakai H, Pandey K, Huang Z, Salazar FH, Xu H, Wieland SF, Marion PL, Kay MA. Inhibition of hepatitis B virus in mice by RNA interference. Nat Biotechnol 2003, 21:639-644. 10.1038/nbt824, 12740585.
18. Shlomai A, Shaul Y. Inhibition of hepatitis B virus expression and replication by RNA interference. Hepatology 2003, 37:764-770. 10.1053/jhep.2003.50146, 12668968.
19. Mason WS, Aldrich C, Summers J, Taylor JM. Asymmetric replication of duck hepatitis B virus DNA in liver cells: Free minus-strand DNA. Proc Natl Acad Sci USA 1982, 79:3997-4001. 10.1073/pnas.79.13.3997, 346563, 6287459.
20. Weiser B. As they lay dying, Part 1. The doctor's agony: deciding to end life-saving therapy. Washington Post 1983, 17. A1, A16.
21. Mason WS, Halpern MS, England JM, Seal G, Egan J, Coates L, Aldrich C, Summers J. Experimental transmission of duck hepatitis B virus. Virology 1983, 131:375-384. 10.1016/0042-6822(83)90505-6, 6659368.
22. Behlke MA. Chemical modification of siRNAs for in vivo use. Oligonucleotides 2008, 18:305-319. 10.1089/oli.2008.0164, 19025401.
23. Morrissey DV, Lockridge JA, Shaw L, Blanchard K, Jensen K, Breen W, Hartsough K, Machemer L, Radka S, Jadhav V, Vaish N, Zinnen S, Vargeese C, Bowman K, Shaffer CS, Jeffs LB, Judge A, MacLachlan I, Polisky B. Potent and persistent in vivo anti-HBV activity of chemically modified siRNAs. Nat Biotechnol 2005, 23:1002-1007. 10.1038/nbt1122, 16041363.
24. Muhonen P, Tennila T, Azhayeva E, Parthasarathy RN, Janckila AJ, Vaananen HK, Azhayev A, Laitala-Leinonen T. RNA interference tolerates 2'-fluoro modifications at the Argonaute2 cleavage site. Chem Biodivers 2007, 4:858-873. 10.1002/cbdv.200790073, 17511001.
25. Robbins M, Judge A, Liang L, McClintock K, Yaworski E, MacLachlan I. 2'-O-methyl-modified RNAs act as TLR7 antagonists. Mol Ther 2007, 15:1663-1669. 10.1038/sj.mt.6300240, 17579574.
26. Jackson AL, Burchard J, Leake D, Reynolds A, Schelter J, Guo J, Johnson JM, Lim L, Karpilow J, Nichols K, Marshall W, Khvorova A, Linsley PS. Position-specific chemical modification of siRNAs reduces "off-target" transcript silencing. RNA 2006, 12:1197-1205. 10.1261/rna.30706, 1484422, 16682562.
27. Fisher M, Abramov M, Van Aerschot A, Xu D, Juliano RL, Herdewijn P. Inhibition of MDR1 expression with altritol-modified siRNAs. Nucleic Acids Res 2007, 35:1064-1074. 10.1093/nar/gkl1126, 1851637, 17264131.
28. Hean J, Crowther C, Ely A, ul Islam R, Barichievy S, Bloom K, Weinberg MS, van Otterlo W, de Koning C, Salazar F, Marion P, Roesch E, LeMaitre M, Herdewijn P, Arbuthnot P. Inhibition of Hepatitis B virus replication in vivo using lipoplexes containing altritol-modified antiviral siRNAs. Artificial DNA: PNA & XNA 2010,
29. Hornung V, Guenthner-Biller M, Bourquin C, Ablasser A, Schlee M, Uematsu S, Noronha A, Manoharan M, Akira S, de Fougerolles A, Endres S, Hartmann G. Sequence-specific potent induction of IFN-alpha by short interfering RNA in plasmacytoid dendritic cells through TLR7. Nat Med 2005, 11:263-270. 10.1038/nm1191, 15723075.
30. 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 2005, 23:457-462. 10.1038/nbt1081, 15778705.
31. Soutschek J, Akinc A, Bramlage B, Charisse K, Constien R, Donoghue M, Elbashir S, Geick A, Hadwiger P, Harborth J, John M, Kesavan V, Lavine G, Pandey RK, Racie T, Rajeev KG, Rohl I, Toudjarska I, Wang G, Wuschko S, Bumcrot D, Koteliansky V, Limmer S, Manoharan M, Vornlocher HP. Therapeutic silencing of an endogenous gene by systemic administration of modified siRNAs. Nature 2004, 432:173-178. 10.1038/nature03121, 15538359.
32. Khvorova A, Reynolds A, Jayasena SD. Functional siRNAs and miRNAs exhibit strand bias. Cell 2003, 115:209-216. 10.1016/S0092-8674(03)00801-8, 14567918.
33. Chen PY, Weinmann L, Gaidatzis D, Pei Y, Zavolan M, Tuschl T, Meister G. Strand-specific 5'-O-methylation of siRNA duplexes controls guide strand selection and targeting specificity. RNA 2008, 14:263-274. 10.1261/rna.789808, 2212253, 18094121.
34. Myers JW, Jones JT, Meyer T, Ferrell JE. Recombinant Dicer efficiently converts large dsRNAs into siRNAs suitable for gene silencing. Nat Biotechnol 2003, 21:324-328. 10.1038/nbt792, 12592410.
35. Yang D, Buchholz F, Huang Z, Goga A, Chen CY, Brodsky FM, Bishop JM. Short RNA duplexes produced by hydrolysis with Escherichia coli RNase III mediate effective RNA interference in mammalian cells. Proc Natl Acad Sci USA 2002, 99:9942-9947. 10.1073/pnas.152327299, 126604, 12096193.
36. Ghildiyal M, Seitz H, Horwich MD, Li C, Du T, Lee S, Xu J, Kittler EL, Zapp ML, Weng Z, Zamore PD. Endogenous siRNAs derived from transposons and mRNAs in Drosophila somatic cells. Science 2008, 320:1077-1081. 10.1126/science.1157396, 18403677.
37. Tam OH, Aravin AA, Stein P, Girard A, Murchison EP, Cheloufi S, Hodges E, Anger M, Sachidanandam R, Schultz RM, Hannon GJ. Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes. Nature 2008, 453:534-538. 10.1038/nature06904, 18404147.
38. Xuan B, Qian Z, Hong J, Huang W. EsiRNAs inhibit Hepatitis B virus replication in mice model more efficiently than synthesized siRNAs. Virus Res 2006, 118:150-155. 10.1016/j.virusres.2005.12.005, 16423421.
39. Wu Y, Huang AL, Tang N, Zhang BQ, Lu NF. Specific anti-viral effects of RNA interference on replication and expression of hepatitis B virus in mice. Chin Med J (Engl) 2005, 118:1351-1356.
40. Zhang XN, Xiong W, Wang JD, Hu YW, Xiang L, Yuan ZH. siRNA-mediated inhibition of HBV replication and expression. World J Gastroenterol 2004, 10:2967-2971.
41. Starkey JL, Chiari EF, Isom HC. Hepatitis B virus (HBV)-specific short hairpin RNA is capable of reducing the formation of HBV covalently closed circular (CCC) DNA but has no effect on established CCC DNA in vitro. J Gen Virol 2009, 90:115-126. 10.1099/vir.0.004408-0, 2659548, 19088280.
42. Hamasaki K, Nakao K, Matsumoto K, Ichikawa T, Ishikawa H, Eguchi K. Short interfering RNA-directed inhibition of hepatitis B virus replication. FEBS Lett 2003, 543:51-54. 10.1016/S0014-5793(03)00400-9, 12753904.
43. Grimm D, Streetz KL, Jopling CL, Storm TA, Pandey K, Davis CR, Marion P, Salazar F, Kay MA. Fatality in mice due to oversaturation of cellular microRNA/short hairpin RNA pathways. Nature 2006, 441:537-541. 10.1038/nature04791, 16724069.
44. Ely A, Naidoo T, Arbuthnot P. Efficient silencing of gene expression with modular trimeric Pol II expression cassettes comprising microRNA shuttles. Nucleic Acids Res 2009, 37:e91. 10.1093/nar/gkp446, 2715259, 19474340.
45. Ely A, Naidoo T, Mufamadi S, Crowther C, Arbuthnot P. Expressed anti-HBV primary microRNA shuttles inhibit viral replication efficiently in vitro and in vivo. Mol Ther 2008, 16:1105-1112. 10.1038/mt.2008.82, 18431360.
46. Snyder LL, Esser JM, Pachuk CJ, Steel LF. Vector design for liver-specific expression of multiple interfering RNAs that target hepatitis B virus transcripts. Antiviral Res 2008, 80:36-44. 10.1016/j.antiviral.2008.04.001, 2573035, 18499277.
47. Liu YP, Haasnoot J, ter Brake O, Berkhout B, Konstantinova P. Inhibition of HIV-1 by multiple siRNAs expressed from a single microRNA polycistron. Nucleic Acids Res 2008, 36:2811-2824. 10.1093/nar/gkn109, 2396423, 18346971.
48. Gill DR, Pringle IA, Hyde SC. Progress and prospects: the design and production of plasmid vectors. Gene Ther 2009, 16:165-171. 10.1038/gt.2008.183, 19129858.
49. Chattopadhyay S, Ely A, Bloom K, Weinberg MS, Arbuthnot P. Inhibition of hepatitis B virus replication with linear DNA sequences expressing antiviral micro-RNA shuttles. Biochem Biophys Res Commun 2009, 389:484-489. 10.1016/j.bbrc.2009.09.004, 19733548.
50. Schakowski F, Gorschluter M, Junghans C, Schroff M, Buttgereit P, Ziske C, Schottker B, Konig-Merediz SA, Sauerbruch T, Wittig B, Schmidt-Wolf IG. A novel minimal-size vector (MIDGE) improves transgene expression in colon carcinoma cells and avoids transfection of undesired DNA. Mol Ther 2001, 3:793-800. 10.1006/mthe.2001.0322, 11356084.
51. Johansson P, Lindgren T, Lundstrom M, Holmstrom A, Elgh F, Bucht G. PCR-generated linear DNA fragments utilized as a hantavirus DNA vaccine. Vaccine 2002, 20:3379-3388. 10.1016/S0264-410X(02)00265-7, 12213408.
52. Salman H, Zbaida D, Rabin Y, Chatenay D, Elbaum M. Kinetics and mechanism of DNA uptake into the cell nucleus. Proc Natl Acad Sci USA 2001, 98:7247-7252. 10.1073/pnas.121067698, 34654, 11390964.
53. Yang PL, Althage A, Chung J, Chisari FV. Hydrodynamic injection of viral DNA: a mouse model of acute hepatitis B virus infection. Proc Natl Acad Sci USA 2002, 99:13825-13830. 10.1073/pnas.202398599, 129782, 12374864.
54. Mercer DF, Schiller DE, Elliott JF, Douglas DN, Hao C, Rinfret A, Addison WR, Fischer KP, Churchill TA, Lakey JR, Tyrrell DL, Kneteman NM. Hepatitis C virus replication in mice with chimeric human livers. Nat Med 2001, 7:927-933. 10.1038/90968, 11479625.
55. Meuleman P, Leroux-Roels G. The human liver-uPA-SCID mouse: a model for the evaluation of antiviral compounds against HBV and HCV. Antiviral Res 2008, 80:231-238. 10.1016/j.antiviral.2008.07.006, 18706933.
56. Summers J, Smolec JM, Snyder R. A virus similar to human hepatitis B virus associated with hepatitis and hepatoma in woodchucks. Proc Natl Acad Sci USA 1978, 75:4533-4537. 10.1073/pnas.75.9.4533, 336150, 212758.
57. Walter E, Keist R, Niederost B, Pult I, Blum HE. Hepatitis B virus infection of tupaia hepatocytes in vitro and in vivo. Hepatology 1996, 24:1-5.
58. Asabe S, Wieland SF, Chattopadhyay PK, Roederer M, Engle RE, Purcell RH, Chisari FV. The size of the viral inoculum contributes to the outcome of hepatitis B virus infection. J Virol 2009, 83:9652-9662. 10.1128/JVI.00867-09, 2748002, 19625407.
59. Zhang L, Peeples ME, Boucher RC, Collins PL, Pickles RJ. Respiratory syncytial virus infection of human airway epithelial cells is polarized, specific to ciliated cells, and without obvious cytopathology. J Virol 2002, 76:5654-5666. 10.1128/JVI.76.11.5654-5666.2002, 137037, 11991994.
60. Wu GY, Wu CH. Receptor-mediated gene delivery and expression in vivo. J Biol Chem 1988, 263:14621-14624.
61. Carmona S, Jorgensen MR, Kolli S, Crowther C, Salazar FH, Marion PL, Fujino M, Natori Y, Thanou M, Arbuthnot P, Miller AD. Controlling HBV replication in vivo by intravenous administration of triggered PEGylated siRNA-nanoparticles. Mol Pharm 2009, 6:706-717. 10.1021/mp800157x, 19159285.
62. Semple SC, Akinc A, Chen J, Sandhu AP, Mui BL, Cho CK, Sah DW, Stebbing D, Crosley EJ, Yaworski E, Hafez IM, Dorkin JR, Qin J, Lam K, Rajeev KG, Wong KF, Jeffs LB, Nechev L, Eisenhardt ML, Jayaraman M, Kazem M, Maier MA, Srinivasulu M, Weinstein MJ, Chen Q, Alvarez R, Barros SA, De S, Klimuk SK, et al. Rational design of cationic lipids for siRNA delivery. Nat Biotechnol 28:172-176. 10.1038/nbt.1602, 20081866.
63. 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 2005, 102:773-778. 10.1073/pnas.0409028102, 545555, 15640346.
64. Giering JC, Grimm D, Storm TA, Kay MA. Expression of shRNA from a tissue-specific pol II promoter is an effective and safe RNAi therapeutic. Mol Ther 2008, 16:1630-1636. 10.1038/mt.2008.144, 18665161.
65. Crowther C, Ely A, Hornby J, Mufamadi S, Salazar F, Marion P, Arbuthnot P. Efficient inhibition of hepatitis B virus replication in vivo, using polyethylene glycol-modified adenovirus vectors. Hum Gene Ther 2008, 19:1325-1331. 10.1089/hum.2008.066, 19848584.
66. Rauschhuber C, Xu H, Salazar FH, Marion PL, Ehrhardt A. Exploring gene-deleted adenoviral vectors for delivery of short hairpin RNAs and reduction of hepatitis B virus infection in mice. J Gene Med 2008, 10:878-889. 10.1002/jgm.1207, 18470951.
67. Chen CC, Ko TM, Ma HI, Wu HL, Xiao X, Li J, Chang CM, Wu PY, Chen CH, Han JM, Yu CP, Jeng KS, Hu CP, Tao MH. Long-term inhibition of hepatitis B virus in transgenic mice by double-stranded adeno-associated virus 8-delivered short hairpin RNA. Gene Ther 2007, 14:11-19. 10.1038/sj.gt.3302846, 16929350.
68. Chen CC, Sun CP, Ma HI, Fang CC, Wu PY, Xiao X, Tao MH. Comparative study of anti-hepatitis B virus RNA interference by double-stranded adeno-associated virus serotypes 7, 8, and 9. Mol Ther 2009, 17:352-359. 10.1038/mt.2008.245, 2835062, 19066602.
69. Davis ME, Zuckerman JE, Choi CH, Seligson D, Tolcher A, Alabi CA, Yen Y, Heidel JD, Ribas A. Evidence of RNAi in humans from systemically administered siRNA via targeted nanoparticles. Nature 2010, doi:10.1038/nature08956.