In vivo therapeutic potential of dicer-hunting siRNAs targeting infectious hepatitis C virus

Scientific Reports

Volumn 4, Issue , 2014, Pages

  Watanabe, Tsunamasa ^a,b,f   Hatakeyama, Hiroto ^c   Matsuda Yasui, Chiho ^a   Sato, Yusuke ^c   Sudoh, Masayuki ^d   Takagi, Asako ^a   Hirata, Yuichi ^a,b   Ohtsuki, Takahiro ^a   Arai, Masaaki ^e   Inoue, Kazuaki ^b   Harashima, Hideyoshi ^c   Kohara, Michinori ^a  

^a TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

^b SHOWA UNIVERSITY FUJIGAOKA HOSPITAL   (Japan)

^c HOKKAIDO UNIVERSITY   (Japan)

^d CHUGAI PHARMACEUTICAL CO LTD   (Japan)

^e MITSUBISHI TANABE PHARMA CORPORATION   (Japan)

^f NAGOYA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICAL SCIENCES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

5' UNTRANSLATED REGION; RIBONUCLEASE III; SMALL INTERFERING RNA; VIRUS RNA;

5' UNTRANSLATED REGION; ANIMAL; CELL LINE; DISEASE MODEL; GENE SILENCING; GENETICS; HEPACIVIRUS; HEPATITIS C; HUMAN; LIVER CELL; MALE; METABOLISM; MOUSE; PH; RNA INTERFERENCE; TRANSGENIC MOUSE; VIROLOGY; VIRUS GENOME; VIRUS REPLICATION;

5' UNTRANSLATED REGIONS; ANIMALS; CELL LINE; DISEASE MODELS, ANIMAL; GENE SILENCING; GENOME, VIRAL; HEPACIVIRUS; HEPATITIS C; HEPATOCYTES; HUMANS; HYDROGEN-ION CONCENTRATION; MALE; MICE; MICE, TRANSGENIC; RIBONUCLEASE III; RNA INTERFERENCE; RNA, SMALL INTERFERING; RNA, VIRAL; VIRUS REPLICATION;

EID: 84899118380     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep04750     Document Type: Article

References (50)

1. Hoofnagle, J. H. & Seeff, L. B. Peginterferon and ribavirin for chronic hepatitis C. N Engl J Med 355, 2444-2451 (2006). (Pubitemid 44903748)
2. De Francesco, R. & Migliaccio, G. Challenges and successes in developing new therapies for hepatitis C. Nature 436, 953-960 (2005). (Pubitemid 41191671)
3. Gao, M. et al Chemical genetics strategy identifies an HCV NS5A inhibitor with a potent clinical effect. Nature 465, 96-100 (2010).
4. Elbashir, S. M., 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). (Pubitemid 32494397)
5. Hannon, G. J. RNA interference. Nature 418, 244-251 (2002). (Pubitemid 34773784)
6. Reynolds, A., Leake, D., Boese, Q., Scaringe, S., Marshall, W. S. & Khvorova, A. Rational siRNA design for RNA interference. Nat Biotechnol 22, 326-330 (2004). (Pubitemid 38295766)
7. Ui-Tei, K. et al. Guidelines for the selection of highly effective siRNA sequences for mammalian and chick RNA interference. Nucleic acids research 32, 936-948 (2004). (Pubitemid 38854696)
8. Patzel, V., Rutz, S., Dietrich, I., Koberle, C., Scheffold, A. & Kaufmann, S. H. Design of siRNAs producing unstructured guide-RNAs results in improved RNA interference efficiency. Nat Biotechnol 23, 1440-1444 (2005). (Pubitemid 41679398)
9. Ameres, S. L., Martinez, J. & Schroeder, R. Molecular basis for target RNA recognition and cleavage by human RISC. Cell 130, 101-112 (2007). (Pubitemid 47031315)
10. Tafer, H. et al. The impact of target site accessibility on the design of effective siRNAs. Nat Biotechnol 26, 578-583 (2008). (Pubitemid 351668044)
11. Das, A. T. et al. Human immunodeficiency virus type 1 escapes from RNA interference-mediated inhibition. J Virol 78, 2601-2605 (2004). (Pubitemid 38228957)
12. Konishi, M. et al. siRNA-resistance in treatedHCVreplicon cells is correlated with the development of specific HCV mutations. J Viral Hepat 13, 756-761 (2006). (Pubitemid 44583501)
13. Wilson, J. A., Richardson, C. D. & Hepatitis, C. virus replicons escape RNA interference induced by a short interfering RNA directed against the NS5b coding region. J Virol 79, 7050-7058 (2005). (Pubitemid 40677336)
14. Naito, Y., Ui-Tei, K., Nishikawa, T., Takebe, Y. & Saigo, K. siVirus: web-based antiviral siRNA design software for highly divergent viral sequences. Nucleic acids research 34, W448-450 (2006). (Pubitemid 44529810)
15. Westerhout, E. M., Ooms, M., Vink, M., Das, A. T. & Berkhout, B. HIV-1 can escape from RNA interference by evolving an alternative structure in its RNA genome. Nucleic acids research 33, 796-804 (2005). (Pubitemid 40361009)
16. Brown, K. M., Chu, C. Y. & Rana, T. M. Target accessibility dictates the potency of human RISC. Nat Struct Mol Biol 12, 469-470 (2005). (Pubitemid 43085910)
17. Overhoff, M. et al. Local RNA target structure influences siRNA efficacy: a systematic global analysis. J Mol Biol 348, 871-881 (2005). (Pubitemid 40544388)
18. Gredell, J. A., Berger, A. K. & Walton, S. P. Impact of target mRNA structure on siRNA silencing efficiency: A large-scale study. Biotechnol Bioeng 100, 744-755 (2008). (Pubitemid 351914001)
19. de Fougerolles, A., Vornlocher, H. P., Maraganore, J. & Lieberman, J. Interfering with disease: a progress report on siRNA-based therapeutics. Nat Rev Drug Discov 6, 443-453 (2007). (Pubitemid 47064567)
20. Kogure, K., Akita, H., Yamada, Y.&Harashima, H. Multifunctional envelope-type nano device (MEND) as a non-viral gene delivery system. Adv Drug Deliv Rev 60, 559-571 (2008). (Pubitemid 351215573)
21. Sato, Y., Hatakeyama, H., Sakurai, Y., Hyodo, M., Akita, H. & Harashima, H. A pH-sensitive cationic lipid facilitates the delivery of liposomal siRNA and gene silencing activity in vitro and in vivo. Journal of controlled release: official journal of the Controlled Release Society 163, 267-276 (2012).
22. Connor, J., Yatvin, M. B. & Huang, L. pH-sensitive liposomes: acid-induced liposome fusion. Proc Natl Acad Sci U S A 81, 1715-1718 (1984). (Pubitemid 14101212)
23. Straubinger, R. M., Duzgunes, N. & Papahadjopoulos, D. pH-sensitive liposomes mediate cytoplasmic delivery of encapsulated macromolecules. FEBS Lett 179, 148-154 (1985). (Pubitemid 15153269)
24. Semple, S. C. et al. Rational design of cationic lipids for siRNA delivery. Nat Biotechnol 28, 172-176 (2010).
25. Tsukiyama-Kohara, K., Iizuka, N., Kohara, M. & Nomoto, A. Internal ribosome entry site within hepatitis C virus RNA. J Virol 66, 1476-1483 (1992).
26. Watanabe, T. et al. Intracellular-diced dsRNA has enhanced efficacy for silencing HCV RNA and overcomes variation in the viral genotype. Gene Ther 13, 883-892 (2006).
27. Kim, D. H., Behlke, M. A., Rose, S. D., Chang, M. S., Choi, S. & Rossi, J. J. Synthetic dsRNA Dicer substrates enhance RNAi potency and efficacy. Nat Biotechnol 23, 222-226 (2005). (Pubitemid 40255333)
28. Siolas, D. et al. Synthetic shRNAs as potent RNAi triggers. Nat Biotechnol 23, 227-231 (2005). (Pubitemid 40255334)
29. Jinek, M.&Doudna, J. A. Athree-dimensional view of the molecular machinery of RNA interference. Nature 457, 405-412 (2009).
30. Arai, M. et al. Establishment of infectious HCV virion-producing cells with newly designed full-genome replicon RNA. Arch Virol 156, 295-304 (2011).
31. Pei, Y. & Tuschl, T. On the art of identifying effective and specific siRNAs. Nat Methods 3, 670-676 (2006). (Pubitemid 44275732)
32. Naito, Y., Yoshimura, J., Morishita, S. & Ui-Tei, K. siDirect 2.0: updated software for designing functional siRNA with reduced seed-dependent off-target effect. BMC Bioinformatics 10, 392 (2009).
33. Akinc, A. et al. A combinatorial library of lipid-like materials for delivery of RNAi therapeutics. Nat Biotechnol 26, 561-569 (2008). (Pubitemid 351668042)
34. Mercer, D. F. et al. Hepatitis C virus replication in mice with chimeric human livers. Nat Med 7, 927-933 (2001). (Pubitemid 32756430)
35. Inoue, K. et al. Evaluation of a cyclophilin inhibitor in hepatitis C virus-infected chimeric mice in vivo. Hepatology 45, 921-928 (2007). (Pubitemid 46631561)
36. Tsukiyama-Kohara, K. et al. Activation of the CKI-CDK-Rb-E2F pathway in full genome hepatitis C virus-expressing cells. J Biol Chem 279, 14531-14541 (2004). (Pubitemid 38618840)
37. Sekiguchi, S. et al. Immunization with a recombinant vaccinia virus that encodes nonstructural proteins of the hepatitis C virus suppresses viral protein levels in mouse liver. PLoS One 7, e51656 (2012).
38. Hutvagner, G. & Simard, M. J. Argonaute proteins: key players in RNA silencing. Nat Rev Mol Cell Biol 9, 22-32 (2008).
39. MacRae, I. J., Ma, E., Zhou, M., Robinson, C. V. & Doudna, J. A. In vitro reconstitution of the human RISC-loading complex. Proc Natl Acad SciU S A 105, 512-517 (2008). (Pubitemid 351171739)
40. Yan, X. et al. The role of apolipoprotein E in the elimination of liposomes from blood by hepatocytes in the mouse. Biochem Biophys Res Commun 328, 57-62 (2005). (Pubitemid 40164635)
41. Akinc, A. et al. Targeted delivery of RNAi therapeutics with endogenous and exogenous ligand-based mechanisms. Mol Ther 18, 1357-1364 (2010).
42. Jacobs, F., Wisse, E. & De Geest, B. The role of liver sinusoidal cells in hepatocytedirected gene transfer. Am J Pathol 176, 14-21 (2010).
43. Sakurai, Yea. Gene Silencing via RNAi and siRNA quantification in Tumor Tissue using MEND, a Liposomal siRNA Delivery System. Mol Ther in press, (2013).
44. Jayaraman, M. et al. Maximizing the potency of siRNA lipid nanoparticles for hepatic gene silencing in vivo. Angew Chem Int Ed Engl 51, 8529-8533 (2012).
45. Takahashi, M. et al. In vitro optimization of 2′-OMe-4′- thioribonucleoside-modified anti-microRNA oligonucleotides and its targeting delivery to mouse liver using a liposomal nanoparticle. Nucleic acids research 41, 10659-10667 (2013).
46. Hatakeyama, H. et al. The systemic administration of an anti-miRNA oligonucleotide encapsulated pH-sensitive liposome results in reduced level of hepatic microRNA-122 in mice. Journal of controlled release: official journal of the Controlled Release Society 173, 43-50 (2014).
47. Sakamoto, H. et al. Host sphingolipid biosynthesis as a target for hepatitis C virus therapy. Nat Chem Biol 1, 333-337 (2005).
48. Wakita, T. et al. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat Med 11, 791-796 (2005). (Pubitemid 41021213)
49. Yasui, F., Sudoh, M., Arai, M. & Kohara, M. Synthetic lipophilic antioxidant BO-653 suppresses HCV replication. J Med Virol 85, 241-249 (2013).
50. Honda, M., Beard, M. R., Ping, L. H. & Lemon, S. M. 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 (1999). (Pubitemid 29036768)