In vivo screening of modified siRNAs for non-specific antiviral effect in a small fish model: Number and localization in the strands are important

Nucleic Acids Research

Volumn 40, Issue 10, 2012, Pages 4653-4665

  Schyth, Brian Dall ^a   Bramsen, Jesper Bertram ^b   Pakula, Malgorzata Maria ^b   Larashati, Sekar ^a   Kjems, Jørgen ^b   Wengel, Jesper ^c   Lorenzen, Niels ^a  

^a TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^b AARHUS UNIVERSITY   (Denmark)

^c UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ALTRITOL NUCLEIC ACID; HEXITOL NUCLEIC ACID; INTERFERON; LOCKED NUCLEIC ACID; NUCLEIC ACID; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANTIVIRAL ACTIVITY; ARTICLE; CELL COUNT; CELL POPULATION; CONTROLLED STUDY; DNA MODIFICATION; FISH; GENE LOCATION; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; IMMUNOGENICITY; IN VITRO STUDY; IN VIVO STUDY; INNATE IMMUNITY; MORTALITY; NONHUMAN; NORMAL HUMAN; NUCLEOTIDE MOTIF; PRIORITY JOURNAL; RISK REDUCTION; RNA BINDING; RNA SEQUENCE; SINGLE STRAND CONFORMATION POLYMORPHISM; THERMOSTABILITY;

ANIMALS; ANTIVIRAL AGENTS; DRUG EVALUATION, PRECLINICAL; HUMANS; MODELS, ANIMAL; NUCLEOTIDE MOTIFS; OLIGONUCLEOTIDES; ONCORHYNCHUS MYKISS; RNA INTERFERENCE; RNA, SMALL INTERFERING; TEMPERATURE;

ANIMALIA;

EID: 84861539981     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks033     Document Type: Article

References (61)

1. Fire, A., Xu, S., Montgomery, M.K., Kostas, S.A., Driver, S.E. and Mello, C.C. (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature, 391, 806-811.
2. Elbashir, S.M., Harborth, J., Lendeckel, W., Yalcin, A., Weber, K. and Tuschl, T. (2001) Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature, 411, 494-498.
3. Elbashir, S.M., Martinez, J., Patkaniowska, A., Lendeckel, W. and Tuschl, T. (2001) Functional anatomy of siRNAs for mediating efficient RNAi in Drosophila melanogaster embryo lysate. EMBO J., 20, 6877-6888.
4. Bernstein, E., Caudy, A.A., Hammond, S.M. and Hannon, G.J. (2001) Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature, 409, 363-366.
5. Gregory, R.I., Chendrimada, T.P., Cooch, N. and Shiekhattar, R. (2005) Human RISC couples microRNA Biogenesis and posttranscriptional gene silencing. Cell, 123, 631-640.
6. Hammond, S.M., Bernstein, E., Beach, D. and Hannon, G.J. (2000) An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells. Nature, 404, 293-296.
7. Meister, G., Landthaler, M., Patkaniowska, A., Dorsett, Y., Teng, G. and Tuschl, T. (2004) Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. Mol. Cell, 15, 185-197.
8. Matranga, C., Tomari, Y., Shin, C., Bartel, D.P. and Zamore, P.D. (2005) Passenger-strand cleavage facilitates assembly of siRNA into Ago2-containing RNAi enzyme complexes. Cell, 123, 607-620.
9. Rand, T.A., Petersen, S., Du, F. and Wang, X. (2005) Argonaute2 cleaves the anti-guide strand of siRNA during RISC activation. Cell, 123, 621-629.
10. Leuschner, P.J., Ameres, S.L., Kueng, S. and Martinez, J. (2006) Cleavage of the siRNA passenger strand during RISC assembly in human cells. EMBO Rep., 7, 314-320.
11. Caplen, N.J., Parrish, S., Imani, F., Fire, A. and Morgan, R.A. (2001) Specific inhibition of gene expression by small double-stranded RNAs in invertebrate and vertebrate systems. Proc. Natl Acad. Sci. USA, 98, 9742-9747.
12. Haasnoot, J. and Berkhout, B. (2006) RNA interference: its use as antiviral therapy. Handb. Exp. Pharmacol., 117-150.
13. Roberts, W.K., Clemens, M.J. and Kerr, I.M. (1976) Interferon-induced inhibition of protein synthesis in L-cell extracts: an ATP-dependent step in the activation of an inhibitor by double-stranded RNA. Proc. Natl Acad. Sci. USA, 73, 3136-3140.
14. Farrell, P.J., Sen, G.C., Dubois, M.F., Ratner, L., Slattery, E. and Lengyel, P. (1978) Interferon action: two distinct pathways for inhibition of protein synthesis by double-stranded RNA. Proc. Natl Acad. Sci. USA, 75, 5893-5897.
15. McCartney, S., Vermi, W., Gilfillan, S., Cella, M., Murphy, T.L., Schreiber, R.D., Murphy, K.M. and Colonna, M. (2009) Distinct and complementary functions of MDA5 and TLR3 in poly(I:C)-mediated activation of mouse NK cells. J. Exp. Med., 206, 2967-2976.
16. Kariko, K., Bhuyan, P., Capodici, J., Ni, H., Lubinski, J., Friedman, H. and Weissman, D. (2004) Exogenous siRNA mediates sequence-independent gene suppression by signaling through Toll-like receptor 3. Cells Tissues. Organs, 177, 132-138.
17. Kleinman, M.E., Yamada, K., Takeda, A., Chandrasekaran, V., Nozaki, M., Baffi, J.Z., Albuquerque, R.J.C., Yamasaki, S., Itaya, M., Pan, Y. et al. (2008) Sequence-and target-independent angiogenesis suppression by siRNA via TLR3. Nature, 452, 591-597.
18. Hornung, V., Guenthner-Biller, M., Bourquin, C., Ablasser, A., Schlee, M., Uematsu, S., Noronha, A., Manoharan, M., Akira, S., de Fougerolles, A. et al. (2005) Sequence-specific potent induction of IFN-alpha by short interfering RNA in plasmacytoid dendritic cells through TLR7. Nat. Med., 11, 263-270.
19. Sioud, M. (2006) Innate sensing of self and non-self RNAs by Toll-like receptors. Trends Mol. Med., 12, 167-176.
20. Judge, A.D., Sood, V., Shaw, J.R., Fang, D., McClintock, K. and Maclachlan, I. (2005) Sequence-dependent stimulation of the mammalian innate immune response by synthetic siRNA. Nat. Biotechnol., 23, 457-462.
21. Sioud, M. (2005) Induction of inflammatory cytokines and interferon responses by double-stranded and single-stranded siRNAs is sequence-dependent and requires endosomal localization. J. Mol. Biol., 348, 1079-1090.
22. Marques, J.T. and Williams, B.R. (2005) Activation of the mammalian immune system by siRNAs. Nat. Biotechnol., 23, 1399-1405.
23. Robbins, M., Judge, A., Ambegia, E., Choi, C., Yaworski, E., Palmer, L., McClintock, K. and Maclachlan, I. (2008) Misinterpreting the therapeutic effects of small interfering RNA caused by immune stimulation. Hum. Gene Ther., 19, 991-999.
24. Robbins, M., Judge, A. and Maclachlan, I. (2009) siRNA and innate immunity. Oligonucleotides, 19, 89-102.
25. Schlee, M., Hornung, V. and Hartmann, G. (2006) siRNA and isRNA: two edges of one sword. Mol. Ther., 14, 463-470.
26. Schyth, B.D., Lorenzen, N. and Pedersen, F.S. (2006) Antiviral activity of small interfering RNAs: Specificity testing using heterologous virus reveals interferon-related effects overlooked by conventional mismatch controls. Virology, 349, 134-141.
27. Schyth, B.D., Lorenzen, N. and Pedersen, F.S. (2007) A high throughput in vivo model for testing delivery and antiviral effects of siRNAs in vertebrates. Mol. Ther., 15, 1366-1372.
28. Cho, W.G., Albuquerque, R.J.C., Kleinman, M.E., Tarallo, V., Greco, A., Nozaki, M., Green, M.G., Baffi, J.Z., Ambati, B.K., De Falco, M. et al. (2009) Small interfering RNA-induced TLR3 activation inhibits blood and lymphatic vessel growth. PNAS, 106, 7137-7142.
29. Morrissey, D.V., Lockridge, J.A., Shaw, L., Blanchard, K., Jensen, K., Breen, W., Hartsough, K., Machemer, L., Radka, S., Jadhav, V. et al. (2005) Potent and persistent in vivo anti-HBV activity of chemically modified siRNAs. Nat. Biotechnol., 23, 1002-1007.
30. Czauderna, F., Fechtner, M., Dames, S., Aygun, H., Klippel, A., Pronk, G.J., Giese, K. and Kaufmann, J. (2003) Structural variations and stabilising modifications of synthetic siRNAs in mammalian cells. Nucleic Acids Res., 31, 2705-2716.
31. Cekaite, L., Furset, G., Hovig, E. and Sioud, M. (2007) Gene expression analysis in blood cells in response to unmodified and 20-modified siRNAs reveals TLR-dependent and independent effects. J. Mol. Biol., 365, 90-108.
32. Robbins, M., Judge, A., Liang, L., McClintock, K., Yaworski, E. and Maclachlan, I. (2007) 20-O-methyl-modified RNAs act as TLR7 antagonists. Mol. Ther., 15, 1663-1669.
33. Sioud, M. (2006) Single-stranded small interfering RNA are more immunostimulatory than their double-stranded counterparts: a central role for 20-hydroxyl uridines in immune responses. Eur. J. Immunol., 36, 1222-1230.
34. Soutschek, J., Akinc, A., Bramlage, B., Charisse, K., Constien, R., Donoghue, M., Elbashir, S., Geick, A., Hadwiger, P., Harborth, J. et al. (2004) Therapeutic silencing of an endogenous gene by systemic administration of modified siRNAs. Nature, 432, 173-178.
35. Hamm, S., Latz, E., Hangel, D., Muller, T., Yu, P., Golenbock, D., Sparwasser, T., Wagner, H. and Bauer, S. (2010) Alternating 20-O-ribose methylation is a universal approach for generating non-stimulatory siRNA by acting as TLR7 antagonists. Immunobiology, 215, 559-569.
36. Behlke, M.A. (2008) Chemical modification of siRNAs for in vivo use. Oligonucleotides, 18, 305-319.
37. Judge, A.D., Bola, G., Lee, A.C. and Maclachlan, I. (2006) Design of noninflammatory synthetic siRNA mediating potent gene silencing in vivo. Mol. Ther., 13, 494-505.
38. Bramsen, J.B., Laursen, M.B., Nielsen, A.F., Hansen, T.B., Bus, C., Langkjaer, N., Babu, B.R., Hland, T., Abramov, M., Van Aerschot, A. et al. (2009) A large-scale chemical modification screen identifies design rules to generate siRNAs with high activity, high stability and low toxicity. Nucleic Acids Res., 37, 2867-2881.
39. Bramsen, J.B., Laursen, M.B., Damgaard, C.K., Lena, S.W., Babu, B.R., Wengel, J. and Kjems, J. (2007) Improved silencing properties using small internally segmented interfering RNAs. Nucleic Acids Res., 35, 5886-5897.
40. Elmen, J., Thonberg, H., Ljungberg, K., Frieden, M., Westergaard, M., Xu, Y., Wahren, B., Liang, Z., Aum, H. and Koch, T. (2005) Locked nucleic acid (LNA) mediated improvements in siRNA stability and functionality. Nucleic Acids Res., 33, 439-447.
41. Laursen, M.B., Pakula, M.M., Gao, S., Fluiter, K., Mook, O.R., Baas, F., Langklaer, N., Wengel, S.L., Wengel, J., Kjems, J. et al. (2010) Utilization of unlocked nucleic acid (UNA) to enhance siRNA performance in vitro and in vivo. Mol. Biosyst., 6, 862-70.
42. Fisher, M., Abramov, M., Van Aerschot, A., Xu, D., Juliano, R.L. and Herdewijn, P. (2007) Inhibition of MDR1 expression with altritol-modified siRNAs. Nucleic Acids Res., 35, 1064-1074.
43. Fisher, M., Abramov, M., Van Aerschot, A., Rozenski, J., Dixit, V., Juliano, R.L. and Herdewijn, P. (2009) Biological effects of hexitol and altritol-modified siRNAs targeting B-Raf. Eur J Pharmacol., 606, 38-44.
44. Bobkov, G.V., Mikhailov, S.N., Van Aerschot, A. and Herdewijn, P. (2008) Phosphoramidite building blocks for efficient incorporation of 20-O-aminoethoxy(and propoxy)methyl nucleosides into oligonucleotides. Tetrahedron, 64, 6238-6251.
45. Lorenzen, N., Olesen, N.J., Vesterga rd Jgensen, P.E., Etzerodt, M., Holtet, T.L. and THersen, H.C. (1993) Molecular cloning and expression in Escherichia coli of the glycoprotein gene of VHS virus, and immunization of rainbow trout with the recombinant protein. J. Gen. Virol., 74, 623-630.
46. Skall, H.F., Heuer, O.E., Lorenzen, N., Otte, L. and Olesen, N.J. (1999) Isolation of viral haemorrhagic septicaemia virus (VHSV) from wild marine fish species in the Baltic Sea, Kattegat, Skagerrak and the North Sea. Virus Res., 63, 95-106.
47. Harve, K.S., Lareu, R., Rajagopalan, R. and Raghunath, M. (2010) Understanding how the crowded interior of cells stabilizes DNA/DNA and DNA/RNA hybrids-in silico predictions and in vitro evidence. Nucleic Acids Res., 38, 172-181.
48. Bramsen, J.B., Pakula, M.M., Hansen, T.B., Bus, C., LangkJ, N., Odadzic, D., Smicius, R., Wengel, S.L., Chattopadhyaya, J., Engels, J.W. et al. (2010) A screen of chemical modifications identifies position-specific modification by UNA to most potently reduce siRNA off-target effects. Nucleic Acid Res., 38, 5761-5773.
49. Jepsen, J.S. and Wengel, J. (2004) LNA-antisense rivals siRNA for gene silencing. Curr. Opin. Drug Discov. Devel., 7, 188-194.
50. Sioud, M. and Sensen, D. (2003) Cationic liposome-mediated delivery of siRNAs in adult mice. Biochem. Biophys. Res. Commun., 312, 1220-1225.
51. Barton, G.M. and Kagan, J.C. (2009) A cell biological view of Toll-like receptor function: regulation through compartmentalization. Nat. Rev. Immunol., 9, 535-542.
52. Phelan, P.E., Mellon, M.T. and Kim, C.H. (2005) Functional characterization of full-length TLR3, IRAK-4, and TRAF6 in zebrafish (Danio rerio). Mol. Immunol., 42, 1057-1071.
53. Palti, Y., Gahr, S.A., Purcell, M.K., Hadidi, S., Rexroad, C.E. III and Wiens, G.D. (2010) Identification, characterization and genetic mapping of TLR7, TLR8a1 and TLR8a2 genes in rainbow trout (Oncorhynchus mykiss). Dev. Comp Immunol., 34, 219-233.
54. Rodriguez, M.F., Wiens, G.D., Purcell, M.K. and Palti, Y. (2005) Characterization of Toll-like receptor 3 gene in rainbow trout (Oncorhynchus mykiss). Immunogenetics, 57, 510-519.
55. Reynolds, A., Anderson, E.M., Vermeulen, A., Fedorov, Y., Robinson, K., Leake, D., Karpilow, J., Marshall, W.S. and Khvorova, A. (2006) Induction of the interferon response by siRNA is cell type-and duplex length-dependent. RNA, 12, 988-993.
56. Goodchild, A., Nopper, N., King, A., Doan, T., Tanudji, M., Arndt, G.M., Poidinger, M., Rivory, L.P. and Passioura, T. (2009) Sequence determinants of innate immune activation by short interfering RNAs. BMC. Immunol., 10, 40.
57. Magnadottir, B. (2006) Innate immunity of fish (overview). Fish Shellfish Immunol., 20, 137-151.
58. Collet, B. and Secombes, C.J. (2002) Type I-interferon signalling in fish. Fish. Shellfish. Immunol., 12, 389-397.
59. Oshiumi, H., Tsujita, T., Shida, K., Matsumoto, M., Ikeo, K. and Seya, T. (2003) Prediction of the prototype of the human Toll-like receptor gene family from the pufferfish, Fugu rubripes, genome. Immunogenetics, 54, 791-800.
60. Purcell, M.K., Smith, K.D., Hood, L., Winton, J.R. and Roach, J.C. (2006) Conservation of Toll-like receptor signaling pathways in teleost fish. Comp. Biochem. Physiol. Part D. Genomics Proteomics., 1, 77-88.
61. Robertsen, B. (2006) The interferon system of teleost fish. Fish Shellfish Immunol., 20, 172-191.