Sequence-dependent off-target inhibition of TLR7/8 sensing by synthetic microRNA inhibitors

Nucleic Acids Research

Volumn 43, Issue 2, 2015, Pages 1177-1188

  Sarvestani, Soroush T ^a,b   Stunden, H James ^c   Behlke, Mark A ^d   Forster, Samuel C ^e   McCoy, Claire E ^a,b   Tate, Michelle D ^a,b   Ferrand, Jonathan ^a,b   Lennox, Kim A ^d   Latz, Eicke ^c,f,g   Williams, Bryan R G ^a,b   Gantier, Michael P ^a,b  

^a HUDSON INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c UNIVERSITY HOSPITAL BONN   (Germany)

^d INTEGRATED DNA TECHNOLOGIES   (United States)

^e WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^f UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^g GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOLOGICAL ADJUVANT; MICRORNA; OLIGONUCLEOTIDE; RNA; TLR7 PROTEIN, HUMAN; TLR8 PROTEIN, HUMAN; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8;

ANIMAL; ANTAGONISTS AND INHIBITORS; CHEMISTRY; HEK293 CELL LINE; HUMAN; MOUSE; NUCLEOTIDE MOTIF; NUCLEOTIDE SEQUENCE;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; BASE SEQUENCE; HEK293 CELLS; HUMANS; MICE; MICRORNAS; NUCLEOTIDE MOTIFS; OLIGONUCLEOTIDES; RNA; TOLL-LIKE RECEPTOR 7; TOLL-LIKE RECEPTOR 8;

EID: 84942980435     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku1343     Document Type: Article

References (47)

1. Helwak, A., Kudla, G., Dudnakova, T., Tollervey, D. (2013) Mapping the human miRNA interactome by CLASH reveals frequent noncanonical binding. Cell, 153, 654-665.
2. Selbach, M., Schwanhausser, B., Thierfelder, N., Fang, Z., Khanin, R., Rajewsky, N. (2008) Widespread changes in protein synthesis induced by microRNAs. Nature, 455, 58-63.
3. Eulalio, A., Huntzinger, E., Izaurralde, E. (2008) Getting to the root of miRNA-mediated gene silencing. Cell, 132, 9-14.
4. Lennox, K.A., Behlke, M.A. (2011) Chemical modification and design of anti-miRNA oligonucleotides. Gene Ther., 18, 1111-1120.
5. Hutvagner, G., Simard, M.J., Mello, C.C., Zamore, P.D. (2004) Sequence-specific inhibition of small RNA function. PLoS Biol., 2, E98.
6. Meister, G., Landthaler, M., Dorsett, Y., Tuschl, T. (2004) Sequence-specific inhibition of microRNA-and siRNA-induced RNA silencing. RNA, 10, 544-550.
7. Lennox, K.A., Owczarzy, R., Thomas, D.M., Walder, J.A., Behlke, M.A. (2013) Improved performance of anti-miRNA oligonucleotides using a novel non-nucleotide modifier. Mol. Ther. Nucleic Acids, 2, e117.
8. Friderici, K., Kaehler, M., Rottman, F. (1976) Kinetics of Novikoff cytoplasmic messenger RNA methylation. Biochemistry, 15, 5234-5241.
9. Kariko, K., Buckstein, M., Ni, H., Weissman, D. (2005) Suppression of RNA recognition by Toll-like receptors: the impact of nucleoside modification and the evolutionary origin of RNA. Immunity, 23, 165-175.
10. Robbins, M., Judge, A., Liang, L., McClintock, K., Yaworski, E., MacLachlan, I. (2007) 2-O-methyl-modified RNAs act as TLR7 antagonists. Mol. Ther., 15, 1663-1669.
11. Sioud, M., Furset, G., Cekaite, L. (2007) Suppression of immunostimulatory siRNA-driven innate immune activation by 2-modified RNAs. Biochem. Biophys. Res. Commun., 361, 122-126.
12. Zamanian-Daryoush, M., Marques, J.T., Gantier, M.P., Behlke, M.A., John, M., Rayman, P., Finke, J., Williams, B.R. (2008) Determinants of cytokine induction by small interfering RNA in human peripheral blood mononuclear cells. J. Interferon Cytokine Res., 28, 221-233.
13. Hamm, S., Latz, E., Hangel, D., Muller, T., Yu, P., Golenbock, D., Sparwasser, T., Wagner, H., Bauer, S. (2010) Alternating 2-O-ribose methylation is a universal approach for generating non-stimulatory siRNA by acting as TLR7 antagonist. Immunobiology, 215, 559-569.
14. Sarvestani, S.T., Williams, B.R., Gantier, M.P. (2012) Human Toll-like receptor 8 can be cool too: implications for foreign RNA sensing. J. Interferon Cytokine Res., 32, 350-361.
15. Kane, M., Case, L.K., Wang, C., Yurkovetskiy, L., Dikiy, S., Golovkina, T.V. (2011) Innate immune sensing of retroviral infection via Toll-like receptor 7 occurs upon viral entry. Immunity, 35, 135-145.
16. Wang, J.P., Bowen, G.N., Padden, C., Cerny, A., Finberg, R.W., Newburger, P.E., Kurt-Jones, E.A. (2008) Toll-like receptor-mediated activation of neutrophils by influenza A virus. Blood, 112, 2028-2034.
17. Jockel, S., Nees, G., Sommer, R., Zhao, Y., Cherkasov, D., Hori, H., Ehm, G., Schnare, M., Nain, M., Kaufmann, A. et al. (2012) The 2-O-methylation status of a single guanosine controls transfer RNA-mediated Toll-like receptor 7 activation or inhibition. J. Exp. Med., 209, 235-241.
18. Gantier, M.P., Irving, A.T., Kaparakis-Liaskos, M., Xu, D., Evans, V.A., Cameron, P.U., Bourne, J.A., Ferrero, R.L., John, M., Behlke, M.A. et al. (2010) Genetic modulation of TLR8 response following bacterial phagocytosis. Hum. Mutat., 31, 1069-1079.
19. Heil, F., Hemmi, H., Hochrein, H., Ampenberger, F., Kirschning, C., Akira, S., Lipford, G., Wagner, H., Bauer, S. (2004) Species-specific recognition of single-stranded RNA via toll-like receptor 7 and 8. Science, 303, 1526-1529.
20. Gantier, M.P., Tong, S., Behlke, M.A., Irving, A.T., Lappas, M., Nilsson, U.W., Latz, E., McMillan, N.A., Williams, B.R. (2010) Rational design of immunostimulatory siRNAs. Mol. Ther., 18, 785-795.
21. Gantier, M.P., Tong, S., Behlke, M.A., Xu, D., Phipps, S., Foster, P.S., Williams, B.R. (2008) TLR7 is involved in sequence-specific sensing of single-stranded RNAs in human macrophages. J. Immunol., 180, 2117-2124.
22. Tluk, S., Jurk, M., Forsbach, A., Weeratna, R., Samulowitz, U., Krieg, A.M., Bauer, S., Vollmer, J. (2009) Sequences derived from self-RNA containing certain natural modifications act as suppressors of RNA-mediated inflammatory immune responses. Int. Immunol., 21, 607-619.
23. Ventura, A., Young, A.G., Winslow, M.M., Lintault, L., Meissner, A., Erkeland, S.J., Newman, J., Bronson, R.T., Crowley, D., Stone, J.R. et al. (2008) Targeted deletion reveals essential and overlapping functions of the miR-17 through 92 family of miRNA clusters. Cell, 132, 875-886.
24. Clausen, B.E., Burkhardt, C., Reith, W., Renkawitz, R., Forster, I. (1999) Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic. Res., 8, 265-277.
25. Gantier, M.P., Williams, B.R. (2010) Monitoring innate immune recruitment by siRNAs in mammalian cells. Methods Mol. Biol., 623, 21-33.
26. Gantier, M.P. (2013) Strategies for designing and validating immunostimulatory siRNAs. Methods Mol. Biol., 942, 179-191.
27. Gantier, M.P., Stunden, H.J., McCoy, C.E., Behlke, M.A., Wang, D., Kaparakis-Liaskos, M., Sarvestani, S.T., Yang, Y.H., Xu, D., Corr, S.C. et al. (2012) A miR-19 regulon that controls NF-kappaB signaling. Nucleic Acids Res., 40, 8048-8058.
28. Gorden, K.B., Gorski, K.S., Gibson, S.J., Kedl, R.M., Kieper, W.C., Qiu, X., Tomai, M.A., Alkan, S.S., Vasilakos, J.P. (2005) Synthetic TLR agonists reveal functional differences between human TLR7 and TLR8. J. Immunol., 174, 1259-1268.
29. Barrat, F.J., Meeker, T., Gregorio, J., Chan, J.H., Uematsu, S., Akira, S., Chang, B., Duramad, O., Coffman, R.L. (2005) Nucleic acids of mammalian origin can act as endogenous ligands for Toll-like receptors and may promote systemic lupus erythematosus. J. Exp. Med., 202, 1131-1139.
30. Gorden, K.K., Qiu, X., Battiste, J.J., Wightman, P.P., Vasilakos, J.P., Alkan, S.S. (2006) Oligodeoxynucleotides differentially modulate activation of TLR7 and TLR8 by imidazoquinolines. J. Immunol., 177, 8164-8170.
31. Zuker, M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res., 31, 3406-3415.
32. Gantier, M.P. (2013) The not-so-neutral role of microRNAs in neutrophil biology. J. Leukoc. Biol., 94, 575-583.
33. Haussecker, D. (2012) The business of RNAi therapeutics in 2012. Mol. Ther. Nucleic Acids, 1, e8.
34. Janssen, H.L., Reesink, H.W., Lawitz, E.J., Zeuzem, S., Rodriguez-Torres, M., Patel, K., van der Meer, A.J., Patick, A.K., Chen, A., Zhou, Y. et al. (2013) Treatment of HCV infection by targeting microRNA. N. Engl. J. Med., 368, 1685-1694.
35. Hagedorn, P.H., Yakimov, V., Ottosen, S., Kammler, S., Nielsen, N.F., Hog, A.M., Hedtjarn, M., Meldgaard, M., Moller, M.R., Orum, H. et al. (2013) Hepatotoxic potential of therapeutic oligonucleotides can be predicted from their sequence and modification pattern. Nucleic Acid Ther., 23, 302-310.
36. Vermeulen, A., Robertson, B., Dalby, A.B., Marshall, W.S., Karpilow, J., Leake, D., Khvorova, A., Baskerville, S. (2007) Double-stranded regions are essential design components of potent inhibitors of RISC function. RNA, 13, 723-730.
37. Lennox, K.A., Behlke, M.A. (2010) A direct comparison of anti-microRNA oligonucleotide potency. Pharm. Res., 27, 1788-1799.
38. Judge, A.D., Bola, G., Lee, A.C., MacLachlan, I. (2006) Design of noninflammatory synthetic siRNA mediating potent gene silencing in vivo. Mol. Ther., 13, 494-505.
39. 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.
40. Bailey, T.L., Elkan, C. (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc. Int. Conf. Intell. Syst. Mol. Biol., 2, 28-36.
41. Grant, C.E., Bailey, T.L., Noble, W.S. (2011) FIMO: scanning for occurrences of a given motif. Bioinformatics, 27, 1017-1018.
42. Alexiou, P., Maragkakis, M., Papadopoulos, G.L., Simmosis, V.A., Zhang, L., Hatzigeorgiou, A.G. (2010) The DIANA-mirExTra web server: from gene expression data to microRNA function. PLoS One, 5, e9171.
43. 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.
44. Sarvestani, S.T., Tate, M.D., Moffat, J.M., Jacobi, A.M., Behlke, M.A., Miller, A.R., Beckham, S.A., McCoy, C.E., Chen, W., Mintern, J.D. et al. (2014) Inosine-mediated modulation of RNA sensing by Toll-like receptor 7 (TLR7) and TLR8. J. Virol., 88, 799-810.
45. Wang, J.P., Liu, P., Latz, E., Golenbock, D.T., Finberg, R.W., Libraty, D.H. (2006) Flavivirus activation of plasmacytoid dendritic cells delineates key elements of TLR7 signaling beyond endosomal recognition. J. Immunol., 177, 7114-7121.
46. Zust, R., Cervantes-Barragan, L., Habjan, M., Maier, R., Neuman, B.W., Ziebuhr, J., Szretter, K.J., Baker, S.C., Barchet, W., Diamond, M.S. et al. (2011) Ribose 2-O-methylation provides a molecular signature for the distinction of self and non-self mRNA dependent on the RNA sensor Mda5. Nat. Immunol., 12, 137-143.
47. Daffis, S., Szretter, K.J., Schriewer, J., Li, J., Youn, S., Errett, J., Lin, T.Y., Schneller, S., Zust, R., Dong, H. et al. (2010) 2-O methylation of the viral mRNA cap evades host restriction by IFIT family members. Nature, 468, 452-456.