Overcoming the challenges of siRNA Activation of innate immunity: Design better therapeutic siRNAs

RNA Interference: Challenges and Therapeutic Opportunities

Volumn , Issue , 2014, Pages 301-319

  Sioud, Mouldy ^a  

^a OSLO UNIVERSITY HOSPITAL   (Norway)

Author keywords

2' Ribose modifications; Cancer vaccines; Dendritic cells; Innate immunity; Off target effects; RNAi; siRNA; Toll like receptors

Indexed keywords

EID: 84921769572     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-1-4939-1538-5_19     Document Type: Chapter

References (69)

1. Jorgensen R (1990) Altered gene expression in plants due to trans interactions between homologous genes. Trends Biotechnol 8:340-344.
2. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806-811.
3. Svoboda P, Stein P, Hayashi H, Schultz RM (2000) Selective reduction of dormant maternal mRNAs in mouse oocytes by RNA interference. Development 127:4147-4156.
4. Sen GC (2001) Viruses and interferons. Annu Rev Microbiol 55:255-281.
5. Zamore PD, Tuschl T, Sharp PA, Bartel DP (2000) RNAi: double-stranded RNA directs the ATP-dependent cleavage of mRNA at 21 to 23 nucleotide intervals. Cell 101:25-33.
6. Elbashir SM, Lendeckel W, Tuschl T (2001) RNA interference is mediated by 21- and 22-nucleotide RNAs. Genes Dev 15:188-200.
7. Elbashir SM, Harborth J, Lendeckel W, Yalcin A, Weber K, Tuschl T (2001) Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411:494-498.
8. Sioud M (2004) Therapeutic siRNAs. Trends Pharmacol Sci 25:22-28.
9. Hannon GJ, Rossi JJ (2004) Unlocking the potential of the human genome with RNA interference. Nature 431:371-378.
10. Liu J, Carmell MA, Rivas FV, Marsden CG, Thomson JM, Song JJ, Hammond SM, Joshua-Tor L, Hannon GJ (2004) Argonaute2 is the catalytic engine of mammalian RNAi. Science 305:1437-1441.
11. Song JJ, Smith SK, Hannon GJ, Joshua-Tor L (2004) Crystal structure of Argonaute and its implications for RISC slicer activity. Science 305:1434-1447.
12. Matranga C, Tomari Y, Shin C, Bartel DP, Zamore PD (2005) Passenger-strand cleavage facilitates assembly of siRNA into Ago2- containing RNAi enzyme complexes. Cell 123:607-620.
13. Rand TA, Petersen S, Du F et al (2005) Wang:Argonaute2 cleaves the anti-guide strand of siRNA during RISC activation. Cell 123:621-629.
14. Ma JB, Yuan YR, Meister G, Pei Y, Tuschl T, Partel DJ (2005) Structural basis for 5'-endspecific recognition of guide RNA by the A. fulgidus Piwi protein. Nature 434:666-670.
15. Sioud M, Sorensen DR (2003) Cationic liposome- mediated delivery of siRNAs in adult mice. Biochem Biophys Res Commun 312:122-125.
16. Jackson AL, Bartz SR, Schelter J, Kobayashi SV, Burchard J, Mao M, Li B, Cavet G, Linsley PS (2003) Expression profiling reveals offtarget gene regulation by RNAi. Nat Biotechnol 21:635-637.
17. Semizarov D, Frost L, Sarthy A, Kroeger P, Halbert DN, Fesik SW (2003) Specificity of short interfering RNA determined through gene expression signatures. Proc Natl Acad Sci U S A 100:6347-6352.
18. Sledz CA, Holko M, de Veer MJ, Silverman RH, Williams BR (2003) Activation of the interferon system by short-interfering RNAs. Nat Cell Biol 5:834-839.
19. Parkin J, Cohen B (2001) An overview of the immune system. Lancet 357:1777-1789.
20. Janeway CA, Medzhitov R Jr (2002) Innate immune recognition. Annu Rev Immunol 20:197-216.
21. Takeda K, Akira S (2005) Toll-like receptors in innate immunity. Int Immunol 17:1-14.
22. Sioud M (2006) Innate sensing of self and non-self RNAs by Toll-like receptors. Trends Mol Med 12:167-716.
23. Brennan CA, Anderson KV (2004) Drosophila:the genetics of innate immune recognition and response. Annu Rev Immunol 22:457-483.
24. Lemaitre B, Nicolas E, Michaut L, Reichhart JM, Hoffmann JA (1996) The dorsoventral regulatory gene cassette spatzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 86:973-983.
25. Akira S, Takeda K (2004) Toll-like receptor signaling. Nat Rev Immunol 4:499-511.
26. Li S, Peters GA, Ding K, Zhang X, Qin J, Sen GC (2006) Molecular basis for PKR activation by PACT or dsRNA. Proc Natl Acad Sci U S A 103:10005-10010.
27. Samuel CE (2001) Antiviral actions of interferons. Clin Microbiol Rev 14:778-809.
28. Kato H, Takeuchi O, Sato S, Yoneyama M, Yamamoto M, Matsui K, Uematsu S, Jung A, Kawai T, Ishii KJ, Yamaguchi O, Otsu K, Tsujimura T, Koh CS, Reis e Sousa C, Matsuura Y, Fujita T, Akira S (2006) Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441:101-105.
29. Kato H, Sato S, Yoneyama M, Yamamoto M, Uematsu S, Matsui K, Tsujimura T, Takeda K, Fujita T, Takeuchi O, Akira S (2005) Cell typespecific involvement of RIG-I in antiviral response. Immunity 23:19-28.
30. Meylan E, Tschopp J, Karin M (2006) Intracellular pattern recognition receptors in the host response. Nature 442:39-44.
31. Alexopoulou L, Holt AC, Medzhitov R, Flavell RA (2001) Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 413:732-738.
32. 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.
33. Krieg AM (2002) CpG motifs in bacterial DNA and their immune effects. Annu Rev Immunol 20:709-760.
34. Brentano F, Kyburz D, Schorr O, Gay R, Gay S (2005) The role of Toll-like receptor signaling in the pathogenesis of arthritis. Cell Immunol 233:90-96.
35. Cao W, Liu YJ (2007) Innate immune functions of plasmacytoid dendritic cells. Curr Opin Immunol 19:24-30.
36. Kariko K, Bhuyan P, Capodici J, Weissman D (2004) Small interfering RNAs mediate sequenceindependent gene suppression and induce immune activation by signaling through toll-like receptor 3. J Immunol 172:6545-6549.
37. Sioud M (2005) Induction of inflammatory cytokines and interferon responses by doublestranded and single-stranded siRNAs is sequencedependent and requires endosomal localization. J Mol Biol 348:1079-1090.
38. 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 (2005) Sequencespecific potent induction of IFN-alpha by short interfering RNA in plasmacytoid dendritic cells through TLR7. Nat Med 11:263-270.
39. Judge AD, Sood V, Shaw JR, Fang D, McClintock K, MacLachlan I (2005) Sequencedependent stimulation of the mammalian innate immune response by synthetic siRNA. Nat Biotechnol 23:457-462.
40. Sioud M (2006) Single-stranded small interfering RNA are more immunostimulatory than their double-stranded counterparts: a central role for 2'-hydroxyl uridines in immune responses. Eur J Immunol 36:1222-1230.
41. Cekaite L, Furset G, Hovig E, Sioud M (2007) Gene expression analysis in blood cells in response to unmodified and 2'-modified siRNAs reveals TLR-dependent and independent effects. J Mol Biol 365:90-108.
42. 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 (2005) Potent and persistent in vivo anti-HBV activity of chemically modified siRNAs. Nat Biotechnol 23:1002-1007.
43. Flatekval GF, Sioud M (2009) Modulation of dendritic cell function and maturation with mono- and bifunctional small interfering RNAs targeting indoleamine 2,3 dioxygenase. Immunology 128:e837-e848
44. Judge AD, Bola G, Lee AC, MacLachlan I (2006) Design of noninflammatory synthetic siRNA mediating potent gene silencing in vivo. Mol Ther 13:494-505.
45. Bell JK, Askins J, Hall PR, Davies DR, Segal DM (2006) The dsRNA binding site of human Toll-like receptor 3. Proc Natl Acad Sci U S A 103:8792-8797.
46. 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.
47. Sioud M (2007) RNA interference and innate immunity. Adv Drug Deliv Rev 59:153-163.
48. 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.
49. Furset G, Floisand Y, Sioud M (2008) Impaired expression of indoleamine 2, 3-dioxygenase in monocyte-derived dendritic cells in response to Toll-like receptor-7/8 ligands. Immunology 123:263-271.
50. Robbins M, Judge A, Liang L, McClintock K, Yaworski E, MacLachlan I (2007) 2'- O - methylmodified RNAs act as TLR7 antagonists. Mol Ther 15:1663-1669.
51. Marques JT, Devosse T, Wang D, Zamanian-Daryoush M, Serbinowski P, Hartmann R, Fujita T, Behlke MA, Williams BR (2006) A structural basis for discriminating between self and nonself double-stranded RNAs in mammalian cells. Nat Biotechnol 24:559-565.
52. Robbins MA, Li M, Leung I, Li H, Boyer DV, Song Y, Behlke MA, Rossi JJ (2006) Stable expression of shRNAs in human CD34+ progenitor cells can avoid induction of interferon responses to siRNAs in vitro. Nat Biotechnol 24:566-571.
53. Sioud M (2006) RNA interference below the immune radar. Nat Biotechnol 24:521-522.
54. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281-297.
55. Han J, Lee Y, Yeom KH, Nam JW, Heo I, Rhee JK, Sohn SY, Cho Y, Zhang BT, Kim VN (2006) Molecular basis for the recognition of primary microRNAs by the Drosha-DGCR8 complex. Cell 125:887-901.
56. Furset G, Sioud M (2007) Design of bifunctional siRNAs, combining immunostimulation and gene-silencing in one single siRNA molecule. Biochem Biophys Res Commun 352:642-649.
57. Hornung V, Ellegast J, Kim S, Brzozka K, Jung A, Kato H, Poeck H, Akira S, Conzelmann KK, Schlee M, Endres S, Hartmann G (2006) 5'-Triphosphate RNA is the ligand for RIGI. Science 314:994-997.
58. Cui S, Eisenächer K, Kirchhofer A, Brzózka K, Lammens A, Lammens K, Fujita T, Conzelmann KK, Krug A, Hopfner KP (2008) The C-terminal regulatory domain is the RNA 5'-triphosphate sensor of RIG-I. Mol Cell 29:169-179.
59. Kato H, Takeuchi O, Mikamo-Satoh E, Hirai R, Kawai T, Matsushita K, Hiiragi A, Dermody TS, Fujita T, Akira S (2008) Length-dependent recognition of double-stranded ribonucleic acids by retinoic acid-inducible gene-I and melanoma differentiation-associated gene 5. J Exp Med 205:1601-1610.
60. Bao N, Lye KW, Barton MK (2004) MicroRNA binding sites in Arabidopsis class III HD-ZIP mRNAs are required for methylation of the template chromosome. Dev Cell 7:653-662.
61. 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 (2006) Position-specific chemical modification of siRNAs reduces "off-target" transcript silencing. RNA 12:1197-1205.
62. Banchereau J, Steinman RM (1998) Dendritic cells and the control of immunity. Nature 392:245-252.
63. Rossi M, Young JW (2005) Human dendritic cells: potent antigen-presenting cells at the crossroads of innate and adaptive immunity. J Immunol 175:1373-1381.
64. Pardoll D (2003) Does the immune system see tumors as foreign or self? Annu Rev Immunol 21:807-839.
65. Grutz G (2005) New insights into the molecular mechanism of interleukin-10-mediated immunosuppression. J Leukoc Biol 77:3-15.
66. Munn DH, Zhou M, Attwood JT, Bondarev I, Conway SJ, Marshall B, Brown C, Mellor AL (1998) Prevention of allogeneic fetal rejection by tryptophan catabolism. Science 281:1191-1193.
67. Alexander WS, Hilton DJ (2004) The role of suppressors of cytokine signaling (SOCS) proteins in regulation of the immune response. Annu Rev Immunol 22:503-529.
68. Shen L, Evel-Kabler K, Strube R, Chen SY (2004) Silencing of SOCS1 enhances antigen presentation by dendritic cells and antigenspecific anti-tumor immunity. Nat Biotechnol 22:1546-1553.
69. Sioud M, Saebøe-Larsen S, Hetland TE, Kaern J, Mobergslien A, Kvalheim G (2013) Silencing of indoleamine 2,3-dioxygenase enhances dendritic cell immunogenicity and antitumour immunity in cancer patients. Int J Oncol 43:280-288.