2'-O-Methylation within Bacterial RNA Acts as Suppressor of TLR7/TLR8 Activation in Human Innate Immune Cells

Journal of Innate Immunity

Volumn 7, Issue 5, 2015, Pages 482-493

  Rimbach, Katharina ^a   Kaiser, Steffen ^b   Helm, Mark ^b   Dalpke, Alexander H ^a   Eigenbrod, Tatjana ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

2' O methylation; Bacterial RNA; Immunostimulation; Innate immunity; Peripheral blood mononuclear cells; RNA modification

Indexed keywords

ALPHA INTERFERON; BACTERIAL RNA; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 12P40; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; RESIQUIMOD; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8; TRANSFER RNA;

2' O METHYLATION; ANIMAL CELL; ARTICLE; BACTERIAL STRAIN; CELL ACTIVATION; CELL DIFFERENTIATION; CELL ISOLATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENZYME ACTIVATION; ESCHERICHIA COLI; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOSTIMULATION; INNATE IMMUNITY; MONOCYTE; MOUSE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR BINDING; RNA METHYLATION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ANIMAL; CELL CULTURE; COMPARATIVE STUDY; DENDRITIC CELL; GENETICS; IMMUNOLOGY; IMMUNOSUPPRESSIVE TREATMENT; INBRED MOUSE STRAIN; METABOLISM; METHYLATION; MICROBIOLOGY; SPECIES DIFFERENCE;

ANIMALS; CELLS, CULTURED; DENDRITIC CELLS; ESCHERICHIA COLI; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; IMMUNITY, INNATE; IMMUNOSUPPRESSION; INTERFERON-ALPHA; METHYLATION; MICE; MICE, INBRED STRAINS; MONOCYTES; NF-KAPPA B; RNA, BACTERIAL; SIGNAL TRANSDUCTION; SPECIES SPECIFICITY; TOLL-LIKE RECEPTOR 7; TOLL-LIKE RECEPTOR 8;

EID: 84941995713     PISSN: 1662811X     EISSN: 16628128     Source Type: Journal    
DOI: 10.1159/000375460     Document Type: Article

References (42)

1. 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: Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 2006; 441: 101-105.
2. Hornung V, Ellegast J, Kim S, Brzózka K, Jung A, Kato H, Poeck H, Akira S, Conzelmann K, Schlee M, Endres S, Hartmann G: 5-Triphosphate RNA is the ligand for RIG-I. Science 2006; 314: 994-997.
3. Yoneyama M, Kikuchi M, Natsukawa T, Shinobu N, Imaizumi T, Miyagishi M, Taira K, Akira S, Fujita T: The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat Immunol 2004; 5: 730-737.
4. Hemmi H, Takeuchi O, Kawai T, Kaisho T, Sato S, Sanjo H, Matsumoto M, Hoshino K, Wagner H, Takeda K, Akira S: A Toll-like receptor recognizes bacterial DNA. Nature 2000; 408: 740-745.
5. Heil F, Hemmi H, Hochrein H, Ampenberger F, Kirschning C, Akira S, Lipford G, Wagner H, Bauer S: Species-specific recognition of single-stranded RNA via toll-like receptor 7 and 8. Science 2004; 303: 1526-1529.
6. Diebold SS, Kaisho T, Hemmi H, Akira S, Reis e Sousa C: Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science 2004; 303: 1529-1531.
7. Hemmi H, Kaisho T, Takeuchi O, Sato S, Sanjo H, Hoshino K, Horiuchi T, Tomizawa H, Takeda K, Akira S: Small anti-viral compounds activate immune cells via the TLR7 MyD88-dependent signaling pathway. Nat Immunol 2002; 3: 196-200.
8. Alexopoulou L, Holt AC, Medzhitov R, Flavell RA: Recognition of double-stranded RNA and activation of NF-kappaB by Tolllike receptor 3. Nature 2001; 413: 732-738.
9. Li X, Chen ZJ: Sequence specific detection of bacterial 23S ribosomal RNA by TLR13. Elife 2012; 1:e00102.
10. Forsbach A, Nemorin J, Montino C, Müller C, Samulowitz U, Vicari AP, Jurk M, Mutwiri GK, Krieg AM, Lipford GB, Vollmer J: Identification of RNA sequence motifs stimulating sequence-specific TLR8-dependent immune responses. J Immunol 2008; 180: 3729-3738.
11. Vollmer J, Tluk S, Schmitz C, Hamm S, Jurk M, Forsbach A, Akira S, Kelly KM, Reeves WH, Bauer S, Krieg AM: Immune stimulation mediated by autoantigen binding sites within small nuclear RNAs involves Toll-like receptors 7 and 8. J Exp Med 2005; 202: 1575-1585.
12. Gehrig S, Eberle M, Botschen F, Rimbach K, Eberle F, Eigenbrod T, Kaiser S, Holmes WM, Erdmann VA, Sprinzl M, Bec G, Keith G, Dalpke AH, Helm M: Identification of modifications in microbial, native tRNA that suppress immunostimulatory activity. J Exp Med 2012; 209: 225-233.
13. Czerwoniec A, Dunin-Horkawicz S, Purta E, Kaminska KH, Kasprzak JM, Bujnicki JM, Grosjean H, Rother K: MODOMICS: A database of RNA modification pathways. 2008 update. Nucleic Acids Res 2009; 37:D118-D121.
14. Koski GK, Karikó K, Xu S, Weissman D, Cohen PA, Czerniecki BJ: Cutting edge: innate immune system discriminates between RNA containing bacterial versus eukaryotic structural features that prime for high-level IL-12 secretion by dendritic cells. J Immunol 2004; 172: 3989-3993.
15. Eberle F, Giessler K, Deck C, Heeg K, Peter M, Richert C, Dalpke AH: Modifications in small interfering RNA that separate immunostimulation from RNA interference. J Immunol 2008; 180: 3229-3237.
16. Karikó K, Buckstein M, Ni H, Weissman D: Suppression of RNA recognition by Toll-like receptors: the impact of nucleoside modification and the evolutionary origin of RNA. Immunity 2005; 23: 165-175.
17. Karikó K, Weissman D: Naturally occurring nucleoside modifications suppress the immunostimulatory activity of RNA: implication for therapeutic RNA development. Curr Opin Drug Discov Devel 2007; 10: 523-532.
18. Jöckel S, Nees G, Sommer R, Zhao Y, Cherkasov D, Hori H, Ehm G, Schnare M, Nain M, Kaufmann A, Bauer S: The 2'-O-methylation status of a single guanosine controls transfer RNA-mediated Toll-like receptor 7 activation or inhibition. J Exp Med 2012; 209: 235-241.
19. Hamm S, Latz E, Hangel D, Müller T, Yu P, Golenbock D, Sparwasser T, Wagner H, Bauer S: Alternating 2'-O-ribose methylation is a universal approach for generating non-stimulatory siRNA by acting as TLR7 antagonist. Immunobiology 2010; 215: 559-569.
20. Hornung V, Rothenfusser S, Britsch S, Krug A, Jahrsdörfer B, Giese T, Endres S, Hartmann G: Quantitative expression of toll-like receptor 1-10 mRNA in cellular subsets of human peripheral blood mononuclear cells and sensitivity to CpG oligodeoxynucleotides. J Immunol 2002; 168: 4531-4537.
21. Kaiser S, Rimbach K, Eigenbrod T, Dalpke AH, Helm M: A modified dinucleotide motif specifies tRNA recognition by TLR7. RNA 2014; 20: 1351-1355.
22. Eigenbrod T, Franchi L, Muñoz-Planillo R, Kirschning CJ, Freudenberg MA, Núñez G, Dalpke A: Bacterial RNA mediates activation of caspase-1 and IL-1 release independently of TLRs 3, 7, 9 and TRIF but is dependent on UNC93B. J Immunol 2012; 189: 328-336.
23. Hengesbach M, Kobitski A, Voigts-Hoffmann F, Frauer C, Nienhaus GU, Helm M: RNA intramolecular dynamics by single-molecule FRET. Curr Protoc Nucleic Acid Chem 2008;chapter 11:unit 11. 12.
24. Schildberger A, Rossmanith E, Eichhorn T, Strassl K, Weber V: Monocytes, peripheral blood mononuclear cells, and THP-1 cells exhibit different cytokine expression patterns following stimulation with lipopolysaccharide. Mediators Inflamm 2013; 2013: 697972.
25. Watford WT, Moriguchi M, Morinobu A, O'Shea JJ: The biology of IL-12: coordinating innate and adaptive immune responses. Cytokine Growth Factor Rev 2003; 14: 361-368.
26. Oldenburg M, Krüger A, Ferstl R, Kaufmann A, Nees G, Sigmund A, Bathke B, Lauterbach H, Suter M, Dreher S, Koedel U, Akira S, Kawai T, Buer J, Wagner H, Bauer S, Hochrein H, Kirschning CJ: TLR13 recognizes bacterial 23S rRNA devoid of erythromycin resistance-forming modification. Science 2012; 337: 1111-1115.
27. Ewald SE, Engel A, Lee J, Wang M, Bogyo M, Barton GM: Nucleic acid recognition by Tolllike receptors is coupled to stepwise processing by cathepsins and asparagine endopeptidase. J Exp Med 2011; 208: 643-651.
28. Maschalidi S, Hässler S, Blanc F, Sepulveda FE, Tohme M, Chignard M, van Endert P, Si-Tahar M, Descamps D, Manoury B: Asparagine endopeptidase controls anti-influenza virus immune responses through TLR7 activation. PLoS Pathog 2012; 8:e1002841.
29. Daffis S, Szretter KJ, Schriewer J, Li J, Youn S, Errett J, Lin T, Schneller S, Zust R, Dong H, Thiel V, Sen GC, Fensterl V, Klimstra WB, Pierson TC, Buller RM, Gale M, Shi P, Diamond MS: 2'-O methylation of the viral mRNA cap evades host restriction by IFIT family members. Nature 2010; 468: 452-456.
30. Züst R, Cervantes-Barragan L, Habjan M, Maier R, Neuman BW, Ziebuhr J, Szretter KJ, Baker SC, Barchet W, Diamond MS, Siddell SG, Ludewig B, Thiel V: 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 2011; 12: 137-143.
31. Anderson BR, Muramatsu H, Jha BK, Silverman RH, Weissman D, Karikó K: Nucleoside modifications in RNA limit activation of 2'-5-oligoadenylate synthetase and increase resistance to cleavage by RNase L. Nucleic Acids Res 2011; 39: 9329-9338.
32. Sioud M, Furset G, Cekaite L: Suppression of immunostimulatory siRNA-driven innate immune activation by 2'-modified RNAs. Biochem Biophys Res Commun 2007; 361: 122-126.
33. Sepulveda FE, Maschalidi S, Colisson R, Heslop L, Ghirelli C, Sakka E, Lennon-Duménil A, Amigorena S, Cabanie L, Manoury B: Critical role for asparagine endopeptidase in endocytic Toll-like receptor signaling in dendritic cells. Immunity 2009; 31: 737-748.
34. Kanno A, Yamamoto C, Onji M, Fukui R, Saitoh S, Motoi Y, Shibata T, Matsumoto F, Muta T, Miyake K: Essential role for Toll-like receptor 7 (TLR7)-unique cysteines in an intramolecular disulfide bond, proteolytic cleavage and RNA sensing. Int Immunol 2013; 25: 413-422.
35. Eberle F, Sirin M, Binder M, Dalpke AH: Bacterial RNA is recognized by different sets of immunoreceptors. Eur J Immunol 2009; 39: 2537-2547.
36. Takeuchi O, Kawai T, Mühlradt PF, Morr M, Radolf JD, Zychlinsky A, Takeda K, Akira S: Discrimination of bacterial lipoproteins by Toll-like receptor 6. Int Immunol 2001; 13: 933-940.
37. Takeuchi O, Sato S, Horiuchi T, Hoshino K, Takeda K, Dong Z, Modlin RL, Akira S: Cutting edge: role of Toll-like receptor 1 in mediating immune response to microbial lipoproteins. J Immunol 2002; 169: 10-14.
38. Poltorak A, He X, Smirnova I, Liu MY, van Huffel C, Du X, Birdwell D, Alejos E, Silva M, Galanos C, Freudenberg M, Ricciardi-Castagnoli P, Layton B, Beutler B: Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 1998; 282: 2085-2088.
39. Bogdan C, Mattner J, Schleicher U: The role of type I interferons in non-viral infections. Immunol Rev 2004; 202: 33-48.
40. Schiavoni G, Mauri C, Carlei D, Belardelli F, Pastoris MC, Proietti E: Type I IFN protects permissive macrophages from Legionella pneumophila infection through an IFN-gamma-independent pathway. J Immunol 2004; 173: 1266-1275.
41. Decker T, Müller M, Stockinger S: The yin and yang of type I interferon activity in bacterial infection. Nat Rev Immunol 2005; 5: 675-687.
42. Colak E, Leslie A, Zausmer K, Khatamzas E, Kubarenko AV, Pichulik T, Klimosch SN, Mayer A, Siggs O, Hector A, Fischer R, Klesser B, Rautanen A, Frank M, Hill AV, Manoury B, Beutler B, Hartl D, Simmons A, Weber AN: RNA and imidazoquinolines are sensed by distinct TLR7/8 ectodomain sites resulting in functionally disparate signaling events. J Immunol 2014; 192: 5963-5973.