The 2'-O-methylation status of a single guanosine controls transfer RNA-mediated toll-like receptor 7 activation or inhibition

Journal of Experimental Medicine

Volumn 209, Issue 2, 2012, Pages 235-241

  Jöckel, Stefanie ^a   Nees, Gernot ^a   Sommer, Romy ^a   Zhao, Yang ^a   Cherkasov, Dmitry ^a   Hori, Hiroyuki ^b   Ehm, Gundi ^a   Schnare, Markus ^a   Nain, Marianne ^a   Kaufmann, Andreas ^a   Bauer, Stefan ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b EHIME UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

2' O METHYLTRANSFERASE; ALPHA INTERFERON; BACTERIAL RNA; GUANOSINE; METHYLTRANSFERASE; TOLL LIKE RECEPTOR 7; TRANSFER RNA; UNCLASSIFIED DRUG;

ACINETOBACTER LWOFFII; ANIMAL CELL; ANTIVIRAL ACTIVITY; ARTICLE; BACTERIAL STRAIN; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DENDRITIC CELL; ESCHERICHIA COLI; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; IMMUNOSTIMULATION; IN VITRO STUDY; INFLUENZA VIRUS A; INNATE IMMUNITY; KNOCKOUT GENE; MIXED INFECTION; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA ISOLATION; RNA METHYLATION; STAPHYLOCOCCUS AUREUS; THERMUS THERMOPHILUS;

ANIMALS; BACTERIA; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DENDRITIC CELLS; GUANOSINE; HUMANS; IMMUNITY, INNATE; IMMUNIZATION; INTERFERON-ALPHA; LEUKOCYTES, MONONUCLEAR; MEMBRANE GLYCOPROTEINS; MICE; MICE, KNOCKOUT; OLIGONUCLEOTIDES; RNA, TRANSFER; TOLL-LIKE RECEPTOR 7; TRNA METHYLTRANSFERASES;

EID: 84863115824     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20111075     Document Type: Article

References (31)

1. Barrat, F.J., T. Meeker, J. Gregorio, J.H. Chan, S. Uematsu, S. Akira, B. Chang, O. Duramad, and R.L. Coffman. 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. http://dx.doi.org/10.1084/jem.20050914
2. Björk, G.R. 1975. Transductional mapping of gene trmA responsible for the production of 5-methyluridine in transfer ribonucleic acid of Escherichia coli. J. Bacteriol. 124:92-98.
3. Björk, G.R., J.U. Ericson, C.E. Gustafsson, T.G. Hagervall, Y.H. Jönsson, and P.M. Wikström. 1987. Transfer RNA modification. Annu. Rev. Biochem. 56:263-287. http://dx.doi.org/10.1146/annurev.bi.56.070187.001403
4. Blasius, A.L., and B. Beutler. 2010. Intracellular toll-like receptors. Immunity. 32:305-315. http://dx.doi.org/10.1016/j.immuni.2010.03.012
5. Chomczynski, P., and N. Sacchi. 2006. The single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction: twenty-something years on. Nat. Protoc. 1:581-585. http://dx.doi.org/10.1038/nprot.2006.83
6. Daffis, S., K.J. Szretter, J. Schriewer, J. Li, S. Youn, J. Errett, T.Y. Lin, S. Schneller, R. Zust, H. Dong, et al. 2010. 2'-O methylation of the viral mRNA cap evades host restriction by IFIT family members. Nature. 468:452-456. http://dx.doi.org/10.1038/nature09489
7. De Bie, L.G., M. Roovers, Y. Oudjama, R. Wattiez, C. Tricot, V. Stalon, L. Droogmans, and J.M. Bujnicki. 2003. The yggH gene of Escherichia coli encodes a tRNA (m7G46) methyltransferase. J. Bacteriol. 185:3238-3243. http://dx.doi.org/10.1128/JB.185.10.3238-3243.2003
8. Diebold, S.S., T. Kaisho, H. Hemmi, S. Akira, and C. Reis e Sousa. 2004. Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science. 303:1529-1531. http://dx.doi.org/10.1126/science.1093616
9. Hament, J.M., J.L. Kimpen, A. Fleer, and T.F. Wolfs. 1999. Respiratory viral infection predisposing for bacterial disease: a concise review. FEMS Immunol. Med. Microbiol. 26:189-195. http://dx.doi.org/10.1111/j.1574-695X.1999.tb01389.x
10. Hamm, S., E. Latz, D. Hangel, T. Müller, P. Yu, D. Golenbock, T. Sparwasser, H. Wagner, and S. Bauer. 2010. Alternating 2'-O-ribose methylation is a universal approach for generating non-stimulatory siRNA by acting as TLR7 antagonist. Immunobiology. 215:559-569. http://dx.doi.org/10.1016/j.imbio.2009.09.003
11. Heil, F., H. Hemmi, H. Hochrein, F. Ampenberger, C. Kirschning, S. Akira, G. Lipford, H. Wagner, and S. Bauer. 2004. Species-specific recognition of single-stranded RNA via toll-like receptor 7 and 8. Science. 303:1526-1529. http://dx.doi.org/10.1126/science.1093620
12. Hemmi, H., T. Kaisho, O. Takeuchi, S. Sato, H. Sanjo, K. Hoshino, T. Horiuchi, H. Tomizawa, K. Takeda, and S. Akira. 2002. Small anti-viral compounds activate immune cells via the TLR7 MyD88-dependent signaling pathway. Nat. Immunol. 3:196-200. http://dx.doi.org/10.1038/ni758
13. Hori, H., T. Suzuki, K. Sugawara, Y. Inoue, T. Shibata, S. Kuramitsu, S. Yokoyama, T. Oshima, and K. Watanabe. 2002. Identification and characterization of tRNA (Gm18) methyltransferase from Thermus thermophilus HB8: domain structure and conserved amino acid sequence motifs. Genes Cells. 7:259-272. http://dx.doi.org/10.1046/j.1365-2443.2002.00520.x
14. Hori, H., S. Kubota, K. Watanabe, J.M. Kim, T. Ogasawara, T. Sawasaki, and Y. Endo. 2003. Aquifex aeolicus tRNA (Gm18) methyltransferase has unique substrate specificity. TRNA recognition mechanism of the enzyme. J. Biol. Chem. 278:25081-25090. http://dx.doi.org/10.1074/jbc.M212577200
15. Hornung, V., S. Rothenfusser, S. Britsch, A. Krug, B. Jahrsdörfer, T. Giese, S. Endres, and G. Hartmann. 2002. 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. 168:4531-4537.
16. Hornung, V., M. Guenthner-Biller, C. Bourquin, A. Ablasser, M. Schlee, S. Uematsu, A. Noronha, M. Manoharan, S. Akira, A. de Fougerolles, 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. http://dx.doi.org/10.1038/nm1191
17. Jain, V., M. Kumar, and D. Chatterji. 2006. ppGpp: stringent response and survival. J. Microbiol. 44:1-10.
18. Judge, A.D., G. Bola, A.C. Lee, and I. MacLachlan. 2006. Design of noninflammatory synthetic siRNA mediating potent gene silencing in vivo. Mol. Ther. 13:494-505. http://dx.doi.org/10.1016/j.ymthe.2005.11.002
19. Karikó, K., M. Buckstein, H. Ni, and D. Weissman. 2005. Suppression of RNA recognition by Toll-like receptors: the impact of nucleoside modification and the evolutionary origin of RNA. Immunity. 23:165- 175. http://dx.doi.org/10.1016/j.immuni.2005.06.008
20. Kato, H., O. Takeuchi, S. Sato, M. Yoneyama, M. Yamamoto, K. Matsui, S. Uematsu, A. Jung, T. Kawai, K.J. Ishii, et al. 2006. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature. 441:101-105. http://dx.doi.org/10.1038/nature04734
21. Monroe, K.M., S.M. McWhirter, and R.E. Vance. 2009. Identification of host cytosolic sensors and bacterial factors regulating the type I interferon response to Legionella pneumophila. PLoS Pathog. 5:e1000665. http://dx.doi.org/10.1371/journal.ppat.1000665
22. Ochi, A., K. Makabe, K. Kuwajima, and H. Hori. 2010. Flexible recognition of the tRNA G18 methylation target site by TrmH methyltransferase through first binding and induced fit processes. J. Biol. Chem. 285:9018-9029. http://dx.doi.org/10.1074/jbc.M109.065698
23. Persson, B.C., G. Jäger, and C. Gustafsson. 1997. The spoU gene of Escherichia coli, the fourth gene of the spoT operon, is essential for tRNA (Gm18) 2'-O-methyltransferase activity. Nucleic Acids Res. 25:4093-4097. http://dx.doi.org/10.1093/nar/25.20.4093
24. Robbins, M., A. Judge, L. Liang, K. McClintock, E. Yaworski, and I. MacLachlan. 2007. 2'-O-methyl-modified RNAs act as TLR7 antagonists. Mol. Ther. 15:1663-1669. http://dx.doi.org/10.1038/sj.mt.6300240
25. Schultz, M. 2008. Clinical use of E. coli Nissle 1917 in inflammatory bowel disease. Inflamm. Bowel Dis. 14:1012-1018. http://dx.doi.org/10.1002/ibd.20377
26. Sioud, M., G. Furset, and L. Cekaite. 2007. Suppression of immunostimulatory siRNA-driven innate immune activation by 2'-modified RNAs. Biochem. Biophys. Res. Commun. 361:122-126. http://dx.doi.org/10.1016/j.bbrc.2007.06.177
27. Spiller, S., S. Dreher, G. Meng, A. Grabiec, W. Thomas, T. Hartung, K. Pfeffer, H. Hochrein, H. Brade, W. Bessler, et al. 2007. Cellular recognition of trimyristoylated peptide or enterobacterial lipopolysaccharide via both TLR2 and TLR4. J. Biol. Chem. 282:13190-13198. http://dx.doi.org/10.1074/jbc.M610340200
28. Takeuchi, O., and S. Akira. 2010. Pattern recognition receptors and inflammation. Cell. 140:805-820. http://dx.doi.org/10.1016/j.cell.2010.01.022
29. Tashiro, M., P. Ciborowski, H.D. Klenk, G. Pulverer, and R. Rott. 1987. Role of Staphylococcus protease in the development of influenza pneumonia. Nature. 325:536-537. http://dx.doi.org/10.1038/325536a0
30. Urbonavicius, J., J.M. Durand, and G.R. Björk. 2002. Three modifications in the D and T arms of tRNA influence translation in Escherichia coli and expression of virulence genes in Shigella flexneri. J. Bacteriol. 184:5348- 5357. http://dx.doi.org/10.1128/JB.184.19.5348-5357.2002
31. Züst, R., L. Cervantes-Barragan, M. Habjan, R. Maier, B.W. Neuman, J. Ziebuhr, K.J. Szretter, S.C. Baker, W. Barchet, M.S. Diamond, 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. http://dx.doi.org/10.1038/ni.1979