A toll-like receptor-independent antiviral response induced by double-stranded B-form DNA

Nature Immunology

Volumn 7, Issue 1, 2006, Pages 40-48

  Ishii, Ken J ^a,b   Coban, Cevayir ^a,b   Kato, Hiroki ^b   Takahashi, Ken ^b   Torii, Yuichi ^b   Takeshita, Fumihiko ^c   Ludwig, Holger ^d   Sutter, Gerd ^d   Suzuki, Koichi ^e   Hemmi, Hiroaki ^b   Sato, Shintaro ^b   Yamamoto, Masahiro ^b   Uematsu, Satoshi ^b   Kawai, Taro ^a,b   Takeuchi, Osamu ^a,b   Akira, Shizuo ^a,b  

^a OSAKA UNIVERSITY   (Japan)

^b OSAKA UNIVERSITY   (Japan)

^c YOKOHAMA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d PAUL EHRLICH INSTITUT   (Germany)

^e NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; DOUBLE STRANDED DNA; I KAPPA B KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 3; RNA HELICASE; TOLL LIKE RECEPTOR;

ANIMAL CELL; ANTIVIRAL ACTIVITY; ARTICLE; CONTROLLED STUDY; CPG ISLAND; CYTOKINE PRODUCTION; DENDRITIC CELL; DNA MICROARRAY; DNA SEQUENCE; EMBRYO; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION PROFILING; GENETIC CODE; HUMAN; HUMAN CELL; INNATE IMMUNITY; MOLECULAR MECHANICS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REGULATORY MECHANISM; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; UNINDEXED SEQUENCE; VIRUS IMMUNITY; VIRUS RESISTANCE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CHEMOKINES; DNA; DNA, BACTERIAL; DNA, VIRAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FIBROBLASTS; GENE EXPRESSION; HUMANS; INTERFERON REGULATORY FACTOR-3; INTERFERON TYPE I; MICE; MICE, KNOCKOUT; NF-KAPPA B; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROMOTER REGIONS (GENETICS); PROTEIN-SERINE-THREONINE KINASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS; TRANSFECTION; VIRUS DISEASES;

EID: 29244471275     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni1282     Document Type: Article

References (50)

1. Isaacs, A, Cox, R.A. & Rotem, Z. Foreign nucleic acids as the stimulus to make interferon. Lancet 2, 113-116 (1963).
2. Tokunaga, T. et al. Antitumor activity of deoxyribonucleic acid fraction from Mycobacterium bovis BCG. I. Isolation, physicochemical characterization, and antitumor activity. J. Natl. Cancer Inst. 72, 955-962 (1984).
3. Akira, S. & Takeda, K. Toll-like receptor signalling. Nat. Rev. Immunol. 4, 499-511 (2004).
4. Iwasaki, A. & Medzhitov, R. Toll-like receptor control of the adaptive immune responses. Nat. Immunol. 5, 987-995 (2004).
5. Theofilopoulos, A.N., Baccala, R., Beutler, B. & Kono, D.H. Type I interferons (α/β) in immunity and autoimmunity. Annu. Rev. Immunol. 23, 307-336 (2005).
6. + dendritic cells. J. Immunol. 166, 5000-5007 (2001).
7. Kawai, T. et al. Interferon-alpha induction through Toll-like receptors involves a direct interaction of IRF7 with MyD88 and TRAF6. Nat. Immunol. 5, 1061-1068 (2004).
8. - and TLR9-mediated interferon-α induction. J. Exp. Med. 201, 915-923 (2005).
9. Honda, K. et al. Role of a transductional-transcriptional processor complex involving MyD88 and IRF-7 in Toll-like receptor signaling. Proc. Natl. Acad. Sci. USA 101, 15416-15421 (2004).
10. Sharma, S. et al. Triggering the interferon antiviral response through an IKK-related pathway, Science 300, 1148-1151 (2003).
11. Fitzgerald, K.A. et al. IKKε and TBK1 are essential components of the IRF3 signaling pathway. Nat. Immunol. 4, 491-496 (2003).
12. Hemmi, H. et al. The roles of two IκB kinase-related kinases in lipopolysaccharide and double stranded RNA signaling and viral infection. J. Exp. Med. 199, 1641-1650 (2004).
13. Perry, A.K., Chow, EX, Goodnough, J.B., Yeh, W.C. & Cheng, G. Differential requirement for TANK-binding kinase-1 in type I interferon responses to toll-like receptor activation and viral infection. J. Exp. Med. 199, 1651-1658 (2004).
14. Vallin, H., Perers, A., Alm, G.V. & Ronnblom, L. Anti-double-stranded DNA antibodies and immunostimulatory plasmid DNA in combination mimic the endogenous IFN-α inducer in systemic lupus erythematosus. J. Immunol. 163, 6306-6313 (1999).
15. Boule, M.W. et al. Toll-like receptor 9-dependent and -independent dendritic cell activation by chromatin-immunoglobulin G complexes. J. Exp. Med. 199, 1631-1640 (2004).
16. Decker, P., Singh-Jasuja, H., Haager, S., Kotter, I. & Rammensee, H.G. Nucleosome, the main autoantigen in systemic lupus erythematosus, induces direct dendritic cell activation via a MyD88-independent pathway: Consequences on inflammation. J. Immunol. 174, 3326-3334 (2005).
17. Kawane, K. et al. Impaired thymic development in mouse embryos deficient in apoptotic DNA degradation. Nat. Immunol. 4. 138-144 (2003).
18. Yoshida, H., Okabe, Y., Kawane, K., Fukuyama, H. & Nagata, S. Lethal anemia caused by interferon-beta produced in mouse embryos carrying undigested DNA. Nat. Immunol. 6, 49-56 (2005).
19. Suzuki, K. et al. Activation of target-tissue immune-recognition molecules by double-stranded stranded polynucleotides. Proc. Natl. Acad. Sci. USA 96, 2285-2290 (1999).
20. Ishii, K.J. et al. Genomic DNA released by dying cells induces the maturation of APCs. J. Immunol. 167, 2602-2607 (2001).
21. Li, S. et al. Induction of IFN-regulated factors and antitumoral surveillance by transfected placebo plasmid DNA. Mol. Ther. 11, 112-119 (2005).
22. Yasuda. K, et al. Endosomal translocation of vertebrate DNA activates dendritic cells via TLR9-dependent and -independent pathways. J. Immunol. 174, 6129-6136 (2005).
23. Ishii, K.J. & Akira, S. Innate immune recognition of nucleic acids: Beyond toll-like receptors. Int. J. Cancer 117, 517-523 (2005).
24. RTch, A. & Zhang, S. Timeline: Z-DNA: the long road to biological function, Nat. Rev. Genet. 4, 566-572 (2003).
25. Braun, C.S. et al, The structure of DNA within cationic lipid/DNA complexes. Biophys. J. 84, 1114-1123 (2003).
26. Moller, A., Nordheim, A., Kozlowski, S.A., Patel, D.J. & Rich, A. Bromination stabilizes poly(dG-dC) in the Z-DNA form under low-salt conditions. Biochemistry 23, 54-62 (1984).
27. Kimura, T., Kawai, K., Tojo, S. & Majima, T. One-electron attachment reaction of B- and Z-DNA modified by 8-bromo-2′-deoxyguanosine. J. Org. Chem. 69, 1169-1173 (2004).
28. Kato, H. et al. Cell type-specific involvement of RIG-I in antiviral response. Immunity 23, 19-28 (2005).
29. Yamamoto, M. et al. Role of adaptor TRIF in the My D88-independent toll-like receptor signaling pathway. Science 301, 640-643 (2003).
30. O Yoneyama, M. et al. The RNA helicase RIG-1 has an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol. 5, 730-737 (2004).
31. Kawai, T., et al. IPS-1, an adaptor triggering RIG-1-and Mda5-mediated type I interferon induction. Nat. Immunol. 6, 981-988 (2005).
32. Seth, R.B., Sun, L., Ea, C.K. & Chen, ZJ. Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-κB and IRF 3. Cell 122, 669-682 (2005).
33. Xu, L.G. et al. VISA is an adapter protein required for virus-triggered IFN-β signaling. Mol. Cell 19, 727-740 (2005).
34. Meylar, E. et al. Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature (2005).
35. Drexler, I., et al. Identification of vaccinia virus epitope-specific HLA-A*0201-restricted T cells and comparative analysis of smallpox vaccines. Proc. Natl. Acad. Sci. USA 100, 217-222 (2003).
36. Kim, Y.G. et al. A role for Z-DNA binding in vaccinia virus pathogenesis. Proc. Natl. Acad. Sci. USA 100, 6974-6979 (2003).
37. Hornemann, S. et al, Replication of modified vaccinia virus Ankara in primary chicken embryo fibroblasts requires expression of the interferon resistance gene E3L. J. Virol. 77, 8394-8407 (2003).
38. Watson, J.D. & Crick, FH, Molecular structure of nucleic acids; a structure for deoxyribose nucleic acid. Nature 171, 737-738 (1953).
39. Smith, E.J., Marie, I., Pralkash, A., Garcia-Sastre, A. & Levy, D.E. IRF3 and IRF7 phosphorylation in virus-infected cells does not require double-stranded RNA-dependent protein kinase R or IκB kinase but is blocked by vaccinia virus E3L protein. J. Biol. Chem. 276, 8951-8957 (2001).
40. Kim, Y.G,, Lowenhaupt, K., Oh, D.B., Kim, K.K. & Rich, A. Evidence that vaccinia virulence factor E3L binds to Z-DNA in vivo: Implications for development of a therapy for poxvirus infection. Proc. Natt. Acad. Sci. USA 101, 1514-1518 (2004).
41. Kovacsovics, M. et al. Overexpression of Helicard, a CARD-containing helicase cleaved during apoptosis, accelerates DNA degradation. Curr. Biol. 12, 838-843. (2002).
42. Andrejeva, J. et al. The V proteins of paramyxoviruses bind the IFN-inducible RNA helicase, mda-5, and inhibit its activation of the IFN-beta promoter. Proc. Natl. Acad. Sci. USA 101, 17264-17269 (2004).
43. Yoneyama, M. et al. Shared and unique functions of the DExD/H-Box helicases RIG-I, MDA5, and LGP2 in antiviral innate immunity. J. Immunol. 175, 2851-2858 (2005).
44. Spies, B. et al. Vaccination with plasmid DNA activates dendritic cells via Toll-like receptor 9 (TLR9) but functions in TLR9-deficient mice. J. Immunol. 171, 5908-5912 (2003).
45. +/+ mice display similar immune responses to a DNA vaccine. Immunology 113, 114-120 (2004).
46. Coban, C. et al. Toll-like receptor 9 mediates innate immune activation by the malaria pigment hemozoin. J. Exp. Med. 201, 19-25 (2005).
47. Gursel, M., Verthelyi, D., Gursel, I., Ishii, K.J. & Klinman, D.M. Differential and competitive activation of human immune cells by distinct classes of CpG oligodeoxy-nucleotide. J. Leukoc. Biol. 71, 813-820 (2002).
48. Takeshita, S., Takeshita, F., Haddad, D.E., Ishii, K.J. & Klinman. D.M. CpG oligodeoxy-nucleotides induce murine macrophages to up-regulate chemokine mRNA expression. Cell. Immunol. 206, 101-106 (2000).
49. + T cell activation. Genes Cells 7, 309-320 (2002).
50. + monocytes. J. Immunol. 174, 2273-2279 (2005).