Intracellular detection and immune signaling pathways of DNA vaccines

Expert Review of Vaccines

Volumn 8, Issue 9, 2009, Pages 1161-1170

  Tang, Choon Kit ^a   Pietersz, Geoffrey A ^a  

^a BURNET INSTITUTE   (Australia)

Author keywords

AIM2; DAI; Danger signal; DNA vaccine; Intracellular detection; RIP1; Signaling pathway; TBK1; Toll like receptor 9; Type 1 interferon

Indexed keywords

CYTOKINE; DNA DEPENDENT ACTIVATOR OF INTERFERON REGULATORY FACTOR; DNA VACCINE; I KAPPA B KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON; INTERFERON REGULATORY FACTOR 3; INTERFERON REGULATORY FACTOR 7; INTERLEUKIN 1BETA CONVERTING ENZYME; NUCLEIC ACID; PHOSPHOTRANSFERASE; PROTEIN ABSENT IN MELANOMA 2; TANK BINDING KINASE 1; TOLL LIKE RECEPTOR 9; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; CPG ISLAND; CYTOSOL; DNA IMMUNIZATION; ENZYME ACTIVATION; ENZYME ANALYSIS; HUMAN; IMMUNE RESPONSE; IMMUNOMODULATION; IMMUNOSTIMULATION; NONHUMAN; NUCLEIC ACID ANALYSIS; PRIORITY JOURNAL; REVIEW;

CYTOKINES; DNA-BINDING PROTEINS; HUMANS; NUCLEAR PROTEINS; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, IMMUNOLOGIC; SIGNAL TRANSDUCTION; VACCINES, DNA;

EID: 70249147673     PISSN: 14760584     EISSN: 17448395     Source Type: Journal    
DOI: 10.1586/erv.09.79     Document Type: Review

References (63)

1. Takaoka A, Wang Z, Choi MK et al. DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune response. Nature 448(7152), 501-505 (2007). •• First description of DNA-dependent activator of interferon (IFN) regulatory factors (DAI) as a cytosolic DNA sensor.
2. Takaoka A, Taniguchi T. Cytosolic DNA recognition for triggering innate immune responses. Adv. Drug Deliv. Rev. 60(7), 847-857 (2008).
3. Ishii KJ, Coban C, Kato H et al. A Toll-like receptor-independent antiviral response induced by double-stranded B-form DNA. Nat. Immunol. 7(1), 40-48 (2006).
4. Ishii KJ, Kawagoe T, Koyama S et al. TANK-binding kinase-1 delineates innate and adaptive immune responses to DNA vaccines. Nature 451(7179), 725-729 (2008). •• Discovery of TANK-binding kinase-1 as an important mediator in the DNA vaccine-induced adaptive immune response.
5. Garren H, Robinson WH, Krasulova E et al. Phase 2 trial of a DNA vaccine encoding myelin basic protein for multiple sclerosis. Ann. Neurol. 63(5), 611-620 (2008).
6. Muruve DA, Petrilli V, Zaiss AK et al. The inflammasome recognizes cytosolic microbial and host DNA and triggers an innate immune response. Nature 452(7183), 103-107 (2008).
7. Ishii KJ, Suzuki K, Coban C et al. Genomic DNA released by dying cells induces the maturation of APCs. J. Immunol. 167(5), 2602-2607 (2001).
8. Suzuki K, Mori A, Ishii KJ et al. Activation of target-tissue immune-recognition molecules by double-stranded polynucleotides. Proc. Natl Acad. Sci. USA 96(5), 2285-2290 (1999).
9. Kawane K, Ohtani M, Miwa K et al. Chronic polyarthritis caused by mammalian DNA that escapes from degradation in macrophages. Nature 443(7114), 998-1002 (2006).
10. Napirei M, Karsunky H, Zevnik B, Stephan H, Mannherz HG, Moroy T. Features of systemic lupus erythematosus in DNase1-deficient mice. Nat. Genet. 25(2), 177-181 (2000).
11. Stetson DB, Medzhitov R. Type I interferons in host defense. Immunity 25(3), 373-381 (2006). • Describes the importance of type I IFN in the host defense mechanism.
12. Malinin NL, Boldin MP, Kovalenko AV, Wallach D. MAP3K-related kinase involved in NF-κB induction by TNF, CD95 and IL-1. Nature 385(6616), 540-544 (1997).
13. Nakaya T, Sato M, Hata N et al. Gene induction pathways mediated by distinct IRFs during viral infection. Biochem. Biophys. Res. Commun. 283(5), 1150-1156 (2001).
14. Sato M, Suemori H, Hata N et al. Distinct and essential roles of transcription factors IRF-3 and IRF-7 in response to viruses for IFN-α/β gene induction. Immunity 13(4), 539-548 (2000).
15. Pham HT, Park MY, Kim KK, Kim YG, Ahn JH. Intracellular localization of human ZBP1: differential regulation by the Z-DNA binding domain, Zα, in splice variants. Biochem. Biophys. Res. Commun. 348(1), 145-152 (2006).
16. Burckstummer T, Baumann C, Bluml S et al. An orthogonal proteomic-genomic screen identifies AIM2 as a cytoplasmic DNA sensor for the inflammasome. Nat. Immunol. 10(3), 266-272 (2009). •• Identification of absent in melanoma-2 as a cytosolic DNA sensor.
17. Alexopoulou L, Holt AC, Medzhitov R, Flavell RA. Recognition of double-stranded RNA and activation of NF-κB by Toll-like receptor 3. Nature 413(6857), 732-738 (2001).
18. 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 303(5663), 1529-1531 (2004).
19. Heil F, Hemmi H, Hochrein H et al. Species-specific recognition of single-stranded RNA via toll-like receptor 7 and 8. Science 303(5663), 1526-1529 (2004).
20. Hemmi H, Takeuchi O, Kawai T et al. A Toll-like receptor recognizes bacterial DNA. Nature 408(6813), 740-745 (2000). • Discovery of Toll-like receptor (TLR)9 as the detector of CpG motifs in DNA.
21. Yoneyama M, Kikuchi M, Natsukawa T et al. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol. 5(7), 730-737 (2004).
22. Yoneyama M, Kikuchi M, Matsumoto K et al. Shared and unique functions of the DExD/H-box helicases RIG-I, MDA5, and LGP2 in antiviral innate immunity. J. Immunol. 175(5), 2851-2858 (2005).
23. Shortman K, Liu YJ. Mouse and human dendritic cell subtypes. Nat. Rev. Immunol. 2(3), 151-161 (2002).
24. Hochrein H, O'Keeffe M, Wagner H. Human and mouse plasmacytoid dendritic cells. Hum. Immunol. 63(12), 1103-1110 (2002).
25. Krieg AM, Yi AK, Matson S et al. CpG motifs in bacterial DNA trigger direct B-cell activation. Nature 374(6522), 546-549 (1995).
26. Jiang W, Lederman MM, Harding CV, Rodriguez B, Mohner RJ, Sieg SF. TLR9 stimulation drives naive B cells to proliferate and to attain enhanced antigen presenting function. Eur. J. Immunol. 37(8), 2205-2213 (2007).
27. Ballas ZK. Modulation of NK cell activity by CpG oligodeoxynucleotides. Immunol. Res. 39(1-3), 15-21 (2007).
28. Dearman RJ, Cumberbatch M, Maxwell G, Basketter DA, Kimber I. Toll-like receptor ligand activation of murine bone marrow-derived dendritic cells. Immunology 126(4), 475-484 (2008).
29. Kumagai Y, Takeuchi O, Akira S. TLR9 as a key receptor for the recognition of DNA. Adv. Drug Deliv. Rev. 60(7), 795-804 (2008).
30. +/+ mice display similar immune responses to a DNA vaccine. Immunology 113(1), 114-120 (2004). • Demonstration of TLR9 is not necessary for DNA-induced immune responses.
31. Spies B, Hochrein H, Vabulas M et al. Vaccination with plasmid DNA activates dendritic cells via Toll-like receptor 9 (TLR9) but functions in TLR9-deficient mice. J. Immunol. 171(11), 5908-5912 (2003).
32. Schneeberger A, Wagner C, Zemann A et al. CpG motifs are efficient adjuvants for DNA cancer vaccines. J. Invest. Dermatol. 123(2), 371-379 (2004).
33. Kwissa M, Amara RR, Robinson HL et al. Adjuvanting a DNA vaccine with a TLR9 ligand plus Flt3 ligand results in enhanced cellular immunity against the simian immunodeficiency virus. J. Exp. Med. 204(11), 2733-2746 (2007).
34. Schroder K, Spille M, Pilz A et al. Differential effects of CpG DNA on IFN-b induction and STAT1 activation in murine macrophages versus dendritic cells: alternatively activated STAT1 negatively regulates TLR signaling in macrophages. J. Immunol. 179(6), 3495-3503 (2007).
35. Schmitz F, Heit A, Guggemoos S et al. Interferon-regulatory-factor 1 controls Toll-like receptor 9-mediated IFN-β production in myeloid dendritic cells. Eur. J. Immunol. 37(2), 315-327 (2007).
36. Honda K, Ohba Y, Yanai H et al. Spatiotemporal regulation of MyD88-IRF-7 signalling for robust type-I interferon induction. Nature 434(7036), 1035-1040 (2005).
37. Deigendesch N, Koch-Nolte F, Rothenburg S. ZBP1 subcellular localization and association with stress granules is controlled by its Z-DNA binding domains. Nucleic Acids Res. 34(18), 5007-5020 (2006).
38. Fu Y, Comella N, Tognazzi K, Brown LF, Dvorak HF, Kocher O. Cloning of DLM-1, a novel gene that is up-regulated in activated macrophages, using RNA differential display. Gene 240(1), 157-163 (1999).
39. Wang Z, Choi MK, Ban T et al. Regulation of innate immune responses by DAI (DLM-1/ZBP1) and other DNAsensing molecules. Proc. Natl Acad. Sci. USA 105(14), 5477-5482 (2008).
40. Lippmann J, Rothenburg S, Deigendesch N et al. IFNβ responses induced by intracellular bacteria or cytosolic DNA in different human cells do not require ZBP1 (DLM-1/DAI). Cell. Microbiol. 10(12), 2579-2588 (2008).
41. Yu HB, Finlay BB. The caspase-1 inflammasome: a pilot of innate immune responses. Cell Host Microbe 4(3), 198-208 (2008).
42. Schmitz J, Owyang A, Oldham E et al. IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines. Immunity 23(5), 479-490 (2005).
43. Srinivasula SM, Poyet JL, Razmara M, Datta P, Zhang Z, Alnemri ES. The PYRIN-CARD protein ASC is an activating adaptor for caspase-1. J. Biol. Chem. 277(24), 21119-21122 (2002).
44. Hornung V, Ablasser A, Charrel-Dennis M et al. AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature 458, 514-518 (2009).
45. Youn HS, Lee JY, Fitzgerald KA, Young HA, Akira S, Hwang DH. Specific inhibition of MyD88-independent signaling pathways of TLR3 and TLR4 by resveratrol: molecular targets are A1 and RIP1 in TRIF complex. J. Immunol. 175(5), 3339-3346 (2005).
46. Charrel-Dennis M, Latz E, Halmen KA et al. TLR-independent type I interferon induction in response to an extracellular bacterial pathogen via intracellular recognition of its DNA. Cell Host Microbe 4(6), 543-554 (2008).
47. Sato S, Sugiyama M, Yamamoto M et al. Toll/IL-1 receptor domain-containing adaptor inducing IFN-β (TRIF) associates with TNF receptor-associated factor 6 and TANK-binding kinase 1, and activates two distinct transcription factors, NF-κB and IFN-regulatory factor-3, in the Toll-like receptor signaling. J. Immunol. 171(8), 4304-4310 (2003).
48. Miyahira AK, Shahangian A, Hwang S, Sun R, Cheng G. TANK-binding kinase-1 plays an important role during in vitro and in vivo type I IFN responses to DNA virus infections. J. Immunol. 182(4), 2248-2257 (2009).
49. Chessler AD, Ferreira LR, Chang TH, Fitzgerald KA, Burleigh BA. A novel IFN regulatory factor 3-dependent pathway activated by trypanosomes triggers IFN-β in macrophages and fibroblasts. J. Immunol. 181(11), 7917-7924 (2008).
50. Verpooten D, Ma Y, Hou S, Yan Z, He B. Control of TANK-binding kinase 1-mediated signaling by the γ134.5 protein of herpes simplex virus 1. J. Biol. Chem. 284(2), 1097-1105 (2009).
51. Fitzgerald KA, McWhirter SM, Faia KL et al. IKKε and A1 are essential components of the IRF3 signaling pathway. Nat. Immunol. 4(5), 491-496 (2003).
52. Shimada T, Kawai T, Takeda K et al. IKK-i, a novel lipopolysaccharide- inducible kinase that is related to IκB kinases. Int. Immunol. 11(8), 1357-1362 (1999).
53. Sankar S, Chan H, Romanow WJ, Li J, Bates RJ. IKK-i signals through IRF3 and NFκB to mediate the production of inflammatory cytokines. Cell Signal. 18(7), 982-993 (2006).
54. Hemmi H, Takeuchi O, Sato S et al. The roles of two IκB kinase-related kinases in lipopolysaccharide and double stranded RNA signaling and viral infection. J. Exp. Med. 199(12), 1641-1650 (2004).
55. McWhirter SM, Fitzgerald KA, Rosains J, Rowe DC, Golenbock DT, Maniatis T. IFN-regulatory factor 3-dependent gene expression is defective in A1-deficient mouse embryonic fibroblasts. Proc. Natl Acad. Sci. USA 101(1), 233-238 (2004).
56. Collins T, Williams A, Johnston GI et al. Structure and chromosomal location of the gene for endothelial-leukocyte adhesion molecule 1. J. Biol. Chem. 266(4), 2466-2473 (1991).
57. Kaiser WJ, Upton JW, Mocarski ES. Receptor-interacting protein homotypic interaction motif-dependent control of NF-κB activation via the DNA-dependent activator of IFN regulatory factors. J. Immunol. 181(9), 6427-6434 (2008).
58. Meylan E, Burns K, Hofmann K et al. RIP1 is an essential mediator of Toll-like receptor 3-induced NF-κB activation. Nat. Immunol. 5(5), 503-507 (2004). • Describes the involvement of RIP1 in DAI-dependent activation of NF-κB by DNA stimulation.
59. Kawai T, Takahashi K, Sato S et al. IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nat. Immunol. 6(10), 981-988 (2005).
60. Takeshita F, Ishii KJ, Kobiyama K et al. TRAF4 acts as a silencer in TLR-mediated signaling through the association with TRAF6 and TRIF. Eur. J. Immunol. 35(8), 2477-2485 (2005).
61. Takeshita F, Tanaka T, Matsuda T et al. Toll-like receptor adaptor molecules enhance DNA-raised adaptive immune responses against influenza and tumors through activation of innate immunity. J. Virol. 80(13), 6218-6224 (2006).
62. Sasaki S, Amara RR, Yeow WS, Pitha PM, Robinson HL. Regulation of DNA-raised immune responses by cotransfected interferon regulatory factors. J. Virol. 76(13), 6652-6659 (2002).
63. Bramson JL, Dayball K, Hall JR et al. Super-activated interferon-regulatory factors can enhance plasmid immunization. Vaccine 21(13-14), 1363-1370 (2003).