Innate immune detection of microbial nucleic acids

Trends in Microbiology

Volumn 21, Issue 8, 2013, Pages 413-420

  Gürtler, Claudia ^a   Bowie, Andrew G ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

Antiviral immunity; Cytosolic DNA sensing; RIG I; STING; Toll like receptors

Indexed keywords

BACTERIAL RNA; BETA INTERFERON; DEAD BOX PROTEIN; DNA; HELICASE; INTERFERON; MICROBIAL NUCLEIC ACID; NUCLEIC ACID; PATTERN RECOGNITION RECEPTOR; RETINOIC ACID INDUCIBLE PROTEIN I; RNA; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG; VIRUS RNA;

AUTOIMMUNITY; CYTOKINE PRODUCTION; HUMAN; IMMUNE RESPONSE; INNATE IMMUNITY; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; RECEPTOR UPREGULATION; REVIEW; SIGNAL TRANSDUCTION;

ANTIVIRAL IMMUNITY; CYTOSOLIC DNA SENSING; RIG-I; STING; TOLL-LIKE RECEPTORS;

ANIMALS; AUTOIMMUNITY; HUMANS; IMMUNITY, INNATE; INTERFERON TYPE I; NUCLEIC ACIDS; RECEPTORS, PATTERN RECOGNITION; SIGNAL TRANSDUCTION;

EID: 84881027832     PISSN: 0966842X     EISSN: 18784380     Source Type: Journal    
DOI: 10.1016/j.tim.2013.04.004     Document Type: Review

References (85)

1. Janeway C.A. Approaching the asymptote? Evolution and revolution in immunology. Cold Spring Harb. Symp. Quant. Biol. 1989, 54:1-13.
2. Blander J.M., Sander L.E. Beyond pattern recognition: five immune checkpoints for scaling the microbial threat. Nat. Rev. Immunol. 2012, 12:215-225.
3. O'Neill L.A., Bowie A.G. The family of five: TIR-domain-containing adaptors in Toll-like receptor signalling. Nat. Rev. Immunol. 2007, 7:353-364.
4. Kawai T., Akira S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 2010, 11:373-384.
5. Weber F., et al. Double-stranded RNA is produced by positive-strand RNA viruses and DNA viruses but not in detectable amounts by negative-strand RNA viruses. J. Virol. 2006, 80:5059-5064.
6. Zhang S.Y., et al. TLR3 deficiency in patients with herpes simplex encephalitis. Science 2007, 317:1522-1527.
7. Reinert L.S., et al. TLR3 deficiency renders astrocytes permissive to herpes simplex virus infection and facilitates establishment of CNS infection in mice. J. Clin. Invest. 2012, 122:1368-1376.
8. Lafaille F.G., et al. Impaired intrinsic immunity to HSV-1 in human iPSC-derived TLR3-deficient CNS cells. Nature 2012, 491:769-773.
9. Lee J., et al. Activation of innate immunity is required for efficient nuclear reprogramming. Cell 2012, 151:547-558.
10. Yu P., et al. Nucleic acid-sensing Toll-like receptors are essential for the control of endogenous retrovirus viremia and ERV-induced tumors. Immunity 2012, 37:867-879.
11. Mankan A.K., Hornung V. Retroviral danger from within: TLR7 is in control. Immunity 2012, 37:763-766.
12. Hidmark A., et al. Cutting edge: TLR13 is a receptor for bacterial RNA. J. Immunol. 2012, 189:2717-2721.
13. Oldenburg M., et al. TLR13 recognizes bacterial 23S rRNA devoid of erythromycin resistance-forming modification. Science 2012, 337:1111-1115.
14. Li X.D., Chen Z.J. Sequence specific detection of bacterial 23S ribosomal RNA by TLR13. Elife 2012, 1:e00102.
15. Loo Y.M., Gale M. Immune signaling by RIG-I-like receptors. Immunity 2011, 34:680-692.
16. Pichlmair A., et al. RIG-I-mediated antiviral responses to single-stranded RNA bearing 5'-phosphates. Science 2006, 314:997-1001.
17. Hornung V., et al. 5'-Triphosphate RNA is the ligand for RIG-I. Science 2006, 314:994-997.
18. Kato H., et al. Length-dependent recognition of double-stranded ribonucleic acids by retinoic acid-inducible gene-I and melanoma differentiation-associated gene 5. J. Exp. Med. 2008, 205:1601-1610.
19. Marques J.T., et al. A structural basis for discriminating between self and nonself double-stranded RNAs in mammalian cells. Nat. Biotechnol. 2006, 24:559-565.
20. Rothenfusser S., et al. The RNA helicase Lgp2 inhibits TLR-independent sensing of viral replication by retinoic acid-inducible gene-I. J. Immunol. 2005, 175:5260-5268.
21. Satoh T., et al. LGP2 is a positive regulator of RIG-I- and MDA5-mediated antiviral responses. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:1512-1517.
22. Venkataraman T., et al. Loss of DExD/H box RNA helicase LGP2 manifests disparate antiviral responses. J. Immunol. 2007, 178:6444-6455.
23. Kowalinski E., et al. Structural basis for the activation of innate immune pattern-recognition receptor RIG-I by viral RNA. Cell 2011, 147:423-435.
24. Luo D., et al. Structural insights into RNA recognition by RIG-I. Cell 2011, 147:409-422.
25. Wu B., et al. Structural basis for dsRNA recognition, filament formation, and antiviral signal activation by MDA5. Cell 2013, 152:276-289.
26. Schroder M. Human DEAD-box protein 3 has multiple functions in gene regulation and cell cycle control and is a prime target for viral manipulation. Biochem. Pharmacol. 2010, 79:297-306.
27. Oshiumi H., et al. DEAD/H BOX 3 (DDX3) helicase binds the RIG-I adaptor IPS-1 to up-regulate IFN-beta-inducing potential. Eur. J. Immunol. 2010, 40:940-948.
28. Miyashita M., et al. DDX60, a DEXD/H box helicase, is a novel antiviral factor promoting RIG-I-like receptor-mediated signaling. Mol. Cell. Biol. 2011, 31:3802-3819.
29. Zhang Z., et al. DHX9 pairs with IPS-1 to sense double-stranded RNA in myeloid dendritic cells. J. Immunol. 2011, 187:4501-4508.
30. Zhang Z., et al. DDX1, DDX21, and DHX36 helicases form a complex with the adaptor molecule TRIF to sense dsRNA in dendritic cells. Immunity 2011, 34:866-878.
31. Hemmi H., et al. A Toll-like receptor recognizes bacterial DNA. Nature 2000, 408:740-745.
32. Okabe Y., et al. Toll-like receptor-independent gene induction program activated by mammalian DNA escaped from apoptotic DNA degradation. J. Exp. Med. 2005, 202:1333-1339.
33. Yasuda K., et al. Macrophage activation by a DNA/cationic liposome complex requires endosomal acidification and TLR9-dependent and -independent pathways. J. Leukoc. Biol. 2005, 77:71-79.
34. Yasuda K., et al. Endosomal translocation of vertebrate DNA activates dendritic cells via TLR9-dependent and -independent pathways. J. Immunol. 2005, 174:6129-6136.
35. Ishii K.J., et al. A Toll-like receptor-independent antiviral response induced by double-stranded B-form DNA. Nat. Immunol. 2006, 7:40-48.
36. Stetson D.B., Medzhitov R. Recognition of cytosolic DNA activates an IRF3-dependent innate immune response. Immunity 2006, 24:93-103.
37. Ishii K.J., et al. TANK-binding kinase-1 delineates innate and adaptive immune responses to DNA vaccines. Nature 2008, 451:725-729.
38. Ishikawa H., Barber G.N. STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling. Nature 2008, 455:674-678.
39. Zhong B., et al. The adaptor protein MITA links virus-sensing receptors to IRF3 transcription factor activation. Immunity 2008, 29:538-550.
40. Sun W., et al. ERIS, an endoplasmic reticulum IFN stimulator, activates innate immune signaling through dimerization. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:8653-8658.
41. Ishikawa H., et al. STING regulates intracellular DNA-mediated, type I interferon-dependent innate immunity. Nature 2009, 461:788-792.
42. Tanaka Y., Chen Z.J. STING specifies IRF3 phosphorylation by TBK1 in the cytosolic DNA signaling pathway. Sci. Signal. 2012, 5:ra20.
43. Takaoka A., et al. DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune response. Nature 2007, 448:501-505.
44. Wang Z., et al. Regulation of innate immune responses by DAI (DLM-1/ZBP1) and other DNA-sensing molecules. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:5477-5482.
45. Ablasser A., et al. RIG-I-dependent sensing of poly(dA:dT) through the induction of an RNA polymerase III-transcribed RNA intermediate. Nat. Immunol. 2009, 10:1065-1072.
46. Chiu Y.H., et al. RNA polymerase III detects cytosolic DNA and induces type I interferons through the RIG-I pathway. Cell 2009, 138:576-591.
47. Cheng G., et al. Double-stranded DNA and double-stranded RNA induce a common antiviral signaling pathway in human cells. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:9035-9040.
48. Kim T., et al. Aspartate-glutamate-alanine-histidine box motif (DEAH)/RNA helicase A helicases sense microbial DNA in human plasmacytoid dendritic cells. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:15181-15186.
49. Zhang Z., et al. The helicase DDX41 senses intracellular DNA mediated by the adaptor STING in dendritic cells. Nat. Immunol. 2011, 12:959-965.
50. Unterholzner L., et al. IFI16 is an innate immune sensor for intracellular DNA. Nat. Immunol. 2010, 11:997-1004.
51. Muruve D.A., et al. The inflammasome recognizes cytosolic microbial and host DNA and triggers an innate immune response. Nature 2008, 452:103-107.
52. Hornung V., et al. AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature 2009, 458:514-518.
53. Fernandes-Alnemri T., et al. AIM2 activates the inflammasome and cell death in response to cytoplasmic DNA. Nature 2009, 458:509-513.
54. Burckstummer T., et al. An orthogonal proteomic-genomic screen identifies AIM2 as a cytoplasmic DNA sensor for the inflammasome. Nat. Immunol. 2009, 10:266-272.
55. Roberts T.L., et al. HIN-200 proteins regulate caspase activation in response to foreign cytoplasmic DNA. Science 2009, 323:1057-1060.
56. Keating S.E., et al. Cytosolic DNA sensors regulating type I interferon induction. Trends Immunol. 2011, 32:574-581.
57. Jin T., et al. Structures of the HIN domain:DNA complexes reveal ligand binding and activation mechanisms of the AIM2 inflammasome and IFI16 receptor. Immunity 2012, 36:561-571.
58. Kerur N., et al. IFI16 acts as a nuclear pathogen sensor to induce the inflammasome in response to Kaposi sarcoma-associated herpesvirus infection. Cell Host Microbe 2011, 9:363-375.
59. Li T., et al. Acetylation modulates cellular distribution and DNA sensing ability of interferon-inducible protein IFI16. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:10558-10563.
60. Orzalli M.H., et al. Nuclear IFI16 induction of IRF-3 signaling during herpesviral infection and degradation of IFI16 by the viral ICP0 protein. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:E3008-E3017.
61. McWhirter S.M., et al. A host type I interferon response is induced by cytosolic sensing of the bacterial second messenger cyclic-di-GMP. J. Exp. Med. 2009, 206:1899-1911.
62. Sauer J.D., et al. The N-ethyl-N-nitrosourea-induced Goldenticket mouse mutant reveals an essential function of Sting in the in vivo interferon response to Listeria monocytogenes and cyclic dinucleotides. Infect. Immun. 2011, 79:688-694.
63. Burdette D.L., et al. STING is a direct innate immune sensor of cyclic di-GMP. Nature 2011, 478:515-518.
64. Yin Q., et al. Cyclic di-GMP sensing via the innate immune signaling protein STING. Mol. Cell 2012, 46:735-745.
65. Ouyang S., et al. Structural analysis of the STING adaptor protein reveals a hydrophobic dimer interface and mode of cyclic di-GMP binding. Immunity 2012, 36:1073-1086.
66. Huang Y.H., et al. The structural basis for the sensing and binding of cyclic di-GMP by STING. Nat. Struct. Mol. Biol. 2012, 19:728-730.
67. Shang G., et al. Crystal structures of STING protein reveal basis for recognition of cyclic di-GMP. Nat. Struct. Mol. Biol. 2012, 19:725-727.
68. Shu C., et al. Structure of STING bound to cyclic di-GMP reveals the mechanism of cyclic dinucleotide recognition by the immune system. Nat. Struct. Mol. Biol. 2012, 19:722-724.
69. Monroe K.M., et al. Induction of type I interferons by bacteria. Cell. Microbiol. 2010, 12:881-890.
70. Manzanillo P.S., et al. Mycobacterium tuberculosis activates the DNA-dependent cytosolic surveillance pathway within macrophages. Cell Host Microbe 2012, 11:469-480.
71. Wu J., et al. Cyclic GMP-AMP is an endogenous second messenger in innate immune signaling by cytosolic DNA. Science 2013, 339:826-830.
72. Sun L., et al. Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway. Science 2013, 339:786-791.
73. Fernandes-Alnemri T., et al. The AIM2 inflammasome is critical for innate immunity to Francisella tularensis. Nat. Immunol. 2010, 11:385-393.
74. Saiga H., et al. Critical role of AIM2 in Mycobacterium tuberculosis infection. Int. Immunol. 2012, 24:637-644.
75. Zhang X., et al. Cutting edge: Ku70 is a novel cytosolic DNA sensor that induces type III rather than type I IFN. J. Immunol. 2011, 186:4541-4545.
76. Napirei M., et al. Features of systemic lupus erythematosus in Dnase1-deficient mice. Nat. Genet. 2000, 25:177-181.
77. Yasutomo K., et al. Mutation of DNASE1 in people with systemic lupus erythematosus. Nat. Genet. 2001, 28:313-314.
78. Yoshida H., et al. Lethal anemia caused by interferon-beta produced in mouse embryos carrying undigested DNA. Nat. Immunol. 2005, 6:49-56.
79. Stetson D.B., et al. Trex1 prevents cell-intrinsic initiation of autoimmunity. Cell 2008, 134:587-598.
80. Gall A., et al. Autoimmunity initiates in nonhematopoietic cells and progresses via lymphocytes in an interferon-dependent autoimmune disease. Immunity 2012, 36:120-131.
81. Zhang Z., et al. The E3 ubiquitin ligase TRIM21 negatively regulates the innate immune response to intracellular double-stranded DNA. Nat. Immunol. 2012, 14:172-178.
82. Bowie A.G., Unterholzner L. Viral evasion and subversion of pattern-recognition receptor signalling. Nat. Rev. Immunol. 2008, 8:911-922.
83. Rebsamen M., et al. DAI/ZBP1 recruits RIP1 and RIP3 through RIP homotypic interaction motifs to activate NF-kappaB. EMBO Rep. 2009, 10:916-922.
84. Cristea I.M., et al. Human cytomegalovirus pUL83 stimulates activity of the viral immediate-early promoter through its interaction with the cellular IFI16 protein. J. Virol. 2010, 84:7803-7814.
85. Johnston J.B., et al. A poxvirus-encoded pyrin domain protein interacts with ASC-1 to inhibit host inflammatory and apoptotic responses to infection. Immunity 2005, 23:587-598.