DNA Sensing across the Tree of Life

Trends in Immunology

Volumn 38, Issue 10, 2017, Pages 719-732

  Gallucci, Stefania ^a   Maffei, Massimo E ^b  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF TURIN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYRIBONUCLEASE; DNA; PATHOGEN ASSOCIATED MOLECULAR PATTERN; TOLL LIKE RECEPTOR 9; AIM2 PROTEIN, HUMAN; DNA BINDING PROTEIN; MB21D1 PROTEIN, HUMAN; NUCLEOTIDYLTRANSFERASE; PATTERN RECOGNITION RECEPTOR;

AUTOIMMUNITY; CYTOPLASM; DNA REPAIR; ENDOSOME; HUMAN; INVERTEBRATE; MAMMAL; NONHUMAN; PLANT; PROKARYOTE; REVIEW; ANIMAL; IMMUNOLOGY; INFECTION; INFLAMMATION; INNATE IMMUNITY; METABOLISM; SIGNAL TRANSDUCTION;

ANIMALS; DNA; DNA-BINDING PROTEINS; HUMANS; IMMUNITY, INNATE; INFECTION; INFLAMMATION; NUCLEOTIDYLTRANSFERASES; PLANTS; RECEPTORS, PATTERN RECOGNITION; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 9;

EID: 85028726053     PISSN: 14714906     EISSN: 14714981     Source Type: Journal    
DOI: 10.1016/j.it.2017.07.012     Document Type: Review

References (110)

1. Seong, S.Y., Matzinger, P., Hydrophobicity: an ancient damage-associated molecular pattern that initiates innate immune responses. Nat. Rev. Immunol. 4 (2004), 469–478.
2. Medzhitov, R., Janeway, C. Jr, Innate immune recognition: mechanisms and pathways. Immunol. Rev. 173 (2000), 89–97.
3. Choi, H.W., Klessig, D.F., DAMPs, MAMPs, and NAMPs in plant innate immunity. BMC Plant Biol., 16, 2016, 10.
4. Luecke, S., Paludan, S.R., Innate recognition of alphaherpesvirus DNA. Adv. Virus Res. 92 (2015), 63–100.
5. Watson, R.O., et al. The cytosolic sensor cGAS detects Mycobacterium tuberculosis DNA to induce Type I interferons and activate autophagy. Cell Host Microbe 17 (2015), 811–819.
6. Collins, A.C., et al. Cyclic GMP-AMP synthase is an innate immune DNA sensor for Mycobacterium tuberculosis. Cell Host Microbe 17 (2015), 820–828.
7. Wassermann, R., et al. Mycobacterium tuberculosis differentially activates cGAS- and inflammasome-dependent intracellular immune responses through ESX-1. Cell Host Microbe 17 (2015), 799–810.
8. Wen, F.S., et al. Extracellular DNA is required for root tip resistance to fungal infection. Plant Physiol. 151 (2009), 820–829.
9. Hartmann, G., Nucleic acid immunity. Adv. Immunol. 133 (2017), 121–169.
10. Krieg, A.M., et al. CpG motifs in bacterial DNA trigger direct B-cell activation. Nature 374 (1995), 546–549.
11. van der Oost, J., et al. Unravelling the structural and mechanistic basis of CRISPR-Cas systems. Nat. Rev. Microbiol. 12 (2014), 479–492.
12. Ledford, H., Five big mysteries about CRISPR's origins. Nature 541 (2017), 280–282.
13. Hemmi, H., et al. A Toll-like receptor recognizes bacterial DNA. Nature 408 (2000), 740–745.
14. Webster, B., et al. Cell–cell sensing of viral infection by plasmacytoid dendritic cells. J. Virol. 90 (2016), 10050–10053.
15. Hornung, V., et al. 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 (2002), 4531–4537.
16. Leadbetter, E.A., et al. Chromatin-IgG complexes activate B cells by dual engagement of IgM and Toll-like receptors. Nature 416 (2002), 603–607.
17. Zhang, Q., et al. Circulating mitochondrial DAMPs cause inflammatory responses to injury. Nature 464 (2010), 104–107.
18. Wilkins, H.M., et al. Mitochondrial lysates induce inflammation and Alzheimer's disease-relevant changes in microglial and neuronal cells. J. Alzheimers Dis. 45 (2015), 305–318.
19. Pohar, J., et al. Species-specific minimal sequence motif for oligodeoxyribonucleotides activating mouse TLR9. J. Immunol. 195 (2015), 4396–4405.
20. Coch, C., et al. Higher activation of TLR9 in plasmacytoid dendritic cells by microbial DNA compared with self-DNA based on CpG-specific recognition of phosphodiester DNA. J. Leukoc. Biol. 86 (2009), 663–670.
21. Barrat, F.J., et al. Nucleic acids of mammalian origin can act as endogenous ligands for Toll-like receptors and may promote systemic lupus erythematosus. J. Exp. Med. 202 (2005), 1131–1139.
22. Rommler, F., et al. Guanine-modified inhibitory oligonucleotides efficiently impair TLR7- and TLR9-mediated immune responses of human immune cells. PLoS One, 10, 2015, e0116703.
23. Xu, J., et al. STAT2 is required for TLR-induced murine dendritic cell activation and cross-presentation. J. Immunol. 197 (2016), 326–336.
24. Yan, N., et al. The cytosolic exonuclease TREX1 inhibits the innate immune response to human immunodeficiency virus type 1. Nat. Immunol. 11 (2010), 1005–1013.
25. Stetson, D.B., et al. Trex1 prevents cell-intrinsic initiation of autoimmunity. Cell 134 (2008), 587–598.
26. Wu, J., et al. Cyclic GMP-AMP is an endogenous second messenger in innate immune signaling by cytosolic DNA. Science 339 (2013), 826–830.
27. Sun, L., et al. Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway. Science 339 (2013), 786–791.
28. Tao, J.L., et al. cGAS-cGAMP-STING: the three musketeers of cytosolic DNA sensing and signaling. IUBMB Life 68 (2016), 858–870.
29. Ablasser, A., et al. Cell intrinsic immunity spreads to bystander cells via the intercellular transfer of cGAMP. Nature 503 (2013), 530–534.
30. Kato, K., et al. Cyclic GMP-AMP as an endogenous second messenger in innate immune signaling by cytosolic DNA. Annu. Rev. Biochem. 86 (2017), 541–566.
31. Margolis, S.R., et al. Evolutionary origins of cGAS-STING signaling. Trends Immunol., 2017, 10.1016/j.it.2017.03.004 Published online April 14, 2017.
32. Herzner, A.M., et al. Sequence-specific activation of the DNA sensor cGAS by Y-form DNA structures as found in primary HIV-1 cDNA. Nat. Immunol. 16 (2015), 1025–1033.
33. Gao, D., et al. Activation of cyclic GMP-AMP synthase by self-DNA causes autoimmune diseases. Proc. Natl. Acad. Sci. U. S. A. 112 (2015), E5699–E5705.
34. Gehrke, N., et al. Oxidative damage of DNA confers resistance to cytosolic nuclease TREX1 degradation and potentiates STING-dependent immune sensing. Immunity 39 (2013), 482–495.
35. Coban, C., et al. DNA vaccines: a simple DNA sensing matter?. Hum. Vaccin. Immunother. 9 (2013), 2216–2221.
36. Desmet, C.J., Ishii, K.J., Nucleic acid sensing at the interface between innate and adaptive immunity in vaccination. Nat. Rev. Immunol. 12 (2012), 479–491.
37. Gasser, S., et al. Sensing of dangerous DNA. Mech. Ageing Dev. 165 (2016), 33–46.
38. Hornung, V., et al. AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature 458 (2009), 514–518.
39. Almine, J.F., et al. IFI16 and cGAS cooperate in the activation of STING during DNA sensing in human keratinocytes. Nat. Commun., 8, 2017, 14392.
40. Jonsson, K.L., et al. IFI16 is required for DNA sensing in human macrophages by promoting production and function of cGAMP. Nat. Commun., 8, 2017, 14391.
41. Cridland, J.A., et al. The mammalian PYHIN gene family: phylogeny, evolution and expression. BMC Evol. Biol., 12, 2012, 140.
42. Corrales, L., et al. Antagonism of the STING pathway via activation of the AIM2 inflammasome by intracellular DNA. J. Immunol. 196 (2016), 3191–3198.
43. Kawane, K., et al. DNA degradation and its defects. Cold Spring Harb. Perspect. Biol., 6, 2014, a016394.
44. Lee-Kirsch, M.A., The type I interferonopathies. Annu. Rev. Med. 68 (2017), 297–315.
45. Yasutomo, K., et al. Mutation of DNASE1 in people with systemic lupus erythematosus. Nat. Genet. 28 (2001), 313–314.
46. Jog, N.R., et al. Caspase-activated DNase is required for maintenance of tolerance to lupus nuclear autoantigens. Arthritis Rheum. 64 (2012), 1247–1256.
47. Ho, S.S., et al. The DNA structure-specific endonuclease MUS81 mediates DNA sensor STING-dependent host rejection of prostate cancer cells. Immunity 44 (2016), 1177–1189.
48. Ishii, A., et al. Phylogenetic and expression analysis of amphibian Xenopus Toll-like receptors. Immunogenetics 59 (2007), 281–293.
49. Yeh, D.W., et al. Toll-like receptor 9 and 21 have different ligand recognition profiles and cooperatively mediate activity of CpG-oligodeoxynucleotides in zebrafish. Proc. Natl. Acad. Sci. U. S. A. 110 (2013), 20711–20716.
50. Tabeta, K., et al. The Unc93b1 mutation 3d disrupts exogenous antigen presentation and signaling via Toll-like receptors 3, 7 and 9. Nat. Immunol. 7 (2006), 156–164.
51. Keestra, A.M., et al. Chicken TLR21 is an innate CpG DNA receptor distinct from mammalian TLR9. J. Immunol. 185 (2010), 460–467.
52. Li, Y.W., et al. Molecular cloning of orange-spotted grouper (Epinephelus coioides) TLR21 and expression analysis post Cryptocaryon irritans infection. Fish Shellfish Immunol. 32 (2012), 476–481.
53. Taha-Abdelaziz, K., et al. Characterization of host responses induced by Toll-like receptor ligands in chicken cecal tonsil cells. Vet. Immunol. Immunopathol. 174 (2016), 19–25.
54. Priyam, M., et al. Tracing the evolutionary lineage of pattern recognition receptor homologues in vertebrates: an insight into reptilian immunity via de novo sequencing of the wall lizard splenic transcriptome. Vet. Immunol. Immunopathol. 172 (2016), 26–37.
55. Lahoud, M.H., et al. DEC-205 is a cell surface receptor for CpG oligonucleotides. Proc. Natl. Acad. Sci. U. S. A. 109 (2012), 16270–16275.
56. Gilmore, T.D., Wolenski, F.S., NF-kappa B: where did it come from and why?. Immunol. Rev. 246 (2012), 14–35.
57. Coscia, M.R., et al. Toll-like receptors: an overview from invertebrates to vertebrates. Invertebr. Surviv. J. 8 (2011), 210–226.
58. Buckley, K.M., Rast, J.P., Dynamic evolution on of Toll-like receptor multigene families in echinoderms. Front. Immunol., 3, 2012, 16.
59. Zhu, Z.H., et al. Evolutionary analysis of TLR9 genes reveals the positive selection of extant teleosts in Perciformes. Fish Shellfish Immunol. 35 (2013), 448–457.
60. Wang, P.H., et al. Nucleic acid-induced antiviral immunity in invertebrates: an evolutionary perspective. Dev. Comp. Immunol. 48 (2015), 291–296.
61. Wang, P.H., et al. Nucleic acid-induced antiviral immunity in shrimp. Antiviral Res. 99 (2013), 270–280.
62. Mazzoleni, S., et al. Inhibitory effects of extracellular self-DNA: a general biological process?. New Phytol. 206 (2015), 127–132.
63. Driouich, A., et al. Root border cells and secretions as critical elements in plant host defense. Curr. Opin. Plant Biol. 16 (2013), 489–495.
64. Ceccherini, M.T., et al. In-field detection and quantification of extracellular DNA. J. Plant Nutr. Soil Sci. 172 (2009), 626–629.
65. Mazzoleni, S., et al. Inhibitory and toxic effects of extracellular self-DNA in litter: a mechanism for negative plant-soil feedbacks?. New Phytol. 205 (2015), 1195–1210.
66. Mazzoleni, S., et al. New perspectives on the use of nucleic acids in pharmacological applications: inhibitory action of extracellular self-DNA in biological systems. Phytochem. Rev 13 (2014), 937–946.
67. Hawes, M.C., et al. Extracellular DNA: the tip of root defenses?. Plant Sci. 180 (2011), 741–745.
68. Duran-Flores, D., Heil, M., Growth inhibition by self-DNA: a phenomenon and its multiple explanations. New Phytol. 207 (2015), 482–485.
69. Duran-Flores, D., Heil, M., Damaged-self recognition in common bean (Phaseolus vulgaris) shows taxonomic specificity and triggers signaling via reactive oxygen species (ROS). Front. Plant Sci., 5, 2014, 585.
70. Veresoglou, S.D., et al. Self-DNA: a blessing in disguise?. New Phytol. 207 (2015), 488–490.
71. Huang, X.H., Plant perceptions of extracellular DNA and RNA. Mol. Plant 9 (2016), 956–960.
72. Duran-Flores, D., Heil, M., Sources of specificity in plant damaged-self recognition. Curr. Opin. Plant Biol. 32 (2016), 77–87.
73. Barbero, F., et al. Extracellular self-DNA (esDNA), but not heterologous plant or insect DNA (etDNA), induces plasma membrane depolarization and calcium signaling in Lima bean (Phaseolus lunatus) and maize (Zea mays). Int. J. Mol. Sci., 17, 2016, 14.
74. Gill, S.S., Tuteja, N., Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 48 (2010), 909–930.
75. Shokolenko, I., et al. Oxidative stress induces degradation of mitochondrial DNA. Nucleic Acids Res. 37 (2009), 2539–2548.
76. Liu, X.G., et al. CaMKII promotes TLR-triggered proinflammatory cytokine and type I interferon production by directly binding and activating TAK1 and IRF3 in macrophages. Blood 112 (2008), 4961–4970.
77. Zhang, W.J., et al. DNA-dependent activator of interferon-regulatory factors (DAI) promotes lupus nephritis by activating the calcium pathway. J. Biol. Chem. 288 (2013), 13534–13550.
78. Heil, M., Land, W.G., Danger signals – damaged-self recognition across the tree of life. Front. Plant Sci., 5, 2014, 16.
79. Scheer, J.M., Ryan, C.A., The systemin receptor SR160 from Lycopersicon peruvianum is a member of the LRR receptor kinase family. Proc. Natl. Acad. Sci. U. S. A. 99 (2002), 9585–9590.
80. Quesada, V., The roles of mitochondrial transcription termination factors (MTERFs) in plants. Physiol. Plant. 157 (2016), 389–399.
81. Gualberto, J.M., Newton, K.J., Plant mitochondrial genomes: dynamics and mechanisms of mutation. Annu. Rev. Plant Biol. 68 (2017), 225–252.
82. Preuten, T., et al. Fewer genes than organelles: extremely low and variable gene copy numbers in mitochondria of somatic plant cells. Plant J. 64 (2010), 948–959.
83. Oldenburg, D.J., et al. The amount and integrity of mtDNA in maize decline with development. Planta 237 (2013), 603–617.
84. Xu, J., et al. TLR ligands up-regulate Trex1 expression in murine conventional dendritic cells through type I interferon and NF-kappaB-dependent signaling pathways. J. Leukoc. Biol. 96 (2014), 93–103.
85. Wang, Y.T., et al. Inflammasome activation triggers caspase-1-mediated cleavage of cGAS to regulate responses to DNA virus infection. Immunity 46 (2017), 393–404.
86. Christensen, M.H., Paludan, S.R., Viral evasion of DNA-stimulated innate immune responses. Cell. Mol. Immunol. 14 (2017), 4–13.
87. Diner, B.A., et al. Viral DNA sensors IFI16 and cyclic GMP-AMP synthase possess distinct functions in regulating viral gene expression, immune defenses, and apoptotic responses during herpesvirus infection. Mbio, 7, 2016, 15.
88. Wu, J.J., et al. Inhibition of cGAS DNA sensing by a herpesvirus virion protein. Cell Host Microbe 18 (2015), 333–344.
89. Dutta, D., et al. BRCA1 regulates IFI16 mediated nuclear innate sensing of herpes viral DNA and subsequent induction of the innate inflammasome and interferon-beta responses. PLoS Pathog., 11, 2015, 47.
90. Sun, C.L., et al. Evasion of innate cytosolic DNA sensing by a gammaherpesvirus facilitates establishment of latent infection. J. Immunol. 194 (2015), 1819–1831.
91. Zevini, A., et al. Crosstalk between cytoplasmic RIG-I and STING sensing pathways. Trends Immunol. 38 (2017), 194–205.
92. Holm, C.K., et al. Influenza A virus targets a cGAS-independent STING pathway that controls enveloped RNA viruses. Nat. Commun., 7, 2016, 10680.
93. Rongvaux, A., et al. Apoptotic caspases prevent the induction of type I interferons by mitochondrial DNA. Cell 159 (2014), 1563–1577.
94. White, M.J., et al. Apoptotic caspases suppress mtDNA-induced STING-mediated type I IFN production. Cell 159 (2014), 1549–1562.
95. Julian, M.W., et al. Mitochondrial transcription factor A, an endogenous danger signal, promotes TNFalpha release via RAGE- and TLR9-responsive plasmacytoid dendritic cells. PLoS One, 8, 2013, e72354.
96. Lenert, P., et al. DNA-like class R inhibitory oligonucleotides (INH-ODNs) preferentially block autoantigen-induced B-cell and dendritic cell activation in vitro and autoantibody production in lupus-prone MRL-Fas(lpr/lpr) mice in vivo. Arthritis Res. Ther., 11, 2009, R79.
97. Murakami, Y., et al. The protective effect of the anti-Toll-like receptor 9 antibody against acute cytokine storm caused by immunostimulatory DNA. Sci. Rep., 7, 2017, 44042.
98. Tursi, S.A., et al. Bacterial amyloid curli acts as a carrier for DNA to elicit an autoimmune response via TLR2 and TLR9. PLoS Pathog., 13, 2017, e1006315.
99. Gallo, P.M., et al. Amyloid-DNA composites of bacterial biofilms stimulate autoimmunity. Immunity 42 (2015), 1171–1184.
100. Lood, C., et al. Neutrophil extracellular traps enriched in oxidized mitochondrial DNA are interferogenic and contribute to lupus-like disease. Nat. Med. 22 (2016), 146–153.
101. Caielli, S., et al. Oxidized mitochondrial nucleoids released by neutrophils drive type I interferon production in human lupus. J. Exp. Med. 213 (2016), 697–713.
102. Garcia-Romo, G.S., et al. Netting neutrophils are major inducers of type I IFN production in pediatric systemic lupus erythematosus. Sci. Transl. Med., 3, 2011, 73ra20.
103. Zipfel, C., Plant pattern-recognition receptors. Trends Immunol. 35 (2014), 345–351.
104. Zebelo, S.A., Maffei, M.E., Role of early signalling events in plant-insect interactions. J. Exp. Bot. 66 (2015), 435–448.
105. Cao, Y., et al. Mutations in FLS2 Ser-938 dissect signaling activation in FLS2-mediated Arabidopsis immunity. PLoS Pathog., 9, 2013, e1003313.
106. Kanchiswamy, C.N., et al. Regulation of Arabidopsis defense responses against Spodoptera littoralis by CPK-mediated calcium signaling. BMC Plant Biol., 10, 2010, 97.
107. Liu, W., et al. Novel insights into rice innate immunity against bacterial and fungal pathogens. Annu. Rev. Phytopathol. 52 (2014), 213–241.
108. Yang, D.H., et al. Silencing Nicotiana attenuata calcium-dependent protein kinases, CDPK4 and CDPK5, strongly up-regulates wound- and herbivory-induced jasmonic acid accumulations. Plant Physiol. 159 (2012), 1591–1607.
109. Arimura, G., et al. Recent advances in plant early signaling in response to herbivory. Int. J. Mol. Sci. 12 (2011), 3723–3739.
110. Arimura, G., Maffei, M.E., Calcium and secondary CPK signaling in plants in response to herbivore attack. Biochem. Biophys. Res. Commun. 400 (2010), 455–460.