Cellular sensing of viral DNA and viral evasion mechanisms

Annual Review of Microbiology

Volumn 68, Issue , 2014, Pages 477-492

  Orzalli, Megan H ^a   Knipe, David M ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

CGAS; DNA sensors; Epigenetics; Herpes simplex virus; Human immunodeficiency virus; IFI16; Innate responses; Intrinsic resistance; Vaccinia virus

Indexed keywords

BETA INTERFERON; CYTOKINE; DEXD H BOX HELICASE; DNA DEPENDENT PROTEIN KINASE; DNA DIRECTED RNA POLYMERASE III; HELICASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INFLAMMASOME; PEPTIDES AND PROTEINS; PROTEIN CGAS; PROTEIN IRF 3; PROTEIN PYHIN; PROTEIN STING; UNCLASSIFIED DRUG; VIRUS DNA; DNA VIRUS;

CYTOSOL; EPIGENETICS; HERPES SIMPLEX VIRUS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; LENTIVIRINAE; NONHUMAN; POXVIRUS; PROTEIN EXPRESSION; REVIEW; VACCINIA VIRUS; VIRUS CELL INTERACTION; VIRUS INFECTION; ANIMAL; DNA VIRUS INFECTION; GENETICS; HOST PATHOGEN INTERACTION; IMMUNE EVASION; IMMUNOLOGY; PHYSIOLOGY; VIROLOGY;

ANIMALS; DNA VIRUS INFECTIONS; DNA VIRUSES; DNA, VIRAL; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNE EVASION;

EID: 84907515304     PISSN: 00664227     EISSN: 15453251     Source Type: Book Series    
DOI: 10.1146/annurev-micro-091313-103409     Document Type: Review

References (83)

1. Abe T, Harashima A, Xia T, Konno H, Konno K, et al. 2013. STING recognition of cytoplasmic DNA instigates cellular defense. Mol. Cell 50:5-15
2. Abend JR, Low JA, Imperiale MJ. 2010. Global effects of BKV infection on gene expression in human primary kidney epithelial cells. Virology 397:73-79
3. Ablasser A, Bauernfeind F, Hartmann G, Latz E, Fitzgerald KA, Hornung V. 2009. RIG-I-dependent sensing of poly(dA:dT) through the induction of an RNA polymerase III-transcribed RNA intermediate. Nat. Immunol. 10:1065-72
4. Ablasser A, Hornung V. 2013. DNA sensing unchained. Cell Res. 23:585-87
5. AblasserA, Schmid-Burgk JL, Hemmerling I,Horvath GL, Schmidt T, et al. 2013. Cell intrinsic immunity spreads to bystander cells via the intercellular transfer of cGAMP. Nature 503:530-34
6. Ansari MA, Singh VV, Dutta S, Veettil MV, Dutta D, et al. 2013. Constitutive interferon-inducible protein 16-inflammasome activation during Epstein-Barr virus latency I, II, and III in B and epithelial cells. J. Virol. 87:8606-23
7. Bafica A, Scanga CA, Feng CG, Leifer C, Cheever A, Sher A. 2005. TLR9 regulates Th1 responses and cooperates with TLR2 in mediating optimal resistance to Mycobacterium tuberculosis. J. Exp. Med. 202:1715-24
8. Boutell C, Everett RD. 2013. Regulation of alphaherpesvirus infections by the ICP0 family of proteins. J. Gen. Virol. 94:465-81
9. Brunette RL, Young JM, Whitley DG, Brodsky IE,Malik HS, Stetson DB. 2012. Extensive evolutionary and functional diversity among mammalian AIM2-like receptors. J. Exp. Med. 209:1969-83
10. Bunting SF, Nussenzweig A. 2013. End-joining, translocations and cancer. Nat. Rev. Cancer 13:443-54
11. Cereghini S, Yaniv M. 1984. Assembly of transfected DNA into chromatin: structural changes in the origin-promoter-enhancer region upon replication. EMBO J. 3:1243-53
12. Chiu YH, Macmillan JB, Chen ZJ. 2009. RNA polymerase III detects cytosolic DNA and induces type I interferons through the RIG-I pathway. Cell 138:576-91
13. Cliffe AR, Knipe DM. 2008. Herpes simplex virus ICP0 promotes both histone removal and acetylation on viral DNA during lytic infection. J. Virol. 82:12030-38
14. Conrady CD, Zheng M, Fitzgerald KA, Liu C, Carr DJ. 2012. Resistance to HSV-1 infection in the epithelium resides with the novel innate sensor, IFI-16. Mucosal Immunol. 5:173-83
15. Cristea IM, Moorman NJ, Terhune SS, Cuevas CD, OKeefe ES, et al. 2010. Human cytomegalovirus pUL83 stimulates activity of the viral immediate-early promoter through its interaction with the cellular IFI16 protein. J. Virol. 84:7803-14
16. Cuchet-Lourenco D, Anderson G, Sloan E, Orr A, Everett RD. 2013. The viral ubiquitin ligase ICP0 is neither sufficient nor necessary for degradation of the cellular DNA sensor IFI16 during herpes simplex virus 1 infection. J. Virol. 87:13422-32
17. Eidson KM, Hobbs WE, Manning BJ, Carlson P, DeLuca NA. 2002. Expression of herpes simplex virus ICP0 inhibits the induction of interferon-stimulated genes by viral infection. J. Virol. 76:2180-91
18. Ferguson BJ, Mansur DS, Peters NE, Ren H, Smith GL. 2012. DNA-PK is a DNA sensor for IRF-3- dependent innate immunity. eLife 1:e00047
19. Fernandes-Alnemri T, Yu JW, Datta P, Wu J, Alnemri ES. 2009. AIM2 activates the inflammasome and cell death in response to cytoplasmic DNA. Nature 458:509-13
20. GaoD,Wu J,Wu YT, Du F, Aroh C, et al. 2013. Cyclic GMP-AMP synthase is an innate immune sensor of HIV and other retroviruses. Science 341:903-6
21. Gariano GR, Delloste V, Bronzini M, Gatti D, Luganini A, et al. 2012. The intracellular DNA sensor IFI16 gene acts as restriction factor for human cytomegalovirus replication. PLoS Pathog. 8:e1002498
22. Helenius A. 2013. Virus entry and uncoating. See 41, chapter 4
23. Hemmi H, Takeuchi O, Kawai T, Kaisho T, Sato S, et al. 2000. A Toll-like receptor recognizes bacterial DNA. Nature 408:740-45
24. Hochrein H, Schlatter B, OKeeffe M, Wagner C, Schmitz F, et al. 2004. Herpes simplex virus type-1 induces IFN-α production via Toll-like receptor 9-dependent and -independent pathways. Proc. Natl. Acad. Sci. USA 101:11416-21
25. Horan KA, Hansen K, Jakobsen MR, Holm CK, Soby S, et al. 2013. Proteasomal degradation of herpes simplex virus capsids in macrophages releases DNA to the cytosol for recognition by DNA sensors. J. Immunol. 190:2311-19
26. Hornung V, Ablasser A, Charrel-Dennis M, Bauernfeind F, Horvath G, et al. 2009. AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature 458:514-18
27. Howe JG, Shu MD. 1989. Epstein-Barr virus small RNA (EBER) genes: unique transcription units that combine RNA polymerase II and III promoter elements. Cell 57:825-34
28. Ishii KJ, Coban C, Kato H, Takahashi K, Torii Y, et al. 2006. A Toll-like receptor-independent antiviral response induced by double-stranded B-form DNA. Nat. Immunol. 7:40-48
29. IshikawaH, BarberGN. 2008. STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling. Nature 455:674-78
30. Iwasaki A, Medzhitov R. 2013. Innate responses to viral infections. See 41, chapter 8
31. Jakobsen MR, Bak RO, Andersen A, Berg RK, Jensen SB, et al. 2013. IFI16 senses DNA forms of the lentiviral replication cycle and controls HIV-1 replication. Proc. Natl. Acad. Sci. USA 110:E4571-80
32. Jin T, Perry A, Jiang J, Smith P, Curry JA, et al. 2012. Structures of the HIN domain: DNA complexes reveal ligand binding and activationmechanisms of the AIM2 inflammasome and IFI16 receptor. Immunity 36:561-71
33. Johnson KE, Chikoti L, Chandran B. 2013. Herpes simplex virus 1 infection induces activation and subsequent inhibition of the IFI16 and NLRP3 inflammasomes. J. Virol. 87:5005-18
34. Jones JW, Kayagaki N, Broz P, Henry T, Newton K, et al. 2010. Absent in melanoma 2 is required for innate immune recognition of Francisella tularensis. Proc. Natl. Acad. Sci. USA 107:9771-76
35. Kagan JC. 2012. Signaling organelles of the innate immune system. Cell 151:1168-78
36. Karpova AY, Ronco LV, Howley PM. 2001. Functional characterization of interferon regulatory factor 3a (IRF-3a), an alternative splice isoform of IRF-3. Mol. Cell. Biol. 21:4169-76
37. Kassim SH, Rajasagi NK, Zhao X, Chervenak R, Jennings SR. 2006. In vivo ablation of CD11c-positive dendritic cells increases susceptibility to herpes simplex virus type 1 infection and diminishes NK and T-cell responses. J. Virol. 80:3985-93
38. Kerur N, Veettil MV, Sharma-Walia N, Bottero V, Sadagopan S, et al. 2011. IFI16 acts as a nuclear pathogen sensor to induce the inflammasome in response to Kaposi Sarcoma-associated herpesvirus infection. Cell Host Microbe 9:363-75
39. Kim T, Pazhoor S, BaoM, Zhang Z, Hanabuchi S, et al. 2010. Aspartate-glutamate-alanine-histidine box motif (DEAH)/RNA helicase A helicases sense microbial DNA in human plasmacytoid dendritic cells. Proc. Natl. Acad. Sci. USA 107:15181-86
40. Knipe DM, Cliffe A. 2008. Chromatin control of herpes simplex virus lytic and latent infection. Nat. Rev. Microbiol. 6:211-21
41. Knipe DM, Howley P, eds. 2013. Fields Virology. Philadelphia: LippincottWilliamsWilkins. 6thed.
42. Krug A, Luker GD, BarchetW, Leib DA, Akira S, Colonna M. 2004. Herpes simplex virus type 1 activates murine natural interferon-producing cells through Toll-like receptor 9. Blood 103:1433-37
43. Li T, Chen J, Cristea IM. 2013. Human cytomegalovirus tegument protein pUL83 inhibits IFI16- mediated DNA sensing for immune evasion. Cell Host Microbe 14:591-99
44. Li T, Diner BA, Chen J, Cristea IM. 2012. Acetylation modulates cellular distribution and DNA sensing ability of interferon-inducible protein IFI16. Proc. Natl. Acad. Sci. USA 109:10558-63
45. Li XD, Wu J, Gao D, Wang H, Sun L, Chen ZJ. 2013. Pivotal roles of cGAS-cGAMP signaling in antiviral defense and immune adjuvant effects. Science 341:1390-94
46. McWhirter SM, Barbalat R, Monroe KM, Fontana MF, Hyodo M, et al. 2009. A host type I interferon response is induced by cytosolic sensing of the bacterial second messenger cyclic-di-GMP. J. Exp. Med. 206:1899-911
47. Melchjorsen J, Rintahaka J, Søby S, Horan KA, Poltajainen A, et al. 2010. Early innate recognition of herpes simplex virus in human primary macrophages is mediated via the MDA5/MAVS-dependent and MDA5/MAVS/RNA polymerase III-independent pathways. J. Virol. 84:11350-58
48. Monroe KM, McWhirter SM, Vance RE. 2009. Identification of host cytosolic sensors and bacterial factors regulating the type I interferon response to Legionella pneumophila. PLoS Pathog. 5:e1000665
49. Monroe KM, Yang Z, Johnson JR,Geng X,DoitshG, et al. 2013. IFI16DNA sensor is required for death of lymphoid CD4 T cells abortively infected with HIV. Science 343:428-32
50. Morrone SR, Wang T, Constantoulakis LM, Hooy RM, Delannoy MJ, Sohn J. 2014. Cooperative assembly of IFI16 filaments on dsDNA provides insights into host defense strategy. Proc. Natl. Acad. Sci. USA 111:E62-71
51. Moss B. 2013. Poxviridae. See 41, chapter 66
52. Mossman KL, Macgregor PF, Rozmus JJ, Goryachev AB, Edwards AM, Smiley JR. 2001. Herpes simplex virus triggers and then disarms a host antiviral response. J. Virol. 75:750-58
53. Muruve DA, Petrilli V, ZaissAK, WhiteLR, Clark SA, et al. 2008. The inflammasome recognizes cytosolic microbial and host DNA and triggers an innate immune response. Nature 452:103-7
54. Napetschnig J,Wu H. 2013. Molecular basis of NF-κB signaling. Annu. Rev. Biophys. 42:443-68
55. Oh J, Fraser NW. 2008. Temporal association of the herpes simplex virus genome with histone proteins during a lytic infection. J. Virol. 82:3530-37
56. OrzalliMH,Conwell SE, Berrios C, DeCaprio JA, KnipeDM. 2013. Nuclear interferon-inducible protein 16 promotes silencing of herpesviral and transfected DNA. Proc. Natl. Acad. Sci. USA 110:E4492-501
57. OrzalliMH,DeLucaNA, KnipeDM. 2012. Nuclear IFI16 induction of IRF-3 signaling during herpesviral infection and degradation of IFI16 by the viral ICP0 protein. Proc. Natl. Acad. Sci. USA 109:E3008-17
58. Paludan SR, Bowie AG. 2013. Immune sensing of DNA. Immunity 38:870-80
59. Parvatiyar K, Zhang Z, Teles RM, Ouyang S, Jiang Y, et al. 2012. The helicase DDX41 recognizes the bacterial secondary messengers cyclic di-GMP and cyclic di-AMP to activate a type I interferon immune response. Nat. Immunol. 13:1155-61
60. Peters NE, Ferguson BJ,MazzonM, Fahy AS, Krysztofinska E, et al. 2013. Amechanism for the inhibition of DNA-PK-mediated DNA sensing by a virus. PLoS Pathog. 9:e1003649
61. Pham TH, Kwon KM, Kim YE, Kim KK, Ahn JH. 2013. DNA sensing-independent inhibition of herpes simplex virus 1 replication by DAI/ZBP1. J. Virol. 87:3076-86
62. Preston CM, Harman AN, Nicholl MJ. 2001. Activation of interferon response factor-3 in human cells infected with herpes simplex virus type 1 or human cytomegalovirus. J. Virol. 75:8909-16
63. Rasaiyaah J, Tan CP, Fletcher AJ, Price AJ, Blondeau C, et al. 2013. HIV-1 evades innate immune recognition through specific cofactor recruitment. Nature 503:402-5
64. Rathinam VA, Jiang Z, Waggoner SN, Sharma S, Cole LE, et al. 2010. The AIM2 inflammasome is essential for host defense against cytosolic bacteria and DNA viruses. Nat. Immunol. 11:395-402
65. Rathinam VA, Vanaja SK, Fitzgerald KA. 2012. Regulation of inflammasome signaling. Nat. Immunol. 13:333-42
66. Saitoh T, Fujita N, Hayashi T, Takahara K, Satoh T, et al. 2009. Atg9a controls dsDNA-driven dynamic translocation of STING and the innate immune response. Proc. Natl. Acad. Sci. USA 106:20842-46
67. Schoggins JW, Macduff DA, Imanaka N, Gainey MD, Shrestha B, et al. 2013. Pan-viral specificity of IFN-induced genes reveals new roles for cGAS in innate immunity. Nature 505:691-95
68. Singh VV, Kerur N, Bottero V, Dutta S, Chakraborty S, et al. 2013. Kaposis sarcoma-associated herpesvirus latency in endothelial and B cells activates gamma interferon-inducible protein 16-mediated inflammasomes. J. Virol. 87:4417-31
69. Sorensen LN, Reinert LS, Malmgaard L, Bartholdy C, Thomsen AR, Paludan SR. 2008. TLR2 and TLR9 synergistically control herpes simplex virus infection in the brain. J. Immunol. 181:8604-12
70. Stark GR, Darnell JE Jr. 2012. The JAK-STAT pathway at twenty. Immunity 36:503-14
71. Sun L,Wu J, Du F, Chen X, Chen ZJ. 2012. Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway. Science 339:786-91
72. Takaoka A,Wang Z, ChoiMK, YanaiH,Negishi H, et al. 2007. DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune response. Nature 448:501-5
73. Tanaka Y, Chen ZJ. 2012. STING specifies IRF3 phosphorylation by TBK1 in the cytosolic DNA signaling pathway. Sci. Signaling 5:ra20
74. Unterholzner L. 2013. The interferon response to intracellular DNA: why so many receptors? Immunobiology 218:1312-21
75. Unterholzner L, Keating SE, Baran M, Horan KA, Jensen SB, et al. 2010. IFI16 is an innate immune sensor for intracellular DNA. Nat. Immunol. 11:997-1004
76. Upton JW, Kaiser WJ, Mocarski ES. 2012. DAI/ZBP1/DLM-1 complexes with RIP3 to mediate virusinduced programmed necrosis that is targeted bymurine cytomegalovirus vIRA. Cell HostMicrobe 11:290-97
77. Veeranki S, Choubey D. 2012. Interferon-inducible p200-family protein IFI16, an innate immune sensor for cytosolic and nuclear double-stranded DNA: regulation of subcellular localization. Mol. Immunol. 49:567-71
78. Wathelet MG, Berr PM, Huez GA. 1992. Regulation of gene expression by cytokines and virus in human cells lacking the type-I interferon locus. Eur. J. Biochem. 206:901-10
79. Watson RO,Manzanillo PS,Cox JS. 2012. Extracellular M. tuberculosisDNAtargets bacteria for autophagy by activating the host DNA-sensing pathway. Cell 150:803-15
80. Woodward JJ, Iavarone AT, Portnoy DA. 2010. c-di-AMP secreted by intracellular Listeria monocytogenes activates a host type I interferon response. Science 328:1703-5
81. Wu J, Sun L, Chen X, Du F, Shi H, et al. 2012. Cyclic GMP-AMP is an endogenous second messenger in innate immune signaling by cytosolic DNA. Science 339:826-30
82. Yan N, Regalado-Magdos AD, Stiggelbout B, Lee-Kirsch MA, Lieberman J. 2010. The cytosolic exonuclease TREX1 inhibits the innate immune response to human immunodeficiency virus type 1. Nat. Immunol. 11:1005-13
83. Zhang Z, Yuan B, Bao M, Lu N, Kim T, Liu YJ. 2011. The helicase DDX41 senses intracellular DNA mediated by the adaptor STING in dendritic cells. Nat. Immunol. 12:959-65