The emerging roles of the STING adaptor protein in immunity and diseases

Immunology

Volumn 147, Issue 3, 2016, Pages 285-291

  Liu, Xing ^a,b   Wang, Chen ^a  

^a INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

^b BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

STING; Autoimmunity; Cancer immunology; Cytosolic DNA; Innate immunity; Type I interferon

Indexed keywords

ADAPTOR PROTEIN; AUTOCRINE MOTILITY FACTOR RECEPTOR; BINDING PROTEIN; DINUCLEOTIDE; DNA; ENDOPLASMIC RETICULUM RESIDENT PROTEIN STIMULATOR OF INTERFERON GENES; EXODEOXYRIBONUCLEASE III; INTERFERON RECEPTOR; INTERFERON REGULATORY FACTOR 3; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; LIGASE; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR; PROTEIN; PROTEIN NLRC3; PROTEIN ZDHHC1; RETINOIC ACID INDUCIBLE PROTEIN I; RING FINGER PROTEIN; RING FINGER PROTEIN 5; TANK BINDING KINASE 1; TUMOR NECROSIS FACTOR ALPHA; UBIQUITIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; MEMBRANE PROTEIN; MPYS PROTEIN, HUMAN;

AICARDI GOUTIERES SYNDROME; ANTIVIRAL ACTIVITY; ARTICLE; AUTOIMMUNE DISEASE; AUTOIMMUNITY; CANCER IMMUNOLOGY; CARDIOMYOPATHY; DISEASES; HEART FAILURE; HUMAN; IMMUNE RESPONSE; IMMUNITY; INNATE IMMUNITY; MYOCARDITIS; NEOPLASM; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RHEUMATOID ARTHRITIS; SYSTEMIC LUPUS ERYTHEMATOSUS; VIRUS INFECTION; IMMUNOLOGY;

HUMANS; IMMUNITY, INNATE; MEMBRANE PROTEINS;

EID: 84958618339     PISSN: 00192805     EISSN: 13652567     Source Type: Journal    
DOI: 10.1111/imm.12561     Document Type: Article

References (88)

1. Schenten D, Medzhitov R. The control of adaptive immune responses by the innate immune system. Adv Immunol 2011; 109:87-124.
2. Takeuchi O, Akira S. Pattern recognition receptors and inflammation. Cell 2010; 140:805-20.
3. Akira S, Uematsu S, Takeuchi O. Pathogen recognition and innate immunity. Cell 2006; 124:783-801.
4. Loo YM, Gale M Jr. Immune signaling by RIG-I-like receptors. Immunity 2011; 34:680-92.
5. Nakhaei P, Genin P, Civas A, Hiscott J. RIG-I-like receptors: sensing and responding to RNA virus infection. Semin Immunol 2009; 21:215-22.
6. Weber M, Weber F. RIG-I-like receptors and negative-strand RNA viruses: RLRly bird catches some worms. Cytokine Growth Factor Rev 2014; 25:621-8.
7. Oshiumi H, Miyashita M, Okamoto M, Morioka Y, Okabe M, Matsumoto M, et al. DDX60 Is involved in RIG-I-dependent and independent antiviral responses, and its function is attenuated by virus-induced EGFR activation. Cell Rep 2015; 11:1193-207.
8. Belgnaoui SM, Paz S, Hiscott J. Orchestrating the interferon antiviral response through the mitochondrial antiviral signaling (MAVS) adapter. Curr Opin Immunol 2011; 23:564-72.
9. Paludan SR, Bowie AG. Immune sensing of DNA. Immunity 2013; 38:870-80.
10. Hemmi H, Takeuchi O, Kawai T, Kaisho T, Sato S, Sanjo H, et al. A Toll-like receptor recognizes bacterial DNA. Nature 2000; 408:740-5.
11. Unterholzner L, Keating SE, Baran M, Horan KA, Jensen SB, Sharma S, et al. IFI16 is an innate immune sensor for intracellular DNA. Nat Immunol 2010; 11:997-1004.
12. Zhang Z, Yuan B, Bao M, Lu N, Kim T, Liu YJ. The helicase DDX41 senses intracellular DNA mediated by the adaptor STING in dendritic cells. Nat Immunol 2011; 12:959-65.
13. Sun L, Wu J, Du F, Chen X, Chen ZJ. Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway. Science 2013; 339:786-91.
14. Lee KG, Kim SS, Kui L, Voon DC, Mauduit M, Bist P, et al. Bruton's tyrosine kinase phosphorylates DDX41 and activates its binding of dsDNA and STING to initiate type 1 interferon response. Cell Rep 2015; 10:1055-65.
15. Stavrou S, Blouch K, Kotla S, Bass A, Ross SR. Nucleic acid recognition orchestrates the anti-viral response to retroviruses. Cell Host Microbe 2015; 17:478-88.
16. Ansari MA, Dutta S, Veettil MV, Dutta D, Iqbal J, Kumar B, et al. Herpesvirus genome recognition induced acetylation of nuclear IFI16 is essential for its cytoplasmic translocation, inflammasome and IFN-β responses. PLoS Pathog 2015; 11:e1005019.
17. Ishikawa H, Barber GN. STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling. Nature 2008; 455:674-8.
18. Ishikawa H, Ma Z, Barber GN. STING regulates intracellular DNA-mediated, type I interferon-dependent innate immunity. Nature 2009; 461:788-92.
19. Zhong B, Yang Y, Li S, Wang YY, Li Y, Diao F, et al. The adaptor protein MITA links virus-sensing receptors to IRF3 transcription factor activation. Immunity 2008; 29:538-50.
20. Sun W, Li Y, Chen L, Chen H, You F, Zhou X, et al. ERIS, an endoplasmic reticulum IFN stimulator, activates innate immune signaling through dimerization. Proc Natl Acad Sci U S A 2009; 106:8653-8.
21. Burdette DL, Monroe KM, Sotelo-Troha K, Iwig JS, Eckert B, Hyodo M, et al. STING is a direct innate immune sensor of cyclic di-GMP. Nature 2011; 478:515-U111.
22. Wassermann R, Gulen MF, Sala C, Perin SG, Lou Y, Rybniker J, et al. Mycobacterium tuberculosis differentially activates cGAS- and inflammasome-dependent intracellular immune responses through ESX-1. Cell Host Microbe 2015; 17:799-810.
23. Watson RO, Bell SL, MacDuff DA, Kimmey JM, Diner EJ, Olivas J, et al. The cytosolic sensor cGAS detects Mycobacterium tuberculosis DNA to Induce type I interferons and activate autophagy. Cell Host Microbe 2015; 17:811-9.
24. Sharma S, DeOliveira RB, Kalantari P, Parroche P, Goutagny N, Jiang Z, et al. Innate immune recognition of an AT-rich stem-loop DNA motif in the Plasmodium falciparum genome. Immunity 2011; 35:194-207.
25. Hartlova A, Erttmann SF, Raffi FA, Schmalz AM, Resch U, Anugula S, et al. DNA damage primes the type I interferon system via the cytosolic DNA sensor STING to promote anti-microbial innate immunity. Immunity 2015; 42:332-43.
26. Wu J, Cai B, Sun W, Huang R, Liu X, Lin M, et al. Genome-wide analysis of host-Plasmodium yoelii interactions reveals regulators of the type I interferon response. Cell Rep 2015; 12:661-72.
27. Dai P, Wang W, Cao H, Avogadri F, Dai L, Drexler I, et al. Modified vaccinia virus Ankara triggers type I IFN production in murine conventional dendritic cells via a cGAS/STING-mediated cytosolic DNA-sensing pathway. PLoS Pathog 2014; 10:e1003989.
28. Tamayo R, Pratt JT, Camilli A. Roles of cyclic diguanylate in the regulation of bacterial pathogenesis. Annu Rev Microbiol 2007; 61:131-48.
29. Karaolis DK, Means TK, Yang D, Takahashi M, Yoshimura T, Muraille E, et al. Bacterial c-di-GMP is an immunostimulatory molecule. J Immunol 2007; 178:2171-81.
30. McWhirter SM, Barbalat R, Monroe KM, Fontana MF, Hyodo M, Joncker NT, 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; 206:1899-911.
31. Kobayashi H, Kobayashi CI, Nakamura-Ishizu A, Karigane D, Haeno H, Yamamoto KN, et al. Bacterial c-di-GMP affects hematopoietic stem/progenitors and their niches through STING. Cell Rep 2015; 11:71-84.
32. Woodward JJ, Iavarone AT, Portnoy DA. c-di-AMP secreted by intracellular Listeria monocytogenes activates a host type I interferon response. Science 2010; 328:1703-5.
33. Archer KA, Durack J, Portnoy DA. STING-dependent type I IFN production inhibits cell-mediated immunity to Listeria monocytogenes. PLoS Pathog 2014; 10:e1003861.
34. Sauer JD, Sotelo-Troha K, von Moltke J, Monroe KM, Rae CS, Brubaker SW, 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; 79:688-94.
35. Shu C, Yi G, Watts T, Kao CC, Li P. Structure of STING bound to cyclic di-GMP reveals the mechanism of cyclic dinucleotide recognition by the immune system. Nat Struct Mol Biol 2012; 19:722-4.
36. Shang G, Zhu D, Li N, Zhang J, Zhu C, Lu D, et al. Crystal structures of STING protein reveal basis for recognition of cyclic di-GMP. Nat Struct Mol Biol 2012; 19:725-7.
37. Ouyang S, Song X, Wang Y, Ru H, Shaw N, Jiang Y, et al. Structural analysis of the STING adaptor protein reveals a hydrophobic dimer interface and mode of cyclic di-GMP binding. Immunity 2012; 36:1073-86.
38. Huang YH, Liu XY, Du XX, Jiang ZF, Su XD. The structural basis for the sensing and binding of cyclic di-GMP by STING. Nat Struct Mol Biol 2012; 19:728-30.
39. Yin Q, Tian Y, Kabaleeswaran V, Jiang X, Tu D, Eck MJ, et al. Cyclic di-GMP sensing via the innate immune signaling protein STING. Mol Cell 2012; 46:735-45.
40. Cavlar T, Deimling T, Ablasser A, Hopfner KP, Hornung V. Species-specific detection of the antiviral small-molecule compound CMA by STING. EMBO J 2013; 32:1440-50.
41. Gao P, Ascano M, Zillinger T, Wang W, Dai P, Serganov AA, et al. Structure-function analysis of STING activation by c[G(2′, 5′)pA(3′, 5′)p] and targeting by antiviral DMXAA. Cell 2013; 154:748-62.
42. Gao P, Zillinger T, Wang W, Ascano M, Dai P, Hartmann G, et al. Binding-pocket and lid-region substitutions render human STING sensitive to the species-specific drug DMXAA. Cell Rep 2014; 8:1668-76.
43. Li XD, Wu J, Gao D, Wang H, Sun L, Chen ZJ. Pivotal roles of cGAS-cGAMP signaling in antiviral defense and immune adjuvant effects. Science 2013; 341:1390-4.
44. Gao P, Ascano M, Wu Y, Barchet W, Gaffney BL, Zillinger T, et al. Cyclic [G(2′, 5′)pA(3′, 5′)p] is the metazoan second messenger produced by DNA-activated cyclic GMP-AMP synthase. Cell 2013; 153:1094-107.
45. Diner EJ, Burdette DL, Wilson SC, Monroe KM, Kellenberger CA, Hyodo M, et al. The innate immune DNA sensor cGAS produces a noncanonical cyclic dinucleotide that activates human STING. Cell Rep 2013; 3:1355-61.
46. Ablasser A, Goldeck M, Cavlar T, Deimling T, Witte G, Rohl I, et al. cGAS produces a 2′-5′-linked cyclic dinucleotide second messenger that activates STING. Nature 2013; 498:380-4.
47. Zhang X, Shi H, Wu J, Zhang X, Sun L, Chen C, et al. Cyclic GMP-AMP containing mixed phosphodiester linkages is an endogenous high-affinity ligand for STING. Mol Cell 2013; 51:226-35.
48. Saitoh T, Fujita N, Hayashi T, Takahara K, Satoh T, Lee H, et al. Atg9a controls dsDNA-driven dynamic translocation of STING and the innate immune response. Proc Natl Acad Sci U S A 2009; 106:20842-6.
49. Wang Q, Liu X, Cui Y, Tang Y, Chen W, Li S, et al. The E3 ubiquitin ligase AMFR and INSIG1 Bridge the activation of TBK1 kinase by modifying the adaptor STING. Immunity 2014; 41:919-33.
50. Shu HB, Wang YY. Adding to the STING. Immunity 2014; 41:871-3.
51. Goldstein JL, DeBose-Boyd RA, Brown MS. Protein sensors for membrane sterols. Cell 2006; 124:35-46.
52. Tsuchida T, Zou JA, Saitoh T, Kumar H, Abe T, Matsuura Y, et al. The ubiquitin ligase TRIM56 regulates innate immune responses to intracellular double-stranded DNA. Immunity 2010; 33:765-76.
53. Zhang J, Hu MM, Wang YY, Shu HB. TRIM32 protein modulates type I interferon induction and cellular antiviral response by targeting MITA/STING protein for K63-linked Ubiquitination. J Biol Chem 2012; 287:28646-55.
54. Liu X, Wang Q, Pan YD, Wang C. Sensing and responding to cytosolic viruses invasions: an orchestra of kaleidoscopic ubiquitinations. Cytokine Growth Factor Rev 2015; 26:379-387.
55. Shi HX, Yang K, Liu X, Liu XY, Wei B, Shan YF, et al. Positive regulation of interferon regulatory factor 3 activation by Herc5 via ISG15 modification. Mol Cell Biol 2010; 30:2424-36.
56. Liu X, Chen W, Wang Q, Li L, Wang C. Negative regulation of TLR inflammatory signaling by the SUMO-deconjugating enzyme SENP6. PLoS Pathog 2013; 9:e1003480.
57. Shi HX, Liu X, Wang Q, Tang PP, Liu XY, Shan YF, et al. Mitochondrial ubiquitin ligase MARCH5 promotes TLR7 signaling by attenuating TANK action. PLoS Pathog 2011; 7:e1002057.
58. Tanaka Y, Chen ZJJ. STING specifies IRF3 phosphorylation by TBK1 in the cytosolic DNA signaling pathway. Sci Signal 2012; 5:ra20.
59. Konno H, Konno K, Barber GN. Cyclic dinucleotides trigger ULK1 (ATG1) phosphorylation of STING to prevent sustained innate immune signaling. Cell 2013; 155:688-98.
60. Liu X, Wang Q, Chen W, Wang C. Dynamic regulation of innate immunity by ubiquitin and ubiquitin-like proteins. Cytokine Growth Factor Rev 2013; 24:559-70.
61. Zhong B, Zhang L, Lei C, Li Y, Mao AP, Yang Y, et al. The ubiquitin ligase RNF5 regulates antiviral responses by mediating degradation of the adaptor protein MITA. Immunity 2009; 30:397-407.
62. Qin Y, Zhou MT, Hu MM, Hu YH, Zhang J, Guo L, et al. RNF26 temporally regulates virus-triggered type I interferon induction by two distinct mechanisms. PLoS Pathog 2014; 10:e1004358.
63. Zhang L, Mo JY, Swanson KV, Wen HT, Petrucelli A, Gregory SM, et al. NLRC3, a member of the NLR family of proteins, is a negative regulator of innate immune signaling induced by the DNA sensor STING. Immunity 2014; 40:329-41.
64. Zhou Q, Lin H, Wang SY, Wang S, Ran Y, Liu Y, et al. The ER-associated protein ZDHHC1 Is a positive regulator of DNA virus-triggered, MITA/STING-dependent innate immune signaling. Cell Host Microbe 2014; 16:450-61.
65. Oku S, Takahashi N, Fukata Y, Fukata M. In silico screening for palmitoyl substrates reveals a role for DHHC1/3/10 (zDHHC1/3/11)-mediated neurochondrin palmitoylation in its targeting to Rab5-positive endosomes. J Biol Chem 2013; 288:19816-29.
66. Nitta S, Sakamoto N, Nakagawa M, Kakinuma S, Mishima K, Kusano-Kitazume A, et al. Hepatitis C virus NS4B protein targets STING and abrogates RIG-I-mediated type I interferon-dependent innate immunity. Hepatology 2013; 57:46-58.
67. Ding Q, Cao X, Lu J, Huang B, Liu YJ, Kato N, et al. Hepatitis C virus NS4B blocks the interaction of STING and TBK1 to evade host innate immunity. J Hepatol 2013; 59:52-8.
68. Lau L, Gray EE, Brunette RL, Stetson DB. DNA tumor virus oncogenes antagonize the cGAS-STING DNA sensing pathway. Science 2015; 350:568-571.
69. Aguirre S, Maestre AM, Pagni S, Patel JR, Savage T, Gutman D, et al. DENV inhibits type I IFN production in infected cells by cleaving human STING. PLoS Pathog 2012; 8:e1002934.
70. Yu CY, Chang TH, Liang JJ, Chiang RL, Lee YL, Liao CL, et al. Dengue virus targets the adaptor protein MITA to subvert host innate immunity. PLoS Pathog 2012; 8:e1002780.
71. Smith S, Jefferies C. Role of DNA/RNA sensors and contribution to autoimmunity. Cytokine Growth Factor Rev 2014; 25:745-57.
72. 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 2005; 6:49-56.
73. Kawane K, Ohtani M, Miwa K, Kizawa T, Kanbara Y, Yoshioka Y, et al. Chronic polyarthritis caused by mammalian DNA that escapes from degradation in macrophages. Nature 2006; 443:998-1002.
74. Lan YY, Londono D, Bouley R, Rooney MS, Hacohen N. Dnase2a deficiency uncovers lysosomal clearance of damaged nuclear DNA via autophagy. Cell Rep 2014; 9:180-92.
75. Ahn J, Gutman D, Saijo S, Barber GN. STING manifests self DNA-dependent inflammatory disease. Proc Natl Acad Sci USA 2012; 109:19386-91.
76. Mazur DJ, Perrino FW. Identification and expression of the TREX1 and TREX2 cDNA sequences encoding mammalian 3′→5′ exonucleases. J Biol Chem 1999; 274:19655-60.
77. Stetson DB, Ko JS, Heidmann T, Medzhitov R. Trex1 prevents cell-intrinsic initiation of autoimmunity. Cell 2008; 134:587-98.
78. Crow YJ, Hayward BE, Parmar R, Robins P, Leitch A, Ali M, et al. Mutations in the gene encoding the 3′-5′ DNA exonuclease TREX1 cause Aicardi-Goutieres syndrome at the AGS1 locus. Nat Genet 2006; 38:917-20.
79. Lee-Kirsch MA, Gong M, Chowdhury D, Senenko L, Engel K, Lee YA, et al. Mutations in the gene encoding the 3′-5′ DNA exonuclease TREX1 are associated with systemic lupus erythematosus. Nat Genet 2007; 39:1065-7.
80. Hasan M, Fermaintt CS, Gao N, Sakai T, Miyazaki T, Jiang S, et al. Cytosolic nuclease TREX1 regulates oligosaccharyltransferase activity independent of nuclease activity to suppress immune activation. Immunity 2015; 43:463-74.
81. Ablasser A, Hemmerling I, Schmid-Burgk JL, Behrendt R, Roers A, Hornung V. TREX1 deficiency triggers cell-autonomous immunity in a cGAS-dependent manner. J Immunol 2014; 192:5993-7.
82. Gehrke N, Mertens C, Zillinger T, Wenzel J, Bald T, Zahn S, et al. Oxidative damage of DNA confers resistance to cytosolic nuclease TREX1 degradation and potentiates STING-dependent immune sensing. Immunity 2013; 39:482-95.
83. Morita M, Stamp G, Robins P, Dulic A, Rosewell I, Hrivnak G, et al. Gene-targeted mice lacking the Trex1 (DNase III) 3′→5′ DNA exonuclease develop inflammatory myocarditis. Mol Cell Biol 2004; 24:6719-27.
84. Gall A, Treuting P, Elkon KB, Loo YM, Gale M Jr, Barber GN, et al. Autoimmunity initiates in nonhematopoietic cells and progresses via lymphocytes in an interferon-dependent autoimmune disease. Immunity 2012; 36:120-31.
85. Woo SR, Fuertes MB, Corrales L, Spranger S, Furdyna MJ, Leung MY, et al. STING-dependent cytosolic DNA sensing mediates innate immune recognition of immunogenic tumors. Immunity 2014; 41:830-42.
86. Deng L, Liang H, Xu M, Yang X, Burnette B, Arina A, et al. STING-dependent cytosolic DNA sensing promotes radiation-induced type I interferon-dependent antitumor immunity in immunogenic tumors. Immunity 2014; 41:843-52.
87. Corrales L, Glickman LH, McWhirter SM, Kanne DB, Sivick KE, Katibah GE, et al. Direct activation of STING in the tumor microenvironment leads to potent and systemic tumor regression and immunity. Cell Rep 2015; 11:1018-30.
88. Shen YJ, Le Bert N, Chitre AA, Koo CX, Nga XH, Ho SS, et al. Genome-derived cytosolic DNA mediates type I interferon-dependent rejection of B cell lymphoma cells. Cell Rep 2015; 11:460-73.