On taking the STING out of immune activation

Journal of Leukocyte Biology

Volumn 103, Issue 6, 2018, Pages 1189-1195

  Banete, Andra ^a   Seaver, Kyle ^a   Bakshi, Devyani ^a   Gee, Katrina ^a   Basta, Sameh ^a  

^a QUEEN S UNIVERSITY   (Canada)

Author keywords

IFN; immune evasion; tumor; virus

Indexed keywords

ADAPTOR PROTEIN; EXTRACHROMOSOMAL DNA; INTERFERON REGULATORY FACTOR 3; INTERFERON REGULATORY FACTOR 7; STIMULATOR OF INTERFERON GENE PROTEIN; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; CANCER CELL; CELL MIGRATION; CELL PROLIFERATION; CYTOTOXIC T LYMPHOCYTE; DNA VIRUS INFECTION; HUMAN; IMMUNE RESPONSE; IMMUNOREGULATION; IMMUNOSTIMULATION; INFECTION SENSITIVITY; INTERFERON PRODUCTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; TUMOR IMMUNITY;

EID: 85041801783     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1002/JLB.2MIR0917-383R     Document Type: Review

References (90)

1. Takeuchi O, Akira S. Pattern recognition receptors and inflammation. Cell. 2010;140:805–820.
2. Ishikawa H, Barber GN. STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling. Nature. 2008;455:674–678.
3. Zhong B, Ma HY, Yang Q, Gu FR, Yin GQ, Xia CM. Decrease in toll-like receptors 2 and 4 in the spleen of mouse with endotoxic tolerance. Inflamm Res. 2008;57:252–259.
4. Petrof EO, Claud EC, Sun J, et al. Bacteria-free solution derived from lactobacillus plantarum inhibits multiple NF-kappaB pathways and inhibits proteasome function. Inflamm Bowel Dis. 2009.
5. Jin L, Waterman PM, Jonscher KR, Short CM, Reisdorph NA, Cambier JC. MPYS, a novel membrane tetraspanner, is associated with major histocompatibility complex class II and mediates transduction of apoptotic signals. Mol Cell Biol. 2008;28:5014–5026.
6. Chen H, Sun H, You F, et al. Activation of STAT6 by STING is critical for antiviral innate immunity. Cell. 2011;147:436–446.
7. Ishikawa H, Ma Z, Barber GN. STING regulates intracellular DNA-mediated, type I interferon-dependent innate immunity. Nature. 2009;461:788–792.
8. Ablasser A, Goldeck M, Cavlar T, et al. cGAS produces a 2'-5'-linked cyclic dinucleotide second messenger that activates STING. Nature. 2013;498:380–384.
9. Burdette DL, Vance RE. STING and the innate immune response to nucleic acids in the cytosol. Nat Immunol. 2013;14:19–26.
10. Honke N, Shaabani N, Cadeddu G, et al. Enforced viral replication activates adaptive immunity and is essential for the control of a cytopathic virus. Nat Immunol. 2012;13:51–57.
11. Woodward JJ, Iavarone AT, Portnoy DA. c-di-AMP secreted by intracellular Listeria monocytogenes activates a host type I interferon response. Science. 2010;328:1703–1705.
12. Ajami B, Bennett JL, Krieger C, Tetzlaff W, Rossi FM. Local self-renewal can sustain CNS microglia maintenance and function throughout adult life. Nat Neurosci;10:1538–1543.
13. Parker ZM, Murphy AA, Leib DA. Role of the DNA sensor STING in protection from lethal infection following corneal and intracerebral challenge with herpes simplex virus 1. J Virol. 2015;89:11080–11091.
14. Dominguez CX, Amezquita RA, Guan T, et al. The transcription factors ZEB2 and T-bet cooperate to program cytotoxic T cell terminal differentiation in response to LCMV viral infection. J Exp Med. 2015;212:2041–2056.
15. Fu YZ, Su S, Gao YQ, et al. Human cytomegalovirus tegument protein UL82 inhibits STING-mediated signaling to evade antiviral immunity. Cell Host Microbe. 2017;21:231–243.
16. Behnsen J, Perez-Lopez A, Nuccio SP, Raffatellu M. Exploiting host immunity: the Salmonella paradigm. Trends Immunol. 2015;36:112–120.
17. Woo SR, Fuertes MB, Corrales L, et al. STING-dependent cytosolic DNA sensing mediates innate immune recognition of immunogenic tumors. Immunity. 2014;41:830–842.
18. Corrales L, Glickman LH, McWhirter SM, et al. Direct activation of STING in the tumor microenvironment leads to potent and systemic tumor regression and immunity. Cell Rep. 2015;11:1018–1030.
19. Abe T, Harashima A, Xia T, et al. STING recognition of cytoplasmic DNA instigates cellular defense. Mol Cell. 2013;50:5–15.
20. Arnold CE, Gordon P, Barker RN, Wilson HM. The activation status of human macrophages presenting antigen determines the efficiency of Th17 responses. Immunobiology. 2015;220:10–19.
21. Schoggins JW, MacDuff DA, Imanaka N, et al. Pan-viral specificity of IFN-induced genes reveals new roles for cGAS in innate immunity. Nature. 2014;505:691–695.
22. Dixit E, Boulant S, Zhang Y, et al. Peroxisomes are signaling platforms for antiviral innate immunity. Cell. 2010;141:668–681.
23. Wu B, Peisley A, Richards C, et al. Structural basis for dsRNA recognition, filament formation, and antiviral signal activation by MDA5. Cell. 2013;152:276–289.
24. Horner SM, Liu HM, Park HS, Briley J. Mitochondrial-associated endoplasmic reticulum membranes (MAM) form innate immune synapses and are targeted by hepatitis C virus. Proc Natl Acad Sci USA. 2011;108:14590–14595.
25. Gack MU, Shin YC, Joo CH, et al. TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity. Nature. 2007;446:916–920.
26. Zhong B, Yang Y, Li S, et al. The adaptor protein MITA links virus-sensing receptors to IRF3 transcription factor activation. Immunity. 2008;29:538–550.
27. Nazmi A, Mukhopadhyay R, Dutta K, Basu A. STING mediates neuronal innate immune response following Japanese encephalitis virus infection. Sci Rep. 2012;2:347.
28. Chaplin DD. Overview of the immune response. J Allergy Clin Immunol. 2010;125:S3–23.
29. Wu JJ, Li W, Shao Y, et al. Inhibition of cGAS DNA sensing by a Herpesvirus Virion Protein. Cell Host Microbe. 2015;18:333–344.
30. Fan X, Zhang H, Cheng Y, Jiang X, Zhu J, Jin T. Double roles of macrophages in human neuroimmune diseases and their animal models. Mediat Inflamm. 2016;2016:8489251.
31. Aguirre S, Maestre AM, Pagni S, et al. DENV inhibits type I IFN production in infected cells by cleaving human STING. PLoS Pathog. 2012;8:e1002934.
32. Maringer K, Fernandez-Sesma A. Message in a bottle: lessons learned from antagonism of STING signalling during RNA virus infection. Cytokine Growth Factor Rev. 2014;25:669–679.
33. Horner SM. Activation and evasion of antiviral innate immunity by hepatitis C virus. J Mol Biol. 2014;426:1198–1209.
34. Meylan E, Curran J, Hofmann K, et al. Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature. 2005;437:1167–1172.
35. Aagaard A, Listwan P, Cowieson N, et al. An inflammatory role for the mammalian carboxypeptidase inhibitor latexin: relationship to cystatins and the tumor suppressor TIG1. Structure. 2005;13:309–317.
36. Nitta S, Sakamoto N, Nakagawa M, 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.
37. Bernhard CA, Ried C, Kochanek S, Brocker T. CD169+ macrophages are sufficient for priming of CTLs with specificities left out by cross-priming dendritic cells. Proc Natl Acad Sci USA. 2015;112:5461–5466.
38. McLaughlin-Drubin ME, Munger K. The human papillomavirus E7 oncoprotein. Virology. 2009;384:335–344.
39. de Souza RF, Iyer LM, Aravind L. Diversity and evolution of chromatin proteins encoded by DNA viruses. Biochim Biophys Acta. 2010;1799:302–318.
40. Sharma S, tenOever BR, Grandvaux N, Zhou GP, Lin R, Hiscott J. Triggering the interferon antiviral response through an IKK-related pathway. Science. 2003;300:1148–1151.
41. Fitzgerald KA, McWhirter SM, Faia KL, et al. IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat Immunol. 2003;4:491–496.
42. Tanaka Y, Chen ZJ. STING specifies IRF3 phosphorylation by TBK1 in the cytosolic DNA signaling pathway. Sci Signal. 2012;5. ra20.
43. Christensen MH, Jensen SB, Miettinen JJ, et al. HSV-1 ICP27 targets the TBK1-activated STING signalsome to inhibit virus-induced type I IFN expression. EMBO J. 2016;35:1385–1399.
44. Parker BS, Rautela J, Hertzog PJ. Antitumour actions of interferons: implications for cancer therapy. Nat Rev Cancer. 2016;16:131–144.
45. Dunn GP, Koebel CM, Schreiber RD. Interferons, immunity and cancer immunoediting. Nat Rev Immunol. 2006;6:836–848.
46. Hobohm U, Stanford JL, Grange JM. Pathogen-associated molecular pattern in cancer immunotherapy. Crit Rev Immunol. 2008;28:95–107.
47. Kawai T, Akira S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol. 2010;11:373–384.
48. Switaj T, Jalili A, Jakubowska AB, et al. CpG immunostimulatory oligodeoxynucleotide 1826 enhances antitumor effect of interleukin 12 gene-modified tumor vaccine in a melanoma model in mice. Clin Cancer Res. 2004;10:4165–4175.
49. Barker JR, Koestler BJ, Carpenter VK, et al. STING-dependent recognition of cyclic di-AMP mediates type I interferon responses during Chlamydia trachomatis infection. MBio. 2013;4:e00018–13.
50. Burdette DL, Monroe KM, Sotelo-Troha K, et al. STING is a direct innate immune sensor of cyclic di-GMP. Nature. 2011;478:515–518.
51. Barber GN. STING-dependent cytosolic DNA sensing pathways. Trends Immunol. 2014;35:88–93.
52. Gao D, Wu J, Wu YT, et al. Cyclic GMP-AMP synthase is an innate immune sensor of HIV and other retroviruses. Science. 2013;341:903–906.
53. Diamond MS, Kinder M, Matsushita H, et al. Type I interferon is selectively required by dendritic cells for immune rejection of tumors. J Exp Med. 2011;208:1989–2003.
54. Basta S, Alatery A. The cross-priming pathway: a portrait of an intricate immune system. Scand J Immunol. 2007;65:311–319.
55. Oh JZ, Kurche JS, Burchill MA, Kedl RM. TLR7 enables cross-presentation by multiple dendritic cell subsets through a type I IFN-dependent pathway. Blood. 2011;118:3028–3038.
56. Le Bon A, Montoya M, Edwards MJ, et al. A role for the transcription factor RelB in IFN-alpha production and in IFN-alpha-stimulated cross-priming. Eur J Immunol. 2006.
57. Durand V, Wong SY, Tough DF, Le Bon A. IFN-alpha/beta-dependent cross-priming induced by specific toll-like receptor agonists. Vaccine. 2006;24(Suppl 2):S2–22–23.
58. Le Bon A, Etchart N, Rossmann C, et al. Cross-priming of CD8+ T cells stimulated by virus-induced type I interferon. Nat Immunol. 2003;4:1009–1015.
59. Fuertes MB, Kacha AK, Kline J, et al. Host type I IFN signals are required for antitumor CD8+ T cell responses through CD8+ dendritic cells. J Exp Med. 2011;208:2005–2016.
60. Dunn GP, Bruce AT, Sheehan KC, et al. A critical function for type I interferons in cancer immunoediting. Nat Immunol. 2005;6:722–729.
61. Klarquist J, Hennies CM, Lehn MA, Reboulet RA, Feau S, Janssen EM. STING-mediated DNA sensing promotes antitumor and autoimmune responses to dying cells. J Immunol. 2014;193:6124–6134.
62. Deng L, Liang H, Xu M, et al. STING-dependent cytosolic DNA sensing promotes radiation-induced type i interferon-dependent antitumor immunity in immunogenic tumors. Immunity. 2014;41:843–852.
63. Barber GN. STING: infection, inflammation and cancer. Nat Rev Immunol. 2015;15:760–770.
64. Sokolowska O, Nowis D. STING signaling in cancer cells: important or not?. Arch Immunol Ther Exp (Warsz). 2017; doi: 10.1007/s00005-017-0481-7.
65. Baird JR, Friedman D, Cottam B, et al. Radiotherapy combined with novel STING-targeting oligonucleotides results in regression of established tumors. Cancer Res. 2016;76:50–61.
66. Stetson DB, Ko JS, Heidmann T, Medzhitov R. Trex1 prevents cell-intrinsic initiation of autoimmunity. Cell. 2008;134:587–598.
67. Sistigu A, Yamazaki T, Vacchelli E, et al. Cancer cell-autonomous contribution of type I interferon signaling to the efficacy of chemotherapy. Nat Med. 2014;20:1301–1309.
68. Ahn J, Konno H, Barber GN. Diverse roles of STING-dependent signaling on the development of cancer. Oncogene. 2015;34:5302–5308.
69. Xia T, Konno H, Ahn J, Barber GN. Deregulation of STING signaling in colorectal carcinoma constrains DNA damage responses and correlates with tumorigenesis. Cell Rep. 2016;14:282–297.
70. Konno H, Konno K, Barber GN. Cyclic dinucleotides trigger ULK1 (ATG1) phosphorylation of STING to prevent sustained innate immune signaling. Cell. 2013;155:688–698.
71. Ahn J, Gutman D, Saijo S, Barber GN. STING manifests self DNA-dependent inflammatory disease. Proc Natl Acad Sci USA. 2012;109:19386–19391.
72. Wong PM, Feng Y, Wang J, Shi R, Jiang X. Regulation of autophagy by coordinated action of mTORC1 and protein phosphatase 2A. Nat Commun. 2015;6:8048.
73. Zou Y, Chen Z, He X, et al. High expression levels of unc-51-like kinase 1 as a predictor of poor prognosis in colorectal cancer. Oncol Lett. 2015;10:1583–1588.
74. Li Y, Wilson HL, Kiss-Toth E. Regulating STING in health and disease. J Inflamm (Lond). 2017;14:11.
75. Zhao G, Liu L, Zhao T, et al. Upregulation of miR-24 promotes cell proliferation by targeting NAIF1 in non-small cell lung cancer. Tumour Biol. 2015;36:3693–3701.
76. Volinia S, Calin GA, Liu CG, et al. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci USA. 2006;103:2257–2261.
77. Zhang H, Duan J, Qu Y, et al. Onco-miR-24 regulates cell growth and apoptosis by targeting BCL2L11 in gastric cancer. Protein Cell. 2016;7:141–151.
78. Huang Z, Chen X, Yu B, Chen D. Cloning and functional characterization of rat stimulator of interferon genes (STING) regulated by miR-24. Dev Comp Immunol. 2012;37:414–420.
79. Devarajan E, Sahin AA, Chen JS, et al. Down-regulation of caspase 3 in breast cancer: a possible mechanism for chemoresistance. Oncogene. 2002;21:8843–8851.
80. Shen XG, Wang C, Li Y, et al. Downregulation of caspase-9 is a frequent event in patients with stage II colorectal cancer and correlates with poor clinical outcome. Colorectal Dis. 2010;12:1213–1218.
81. Huang Q, Li F, Liu X, et al. Caspase 3-mediated stimulation of tumor cell repopulation during cancer radiotherapy. Nat Med. 2011;17:860–866.
82. Gregory CD, Pound JD. Cell death in the neighbourhood: direct microenvironmental effects of apoptosis in normal and neoplastic tissues. J Pathol. 2011;223:177–194.
83. Bondanza A, Zimmermann VS, Rovere-Querini P, et al. Inhibition of phosphatidylserine recognition heightens the immunogenicity of irradiated lymphoma cells in vivo. J Exp Med. 2004;200:1157–1165.
84. White MJ, McArthur K, Metcalf D, et al. Apoptotic caspases suppress mtDNA-induced STING-mediated type I IFN production. Cell. 2014;159:1549–1562.
85. Rongvaux A, Jackson R, Harman CC, et al. Apoptotic caspases prevent the induction of type I interferons by mitochondrial DNA. Cell. 2014;159:1563–1577.
86. Song S, Peng P, Tang Z, et al. Decreased expression of STING predicts poor prognosis in patients with gastric cancer. Sci Rep. 2017;7:39858.
87. Bu Y, Liu F, Jia QA, Yu SN. Decreased expression of TMEM173 predicts poor prognosis in patients with hepatocellular carcinoma. PLoS One. 2016;11:e0165681.
88. Kang MH, Reynolds CP. Bcl-2 inhibitors: targeting mitochondrial apoptotic pathways in cancer therapy. Clin Cancer Res. 2009;15:1126–1132.
89. MacKenzie SH, Clark AC. Targeting cell death in tumors by activating caspases. Curr Cancer Drug Targets. 2008;8:98–109.
90. Hensley P, Mishra M, Kyprianou N. Targeting caspases in cancer therapeutics. Biol Chem. 2013;394:831–843.