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Current Pharmaceutical Design

Editor-in-Chief

ISSN (Print): 1381-6128
ISSN (Online): 1873-4286

Review Article

Stimulator of Interferon Genes Signaling Pathway and its Role in Anti-tumor Immune Therapy

Author(s): Yuanjin Gong, Chang Chang, Xi Liu, Yan He*, Yiqi Wu*, Song Wang and Chongyou Zhang

Volume 26, Issue 26, 2020

Page: [3085 - 3095] Pages: 11

DOI: 10.2174/1381612826666200610183048

Price: $65

Abstract

Stimulator of interferon genes is an important innate immune signaling molecule in the body and is involved in the innate immune signal transduction pathway induced by pathogen-associated molecular patterns or damage-associated molecular patterns. Stimulator of interferon genes promotes the production of type I interferon and thus plays an important role in the innate immune response to infection. In addition, according to a recent study, the stimulator of interferon genes pathway also contributes to anti-inflammatory and anti-tumor reactions. In this paper, current researches on the Stimulator of interferon genes signaling pathway and its relationship with tumor immunity are reviewed. Meanwhile, a series of critical problems to be addressed in subsequent studies are discussed as well.

Keywords: STING, innate immune response, type I interferon, cGAMP, cGAS, anti-tumor immunity.

[1]
Ishikawa H, Barber GN. STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling. Nature 2008; 455(7213): 674-8.
[http://dx.doi.org/10.1038/nature07317] [PMID: 18724357]
[2]
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(3-4): 414-20.
[http://dx.doi.org/10.1016/j.dci.2012.02.010] [PMID: 22387590]
[3]
Zhong B, Yang Y, Li S, et al. The adaptor protein MITA links virus-sensing receptors to IRF3 transcription factor activation. Immunity 2008; 29(4): 538-50.
[http://dx.doi.org/10.1016/j.immuni.2008.09.003] [PMID: 18818105]
[4]
Ouyang S, Song X, Wang 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(6): 1073-86.
[http://dx.doi.org/10.1016/j.immuni.2012.03.019] [PMID: 22579474]
[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(16): 5014-26.
[http://dx.doi.org/10.1128/MCB.00640-08] [PMID: 18559423]
[6]
Sun W, Li Y, Chen L, et al. ERIS, an endoplasmic reticulum IFN stimulator, activates innate immune signaling through dimerization. Proc Natl Acad Sci USA 2009; 106(21): 8653-8.
[http://dx.doi.org/10.1073/pnas.0900850106] [PMID: 19433799]
[7]
Su YC, Tu ZL, Yang CY, et al. Crystallization studies of the murine c-di-GMP sensor protein STING. Acta Crystallogr Sect F Struct Biol Cryst Commun 2012; 68(Pt 8): 906-10.
[http://dx.doi.org/10.1107/S1744309112024372] [PMID: 22869119]
[8]
Ishikawa H, Barber GN. The STING pathway and regulation of innate immune signaling in response to DNA pathogens. Cell Mol Life Sci 2011; 68(7): 1157-65.
[http://dx.doi.org/10.1007/s00018-010-0605-2] [PMID: 21161320]
[9]
Takeuchi O, Akira S. Pattern recognition receptors and inflammation. Cell 2010; 140(6): 805-20.
[http://dx.doi.org/10.1016/j.cell.2010.01.022] [PMID: 20303872]
[10]
Fuertes MB, Woo SR, Burnett B, Fu YX, Gajewski TF. Type I interferon response and innate immune sensing of cancer. Trends Immunol 2013; 34(2): 67-73.
[http://dx.doi.org/10.1016/j.it.2012.10.004] [PMID: 23122052]
[11]
Stark GR, Kerr IM, Williams BR, Silverman RH, Schreiber RD. How cells respond to interferons. Annu Rev Biochem 1998; 67: 227-64.
[http://dx.doi.org/10.1146/annurev.biochem.67.1.227] [PMID: 9759489]
[12]
Kwon Y, Park OJ, Kim J, Cho JH, Yun CH, Han SH. Cyclic dinucleotides inhibit osteoclast differentiation through stingmediated interferon-beta signaling. J Bone Mineral Research: the official journal of the American Society for Bone and Mineral Research 2019; 34(7): 1366-75.
[13]
Zhang Y, Yeruva L, Marinov A, et al. The DNA sensor, cyclic GMP-AMP synthase, is essential for induction of IFN-beta during Chlamydia trachomatis infection. J Immunol (Baltimore, Md: 1950) 2014; 193(5): 2394-404.
[14]
Ishikawa H, Ma Z, Barber GN. STING regulates intracellular DNA-mediated, type I interferon-dependent innate immunity. Nature 2009; 461(7265): 788-92.
[http://dx.doi.org/10.1038/nature08476] [PMID: 19776740]
[15]
Ran Y, Shu HB, Wang YY. MITA/STING: a central and multifaceted mediator in innate immune response. Cytokine Growth Factor Rev 2014; 25(6): 631-9.
[http://dx.doi.org/10.1016/j.cytogfr.2014.05.003] [PMID: 24929887]
[16]
Yoneyama M, Kikuchi M, Natsukawa T, et al. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat Immunol 2004; 5(7): 730-7.
[http://dx.doi.org/10.1038/ni1087] [PMID: 15208624]
[17]
Y C.. Mycobacterium tuberculosis-induced IFN-β production requires cytosolic DNA and RNA sensing pathways. J Exp Med 2018; 215(11): 2919-35.
[18]
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(6): 669-79.
[http://dx.doi.org/10.1016/j.cytogfr.2014.08.004] [PMID: 25212897]
[19]
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(10)e1002934
[http://dx.doi.org/10.1371/journal.ppat.1002934] [PMID: 23055924]
[20]
Christensen MH, Paludan SR. Viral evasion of DNA-stimulated innate immune responses. Cell Mol Immunol 2017; 14(1): 4-13.
[http://dx.doi.org/10.1038/cmi.2016.06] [PMID: 26972769]
[21]
Medzhitov R, Janeway CA Jr. Innate immunity: the virtues of a nonclonal system of recognition. Cell 1997; 91(3): 295-8.
[http://dx.doi.org/10.1016/S0092-8674(00)80412-2] [PMID: 9363937]
[22]
Paladino P, Cummings DT, Noyce RS, Mossman KL. The IFNindependent response to virus particle entry provides a first line of antiviral defense that is independent of TLRs and retinoic acidinducible gene I. J Immunol (Baltimore, Md : 1950) 2006; 177(11): 8008-16.
[23]
Wang X, Smith C, Yin H. Targeting Toll-like receptors with small molecule agents. Chem Soc Rev 2013; 42(12): 4859-66.
[http://dx.doi.org/10.1039/c3cs60039d] [PMID: 23503527]
[24]
Cheng L, Sun J, Xu W, Dong L, Hu Y, Zhou M. OAHG: an integrated resource for annotating human genes with multi-level ontologies. Sci Rep 2016; 6: 34820.
[http://dx.doi.org/10.1038/srep34820] [PMID: 27703231]
[25]
Cheng L, Jiang Y, Ju H, et al. InfAcrOnt: calculating cross-ontology term similarities using information flow by a random walk. BMC Genomics 2018; 19(Suppl. 1): 919.
[http://dx.doi.org/10.1186/s12864-017-4338-6] [PMID: 29363423]
[26]
Cheng L, Hu Y, Sun J, Zhou M, Jiang Q. DincRNA: a comprehensive web-based bioinformatics toolkit for exploring disease associations and ncRNA function. Bioinformatics 2018; 34(11): 1953-6.
[http://dx.doi.org/10.1093/bioinformatics/bty002] [PMID: 29365045]
[27]
Cheng L, Yang H, Zhao H, et al. MetSigDis: a manually curated resource for the metabolic signatures of diseases. Brief Bioinform 2019; 20(1): 203-9.
[http://dx.doi.org/10.1093/bib/bbx103] [PMID: 28968812]
[28]
Cheng L, Wang P, Tian R, et al. LncRNA2Target v2.0: a comprehensive database for target genes of lncRNAs in human and mouse. Nucleic Acids Res 2019; 47(D1): D140-4.
[http://dx.doi.org/10.1093/nar/gky1051] [PMID: 30380072]
[29]
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(6121): 786-91.
[http://dx.doi.org/10.1126/science.1232458] [PMID: 23258413]
[30]
Parker D, Martin FJ, Soong G, et al. Streptococcus pneumoniae DNA initiates type I interferon signaling in the respiratory tract. MBio 2011; 2(3): e00016-11.
[http://dx.doi.org/10.1128/mBio.00016-11] [PMID: 21586648]
[31]
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(10): 959-65.
[http://dx.doi.org/10.1038/ni.2091] [PMID: 21892174]
[32]
Unterholzner L, Keating SE, Baran M, et al. IFI16 is an innate immune sensor for intracellular DNA. Nat Immunol 2010; 11(11): 997-1004.
[http://dx.doi.org/10.1038/ni.1932] [PMID: 20890285]
[33]
Thompson MR, Sharma S, Atianand M, et al. Interferon γ-inducible protein (IFI) 16 transcriptionally regulates type i interferons and other interferon-stimulated genes and controls the interferon response to both DNA and RNA viruses. J Biol Chem 2014; 289(34): 23568-81.
[http://dx.doi.org/10.1074/jbc.M114.554147] [PMID: 25002588]
[34]
Brubaker SW, Bonham KS, Zanoni I, Kagan JC. Innate immune pattern recognition: a cell biological perspective. Annu Rev Immunol 2015; 33: 257-90.
[http://dx.doi.org/10.1146/annurev-immunol-032414-112240] [PMID: 25581309]
[35]
Civril F, Deimling T, de Oliveira Mann CC, et al. Structural mechanism of cytosolic DNA sensing by cGAS. Nature 2013; 498(7454): 332-7.
[http://dx.doi.org/10.1038/nature12305] [PMID: 23722159]
[36]
Zhang X, Shi H, Wu J, et al. Cyclic GMP-AMP containing mixed phosphodiester linkages is an endogenous high-affinity ligand for STING. Mol Cell 2013; 51(2): 226-35.
[http://dx.doi.org/10.1016/j.molcel.2013.05.022] [PMID: 23747010]
[37]
Shang G, Zhang C, Chen ZJ, Bai XC, Zhang X. Cryo-EM structures of STING reveal its mechanism of activation by cyclic GMP-AMP. Nature 2019; 567(7748): 389-93.
[http://dx.doi.org/10.1038/s41586-019-0998-5] [PMID: 30842659]
[38]
Liu S, Cai X, Wu J, et al. Phosphorylation of innate immune adaptor proteins MAVS, STING, and TRIF induces IRF3 activation. Science 2015; 347(6227)aaa2630
[http://dx.doi.org/10.1126/science.aaa2630] [PMID: 25636800]
[39]
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(7485): 691-5.
[http://dx.doi.org/10.1038/nature12862] [PMID: 24284630]
[40]
B G. K P, J A, N M S B, TM S. Emerging alphaviruses are sensitive to cellular states induced by a novel small-molecule agonist of the STING pathway. J Virol 2018; 92(6)
[41]
Ma Z, Jacobs SR, West JA, et al. Modulation of the cGAS-STING DNA sensing pathway by gammaherpesviruses. Proc Natl Acad Sci USA 2015; 112(31): E4306-15.
[http://dx.doi.org/10.1073/pnas.1503831112] [PMID: 26199418]
[42]
Orzalli MH, Broekema NM, Diner BA, et al. cGAS-mediated stabilization of IFI16 promotes innate signaling during herpes simplex virus infection. Proc Natl Acad Sci USA 2015; 112(14): E1773-81.
[http://dx.doi.org/10.1073/pnas.1424637112] [PMID: 25831530]
[43]
Almine JF, O'Hare CA, Dunphy G, et al. IFI16 and cGAS cooperate in the activation of STING during DNA sensing in human keratinocytes 2017; 8 14392.
[44]
Gluck S, Guey B, Gulen MF, et al. Innate immune sensing of cytosolic chromatin fragments through cGAS promotes senescence. Nature Cell Biol 2017; 19(9): 1061-70.
[45]
Stavrou S, Aguilera AN, Blouch K, Ross SR. DDX41 Recognizes RNA/DNA retroviral reverse transcripts and is critical for in vivo control of murine leukemia virus infection. mbio 2018;; 9(3) e00923.
[46]
Lai JH, Wang MY, Huang CY, et al. Infection with the dengue RNA virus activates TLR9 signaling in human dendritic cells. EMBO Rep 2018; 19(8)e46182
[http://dx.doi.org/10.15252/embr.201846182]
[47]
Mankan AK, Schmidt T, Chauhan D, et al. Cytosolic RNA:DNA hybrids activate the cGAS-STING axis. EMBO J 2014; 33(24): 2937-46.
[http://dx.doi.org/10.15252/embj.201488726] [PMID: 25425575]
[48]
Bridgeman A, Maelfait J, Davenne T, et al. Viruses transfer the antiviral second messenger cGAMP between cells. Science 2015; 349(6253): 1228-32.
[http://dx.doi.org/10.1126/science.aab3632] [PMID: 26229117]
[49]
Gentili M, Kowal J, Tkach M, et al. Transmission of innate immune signaling by packaging of cGAMP in viral particles. Science 2015; 349(6253): 1232-6.
[http://dx.doi.org/10.1126/science.aab3628] [PMID: 26229115]
[50]
Chiu YH, Macmillan JB, Chen ZJ. RNA polymerase III detects cytosolic DNA and induces type I interferons through the RIG-I pathway. Cell 2009; 138(3): 576-91.
[http://dx.doi.org/10.1016/j.cell.2009.06.015] [PMID: 19631370]
[51]
Unterholzner L. The interferon response to intracellular DNA: why so many receptors? Immunobiology 2013; 218(11): 1312-21.
[http://dx.doi.org/10.1016/j.imbio.2013.07.007] [PMID: 23962476]
[52]
Burdette DL, Monroe KM, Sotelo-Troha K, et al. STING is a direct innate immune sensor of cyclic di-GMP. Nature 2011; 478(7370): 515-8.
[http://dx.doi.org/10.1038/nature10429] [PMID: 21947006]
[53]
Larabi A, Devos JM, Ng SL, et al. Crystal structure and mechanism of activation of TANK-binding kinase 1. Cell Rep 2013; 3(3): 734-46.
[http://dx.doi.org/10.1016/j.celrep.2013.01.034] [PMID: 23453971]
[54]
Goncalves A, Bürckstümmer T, Dixit E, et al. Functional dissection of the TBK1 molecular network. PLoS One 2011; 6(9)e23971
[http://dx.doi.org/10.1371/journal.pone.0023971] [PMID: 21931631]
[55]
Pomerantz JL, Baltimore D. NF-kappaB activation by a signaling complex containing TRAF2, TANK and TBK1, a novel IKK-related kinase. EMBO J 1999; 18(23): 6694-704.
[http://dx.doi.org/10.1093/emboj/18.23.6694] [PMID: 10581243]
[56]
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(5622): 1148-51.
[http://dx.doi.org/10.1126/science.1081315] [PMID: 12702806]
[57]
Ishii KJ, Kawagoe T, Koyama S, et al. TANK-binding kinase-1 delineates innate and adaptive immune responses to DNA vaccines. Nature 2008; 451(7179): 725-9.
[http://dx.doi.org/10.1038/nature06537] [PMID: 18256672]
[58]
H.C H. JE H. Chemistry BAJTJob cytosolic DNA promotes signal transducer and activator of transcription 3 (STAT3) phosphorylation by TANK-binding Kinase 1 (TBK1) to restrain STAT3 activity. J Biol Chem 2017; 292(13): 5405-17.
[59]
Juang YT, Lowther W, Kellum M, et al. Primary activation of interferon A and interferon B gene transcription by interferon regulatory factor 3. Proc Natl Acad Sci USA 1998; 95(17): 9837-42.
[http://dx.doi.org/10.1073/pnas.95.17.9837] [PMID: 9707562]
[60]
Novoselova EG, Khrenov MO, Parfenyuk SB, Novoselova TV, Lunin SM, Fesenko EE. The NF-kappaB, IRF3, and SAPK/JNK signaling cascades of animal immune cells and their role in the progress of type 1 diabetes mellitus. Doklady biological sciences: proceedings of the Academy of Sciences of the USSR, Biological sciences sections 2014; 457(1): 255-7..
[61]
Becher PM, Hinrichs S, Fluschnik N, et al. Role of Toll-like receptors and interferon regulatory factors in different experimental heart failure models of diverse etiology: IRF7 as novel cardiovascular stress-inducible factor. PLoS One 2018; 13(3)e0193844
[http://dx.doi.org/10.1371/journal.pone.0193844] [PMID: 29538462]
[62]
Wang YY, Ye ZY, Zhao ZS, Tao HQ, Li SG. Systems biology approach to identification of biomarkers for metastatic progression in gastric cancer. J Cancer Res Clin Oncol 2010; 136(1): 135-41.
[http://dx.doi.org/10.1007/s00432-009-0644-y] [PMID: 19649653]
[63]
Rustagi A, Gale M Jr. Innate antiviral immune signaling, viral evasion and modulation by HIV-1. J Mol Biol 2014; 426(6): 1161-77.
[http://dx.doi.org/10.1016/j.jmb.2013.12.003] [PMID: 24326250]
[64]
Takahasi K, Suzuki NN, Horiuchi M, et al. X-ray crystal structure of IRF-3 and its functional implications. Nat Struct Biol 2003; 10(11): 922-7.
[http://dx.doi.org/10.1038/nsb1001] [PMID: 14555995]
[65]
Qin BY, Liu C, Lam SS, et al. Crystal structure of IRF-3 reveals mechanism of autoinhibition and virus-induced phosphoactivation. Nat Struct Biol 2003; 10(11): 913-21.
[http://dx.doi.org/10.1038/nsb1002] [PMID: 14555996]
[66]
Jin L, Hill KK, Filak H, et al. MPYS is required for IFN response factor 3 activation and type I IFN production in the response of cultured phagocytes to bacterial second messengers cyclic-di-AMP and cyclic-di-GMP. Journal of immunology (Baltimore, Md : 1950) 2011; 187(5): 2595-601..
[http://dx.doi.org/10.4049/jimmunol.1100088]
[67]
Schoggins JW, Rice CM. Interferon-stimulated genes and their antiviral effector functions. Curr Opin Virol 2011; 1(6): 519-25.
[http://dx.doi.org/10.1016/j.coviro.2011.10.008] [PMID: 22328912]
[68]
Akira S, Saitoh T, Kawai T. [Nucleic acids recognition by innate immunity]. Uirusu 2012; 62(1): 39-45.
[http://dx.doi.org/10.2222/jsv.62.39] [PMID: 23189823]
[69]
Tsuchida T, Zou J, Saitoh T, et al. The ubiquitin ligase TRIM56 regulates innate immune responses to intracellular double-stranded DNA. Immunity 2010; 33(5): 765-76.
[http://dx.doi.org/10.1016/j.immuni.2010.10.013] [PMID: 21074459]
[70]
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(34): 28646-55.
[http://dx.doi.org/10.1074/jbc.M112.362608] [PMID: 22745133]
[71]
Zhong B, Zhang L, Lei C, et al. The ubiquitin ligase RNF5 regulates antiviral responses by mediating degradation of the adaptor protein MITA. Immunity 2009; 30(3): 397-407.
[http://dx.doi.org/10.1016/j.immuni.2009.01.008] [PMID: 19285439]
[72]
Qin Y, Zhou MT, Hu MM, et al. RNF26 temporally regulates virus-triggered type I interferon induction by two distinct mechanisms. PLoS Pathog 2014; 10(9)e1004358
[http://dx.doi.org/10.1371/journal.ppat.1004358] [PMID: 25254379]
[73]
Heaton SM, Borg NA, Dixit VM. Ubiquitin in the activation and attenuation of innate antiviral immunity. J Exp Med 2016; 213(1): 1-13.
[http://dx.doi.org/10.1084/jem.20151531] [PMID: 26712804]
[74]
Konno H, Konno K, Barber GN. Cyclic dinucleotides trigger ULK1 (ATG1) phosphorylation of STING to prevent sustained innate immune signaling. Cell 2013; 155(3): 688-98.
[http://dx.doi.org/10.1016/j.cell.2013.09.049] [PMID: 24119841]
[75]
Tanaka Y, Chen ZJ. STING specifies IRF3 phosphorylation by TBK1 in the cytosolic DNA signaling pathway. Sci Signal 2012; 5(214): ra20.
[http://dx.doi.org/10.1126/scisignal.2002521] [PMID: 22394562]
[76]
Z H. , XC, BY. Developmental CDJ, immunology c Cloning and functional characterization of rat stimulator of interferon genes (STING) regulated by miR-24 2012; 37: 414-20..
[77]
Wang G, Yan Y, Zheng Z, Zhang T. The mechanism of hsa-miR-424-5 combining PD-1 through mTORC signaling pathway to stimulate immune effect and participate in type 1 diabetes 2020.40(3): BSR20193800.
[78]
Ablasser A, Hertrich C, Waßermann R, Hornung V. Nucleic acid driven sterile inflammation. Clin Immunol 2013; 147(3): 207-15.
[http://dx.doi.org/10.1016/j.clim.2013.01.003] [PMID: 23419883]
[79]
Pokatayev V, Hasin N, Chon H, et al. RNase H2 catalytic core Aicardi-Goutières syndrome-related mutant invokes cGAS-STING innate immune-sensing pathway in mice. J Exp Med 2016; 213(3): 329-36.
[http://dx.doi.org/10.1084/jem.20151464] [PMID: 26880576]
[80]
Toda S, Nishi C, Yanagihashi Y, Segawa K, Nagata S. Clearance of apoptotic cells and pyrenocytes. Curr Top Dev Biol 2015; 114: 267-95.
[http://dx.doi.org/10.1016/bs.ctdb.2015.07.017] [PMID: 26431571]
[81]
Barber GN. STING: infection, inflammation and cancer. Nat Rev Immunol 2015; 15(12): 760-70.
[http://dx.doi.org/10.1038/nri3921] [PMID: 26603901]
[82]
Ahn J, Ruiz P, Barber GN. Intrinsic self-DNA triggers inflammatory disease dependent on STING. J Immunol (Baltimore, Md : 1950) 2014; 193(9): 4634-2..
[http://dx.doi.org//10.4049/jimmunol.1401337]
[83]
Ahn J, Konno H, Barber GN. Diverse roles of STING-dependent signaling on the development of cancer. Oncogene 2015; 34(41): 5302-8.
[http://dx.doi.org/10.1038/onc.2014.457] [PMID: 25639870]
[84]
DH OD. Mao Y, Mele DA. The next generation of pattern recognition receptor agonists: improving response rates in cancer immunotherapy. Curr Med Chem 2019. Online ahead of print.
[85]
Cui J, Chen Y, Wang HY, Wang RF. Mechanisms and pathways of innate immune activation and regulation in health and cancer. Hum Vaccin Immunother 2014; 10(11): 3270-85.
[http://dx.doi.org/10.4161/21645515.2014.979640] [PMID: 25625930]
[86]
An X, Zhu Y, Zheng T, et al. An analysis of the expression and association with immune cell infiltration of the cgas/sting pathway in pan-cancer. Mol Ther Nucleic Acids 2019; 14: 80-9.
[http://dx.doi.org/10.1016/j.omtn.2018.11.003] [PMID: 30583098]
[87]
Ohkuri T, Ghosh A, Kosaka A, et al. STING contributes to antiglioma immunity via triggering type I IFN signals in the tumor microenvironment. Cancer Immunol Res 2014; 2(12): 1199-208.
[http://dx.doi.org/10.1158/2326-6066.CIR-14-0099] [PMID: 25300859]
[88]
Ohkuri T, Kosaka A, Ishibashi K, et al. Intratumoral administration of cGAMP transiently accumulates potent macrophages for anti-tumor immunity at a mouse tumor site. Cancer Immunol Immunother 2017; 66(6): 705-16.
[http://dx.doi.org/10.1007/s00262-017-1975-1] [PMID: 28243692]
[89]
Della-Corte CM, Shen T, Gay CM, et al. STING pathway expression identifies non-small cell lung cancers with an immune-responsive phenotype. J Thorac Oncol 2020; 15(5): 777-91.
[90]
Sharma A, Johnson A. Exosome DNA: Critical regulator of tumor immunity and a diagnostic biomarker. J Cell Physiol 2020; 235(3): 1921-32.
[91]
Härtlova A, Erttmann SF, Raffi FA, 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(2): 332-43.
[http://dx.doi.org/10.1016/j.immuni.2015.01.012] [PMID: 25692705]
[92]
Woo SR, Fuertes MB, Corrales L, et al. STING-dependent cytosolic DNA sensing mediates innate immune recognition of immunogenic tumors. Immunity 2014; 41(5): 830-42.
[http://dx.doi.org/10.1016/j.immuni.2014.10.017] [PMID: 25517615]
[93]
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(10): 1989-2003.
[http://dx.doi.org/10.1084/jem.20101158] [PMID: 21930769]
[94]
Barry M, Bleackley RC. Cytotoxic T lymphocytes: all roads lead to death. Nat Rev Immunol 2002; 2(6): 401-9.
[http://dx.doi.org/10.1038/nri819] [PMID: 12093006]
[95]
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(5): 843-52.
[http://dx.doi.org/10.1016/j.immuni.2014.10.019] [PMID: 25517616]
[96]
Demaria O, De Gassart A, Coso S, et al. STING activation of tumor endothelial cells initiates spontaneous and therapeutic antitumor immunity. Proc Natl Acad Sci USA 2015; 112(50): 15408-13.
[http://dx.doi.org/10.1073/pnas.1512832112] [PMID: 26607445]
[97]
Koshy ST, Cheung AS, Gu L, Graveline AR, Mooney DJ. Liposomal delivery enhances immune activation by sting agonists for cancer immunotherapy. Adv Biosyst 2017; 1(1-2)1600013
[http://dx.doi.org/10.1002/adbi.201600013] [PMID: 30258983]
[98]
Corrales L, Gajewski TF. 2015.
[99]
Berges C, Naujokat C, Tinapp S, et al. A cell line model for the differentiation of human dendritic cells. Biochem Biophys Res Commun 2005; 333(3): 896-907.
[http://dx.doi.org/10.1016/j.bbrc.2005.05.171] [PMID: 15963458]
[100]
Corrales L, Matson V, Flood B, Spranger S, Gajewski TF. Innate immune signaling and regulation in cancer immunotherapy. Cell Res 2017; 27(1): 96-108.
[http://dx.doi.org/10.1038/cr.2016.149] [PMID: 27981969]
[101]
Corrales L, McWhirter SM, Dubensky TW Jr, Gajewski TF. The host STING pathway at the interface of cancer and immunity. J Clin Invest 2016; 126(7): 2404-11.
[http://dx.doi.org/10.1172/JCI86892] [PMID: 27367184]
[102]
Gravekamp C, Chandra D. Targeting STING pathways for the treatment of cancer. OncoImmunology 2015; 4(12)e988463
[http://dx.doi.org/10.4161/2162402X.2014.988463] [PMID: 26587334]
[103]
Falahat R, Perez-Villarroel P, Mailloux AW, et al. STING signaling in melanoma cells shapes antigenicity and can promote antitumor T-cell activity. Cancer Immunol Res 2019; 7(11): 1837-48.
[http://dx.doi.org/10.1158/2326-6066.CIR-19-0229] [PMID: 31462408]
[104]
Zhu Q, Man SM, Gurung P, et al. 2014.
[105]
Lu S, Concha-Benavente F, Shayan G, et al. STING activation enhances cetuximab-mediated NK cell activation and DC maturation and correlates with HPV+ status in head and neck cancer. Oral Oncol 2018; 78: 186-93.
[http://dx.doi.org/10.1016/j.oraloncology.2018.01.019] [PMID: 29496049]
[106]
Sen T, Rodriguez BL, Chen L, et al. Targeting DNA damage response promotes antitumor immunity through sting-mediated t-cell activation in small cell lung cancer. Cancer Discov 2019; 9(5): 646-61.
[http://dx.doi.org/10.1158/2159-8290.CD-18-1020] [PMID: 30777870]
[107]
Bui JD, Schreiber RD. Cancer immunosurveillance, immunoediting and inflammation: independent or interdependent processes? Curr Opin Immunol 2007; 19(2): 203-8.
[http://dx.doi.org/10.1016/j.coi.2007.02.001] [PMID: 17292599]
[108]
Junkins RD, Gallovic MD, Johnson BM, et al. 2018.
[109]
Yi G, Brendel VP, Shu C, Li P, Palanathan S, Cheng Kao C. Single nucleotide polymorphisms of human STING can affect innate immune response to cyclic dinucleotides. PLoS One 2013; 8(10)e77846
[http://dx.doi.org/10.1371/journal.pone.0077846] [PMID: 24204993]
[110]
Sauer JD, Sotelo-Troha K, von Moltke J, 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(2): 688-94.
[http://dx.doi.org/10.1128/IAI.00999-10] [PMID: 21098106]
[111]
Kim YJ. STINGing the Tumor’s immune evasion mechanism. OncoImmunology 2018; 7(4)e1083673
[http://dx.doi.org/10.1080/2162402X.2015.1083673] [PMID: 29632707]
[112]
Fu J, Kanne DB, Leong M, et al. STING agonist formulated cancer vaccines can cure established tumors resistant to PD-1 blockade. Sci Transl Med 2015; 7(283)283ra52
[http://dx.doi.org/10.1126/scitranslmed.aaa4306] [PMID: 25877890]
[113]
Spranger S, Koblish HK, Horton B, Scherle PA, Newton R, Gajewski TF. Mechanism of tumor rejection with doublets of CTLA-4, PD-1/PD-L1, or IDO blockade involves restored IL-2 production and proliferation of CD8(+) T cells directly within the tumor microenvironment. J Immunother Cancer 2014; 2: 3.
[http://dx.doi.org/10.1186/2051-1426-2-3] [PMID: 24829760]
[114]
Ghaffari A, Peterson N, Khalaj K, et al. STING agonist therapy in combination with PD-1 immune checkpoint blockade enhances response to carboplatin chemotherapy in high-grade serous ovarian cancer. Br J Cancer 2018; 119(4): 440-9.
[http://dx.doi.org/10.1038/s41416-018-0188-5] [PMID: 30046165]
[115]
Liu D, Wu H, Wang C, et al. STING directly activates autophagy to tune the innate immune response. Cell Death Differ 2019; 26(9): 1735-49.
[http://dx.doi.org/10.1038/s41418-018-0251-z] [PMID: 30568238]
[116]
Gui X, Yang H, Li T, et al. Autophagy induction via STING trafficking is a primordial function of the cGAS pathway. Nature 2019; 567(7747): 262-6.
[http://dx.doi.org/10.1038/s41586-019-1006-9] [PMID: 30842662]
[117]
Diner BA, Lum KK, Toettcher JE, Cristea IM. 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 2016; 7(6): e01553-16.
[http://dx.doi.org/10.1128/mBio.01553-16] [PMID: 27935834]
[118]
Ohkuri T, Ghosh A, Kosaka A, Sarkar SN, Okada H. Protective role of STING against gliomagenesis: Rational use of STING agonist in anti-glioma immunotherapy. OncoImmunology 2015; 4(4)e999523
[http://dx.doi.org/10.1080/2162402X.2014.999523] [PMID: 26137417]
[119]
Watkins-Schulz R, Tiet P, Gallovic MD, et al. A microparticle platform for STING-targeted immunotherapy enhances natural killer cell- and CD8+ T cell-mediated anti-tumor immunity. Biomaterials 2019; 205: 94-105.
[http://dx.doi.org/10.1016/j.biomaterials.2019.03.011] [PMID: 30909112]
[120]
Shae D, Becker KW, Christov P, et al. Endosomolytic polymersomes increase the activity of cyclic dinucleotide STING agonists to enhance cancer immunotherapy. Nat Nanotechnol 2019; 14(3): 269-78.
[http://dx.doi.org/10.1038/s41565-018-0342-5] [PMID: 30664751]
[121]
Leach DG, Dharmaraj N, Piotrowski SL, et al. STINGel: Controlled release of a cyclic dinucleotide for enhanced cancer immunotherapy. Biomaterials 2018; 163: 67-75.
[http://dx.doi.org/10.1016/j.biomaterials.2018.01.035] [PMID: 29454236]
[122]
Yang H, Lee WS, Kong SJ, et al. STING activation reprograms tumor vasculatures and synergizes with VEGFR2 blockade. J Clin Invest 2019; 129(10): 4350-64.
[http://dx.doi.org/10.1172/JCI125413] [PMID: 31343989]
[123]
Moore E, Clavijo PE, Davis R, et al. Established T Cell-inflamed tumors rejected after adaptive resistance was reversed by combination STING activation and PD-1 pathway blockade. Cancer Immunol Res 2016; 4(12): 1061-71.
[http://dx.doi.org/10.1158/2326-6066.CIR-16-0104] [PMID: 27821498]
[124]
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(1): 50-61.
[http://dx.doi.org/10.1158/0008-5472.CAN-14-3619] [PMID: 26567136]
[125]
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(7): 1018-30.
[http://dx.doi.org/10.1016/j.celrep.2015.04.031] [PMID: 25959818]
[126]
Weiss JM, Guérin MV, Regnier F, et al. The STING agonist DMXAA triggers a cooperation between T lymphocytes and myeloid cells that leads to tumor regression. OncoImmunology 2017; 6(10)e1346765
[http://dx.doi.org/10.1080/2162402X.2017.1346765] [PMID: 29123960]
[127]
Bähr O, Gross S, Harter PN, et al. ASA404, a vascular disrupting agent, as an experimental treatment approach for brain tumors. Oncol Lett 2017; 14(5): 5443-51.
[PMID: 29098034]
[128]
Jing W, McAllister D, Vonderhaar EP, et al. STING agonist inflames the pancreatic cancer immune microenvironment and reduces tumor burden in mouse models. J Immunother Cancer 2019; 7(1): 115.
[http://dx.doi.org/10.1186/s40425-019-0573-5] [PMID: 31036082]
[129]
Curran E, Chen X, Corrales L, et al. STING pathway activation stimulates potent immunity against acute myeloid leukemia. Cell Rep 2016; 15(11): 2357-66.
[http://dx.doi.org/10.1016/j.celrep.2016.05.023] [PMID: 27264175]
[130]
Chen D, Tong J, Yang L, et al. PUMA amplifies necroptosis signaling by activating cytosolic DNA sensors. Proc Natl Acad Sci USA 2018; 115(15): 3930-5.
[PMID: 29581256]
[131]
Laganà AS, Vitale SG, Salmeri FM, et al. Unus pro omnibus, omnes pro uno: A novel, evidence-based, unifying theory for the pathogenesis of endometriosis. Med Hypotheses 2017; 103: 10-20.
[PMID: 28571791]
[132]
Sturlese E, Salmeri FM, Retto G, et al. Dysregulation of the Fas/FasL system in mononuclear cells recovered from peritoneal fluid of women with endometriosis. J Reprod Immunol 2011; 92(1-2): 74-81.
[PMID: 21978769]
[133]
Wang H, Jin P, Sabatino M, et al. Comparison of endometrial regenerative cells and bone marrow stromal cells. J Transl Med 2012; 10: 207.
[PMID: 23038994]
[134]
Li L, Wang TL, Seckin T, Sehars J, Shih le-M. Epithelial cells in endometriosis and adenomyosis upregulate sting expression. Reprod Sci 2020; 27(5)
[135]
Laganà AS, Vitale SG, Sapia F, et al. miRNA expression for early diagnosis of preeclampsia onset: hope or hype? J Matern Fetal Neonatal Med 2018; 31(6): 817-21.
[PMID: 28282763]
[136]
Chiofalo B, Laganà AS, Vaiarelli A, et al. Do miRNAs play a role in fetal growth restriction? A fresh look to a busy corner. BioMed Res Int 2017; 20176073167
[PMID: 28466013]
[137]
2018.
[138]
Larkin B, Ilyukha V. 2017.
[139]
Kitai Y, Kawasaki T, Sueyoshi T, Kobiyama K, Ishii KJ. DNA-Containing Exosomes Derived from Cancer Cells Treated with Topotecan Activate a STING-Dependent Pathway and Reinforce Antitumor Immunity 2017; 198(4): 1649-59.
[140]
Ramanjulu JM, Pesiridis GS, Yang J, et al. Design of amidobenzimidazole STING receptor agonists with systemic activity. Nature 2018; 564(7736): 439-43.
[http://dx.doi.org/10.1038/s41586-018-0705-y] [PMID: 30405246]
[141]
Chen H, Sun H, You F, et al. Activation of STAT6 by STING is critical for antiviral innate immunity. Cell 2011; 147(2): 436-46.
[http://dx.doi.org/10.1016/j.cell.2011.09.022] [PMID: 22000020]
[142]
Wang Z, Celis E. STING activator c-di-GMP enhances the anti-tumor effects of peptide vaccines in melanoma-bearing mice. Cancer Immunol Immunother 2015; 64(8): 1057-66.
[http://dx.doi.org/10.1007/s00262-015-1713-5] [PMID: 25986168]

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