REVIEW
Crosstalk between RNA viruses and DNA sensors: Role of the cGAS-STING signalling pathway
Yiyun Michelle Fan,
Yizhuo Lyanne Zhang,
Honglin Luo,
Yasir Mohamud,
Yiyun Michelle Fan
Center for Heart Lung Innovation, St. Paul's Hospital, University of British Columbia, Vancouver, British Columbia, Canada
Department of Cellular & Physiological Sciences, University of British Columbia, Vancouver, British Columbia, Canada
Search for more papers by this authorYizhuo Lyanne Zhang
Center for Heart Lung Innovation, St. Paul's Hospital, University of British Columbia, Vancouver, British Columbia, Canada
Department of Cellular & Physiological Sciences, University of British Columbia, Vancouver, British Columbia, Canada
Search for more papers by this authorCorresponding Author
Honglin Luo
Center for Heart Lung Innovation, St. Paul's Hospital, University of British Columbia, Vancouver, British Columbia, Canada
Department of Pathology and Laboratory Medicine, University of British Columbia, Vancouver, British Columbia, Canada
Correspondence
Honglin Luo and Yasir Mohamud, Centre for Heart Lung Innovation, Department of Pathology and Laboratory of Medicine, University of British Columbia, St. Paul's Hospital, Room 166, 1081 Burrard Street, Vancouver, BC V6Z 1Y6, Canada.
Email: [email protected] and [email protected]
Search for more papers by this authorCorresponding Author
Yasir Mohamud
Center for Heart Lung Innovation, St. Paul's Hospital, University of British Columbia, Vancouver, British Columbia, Canada
Department of Pathology and Laboratory Medicine, University of British Columbia, Vancouver, British Columbia, Canada
Correspondence
Honglin Luo and Yasir Mohamud, Centre for Heart Lung Innovation, Department of Pathology and Laboratory of Medicine, University of British Columbia, St. Paul's Hospital, Room 166, 1081 Burrard Street, Vancouver, BC V6Z 1Y6, Canada.
Email: [email protected] and [email protected]
Search for more papers by this authorYiyun Michelle Fan,
Yizhuo Lyanne Zhang,
Honglin Luo,
Yasir Mohamud,
Yiyun Michelle Fan
Center for Heart Lung Innovation, St. Paul's Hospital, University of British Columbia, Vancouver, British Columbia, Canada
Department of Cellular & Physiological Sciences, University of British Columbia, Vancouver, British Columbia, Canada
Search for more papers by this authorYizhuo Lyanne Zhang
Center for Heart Lung Innovation, St. Paul's Hospital, University of British Columbia, Vancouver, British Columbia, Canada
Department of Cellular & Physiological Sciences, University of British Columbia, Vancouver, British Columbia, Canada
Search for more papers by this authorCorresponding Author
Honglin Luo
Center for Heart Lung Innovation, St. Paul's Hospital, University of British Columbia, Vancouver, British Columbia, Canada
Department of Pathology and Laboratory Medicine, University of British Columbia, Vancouver, British Columbia, Canada
Correspondence
Honglin Luo and Yasir Mohamud, Centre for Heart Lung Innovation, Department of Pathology and Laboratory of Medicine, University of British Columbia, St. Paul's Hospital, Room 166, 1081 Burrard Street, Vancouver, BC V6Z 1Y6, Canada.
Email: [email protected] and [email protected]
Search for more papers by this authorCorresponding Author
Yasir Mohamud
Center for Heart Lung Innovation, St. Paul's Hospital, University of British Columbia, Vancouver, British Columbia, Canada
Department of Pathology and Laboratory Medicine, University of British Columbia, Vancouver, British Columbia, Canada
Correspondence
Honglin Luo and Yasir Mohamud, Centre for Heart Lung Innovation, Department of Pathology and Laboratory of Medicine, University of British Columbia, St. Paul's Hospital, Room 166, 1081 Burrard Street, Vancouver, BC V6Z 1Y6, Canada.
Email: [email protected] and [email protected]
Search for more papers by this authorYiyun Michelle Fan and Yizhuo Lyanne Zhang contributed equally to this study.
Abstract
Despite only comprising half of all known viral species, RNA viruses are disproportionately responsible for many of the worst epidemics in human history, including outbreaks of influenza, poliomyelitis, Ebola, and most recently, the coronavirus disease-2019 (COVID-19) pandemic. The propensity for RNA viruses to replicate in cytosolic compartments has led to an evolutionary arms race and the emergence of cytosolic sensors to recognise and initiate the host innate immune response. Although significant progress has been made in identifying and characterising cytosolic RNA sensors as anti-viral innate immune factors, the potential role for cytosolic DNA sensors in RNA viral infection is only recently being appreciated. Among these, the cyclic GMP-AMP synthase (cGAS)-stimulator of interferon genes (STING) pathway has attracted increasing attention. The cGAS-STING signalling pathway has emerged as a key innate immune signalling axis that is implicated in diverse human diseases from infectious diseases to neurodegeneration and cancer. Here we review the existing literature on RNA viruses and their reciprocal interactions with the cGAS-STING pathway and share insights into RNA virus diversity by touching on the similarities and differences of RNA viral strategies.
CONFLICT OF INTEREST
The authors declare no conflict of interest.
Open Research
DATA AVAILABLITY STATEMENT
Data sharing is not applicable as no datasets were generated or analysed in the current study.
REFERENCES
- 1Jacob ST, Crozier I, Fischer WA, 2nd, et al. Ebola virus disease. Nat Rev Dis Primers. 2020; 6:13. https://doi.org/10.1038/s41572-020-0147-3
- 2Hayward A. Origin of the retroviruses: when, where, and how? Curr Opin Virol. 2017; 25: 23-27. https://doi.org/10.1016/j.coviro.2017.06.006
- 3Saez-Cirion A, Manel N. Immune responses to retroviruses. Annu Rev Immunol. 2018; 36: 193-220. https://doi.org/10.1146/annurev-immunol-051116-052155
- 4Hiscox JA. RNA viruses: hijacking the dynamic nucleolus. Nat Rev Microbiol. 2007; 5: 119-127. https://doi.org/10.1038/nrmicro1597
- 5Carrasco-Hernandez R, Jacome R, Lopez Vidal Y, Ponce de Leon S. Are RNA viruses candidate agents for the next global pandemic? A review. ILAR J. 2017; 58: 343-358. https://doi.org/10.1093/ilar/ilx026
- 6Zhou P, Yang XL, Wang XG, et al. A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature. 2020; 579: 270-273. https://doi.org/10.1038/s41586-020-2012-7
- 7Zhu N, Zhang D, Wang W, et al. A novel coronavirus from patients with pneumonia in China, 2019. N Engl J Med. 2020; 382: 727-733. https://doi.org/10.1056/NEJMoa2001017
- 8Ehreth J. The economics of vaccination from a global perspective: present and future. 2-3 December, 2004, Vaccines: all things considered, San Francisco, CA, USA. Expert Rev Vaccines. 2005; 4: 19-21. https://doi.org/10.1586/14760584.4.1.19
- 9Chen N, Xia P, Li S, Zhang T, Wang TT, Zhu J. RNA sensors of the innate immune system and their detection of pathogens. IUBMB Life. 2017; 69: 297-304. https://doi.org/10.1002/iub.1625
- 10Katze MG, Fornek JL, Palermo RE, Walters KA, Korth MJ. Innate immune modulation by RNA viruses: emerging insights from functional genomics. Nat Rev Immunol. 2008; 8: 644-654. https://doi.org/10.1038/nri2377
- 11Xu Q, Tang Y, Huang G. Innate immune responses in RNA viral infection. Front Med. 2021; 15: 333-346. https://doi.org/10.1007/s11684-020-0776-7
- 12Mesev EV, LeDesma RA, Ploss A. Decoding type I and III interferon signalling during viral infection. Nat Microbiol. 2019; 4: 914-924. https://doi.org/10.1038/s41564-019-0421-x
- 13Wack A, Terczynska-Dyla E, Hartmann R. Guarding the frontiers: the biology of type III interferons. Nat Immunol. 2015; 16: 802-809. https://doi.org/10.1038/ni.3212
- 14Castro F, Cardoso AP, Goncalves RM, Serre K, Oliveira MJ. Interferon-gamma at the crossroads of tumor immune surveillance or evasion. Front Immunol. 2018; 9:Artn 847. https://doi.org/10.3389/Fimmu.2018.00847
- 15Chiang SC, Theorell J, Entesarian M, et al. Comparison of primary human cytotoxic T-cell and natural killer cell responses reveal similar molecular requirements for lytic granule exocytosis but differences in cytokine production. Blood. 2013; 121: 1345-1356. https://doi.org/10.1182/blood-2012-07-442558
- 16Lee AJ, Ashkar AA. The dual nature of type I and type II interferons. Front Immunol. 2018; 9. https://doi.org/10.3389/fimmu.2018.02061
- 17Larkin B, Ilyukha V, Sorokin M, Buzdin A, Vannier E, Poltorak A. Cutting edge: activation of STING in T cells induces type I IFN responses and cell death. J Immunol. 2017; 199: 397-402. https://doi.org/10.4049/jimmunol.1601999
- 18Souza-Fonseca-Guimaraes F, Parlato M, de Oliveira RB, et al. Interferon-gamma and granulocyte/monocyte colony-stimulating factor production by natural killer cells involves different signaling pathways and the adaptor stimulator of interferon genes (STING). J Biol Chem. 2013; 288: 10715-10721. https://doi.org/10.1074/jbc.M112.435602
- 19Serrano R, Lettau M, Zarobkiewicz M, Wesch D, Peters C, Kabelitz D. Stimulatory and inhibitory activity of STING ligands on tumor-reactive human gamma/delta T cells. Oncoimmunology. 2022; 11:2030021. https://doi.org/10.1080/2162402X.2022.2030021
- 20Nishikawa Y, Matsuzaki Y, Kimura K, Rokunohe A, Nakano H, Sawamura D. Modulation of stimulator of interferon genes (STING) expression by interferon-gamma in human keratinocytes. Biochem Genet. 2018; 56: 93-102. https://doi.org/10.1007/s10528-017-9832-7
- 21Murira A, Lamarre A. Type-I interferon responses: from friend to foe in the battle against chronic viral infection. Front Immunol. 2016; 7:609. https://doi.org/10.3389/fimmu.2016.00609
- 22Uehata T, Takeuchi O. RNA recognition and immunity-innate immune sensing and its posttranscriptional regulation mechanisms. Cells. 2020; 9:Artn 1701. https://doi.org/10.3390/Cells9071701
- 23McNab F, Mayer-Barber K, Sher A, Wack A, O'Garra A. Type I interferons in infectious disease. Nat Rev Immunol. 2015; 15: 87-103. https://doi.org/10.1038/nri3787
- 24Decout A, Katz JD, Venkatraman S, Ablasser A. The cGAS-STING pathway as a therapeutic target in inflammatory diseases. Nat Rev Immunol. 2021. https://doi.org/10.1038/s41577-021-00524-z
- 25Motwani M, Pesiridis S, Fitzgerald KA. DNA sensing by the cGAS-STING pathway in health and disease. Nat Rev Genet. 2019; 20: 657-674. https://doi.org/10.1038/s41576-019-0151-1
- 26Sun 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: 786-791. https://doi.org/10.1126/science.1232458
- 27Burdette DL, Monroe KM, Sotelo-Troha K, et al. STING is a direct innate immune sensor of cyclic di-GMP. Nature. 2011; 478: 515-518. https://doi.org/10.1038/nature10429
- 28Ishikawa H, Barber GN. STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling. Nature. 2008; 455: 674-678. https://doi.org/10.1038/nature07317
- 29Dobbs N, Burnaevskiy N, Chen D, Gonugunta VK, Alto NM, Yan N. STING activation by translocation from the ER is associated with infection and autoinflammatory disease. Cell Host Microbe. 2015; 18: 157-168. https://doi.org/10.1016/j.chom.2015.07.001
- 30Mukai K, Konno H, Akiba T, et al. Activation of STING requires palmitoylation at the Golgi. Nat Commun. 2016; 7:11932. https://doi.org/10.1038/ncomms11932
- 31Taguchi T, Mukai K, Takaya E, Shindo R. STING operation at the ER/Golgi interface. Front Immunol. 2021; 12:646304. https://doi.org/10.3389/fimmu.2021.646304
- 32Kemmoku H, Kuchitsu Y, Mukai K, Taguchi T. Specific association of TBK1 with the trans-Golgi network following STING stimulation. Cell Struct Funct. 2022. https://doi.org/10.1247/csf.21080
- 33Balka KR, Louis C, Saunders TL, et al. TBK1 and IKK epsilon act redundantly to mediate STING-induced NF-kappa B responses in myeloid cells. Cell Rep. 2020; 31:Artn 107492. https://doi.org/10.1016/J.Celrep.2020.03.056
- 34Abe T, Barber GN. Cytosolic-DNA-mediated, STING-dependent proinflammatory gene induction necessitates canonical NF-kappa B activation through TBK1. J Virol. 2014; 88: 5328-5341. https://doi.org/10.1128/Jvi.00037-14
- 35Ahn J, Barber GN. STING signaling and host defense against microbial infection. Exp Mol Med. 2019; 51: 1-10. https://doi.org/10.1038/s12276-019-0333-0
- 36Gonugunta VK, Sakai T, Pokatayev V, et al. Trafficking-mediated STING degradation requires sorting to acidified endolysosomes and can be targeted to enhance anti-tumor response. Cell Rep. 2017; 21: 3234-3242. https://doi.org/10.1016/j.celrep.2017.11.061
- 37Mukai K, Ogawa E, Uematsu R, et al. Homeostatic regulation of STING by retrograde membrane traffic to the ER. Nat Commun. 2021; 12: 61. https://doi.org/10.1038/s41467-020-20234-9
- 38Deng Z, Chong Z, Law CS, et al. A defect in COPI-mediated transport of STING causes immune dysregulation in COPA syndrome. J Exp Med. 2020; 217. https://doi.org/10.1084/jem.20201045
- 39Abe T, Harashima A, Xia T, et al. STING recognition of cytoplasmic DNA instigates cellular defense. Mol Cell. 2013; 50: 5-15. https://doi.org/10.1016/j.molcel.2013.01.039
- 40Zevini A, Olagnier D, Hiscott J. Crosstalk between cytoplasmic RIG-I and STING sensing pathways. Trends Immunol. 2017; 38: 194-205. https://doi.org/10.1016/j.it.2016.12.004
- 41Cao L, Liu S, Li Y, et al. The nuclear matrix protein SAFA surveils viral RNA and facilitates immunity by activating antiviral enhancers and super-enhancers. Cell Host Microbe. 2019; 26: 369-384.e368. https://doi.org/10.1016/j.chom.2019.08.010
- 42Liu BY, Yu XJ, Zhou CM. SAFA initiates innate immunity against cytoplasmic RNA virus SFTSV infection. PLoS Pathog. 2021; 17:e1010070. https://doi.org/10.1371/journal.ppat.1010070
- 43Zhang 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: 959-965. https://doi.org/10.1038/ni.2091
- 44Dunphy G, Flannery SM, Almine JF, et al. Non-canonical activation of the DNA sensing adaptor STING by ATM and IFI16 mediates NF-kappaB signaling after nuclear DNA damage. Mol Cell. 2018; 71: 745-760.e745. https://doi.org/10.1016/j.molcel.2018.07.034
- 45Holm CK, Jensen SB, Jakobsen MR, et al. Virus-cell fusion as a trigger of innate immunity dependent on the adaptor STING. Nat Immunol. 2012; 13: 737-743. https://doi.org/10.1038/ni.2350
- 46Moretti J, Roy S, Bozec D, et al. STING Senses microbial viability to orchestrate stress-mediated autophagy of the endoplasmic reticulum. Cell. 2017; 171: 809-823.e813 https://doi.org/10.1016/j.cell.2017.09.034
- 47Smith JA. STING, the endoplasmic reticulum, and mitochondria: is three a crowd or a conversation? Front Immunol. 2020; 11:611347. https://doi.org/10.3389/fimmu.2020.611347
- 48Cheng W-Y, He X-B, Jia H-J, et al. The cGas–sting signaling pathway is required for the innate immune response against ectromelia virus. Front Immunol. 2018; 9. https://doi.org/10.3389/fimmu.2018.01297
- 49Reinert LS, Lopušná K, Winther H, et al. Sensing of HSV-1 by the cGAS-STING pathway in microglia orchestrates antiviral defence in the CNS. Nat Commun. 2016; 7:13348. https://doi.org/10.1038/ncomms13348
- 50He J, Hao R, Liu D, et al. Inhibition of hepatitis B virus replication by activation of the cGAS-STING pathway. J Gen Virol. 2016; 97: 3368-3378. https://doi.org/10.1099/jgv.0.000647
- 51Phelan T, Little MA, Brady G. Targeting of the cGAS-STING system by DNA viruses. Biochem Pharmacol. 2020; 174:113831. https://doi.org/10.1016/j.bcp.2020.113831
- 52Li W, Avey D, Fu B, et al. Kaposi's Sarcoma-associated herpesvirus inhibitor of cGAS (KicGAS), encoded by ORF52, is an abundant tegument protein and is required for production of infectious progeny viruses. J Virol. 2016; 90: 5329-5342. https://doi.org/10.1128/JVI.02675-15
- 53Fu YZ, Guo Y, Zou HM, et al. Human cytomegalovirus protein UL42 antagonizes cGAS/MITA-mediated innate antiviral response. PLoS Pathog. 2019; 15:e1007691. https://doi.org/10.1371/journal.ppat.1007691
- 54Hong Y, Jeong H, Park K, et al. STING facilitates nuclear import of herpesvirus genome during infection. Proc Natl Acad Sci U S A. 2021; 118. https://doi.org/10.1073/pnas.2108631118
- 55Ablasser A, Schmid-Burgk JL, Hemmerling I, et al. Cell intrinsic immunity spreads to bystander cells via the intercellular transfer of cGAMP. Nature. 2013; 503: 530-534. https://doi.org/10.1038/nature12640
- 56Jentsch TJ. VRACs and other ion channels and transporters in the regulation of cell volume and beyond. Nat Rev Mol Cell Biol. 2016; 17: 293-307. https://doi.org/10.1038/nrm.2016.29
- 57Voss FK, Ullrich F, Munch J, et al. Identification of LRRC8 heteromers as an essential component of the volume-regulated anion channel VRAC. Science. 2014; 344: 634-638. https://doi.org/10.1126/science.1252826
- 58Zhou C, Chen X, Planells-Cases R, et al. Transfer of cGAMP into bystander cells via LRRC8 volume-regulated anion channels augments STING-mediated interferon responses and anti-viral immunity. Immunity. 2020; 52: 767-781.e766. https://doi.org/10.1016/j.immuni.2020.03.016
- 59Luteijn RD, Zaver SA, Gowen BG, et al. SLC19A1 transports immunoreactive cyclic dinucleotides. Nature. 2019; 573: 434-438. https://doi.org/10.1038/s41586-019-1553-0
- 60Ritchie C, Cordova AF, Hess GT, Bassik MC, Li L. SLC19A1 is an importer of the immunotransmitter cGAMP. Mol Cell. 2019; 75: 372-381. https://doi.org/10.1016/j.molcel.2019.05.006
- 61Zhou Y, Fei M, Zhang G, et al. Blockade of the phagocytic receptor MerTK on tumor-associated macrophages enhances P2X7R-dependent STING activation by tumor-derived cGAMP. Immunity. 2020; 52: 357-373.e359. https://doi.org/10.1016/j.immuni.2020.01.014
- 62Bridgeman A, Maelfait J, Davenne T, et al. Viruses transfer the antiviral second messenger cGAMP between cells. Science. 2015; 349: 1228-1232. https://doi.org/10.1126/science.aab3632
- 63Gentili M, Kowal J, Tkach M, et al. Transmission of innate immune signaling by packaging of cGAMP in viral particles. Science. 2015; 349: 1232-1236. https://doi.org/10.1126/science.aab3628
- 64Aarreberg LD, Esser-Nobis K, Driscoll C, Shuvarikov A, Roby JA, Gale M, Jr. Interleukin-1beta induces mtDNA release to activate innate immune signaling via cGAS-STING. Mol Cell. 2019; 74: 801-815.e806. https://doi.org/10.1016/j.molcel.2019.02.038
- 65Aguirre S, Luthra P, Sanchez-Aparicio MT, et al. Dengue virus NS2B protein targets cGAS for degradation and prevents mitochondrial DNA sensing during infection. Nat Microbiol. 2017; 2:17037. https://doi.org/10.1038/nmicrobiol.2017.37
- 66Sun B, Sundstrom KB, Chew JJ, et al. Dengue virus activates cGAS through the release of mitochondrial DNA. Sci Rep. 2017; 7:3594. https://doi.org/10.1038/s41598-017-03932-1
- 67Franz KM, Neidermyer WJ, Tan YJ, Whelan SPJ, Kagan JC. STING-dependent translation inhibition restricts RNA virus replication. Proc Natl Acad Sci U S A. 2018; 115: E2058-E2067. https://doi.org/10.1073/pnas.1716937115
- 68Li S, Yang J, Zhu Y, et al. Chicken DNA sensing cGAS-STING signal pathway mediates broad spectrum antiviral functions. Vaccines (Basel). 2020; 8. https://doi.org/10.3390/vaccines8030369
- 69Cui S, Yu Q, Chu L, et al. Nuclear cGAS functions non-canonically to enhance antiviral immunity via recruiting methyltransferase Prmt5. Cell Rep. 2020; 33:108490. https://doi.org/10.1016/j.celrep.2020.108490
- 70Ishikawa H, Ma Z, Barber GN. STING regulates intracellular DNA-mediated, type I interferon-dependent innate immunity. Nature. 2009; 461: 788-792. https://doi.org/10.1038/nature08476
- 71Moriyama M, Koshiba T, Ichinohe T. Influenza A virus M2 protein triggers mitochondrial DNA-mediated antiviral immune responses. Nat Commun. 2019; 10:4624. https://doi.org/10.1038/s41467-019-12632-5
- 72Zhong 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. https://doi.org/10.1016/j.immuni.2008.09.003
- 73McGuckin Wuertz K, Treuting PM, Hemann EA, et al. STING is required for host defense against neuropathological West Nile virus infection. PLoS Pathog. 2019; 15:e1007899. https://doi.org/10.1371/journal.ppat.1007899
- 74Schoggins 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. https://doi.org/10.1038/nature12862
- 75You F, Wang P, Yang L, et al. ELF4 is critical for induction of type I interferon and the host antiviral response. Nat Immunol. 2013; 14: 1237-1246. https://doi.org/10.1038/ni.2756
- 76Humphries F, Shmuel-Galia L, Jiang Z, et al. A diamidobenzimidazole STING agonist protects against SARS-CoV-2 infection. Sci Immunol. 2021; 6. https://doi.org/10.1126/sciimmunol.abi9002
- 77Li M, Ferretti M, Ying B, et al. Pharmacological activation of STING blocks SARS-CoV-2 infection. Sci Immunol. 2021; 6. https://doi.org/10.1126/sciimmunol.abi9007
- 78Liu W, Reyes HM, Yang JF, et al. Activation of STING signaling pathway effectively blocks human coronavirus infection. J Virol. 2021; 95. https://doi.org/10.1128/JVI.00490-21
- 79Langereis MA, Rabouw HH, Holwerda M, Visser LJ, van Kuppeveld FJ. Knockout of cGAS and STING rescues virus infection of plasmid DNA-transfected cells. J Virol. 2015; 89: 11169-11173. https://doi.org/10.1128/JVI.01781-15
- 80Geng T, Lin T, Yang D, et al. A critical role for STING signaling in limiting pathogenesis of Chikungunya virus. J Infect Dis. 2021; 223: 2186-2196. https://doi.org/10.1093/infdis/jiaa694
- 81Webb LG, Veloz J, Pintado-Silva J, et al. Chikungunya virus antagonizes cGAS-STING mediated type-I interferon responses by degrading cGAS. PLoS Pathog. 2020; 16:e1008999. https://doi.org/10.1371/journal.ppat.1008999
- 82Yi G, Wen Y, Shu C, et al. Hepatitis C virus NS4B can suppress STING accumulation to evade innate immune responses. J Virol. 2016; 90: 254-265. https://doi.org/10.1128/JVI.01720-15
- 83Holm CK, Rahbek SH, Gad HH, et al. Influenza A virus targets a cGAS-independent STING pathway that controls enveloped RNA viruses. Nat Commun. 2016; 7:10680. https://doi.org/10.1038/ncomms10680
- 84Iampietro M, Dumont C, Mathieu C, et al. Activation of cGAS/STING pathway upon paramyxovirus infection. iScience. 2021; 24:102519. https://doi.org/10.1016/j.isci.2021.102519
- 85Sato H, Hoshi M, Ikeda F, Fujiyuki T, Yoneda M, Kai C. Downregulation of mitochondrial biogenesis by virus infection triggers antiviral responses by cyclic GMP-AMP synthase. PLoS Pathog. 2021; 17:e1009841. https://doi.org/10.1371/journal.ppat.1009841
- 86Jahun AS, Sorgeloos F, Chaudhry Y, et al. Leaked genomic and mitochondrial DNA contribute to the host response to noroviruses in a STING-dependent manner. bioRxiv. 2021. https://doi.org/10.1099/jgv.0.001660
- 87Yu P, Miao Z, Li Y, Bansal R, Peppelenbosch MP, Pan Q. cGAS-STING effectively restricts murine norovirus infection but antagonizes the antiviral action of N-terminus of RIG-I in mouse macrophages. Gut Microbes. 2021; 13:1959839. https://doi.org/10.1080/19490976.2021.1959839
- 88Liu Y, Cherry S. Zika virus infection activates sting-dependent antiviral autophagy in the Drosophila brain. Autophagy. 2019; 15: 174-175. https://doi.org/10.1080/15548627.2018.1528813
- 89Zhang R, Qin X, Yang Y, et al. STING1 is essential for an RNA-virus triggered autophagy. Autophagy. 2021: 1-13. https://doi.org/10.1080/15548627.2021.1959086
- 90McKnight KL, Swanson KV, Austgen K, et al. Stimulator of interferon genes (STING) is an essential proviral host factor for human rhinovirus species A and C. Proc Natl Acad Sci U S A. 2020; 117: 27598-27607. https://doi.org/10.1073/pnas.2014940117
- 91Zhu Q, Hu H, Liu H, Shen H, Yan Z, Gao L. A synthetic STING agonist inhibits the replication of human parainfluenza virus 3 and rhinovirus 16 through distinct mechanisms. Antiviral Res. 2020; 183:104933. https://doi.org/10.1016/j.antiviral.2020.104933
- 92Schneider WM, Chevillotte MD, Rice CM. Interferon-stimulated genes: a complex web of host defenses. Annu Rev Immunol. 2014; 32: 513-545. https://doi.org/10.1146/annurev-immunol-032713-120231
- 93de Oliveira Mann CC, Hopfner KP. Nuclear cGAS: guard or prisoner? EMBO J. 2021; 40:e108293. https://doi.org/10.15252/embj.2021108293
- 94Pepin G, De Nardo D, Rootes CL, et al. Connexin-dependent transfer of cGAMP to phagocytes modulates antiviral responses. mBio. 2020; 11. https://doi.org/10.1128/mBio.03187-19
- 95Zhang T, Yin C, Boyd DF, et al. Influenza virus Z-RNAs induce ZBP1-mediated necroptosis. Cell. 2020; 180: 1115-1129. https://doi.org/10.1016/j.cell.2020.02.050
- 96Zhou Z, Zhang X, Lei X, et al. Sensing of cytoplasmic chromatin by cGAS activates innate immune response in SARS-CoV-2 infection. Acta Pharm. Sin. B. 2021. https://doi.org/10.1016/j.apsb.2021.02.011
- 97Nazmi A, Mukhopadhyay R, Dutta K, Basu A. STING mediates neuronal innate immune response following Japanese encephalitis virus infection. Sci Rep. 2012; 2:347. https://doi.org/10.1038/srep00347
- 98Lahaye X, Gentili M, Silvin A, et al. NONO detects the nuclear HIV capsid to promote cGAS-mediated innate immune activation. Cell. 2018; 175: 488-501.e422. https://doi.org/10.1016/j.cell.2018.08.062
- 99Ng CS, Stobart CC, Luo H. Innate immune evasion mediated by picornaviral 3C protease: possible lessons for coronaviral 3C-like protease? Rev Med Virol. 2021; 31: 1-22. https://doi.org/10.1002/rmv.2206
- 100Chen X, Yang X, Zheng Y, Yang Y, Xing Y, Chen Z. SARS coronavirus papain-like protease inhibits the type I interferon signaling pathway through interaction with the STING-TRAF3-TBK1 complex. Protein Cell. 2014; 5: 369-381. https://doi.org/10.1007/s13238-014-0026-3
- 101Clementz MA, Chen Z, Banach BS, et al. Deubiquitinating and interferon antagonism activities of coronavirus papain-like proteases. J Virol. 2010; 84: 4619-4629. https://doi.org/10.1128/JVI.02406-09
- 102Sun L, Xing Y, Chen X, et al. Coronavirus papain-like proteases negatively regulate antiviral innate immune response through disruption of STING-mediated signaling. PLoS ONE. 2012; 7:e30802. https://doi.org/10.1371/journal.pone.0030802
- 103Xing Y, Chen J, Tu J, et al. The papain-like protease of porcine epidemic diarrhea virus negatively regulates type I interferon pathway by acting as a viral deubiquitinase. J Gen Virol. 2013; 94: 1554-1567. https://doi.org/10.1099/vir.0.051169-0
- 104Rui Y, Su J, Shen S, et al. Unique and complementary suppression of cGAS-STING and RNA sensing- triggered innate immune responses by SARS-CoV-2 proteins. Signal Transduct Target Ther. 2021; 6:123. https://doi.org/10.1038/s41392-021-00515-5
- 105Aguirre 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. https://doi.org/10.1371/journal.ppat.1002934
- 106Dalrymple NA, Cimica V, Mackow ER. Dengue virus NS proteins inhibit RIG-I/MAVS signaling by blocking TBK1/IRF3 phosphorylation: dengue virus serotype 1 NS4A is a unique interferon-regulating virulence determinant. mBio. 2015; 6: e00553-00515. https://doi.org/10.1128/mBio.00553-15
- 107Ding Q, Gaska JM, Douam F, et al. Species-specific disruption of STING-dependent antiviral cellular defenses by the Zika virus NS2B3 protease. Proc Natl Acad Sci U S A. 2018; 115: E6310-E6318. https://doi.org/10.1073/pnas.1803406115
- 108Stabell AC, Meyerson NR, Gullberg RC, et al. Dengue viruses cleave STING in humans but not in nonhuman primates, their presumed natural reservoir. Elife. 2018; 7. https://doi.org/10.7554/eLife.31919
- 109Su CI, Kao YT, Chang CC, et al. DNA-induced 2'3'-cGAMP enhances haplotype-specific human STING cleavage by dengue protease. Proc Natl Acad Sci U S A. 2020; 117: 15947-15954. https://doi.org/10.1073/pnas.1922243117
- 110Wu Z, Zhang W, Wu Y, et al. Binding of the duck tembusu virus protease to STING is mediated by NS2B and is crucial for STING cleavage and for impaired induction of IFN-beta. J Immunol. 2019; 203: 3374-3385. https://doi.org/10.4049/jimmunol.1900956
- 111Ding Q, Cao X, Lu J, et al. Hepatitis C virus NS4B blocks the interaction of STING and TBK1 to evade host innate immunity. J Hepatol. 2013; 59: 52-58. https://doi.org/10.1016/j.jhep.2013.03.019
- 112Nitta 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. https://doi.org/10.1002/hep.26017
- 113Zheng Y, Liu Q, Wu Y, et al. Zika virus elicits inflammation to evade antiviral response by cleaving cGAS via NS1-caspase-1 axis. EMBO J. 2018; 37. https://doi.org/10.15252/embj.201899347
- 114Zhang W, Jiang B, Zeng M, et al. Binding of duck tembusu virus nonstructural protein 2A to duck STING disrupts induction of its signal transduction cascade to inhibit beta interferon induction. J Virol. 2020; 94. https://doi.org/10.1128/JVI.01850-19
- 115Ritchie C, Li LY. cGAMP as an adjuvant in antiviral vaccines and cancer immunotherapy. Biochemistry. 2020; 59: 1713-1715. https://doi.org/10.1021/acs.biochem.0c00226
- 116Wang J, Li PY, Yu Y, et al. Pulmonary surfactant-biomimetic nanoparticles potentiate heterosubtypic influenza immunity. Science. 2020; 367: 869:ARTN eaau0810. https://doi.org/10.1126/science.aau0810
- 117Shirey KA, Nhu QM, Yim KC, et al. The anti-tumor agent, 5,6-dimethylxanthenone-4-acetic acid (DMXAA), induces IFN-beta-mediated antiviral activity in vitro and in vivo. J Leukoc Biol. 2011; 89: 351-357. https://doi.org/10.1189/jlb.0410216
- 118Sheridan C. Drug developers switch gears to inhibit STING. Nat Biotechnol. 2019; 37: 199-201. https://doi.org/10.1038/s41587-019-0060-z
- 119Neufeldt CJ, Cerikan B, Cortese M, et al. SARS-CoV-2 infection induces a pro-inflammatory cytokine response through cGAS-STING and NF-kappaB. Commun Biol. 2022; 5:45. https://doi.org/10.1038/s42003-021-02983-5
- 120Decout A, Katz JD, Venkatraman S, Ablasser A. The cGAS-STING pathway as a therapeutic target in inflammatory diseases. Nat Rev Immunol. 2021; 21: 548-569. https://doi.org/10.1038/s41577-021-00524-z
- 121Xu Y, Zhang Y, Sun S, et al. The innate immune DNA sensing cGAS-STING signaling pathway mediates Anti-PRRSV function. Viruses. 2021; 13. https://doi.org/10.3390/v13091829
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