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STING regulates intracellular DNA-mediated, type I interferon-dependent innate immunity
Open accessAbstract
The innate immune system is critical for the early detection of invading pathogens and for initiating cellular host defence countermeasures, which include the production of type I interferon (IFN). However, little is known about how the innate immune system is galvanized to respond to DNA-based microbes. Here we show that STING (stimulator of interferon genes) is critical for the induction of IFN by non-CpG intracellular DNA species produced by various DNA pathogens after infection. Murine embryonic fibroblasts, as well as antigen presenting cells such as macrophages and dendritic cells (exposed to intracellular B-form DNA, the DNA virus herpes simplex virus 1 (HSV-1) or bacteria Listeria monocytogenes), were found to require STING to initiate effective IFN production. Accordingly, Sting-knockout mice were susceptible to lethal infection after exposure to HSV-1. The importance of STING in facilitating DNA-mediated innate immune responses was further evident because cytotoxic T-cell responses induced by plasmid DNA vaccination were reduced in Sting-deficient animals. In the presence of intracellular DNA, STING relocalized with TANK-binding kinase 1 (TBK1) from the endoplasmic reticulum to perinuclear vesicles containing the exocyst component Sec5 (also known as EXOC2). Collectively, our studies indicate that STING is essential for host defence against DNA pathogens such as HSV-1 and facilitates the adjuvant activity of DNA-based vaccines.
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“TBK1 also activates NF‐κB to induce expression of IFN and inflammatory cytokines.65, 66, 67”
From Cellular senescence and senescence-associated secretory phenotype via the cGAS-STING signaling pathway in cancer (2020) · cites this paper as [66]
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SAMHD1 Host Restriction Factor: A Link with Innate Immune Sensing of Retrovirus Infection
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Vandevenne, P., Sadzot‐Delvaux, C., & Piette, J. G. (2010) · Biochemical Pharmacology · doi:10.1016/j.bcp.2010.07.001 · Cited by 54
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“Indeed, STING knockout mice are highly susceptible to infection with, for example, herpes viruses (Ishikawa et al., 2009b).”
BackgroundInfluentialBioactive modulators targeting STING adaptor in cGAS-STING pathway
Feng, X., Liu, D., Li, Z., & Bian, J. (2019) · Drug Discovery Today · doi:10.1016/j.drudis.2019.11.007 · Cited by 53
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“STING signaling is critical for type-I IFN responses [20,80].”
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Ke, X., Hu, T., & Jiang, M. (2021) · The FASEB Journal · doi:10.1096/fj.202101199r · Cited by 52
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The interplay between autophagy and cGAS-STING signaling and its implications for cancer
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cGAS-STING targeting offers novel therapeutic opportunities in neurological diseases
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“. There, being in close proximity with a component of the exocyst (sec5) and the translocon (Sec61β), TRAF3 allows the activation of TBK1 and IRF3 leading to activation of the type I IFN response. A similar scenario was recently proposed for STING (yellow circles) where in response to DNA virus infection, it traffics…”
BackgroundNonstructural NS1 proteins of several mosquito-borne Flavivirus do not inhibit TLR3 signaling
Baronti, C., Sire, J., de Lamballerie, X. N., & Quérat, G. (2010) · Virology · doi:10.1016/j.virol.2010.05.020 · Cited by 54
Interferon regulatory factor 3 in adaptive immune responses
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“In contrast to the redundancy of DNA sensors, the adaptor protein stimulator of interferon genes (STING) appears to be central for the production of type I IFN in response to cytosolic dsDNA [31].”
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BackgroundInfluentialcGAS-STING Activation in the Tumor Microenvironment and Its Role in Cancer Immunity
Pépin, G., & Gantier, M. P. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-981-10-5987-2_8 · Cited by 53
An emerging role for calcium signalling in innate and autoimmunity via the cGAS-STING axis
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BackgroundER-Mitochondria Communication in Cells of the Innate Immune System
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BackgroundTBC1D9 regulates TBK1 activation through Ca2+ signaling in selective autophagy
Nozawa, T., Sano, S., Minowa‐Nozawa, A., Toh, H., Nakajima, S., Murase, K., Aikawa, C., & Nakagawa, I. (2020) · Nature Communications · doi:10.1038/s41467-020-14533-4 · Cited by 55
Regulation and inhibition of the DNA sensor cGAS
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“Stimulation of STING leads to the recruitment and phosphorylation of the transcription factors IRF3 and NF j B through the kinases TBK1 and IKK e (Ishikawa & Barber, 2008; Ishikawa et al , 2009; Diner et al , 2013; Zhang et al , 2013; Ablasser et al , 2013a; Shang et al , 2019; Zhang et al , 2019).”
The STING1-MYD88 complex drives ACOD1/IRG1 expression and function in lethal innate immunity
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“…interactor 1 (STING1, also known as TMEM173 or STING) is a wellknownregulatorof thecyclicGMP-AMPsynthase (CGAS)-dependentDNAsensorpathway,whichdrivesantiviral immunity by producing type I interferons (IFNs) (Ishikawa andBarber, 2008; Ishikawa et al., 2009; Sun et al., 2009; Zhong et al., 2008).”
BackgroundOrigins and diversification of animal innate immune responses against viral infections
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“STING (also named MITA, MPYS and ERIS), encoded by the TMEM173 gene, is an evolutionary conserved transmembrane protein consisting of 379 amino acids with amolecular weight of 42 kDa, widely existing in diverse species and cell lineages, including endothelial cells, epithelial cells, immune cells (T cells, macrophages…”
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“The cGAMP is then detected by the ER membrane protein STING, which exists as a dimer with two cytoplasmic domains (31, 46).”
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Fish MAVS is involved in RLR pathway-mediated IFN response
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“Responses driven by the nucleic acid sensor cGAS/STING pathway are important for the induction of IFNI (Ablasser et al., 2013; Ishikawa and Barber, 2008; Ishikawa et al., 2009; Sun et al., 2013), and we next questioned the involvement of the cGAS/STING axis in silica-induced exacerbation of M.”
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Herpes Simplex Virus and Pattern Recognition Receptors: An Arms Race
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“In response to HSV-1 infection, STING is required for IFN production in multiple cell lines, including murine embryonic fibroblasts, macrophages and dendritic cells (52).”
BackgroundGarcia, G., Irudayam, J. I., Jeyachandran, A. V., Dubey, S., Chang, C. C., Cario, S. C., Price, N., Arumugam, S., Marquez, A. L., Shah, A., et al. (2023) · Cell Reports Medicine · doi:10.1016/j.xcrm.2023.101024 · Cited by 52
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Type I interferon in neurological disease—The devil from within
Hofer, M. J., & Campbell, I. L. (2013) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2013.03.006 · Cited by 50
“Interestingly, STING may also be a direct sensor of microbial DNA [18] and CDNs [19] suggesting that STING has a bi-modal role”
BackgroundSTING-ing the Antiviral Pathway
Nakhaei, P., Hiscott, J. B., & Lin, R. (2009) · Journal of Molecular Cell Biology · doi:10.1093/jmcb/mjp048 · Cited by 50
“for the non-CpG intracellular DNA-mediated induction of type I IFN and was essential for host defence against DNA pathogens (Ishikawa et al., 2009).”
BackgroundInfluentialRoyer, D. J., & Carr, D. J. J. (2015) · Mucosal Immunology · doi:10.1038/mi.2015.124 · Cited by 50
Long story short: p53 mediates innate immunity
Miciak, J. J., & Bunz, F. (2016) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2016.03.001 · Cited by 49
“DNA damage primes the type I interferon system via the cytosolic DNA sensor STING to promote anti-microbial innate immunity.”
BackgroundInfluentialLiu, C., Huang, S., Wang, X., Wen, M., Zheng, J., Wang, W., Fu, Y., Tian, S.-L., Li, L., Li, Z., et al. (2019) · The Journal of Immunology · doi:10.4049/jimmunol.1800656 · Cited by 50
“STING (also called MITA or ERIS) (22–25) and MAVS (also called IPS1, VISA, or Cardif) (26–29) are essential adaptors for the cytoplasmic DNA- and RNA-triggered production of type I IFNs, respectively.”
BackgroundInfluentialThe abscopal effect: a sense of DNA damage is in the air
Lippert, T. P., & Greenberg, R. A. (2021) · Journal of Clinical Investigation · doi:10.1172/jci148274 · Cited by 53
Considerations for the delivery of STING ligands in cancer immunotherapy
Petrovic, M., Borchard, G., & Jordan, O. (2021) · Journal of Controlled Release · doi:10.1016/j.jconrel.2021.09.033 · Cited by 51
Innate Immune Responses to Hepatitis C Virus
Schoggins, J. W., & Rice, C. M. (2013) · Current topics in microbiology and immunology · doi:10.1007/978-3-642-27340-7_9 · Cited by 52
Diversity of Pathogen Sensors in Dendritic Cells
Cerboni, S., Gentili, M., & Manel, N. (2013) · Advances in immunology · doi:10.1016/b978-0-12-417028-5.00008-9 · Cited by 63
cGAS/STING: novel perspectives of the classic pathway
Gao, M., He, Y., Tang, H., Chen, X., Liu, S., & Tao, Y. (2020) · Molecular Biomedicine · doi:10.1186/s43556-020-00006-z · Cited by 50
“This interaction activates downstream phosphatidylinositol 3-kinase class III and induces autophagy to remove cytosolic pathogen DNA independent of TBK1 activation [17].”
BackgroundInfluentialGenetic Predisposition to Persistent Human Papillomavirus-Infection and Virus-Induced Cancers
Espinoza, H. V., Ha, K. T., Pham, T., & Espinoza, J. L. (2021) · Microorganisms · doi:10.3390/microorganisms9102092 · Cited by 49
“The protein product of EXOC1 contributes to the formation of the exocyst complex, which facilitates the vesicle transport, secretion and cellular migration and appears to influence the immune response to viral infection [80] and has been implicated in the progression of human oral squamous cell carcinoma [81].”
BackgroundJi, H., Wang, W., Li, X., Han, X., Zhang, X., Wang, J., Liu, C., Huang, L., & Gao, W. (2022) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.1c16737 · Cited by 50
Responsive manganese-based nanoplatform amplifying cGAS-STING activation for immunotherapy
He, Q., Zheng, R., Ma, J., Zhao, L., Shi, Y., & Qiu, J. (2023) · Biomaterials Research · doi:10.1186/s40824-023-00374-x · Cited by 49
“cGAS-STING signaling pathway has become a key innate immune pathway, promoting different immune responses and affecting tumor progression and metastasis [37].”
BackgroundThe role of mtDAMPs in the trauma-induced systemic inflammatory response syndrome
Ye, J., Hu, X., Wang, Z., Li, R., Gan, L., Zhang, M., & Wang, T. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1164187 · Cited by 53
Motani, K., Ito, S., & Nagata, S. (2015) · The Journal of Immunology · doi:10.4049/jimmunol.1402705 · Cited by 48
“DNA is dependent on STING (24, 25) as well as cGAS (26, 27).”
BackgroundHantavirus Regulation of Type I Interferon Responses
Matthys, V. S., & Mackow, E. R. (2012) · Advances in Virology · doi:10.1155/2012/524024 · Cited by 49
“CARDs direct interactions with the mitochondrially located adaptor protein MAVS (also known as IPS-1/CARDIF/VISA), and further activate the assembly of downstream signaling complexes containing the ER-retained protein STING (stimulator of interferon genes) (also termed MITA/ERIS) [59–65] (Figure 1).”
BackgroundPreclinical and clinical development of DNA vaccines for prostate cancer
Colluru, V. T., Johnson, L. E., Olson, B. M., & McNeel, D. G. (2013) · Urologic Oncology Seminars and Original Investigations · doi:10.1016/j.urolonc.2013.09.014 · Cited by 49
The role of dendritic cells in immunity against primary herpes simplex virus infections
Bedoui, S., & Greyer, M. (2014) · Frontiers in Microbiology · doi:10.3389/fmicb.2014.00533 · Cited by 51
Lam, E., & Falck-Pedersen, E. (2014) · Journal of Virology · doi:10.1128/jvi.02608-14 · Cited by 49
“(TBK1) (28), and TBK1 (19, 30) phosphorylates cytosolic inter-”
BackgroundGEF-H1 controls microtubule-dependent sensing of nucleic acids for antiviral host defenses
Chiang, H.-S., Zhao, Y., Song, J.-H., Liu, S., Wang, N., Terhorst, C., Sharpe, A. H., Basavappa, M. G., Jeffrey, K. L., & Reinecker, H. (2013) · Nature Immunology · doi:10.1038/ni.2766 · Cited by 49
“TBK1 and IRF3 activation also occurs downstream of stimulator of interferon genes (STING; also known as TMEM173, MPYS, ERIS or MITA), in the detection of viral nucleic acids and B-form DNA (B-DNA or poly(dA:dT)) by DDX proteins) 21 .”
Nucleic acid sensing by T cells initiates Th2 cell differentiation
Imanishi, T., Ishihara, C., Badr, M. E. S. G., Hashimoto, A. S., Kimura, Y., Kawai, T., Takeuchi, O., Ishii, K. J., Taniguchi, S., Noda, T., et al. (2014) · Nature Communications · doi:10.1038/ncomms4566 · Cited by 49
Self-citationCyclic dinucleotides at the forefront of innate immunity
Zaver, S. A., & Woodward, J. J. (2020) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2019.12.004 · Cited by 50
Long, J., Yang, C., Zheng, Y., Loughran, P., Guang, F., Li, Y., Liao, H., Scott, M. J., Tang, D., Billiar, T. R., et al. (2020) · Science Advances · doi:10.1126/sciadv.abc5447 · Cited by 48
Smolarz, M., Zawrotniak, M., Satała, D., & Rąpała‐Kozik, M. (2021) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2021.681030 · Cited by 50
“Among them, the following receptors have been distinguished: RIG-I-like (RLR), NOD-like (NLR), AIM2-like (ALR), Toll-like (TLR), cGAS, and IFI16 (Ishikawa et al., 2009; Kawasaki and Kawai, 2014; Barrat et al., 2016; Khan et al., 2019).”
InfluentialLozano‐Ruiz, B., Bachiller, V., García‐Martinez, I., Zapater, P., Gómez‐Hurtado, I., Moratalla, A., Giménez, P., Bellot, P., Francés, R., Such, J. M., et al. (2014) · Journal of Hepatology · doi:10.1016/j.jhep.2014.08.027 · Cited by 49
Balancing life and death: BCL‐2 family members at diverse ER–mitochondrial contact sites
Means, R. E., & Katz, S. G. (2021) · FEBS Journal · doi:10.1111/febs.16241 · Cited by 50
Gołąbek-Grenda, A., & Olejnik, A. M. (2022) · Cellular Signalling · doi:10.1016/j.cellsig.2022.110375 · Cited by 53
The Dual Role of the Innate Immune System in the Effectiveness of mRNA Therapeutics
Muslimov, A. R., Tereshchenko, V., Shevyrev, D., Rogova, A. S., Lepik, K. V., Reshetnikov, V. V., & Ivanov, R. A. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241914820 · Cited by 51
“Activated cGAS leads to the production of 2 (cid:48) -3 (cid:48) -cyclic GMP–AMP (cGAMP), a secondary messenger molecule and potent agonist of STING [209].”
BackgroundBarber, G. N. (2011) · Nature Immunology · doi:10.1038/ni.2118 · Cited by 48
Self-citationLandrigan, A., Wong, M. T., & Utz, P. J. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1003414 · Cited by 50
“Of interest given our findings of costimulatory activity of non-CpG ODNs, the stimulator of IFN genes protein that associates with TANK-binding kinase-1 promotes the proinflammatory response of dendritic cells, macrophages, and fibroblasts to a variety of DNA stimuli, including DNA lacking CpG motifs (61, 62).”
BackgroundLee, E. H., Jang, H.-E., Kang, Y. Y., Kim, J., Ahn, J., & Mok, H. (2015) · Acta Biomaterialia · doi:10.1016/j.actbio.2015.10.025 · Cited by 48
Tegtmeyer, P.-K., Spanier, J., Borst, K., Becker, J., Riedl, A., Hirche, C., Ghita, L., Skerra, J., Baumann, K., Lienenklaus, S., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-10863-0 · Cited by 47
STING is required for host defense against neuropathological West Nile virus infection
Wuertz, K. M., Treuting, P. M., Hemann, E. A., Esser‐Nobis, K., Snyder, A. G., Graham, J. B., Daniels, B. P., Wilkins, C. R., Snyder, J. M., Voss, K., et al. (2019) · PLoS Pathogens · doi:10.1371/journal.ppat.1007899 · Cited by 49
“However its role in the defense against RNA viruses is poorly understood [47] [48] [49] [50] [51] [52] [53] [54] .”
BackgroundMethodResultInfluentialThe Functional Deubiquitinating Enzymes in Control of Innate Antiviral Immunity
Zong, Z., Zhang, Z., Wu, L., Zhang, L., & Zhou, F. (2020) · Advanced Science · doi:10.1002/advs.202002484 · Cited by 49
Liu, Y., Tang, Q., Rao, Z., Fang, Y., Jiang, X., Liu, W., Luan, F., & Zeng, N. (2021) · Antiviral Research · doi:10.1016/j.antiviral.2021.105143 · Cited by 46
Metadata
- Authors
- Ishikawa, H., Ma, Z., & Barber, G. N.
- Affiliations
- University of Miami (US)
- Corresponding author
- Barber, Glen N.
- Venue
- Nature
- Published
- 2009-09-23
- Volume
- 461
- Issue
- 7265
- Pages
- 788-792
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC4664154
- OpenAlex
- W1968178474
- Semantic Scholar
- 1098beb4c76eacfcc093a88d02d02a681585e7c4
- Cited by
- 2,759
- References
- 31
- Citations by year
- 2026: 184 · 2025: 229 · 2024: 240 · 2023: 240 · 2022: 237 · 2021: 249 · 2020: 212 · 2019: 182 · 2018: 147 · 2017: 170 · 2016: 110 · 2015: 118 · 2014: 114 · 2013: 115 · 2012: 78
- FWCI
- 30.14
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- National Institutes of Health
- National Institute of Allergy and Infectious Diseases (AI079336, R56AI079336, R01AI079336)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › interferon and immune responses
- Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
- Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
- Keywords
- STING, mita, Eris, type I interferon, innate immunity, herpes simplex virus type 1, TBK1, Sec5, endosomes, DNA vaccine, plasmid DNA immunization, Listeria monocytogenes, viral susceptibility, dendritic cells
- MeSH terms
- STING Protein, Animals, Antigen-Presenting Cells, DNA, Bacterial, DNA, Viral, Endoplasmic Reticulum, Fibroblasts, Immunity, Innate, Interferon Type I, Listeria monocytogenes, Membrane Proteins, Plasmids, T-Lymphocytes, Cytotoxic, Protein Serine-Threonine Kinases, Herpesvirus 1, Human, Mice, Knockout, Vaccines, DNA, Protein Transport, Cytoplasmic Vesicles, Vesicular Transport Proteins, Intracellular Space, Mice
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