STING Requires the Adaptor TRIF to Trigger Innate Immune Responses to Microbial Infection

Cell Host and Microbe

Volumn 20, Issue 3, 2016, Pages 329-341

  Wang, Xin ^a   Majumdar, Tanmay ^b,c   Kessler, Patricia ^a   Ozhegov, Evgeny ^b   Zhang, Ying ^a   Chattopadhyay, Saurabh ^a,d   Barik, Sailen ^b   Sen, Ganes C ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

^b CLEVELAND STATE UNIVERSITY   (United States)

^c UNIVERSITY OF DELHI   (India)

^d MEDICAL COLLEGE OF OHIO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; INTERFERON; INTERLEUKIN 6; MEMBRANE PROTEIN; MESSENGER RNA; STING PROTEIN; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; UNCLASSIFIED DRUG; MPYS PROTEIN, MOUSE; PROTEIN BINDING; TICAM-1 PROTEIN, MOUSE; VESICULAR TRANSPORT ADAPTOR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DIMERIZATION; GENETIC ASSOCIATION; HERPES SIMPLEX ENCEPHALITIS; HERPES SIMPLEX VIRUS 1; INNATE IMMUNITY; INTRACELLULAR SIGNALING; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; VIRUS INFECTION; ANIMAL; CELL LINE; DISEASE MODEL; HERPES SIMPLEX; HUMAN; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; PATHOGENICITY; PATHOLOGY; PROTEIN ANALYSIS; PROTEIN MULTIMERIZATION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; VIROLOGY;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; CELL LINE; DISEASE MODELS, ANIMAL; HERPES SIMPLEX; HERPESVIRUS 1, HUMAN; HUMANS; IMMUNITY, INNATE; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN MULTIMERIZATION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

EID: 84995572457     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2016.08.002     Document Type: Article

References (45)

1. Ahn, J., Xia, T., Konno, H., Konno, K., Ruiz, P., Barber, G.N., Inflammation-driven carcinogenesis is mediated through STING. Nat. Commun., 5, 2014, 5166.
2. Ahn, J., Konno, H., Barber, G.N., Diverse roles of STING-dependent signaling on the development of cancer. Oncogene 34 (2015), 5302–5308.
3. Archer, K.A., Durack, J., Portnoy, D.A., STING-dependent type I IFN production inhibits cell-mediated immunity to Listeria monocytogenes. PLoS Pathog., 10, 2014, e1003861.
4. Barber, G.N., STING: infection, inflammation and cancer. Nat. Rev. Immunol. 15 (2015), 760–770.
5. Blaho, J.A., Morton, E.R., Yedowitz, J.C., Herpes simplex virus: propagation, quantification, and storage. Curr. Protoc. Microbiol., Chapter 14, 2005 Unit 14E 11.
6. Cai, X., Chiu, Y.H., Chen, Z.J., The cGAS-cGAMP-STING pathway of cytosolic DNA sensing and signaling. Mol. Cell 54 (2014), 289–296.
7. Deng, L., Liang, H., Xu, M., Yang, X., Burnette, B., Arina, A., Li, X.D., Mauceri, H., Beckett, M., Darga, T., et al. STING-dependent cytosolic DNA sensing promotes radiation-induced type I interferon-dependent antitumor immunity in immunogenic tumors. Immunity 41 (2014), 843–852.
8. Dey, B., Dey, R.J., Cheung, L.S., Pokkali, S., Guo, H., Lee, J.H., Bishai, W.R., A bacterial cyclic dinucleotide activates the cytosolic surveillance pathway and mediates innate resistance to tuberculosis. Nat. Med. 21 (2015), 401–406.
9. Dobbs, N., Burnaevskiy, N., Chen, D., Gonugunta, V.K., Alto, N.M., Yan, N., STING activation by translocation from the ER is associated with infection and autoinflammatory disease. Cell Host Microbe 18 (2015), 157–168.
10. Fitzgerald, K.A., Rowe, D.C., Barnes, B.J., Caffrey, D.R., Visintin, A., Latz, E., Monks, B., Pitha, P.M., Golenbock, D.T., LPS-TLR4 signaling to IRF-3/7 and NF-kappaB involves the toll adapters TRAM and TRIF. J. Exp. Med. 198 (2003), 1043–1055.
11. Gao, P., Ascano, M., Zillinger, T., Wang, W., Dai, P., Serganov, A.A., Gaffney, B.L., Shuman, S., Jones, R.A., Deng, L., et al. Structure-function analysis of STING activation by c[G(2′,5′)pA(3′,5′)p] and targeting by antiviral DMXAA. Cell 154 (2013), 748–762.
12. Han, K.J., Yang, Y., Xu, L.G., Shu, H.B., Analysis of a TIR-less splice variant of TRIF reveals an unexpected mechanism of TLR3-mediated signaling. J. Biol. Chem. 285 (2010), 12543–12550.
13. Härtlova, A., Erttmann, S.F., Raffi, F.A., Schmalz, A.M., Resch, U., Anugula, S., Lienenklaus, S., Nilsson, L.M., Kröger, A., Nilsson, J.A., et al. DNA damage primes the type I interferon system via the cytosolic DNA sensor STING to promote anti-microbial innate immunity. Immunity 42 (2015), 332–343.
14. Hoebe, K., Du, X., Georgel, P., Janssen, E., Tabeta, K., Kim, S.O., Goode, J., Lin, P., Mann, N., Mudd, S., et al. Identification of Lps2 as a key transducer of MyD88-independent TIR signalling. Nature 424 (2003), 743–748.
15. Huang, Y.H., Liu, X.Y., Du, X.X., Jiang, Z.F., Su, X.D., The structural basis for the sensing and binding of cyclic di-GMP by STING. Nat. Struct. Mol. Biol. 19 (2012), 728–730.
16. Ishikawa, H., Ma, Z., Barber, G.N., STING regulates intracellular DNA-mediated, type I interferon-dependent innate immunity. Nature 461 (2009), 788–792.
17. Janeway, C.A. Jr., Medzhitov, R., Innate immune recognition. Annu. Rev. Immunol. 20 (2002), 197–216.
18. Jeremiah, N., Neven, B., Gentili, M., Callebaut, I., Maschalidi, S., Stolzenberg, M.C., Goudin, N., Frémond, M.L., Nitschke, P., Molina, T.J., et al. Inherited STING-activating mutation underlies a familial inflammatory syndrome with lupus-like manifestations. J. Clin. Invest. 124 (2014), 5516–5520.
19. Johnson, K.E., Bottero, V., Flaherty, S., Dutta, S., Singh, V.V., Chandran, B., IFI16 restricts HSV-1 replication by accumulating on the hsv-1 genome, repressing HSV-1 gene expression, and directly or indirectly modulating histone modifications. PLoS Pathog., 10, 2014, e1004503.
20. Joung, S.M., Park, Z.Y., Rani, S., Takeuchi, O., Akira, S., Lee, J.Y., Akt contributes to activation of the TRIF-dependent signaling pathways of TLRs by interacting with TANK-binding kinase 1. J. Immunol. 186 (2011), 499–507.
21. Liu, Y., Jesus, A.A., Marrero, B., Yang, D., Ramsey, S.E., Montealegre Sanchez, G.A., Tenbrock, K., Wittkowski, H., Jones, O.Y., Kuehn, H.S., et al. Activated STING in a vascular and pulmonary syndrome. N. Engl. J. Med. 371 (2014), 507–518.
22. Ma, X., Helgason, E., Phung, Q.T., Quan, C.L., Iyer, R.S., Lee, M.W., Bowman, K.K., Starovasnik, M.A., Dueber, E.C., Molecular basis of Tank-binding kinase 1 activation by transautophosphorylation. Proc. Natl. Acad. Sci. USA 109 (2012), 9378–9383.
23. Majumdar, T., Chattopadhyay, S., Ozhegov, E., Dhar, J., Goswami, R., Sen, G.C., Barik, S., Induction of interferon-stimulated genes by IRF3 promotes replication of Toxoplasma gondii. PLoS Pathog., 11, 2015, e1004779.
24. Menasria, R., Boivin, N., Lebel, M., Piret, J., Gosselin, J., Boivin, G., Both TRIF and IPS-1 adaptor proteins contribute to the cerebral innate immune response against herpes simplex virus 1 infection. J. Virol. 87 (2013), 7301–7308.
25. Meylan, E., Burns, K., Hofmann, K., Blancheteau, V., Martinon, F., Kelliher, M., Tschopp, J., RIP1 is an essential mediator of Toll-like receptor 3-induced NF-kappa B activation. Nat. Immunol. 5 (2004), 503–507.
26. O'Neill, L.A., Bowie, A.G., The family of five: TIR-domain-containing adaptors in Toll-like receptor signalling. Nat. Rev. Immunol. 7 (2007), 353–364.
27. Orzalli, M.H., Broekema, N.M., Diner, B.A., Hancks, D.C., Elde, N.C., Cristea, I.M., Knipe, D.M., cGAS-mediated stabilization of IFI16 promotes innate signaling during herpes simplex virus infection. Proc. Natl. Acad. Sci. USA 112 (2015), E1773–E1781.
28. Ouyang, S., Song, X., Wang, Y., Ru, H., Shaw, N., Jiang, Y., Niu, F., Zhu, Y., Qiu, W., Parvatiyar, K., et al. Structural analysis of the STING adaptor protein reveals a hydrophobic dimer interface and mode of cyclic di-GMP binding. Immunity 36 (2012), 1073–1086.
29. Paludan, S.R., Bowie, A.G., Immune sensing of DNA. Immunity 38 (2013), 870–880.
30. Pandey, S., Kawai, T., Akira, S., Microbial sensing by Toll-like receptors and intracellular nucleic acid sensors. Cold Spring Harb. Perspect. Biol., 7, 2014, a016246.
31. Parker, Z.M., Murphy, A.A., Leib, D.A., Role of the DNA sensor STING in protection from lethal infection following corneal and intracerebral challenge with herpes simplex virus 1. J. Virol. 89 (2015), 11080–11091.
32. Ran, Y., Shu, H.B., Wang, Y.Y., MITA/STING: a central and multifaceted mediator in innate immune response. Cytokine Growth Factor Rev. 25 (2014), 631–639.
33. Sancho-Shimizu, V., Pérez de Diego, R., Lorenzo, L., Halwani, R., Alangari, A., Israelsson, E., Fabrega, S., Cardon, A., Maluenda, J., Tatematsu, M., et al. Herpes simplex encephalitis in children with autosomal recessive and dominant TRIF deficiency. J. Clin. Invest. 121 (2011), 4889–4902.
34. Sun, W., Li, Y., Chen, L., Chen, H., You, F., Zhou, X., Zhou, Y., Zhai, Z., Chen, D., Jiang, Z., ERIS, an endoplasmic reticulum IFN stimulator, activates innate immune signaling through dimerization. Proc. Natl. Acad. Sci. USA 106 (2009), 8653–8658.
35. Tanaka, Y., Chen, Z.J., STING specifies IRF3 phosphorylation by TBK1 in the cytosolic DNA signaling pathway. Sci. Signal., 5, 2012, ra20.
36. Tatematsu, M., Ishii, A., Oshiumi, H., Horiuchi, M., Inagaki, F., Seya, T., Matsumoto, M., A molecular mechanism for Toll-IL-1 receptor domain-containing adaptor molecule-1-mediated IRF-3 activation. J. Biol. Chem. 285 (2010), 20128–20136.
37. Tsuchida, T., Zou, J., Saitoh, T., Kumar, H., Abe, T., Matsuura, Y., Kawai, T., Akira, S., The ubiquitin ligase TRIM56 regulates innate immune responses to intracellular double-stranded DNA. Immunity 33 (2010), 765–776.
38. Wang, X., Helfer, C.M., Pancholi, N., Bradner, J.E., You, J., Recruitment of Brd4 to the human papillomavirus type 16 DNA replication complex is essential for replication of viral DNA. J. Virol. 87 (2013), 3871–3884.
39. Wang, Q., Liu, X., Cui, Y., Tang, Y., Chen, W., Li, S., Yu, H., Pan, Y., Wang, C., The E3 ubiquitin ligase AMFR and INSIG1 bridge the activation of TBK1 kinase by modifying the adaptor STING. Immunity 41 (2014), 919–933.
40. Woo, S.R., Fuertes, M.B., Corrales, L., Spranger, S., Furdyna, M.J., Leung, M.Y., Duggan, R., Wang, Y., Barber, G.N., Fitzgerald, K.A., et al. STING-dependent cytosolic DNA sensing mediates innate immune recognition of immunogenic tumors. Immunity 41 (2014), 830–842.
41. Wu, J., Chen, Z.J., Innate immune sensing and signaling of cytosolic nucleic acids. Annu. Rev. Immunol. 32 (2014), 461–488.
42. Yamamoto, M., Sato, S., Mori, K., Hoshino, K., Takeuchi, O., Takeda, K., Akira, S., Cutting edge: a novel Toll/IL-1 receptor domain-containing adapter that preferentially activates the IFN-beta promoter in the Toll-like receptor signaling. J. Immunol. 169 (2002), 6668–6672.
43. Zhang, J., Hu, M.M., Wang, Y.Y., Shu, H.B., TRIM32 protein modulates type I interferon induction and cellular antiviral response by targeting MITA/STING protein for K63-linked ubiquitination. J. Biol. Chem. 287 (2012), 28646–28655.
44. Zhou, Q., Lin, H., Wang, S., Wang, S., Ran, Y., Liu, Y., Ye, W., Xiong, X., Zhong, B., Shu, H.B., Wang, Y.Y., The ER-associated protein ZDHHC1 is a positive regulator of DNA virus-triggered, MITA/STING-dependent innate immune signaling. Cell Host Microbe 16 (2014), 450–461.
45. Zhu, Q., Man, S.M., Gurung, P., Liu, Z., Vogel, P., Lamkanfi, M., Kanneganti, T.D., Cutting edge: STING mediates protection against colorectal tumorigenesis by governing the magnitude of intestinal inflammation. J. Immunol. 193 (2014), 4779–4782.