TRIM56-mediated monoubiquitination of cGAS for cytosolic DNA sensing

Nature Communications

Volumn 9, Issue 1, 2018, Pages

  Seo, Gil Ju ^a   Kim, Charlotte ^a   Shin, Woo Jin ^a   Sklan, Ella H ^a,b   Eoh, Hyungjin ^a   Jung, Jae U ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b TEL AVIV UNIVERSITY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIMICROBIAL ACTIVITY; BIOLOGICAL PRODUCTION; CHEMICAL REACTION; DNA; GENETIC ANALYSIS; IMMUNITY; INDUCED RESPONSE; SENSOR;

HUMAN HERPESVIRUS 1; INFLUENZA A VIRUS; MUS;

ALPHA BETA INTERFERON RECEPTOR; CYCLIC GMP; DNA; MB21D1 PROTEIN, HUMAN; NUCLEOTIDYLTRANSFERASE; TRIM56 PROTEIN, HUMAN; TRIPARTITE MOTIF PROTEIN; UBIQUITIN PROTEIN LIGASE;

ANIMAL; C57BL MOUSE; CHLOROCEBUS AETHIOPS; CYTOSOL; FEMALE; HEK293 CELL LINE; HERPES SIMPLEX; HUMAN; HUMAN ALPHAHERPESVIRUS 1; IMMUNOLOGY; INNATE IMMUNITY; KNOCKOUT MOUSE; MALE; MASS SPECTROMETRY; METABOLISM; MOUSE; SIGNAL TRANSDUCTION; UBIQUITINATION; VERO CELL LINE;

ANIMALS; CERCOPITHECUS AETHIOPS; CYCLIC GMP; CYTOSOL; DNA; FEMALE; HEK293 CELLS; HERPES SIMPLEX; HERPESVIRUS 1, HUMAN; HUMANS; IMMUNITY, INNATE; MALE; MASS SPECTROMETRY; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NUCLEOTIDYLTRANSFERASES; RECEPTOR, INTERFERON ALPHA-BETA; SIGNAL TRANSDUCTION; TRIPARTITE MOTIF PROTEINS; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION; VERO CELLS;

EID: 85044062135     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/s41467-018-02936-3     Document Type: Article

References (50)

1. Medzhitov, R. & Janeway, C. Jr. The Toll receptor family and microbial recognition. Trends Microbiol. 8, 452–456 (2000).
2. Elinav, E., Strowig, T., Henao-Mejia, J. & Flavell, R. A. Regulation of the antimicrobial response by NLR proteins. Immunity 34, 665–679 (2011).
3. Kawai, T. & Akira, S. Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 34, 637–650 (2011).
4. Paludan, S. R. & Bowie, A. G. Immune sensing of DNA. Immunity 38, 870–880 (2013).
5. Fernandes-Alnemri, T., Yu, J. W., Datta, P., Wu, J. & Alnemri, E. S. AIM2 activates the inflammasome and cell death in response to cytoplasmic DNA. Nature 458, 509–513 (2009).
6. Hornung, V. et al. AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature 458, 514–518 (2009).
7. Roberts, T. L. et al. HIN-200 proteins regulate caspase activation in response to foreign cytoplasmic DNA. Science 323, 1057–1060 (2009).
8. Takaoka, A. et al. DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune response. Nature 448, 501–505 (2007).
9. Zhang, Z. et al. The helicase DDX41 senses intracellular DNA mediated by the adaptor STING in dendritic cells. Nat. Immunol. 12, 959–965 (2011).
10. Ferguson, B. J., Mansur, D. S., Peters, N. E., Ren, H. & Smith, G. L. DNA-PK is a DNA sensor for IRF-3-dependent innate immunity. eLife 1, e00047 (2012).
11. Unterholzner, L. et al. IFI16 is an innate immune sensor for intracellular DNA. Nat. Immunol. 11, 997–1004 (2010).
12. Ablasser, A. et al. RIG-I-dependent sensing of poly(dA:dT) through the induction of an RNA polymerase III-transcribed RNA intermediate. Nat. Immunol. 10, 1065–1072 (2009).
13. Chiu, Y. H., Macmillan, J. B. & Chen, Z. J. RNA polymerase III detects cytosolic DNA and induces type I interferons through the RIG-I pathway. Cell 138, 576–591 (2009).
14. Li, X. D. et al. Pivotal roles of cGAS-cGAMP signaling in antiviral defense and immune adjuvant effects. Science 341, 1390–1394 (2013).
15. Sun, L., Wu, J., Du, F., Chen, X. & Chen, Z. J. Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway. Science 339, 786–791 (2013).
16. Gao, P. et al. Cyclic [G(2’,5’)pA(3’,5’)p] is the metazoan second messenger produced by DNA-activated cyclic GMP-AMP synthase. Cell 153, 1094–1107 (2013).
17. Kranzusch, P. J., Lee, A. S., Berger, J. M. & Doudna, J. A. Structure of human cGAS reveals a conserved family of second-messenger enzymes in innate immunity. Cell Rep. 3, 1362–1368 (2013).
18. Wu, J. et al. Cyclic GMP-AMP is an endogenous second messenger in innate immune signaling by cytosolic DNA. Science 339, 826–830 (2013).
19. Ablasser, A. et al. cGAS produces a 2’-5’-linked cyclic dinucleotide second messenger that activates STING. Nature 498, 380–384 (2013).
20. Bhat, N. & Fitzgerald, K. A. Recognition of cytosolic DNA by cGAS and other STING-dependent sensors. Eur. J. Immunol. 44, 634–640 (2014).
21. Liang, Q. et al. Crosstalk between the cGAS DNA sensor and Beclin-1 autophagy protein shapes innate antimicrobial immune responses. Cell Host Microbe 15, 228–238 (2014).
22. Chen, Q., Sun, L. & Chen, Z. J. Regulation and function of the cGAS-STING pathway of cytosolic DNA sensing. Nat. Immunol. 17, 1142–1149 (2016).
23. Xia, P. et al. Glutamylation of the DNA sensor cGAS regulates its binding and synthase activity in antiviral immunity. Nat. Immunol. 17, 369–378 (2016).
24. Seo, G. J. et al. Akt kinase-mediated checkpoint of cGAS DNA sensing pathway. Cell Rep. 13, 440–449 (2015).
25. Welchman, R. L., Gordon, C. & Mayer, R. J. Ubiquitin and ubiquitin-like proteins as multifunctional signals. Nat. Rev. Mol. Cell Biol. 6, 599–609 (2005).
26. Wang, Q. et al. The E3 ubiquitin ligase RNF185 facilitates the cGAS-mediated innate immune response. PLoS Pathog. 13, e1006264 (2017).
27. Ozato, K., Shin, D. M., Chang, T. H. & Morse, H. C. 3rd TRIM family proteins and their emerging roles in innate immunity. Nat. Rev. Immunol. 8, 849–860 (2008).
28. Yan, J., Li, Q., Mao, A. P., Hu, M. M. & Shu, H. B. TRIM4 modulates type I interferon induction and cellular antiviral response by targeting RIG-I for K63-linked ubiquitination. J. Mol. Cell Biol. 6, 154–163 (2014).
29. Liu, B. et al. The C-terminal tail of TRIM56 dictates antiviral restriction of influenza A and B viruses by impeding viral RNA synthesis. J. Virol. 90, 4369–4382 (2016).
30. Liu, B. et al. Overlapping and distinct molecular determinants dictating the antiviral activities of TRIM56 against flaviviruses and coronavirus. J. Virol. 88, 13821–13835 (2014).
31. Wang, J. et al. TRIM56 is a virus- and interferon-inducible E3 ubiquitin ligase that restricts pestivirus infection. J. Virol. 85, 3733–3745 (2011).
32. Kamanova, J., Sun, H., Lara-Tejero, M. & Galan, J. E. The Salmonella effector protein SopA modulates innate immune responses by targeting TRIM E3 ligase family members. PLoS Pathog. 12, e1005552 (2016).
33. Tsuchida, T. et al. The ubiquitin ligase TRIM56 regulates innate immune responses to intracellular double-stranded DNA. Immunity 33, 765–776 (2010).
34. Wang, Q. et al. The E3 ubiquitin ligase AMFR and INSIG1 bridge the activation of TBK1 kinase by modifying the adaptor STING. Immunity 41, 919–933 (2014).
35. Jain, A., Liu, R., Xiang, Y. K. & Ha, T. Single-molecule pull-down for studying protein interactions. Nat. Protoc. 7, 445–452 (2012).
36. Gao, D. et al. Cyclic GMP-AMP synthase is an innate immune sensor of HIV and other retroviruses. Science 341, 903–906 (2013).
37. Kanai, R. et al. Effect of gamma 34.5 deletions on oncolytic herpes simplex virus activity in brain tumors. J. Virol. 86, 4420–4431 (2012).
38. Li, Y. et al. ICP34.5 protein of herpes simplex virus facilitates the initiation of protein translation by bridging eukaryotic initiation factor 2alpha (eIF2alpha) and protein phosphatase 1. J. Biol. Chem. 286, 24785–24792 (2011).
39. Orvedahl, A. et al. HSV-1 ICP34.5 confers neurovirulence by targeting the Beclin 1 autophagy protein. Cell Host Microbe 1, 23–35 (2007).
40. Zhang, X. et al. The cytosolic DNA sensor cGAS forms an oligomeric complex with DNA and undergoes switch-like conformational changes in the activation loop. Cell Rep. 6, 421–430 (2014).
41. Li, X. et al. Cyclic GMP-AMP synthase is activated by double-stranded DNA-induced oligomerization. Immunity 39, 1019–1031 (2013).
42. Jain, A. et al. Probing cellular protein complexes using single-molecule pull-down. Nature 473, 484–488 (2011).
43. Loedige, I. et al. The NHL domain of BRAT is an RNA-binding domain that directly contacts the hunchback mRNA for regulation. Genes Dev. 28, 749–764 (2014).
44. Schwamborn, J. C., Berezikov, E. & Knoblich, J. A. The TRIM-NHL protein TRIM32 activates microRNAs and prevents self-renewal in mouse neural progenitors. Cell 136, 913–925 (2009).
45. Wang, Y. et al. Inflammasome activation triggers caspase-1-mediated cleavage of cGAS to regulate responses to DNA virus infection. Immunity 46, 393–404 (2017).
46. Shen, Y. et al. TRIM56 is an essential component of the TLR3 antiviral signaling pathway. J. Biol. Chem. 287, 36404–36413 (2012).
47. Kane, M. et al. Identification of interferon-stimulated genes with antiretroviral activity. Cell Host Microbe 20, 392–405 (2016).
48. Robledo, C. et al. Molecular characterization of the region 7q22.1 in splenic marginal zone lymphomas. PLoS ONE 6, e24939 (2011).
49. Roy, D., Sin, S. H., Damania, B. & Dittmer, D. P. Tumor suppressor genes FHIT and WWOX are deleted in primary effusion lymphoma (PEL) cell lines. Blood 118, e32–39 (2011).
50. Gack, M. U., Nistal-Villan, E., Inn, K. S., Garcia-Sastre, A. & Jung, J. U. Phosphorylation-mediated negative regulation of RIG-I antiviral activity. J. Virol. 84, 3220–3229 (2010).