Activation of STING requires palmitoylation at the Golgi

Nature Communications

Volumn 7, Issue , 2016, Pages

  Mukai, Kojiro ^a,b   Konno, Hiroyasu ^c   Akiba, Tatsuya ^a   Uemura, Takefumi ^d   Waguri, Satoshi ^d   Kobayashi, Toshihide ^b   Barber, Glen N ^c   Arai, Hiroyuki ^a   Taguchi, Tomohiko ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b RIKEN   (Japan)

^c UNIVERSITY OF MIAMI   (United States)

^d FUKUSHIMA MEDICAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

2 BROMOPALMITIC ACID; 2-BROMOPALMITATE; INTERFERON; MEMBRANE PROTEIN; MPYS PROTEIN, HUMAN; PALMITIC ACID DERIVATIVE; PROTEIN SERINE THREONINE KINASE; TBK1 PROTEIN, HUMAN; VADIMEZAN; XANTHONE DERIVATIVE;

CELL ORGANELLE; CHEMICAL REACTION; DNA; GENE EXPRESSION; IMMUNE RESPONSE; INHIBITOR; MOLECULAR ANALYSIS; MUTATION; PATHOGEN; TRANSLOCATION;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AUTOIMMUNE DISEASE; AUTOINFLAMMATORY DISEASE; AUTOPHOSPHORYLATION; CONTROLLED STUDY; GENE; GENE ACTIVATION; GOLGI COMPLEX; MOUSE; NONHUMAN; PALMITOYLATION; PROTEIN DEGRADATION; PROTEIN PROCESSING; SIGNAL TRANSDUCTION; STIMULATOR OF INTERFERON GENE; AGONISTS; ANIMAL; ANTAGONISTS AND INHIBITORS; CHLOROCEBUS AETHIOPS; CV-1 CELL LINE; ENDOPLASMIC RETICULUM; FIBROBLAST; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEK293 CELL LINE; HUMAN; HUMAN ALPHAHERPESVIRUS 1; IMMUNOLOGY; INNATE IMMUNITY; LIPOYLATION; MAMMALIAN EMBRYO; METABOLISM; MUTATION; PRIMARY CELL CULTURE; PROTEIN TRANSPORT; VIROLOGY;

ANIMALS; CERCOPITHECUS AETHIOPS; COS CELLS; EMBRYO, MAMMALIAN; ENDOPLASMIC RETICULUM; FIBROBLASTS; GENE EXPRESSION REGULATION; GOLGI APPARATUS; HEK293 CELLS; HERPESVIRUS 1, HUMAN; HUMANS; IMMUNITY, INNATE; INTERFERON TYPE I; LIPOYLATION; MEMBRANE PROTEINS; MICE; MUTATION; PALMITATES; PRIMARY CELL CULTURE; PROTEIN TRANSPORT; PROTEIN-SERINE-THREONINE KINASES; XANTHONES;

EID: 84975849555     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms11932     Document Type: Article

References (40)

1. Palm, N. W. & Medzhitov, R. Pattern recognition receptors and control of adaptive immunity. Immunol. Rev. 227, 221-233 (2009).
2. Takeuchi, O. & Akira, S. Pattern recognition receptors and inflammation. Cell 140, 805-820 (2010).
3. Blasius, A. L. & Beutler, B. Intracellular toll-like receptors. Immunity 32, 305-315 (2010).
4. Yoneyama, M. et al. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol. 5, 730-737 (2004).
5. Ye, Z. & Ting, J. P. NLR, the nucleotide-binding domain leucine-rich repeat containing gene family. Curr. Opin. Immunol. 20, 3-9 (2008).
6. Ishikawa, H., Ma, Z. & Barber, G. N. STING regulates intracellular DNA-mediated, type I interferon-dependent innate immunity. Nature 461, 788-792 (2009).
7. Ishikawa, H. & Barber, G. N. STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling. Nature 455, 674-678 (2008).
8. Zhong, B. et al. The adaptor protein MITA links virus-sensing receptors to IRF3 transcription factor activation. Immunity 29, 538-550 (2008).
9. Sun, W. et al. ERIS, an endoplasmic reticulum IFN stimulator, activates innate immune signalling through dimerization. Proc. Natl Acad. Sci. USA 106, 8653-8658 (2009).
10. Jin, L. et al. MPYS, a novel membrane tetraspanner, is associated with major histocompatibility complex class II and mediates transduction of apoptotic signals. Mol. Cell. Biol. 28, 5014-5026 (2008).
11. Wu, J. et al. Cyclic GMP-AMP is an endogenous second messenger in innate immune signalling by cytosolic DNA. Science 339, 826-830 (2013).
12. Burdette, D. L. et al. STING is a direct innate immune sensor of cyclic di-GMP. Nature 478, 515-518 (2011).
13. Abe, T. et al. STING recognition of cytoplasmic DNA instigates cellular defense. Mol. Cell 50, 5-15 (2013).
14. Gall, A. et al. Autoimmunity initiates in nonhematopoietic cells and progresses via lymphocytes in an interferon-dependent autoimmune disease. Immunity 36, 120-131 (2012).
15. Ahn, J., Gutman, D., Saijo, S. & Barber, G. N. STING manifests self DNA-dependent inflammatory disease. Proc. Natl Acad. Sci. USA 109, 19386-19391 (2012).
16. Ahn, J., Ruiz, P. & Barber, G. N. Intrinsic self-DNA triggers inflammatory disease dependent on STING. J. Immunol. 193, 4634-4642 (2014).
17. Lee-Kirsch, M. A. et al. Mutations in the gene encoding the 3'-5' DNA exonuclease TREX1 are associated with systemic lupus erythematosus. Nat. Genet. 39, 1065-1067 (2007).
18. Rice, G. et al. Heterozygous mutations in TREX1 cause familial chilblain lupus and dominant Aicardi-Goutieres syndrome. Am. J. Hum. Genet. 80, 811-815 (2007).
19. Liu, Y. et al. Activated STING in a vascular and pulmonary syndrome. N. Engl. J. Med. 371, 507-518 (2014).
20. Jeremiah, N. et al. Inherited STING-Activating mutation underlies a familial inflammatory syndrome with lupus-like manifestations. J. Clin. Invest. 124, 5516-5520 (2014).
21. Dobbs, N. et al. STING activation by translocation from the ER is associated with infection and autoinflammatory disease. Cell Host Microbe 18, 157-168 (2015).
22. Saitoh, T. et al. Atg9a controls dsDNA-driven dynamic translocation of STING and the innate immune response. Proc. Natl Acad. Sci. USA 106, 20842-20846 (2009).
23. Konno, H., Konno, K. & Barber, G. N. Cyclic dinucleotides trigger ULK1 (ATG1) phosphorylation of STING to prevent sustained innate immune signalling. Cell 155, 688-698 (2013).
24. Misaki, R., Nakagawa, T., Fukuda, M., Taniguchi, N. & Taguchi, T. Spatial segregation of degradation-And recycling-trafficking pathways in COS-1 cells. Biochem. Biophys. Res. Commun. 360, 580-585 (2007).
25. Soulat, D. et al. The DEAD-box helicase DDX3X is a critical component of the TANK-binding kinase 1-dependent innate immune response. EMBO J. 27, 2135-2146 (2008).
26. Lippincott-Schwartz, J. et al. Microtubule-dependent retrograde transport of proteins into the ER in the presence of brefeldin A suggests an ER recycling pathway. Cell 60, 821-836 (1990).
27. Griffiths, G. & Simons, K. The trans Golgi network: sorting at the exit site of the Golgi complex. Science 234, 438-443 (1986).
28. De Matteis, M. A. & Luini, A. Exiting the Golgi complex. Nat. Rev. Mol. Cell Biol. 9, 273-284 (2008).
29. Shima, D. T., Haldar, K., Pepperkok, R., Watson, R. & Warren, G. Partitioning of the Golgi apparatus during mitosis in living HeLa cells. J. Cell Biol. 137, 1211-1228 (1997).
30. Linder, M. E. & Deschenes, R. J. Palmitoylation: policing protein stability and traffic. Nat. Rev. Mol. Cell Biol. 8, 74-84 (2007).
31. Ouyang, S. et al. Structural analysis of the STING adaptor protein reveals a hydrophobic dimer interface and mode of cyclic di-GMP binding. Immunity 36, 1073-1086 (2012).
32. Drisdel, R. C., Alexander, J. K., Sayeed, A. & Green, W. N. Assays of protein palmitoylation. Methods 40, 127-134 (2006).
33. Tanaka, Y. & Chen, Z. J. STING specifies IRF3 phosphorylation by TBK1 in the cytosolic DNA signalling pathway. Sci. Signal 5, ra20 (2012).
34. Duran, J. M. et al. Sphingomyelin organization is required for vesicle biogenesis at the Golgi complex. EMBO J. 31, 4535-4546 (2012).
35. Fukata, M., Fukata, Y., Adesnik, H., Nicoll, R. A. & Bredt, D. S. Identification of PSD-95 palmitoylating enzymes. Neuron 44, 987-996 (2004).
36. Ahn, J. & Barber, G. N. Self-DNA, STING-dependent signalling and the origins of autoinflammatory disease. Curr. Opin. Immunol. 31, 121-126 (2014).
37. West, A. P. et al. Mitochondrial DNA stress primes the antiviral innate immune response. Nature 520, 553-557 (2015).
38. Stetson, D. B. & Medzhitov, R. Recognition of cytosolic DNA activates an IRF3-dependent innate immune response. Immunity 24, 93-103 (2006).
39. Woodward, J. J., Iavarone, A. T. & Portnoy, D. A. c-di-AMP secreted by intracellular Listeria monocytogenes activates a host type I interferon response. Science 328, 1703-1705 (2010).
40. Uemura, T. et al. A cluster of thin tubular structures mediates transformation of the endoplasmic reticulum to autophagic isolation membrane. Mol. Cell. Biol. 34, 1695-1706 (2014).