XStructure-function analysis of STING activation by c[G(2′,5′) pA(3′,5′)p] and targeting by antiviral DMXAA

Cell

Volumn 154, Issue 4, 2013, Pages

  Gao, Pu ^a   Ascano, Manuel ^b   Zillinger, Thomas ^c   Wang, Weiyi ^a   Dai, Peihong ^a   Serganov, Artem A ^b   Gaffney, Barbara L ^d   Shuman, Stewart ^a   Jones, Roger A ^d   Deng, Liang ^a   Hartmann, Gunther ^c   Barchet, Winfried ^c   Tuschl, Thomas ^b   Patel, Dinshaw J ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b ROCKEFELLER UNIVERSITY   (United States)

^c UNIVERSITY HOSPITAL BONN   (Germany)

^d RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; CYCLIC GMP; DINUCLEOTIDE; INTERFERON; PROTEIN; STING PROTEIN; UNCLASSIFIED DRUG; VADIMEZAN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DIMERIZATION; HUMAN; ISOMER; MOUSE; NONHUMAN; NUCLEOTIDE BINDING SITE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION;

METAZOA;

EID: 84882815198     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2013.07.023     Document Type: Article

References (34)

1. A. Ablasser, M. Goldeck, T. Cavlar, T. Deimling, G. Witte, I. Röhl, K.P. Hopfner, J. Ludwig, and V. Hornung cGAS produces a 2′-5′-linked cyclic dinucleotide second messenger that activates STING Nature 498 2013 380 384
2. B.C. Baguley, and L.M. Ching DMXAA: an antivascular agent with multiple host responses Int. J. Radiat. Oncol. Biol. Phys. 54 2002 1503 1511
3. D.L. Burdette, and R.E. Vance STING and the innate immune response to nucleic acids in the cytosol Nat. Immunol. 14 2013 19 26
4. D.L. Burdette, K.M. Monroe, K. Sotelo-Troha, J.S. Iwig, B. Eckert, M. Hyodo, Y. Hayakawa, and R.E. Vance STING is a direct innate immune sensor of cyclic di-GMP Nature 478 2011 515 518
5. T. Cavlar, T. Deimling, A. Ablasser, K.P. Hopfner, and V. Hornung Species-specific detection of the antiviral small-molecule compound CMA by STING EMBO J. 32 2013 1440 1450
6. F. Civril, T. Deimling, C.C. de Oliveira Mann, A. Ablasser, M. Moldt, G. Witte, V. Hornung, and K.P. Hopfner Structural mechanism of cytosolic DNA sensing by cGAS Nature 498 2013 332 337
7. J. Conlon, D.L. Burdette, S. Sharma, N. Bhat, M. Thompson, Z. Jiang, V.A. Rathinam, B. Monks, T. Jin, and T.S. Xiao Mouse, but not human STING, binds and signals in response to the vascular disrupting agent 5,6-dimethylxanthenone-4- acetic acid J. Immunol. 190 2013 5216 5225
8. E.J. Diner, D.L. Burdette, S.C. Wilson, K.M. Monroe, C.A. Kellenberger, M. Hyodo, Y. Hayakawa, M.C. Hammond, and R.E. Vance The innate immune DNA sensor cGAS produces a noncanonical cyclic dinucleotide that activates human STING Cell Rep 3 2013 1355 1361
9. A. Gall, P. Treuting, K.B. Elkon, Y.M. Loo, M. Gale Jr., G.N. Barber, and D.B. Stetson Autoimmunity initiates in nonhematopoietic cells and progresses via lymphocytes in an interferon-dependent autoimmune disease Immunity 36 2012 120 131
10. P. Gao, M. Ascano, Y. Wu, W. Barchet, B.L. Gaffney, T. Zillinger, A.A. Serganov, Y. Liu, R.A. Jones, and G. Hartmann Cyclic [G(2′,5′) pA(3′,5′)p] is the metazoan second messenger produced by DNA-activated cyclic GMP-AMP synthase Cell 153 2013 1094 1107
11. Y.H. Huang, X.Y. Liu, X.X. Du, Z.F. Jiang, and X.D. Su The structural basis for the sensing and binding of cyclic di-GMP by STING Nat. Struct. Mol. Biol. 19 2012 728 730
12. H. Ishikawa, and G.N. Barber STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling Nature 455 2008 674 678
13. S.E. Keating, M. Baran, and A.G. Bowie Cytosolic DNA sensors regulating type I interferon induction Trends Immunol. 32 2011 574 581
14. S. Kim, L. Li, Z. Maliga, Q. Yin, H. Wu, and T.J. Mitchison Anticancer flavonoids are mouse-selective STING agonists ACS Chem. Biol. 2013
15. P.N. Lara Jr., J.Y. Douillard, K. Nakagawa, J. von Pawel, M.J. McKeage, I. Albert, G. Losonczy, M. Reck, D.S. Heo, and X. Fan Randomized phase III placebo-controlled trial of carboplatin and paclitaxel with or without the vascular disrupting agent vadimezan (ASA404) in advanced non-small-cell lung cancer J. Clin. Oncol. 29 2011 2965 2971
16. S. Ouyang, X. Song, Y. Wang, H. Ru, N. Shaw, Y. Jiang, F. Niu, Y. Zhu, W. Qiu, and K. Parvatiyar Structural analysis of the STING adaptor protein reveals a hydrophobic dimer interface and mode of cyclic di-GMP binding Immunity 36 2012 1073 1086
17. S.R. Paludan, and A.G. Bowie Immune sensing of DNA Immunity 38 2013 870 880
18. D. Prantner, D.J. Perkins, W. Lai, M.S. Williams, S. Sharma, K.A. Fitzgerald, and S.N. Vogel 5,6-Dimethylxanthenone-4-acetic acid (DMXAA) activates stimulator of interferon gene (STING)-dependent innate immune pathways and is regulated by mitochondrial membrane potential J. Biol. Chem. 287 2012 39776 39788
19. S.B. Rasmussen, K.A. Horan, C.K. Holm, A.J. Stranks, T.C. Mettenleiter, A.K. Simon, S.B. Jensen, F.J. Rixon, B. He, and S.R. Paludan Activation of autophagy by α-herpesviruses in myeloid cells is mediated by cytoplasmic viral DNA through a mechanism dependent on stimulator of IFN genes J. Immunol. 187 2011 5268 5276
20. J.W. Schoggins, S.J. Wilson, M. Panis, M.Y. Murphy, C.T. Jones, P. Bieniasz, and C.M. Rice A diverse range of gene products are effectors of the type I interferon antiviral response Nature 472 2011 481 485
21. G. Shang, D. Zhu, N. Li, J. Zhang, C. Zhu, D. Lu, C. Liu, Q. Yu, Y. Zhao, S. Xu, and L. Gu Crystal structures of STING protein reveal basis for recognition of cyclic di-GMP Nat. Struct. Mol. Biol. 19 2012 725 727
22. C. Shu, G. Yi, T. Watts, C.C. Kao, and P. Li Structure of STING bound to cyclic di-GMP reveals the mechanism of cyclic dinucleotide recognition by the immune system Nat. Struct. Mol. Biol. 19 2012 722 724
23. W. Sun, Y. Li, L. Chen, H. Chen, F. You, X. Zhou, Y. Zhou, Z. Zhai, D. Chen, and Z. Jiang ERIS, an endoplasmic reticulum IFN stimulator, activates innate immune signaling through dimerization Proc. Natl. Acad. Sci. USA 106 2009 8653 8658
24. L. Sun, J. Wu, F. Du, X. Chen, and Z.J. Chen Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway Science 339 2013 786 791
25. J. Wu, L. Sun, X. Chen, F. Du, H. Shi, C. Chen, and Z.J. Chen Cyclic GMP-AMP is an endogenous second messenger in innate immune signaling by cytosolic DNA Science 339 2013 826 830
26. Q. Yin, Y. Tian, V. Kabaleeswaran, X. Jiang, D. Tu, M.J. Eck, Z.J. Chen, and H. Wu Cyclic di-GMP sensing via the innate immune signaling protein STING Mol. Cell 46 2012 735 745
27. X. Zhang, H. Shi, J. Wu, X. Zhang, L. Sun, C. Chen, and Z.J. Chen Cyclic GMP-AMP Containing Mixed Phosphodiester Linkages Is An Endogenous High-Affinity Ligand for STING Mol. Cell 51 2013 226 235
28. B. Zhong, Y. Yang, S. Li, Y.Y. Wang, Y. Li, F. Diao, C. Lei, X. He, L. Zhang, P. Tien, and H.B. Shu The adaptor protein MITA links virus-sensing receptors to IRF3 transcription factor activation Immunity 29 2008 538 550
29. P.D. Adams, P.V. Afonine, G. Bunkóczi, V.B. Chen, I.W. Davis, N. Echols, J.J. Headd, L.W. Hung, G.J. Kapral, and R.W. Grosse-Kunstleve PHENIX: a comprehensive Python-based system for macromolecular structure solution Acta Crystallogr. D Biol. Crystallogr. 66 2010 213 221
30. P. Emsley, B. Lohkamp, W.G. Scott, and K. Cowtan Features and development of Coot Acta Crystallogr. D Biol. Crystallogr. 66 2010 486 501
31. A.J. McCoy, R.W. Grosse-Kunstleve, P.D. Adams, M.D. Winn, L.C. Storoni, and R.J. Read Phaser crystallographic software J. Appl. Cryst. 40 2007 658 674
32. G.N. Murshudov, A.A. Vagin, and E.J. Dodson Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr. D Biol. Crystallogr. 53 1997 240 255
33. Z. Otwinowski, and W. Minor Processing of X-ray Diffraction Data Collected in Oscillation Mode Methods Enzymol. 276 1997 307 326
34. J.J. Woodward, A.T. Iavarone, and D.A. Portnoy c-di-AMP secreted by intracellular Listeria monocytogenes activates a host type I interferon response Science 328 2010 1703 1705