The activation mechanism of 2′-5′-oligoadenylate synthetase gives new insights into OAS/cGAS triggers of innate immunity

Structure

Volumn 23, Issue 5, 2015, Pages 851-862

  Lohöfener, Jan ^a   Steinke, Nicola ^a,c   Kay Fedorov, Penelope ^a   Baruch, Petra ^a   Nikulin, Alexey ^b   Tishchenko, Svetlana ^b   Manstein, Dietmar J ^a   Fedorov, Roman ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b INSTITUTE OF PROTEIN RESEARCH   (Russian Federation)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

2',5' OLIGOADENYLATE SYNTHETASE; DOUBLE STRANDED RNA; MAGNESIUM; NUCLEOTIDYLTRANSFERASE;

ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME ACTIVATION; ENZYME ACTIVE SITE; GENETICS; IMMUNOLOGY; INNATE IMMUNITY; METABOLISM; PIG; POINT MUTATION; PROTEIN SECONDARY STRUCTURE; X RAY CRYSTALLOGRAPHY;

2',5'-OLIGOADENYLATE SYNTHETASE; ANIMALS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; ENZYME ACTIVATION; IMMUNITY, INNATE; MAGNESIUM; MODELS, MOLECULAR; NUCLEOTIDYLTRANSFERASES; POINT MUTATION; PROTEIN STRUCTURE, SECONDARY; RNA, DOUBLE-STRANDED; SWINE;

EID: 84930190707     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2015.03.012     Document Type: Article

References (48)

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. 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
3. P.B. Balbo, and A. Bohm Mechanism of poly(A) polymerase: structure of the enzyme-MgATP-RNA ternary complex and kinetic analysis Structure 15 2007 1117 1131
4. N. Bhat, and K.A. Fitzgerald Recognition of cytosolic DNA by cGAS and other STING-dependent sensors Eur. J. Immunol. 44 2014 634 640
5. P. Broz, and D.M. Monack Newly described pattern recognition receptors team up against intracellular pathogens Nat. Rev. Immunol. 13 2013 551 565
6. A.T. Brunger Version 1.2 of the Crystallography and NMR system Nat. Protoc. 2 2007 2728 2733
7. A. Chakrabarti, B.K. Jha, and R.H. Silverman New insights into the role of RNase L in innate immunity J. Interf. Cytokine Res. 31 2011 49 57
8. 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
9. J. Donovan, M. Dufner, and A. Korennykh Structural basis for cytosolic double-stranded RNA surveillance by human oligoadenylate synthetase 1 Proc. Natl. Acad. Sci. USA 110 2013 1652 1657
10. P. Emsley, B. Lohkamp, W.G. Scott, and K. Cowtan Features and development of Coot Acta Crystallogr. D Biol. Crystallogr. 66 2010 486 501
11. J. Führing, J.T. Cramer, F.H. Routier, A.-C. Lamerz, P. Baruch, R. Gerardy-Schahn, and R. Fedorov Catalytic mechanism and allosteric regulation of UDP-glucose pyrophosphorylase from Leishmania major ACS Catal. 3 2013 2976 2985
12. 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
13. R. Hartmann, J. Justesen, S.N. Sarkar, G.C. Sen, and V.C. Yee Crystal structure of the 2'-specific and double-stranded RNA-activated interferon-induced antiviral protein 2'-5'-oligoadenylate synthetase Mol. Cell 12 2003 1173 1185
14. V. Hornung, R. Hartmann, A. Ablasser, and K.-P. Hopfner OAS proteins and cGAS: unifying concepts in sensing and responding to cytosolic nucleic acids Nat. Rev. Immunol. 14 2014 521 528
15. A.G. Hovanessian, and J. Justesen The human 2'-5' oligoadenylate synthetase family: unique interferon-inducible enzymes catalyzing 2'-5' instead of 3'-5' phosphodiester bond formation Biochimie 89 2007 779 788
16. M.S. Ibsen, H.H. Gad, K. Thavachelvam, T. Boesen, P. Desprès, and R. Hartmann The 2'-5'-oligoadenylate synthetase 3 enzyme potently synthesizes the 2'-5'-oligoadenylates required for RNase L activation J. Virol. 88 2014 14222 14231
17. H. Ishikawa, Z. Ma, and G.N. Barber STING regulates intracellular DNA-mediated, type I interferon-dependent innate immunity Nature 461 2009 788 792
18. W. Kabsch Xds Acta Crystallogr. D Biol. Crystallogr. 66 2010 125 132
19. A. Kajaste-Rudnitski, T. Mashimo, M.-P. Frenkiel, J.-L. Guénet, M. Lucas, and P. Desprès The 2',5'-oligoadenylate synthetase 1b is a potent inhibitor of West Nile virus replication inside infected cells J. Biol. Chem. 281 2006 4624 4637
20. T. Kawai, and S. Akira Toll-like receptors and their crosstalk with other innate receptors in infection and immunity Immunity 34 2011 637 650
21. R. Kodym, E. Kodym, and M.D. Story 2'-5'-Oligoadenylate synthetase is activated by a specific RNA sequence motif Biochem. Biophys. Res. Commun. 388 2009 317 322
22. S. Koyama, K.J. Ishii, C. Coban, and S. Akira Innate immune response to viral infection Cytokine 43 2008 336 341
23. P.J. Kranzusch, A.S.-Y. Lee, J.M. Berger, and J.A. Doudna Structure of human cGAS reveals a conserved family of second-messenger enzymes in innate immunity Cell Rep. 3 2013 1362 1368
24. P.J. Kranzusch, A.S.-Y. Lee, S.C. Wilson, M.S. Solovykh, R.E. Vance, J.M. Berger, and J.A. Doudna Structure-guided reprogramming of human cGAS dinucleotide linkage specificity Cell 158 2014 1011 1021
25. H. Kristiansen, H.H. Gad, S. Eskildsen-Larsen, P. Despres, and R. Hartmann The oligoadenylate synthetase family: an ancient protein family with multiple antiviral activities J. Interf. Cytokine Res. 31 2011 41 47
26. G. Langer, S.X. Cohen, V.S. Lamzin, and A. Perrakis Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7 Nat. Protoc. 3 2008 1171 1179
27. M.S. Lee, B. Kim, G.T. Oh, and Y.-J. Kim OASL1 inhibits translation of the type I interferon-regulating transcription factor IRF7 Nat. Immunol. 14 2013 346 355
28. X.-D. Li, J. Wu, D. Gao, H. Wang, L. Sun, and Z.J. Chen Pivotal roles of cGAS-cGAMP signaling in antiviral defense and immune adjuvant effects Science 341 2013 1390 1394
29. 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. Crystallogr. 40 2007 658 674
30. B. Morin, N. Rabah, J. Boretto-Soler, H. Tolou, K. Alvarez, and B. Canard High yield synthesis, purification and characterisation of the RNase L activators 5'-triphosphate 2'-5'-oligoadenylates Antiviral Res. 87 2010 345 352
31. G.N. Murshudov, P. Skubák, A.A. Lebedev, N.S. Pannu, R.A. Steiner, R.A. Nicholls, M.D. Winn, F. Long, and A.A. Vagin REFMAC5 for the refinement of macromolecular crystal structures Acta Crystallogr. D Biol. Crystallogr. 67 2011 355 367
32. J. Navaza AMoRe: an automated package for molecular replacement Acta Crystallogr. A 50 1994 157 163
33. M.H. Orzalli, and D.M. Knipe Cellular sensing of viral DNA and viral evasion mechanisms Annu. Rev. Microbiol. 68 2014 477 492
34. B. Pan, Y. Xiong, and T.A. Steitz How the CCA-adding enzyme selects adenine over cytosine at position 76 of tRNA Science 330 2010 937 940
35. C. Peneff, P. Ferrari, V. Charrier, Y. Taburet, C. Monnier, V. Zamboni, J. Winter, M. Harnois, F. Fassy, and Y. Bourne Crystal structures of two human pyrophosphorylase isoforms in complexes with UDPGlc (Gal)NAc: role of the alternatively spliced insert in the enzyme oligomeric assembly and active site architecture EMBO J. 20 2001 6191 6202
36. D. Rebouillat, A. Hovnanian, I. Marié, and A.G. Hovanessian The 100-kDa 2'-5'-oligoadenylate synthetase catalyzing preferentially the synthesis of dimeric pppA2'p5'A molecules is composed of three homologous domains J. Biol. Chem. 274 1999 1557 1565
37. S. Reikine, J.B. Nguyen, and Y. Modis Pattern recognition and signaling mechanisms of RIG-I and MDA5 Front. Immunol. 5 2014 342
38. P.C. Ronald, and B. Beutler Plant and animal sensors of conserved microbial signatures Science 330 2010 1061 1064
39. S.N. Sarkar, S. Bandyopadhyay, A. Ghosh, and G.C. Sen Enzymatic characteristics of recombinant medium isozyme of 2'-5' oligoadenylate synthetase J. Biol. Chem. 274 1999 1848 1855
40. R.H. Silverman Viral encounters with 2',5'-oligoadenylate synthetase and RNase L during the interferon antiviral response J. Virol. 81 2007 12720 12729
41. T. Steiner, A.-C. Lamerz, P. Hess, C. Breithaupt, S. Krapp, G. Bourenkov, R. Huber, R. Gerardy-Schahn, and U. Jacob Open and closed structures of the UDP-glucose pyrophosphorylase from Leishmania major J. Biol. Chem. 282 2007 13003 13010
42. T.A. Steitz, and J.A. Steitz A general two-metal-ion mechanism for catalytic RNA Proc. Natl. Acad. Sci. USA 90 1993 6498 6502
43. 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
44. S. Torralba, J. Sojat, and R. Hartmann 2'-5' oligoadenylate synthetase shares active site architecture with the archaeal CCA-adding enzyme Cell. Mol. Life Sci. 65 2008 2613 2620
45. M.D. Winn, C.C. Ballard, K.D. Cowtan, E.J. Dodson, P. Emsley, P.R. Evans, R.M. Keegan, E.B. Krissinel, A.G.W. Leslie, and A. McCoy Overview of the CCP4 suite and current developments Acta Crystallogr. D Biol. Crystallogr. 67 2011 235 242
46. 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
47. W. Yang, J. Lee, and M. Nowotny Making and breaking nucleic acids: two-Mg2+-ion catalysis and substrate specificity Mol. Cell 22 2006 5 13
48. J. Zhu, Y. Zhang, A. Ghosh, R.A. Cuevas, A. Forero, J. Dhar, M.S. Ibsen, J.L. Schmid-Burgk, T. Schmidt, and M.K. Ganapathiraju Antiviral activity of human OASL protein is mediated by enhancing signaling of the RIG-I RNA sensor Immunity 40 2014 936 948