Inhibition of cGAS DNA Sensing by a Herpesvirus Virion Protein

Cell Host and Microbe

Volumn 18, Issue 3, 2015, Pages 333-344

  Wu, Jian Jun ^a   Li, Wenwei ^a   Shao, Yaming ^a   Avey, Denis ^a   Fu, Bishi ^a   Gillen, Joseph ^a   Hand, Travis ^a   Ma, Siming ^a   Liu, Xia ^a   Miley, Wendell ^b   Konrad, Andreas ^c   Neipel, Frank ^d   Stürzl, Michael ^c   Whitby, Denise ^b   Li, Hong ^a   Zhu, Fanxiu ^a  

^a FLORIDA STATE UNIVERSITY   (United States)

^b FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

^c UNIVERSITY HOSPITAL ERLANGEN   (Germany)

^d UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC GMP; CYCLIC GMP AMP SYNTHASE; ORF 52 PROTEIN; UNCLASSIFIED DRUG; VIRUS DNA; VIRUS PROTEIN; MB21D1 PROTEIN, HUMAN; NUCLEOTIDYLTRANSFERASE; VIRAL PROTEIN;

ARTICLE; DNA BINDING; ENZYME ACTIVITY; HERPES VIRUS INFECTION; HUMAN; HUMAN CELL; HUMAN HERPESVIRUS 8; IMMUNE RESPONSE; KAPOSI SARCOMA; KAPOSI SARCOMA ASSOCIATED HERPESVIRUS INFECTION; MUTANT; NONHUMAN; PRIORITY JOURNAL; VIRION; ANTAGONISTS AND INHIBITORS; CELL LINE; HOST PATHOGEN INTERACTION; IMMUNE EVASION; METABOLISM; PHYSIOLOGY;

CELL LINE; DNA, VIRAL; HERPESVIRUS 8, HUMAN; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNE EVASION; NUCLEOTIDYLTRANSFERASES; VIRAL PROTEINS;

EID: 84941271782     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2015.07.015     Document Type: Article

References (69)

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. A. Ablasser, J.L. Schmid-Burgk, I. Hemmerling, G.L. Horvath, T. Schmidt, E. Latz, and V. Hornung Cell intrinsic immunity spreads to bystander cells via the intercellular transfer of cGAMP Nature 503 2013 530 534
3. A. Ablasser, I. Hemmerling, J.L. Schmid-Burgk, R. Behrendt, A. Roers, and V. Hornung TREX1 deficiency triggers cell-autonomous immunity in a cGAS-dependent manner J. Immunol. 192 2014 5993 5997
4. J. Ahn, and G.N. Barber Self-DNA, STING-dependent signaling and the origins of autoinflammatory disease Curr. Opin. Immunol. 31 2014 121 126
5. M.S. Anderson, M.S. Loftus, and D.H. Kedes Maturation and vesicle-mediated egress of primate gammaherpesvirus rhesus monkey rhadinovirus require inner tegument protein ORF52 J. Virol. 88 2014 9111 9128
6. G.N. Barber STING-dependent cytosolic DNA sensing pathways Trends Immunol. 35 2014 88 93
7. M. Becker-Hapak, and S.F. Dowdy Protein transduction: generation of full-length transducible proteins using the TAT system Curr. Protoc. Cell Biol. 18 2003 10.1002/0471143030.cb2002s18
8. E. Bortz, J.P. Whitelegge, Q. Jia, Z.H. Zhou, J.P. Stewart, T.-T. Wu, and R. Sun Identification of proteins associated with murine gammaherpesvirus 68 virions J. Virol. 77 2003 13425 13432
9. E. Bortz, L. Wang, Q. Jia, T.-T. Wu, J.P. Whitelegge, H. Deng, Z.H. Zhou, and R. Sun Murine gammaherpesvirus 68 ORF52 encodes a tegument protein required for virion morphogenesis in the cytoplasm J. Virol. 81 2007 10137 10150
10. K.F. Brulois, H. Chang, A.S.-Y. Lee, A. Ensser, L.-Y. Wong, Z. Toth, S.H. Lee, H.-R. Lee, J. Myoung, D. Ganem, and et al. Construction and manipulation of a new Kaposi's sarcoma-associated herpesvirus bacterial artificial chromosome clone J. Virol. 86 2012 9708 9720
11. T. Bürckstümmer, C. Baumann, S. Blüml, E. Dixit, G. Dürnberger, H. Jahn, M. Planyavsky, M. Bilban, J. Colinge, K.L. Bennett, and G. Superti-Furga An orthogonal proteomic-genomic screen identifies AIM2 as a cytoplasmic DNA sensor for the inflammasome Nat. Immunol. 10 2009 266 272
12. X. Cai, Y.H. Chiu, and Z.J. Chen The cGAS-cGAMP-STING pathway of cytosolic DNA sensing and signaling Mol. Cell 54 2014 289 296
13. E. Cesarman, Y. Chang, P.S. Moore, J.W. Said, and D.M. Knowles Kaposi's sarcoma-associated herpesvirus-like DNA sequences in AIDS-related body-cavity-based lymphomas N. Engl. J. Med. 332 1995 1186 1191
14. Y. Chang, E. Cesarman, M.S. Pessin, F. Lee, J. Culpepper, D.M. Knowles, and P.S. Moore Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposi's sarcoma Science 266 1994 1865 1869
15. 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
16. A.C. Collins, H. Cai, T. Li, L.H. Franco, X.D. Li, V.R. Nair, C.R. Scharn, C.E. Stamm, B. Levine, Z.J. Chen, and M.U. Shiloh Cyclic GMP-AMP synthase is an innate immune DNA sensor for Mycobacterium tuberculosis Cell Host Microbe 17 2015 820 828
17. P. Dai, W. Wang, H. Cao, F. Avogadri, L. Dai, I. Drexler, J.A. Joyce, X.-D. Li, Z. Chen, T. Merghoub, and et al. Modified vaccinia virus Ankara triggers type I IFN production in murine conventional dendritic cells via a cGAS/STING-mediated cytosolic DNA-sensing pathway PLoS Pathog. 10 2014 e1003989
18. T. Fernandes-Alnemri, J.-W. Yu, P. Datta, J. Wu, and E.S. Alnemri AIM2 activates the inflammasome and cell death in response to cytoplasmic DNA Nature 458 2009 509 513
19. B. Fu, E. Kuang, W. Li, D. Avey, X. Li, Z. Turpin, A. Valdes, K. Brulois, J. Myoung, and F. Zhu Activation of p90 ribosomal S6 kinases by ORF45 of Kaposi's sarcoma-associated herpesvirus is critical for optimal production of infectious viruses J. Virol. 89 2015 195 207
20. M.U. Gack Mechanisms of RIG-I-like receptor activation and manipulation by viral pathogens J. Virol. 88 2014 5213 5216
21. D. Ganem Kaposi's sarcoma-associated herpesvirus D.M. Knipe, P.M. Howley, D.E. Griffin, R.A. Lamb, M.A. Martin, B. Roizman, S.E. Straus, Fields Virology 2007 Lippincott Williams & Wilkins Philadelphia 2847 2888
22. D. Ganem KSHV and the pathogenesis of Kaposi sarcoma: listening to human biology and medicine J. Clin. Invest. 120 2010 939 949
23. S.J. Gao, C. Boshoff, S. Jayachandra, R.A. Weiss, Y. Chang, and P.S. Moore KSHV ORF K9 (vIRF) is an oncogene which inhibits the interferon signaling pathway Oncogene 15 1997 1979 1985
24. D. Gao, J. Wu, Y.-T. Wu, F. Du, C. Aroh, N. Yan, L. Sun, and Z.J. Chen Cyclic GMP-AMP synthase is an innate immune sensor of HIV and other retroviruses Science 341 2013 903 906
25. P. Gao, M. Ascano, Y. Wu, W. Barchet, B.L. Gaffney, T. Zillinger, A.A. Serganov, Y. Liu, R.A. Jones, G. Hartmann, and 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 2013 1094 1107
26. P. Gao, M. Ascano, T. Zillinger, W. Wang, P. Dai, A.A. Serganov, B.L. Gaffney, S. Shuman, R.A. Jones, L. Deng, and 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
27. K. Hansen, T. Prabakaran, A. Laustsen, S.E. Jørgensen, S.H. Rahbæk, S.B. Jensen, R. Nielsen, J.H. Leber, T. Decker, K.A. Horan, and et al. Listeria monocytogenes induces IFNβ expression through an IFI16-, cGAS- and STING-dependent pathway EMBO J. 33 2014 1654 1666
28. J.W. Heine, R.W. Honess, E. Cassai, and B. Roizman Proteins specified by herpes simplex virus. XII. The virion polypeptides of type 1 strains J. Virol. 14 1974 640 651
29. K. Hew, S.L. Dahlroth, L.X. Pan, T. Cornvik, and P. Nordlund The core domain of VP22 from herpes simplex virus 1 reveals a surprising structural conservation in both the alpha and the gamma herpesvirus subfamilies J. Gen. Virol. 2015
30. K.A. Horan, K. Hansen, M.R. Jakobsen, C.K. Holm, S. Søby, L. Unterholzner, M. Thompson, J.A. West, M.B. Iversen, S.B. Rasmussen, and et al. Proteasomal degradation of herpes simplex virus capsids in macrophages releases DNA to the cytosol for recognition by DNA sensors J. Immunol. 190 2013 2311 2319
31. V. Hornung, A. Ablasser, M. Charrel-Dennis, F. Bauernfeind, G. Horvath, D.R. Caffrey, E. Latz, and K.A. Fitzgerald AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC Nature 458 2009 514 518
32. S. Hwang, K.S. Kim, E. Flano, T.-T. Wu, L.M. Tong, A.N. Park, M.J. Song, D.J. Sanchez, R.M. O'Connell, G. Cheng, and R. Sun Conserved herpesviral kinase promotes viral persistence by inhibiting the IRF-3-mediated type I interferon response Cell Host Microbe 5 2009 166 178
33. K.-S. Inn, S.-H. Lee, J.Y. Rathbun, L.-Y. Wong, Z. Toth, K. Machida, J.-H.J. Ou, and J.U. Jung Inhibition of RIG-I-mediated signaling by Kaposi's sarcoma-associated herpesvirus-encoded deubiquitinase ORF64 J. Virol. 85 2011 10899 10904
34. E. Johannsen, M. Luftig, M.R. Chase, S. Weicksel, E. Cahir-McFarland, D. Illanes, D. Sarracino, and E. Kieff Proteins of purified Epstein-Barr virus Proc. Natl. Acad. Sci. USA 101 2004 16286 16291
35. H. Konno, K. Konno, and G.N. Barber Cyclic dinucleotides trigger ULK1 (ATG1) phosphorylation of STING to prevent sustained innate immune signaling Cell 155 2013 688 698
36. P.J. Kranzusch, A.S. 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
37. E. Lam, S. Stein, and E. Falck-Pedersen Adenovirus detection by the cGAS/STING/TBK1 DNA sensing cascade J. Virol. 88 2014 974 981
38. X. Li, C. Shu, G. Yi, C.T. Chaton, C.L. Shelton, J. Diao, X. Zuo, C.C. Kao, A.B. Herr, and P. Li Cyclic GMP-AMP synthase is activated by double-stranded DNA-induced oligomerization Immunity 39 2013 1019 1031
39. 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
40. Q. Liang, B. Fu, F. Wu, X. Li, Y. Yuan, and F. Zhu ORF45 of Kaposi's sarcoma-associated herpesvirus inhibits phosphorylation of interferon regulatory factor 7 by IKKε and TBK1 as an alternative substrate J. Virol. 86 2012 10162 10172
41. Q. Liang, G.J. Seo, Y.J. Choi, M.J. Kwak, J. Ge, M.A. Rodgers, M. Shi, B.J. Leslie, K.P. Hopfner, T. Ha, and et al. Crosstalk between the cGAS DNA sensor and Beclin-1 autophagy protein shapes innate antimicrobial immune responses Cell Host Microbe 15 2014 228 238
42. R. Lin, P. Genin, Y. Mamane, M. Sgarbanti, A. Battistini, W.J. Harrington Jr., G.N. Barber, and J. Hiscott HHV-8 encoded vIRF-1 represses the interferon antiviral response by blocking IRF-3 recruitment of the CBP/p300 coactivators Oncogene 20 2001 800 811
43. J. Myoung, and D. Ganem Generation of a doxycycline-inducible KSHV producer cell line of endothelial origin: maintenance of tight latency with efficient reactivation upon induction J. Virol. Methods 174 2011 12 21
44. K. Nealon, W.W. Newcomb, T.R. Pray, C.S. Craik, J.C. Brown, and D.H. Kedes Lytic replication of Kaposi's sarcoma-associated herpesvirus results in the formation of multiple capsid species: isolation and molecular characterization of A, B, and C capsids from a gammaherpesvirus J. Virol. 75 2001 2866 2878
45. C.M. O'Connor, and D.H. Kedes Mass spectrometric analyses of purified rhesus monkey rhadinovirus reveal 33 virion-associated proteins J. Virol. 80 2006 1574 1583
46. M.H. Orzalli, and D.M. Knipe Cellular sensing of viral DNA and viral evasion mechanisms Annu. Rev. Microbiol. 68 2014 477 492
47. S.R. Paludan, A.G. Bowie, K.A. Horan, and K.A. Fitzgerald Recognition of herpesviruses by the innate immune system Nat. Rev. Immunol. 11 2011 143 154
48. G. Sander, A. Konrad, M. Thurau, E. Wies, R. Leubert, E. Kremmer, H. Dinkel, T. Schulz, F. Neipel, and M. Stürzl Intracellular localization map of human herpesvirus 8 proteins J. Virol. 82 2008 1908 1922
49. N. Sathish, and Y. Yuan Evasion and subversion of interferon-mediated antiviral immunity by Kaposi's sarcoma-associated herpesvirus: an overview J. Virol. 85 2011 10934 10944
50. 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
51. J.W. Schoggins, D.A. MacDuff, N. Imanaka, M.D. Gainey, B. Shrestha, J.L. Eitson, K.B. Mar, R.B. Richardson, A.V. Ratushny, V. Litvak, and et al. Pan-viral specificity of IFN-induced genes reveals new roles for cGAS in innate immunity Nature 505 2014 691 695
52. J. Soulier, L. Grollet, E. Oksenhendler, P. Cacoub, D. Cazals-Hatem, P. Babinet, M.F. d'Agay, J.P. Clauvel, M. Raphael, L. Degos, and et al. Kaposi's sarcoma-associated herpesvirus-like DNA sequences in multicentric Castleman's disease Blood 86 1995 1276 1280
53. P.G. Spear, and B. Roizman Proteins specified by herpes simplex virus. V. Purification and structural proteins of the herpesvirion J. Virol. 9 1972 143 159
54. K.M. Storek, N.A. Gertsvolf, M.B. Ohlson, and D.M. Monack cGAS and Ifi204 cooperate to produce type I IFNs in response to Francisella infection J. Immunol. 194 2015 3236 3245
55. 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
56. Y. Tanaka, and Z.J. Chen STING specifies IRF3 phosphorylation by TBK1 in the cytosolic DNA signaling pathway Sci. Signal. 5 2012 ra20
57. L. Wang, H. Guo, N. Reyes, S. Lee, E. Bortz, F. Guo, R. Sun, L. Tong, and H. Deng Distinct domains in ORF52 tegument protein mediate essential functions in murine gammaherpesvirus 68 virion tegumentation and secondary envelopment J. Virol. 86 2012 1348 1357
58. S. Wang, K. Wang, J. Li, and C. Zheng Herpes simplex virus 1 ubiquitin-specific protease UL36 inhibits beta interferon production by deubiquitinating TRAF3 J. Virol. 87 2013 11851 11860
59. R. Wassermann, M.F. Gulen, C. Sala, S.G. Perin, Y. Lou, J. Rybniker, J.L. Schmid-Burgk, T. Schmidt, V. Hornung, S.T. Cole, and A. Ablasser Mycobacterium tuberculosis differentially activates cGAS- and inflammasome-dependent intracellular immune responses through ESX-1 Cell Host Microbe 17 2015 799 810
60. R.O. Watson, S.L. Bell, D.A. MacDuff, J.M. Kimmey, E.J. Diner, J. Olivas, R.E. Vance, C.L. Stallings, H.W. Virgin, and J.S. Cox The cytosolic sensor cGAS detects Mycobacterium tuberculosis DNA to induce type I interferons and activate autophagy Cell Host Microbe 17 2015 811 819
61. 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
62. K. Yang, J. Wang, M. Wu, M. Li, Y. Wang, and X. Huang Mesenchymal stem cells detect and defend against gammaherpesvirus infection via the cGAS-STING pathway Sci. Rep. 5 2015 7820
63. M. Yoneyama, K. Onomoto, M. Jogi, T. Akaboshi, and T. Fujita Viral RNA detection by RIG-I-like receptors Curr. Opin. Immunol. 32 2015 48 53
64. Z. Zhang, B. Yuan, M. Bao, N. Lu, T. Kim, and Y.-J. Liu The helicase DDX41 senses intracellular DNA mediated by the adaptor STING in dendritic cells Nat. Immunol. 12 2011 959 965
65. X. Zhang, J. Wu, F. Du, H. Xu, L. Sun, Z. Chen, C.A. Brautigam, X. Zhang, and Z.J. Chen The cytosolic DNA sensor cGAS forms an oligomeric complex with DNA and undergoes switch-like conformational changes in the activation loop Cell Rep. 6 2014 421 430
66. F.X. Zhu, S.M. King, E.J. Smith, D.E. Levy, and Y. Yuan A Kaposi's sarcoma-associated herpesviral protein inhibits virus-mediated induction of type I interferon by blocking IRF-7 phosphorylation and nuclear accumulation Proc. Natl. Acad. Sci. USA 99 2002 5573 5578
67. F.X. Zhu, J.M. Chong, L. Wu, and Y. Yuan Virion proteins of Kaposi's sarcoma-associated herpesvirus J. Virol. 79 2005 800 811
68. F.X. Zhu, N. Sathish, and Y. Yuan Antagonism of host antiviral responses by Kaposi's sarcoma-associated herpesvirus tegument protein ORF45 PLoS ONE 5 2010 e10573
69. L. Zinzula, and E. Tramontano Strategies of highly pathogenic RNA viruses to block dsRNA detection by RIG-I-like receptors: hide, mask, hit Antiviral Res. 100 2013 615 635