cGAS-STING signaling regulates initial innate control of cytomegalovirus infection

Journal of Virology

Volumn 90, Issue 17, 2016, Pages 7789-7797

  Lio, Chan Wang J ^a   McDonald, Bryan ^a   Takahashi, Mariko ^a   Dhanwani, Rekha ^a   Sharma, Nikita ^a   Huang, Jenny ^a   Pham, Elise ^a   Benedict, Chris A ^a   Sharma, Sonia ^a  

^a LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC GMP AMP SYNTHASE; INTERFERON; INTERFERON REGULATORY FACTOR 3; PROTEIN STING; REGULATOR PROTEIN; UNCLASSIFIED DRUG; IRF3 PROTEIN, HUMAN; MB21D1 PROTEIN, HUMAN; MEMBRANE PROTEIN; MPYS PROTEIN, HUMAN; NUCLEOTIDYLTRANSFERASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; CONTROLLED STUDY; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTION; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIMARY CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; SIGNAL TRANSDUCTION; VIRUS REPLICATION; ANIMAL; C57BL MOUSE; DISEASE MODEL; IMMUNOLOGY; INNATE IMMUNITY; METABOLISM; SECRETION (PROCESS); UMBILICAL VEIN ENDOTHELIAL CELL; VIROLOGY;

ANIMALS; CYTOMEGALOVIRUS INFECTIONS; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; IMMUNITY, INNATE; INTERFERON REGULATORY FACTOR-3; INTERFERON TYPE I; MEMBRANE PROTEINS; MICE, INBRED C57BL; NUCLEOTIDYLTRANSFERASES; SIGNAL TRANSDUCTION;

EID: 84983535114     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01040-16     Document Type: Article

References (47)

1. Cannon MJ, Schmid DS, Hyde TB. 2010. Review of cytomegalovirus seroprevalence and demographic characteristics associated with infection. Rev Med Virol 20:202-213. http://dx.doi.org/10.1002/rmv.655.
2. Brodin P, Jojic V, Gao T, Bhattacharya S, Angel CJ, Furman D, Shen-Orr S, Dekker CL, Swan GE, Butte AJ, Maecker HT, Davis MM. 2015. Variation in the human immune system is largely driven by nonheritable influences. Cell 160:37-47. http://dx.doi.org/10.1016/j.cell.2014.12.020.
3. Cobbs CS. 2013. Cytomegalovirus and brain tumor: epidemiology, biology and therapeutic aspects. Curr Opin Oncol 25:682-688. http://dx.doi .org/10.1097/CCO.0000000000000005.
4. Herbein G, Kumar A. 2014. The oncogenic potential of human cytomegalovirus and breast cancer. Front Oncol 4:230. http://dx.doi.org/10.3389/fonc.2014.00230.
5. Stern-Ginossar N, Weisburd B, Michalski A, Le VT, Hein MY, Huang SX, Ma M, Shen B, Qian SB, Hengel H, Mann M, Ingolia NT, Weissman JS. 2012. Decoding human cytomegalovirus. Science 338:1088-1093. http://dx.doi.org/10.1126/science.1227919.
6. Rawlinson WD, Farrell HE, Barrell BG. 1996. Analysis of the complete DNA sequence of murine cytomegalovirus. J Virol 70:8833-8849.
7. Schneider K, Loewendorf A, De Trez C, Fulton J, Rhode A, Shumway H, Ha S, Patterson G, Pfeffer K, Nedospasov SA, Ware CF, Benedict CA. 2008. Lymphotoxin-mediated crosstalk between B cells and splenic stroma promotes the initial type I interferon response to cytomegalovirus. Cell Host Microbe 3:67-76. http://dx.doi.org/10.1016/j.chom.2007.12.008.
8. Verma S, Wang Q, Chodaczek G, Benedict CA. 2013. Lymphoid-tissue stromal cells coordinate innate defense to cytomegalovirus. J Virol 87:6201-6210. http://dx.doi.org/10.1128/JVI.00113-13.
9. Krug A, French AR, Barchet W, Fischer JA, Dzionek A, Pingel JT, Orihuela MM, Akira S, Yokoyama WM, Colonna M. 2004. TLR9-dependent recognition of MCMV by IPC and DC generates coordinated cytokine responses that activate antiviral NK cell function. Immunity 21:107-119. http://dx.doi.org/10.1016/j.immuni.2004.06.007.
10. Dalod M, Salazar-Mather TP, Malmgaard L, Lewis C, Asselin-Paturel C, Brière F, Trinchieri G, Biron CA. 2002. Interferon α/β and interleukin 12 responses to viral infections: pathways regulating dendritic cell cytokine expression in vivo. J Exp Med 195:517-528. http://dx.doi.org/10.1084/jem .20011672.
11. Verma S, Benedict CA. 2011. Sources and signals regulating type I interferon production: lessons learned from cytomegalovirus. J Interferon Cytokine Res 31:211-218. http://dx.doi.org/10.1089/jir.2010.0118.
12. Swiecki M, Gilfillan S, Vermi W, Wang Y, Colonna M. 2010. Plasmacytoid dendritic cell ablation impacts early interferon responses and antiviral NK and CD8(+) T cell accrual. Immunity 33:955-966. http://dx.doi .org/10.1016/j.immuni.2010.11.020.
13. Benedict CA, Banks TA, Senderowicz L, Ko M, Britt WJ, Angulo A, Ghazal P, Ware CF. 2001. Lymphotoxins and cytomegalovirus cooperatively induce interferon-b, establishing host-virus détente. Immunity 15:617-626. http://dx.doi.org/10.1016/S1074-7613(01)00222-9.
14. Banks TA, Rickert S, Benedict CA, Ma L, Ko M, Meier J, Ha W, Schneider K, Granger SW, Turovskaya O, Elewaut D, Otero D, French AR, Henry SC, Hamilton JD, Scheu S, Pfeffer K, Ware CF. 2005. A lymphotoxin-IFN-beta axis essential for lymphocyte survival revealed during cytomegalovirus infection. J Immunol 174:7217-7225. http://dx .doi.org/10.4049/jimmunol.174.11.7217.
15. DeFilippis VR, Alvarado D, Sali T, Rothenburg S, Fruh K. 2010. Human cytomegalovirus induces the interferon response via the DNA sensor ZBP1. J Virol 84:585-598. http://dx.doi.org/10.1128/JVI.01748-09.
16. Li T, Chen J, Cristea IM. 2013. Human cytomegalovirus tegument protein pUL83 inhibits IFI16-mediated DNA sensing for immune evasion. Cell Host Microbe 14:591-599. http://dx.doi.org/10.1016/j.chom.2013.10.007.
17. Dell'Oste V, Gatti D, Gugliesi F, De Andrea M, Bawadekar M, Lo Cigno I, Biolatti M, Vallino M, Marschall M, Gariglio M, Landolfo S. 2014. Innate nuclear sensor IFI16 translocates into the cytoplasm during the early stage of in vitro human cytomegalovirus infection and is entrapped in the egressing virions during the late stage. J Virol 88:6970-6982. http://dx.doi.org/10.1128/JVI.00384-14.
18. Gariano GR, Dell'Oste V, Bronzini M, Gatti D, Luganini A, De Andrea M, Gribaudo G, Gariglio M, Landolfo S. 2012. The intracellular DNA sensor IFI16 gene acts as restriction factor for human cytomegalovirus replication. PLoS Pathog 8:e1002498. http://dx.doi.org/10.1371/journal .ppat.1002498.
19. Ishikawa H, Ma Z, Barber GN. 2009. STING regulates intracellular DNA-mediated, type I interferon-dependent innate immunity. Nature 461:788-792. http://dx.doi.org/10.1038/nature08476.
20. Orzalli MH, Knipe DM. 2014. Cellular sensing of viral DNA and viral evasion mechanisms. Annu Rev Microbiol 68:477-492. http://dx.doi.org /10.1146/annurev-micro-091313-103409.
21. Sharma S, tenOever BR, Grandvaux N, Zhou GP, Lin R, Hiscott J. 2003. Triggering the interferon antiviral response through an IKK-related pathway. Science 300:1148-1151. http://dx.doi.org/10.1126/science.1081315.
22. Fitzgerald KA, McWhirter SM, Faia KL, Rowe DC, Latz E, Golenbock DT, Coyle AJ, Liao SM, Maniatis T. 2003. IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat Immunol 4:491-496. http://dx.doi.org/10.1038/ni921.
23. Maniatis T, Falvo JV, Kim TH, Kim TK, Lin CH, Parekh BS, Wathelet MG. 1998. Structure and function of the interferon-beta enhanceosome. Cold Spring Harb Symp Quant Biol 63:609-620. http://dx.doi.org/10.1101/sqb.1998.63.609.
24. Sauer JD, Sotelo-Troha K, von Moltke J, Monroe KM, Rae CS, Brubaker SW, Hyodo M, Hayakawa Y, Woodward JJ, Portnoy DA, Vance RE. 2011. The N-ethyl-N-nitrosourea-induced Goldenticket mouse mutant reveals an essential function of Sting in the in vivo interferon response to Listeria monocytogenes and cyclic dinucleotides. Infect Immun 79:688-694. http://dx.doi.org/10.1128/IAI.00999-10.
25. + entry. Nature 499:238-242. http://dx.doi.org/10.1038/nature12229.
26. Shalem O, Sanjana NE, Hartenian E, Shi X, Scott DA, Mikkelsen TS, Heckl D, Ebert BL, Root DE, Doench JG, Zhang F. 2014. Genome-scale CRISPR-Cas9 knockout screening in human cells. Science 343:84-87. http://dx.doi.org/10.1126/science.1247005.
27. Raftery MJ, Schwab M, Eibert SM, Samstag Y, Walczak H, Schonrich G. 2001. Targeting the function of mature dendritic cells by human cytomegalovirus:a multilayered viral defense strategy. Immunity 15:997-1009. http://dx.doi.org/10.1016/S1074-7613(01)00239-4.
28. Redwood AJ, Messerle M, Harvey NL, Hardy CM, Koszinowski UH, Lawson MA, Shellam GR. 2005. Use of a murine cytomegalovirus K181-derived bacterial artificial chromosome as a vaccine vector for immunocontraception. J Virol 79:2998-3008. http://dx.doi.org/10.1128/JVI.79.5.2998-3008.2005.
29. Jarvis MA, Nelson JA. 2002. Human cytomegalovirus persistence and latency in endothelial cells and macrophages. Curr Opin Microbiol 5:403-407. http://dx.doi.org/10.1016/S1369-5274(02)00334-X.
30. Li G, Kamil JP. 2016. Viral regulation of cell tropism in human cytomegalovirus. J Virol 90:626-629. http://dx.doi.org/10.1128/JVI.01500-15.
31. Compton T, Kurt-Jones EA, Boehme KW, Belko J, Latz E, Golenbock DT, Finberg RW. 2003. Human cytomegalovirus activates inflammatory cytokine responses via CD14 and Toll-like receptor 2. J Virol 77:4588-4596. http://dx.doi.org/10.1128/JVI.77.8.4588-4596.2003.
32. Juckem LK, Boehme KW, Feire AL, Compton T. 2008. Differential initiation of innate immune responses induced by human cytomegalovirus entry into fibroblast cells. J Immunol 180:4965-4977. http://dx.doi .org/10.4049/jimmunol.180.7.4965.
33. Horan KA, Hansen K, Jakobsen MR, Holm CK, Soby S, Unterholzner L, Thompson M, West JA, Iversen MB, Rasmussen SB, Ellermann-Eriksen S, Kurt-Jones E, Landolfo S, Damania B, Melchjorsen J, Bowie AG, Fitzgerald KA, Paludan SR. 2013. Proteasomal degradation of herpes simplex virus capsids in macrophages releases DNA to the cytosol for recognition byDNAsensors. J Immunol 190:2311-2319. http://dx.doi.org /10.4049/jimmunol.1202749.
34. Li XD, Wu J, Gao D, Wang H, Sun L, Chen ZJ. 2013. Pivotal roles of cGAS-cGAMP signaling in antiviral defense and immune adjuvant effects. Science 341:1390-1394. http://dx.doi.org/10.1126/science.1244040.
35. Paijo J, Doring M, Spanier J, Grabski E, Nooruzzaman M, Schmidt T, Witte G, Messerle M, Hornung V, Kaever V, Kalinke U. 2016. cGAS senses human cytomegalovirus and induces type I interferon responses in human monocyte-derived cells. PLoS Pathog 12:e1005546. http://dx.doi .org/10.1371/journal.ppat.1005546.
36. Haynes LD, Verma S, McDonald B, Wu R, Tacke R, Nowyhed HN, Ekstein J, Feuvrier A, Benedict CA, Hedrick CC. 2015. Cardif (MAVS) regulates the maturation ofNKcells. J Immunol 195:2157-2167. http://dx .doi.org/10.4049/jimmunol.1402060.
37. Wu J, Chen ZJ. 2014. Innate immune sensing and signaling of cytosolic nucleic acids. Annu Rev Immunol 32:461-488. http://dx.doi.org/10.1146/annurev-immunol-032713-120156.
38. Schoggins JW, MacDuff DA, Imanaka N, Gainey MD, Shrestha B, Eitson JL, Mar KB, Richardson RB, Ratushny AV, Litvak V, Dabelic R, Manicassamy B, Aitchison JD, Aderem A, Elliott RM, Garcia-Sastre A, Racaniello V, Snijder EJ, Yokoyama WM, Diamond MS, Virgin HW, Rice CM. 2014. Pan-viral specificity of IFN-induced genes reveals new roles for cGAS in innate immunity. Nature 505:691-695. http://dx.doi .org/10.1038/nature12862.
39. Lam E, Falck-Pedersen E. 2014. Unabated adenovirus replication following activation of the cGAS/STING-dependent antiviral response in human cells. J Virol 88:14426-14439. http://dx.doi.org/10.1128/JVI .02608-14.
40. Malhotra D, Fletcher AL, Turley SJ. 2013. Stromal and hematopoietic cells in secondary lymphoid organs: partners in immunity. Immunol Rev 251:160-176. http://dx.doi.org/10.1111/imr.12023.
41. Hsu KM, Pratt JR, Akers WJ, Achilefu SI, Yokoyama WM. 2009. Murine cytomegalovirus displays selective infection of cells within hours after systemic administration. J Gen Virol 90:33-43. http://dx.doi.org/10.1099/vir.0.006668-0.
42. Baptista AP, Roozendaal R, Reijmers RM, Koning JJ, Unger WW, Greuter M, Keuning ED, Molenaar R, Goverse G, Sneeboer MM, den Haan JM, Boes M, Mebius RE. 2014. Lymph node stromal cells constrain immunity viaMHCclass II self-antigen presentation. eLife 3:e04433. http://dx.doi.org/10.7554/eLife.04433.
43. Hiscott J, Grandvaux N, Sharma S, Tenoever BR, Servant MJ, Lin R. 2003. Convergence of the NF-kappaB and interferon signaling pathways in the regulation of antiviral defense and apoptosis. Ann N Y Acad Sci 1010:237-248. http://dx.doi.org/10.1196/annals.1299.042.
44. Sun C, Schattgen SA, Pisitkun P, Jorgensen JP, Hilterbrand AT, Wang LJ, West JA, Hansen K, Horan KA, Jakobsen MR, O'Hare P, Adler H, Sun R, Ploegh HL, Damania B, Upton JW, Fitzgerald KA, Paludan SR. 2015. Evasion of innate cytosolic DNA sensing by a gammaherpesvirus facilitates establishment of latent infection. J Immunol 194:1819-1831. http://dx.doi.org/10.4049/jimmunol.1402495.
45. Ablasser A, Schmid-Burgk JL, Hemmerling I, Horvath GL, Schmidt T, Latz E, Hornung V. 2013. Cell intrinsic immunity spreads to bystander cells via the intercellular transfer of cGAMP. Nature 503:530-534. http://dx.doi.org/10.1038/nature12640.
46. Gentili M, Kowal J, Tkach M, Satoh T, Lahaye X, Conrad C, Boyron M, Lombard B, Durand S, Kroemer G, Loew D, Dalod M, Thery C, Manel N. 2015. Transmission of innate immune signaling by packaging of cGAMP in viral particles. Science 349:1232-1236. http://dx.doi.org/10.1126/science.aab3628.
47. Bridgeman A, Maelfait J, Davenne T, Partridge T, Peng Y, Mayer A, Dong T, Kaever V, Borrow P, Rehwinkel J. 2015. Viruses transfer the antiviral second messenger cGAMP between cells. Science 349:1228-1232. http://dx.doi.org/10.1126/science.aab3632.