A Temporal Gate for Viral Enhancers to Co-opt Toll-Like-Receptor Transcriptional Activation Pathways upon Acute Infection
Here we discover how inflammatory signalling may unintentionally promote infection, as a result of viruses evolving DNA sequences, known as enhancers, which act as a bait to prey on the infected cell transcription factors induced by inflammation. The major inflammatory transcription factors activated are part of the TLR-signalling pathway. We find the prototypical viral enhancer of cytomegalovirus can be paradoxically boosted by activation of inflammatory “anti-viral” TLR-signalling independent of viral structural proteins. This leads to an increase in viral gene expression and replication in cell-culture and upon infection of mice. We identify an axis of inflammatory transcription factors, acting downstream of TLR-signalling but upstream of interferon inhibition. Mechanistically, the central TLR-adapter protein MyD88 is shown to play a critical role in promoting viral enhancer activity in the first 6h of infection. The co-option of TLR-signalling exceeds the usage of NFκB, and we identify IRF3 and 5 as newly found viral-enhancer interacting inflammatory transcription factors. Taken together this study reveals how virus enhancers, employ a path of least resistance by directly harnessing within a short temporal window, the activation of anti-viral signalling in macrophages to drive viral gene expression and replication to an extent that has not been recognised before.
Vyšlo v časopise:
A Temporal Gate for Viral Enhancers to Co-opt Toll-Like-Receptor Transcriptional Activation Pathways upon Acute Infection. PLoS Pathog 11(4): e32767. doi:10.1371/journal.ppat.1004737
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1004737
Souhrn
Here we discover how inflammatory signalling may unintentionally promote infection, as a result of viruses evolving DNA sequences, known as enhancers, which act as a bait to prey on the infected cell transcription factors induced by inflammation. The major inflammatory transcription factors activated are part of the TLR-signalling pathway. We find the prototypical viral enhancer of cytomegalovirus can be paradoxically boosted by activation of inflammatory “anti-viral” TLR-signalling independent of viral structural proteins. This leads to an increase in viral gene expression and replication in cell-culture and upon infection of mice. We identify an axis of inflammatory transcription factors, acting downstream of TLR-signalling but upstream of interferon inhibition. Mechanistically, the central TLR-adapter protein MyD88 is shown to play a critical role in promoting viral enhancer activity in the first 6h of infection. The co-option of TLR-signalling exceeds the usage of NFκB, and we identify IRF3 and 5 as newly found viral-enhancer interacting inflammatory transcription factors. Taken together this study reveals how virus enhancers, employ a path of least resistance by directly harnessing within a short temporal window, the activation of anti-viral signalling in macrophages to drive viral gene expression and replication to an extent that has not been recognised before.
Zdroje
. . Beutler B, Eidenschenk C, Crozat K, Imler JL, Takeuchi O, et al. (2007) Genetic analysis of resistance to viral infection. Nat Rev Immunol 7: 753–766. 17893693
2. Kumar H, Kawai T, Akira S (2011) Pathogen Recognition by the Innate Immune System. International Reviews of Immunology: Informa Clin Med. pp. 16–34.
3. Takeuchi O, Akira S (2010) Pattern recognition receptors and inflammation. Cell 140: 805–820. doi: 10.1016/j.cell.2010.01.022 20303872
4. Kawai T, Akira S (2006) TLR signaling. Cell Death Differ 13: 816–825. 16410796
5. Kawai T, Akira S (2006) Innate immune recognition of viral infection. Nat Immunol 7: 131–137. 16424890
6. Hoebe K, Du X, Georgel P, Janssen E, Tabeta K, et al. (2003) Identification of Lps2 as a key transducer of MyD88-independent TIR signalling. Nature 424: 743–748. 12872135
7. Honda K, Takaoka A, Taniguchi T (2006) Type I interferon [corrected] gene induction by the interferon regulatory factor family of transcription factors. Immunity 25: 349–360. 16979567
8. Takaoka A, Yanai H (2006) Interferon signalling network in innate defence. Cell Microbiol 8: 907–922. 16681834
9. Yurochko AD, Huang ES (1999) Human cytomegalovirus binding to human monocytes induces immunoregulatory gene expression. J Immunol 162: 4806–4816. 10202024
10. Takeuchi O, Akira S (2007) Recognition of viruses by innate immunity. Immunol Rev 220: 214–224. 17979849
11. Barbalat R, Lau L, Locksley RM, Barton GM (2009) Toll-like receptor 2 on inflammatory monocytes induces type I interferon in response to viral but not bacterial ligands. Nat Immunol 10: 1200–1207. doi: 10.1038/ni.1792 19801985
12. Compton T, Kurt-Jones EA, Boehme KW, Belko J, Latz E, et al. (2003) Human cytomegalovirus activates inflammatory cytokine responses via CD14 and Toll-like receptor 2. J Virol 77: 4588–4596. 12663765
13. Boehme KW, Guerrero M, Compton T (2006) Human cytomegalovirus envelope glycoproteins B and H are necessary for TLR2 activation in permissive cells. J Immunol 177: 7094–7102. 17082626
14. Leoni V, Gianni T, Salvioli S, Campadelli-Fiume G (2012) Herpes Simplex Virus Glycoproteins gH/gL and gB Bind Toll-Like Receptor 2, and Soluble gH/gL Is Sufficient To Activate NFκB. J Virol 86: 6555–6562. doi: 10.1128/JVI.00295-12 22496225
15. Tabeta K, Georgel P, Janssen E, Du X, Hoebe K, et al. (2004) Toll-like receptors 9 and 3 as essential components of innate immune defense against mouse cytomegalovirus infection. Proc Natl Acad Sci USA 101: 3516–3521. 14993594
16. Szomolanyi-Tsuda E, Liang X, Welsh RM, Kurt-Jones EA, Finberg RW (2006) Role for TLR2 in NK cell-mediated control of murine cytomegalovirus in vivo. J Virol 80: 4286–4291. 16611887
17. 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. doi: 10.1128/JVI.01748-09 19846511
18. Rathinam VA, Jiang Z, Waggoner SN, Sharma S, Cole LE, et al. (2010) The AIM2 inflammasome is essential for host defense against cytosolic bacteria and DNA viruses. Nat Immunol 11: 395–402. doi: 10.1038/ni.1864 20351692
19. Bresnahan WA, Shenk T (2000) A Subset of Viral Transcripts Packaged Within Human Cytomegalovirus Particles. Science. pp. 2373–2376. 10875924
20. Vandevenne P, Sadzot-Delvaux C, Piette J (2010) Innate immune response and viral interference strategies developed by human herpesviruses. Biochem Pharmacol 80: 1955–1972. doi: 10.1016/j.bcp.2010.07.001 20620129
21. Babic M, Krmpotic A, Jonjic S (2011) All is fair in virus-host interactions: NK cells and cytomegalovirus. Trends Mol Med 17: 677–685. doi: 10.1016/j.molmed.2011.07.003 21852192
22. Jackson SE, Mason GM, Wills MR (2011) Human cytomegalovirus immunity and immune evasion. Virus Res 157: 151–160. doi: 10.1016/j.virusres.2010.10.031 21056604
23. Lemmermann NA, Fink A, Podlech J, Ebert S, Wilhelmi V, et al. (2012) Murine cytomegalovirus immune evasion proteins operative in the MHC class I pathway of antigen processing and presentation: state of knowledge, revisions, and questions. Med Microbiol Immunol 201: 497–512. doi: 10.1007/s00430-012-0257-y 22961127
24. Browne EP, Shenk T (2003) Human cytomegalovirus UL83-coded pp65 virion protein inhibits antiviral gene expression in infected cells. Proc Natl Acad Sci U S A 100: 11439–11444. 12972646
25. Abate DA, Watanabe S, Mocarski ES (2004) Major Human Cytomegalovirus Structural Protein pp65 (ppUL83) Prevents Interferon Response Factor 3 Activation in the Interferon Response. J Virol 78: 10995–11006. 15452220
26. Taylor RT, Bresnahan WA (2005) Human cytomegalovirus immediate-early 2 gene expression blocks virus-induced beta interferon production. J Virol 79: 3873–3877. 15731283
27. Taylor RT, Bresnahan WA (2006) Human cytomegalovirus immediate-early 2 protein IE86 blocks virus-induced chemokine expression. J Virol 80: 920–928. 16378994
28. Miller DM, Zhang Y, Rahill BM, Waldman WJ, Sedmak DD (1999) Human Cytomegalovirus Inhibits IFN-α-Stimulated Antiviral and Immunoregulatory Responses by Blocking Multiple Levels of IFN-α Signal Transduction. J Immunol 162: 6107–6113. 10229853
29. Mathers C, Schafer X, Martinez-Sobrido L, Munger J (2014) The Human Cytomegalovirus UL26 Protein Antagonizes NF-kappaB Activation. J Virol 88: 14289–14300. doi: 10.1128/JVI.02552-14 25275128
30. Le VT, Trilling M, Wilborn M, Hengel H, Zimmermann A (2008) Human cytomegalovirus interferes with signal transducer and activator of transcription (STAT) 2 protein stability and tyrosine phosphorylation. J Gen Virol 89: 2416–2426. doi: 10.1099/vir.0.2008/001669-0 18796709
31. Le VT, Trilling M, Zimmermann A, Hengel H (2008) Mouse cytomegalovirus inhibits beta interferon (IFN-beta) gene expression and controls activation pathways of the IFN-beta enhanceosome. J Gen Virol 89: 1131–1141. doi: 10.1099/vir.0.83538-0 18420790
32. Zimmermann A, Trilling M, Wagner M, Wilborn M, Bubic I, et al. (2005) A cytomegaloviral protein reveals a dual role for STAT2 in IFN-γ signaling and antiviral responses. J Ex Med 201: 1543–1553. 15883169
33. Doring M, Lessin I, Frenz T, Spanier J, Kessler A, et al. (2014) M27 expressed by cytomegalovirus counteracts effective type I interferon induction of myeloid cells but not of plasmacytoid dendritic cells. J Virol 88: 13638–13650. doi: 10.1128/JVI.00216-14 25231302
34. Fliss PM, Jowers TP, Brinkmann MM, Holstermann B, Mack C, et al. (2012) Viral mediated redirection of NEMO/IKKgamma to autophagosomes curtails the inflammatory cascade. PLoS Pathog 8: e1002517. doi: 10.1371/journal.ppat.1002517 22319449
35. Mack C, Sickmann A, Lembo D, Brune W (2008) Inhibition of proinflammatory and innate immune signaling pathways by a cytomegalovirus RIP1-interacting protein. Proc Natl Acad Sci U S A 105: 3094–3099. doi: 10.1073/pnas.0800168105 18287053
36. Krause E, de Graaf M, Fliss PM, Dolken L, Brune W (2014) Murine cytomegalovirus virion-associated protein M45 mediates rapid NF-kappaB activation after infection. J Virol 88: 9963–9975. doi: 10.1128/JVI.00684-14 24942588
37. Varnum SM, Streblow DN, Monroe ME, Smith P, Auberry KJ, et al. (2004) Identification of proteins in human cytomegalovirus (HCMV) particles: the HCMV proteome. J Virol 78: 10960–10966. 15452216
38. Angulo A, Messerle M, Koszinowski UH, Ghazal P (1998) Enhancer requirement for murine cytomegalovirus growth and genetic complementation by the human cytomegalovirus enhancer. J Virol 72: 8502–8509. 9765387
39. Ghazal P, Messerle M, Osborn K, Angulo A (2003) An essential role of the enhancer for murine cytomegalovirus in vivo growth and pathogenesis. J Virol 77: 3217–3228. 12584345
40. Meier JL, Stinski MF (2006) Major Immediate-Early Enhancer and its Geneproducts. In: Reddehase MJ, Lemmermann N, editors. Cytomegaloviruses: Molecular Biology and Immunity. 1 ed. Wymondham, Norfolk United Kingdom: Caister Academic Press. pp. 151–166.
41. Stinski MF, Isomura H (2008) Role of the cytomegalovirus major immediate early enhancer in acute infection and reactivation from latency. Med Microbiol Immunol 197: 223–231. 18097687
42. Podlech J, Pintea R, Kropp KA, Fink A, Lemmermann NAW, et al. (2010) Enhancerless Cytomegalovirus Is Capable of Establishing a Low-Level Maintenance Infection in Severely Immunodeficient Host Tissues but Fails in Exponential Growth. J Virol 84: 6254–6261. doi: 10.1128/JVI.00419-10 20375164
43. Boshart M, Weber F, Jahn G, Dorsch-Hasler K, Fleckenstein B, et al. (1985) A very strong enhancer is located upstream of an immediate early gene of human cytomegalovirus. Cell 41: 521–530. 2985280
44. Dorsch-Häsler K, Keil GM, Weber F, Jasin M, Schaffner W, et al. (1985) A long and complex enhancer activates transcription of the gene coding for the highly abundant immediate early mRNA in murine cytomegalovirus. Proc Natl Acad Sci USA. pp. 8325–8329. 3001696
45. Ghazal P, Lubon H, Fleckenstein B, Hennighausen L (1987) Binding of transcription factors and creation of a large nucleoprotein complex on the human cytomegalovirus enhancer. Proc Natl Acad Sci U S A 84: 3658–3662. 3035545
46. Lee Y, Sohn WJ, Kim DS, Kwon HJ (2004) NF-KB and c-Jun-dependent regulation of human cytomegalovirus immediate-early gene enhancer/promoter in response to lipopolysaccharide and bacterial CpG-oligodeoxynucleotides in macrophage cell line RAW 264.7. Eur J Biochem 271: 1094–1105. 15009188
47. Kropp KA, Angulo A, Ghazal P (2014) Viral enhancer mimicry of host innate-immune promoters. PLoS Pathog 10: e1003804. doi: 10.1371/journal.ppat.1003804 24516378
48. Iversen AC, Steinkjer B, Nilsen N, Bohnhorst J, Moen SH, et al. (2009) A proviral role for CpG in cytomegalovirus infection. J Immunol 182: 5672–5681. doi: 10.4049/jimmunol.0801268 19380814
49. Mocarski ES (2002) Virus self-improvement through inflammation: No pain, no gain. Proc Natl Acad Sci USA 99: 3362–3364. 11904398
50. Benedict CA, Angulo A, Patterson G, Ha SW, Huang H, et al. (2004) Neutrality of the canonical NF-kappa B-dependent pathway for human and murine cytomegalovirus transcription and replication in vitro. J Virol 78: 741–750. 14694106
51. Gustems M, Borst E, Benedict CA, Perez C, Messerle M, et al. (2006) Regulation of the transcription and replication cycle of human cytomegalovirus is insensitive to genetic elimination of the cognate NF-kappa B binding sites in the enhancer. J Virol 80: 9899–9904. 16973595
52. Verhaegen M, Christopoulos TK (2002) Recombinant Gaussia luciferase. Overexpression, purification, and analytical application of a bioluminescent reporter for DNA hybridization. Anal Chem 74: 4378–4385. 12236345
53. Wurdinger T, Badr C, Pike L, de Kleine R, Weissleder R, et al. (2008) A secreted luciferase for ex vivo monitoring of in vivo processes. Nat Methods 5: 171–173. doi: 10.1038/nmeth.1177 18204457
54. Lacaze P, Forster T, Ross A, Kerr LE, Salvo-Chirnside E, et al. (2011) Temporal profiling of the coding and noncoding murine cytomegalovirus transcriptomes. J Virol 85: 6065–6076. doi: 10.1128/JVI.02341-10 21471238
55. Busche A, Angulo A, Kay-Jackson P, Ghazal P, Messerle M (2008) Phenotypes of major immediate-early gene mutants of mouse cytomegalovirus. Med Microbiol Immunol 197: 233–240. doi: 10.1007/s00430-008-0076-3 18239940
56. Messerle M, Keil GM, Koszinowski UH (1991) Structure and expression of murine cytomegalovirus immediate-early gene 2. J Virol 65: 1638–1643. 1847480
57. Matsumoto M, Funami K, Tanabe M, Oshiumi H, Shingai M, et al. (2003) Subcellular localization of Toll-like receptor 3 in human dendritic cells. J Immunol 171: 3154–3162. 12960343
58. Paun A, Reinert JT, Jiang Z, Medin C, Balkhi MY, et al. (2008) Functional characterization of murine interferon regulatory factor 5 (IRF-5) and its role in the innate antiviral response. J Biol Chem 283: 14295–14308. doi: 10.1074/jbc.M800501200 18332133
59. Vercammen E, Staal J, Beyaert R (2008) Sensing of viral infection and activation of innate immunity by toll-like receptor 3. Clin Microbiol Rev 21: 13–25. doi: 10.1128/CMR.00022-07 18202435
60. Pohar J, Pirher N, Bencina M, Mancek-Keber M, Jerala R (2013) The role of UNC93B1 protein in surface localization of TLR3 receptor and in cell priming to nucleic acid agonists. J Biol Chem 288: 442–454. doi: 10.1074/jbc.M112.413922 23166319
61. Gribaudo G, Ravaglia S, Caliendo A, Cavallo R, Gariglio M, et al. (1993) Interferons inhibit onset of murine cytomegalovirus immediate-early gene transcription. Virology 197: 303–311. 8212566
62. Landolfo S, Gribaudo G, Angeretti A, Gariglio M (1995) Mechanisms of viral inhibition by interferons. Pharmacol Ther 65: 415–442. 7544016
63. Dag F, Dolken L, Holzki J, Drabig A, Weingartner A, et al. (2014) Reversible silencing of cytomegalovirus genomes by type I interferon governs virus latency. PLoS Pathog 10: e1003962. doi: 10.1371/journal.ppat.1003962 24586165
64. Kropp KA, Robertson KA, Sing G, Rodriguez-Martin S, Blanc M, et al. (2011) Reversible Inhibition of Murine Cytomegalovirus Replication by Gamma Interferon (IFN-γ) in Primary Macrophages Involves a Primed Type I IFN-Signaling Subnetwork for Full Establishment of an Immediate-Early Antiviral State. J Virol 85: 10286–10299. doi: 10.1128/JVI.00373-11 21775459
65. Mocarski ESJ, Shenk T, Pass RF (2007) Cytomegaloviruses. In: Knipe DM, Howley PM, editors. Fields Virology. 5 ed. Philadelphia: Lippincott Williams & Wilkins. pp. 2701–2772. 18002552
66. Chang YN, Crawford S, Stall J, Rawlins DR, Jeang KT, et al. (1990) The palindromic series I repeats in the simian cytomegalovirus major immediate-early promoter behave as both strong basal enhancers and cyclic AMP response elements. J Virol 64: 264–277. 2152815
67. Keller MJ, Wu AW, Andrews JI, McGonagill PW, Tibesar EE, et al. (2007) Reversal of human cytomegalovirus major immediate-early enhancer/promoter silencing in quiescently infected cells via the cyclic AMP signaling pathway. J Virol 81: 6669–6681. 17301150
68. Lashmit P, Wang SH, Li HM, Isomura H, Stinski MF (2009) The CREB Site in the Proximal Enhancer Is Critical for Cooperative Interaction with the Other Transcription Factor Binding Sites To Enhance Transcription of the Major Intermediate-Early Genes in Human Cytomegalovirus-Infected Cells. J Virol 83: 8893–8904. doi: 10.1128/JVI.02239-08 19553322
69. Isern E, Gustems M, Messerle M, Borst E, Ghazal P, et al. (2011) The Activator Protein 1 Binding Motifs within the Human Cytomegalovirus Major Immediate-Early Enhancer Are Functionally Redundant and Act in a Cooperative Manner with the NF-kappa B Sites during Acute Infection. J Virol 85: 1732–1746. doi: 10.1128/JVI.01713-10 21106746
70. Isomura H, Stinski MF, Kudoh A, Daikoku T, Shirata N, et al. (2005) Two Sp1/Sp3 binding sites in the major immediate-early proximal enhancer of human cytomegalovirus have a significant role in viral replication. J Virol 79: 9597–9607. 16014922
71. Franceschini A, Szklarczyk D, Frankild S, Kuhn M, Simonovic M, et al. (2013) STRING v9.1: protein-protein interaction networks, with increased coverage and integration. Nucleic Acids Res 41: D808–815. doi: 10.1093/nar/gks1094 23203871
72. Chan YJ, Chiou CJ, Huang Q, Hayward GS (1996) Synergistic interactions between overlapping binding sites for the serum response factor and ELK-1 proteins mediate both basal enhancement and phorbol ester responsiveness of primate cytomegalovirus major immediate-early promoters in monocyte and T-lymphocyte cell types. J Virol 70: 8590–8605. 8970984
73. Wright E, Bain M, Teague L, Murphy J, Sinclair J (2005) Ets-2 repressor factor recruits histone deacetylase to silence human cytomegalovirus immediate-early gene expression in non-permissive cells. J Gen Virol 86: 535–544. 15722512
74. Angulo A, Ghazal P (1995) Regulation of human cytomegalovirus by retinoic acid. Scandinavian journal of infectious diseases Supplementum 99: 113–115. 8668933
75. Angulo A, Suto C, Boehm MF, Heyman RA, Ghazal P (1995) Retinoid activation of retinoic acid receptors but not of retinoid X receptors promotes cellular differentiation and replication of human cytomegalovirus in embryonal cells. J Virol 69: 3831–3837. 7745731
76. Angulo A, Suto C, Heyman RA, Ghazal P (1996) Characterization of the sequences of the human cytomegalovirus enhancer that mediate differential regulation by natural and synthetic retinoids. Mol Endocrinol 10: 781–793. 8813719
77. Angulo A, Chandraratna RA, LeBlanc JF, Ghazal P (1998) Ligand induction of retinoic acid receptors alters an acute infection by murine cytomegalovirus. J Virol 72: 4589–4600. 9573222
78. Liu PT, Krutzik SR, Kim J, Modlin RL (2005) Cutting edge: all-trans retinoic acid down-regulates TLR2 expression and function. J Immunol 174: 2467–2470. 15728448
79. Bernardo AR, Cosgaya JM, Aranda A, Jimenez-Lara AM (2013) Synergy between RA and TLR3 promotes type I IFN-dependent apoptosis through upregulation of TRAIL pathway in breast cancer cells. Cell Death & Disease 4: e479.
80. Sussman F, de Lera AR (2005) Ligand recognition by RAR and RXR receptors: binding and selectivity. J Med Chem 48: 6212–6219. 16190748
81. Burger-Kentischer A, Abele IS, Finkelmeier D, Wiesmuller KH, Rupp S (2010) A new cell-based innate immune receptor assay for the examination of receptor activity, ligand specificity, signalling pathways and the detection of pyrogens. J Immunol Methods 358: 93–103. doi: 10.1016/j.jim.2010.03.020 20385141
82. Hiscott J (2007) Triggering the innate antiviral response through IRF-3 activation. J Biol Chem 282: 15325–15329. 17395583
83. Honda K, Yanai H, Takaoka A, Taniguchi T (2005) Regulation of the type I IFN induction: a current view. Int Immunol 17: 1367–1378. 16214811
84. Kamijo R, Harada H, Matsuyama T, Bosland M, Gerecitano J, et al. (1994) Requirement for Transcription Factor Irf-1 in No Synthase Induction in Macrophages. Science 263: 1612–1615. 7510419
85. Barnes BJ, Moore PA, Pitha PM (2001) Virus-specific activation of a novel interferon regulatory factor, IRF-5, results in the induction of distinct interferon alpha genes. J Biol Chem 276: 23382–23390. 11303025
86. Bryne JC, Valen E, Tang MH, Marstrand T, Winther O, et al. (2008) JASPAR, the open access database of transcription factor-binding profiles: new content and tools in the 2008 update. Nucleic Acids Res 36: D102–106. 18006571
87. Takaoka A, Yanai H, Kondo S, Duncan G, Negishi H, et al. (2005) Integral role of IRF-5 in the gene induction programme activated by Toll-like receptors. Nature 434: 243–249. 15665823
88. Yasuda K, Richez C, Maciaszek JW, Agrawal N, Akira S, et al. (2007) Murine Dendritic Cell Type I IFN Production Induced by Human IgG-RNA Immune Complexes Is IFN Regulatory Factor (IRF)5 and IRF7 Dependent and Is Required for IL-6 Production. J Immunol 178: 6876–6885. 17513736
89. Barnes BJ, Richards J, Mancl M, Hanash S, Beretta L, et al. (2004) Global and distinct targets of IRF-5 and IRF-7 during innate response to viral infection. J Biol Chem 279: 45194–45207. 15308637
90. O'Neill LA, Golenbock D, Bowie AG (2013) The history of Toll-like receptors—redefining innate immunity. Nat Rev Immunol 13: 453–460. doi: 10.1038/nri3446 23681101
91. Amsler L, Verweij MC, DeFilippis VR (2013) The tiers and dimensions of evasion of the type I interferon response by human cytomegalovirus. J Mol Biol 425: 4857–4871. doi: 10.1016/j.jmb.2013.08.023 24013068
92. Boehme KW, Compton T (2006) Virus Entry and Activation of Innate Immunity. In: Reddehase MJ, Lemmermann N, editors. Cytomegaloviruses: Molecular Biology and Immunity. 1 ed. Norfolk, UK: Caister Academic Press. pp. 111–130.
93. Santoro MG, Rossi A, Amici C (2003) NF-kappaB and virus infection: who controls whom. EMBO J 22: 2552–2560. 12773372
94. Gringhuis SI, van der Vlist M, van den Berg LM, den Dunnen J, Litjens M, et al. (2010) HIV-1 exploits innate signaling by TLR8 and DC-SIGN for productive infection of dendritic cells. Nat Immunol 11: 419–426. doi: 10.1038/ni.1858 20364151
95. DeMeritt IB, Milford LE, Yurochko AD (2004) Activation of the NF-kappa B pathway in human cytomegalovirus-infected cells is necessary for efficient transactivation of the major immediate-early promoter. J Virol 78: 4498–4507. 15078930
96. DeMeritt IB, Podduturi JP, Tilley AM, Nogalski MT, Yurochko AD (2006) Prolonged activation of NF-kappaB by human cytomegalovirus promotes efficient viral replication and late gene expression. Virology 346: 15–31. 16303162
97. Caposio P, Luganini A, Bronzini M, Landolfo S, Gribaudo G (2010) The Elk-1 and Serum Response Factor Binding Sites in the Major Immediate-Early Promoter of Human Cytomegalovirus Are Required for Efficient Viral Replication in Quiescent Cells and Compensate for Inactivation of the NF-κB Sites in Proliferating Cells. J Virol 84: 4481–4493. doi: 10.1128/JVI.02141-09 20147408
98. Pevny LH, LovellBadge R (1997) Sox genes find their feet. Current Opinion in Genetics & Development 7: 338–344.
99. Jiang T, Hou CC, She ZY, Yang WX (2013) The SOX gene family: function and regulation in testis determination and male fertility maintenance. Mol Biol Rep 40: 2187–2194. doi: 10.1007/s11033-012-2279-3 23184044
100. Liu R, Baillie J, Sissons JGP, Sinclair JH (1994) The transcription factor YY1 binds to negative regulatory elements in the human cytomegalovirus major immediate early enhancer/promoter and mediates repression in nonpermissive cells. Nucleic Acids Research 22: 2453–2459. 8041605
101. Netterwald J, Yang S, Wang W, Ghanny S, Cody M, et al. (2005) Two gamma interferon-activated site-like elements in the human cytomegalovirus major immediate-early promoter/enhancer are important for viral replication. J Virol 79: 5035–5046. 15795289
102. de Martin R (1996) Synergistic Activation of Interleukin-8 Gene Transcription by All-trans-retinoic Acid and Tumor Necrosis Factor-alpha Involves the Transcription Factor NF-kappa B. J Biol Chem 271: 26954–26961. 8900181
103. Grossman A, Mittrucker HW, Nicholl J, Suzuki A, Chung S, et al. (1996) Cloning of human lymphocyte-specific interferon regulatory factor (hLSIRF/hIRF4) and mapping of the gene to 6p23-p25. Genomics 37: 229–233. 8921401
104. Kondo S, Schutte BC, Richardson RJ, Bjork BC, Knight AS, et al. (2002) Mutations in IRF6 cause Van der Woude and popliteal pterygium syndromes. Nat Genet 32: 285–289. 12219090
105. Xu WD, Pan HF, Xu Y, Ye DQ (2013) Interferon regulatory factor 5 and autoimmune lupus. Expert Rev Mol Med 15: e6. doi: 10.1017/erm.2013.7 23883595
106. Schoenemeyer A, Barnes BJ, Mancl ME, Latz E, Goutagny N, et al. (2005) The interferon regulatory factor, IRF5, is a central mediator of toll-like receptor 7 signaling. J Biol Chem 280: 17005–17012. 15695821
107. Kawai T, Akira S (2010) The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol 11: 373–384. doi: 10.1038/ni.1863 20404851
108. Akira S, Uematsu S, Takeuchi O (2006) Pathogen recognition and innate immunity. Cell 124: 783–801. 16497588
109. Barro M, Patton JT (2007) Rotavirus NSP1 inhibits expression of type I interferon by antagonizing the function of interferon regulatory factors IRF3, IRF5, and IRF7. J Virol 81: 4473–4481. 17301153
110. Martin HJ, Lee JM, Walls D, Hayward SD (2007) Manipulation of the toll-like receptor 7 signaling pathway by Epstein-Barr virus. J Virol 81: 9748–9758. 17609264
111. Arany I, Grattendick KJ, Whitehead WE, Ember IA, Tyring SK (2003) A functional interferon regulatory factor-1 (IRF-1)-binding site in the upstream regulatory region (URR) of human papillomavirus type 16. Virology 310: 280–286. 12781715
112. Alcantara FF, Tang H, McLachlan A (2002) Functional characterization of the interferon regulatory element in the enhancer 1 region of the hepatitis B virus genome. Nucleic Acids Res 30: 2068–2075. 11972347
113. Sgarbanti M, Remoli AL, Marsili G, Ridolfi B, Borsetti A, et al. (2008) IRF-1 is required for full NF-kappaB transcriptional activity at the human immunodeficiency virus type 1 long terminal repeat enhancer. J Virol 82: 3632–3641. doi: 10.1128/JVI.00599-07 18216101
114. Lazear HM, Lancaster A, Wilkins C, Suthar MS, Huang A, et al. (2013) IRF-3, IRF-5, and IRF-7 coordinately regulate the type I IFN response in myeloid dendritic cells downstream of MAVS signaling. PLoS Pathog 9: e1003118. doi: 10.1371/journal.ppat.1003118 23300459
115. Ramsey SA, Klemm SL, Zak DE, Kennedy KA, Thorsson V, et al. (2008) Uncovering a macrophage transcriptional program by integrating evidence from motif scanning and expression dynamics. PLoS Comput Biol 4: e1000021. doi: 10.1371/journal.pcbi.1000021 18369420
116. Suet Ting Tan R, Lin B, Liu Q, Tucker-Kellogg L, Ho B, et al. (2013) The synergy in cytokine production through MyD88-TRIF pathways is co-ordinated with ERK phosphorylation in macrophages. Immunol Cell Biol 91: 377–387. doi: 10.1038/icb.2013.13 23567895
117. Kobayashi K, Inohara N, Hernandez LD, Galan JE, Nunez G, et al. (2002) RICK/Rip2/CARDIAK mediates signalling for receptors of the innate and adaptive immune systems. Nature 416: 194–199. 11894098
118. Simmen KA, Singh J, Luukkonen BG, Lopper M, Bittner A, et al. (2001) Global modulation of cellular transcription by human cytomegalovirus is initiated by viral glycoprotein B. Proc Natl Acad Sci U S A 98: 7140–7145. 11390970
119. Boyle KA, Pietropaolo RL, Compton T (1999) Engagement of the cellular receptor for glycoprotein B of human cytomegalovirus activates the interferon-responsive pathway. Mol Cell Biol 19: 3607–3613. 10207084
120. Cai M, Li M, Wang K, Wang S, Lu Q, et al. (2013) The herpes simplex virus 1-encoded envelope glycoprotein B activates NF-kappaB through the Toll-like receptor 2 and MyD88/TRAF6-dependent signaling pathway. PLoS One 8: e54586. doi: 10.1371/journal.pone.0054586 23382920
121. Lemmermann NAW, Podlech J, Seckert CK, Kropp KA, Grzimek NKA, et al. (2010) CD8 T-Cell Immunotherapy of Cytomegalovirus Disease in the Murine Model. In: Stefan DKa, editor. Immunology of Infection. Volume 37 ed: Academic Press. pp. 369–420.
122. Adachi O, Kawai T, Takeda K, Matsumoto M, Tsutsui H, et al. (1998) Targeted disruption of the MyD88 gene results in loss of IL-1- and IL-18-mediated function. Immunity 9: 143–150. 9697844
123. Podlech J, Holtappels R, Grzimek NKA, Reddehase MJ (2002) Animal models: Murine cytomegalovirus. Method Microbiol 32: 493–525.
124. Wagner M, Jonjic S, Koszinowski UH, Messerle M (1999) Systematic excision of vector sequences from the BAC-cloned herpesvirus genome during virus reconstitution. J Virol 73: 7056–7060. 10400809
125. Angulo A, Ghazal P, Messerle M (2000) The major immediate-early gene ie3 of mouse cytomegalovirus is essential for viral growth. J Virol 74: 11129–11136. 11070009
126. Lee EC, Yu D, Martinez de Velasco J, Tessarollo L, Swing DA, et al. (2001) A highly efficient Escherichia coli-based chromosome engineering system adapted for recombinogenic targeting and subcloning of BAC DNA. Genomics 73: 56–65. 11352566
127. Messerle M, Crnkovic I, Hammerschmidt W, Ziegler H, Koszinowski UH (1997) Cloning and mutagenesis of a herpesvirus genome as an infectious bacterial artificial chromosome. Proc Natl Acad Sci USA 94: 14759–14763. 9405686
128. Heckman KL, Pease LR (2007) Gene splicing and mutagenesis by PCR-driven overlap extension. Nature protocols 2: 924–932. 17446874
129. Warming S, Costantino N (2005) Simple and highly efficient BAC recombineering using galK selection. Nucleic Acids Research 33: 1–12. 15640442
130. Lacaze PA (2011) Systems analysis of the dynamic macrophage response to productive and non-productive murine cytomegalovirus infection [Doctoral]. Edinburgh: University of Edinburgh.
131. Mahy BW, Kangro HO (1996) Virology methods manual: Academic Press London, UK.
132. Lembo D, Donalisio M, Hofer A, Cornaglia M, Brune W, et al. (2004) The Ribonucleotide Reductase R1 Homolog of Murine Cytomegalovirus Is Not a Functional Enzyme Subunit but Is Required for Pathogenesis. J Virol 78: 4278–4288. 15047841
133. Johnson DS, Mortazavi A, Myers RM, Wold B (2007) Genome-wide mapping of in vivo protein-DNA interactions. Science 316: 1497–1502. 17540862
134. Pradeepa MM, Sutherland HG, Ule J, Grimes GR, Bickmore WA (2012) Psip1/Ledgf p52 binds methylated histone H3K36 and splicing factors and contributes to the regulation of alternative splicing. PLoS Genet 8: e1002717. doi: 10.1371/journal.pgen.1002717 22615581
135. Carey MF, Peterson CL, Smale ST (2009) Chromatin immunoprecipitation (ChIP). Cold Spring Harb Protoc 2009: pdb prot5279. doi: 10.1101/pdb.prot5279 20147264
136. Simon CO, Kuhnapfel B, Reddehase MJ, Grzimek NKA (2007) Murine cytomegalovirus major immediate-early enhancer region operating as a genetic switch in bidirectional gene pair transcription. J Virol 81: 7805–7810. 17494084
137. Simon CO, Seckert CK, Dreis D, Reddehase MJ, Grzimek NK (2005) Role for tumor necrosis factor alpha in murine cytomegalovirus transcriptional reactivation in latently infected lungs. J Virol 79: 326–340. 15596827
138. Royston J (1982) An extension of Shapiro and Wilk's W test for normality to large samples. Applied Statistics 31: 115–124.
139. Grubbs FE (1950) Sample Criteria for Testing Outlying Observations. Ann Math Stat 21: 27–58.
140. Team RC (2014) R: A Language and Environment for Statistical Computing [Internet]. 2013.
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