Immune evasion by Epstein-Barr virus

Current Topics in Microbiology and Immunology

Volumn 391, Issue , 2015, Pages 355-381

  Ressing, Maaike E ^a,b   Gram, Anna M ^a,b   Hooykaas, Marjolein J G ^a   Piersma, Sytse J ^a   Wiertz, Emmanuel J H J ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

EPSTEIN BARR VIRUS ANTIGEN 1; EPSTEIN BARR VIRUS ANTIGEN 2; HLA ANTIGEN CLASS 1; HLA ANTIGEN CLASS 2; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON; INTERFERON REGULATORY FACTOR 3; INTERFERON REGULATORY FACTOR 7; LATENT MEMBRANE PROTEIN 1; MICRORNA; PATTERN RECOGNITION RECEPTOR; RETINOIC ACID INDUCIBLE PROTEIN I; SMALL UNTRANSLATED RNA; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 9; EPSTEIN BARR VIRUS ANTIGEN;

ADAPTIVE IMMUNITY; ANTIGEN PRESENTATION; B LYMPHOCYTE; BARF1 GENE; BCRF1 GENE; BGLF4 GENE; BGLF5 GENE; BILF1 GENE; BLLF3 GENE; BNLF2A GENE; BPLF1 GENE; BRLF1 GENE; BRLF4 GENE; BZLF1 GENE; BZLF2 GENE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DOWN REGULATION; EBNA1 GENE; EBNA2 GENE; ENZYME ACTIVITY; ENZYME INHIBITION; EPITHELIUM CELL; EPSTEIN BARR VIRUS; EPSTEIN BARR VIRUS INFECTION; GENE PRODUCT; HERPES SIMPLEX; HERPES SIMPLEX VIRUS 2; HUMAN; IMMUNE EVASION; IN VITRO STUDY; INNATE IMMUNITY; LMP1 GENE; LMP2A GENE; LMP2B GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; RNA DEGRADATION; SIGNAL TRANSDUCTION; VIRUS GENOME; VIRUS LATENCY; VIRUS REACTIVATION; VIRUS REPLICATION; ANIMAL; GENETICS; IMMUNOLOGY; VIROLOGY;

ANIMALS; EPSTEIN-BARR VIRUS INFECTIONS; EPSTEIN-BARR VIRUS NUCLEAR ANTIGENS; HERPESVIRUS 4, HUMAN; HUMANS; IMMUNE EVASION;

EID: 84943263100     PISSN: 0070217X     EISSN: 21969965     Source Type: Book Series    
DOI: 10.1007/978-3-319-22834-1_12     Document Type: Chapter

References (148)

1. Adamson AL, Kenney S (2001) Epstein-Barr virus immediate-early protein BZLF1 Is SUMO-1 modified and disrupts promyelocytic leukemia bodies. J Virol 75:2388-2399
2. Aman P, von Gabain A (1990) An Epstein-Barr virus immortalization associated gene segment interferes specifically with the IFN-induced anti-proliferative response in human B-lymphoid cell lines. The EMBO J 9:147-152
3. Ambrosio MR, Navari M, Di LL, Leon EA, Onnis A, Gazaneo S, Mundo L, Ulivieri C, Gomez G et al (2014).The Epstein Barr-encoded BART-6-3p microRNA affects regulation of cell growth and immuno response in Burkitt lymphoma. Infect Agent Cancer 9:12
4. Amoroso R, Fitzsimmons L, Thomas WA, Kelly GL, Rowe M, Bell AI (2011) Quantitative studies of Epstein-Barr virus-encoded microRNAs provide novel insights into their regulation. J Virol 85:996-1010
5. Ansari MA, Singh VV, Dutta S, Veettil MV, Dutta D, Chikoti L, Lu J, Everly D, Chandran B (2013) Constitutive interferon-inducible protein 16-Inflammasome activation during Epstein-Barr virus latency I, II, and III in B and epithelial cells. J Virol 87:8606-8623
6. Apcher S, Komarova A, Daskalogianni C, Yin Y, Malbert-Colas L, Fahraeus R (2009) mRNA translation regulation by the Gly-Ala repeat of Epstein-Barr virus nuclear antigen 1. J Virol 83:1289-1298
7. Ariza ME, Glaser R, Kaumaya PTP, Jones C, Williams MV (2009) The EBV-encoded dUTPase activates NF-kB through the TLR2 and MyD88-dependent signaling pathway. J Immunol 182:851-859
8. Ariza ME, Rivailler P, Glaser R, Chen M, Williams MV (2013) Epstein-Barr virus encoded dUTPase containing exosomes modulate innate and adaptive immune responses in human dendritic cells and peripheral blood mononuclear cells. PLoS ONE 8:e69827
9. Azzi T, Lunemann A, Murer A, Ueda S, Béziat V, Malmberg KJ, Staubli G, Gysin C, Berger C et al (2014) Role for early-differentiated natural killer cells in infectious mononucleosis. Blood 124:2533-2543
10. Bentz GL, Liu R, Hahn AM, Shackelford J, Pagano JS (2010) Epstein-Barr virus BRLF1 inhibits transcription of IRF3 and IRF7 and suppresses induction of interferon-ß. Virology 402:121-128
11. Blake N, Lee S, Redchenko I, Thomas W, Steven N, Leese A, Steigerwald-Mullen P, Kurilla MG, Frappier L et al (1997) Human CD8+ T Cell responses to EBV EBNA1: HLA class I presentation of the (Gly-Ala)-containing protein requires exogenous processing. Immunity 7:791-802
12. Bristol JA, Robinson AR, Barlow EA, Kenney SC (2010) The Epstein-Barr virus BZLF1 protein inhibits tumor necrosis factor receptor 1 expression through effects on cellular C/EBP proteins. J Virol 84:12362-12374
13. Brooks DG, Trifilo MJ, Edelmann KH, Teyton L, McGavern DB, Oldstone MBA (2006) Interleukin-10 determines viral clearance or persistence in vivo. Nat Med 12:1301-1309
14. Cahir-McFarland ED, Davidson DM, Schauer SL, Duong J, Kieff E (2000) NF-kB inhibition causes spontaneous apoptosis in Epstein-Barr virus-transformed lymphoblastoid cells. Proc Natl Acad Sci 97:6055-6060
15. Cai X, Schafer A, Lu S, Bilello JP, Desrosiers RC, Edwards R, Raab-Traub N, Cullen BR (2006) Epstein-Barr virus microRNAs are evolutionarily conserved and differentially expressed. PLoS Pathog 2:e23
16. Cayrol C, Flemington EK (1995) Identification of cellular target genes of the Epstein-Barr virus transactivator Zta: activation of transforming growth factor beta igh3 (TGF-beta igh3) and TGF-beta 1. J Virol 69:4206-4212
17. + regulates cytotoxic functions of NK and CD8 T cells in chronic EBV infection through NKG2D. Science 341:186-191
18. Chang LS, Wang JT, Doong SL, Lee CP, Chang CW, Tsai CH, Yeh SW, Hsieh CY, Chen MR (2012) Epstein-Barr virus BGLF4 kinase downregulates NF-kB transactivation through phosphorylation of coactivator UXT. J Virol 86:12176-12186
19. Chatterjee B, Leung CS, Münz C (2014) Animal models of Epstein Barr virus infection. J Immunol Methods 410:80-87
20. Chijioke O, Muller A, Feederle R, Barros M, Krieg C, Emmel V, Marcenaro E, Leung CS, Antsiferova O et al (2013) Human natural killer cells prevent infectious mononucleosis features by targeting lytic Epstein-Barr virus infection. Cell Rep 5:1489-1498
21. Chung BKT (2013) Innate immune control of EBV-infected B cells by invariant natural killer T cells. Blood 122:2600-2608
22. Clarke PA, Schwemmle M, Schickinger J, Hilse K, Clemens MJ (1991) Binding of Epstein-Barr virus small RNA EBER-1 to the double-stranded RNA-activated protein kinase DAI. Nucleic Acids Res 19:243-248
23. Cohen JI, Lekstrom K (1999) Epstein-Barr virus BARF1 protein is dispensable for B-cell transformation and inhibits alpha interferon secretion from mononuclear cells. J Virol 73:7627-7632
24. Croft NP, Shannon-Lowe C, Bell AI, Horst D, Kremmer E, Ressing ME, Wiertz EJHJ, Middeldorp JM, Rowe M et al (2009) Stage-specific inhibition of MHC class I presentation by the Epstein-Barr virus BNLF2a protein during virus lytic cycle. PLoS Pathog 5:e1000490
25. Deribe YL, Pawson T, Dikic I (2010) Post-translational modifications in signal integration. Nat Struct Mol Biol 17:666-672
26. Dolken L, Malterer G, Erhard F, Kothe S, Friedel CC, Suffert G, Marcinowski L, Motsch N, Barth S et al (2010) Systematic analysis of viral and cellular microRNA targets in cells latently infected with human gamma-herpesviruses by RISC immunoprecipitation assay. Cell Host Microbe 7:324-334
27. Dreyfus DH, Nagasawa M, Pratt JC, Kelleher CA, Gelfand EW (1999) Inactivation of NF-kB by EBV BZLF-1-encoded ZEBRA protein in human T cells. J Immunol 163:6261-6268
28. Dunmire SK, Odumade OA, Porter JL, Reyes-Genere J, Schmeling DO, Bilgic H, Fan D, Baechler EC, Balfour HH et al (2014) Primary EBV infection induces an expression profile distinct from other viruses but similar to hemophagocytic syndromes. PLoS One 9:e85422
29. Fathallah I, Parroche P, Gruffat H, Zannetti C, Johansson H, Yue J, Manet E, Tommasino M, Sylla BS et al (2010) EBV latent membrane protein 1 is a negative regulator of TLR9. J Immunol 185:6439-6447
30. Feederle R, Linnstaedt SD, Bannert H, Lips H, Bencun M, Cullen BR, Delecluse HJ (2011) A viral microRNA cluster strongly potentiates the transforming properties of a human herpesvirus. PLoS Pathog 7:e1001294
31. Gaudreault E, Fiola S, Olivier M, Gosselin J (2007) Epstein-Barr virus induces MCP-1 secretion by human monocytes via TLR2. J Virol 81:8016-8024
32. Geiger TR, Martin JM (2006) The Epstein-Barr virus-encoded LMP-1 oncoprotein negatively affects Tyk2 phosphorylation and interferon signaling in human B cells. J Virol 80:11638-11650
33. Gires O, Kohlhuber F, Kilger E, Baumann M, Kieser A, Kaiser C, Zeidler R, Scheffer B, Ueffing M et al (1999) Latent membrane protein 1 of Epstein-Barr virus interacts with JAK3 and activates STAT proteins. EMBO J 18:3064-3073
34. Glaser R, Litsky ML, Padgett DA, Baiocchi RA, Yang EV, Chen M, Yeh PE, Green-Church KB, Caligiuri MA et al (2006) EBV-encoded dUTPase induces immune dysregulation: implications for the pathophysiology of EBV-associated disease. Virology 346:205-218
35. Gottwein E, Corcoran DL, Mukherjee N, Skalsky RL, Hafner M, Nusbaum JD, Shamulailatpam P, Love CL, Dave SS et al (2011) Viral microRNA targetome of KSHV-infected primary effusion lymphoma cell lines. Cell Host Microbe 10:515-526
36. Griffin BD, Gram AM, Mulder A, van Leeuwen D, Claas FHJ, Wang F, Ressing ME, Wiertz E (2013) EBV BILF1 evolved to downregulate cell surface display of a wide range of HLA class I molecules through their cytoplasmic tail. J Immunol 190:1672-1684
37. Grundhoff A, Sullivan CS, Ganem D (2006) A combined computational and microarray-based approach identifies novel microRNAs encoded by human gamma-herpesviruses. RNA 12:733-750
38. Gutsch DE, Holley-Guthrie EA, Zhang Q, Stein B, Blanar MA, Baldwin AS, Kenney SC (1994) The bZIP transactivator of Epstein-Barr virus, BZLF1, functionally and physically interacts with the p65 subunit of NF-kappa B. Mol Cell Biol 14:1939-1948
39. Hahn AM, Huye LE, Ning S, Webster-Cyriaque J, Pagano JS (2005) Interferon regulatory factor 7 is negatively regulated by the Epstein-Barr virus immediate-early gene, BZLF-1. J Virol 79:10040-10052
40. Haneklaus M, Gerlic M, Kurowska-Stolarska M, Rainey AA, Pich D, McInnes IB, Hammerschmidt W, O'Neill LA, Masters SL (2012) Cutting edge: miR-223 and EBV miR-BART15 regulate the NLRP3 inflammasome and IL-1beta production. J Immunol 189:3795-3799
41. Hislop AD, Ressing ME, van Leeuwen D, Pudney VA, Horst D, Koppers-Lalic D, Croft NP, Neefjes JJ, Rickinson AB et al (2007) A CD8+ T cell immune evasion protein specific to Epstein-Barr virus and its close relatives in old world primates. J Exp Med 204:1863-1873
42. Ho HH, Ivashkiv LB (2006) Role of STAT3 in type I interferon responses: negative regulation of STAT1-dependent inflammatory gene activation. J Biol Chem 281:14111-14118
43. Hochberg D, Middeldorp JM, Catalina M, Sullivan JL, Luzuriaga K, Thorley-Lawson DA (2004) Demonstration of the Burkitt's lymphoma Epstein-Barr virus phenotype in dividing latently infected memory cells in vivo. Proc Natl Acad Sci 101:239-244
44. Horst D, van Leeuwen D, Croft NP, Garstka MA, Hislop AD, Kremmer E, Rickinson AB, Wiertz EJHJ, Ressing ME (2009) Specific targeting of the EBV lytic phase protein BNLF2a to the transporter associated with antigen processing results in impairment of HLA class I-restricted antigen presentation. J Immunol 182:2313-2324
45. Horst D, Favaloro V, Vilardi F, van Leeuwen HC, Garstka MA, Hislop AD, Rabu C, Kremmer E, Rickinson AB et al (2011) EBV protein BNLF2a exploits host tail-anchored protein integration machinery to inhibit TAP. J Immunol 186:3594-3605
46. Horst D, Burmeister WP, Boer IGJ, van Leeuwen D, Buisson M, Gorbalenya AE, Wiertz EJHJ, Ressing ME (2012) The bridge in the Epstein-Barr virus alkaline exonuclease protein BGLF5 contributes to shutoff activity during productive infection. J Virol 86:9175-9187
47. Huang WT, Lin CW (2014) EBV-encoded miR-BART20-5p and miR-BART8 inhibit the IFNgamma-STAT1 pathway associated with disease progression in nasal NK-cell lymphoma. Am J Pathol 184:1185-1197
48. Izumi KM, Kieff ED (1997) The Epstein-Barr virus oncogene product latent membrane protein 1 engages the tumor necrosis factor receptor-associated death domain protein to mediate B lymphocyte growth transformation and activate NF-kB. Proc Natl Acad Sci 94:12592-12597
49. Jochum S, Ruiss R, Moosmann A, Hammerschmidt W, Zeidler R (2012a) RNAs in Epstein-Barr virions control early steps of infection. Proc Natl Acad Sci USA 109:E1396-E1404
50. Jochum S, Moosmann A, Lang S, Hammerschmidt W, Zeidler R (2012b) The EBV immunoevasins vIL-10 and BNLF2a protect newly infected B cells from immune recognition and elimination. PLoS Pathog 8:e1002704
51. Johannsen E, Luftig M, Chase MR, Weicksel S, Cahir-McFarland E, Illanes D, Sarracino D, Kieff E (2004) Proteins of purified Epstein-Barr virus. Proc Natl Acad Sci USA 101:16286-16291
52. Kanda K, Decker T, Aman P, Wahlström M, von Gabain A, Kallin B (1992) The EBNA2-related resistance towards alpha interferon (IFN-alpha) in Burkitt's lymphoma cells effects induction of IFN-induced genes but not the activation of transcription factor ISGF-3. Mol Cell Biol 12:4930-4936
53. Kanda K, Kempkes B, Bornkamm GW, Gabain AV, Decker T (1999) The Epstein-Barr virus nuclear antigen 2 (EBNA2), a protein required for B lymphocyte immortalization, induces the synthesis of type I interferon in burkitts lymphoma cell lines. In: Biological chemistry, vol 380, p. 213
54. Keating S, Prince S, Jones M, Rowe M (2002) The lytic cycle of Epstein-Barr virus is associated with decreased expression of cell surface major histocompatibility complex class I and class II molecules. J Virol 76:8179-8188
55. Kieser A (2007) Signal transduction by the Epstein-Barr virus oncogene latent membrane protein 1 (LMP1). Sig Transduct 7:20-33
56. Komano J, Maruo S, Kurozumi K, Oda T, Takada K (1999) Oncogenic role of Epstein-Barr virus-encoded RNAs in Burkitt's lymphoma cell line Akata. J Virol 73:9827-9831
57. Kuzembayeva M, Chiu YF, Sugden B (2012) Comparing proteomics and RISC immunoprecipitations to identify targets of Epstein-Barr viral miRNAs. PLoS One 7:e47409
58. Lee SP, Brooks JM, Al-Jarrah H, Thomas WA, Haigh TA, Taylor GS, Humme S, Schepers A, Hammerschmidt W et al (2004) CD8 T cell recognition of endogenously expressed Epstein-Barr virus nuclear antigen 1. J Exp Med 199:1409-1420
59. Lerner MR, Andrews NC, Miller G, Steitz JA (1981) Two small RNAs encoded by Epstein-Barr virus and complexed with protein are precipitated by antibodies from patients with systemic lupus erythematosus. Proc Natl Acad Sci 78:805-809
60. Leslie E, Ning S, Kelliher M, Pagano JS (2007) Interferon regulatory factor 7 is activated by a viral oncoprotein through RIP-dependent ubiquitination. Mol Cell Biol 27:2910-2918
61. Levitskaya J, Coram M, Levitsky V, Imreh S, Steigerwald-Mullen PM, Klein G, Kurilla MG, Masucci MG (1995) Inhibition of antigen processing by the internal repeat region of the Epstein-Barr virus nuclear antigen-1. Nature 375:685-688
62. Levitskaya J, Sharipo A, Leonchiks A, Ciechanover A, Masucci MG (1997) Inhibition of ubiquitin/proteasome-dependent protein degradation by the Gly-Ala repeat domain of the Epstein-Barr virus nuclear antigen 1. Proc Natl Acad Sci 94:12616-12621
63. Lin TC, Liu TY, Hsu SM, Lin CW (2013) Epstein-Barr virus-encoded miR-BART20-5p inhibits T-bet translation with secondary suppression of p53 in invasive nasal NK/T-cell lymphoma. Am J Pathol 182:1865-1875
64. Mackay LK, Long HM, Brooks JM, Taylor GS, Leung CS, Chen A, Wang F, Rickinson AB (2009) T cell detection of a B-cell tropic virus infection: newly-synthesised versus mature viral proteins as antigen sources for CD4 and CD8 epitope display. PLoS Pathog 5:e1000699
65. Meckes DG Jr, Shair KH, Marquitz AR, Kung CP, Edwards RH, Raab-Traub N (2010) Human tumor virus utilizes exosomes for intercellular communication. Proc Natl Acad Sci USA 107:20370-20375
66. Michaud F, Coulombe F, Gaudreault E, Paquet-Bouchard C, Rola-Pleszczynski M, Gosselin J (2010) Epstein-Barr virus interferes with the amplification of IFNa secretion by activating suppressor of cytokine signaling 3 in primary human monocytes. PLoS One 5:e11908
67. Middeldorp JM, Pegtel DM (2008) Multiple roles of LMP1 in Epstein-Barr virus induced immune escape. Semin Cancer Biol 18:388-396
68. Mold C, Bradt BM, Nemerow GR, Cooper NR (1988) Epstein-Barr virus regulates activation and processing of the third component of complement. J Exp Med 168:949-969
69. Morrison TE, Kenney SC (2004) BZLF1, an Epstein-Barr virus immediate-early protein, induces p65 nuclear translocation while inhibiting p65 transcriptional function. Virology 328:219-232
70. Morrison TE, Mauser A, Wong A, Ting JPY, Kenney SC (2001) Inhibition of IFN-y signaling by an Epstein-Barr virus immediate-early protein. Immunity 15:787-799
71. Morrison TE, Mauser A, Klingelhutz A, Kenney SC (2004) Epstein-Barr virus immediate-early protein BZLF1 inhibits tumor necrosis factor alpha-induced signaling and apoptosis by downregulating tumor necrosis factor receptor 1. J Virol 78:544-549
72. Motsch N, Alles J, Imig J, Zhu J, Barth S, Reineke T, Tinguely M, Cogliatti S, Dueck A et al (2012) MicroRNA profiling of Epstein-Barr virus-associated NK/T-cell lymphomas by deep sequencing. PLoS One 7:e42193
73. Munz C (2014) Viral infections in mice with reconstituted human immune system components. Immunol Lett 161:118-124
74. Munz C, Bickham KL, Subklewe M, Tsang ML, Chahroudi A, Kurilla MG, Zhang D, O'Donnell M, Steinman RM (2000) Human CD4(+) T lymphocytes consistently respond to the latent Epstein-Barr virus nuclear antigen EBNA1. J Exp Med 191(10):1649-1660
75. Muromoto R, Ikeda O, Okabe K, Togi S, Kamitani S, Fujimuro M, Harada S, Oritani K, Matsuda T (2009) Epstein-Barr virus-derived EBNA2 regulates STAT3 activation. Biochem Biophys Res Commun 378:439-443
76. Murphy JA, Duerst RJ, Smith TJ, Morrison LA (2003) Herpes simplex virus type 2 virion host shutoff protein regulates alpha/beta interferon but not adaptive immune responses during primary infection in vivo. J Virol 77:9337-9345
77. Nachmani D, Stern-Ginossar N, Sarid R, Mandelboim O (2009) Diverse herpesvirus microRNAs target the stress-induced immune ligand MICB to escape recognition by natural killer cells. Cell Host Microbe 5:376-385
78. Najjar I, Baran-Marszak F, Le Clorennec C, Laguillier C, Schischmanoff O, Youlyouz-Marfak I, Schlee M, Bornkamm GW, Raphaël M et al (2005) Latent membrane protein 1 regulates STAT1 through NF-kB-dependent interferon secretion in Epstein-Barr virus-immortalized B cells. J Virol 79:4936-4943
79. Nanbo A, Inoue K, Adachi-Takasawa K, Takada K (2002) Epstein-Barr virus RNA confers resistance to interferon-alpha-induced apoptosis in Burkitt's lymphoma. EMBO J 21:954-965
80. Nanbo A, Yoshiyama H, Takada K (2005) Epstein-Barr virus-encoded poly(A)-RNA confers resistance to apoptosis mediated through Fas by blocking the PKR pathway in human epithelial intestine 407 cells. J Virol 79:12280-12285
81. Ning S, Campos AD, Darnay BG, Bentz GL, Pagano JS (2008) TRAF6 and the three C-terminal lysine sites on IRF7 are required for its ubiquitination-mediated activation by the tumor necrosis factor receptor family member latent membrane protein 1. Mol Cell Biol 28:6536-6546
82. Ohashi M, Fogg MH, Orlova N, Quink C, Wang F (2012) An Epstein-Barr virus encoded inhibitor of colony stimulating factor-1 signaling is an important determinant for acute and persistent EBV infection. PLoS Pathog 8:e1003095
83. Padgett DA, Hotchkiss AK, Pyter LM, Nelson RJ, Yang E, Yeh PE, Litsky M, Williams M, Glaser R (2004) Epstein-Barr virus-encoded dUTPase modulates immune function and induces sickness behavior in mice. J Med Virol 74:442-448
84. Pagès F, Galon J, Karaschuk G, Dudziak D, Camus M, Lazar V, Camilleri-Broet S, Lagorce-Pagès C, Lebel-Binay S et al (2004) Epstein-Barr virus nuclear antigen 2 induces interleukin-18 receptor expression in B cells. Blood 105:1632-1639
85. Pappworth IY, Wang EC, Rowe M (2007) The switch from latent to productive infection in Epstein-Barr virus-infected B cells is associated with sensitization to NK cell killing. J Virol 81:474-482
86. Pasieka TJ, Lu B, Crosby SD, Wylie KM, Morrison LA, Alexander DE, Menachery VD, Leib DA (2008) Herpes simplex virus virion host shutoff attenuates establishment of the Antiviral State. J Virol 82:5527-5535
87. Pasquier B, Yin L, Fondanèche MC, Relouzat F, Bloch-Queyrat C, Lambert N, Fischer A, de Saint-Basile G, Latour S (2005) Defective NKT cell development in mice and humans lacking the adapter SAP, the X-linked lymphoproliferative syndrome gene product. J Exp Med 201:695-701
88. Pegtel DM, Cosmopoulos K, Thorley-Lawson DA, van Eijndhoven MAJ, Hopmans ES, Lindenberg JL, de Gruijl TD, Würdinger T, Middeldorp JM (2010) Functional delivery of viral miRNAs via exosomes. Proc Natl Acad Sci USA 107:6328-6333
89. Petrara MR, Freguja R, Gianesin K, Zanchetta M, De Rossi A (2013) Epstein-Barr virus-driven lymphomagenesis in the context of human immunodeficiency virus type 1 infection. Front Microbiol 4
90. Pfeffer S, Zavolan M, Grasser FA, Chien M, Russo JJ, Ju J, John B, Enright AJ, Marks D et al (2004) Identification of virus-encoded micrornas. Science 304:734-736
91. Qiu J, Cosmopoulos K, Pegtel M, Hopmans E, Murray P, Middeldorp J, Shapiro M, Thorley-Lawson DA (2011) A novel persistence associated EBV miRNA expression profile is disrupted in neoplasia. PLoS Pathog 7:e1002193
92. Qiu J, Smith P, Leahy L, Thorley-Lawson DA (2015) The Epstein-Barr virus encoded bart mirnas potentiate tumor growth in vivo. PLoS Pathog 11:e1004561
93. Quinn LL, Zuo J, Abbott RJM, Shannon-Lowe C, Tierney RJ, Hislop AD, Rowe M (2014) Cooperation between Epstein-Barr virus immune evasion proteins spreads protection from CD8+ T cell recognition across all three phases of the Lytic cycle. PLoS Pathog 10:e1004322
94. Rao P, Pham HT, Kulkarni A, Yang Y, Liu X, Knipe DM, Cresswell P, Yuan W (2011) Herpes simplex virus 1 glycoprotein B and US3 collaborate to inhibit CD1d antigen presentation and NKT cell function. J Virol 85:8093-8104
95. Rathinam V, Fitzgerald K (2010) Inflammasomes and anti-viral immunity. J Clin Immunol 30:632-637
96. Ressing ME, van Leeuwen D, Verreck FA, Gomez R, Heemskerk B, Toebes M, Mullen MM, Jardetzky TS, Longnecker R et al (2003) Interference with T cell receptor-HLA-DR interactions by Epstein-Barr virus gp42 results in reduced T helper cell recognition. Proc Natl Acad Sci USA 100:11583-11588
97. Ressing ME, van Leeuwen D, Verreck FA, Keating S, Gomez R, Franken KL, Ottenhoff TH, Spriggs M, Schumacher TN et al (2005) Epstein-Barr virus gp42 is posttranslationally modified to produce soluble gp42 that mediates HLA class II immune evasion. J Virol 79:841-852
98. Ressing ME, Horst D, Griffin BD, Tellam J, Zuo J, Khanna R, Rowe M, Wiertz EJ (2008a) Epstein-Barr virus evasion of CD8(+) and CD4(+) T cell immunity via concerted actions of multiple gene products. Semin Cancer Biol 18:397-408
99. Ressing ME, Horst D, Griffin BD, Tellam J, Zuo J, Khanna R, Rowe M, Wiertz EJHJ (2008b) Epstein-Barr virus evasion of CD8+ and CD4+ T cell immunity via concerted actions of multiple gene products. Semin Cancer Biol 18:397-408
100. Richardson C, Fielding C, Rowe M, Brennan P (2003) Epstein-Barr virus regulates STAT1 through latent membrane protein 1. J Virol 77:4439-4443
101. Rigaud S, Fondaneche MC, Lambert N, Pasquier B, Mateo V, Soulas P, Galicier L, Le Deist F, Rieux-Laucat F et al (2006) XIAP deficiency in humans causes an X-linked lymphoproliferative syndrome. Nature 444:110-114
102. Riley KJ, Rabinowitz GS, Yario TA, Luna JM, Darnell RB, Steitz JA (2012) EBV and human microRNAs co-target oncogenic and apoptotic viral and human genes during latency. EMBO J 31:2207-2221
103. Rowe M, Glaunsinger B, van LD, Zuo J, Sweetman D, Ganem D, Middeldorp J, Wiertz EJ, Ressing ME (2007a) Host shutoff during productive Epstein-Barr virus infection is mediated by BGLF5 and may contribute to immune evasion. Proc Natl Acad Sci USA 104:3366-3371
104. Rowe M, Glaunsinger B, van LD, Zuo J, Sweetman D, Ganem D, Middeldorp J, Wiertz EJ, Ressing ME (2007b) Host shutoff during productive Epstein-Barr virus infection is mediated by BGLF5 and may contribute to immune evasion. Proc Natl Acad Sci USA 104:3366-3371
105. Ruf IK, Lackey KA, Warudkar S, Sample JT (2005) Protection from interferon-induced apoptosis by Epstein-Barr virus small RNAs is not mediated by inhibition of PKR. J Virol 79:14562-14569
106. Saffert RT, Kalejta RF (2008) Promyelocytic leukemia-nuclear body proteins: herpesvirus enemies, accomplices, or both? Future Virol 3:265-277
107. Saito S, Murata T, Kanda T, Isomura H, Narita Y, Sugimoto A, Kawashima D, Tsurumi T (2013) Epstein-Barr virus deubiquitinase downregulates TRAF6-mediated NF-kB signaling during productive replication. J Virol 87:4060-4070
108. Salek-Ardakani S, Arrand JR, Mackett M (2002) Epstein-Barr virus encoded interleukin-10 inhibits HLA-class I, ICAM-1, and B7 expression on human monocytes: implications for immune evasion by EBV. Virology 304:342-351
109. Sanchez DJ, Gumperz JE, Ganem D (2005) Regulation of CD1d expression and function by a herpesvirus infection. J Clin Invest 115:1369-1378
110. Seto E, Moosmann A, Gromminger S, Walz N, Grundhoff A, Hammerschmidt W (2010) Micro RNAs of Epstein-Barr virus promote cell cycle progression and prevent apoptosis of primary human B cells. PLoS Pathog 6:e1001063
111. Shah KM, Stewart SE, Wei W, Woodman CBJ, O'Neil JD, Dawson CW, Young LS (2009) The EBV-encoded latent membrane proteins, LMP2A and LMP2B, limit the actions of interferon by targeting interferon receptors for degradation. Oncogene 28:3903-3914
112. Sheridan V, Polychronopoulos L, Dutia BM, Ebrahimi B (2014) A shutoff and exonuclease mutant of murine gammaherpesvirus-68 yields infectious virus and causes RNA loss in type I interferon receptor knock-out cells. J Gen Virol 95(5):1135-1143
113. Skalsky RL, Corcoran DL, Gottwein E, Frank CL, Kang D, Hafner M, Nusbaum JD, Feederle R, Delecluse HJ et al (2012) The viral and cellular microRNA targetome in lymphoblastoid cell lines. PLoS Pathog 8:e1002484
114. Stevenson PG, Simas JP, Efstathiou S (2009) Immune control of mammalian gamma-herpesviruses: lessons from murid herpesvirus-4. J Gen Virol 90:2317-2330
115. Stewart S, Dawson CW, Takada K, Curnow J, Moody CA, Sixbey JW, Young LS (2004) Epstein-Barr virus-encoded LMP2A regulates viral and cellular gene expression by modulation of the NF-kB transcription factor pathway. Proc Natl Acad Sci USA 101:15730-15735
116. Strockbine LD, Cohen JI, Farrah T, Lyman SD, Wagener F, DuBose RF, Armitage RJ, Spriggs MK (1998) The Epstein-Barr virus BARF1 gene encodes a novel, soluble colony-stimulating factor-1 receptor. J Virol 72:4015-4021
117. Strowig T, Gurer C, Ploss A, Liu YF, Arrey F, Sashihara J, Koo G, Rice CM, Young JW et al (2009) Priming of protective T cell responses against virus-induced tumors in mice with human immune system components. J Exp Med 206:1423-1434
118. Swanson-Mungerson M, Bultema R, Longnecker R (2010) Epstein-Barr virus LMP2A imposes sensitivity to apoptosis. J Gen Virol 91:2197-2202
119. Takeuchi O, Akira S (2009) Innate immunity to virus infection. Immunol Rev 227:75-86
120. Tellam J, Connolly G, Green KJ, Miles JJ, Moss DJ, Burrows SR, Khanna R (2004) Endogenous presentation of CD8+ T cell epitopes from Epstein-Barr virus-encoded nuclear antigen 1. J Exp Med 199:1421-1431
121. Traggiai E, Chicha L, Mazzucchelli L, Bronz L, Piffaretti JC, Lanzavecchia A, Manz MG (2004) Development of a human adaptive immune system in cord blood cell-transplanted mice. Science 304:104-107
122. Ulbrecht M, Modrow S, Srivastava R, Peterson PA, Weiss EH (1998) Interaction of HLA-E with peptides and the peptide transporter in vitro: implications for its function in antigen presentation. J Immunol 160:4375-4385
123. Valentine R, Dawson C, Hu C, Shah K, Owen T, Date K, Maia S, Shao J, Arrand J et al (2010) Epstein-Barr virus-encoded EBNA1 inhibits the canonical NF-kappaB pathway in carcinoma cells by inhibiting IKK phosphorylation. Mol Cancer 9:1
124. van deVeerdonk FL, Wever PC, Hermans MHA, Fijnheer R, Joosten LAB, van der Meer JWM, Netea MG, Schneeberger PM (2012) IL-18 serum concentration is markedly elevated in acute EBV infection and can serve as a marker for disease severity. J Infect Dis 206:197-201
125. vanGent M, Griffin BD, Berkhoff EG, van Leeuwen D, Boer IGJ, Buisson M, Hartgers FC, Burmeister WP, Wiertz EJ et al (2011) EBV lytic-phase protein BGLF5 contributes to TLR9 downregulation during productive infection. J Immunol 186:1694-1702
126. vanGent M, Braem SGE, de Jong A, Delagic N, Peeters JGC, Boer IGJ, Moynagh PN, Kremmer E, Wiertz EJ et al (2014) Epstein-Barr virus large tegument protein BPLF1 contributes to innate immune evasion through interference with toll-like receptor signaling. PLoS Pathog 10:e1003960
127. vanGent M, Gram AM, Boer IGJ, Geerdink RJ, Lindenbergh MFS, Lebbink RJ, Wiertz EJ, Ressing ME (2015) Silencing the shutoff protein of Epstein-Barr virus in productively infected B cells points to (innate) targets for immune evasion. J Gen Virol 96(4):858-865
128. Vereide DT, Seto E, Chiu YF, Hayes M, Tagawa T, Grundhoff A, Hammerschmidt W, Sugden B (2014) Epstein-Barr virus maintains lymphomas via its miRNAs. Oncogene 33:1258-1264
129. Voo KS, Fu T, Wang HY, Tellam J, Heslop HE, Brenner MK, Rooney CM, Wang RF (2004) Evidence for the presentation of major histocompatibility complex class I-restricted Epstein-Barr virus nuclear antigen 1 peptides to CD8+ T lymphocytes. J Exp Med 199:459-470
130. Wahl A, Linnstaedt SD, Esoda C, Krisko JF, Martinez-Torres F, Delecluse HJ, Cullen BR, Garcia JV (2013) A cluster of virus-encoded microRNAs accelerates acute systemic Epstein-Barr virus infection but does not significantly enhance virus-induced oncogenesis in vivo. J Virol 87:5437-5446
131. Waldman WJ, Williams J, Lemeshow S, Binkley P, Guttridge D, Kiecolt-Glaser JK, Knight DA, Ladner KJ, Glaser R (2008) Epstein-Barr virus-encoded dUTPase enhances proinflammatory cytokine production by macrophages in contact with endothelial cells: Evidence for depression-induced atherosclerotic risk. Brain Behav Immun 22:215-223
132. Wang F (2013) Nonhuman primate models for Epstein-Barr virus infection. Curr Opin Virol 3:233-237
133. Wang JT, Doong SL, Teng SC, Lee CP, Tsai CH, Chen MR (2009) Epstein-Barr virus BGLF4 kinase suppresses the interferon regulatory factor 3 signaling pathway. J Virol 83:1856-1869
134. Wertz IE, Dixit VM (2010) Signaling to NF-kB: regulation by ubiquitination. Cold Spring Harb Perspect Biol 2:1-19
135. Wood VHJ, O'Neil JD, Wei W, Stewart SE, Dawson CW, Young LS (2007) Epstein-Barr virusencoded EBNA1 regulates cellular gene transcription and modulates the STAT1 and TGF[beta] signaling pathways. Oncogene 26:4135-4147
136. Wu L, Fossum E, Joo CH, Inn KS, Shin YC, Johannsen E, Hutt-Fletcher LM, Hass J, Jung JU (2009) Epstein-Barr virus LF2: an antagonist to type I interferon. J Virol 83:1140-1146
137. Xia T, O'Hara A, Araujo I, Barreto J, Carvalho E, Sapucaia JB, Ramos JC, Luz E, Pedroso C et al (2008) EBV microRNAs in primary lymphomas and targeting of CXCL-11 by ebvmir-BHRF1-3. Cancer Res 68:1436-1442
138. Xu D, Brumm K, Zhang L (2006) The latent membrane protein 1 of Epstein-Barr virus (EBV) primes EBV latency cells for type I interferon production. J Biol Chem 281:9163-9169
139. Yao XD, Rosenthal KL (2011) Herpes simplex virus type 2 virion host shutoff protein suppresses innate dsRNA antiviral pathways in human vaginal epithelial cells. J Gen Virol 92:1981-1993
140. Yin Y, Manoury B, Fahraeus R (2003) Self-inhibition of synthesis and antigen presentation by Epstein-Barr virus-encoded EBNA1. Science 5:1371-1374
141. Zhang L, Pagano JS (2000) Interferon regulatory factor 7 is induced by Epstein-Barr virus latent membrane protein 1. J Virol 74:1061-1068
142. Zhang L, Wu L, Hong K, Pagano JS (2001) Intracellular signaling molecules activated by Epstein-Barr virus for induction of interferon regulatory factor 7. J Virol 75:12393-12401
143. Zhang J, Das SC, Kotalik C, Pattnaik AK, Zhang L (2004) The latent membrane protein 1 of Epstein-Barr virus establishes an Antiviral State via induction of interferon-stimulated genes. J Biol Chem 279:46335-46342
144. Zhao Y, Xu D, Jiang Y, Zhang L (2010) Dual functions of interferon regulatory factors 7C in Epstein-Barr virus-mediated transformation of human B lymphocytes. PLoS One 5:e9459
145. Zhu JY, Pfuhl T, Motsch N, Barth S, Nicholls J, Grasser F, Meister G (2009) Identification of novel Epstein-Barr virus microRNA genes from nasopharyngeal carcinomas. J Virol 83:3333-3341
146. Zuo J, Thomas W, van Leeuwen D, Middeldorp JM, Wiertz EJHJ, Ressing ME, Rowe M (2008) The DNase of gammaherpesviruses impairs recognition by virus-specific CD8+ T cells through an additional host shutoff function. J Virol 82:2385-2393
147. Zuo J, Currin A, Griffin BD, Shannon-Lowe C, Thomas WA, Ressing ME, Wiertz EJHJ, Rowe M (2009) The Epstein-Barr virus G-protein-coupled receptor contributes to immune evasion by targeting MHC class I molecules for degradation. PLoS Pathog 5:e1000255
148. Zuo J, Thomas WA, Haigh TA, Fitzsimmons L, Long HM, Hislop AD, Taylor GS, Rowe M (2011) Epstein-Barr virus evades CD4+ T cell responses in lytic cycle through BZLF1-mediated downregulation of CD74 and the cooperation of vBcl-2. PLoS Pathog 7:e1002455