Innate immune recognition of EBV

Current Topics in Microbiology and Immunology

Volumn 391, Issue , 2015, Pages 265-287

  Lünemann, Anna ^a   Rowe, Martin ^b   Nadal, David ^a  

^a UNIVERSITY CHILDREN S HOSPITAL   (Switzerland)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EPSTEIN BARR VIRUS RNA; MICRORNA; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 10; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 6; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 9; UNCLASSIFIED DRUG; VIRUS RNA;

ANTIGEN RECOGNITION; B LYMPHOCYTE; BONE MARROW CELL; CELL CYCLE; DENDRITIC CELL; EPITHELIUM CELL; EPSTEIN BARR VIRUS; HUMAN; INNATE IMMUNITY; LIFE CYCLE STAGE; MACROPHAGE; MONOCYTE; NATURAL KILLER CELL; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TARGET CELL; VIRUS REPLICATION; VIRUS TRANSMISSION; ANIMAL; EPSTEIN BARR VIRUS INFECTION; GENETICS; IMMUNOLOGY; VIROLOGY;

ANIMALS; B-LYMPHOCYTES; DENDRITIC CELLS; EPSTEIN-BARR VIRUS INFECTIONS; HERPESVIRUS 4, HUMAN; HUMANS; IMMUNITY, INNATE; KILLER CELLS, NATURAL; MACROPHAGES;

EID: 84943244520     PISSN: 0070217X     EISSN: 21969965     Source Type: Book Series    
DOI: 10.1007/978-3-319-22834-1_9     Document Type: Chapter

References (103)

1. Ahmed W, Philip PS, Tariq S, Khan G (2014) Epstein-Barr virus-encoded small RNAs (EBERs) are present in fractions related to exosomes released by EBV-transformed cells. PLoS ONE 9(6):e99163. doi:10.1371/journal.pone.0099163, PONE-D-13-54217 [pii]
2. 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(15):8606-8623. doi:10.1128/JVI.00805-13, JVI.00805-13 [pii]
3. Ariza ME, Glaser R, Kaumaya PT, Jones C, Williams MV (2009) The EBV-encoded dUTPase activates NF-kappa B through the TLR2 and MyD88-dependent signaling pathway. J Immunol 182(2):851-859. doi:182/2/851 [pii]
4. 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(7):e69827. doi:10.1371/ journal.pone.0069827, PONE-D-13-19147 [pii]
5. Azzi T, Lunemann A, Murer A, Ueda S, Beziat V, Malmberg KJ, Staubli G, Gysin C, Berger C, Munz C, Chijioke O, Nadal D (2014) Role for early-differentiated natural killer cells in infectious mononucleosis. Blood 124(16):2533-2543. doi:10.1182/blood-2014-01-553024, blood-2014-01-553024 [pii]
6. Balfour HH Jr, Odumade OA, Schmeling DO, Mullan BD, Ed JA, Knight JA, Vezina HE, Thomas W, Hogquist KA (2013) Behavioral, virologic, and immunologic factors associated with acquisition and severity of primary Epstein-Barr virus infection in university students. J Infect Dis 207(1):80-88. doi:10.1093/infdis/jis646, jis646 [pii]
7. Bjorkstrom NK, Lindgren T, Stoltz M, Fauriat C, Braun M, Evander M, Michaelsson J, Malmberg KJ, Klingstrom J, Ahlm C, Ljunggren HG (2011) Rapid expansion and long-term persistence of elevated NK cell numbers in humans infected with hantavirus. J Exp Med 208(1):13-21. doi:10.1084/jem.20100762, jem.20100762 [pii]
8. Callegari S, Gastaldello S, Faridani OR, Masucci MG (2014) Epstein-Barr virus encoded micro-RNAs target SUMO-regulated cellular functions. FEBS J 281(21):4935-4950. doi:10.1111 /febs.13040
9. Carrega P, Ferlazzo G (2012) Natural killer cell distribution and trafficking in human tissues. Front Immunol 3:347. doi:10.3389/fimmu.2012.00347
10. Chen LC, Wang LJ, Tsang NM, Ojcius DM, Chen CC, Ouyang CN, Hsueh C, Liang Y, Chang KP, Chang YS (2012) Tumour inflammasome-derived IL-1beta recruits neutrophils and improves local recurrence-free survival in EBV-induced nasopharyngeal carcinoma. EMBO Mol Med 4(12):1276-1293. doi:10.1002/emmm.201201569
11. Chijioke O, Muller A, Feederle R, Barros MH, Krieg C, Emmel V, Marcenaro E, Leung CS, Antsiferova O, Landtwing V, Bossart W, Moretta A, Hassan R, Boyman O, Niedobitek G, Delecluse HJ, Capaul R, Munz C (2013) Human natural killer cells prevent infectious mononucleosis features by targeting lytic Epstein-Barr virus infection. Cell Rep 5(6):1489-1498. doi:10.1016/j.celrep.2013.11.041, S2211-1247(13)00725-0 [pii]
12. Cooper MA, Elliott JM, Keyel PA, Yang L, Carrero JA, Yokoyama WM (2009) Cytokine-induced memory-like natural killer cells. Proc Natl Acad Sci USA 106(6):1915-1919. doi:10.1073/p nas.0813192106, 0813192106 [pii]
13. Dorner M, Brandt S, Tinguely M, Zucol F, Bourquin JP, Zauner L, Berger C, Bernasconi M, Speck RF, Nadal D (2009) Plasma cell toll-like receptor (TLR) expression differs from that of B cells, and plasma cell TLR triggering enhances immunoglobulin production. Immunology 128(4):573-579
14. Drescher B, Bai F (2013) Neutrophil in viral infections, friend or foe? Virus Res 171(1):1-7. doi:10.1016/j.virusres.2012.11.002, S0168-1702(12)00447-9 [pii]
15. Dukers DF, Meij P, Vervoort MB, Vos W, Scheper RJ, Meijer CJ, Bloemena E, Middeldorp JM (2000) Direct immunosuppressive effects of EBV-encoded latent membrane protein 1. J Immunol 165(2):663-670. doi:ji_v165n2p663 [pii]
16. Fathallah I, Parroche P, Gruffat H, Zannetti C, Johansson H, Yue J, Manet E, Tommasino M, Sylla BS, Hasan UA (2010) EBV latent membrane protein 1 is a negative regulator of TLR9. J Immunol 185(11):6439-6447. doi:10.4049/jimmunol.0903459, jimmunol.0903459 [pii]
17. Fiola S, Gosselin D, Takada K, Gosselin J (2010) TLR9 contributes to the recognition of EBV by primary monocytes and plasmacytoid dendritic cells. J Immunol 185(6):3620-3631. doi:10. 4049/jimmunol.0903736, jimmunol.0903736 [pii]
18. Flanagan J, Middeldorp J, Sculley T (2003) Localization of the Epstein-Barr virus protein LMP 1 to exosomes. J Gen Virol 84(Pt 7):1871-1879
19. Freud AG, Yu J, Caligiuri MA (2014) Human natural killer cell development in secondary lymphoid tissues. Semin Immunol 26(2):132-137. doi:10.1016/j.smim.2014.02.008, S1044-5323(14)00021-9 [pii]
20. Fujimura Y (2000) Evidence of M cells as portals of entry for antigens in the nasopharyngeal lymphoid tissue of humans. Virchows Arch 436(6):560-566
21. Gandhi MK, Moll G, Smith C, Dua U, Lambley E, Ramuz O, Gill D, Marlton P, Seymour JF, Khanna R (2007) Galectin-1 mediated suppression of Epstein-Barr virus specific T-cell immunity in classic Hodgkin lymphoma. Blood 110(4):1326-1329. doi:10.1182/blood-2007-01-066100, blood-2007-01-066100 [pii]
22. Gasteiger G, Rudensky AY (2014) Interactions between innate and adaptive lymphocytes. Nat Rev Immunol. doi:10.1038/nri3726, nri3726 [pii]
23. Gaudreault E, Fiola S, Olivier M, Gosselin J (2007) Epstein-Barr virus induces MCP-1 secretion by human monocytes via TLR2. J Virol 81(15):8016-8024. doi:10.1128/JVI.00403-07, JVI.00403-07 [pii]
24. Golden-Mason L, McMahan RH, Strong M, Reisdorph R, Mahaffey S, Palmer BE, Cheng L, Kulesza C, Hirashima M, Niki T, Rosen HR (2013) Galectin-9 functionally impairs natural killer cells in humans and mice. J Virol 87(9):4835-4845. doi:10.1128/JVI.01085-12, JVI.01085-12 [pii]
25. Gosselin J, Savard M, Tardif M, Flamand L, Borgeat P (2001) Epstein-Barr virus primes human polymorphonuclear leucocytes for the biosynthesis of leukotriene B4. Clin Exp Immunol 126(3):494-502. doi:1687 [pii]
26. Gottschalk S, Heslop HE, Rooney CM (2005) Adoptive immunotherapy for EBV-associated malignancies. Leuk Lymphoma 46(1):1-10. doi:10.1080/10428190400002202, X6NJBGGNJEVVJBYN [pii]
27. Guerreiro-Cacais AO, Li L, Donati D, Bejarano MT, Morgan A, Masucci MG, Hutt-Fletcher L, Levitsky V (2004) Capacity of Epstein-Barr virus to infect monocytes and inhibit their development into dendritic cells is affected by the cell type supporting virus replication. J Gen Virol 85(Pt 10):2767-2778
28. Haas F, Yamauchi K, Murat M, Bernasconi M, Yamanaka N, Speck RF, Nadal D (2014) Activation of NF-kappaB via endosomal Toll-like receptor 7 (TLR7) or TLR9 suppresses murine herpesvirus 68 reactivation. J Virol 88(17):10002-10012. doi:10.1128/JVI.01486-14
29. Hadinoto V, Shapiro M, Sun CC, Thorley-Lawson DA (2009) The dynamics of EBV shedding implicate a central role for epithelial cells in amplifying viral output. PLoS Pathog 5(7):e1000496. doi:10.1371/journal.ppat.1000496
30. 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(8):3795-3799. doi:10.4049/jimmunol.1200312, jimmunol.1200312 [pii]
31. Hoebe EK, Le Large TY, Tarbouriech N, Oosterhoff D, De Gruijl TD, Middeldorp JM, Greijer AE (2012) Epstein-Barr virus-encoded BARF1 protein is a decoy receptor for macrophage colony stimulating factor and interferes with macrophage differentiation and activation. Viral Immunol 25(6):461-470. doi:10.1089/vim.2012.0034
32. Hoebe EK, Le Large TY, Greijer AE, Middeldorp JM (2013) BamHI-A rightward frame 1, an Epstein-Barr virus-encoded oncogene and immune modulator. Rev Med Virol 23(6):367-383. doi:10.1002/rmv.1758
33. Horowitz A, Newman KC, Evans JH, Korbel DS, Davis DM, Riley EM (2010) Cross-talk between T cells and NK cells generates rapid effector responses to Plasmodium falciparuminfected erythrocytes. J Immunol 184(11):6043-6052. doi:10.4049/jimmunol.1000106, jimmunol. 1000106 [pii]
34. Imai S, Nishikawa J, Takada K (1998) Cell-to-cell contact as an efficient mode of Epstein-Barr virus infection of diverse human epithelial cells. J Virol 72(5):4371-4378
35. Ishii KJ, Koyama S, Nakagawa A, Coban C, Akira S (2008) Host innate immune receptors and beyond: making sense of microbial infections. Cell Host Microbe 3(6):352-363. doi:10.1016/j.chom.2008.05.003, S1931-3128(08)00151-0 [pii]
36. Iskra S, Kalla M, Delecluse HJ, Hammerschmidt W, Moosmann A (2010) Toll-like receptor agonists synergistically increase proliferation and activation of B cells by epstein-barr virus. J Virol 84(7):3612-3623. doi:10.1128/JVI.01400-09
37. Iwakiri D (2014) Epstein-Barr virus-encoded RNAs: key molecules in viral pathogenesis. Cancers (Basel) 6(3):1615-1630. doi:10.3390/cancers6031615, cancers6031615 [pii]
38. Iwakiri D, Zhou L, Samanta M, Matsumoto M, Ebihara T, Seya T, Imai S, Fujieda M, Kawa K, Takada K (2009) Epstein-Barr virus (EBV)-encoded small RNA is released from EBV-infected cells and activates signaling from Toll-like receptor 3. J Exp Med 206(10):2091-2099
39. Iwasaki A, Medzhitov R (2004) Toll-like receptor control of the adaptive immune responses. Nat Immunol 5(10):987-995. doi:10.1038/ni1112, ni1112 [pii]
40. Jacobs BL, Langland JO (1996) When two strands are better than one: the mediators and modulators of the cellular responses to double-stranded RNA. Virology 219(2):339-349. doi:10.1 006/viro.1996.0259, S0042-6822(96)90259-7 [pii]
41. Kalla M, Schmeinck A, Bergbauer M, Pich D, Hammerschmidt W (2010) AP-1 homolog BZLF1 of Epstein-Barr virus has two essential functions dependent on the epigenetic state of the viral genome. In: Proceedings of the National Academy of Sciences of the United States of America 107(2):850-855. doi:10.1073/pnas.0911948107
42. Keryer-Bibens C, Pioche-Durieu C, Villemant C, Souquere S, Nishi N, Hirashima M, Middeldorp J, Busson P (2006) Exosomes released by EBV-infected nasopharyngeal carcinoma cells convey the viral latent membrane protein 1 and the immunomodulatory protein galectin 9. BMC Cancer 6:283. doi:10.1186/1471-2407-6-283, 1471-2407-6-283 [pii]
43. Kieff E, Rickinson AB (2001) In: Knipe DM, Howley PM (eds) Fields Virology. Lippincott Williams and Wilkins, Philadelphia, pp 2511-2574
44. Kiessling R, Klein E, Pross H, Wigzell H (1975a) "Natural" killer cells in the mouse. II. Cytotoxic cells with specificity for mouse Moloney leukemia cells. Characteristics of the killer cell. Eur J Immunol 5(2):117-121. doi:10.1002/eji.1830050209
45. Kiessling R, Klein E, Wigzell H (1975b) "Natural" killer cells in the mouse. I. Cytotoxic cells with specificity for mouse Moloney leukemia cells. Specificity and distribution according to genotype. Eur J Immunol 5(2):112-117. doi:10.1002/eji.1830050208
46. Klibi J, Niki T, Riedel A, Pioche-Durieu C, Souquere S, Rubinstein E, Le Moulec S, Guigay J, Hirashima M, Guemira F, Adhikary D, Mautner J, Busson P (2009) Blood diffusion and Th1-suppressive effects of galectin-9-containing exosomes released by Epstein-Barr virusinfected nasopharyngeal carcinoma cells. Blood 113(9):1957-1966. doi:10.1182/blood-2008-02-142596, blood-2008-02-142596 [pii]
47. Klinke O, Feederle R, Delecluse HJ (2014) Genetics of Epstein-Barr virus microRNAs. Semin Cancer Biol 26:52-59. doi:10.1016/j.semcancer.2014.02.002, S1044-579X(14)00026-1 [pii]
48. Laichalk LL, Thorley-Lawson DA (2005) Terminal differentiation into plasma cells initiates the replicative cycle of Epstein-Barr virus in vivo. J Virol 79(2):1296-1307
49. Lange MJ, Lasiter JC, Misfeldt ML (2009) Toll-like receptors in tonsillar epithelial cells. Int J Pediatr Otorhinolaryngol 73(4):613-621. doi:10.1016/j.ijporl.2008.12.013
50. Lee SM, Kok KH, Jaume M, Cheung TK, Yip TF, Lai JC, Guan Y, Webster RG, Jin DY, Peiris JS (2014) Toll-like receptor 10 is involved in induction of innate immune responses to influenza virus infection. Proc Natl Acad Sci USA 111(10):3793-3798. doi:10.1073/p nas.1324266111, 1324266111 [pii]
51. 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 USA 78(2):805-809
52. Li L, Liu D, Hutt-Fletcher L, Morgan A, Masucci MG, Levitsky V (2002) Epstein-Barr virus inhibits the development of dendritic cells by promoting apoptosis of their monocyte precursors in the presence of granulocyte macrophage-colony-stimulating factor and interleukin-4. Blood 99(10):3725-3734
53. Lopez-Verges S, Milush JM, Schwartz BS, Pando MJ, Jarjoura J, York VA, Houchins JP, Miller S, Kang SM, Norris PJ, Nixon DF, Lanier LL (2011) Expansion of a unique CD57(+)NKG2Chi natural killer cell subset during acute human cytomegalovirus infection. Proc Natl Acad Sci USA 108(36):14725-14732. doi:10.1073/pnas.1110900108, 1110900108 [pii]
54. Lotz M, Tsoukas CD, Fong S, Carson DA, Vaughan JH (1985) Regulation of Epstein-Barr virus infection by recombinant interferons. Selected sensitivity to interferon-gamma. Eur J Immunol 15(5):520-525
55. Lünemann A, Lünemann JD, Munz C (2009) Regulatory NK cell functions in inflammation and autoimmunity. Mol Med. doi:10.2119/molmed.2009.00035
56. Lünemann A, Vanoaica LD, Azzi T, Nadal D, Münz C (2013) A distinct subpopulation of human NK cells restricts B cell transformation by EBV. J Immunol 191(10):4989-4995. doi:10.404 9/jimmunol.1301046
57. 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(18):9748-9758. doi:10.1128/JVI.01122-07, JVI.01122-07 [pii]
58. Merad M, Sathe P, Helft J, Miller J, Mortha A (2013) The dendritic cell lineage: ontogeny and function of dendritic cells and their subsets in the steady state and the inflamed setting. Annu Rev Immunol 31:563-604. doi:10.1146/annurev-immunol-020711-074950
59. Middeldorp JM, Pegtel DM (2008) Multiple roles of LMP1 in Epstein-Barr virus induced immune escape. Semin Cancer Biol 18(6):388-396. doi:10.1016/j.semcancer.2008.10.004, S1044-579X(08)00080-1 [pii]
60. Münz C (2014) Dendritic cells during Epstein Barr virus infection. Front Microbiol 5:308. doi: 10.3389/fmicb.2014.00308
61. Murphy KTP, Walport M, Janeway C (2012) Janeway's Immunobiology, 8th edn. Garland Science, New York
62. Nachmani D, Stern-Ginossar N, Sarid R, Mandelboim O (2009) Diverse herpesvirus micro-RNAs target the stress-induced immune ligand MICB to escape recognition by natural killer cells. Cell Host Microbe 5(4):376-385. doi:10.1016/j.chom.2009.03.003, S1931-3128(09)00094-8 [pii]
63. 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(5):954-965. doi:10.1093/emboj/21.5.954
64. O'Leary JG, Goodarzi M, Drayton DL, von Andrian UH (2006) T cell-and B cell-independent adaptive immunity mediated by natural killer cells. Nat Immunol 7(5):507-516. doi:10.1038/ni1332, ni1332 [pii]
65. 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(12):e1003095. doi:10.1371/journal.ppat.1003095, PPATHOGENS-D-12-02098 [pii]
66. Orange JS (2013) Natural killer cell deficiency. J Allergy Clin Immunol 132(3):515-525; quiz 526. doi:10.1016/j.jaci.2013.07.020, S0091-6749(13)01123-8 [pii]
67. 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(2):474-482. doi:10.1128/JVI.01777-06, JVI.01777-06 [pii]
68. Paust S, Gill HS, Wang BZ, Flynn MP, Moseman EA, Senman B, Szczepanik M, Telenti A, Askenase PW, Compans RW, von Andrian UH (2010) Critical role for the chemokine receptor CXCR6 in NK cell-mediated antigen-specific memory of haptens and viruses. Nat Immunol 11(12):1127-1135. doi:10.1038/ni.1953, ni.1953 [pii]
69. Pegtel DM, Cosmopoulos K, Thorley-Lawson DA, van Eijndhoven MA, Hopmans ES, Lindenberg JL, de Gruijl TD, Wurdinger T, Middeldorp JM (2010) Functional delivery of viral miRNAs via exosomes. Proc Natl Acad Sci USA 107(14):6328-6333. doi:10.1073/p nas.0914843107, 0914843107 [pii]
70. Petitdemange C, Becquart P, Wauquier N, Beziat V, Debre P, Leroy EM, Vieillard V (2011) Unconventional repertoire profile is imprinted during acute chikungunya infection for natural killer cells polarization toward cytotoxicity. PLoS Pathog 7(9):e1002268. doi:10.1371/ journal.ppat.1002268, PPATHOGENS-D-11-00590 [pii]
71. Qiu J, Thorley-Lawson DA (2014) EBV microRNA BART 18-5p targets MAP3K2 to facilitate persistence in vivo by inhibiting viral replication in B cells. Proc Natl Acad Sci USA 111(30):11157-11162. doi:10.1073/pnas.1406136111, 1406136111 [pii]
72. Quan TE, Roman RM, Rudenga BJ, Holers VM, Craft JE (2010) Epstein-Barr virus promotes interferon-alpha production by plasmacytoid dendritic cells. Arthritis Rheum 62(6):1693-1701. doi:10.1002/art.27408
73. Rickinson AB, Long HM, Palendira U, Munz C, Hislop AD (2014) Cellular immune controls over Epstein-Barr virus infection: new lessons from the clinic and the laboratory. Trends Immunol 35(4):159-169. doi:10.1016/j.it.2014.01.003, S1471-4906(14)00016-7 [pii]
74. Robbins PD, Morelli AE (2014) Regulation of immune responses by extracellular vesicles. Nat Rev Immunol 14(3):195-208. doi:10.1038/nri3622, nri3622 [pii]
75. Saitoh T, Komano J, Saitoh Y, Misawa T, Takahama M, Kozaki T, Uehata T, Iwasaki H, Omori H, Yamaoka S, Yamamoto N, Akira S (2012) Neutrophil extracellular traps mediate a host defense response to human immunodeficiency virus-1. Cell Host Microbe 12(1):109-116. doi:10.1016/j.chom.2012.05.015, S1931-3128(12)00201-6 [pii]
76. Samanta M, Iwakiri D, Kanda T, Imaizumi T, Takada K (2006) EB virus-encoded RNAs are recognized by RIG-I and activate signaling to induce type I IFN. EMBO J 25(18):4207-4214. doi:10.1038/sj.emboj.7601314, 7601314 [pii]
77. Savard M, Gosselin J (2006) Epstein-Barr virus immunossuppression of innate immunity mediated by phagocytes. Virus Res 119(2):134-145. doi:10.1016/j.virusres.2006.02.008, S0168-1702(06)00069-4 [pii]
78. Savard M, Belanger C, Tardif M, Gourde P, Flamand L, Gosselin J (2000) Infection of primary human monocytes by Epstein-Barr virus. J Virol 74(6):2612-2619
79. Severa M, Giacomini E, Gafa V, Anastasiadou E, Rizzo F, Corazzari M, Romagnoli A, Trivedi P, Fimia GM, Coccia EM (2013) EBV stimulates TLR-and autophagy-dependent pathways and impairs maturation in plasmacytoid dendritic cells: implications for viral immune escape. Eur J Immunol 43(1):147-158. doi:10.1002/eji.201242552
80. Shannon-Lowe C, Rowe M (2014) Epstein Barr virus entry; kissing and conjugation. Curr Opin Virol 4:78-84. doi:10.1016/j.coviro.2013.12.001, S1879-6257(13)00204-6 [pii]
81. Shannon-Lowe CD, Neuhierl B, Baldwin G, Rickinson AB, Delecluse HJ (2006) Resting B cells as a transfer vehicle for Epstein-Barr virus infection of epithelial cells. Proc Natl Acad Sci USA 103(18):7065-7070. doi:10.1073/pnas.0510512103, 0510512103 [pii]
82. Shannon-Lowe C, Adland E, Bell AI, Delecluse HJ, Rickinson AB, Rowe M (2009) Features distinguishing Epstein-Barr virus infections of epithelial cells and B cells: viral genome expression, genome maintenance, and genome amplification. J Virol 83(15):7749-7760. doi: 10.1128/JVI.00108-09, JVI.00108-09 [pii]
83. Shim AH, Chang RA, Chen X, Longnecker R, He X (2012) Multipronged attenuation of macrophage-colony stimulating factor signaling by Epstein-Barr virus BARF1. Proc Natl Acad Sci U S A 109(32):12962-12967. doi:10.1073/pnas.1205309109, 1205309109 [pii]
84. Speck SH, Ganem D (2010) Viral latency and its regulation: lessons from the gamma-herpesviruses. Cell Host Microbe 8(1):100-115. doi:10.1016/j.chom.2010.06.014
85. Strowig T, Brilot F, Arrey F, Bougras G, Thomas D, Muller WA, Munz C (2008) Tonsilar NK cells restrict B cell transformation by the Epstein-Barr virus via IFN-gamma. PLoS Pathog 4(2):e27. doi:10.1371/journal.ppat.0040027, 07-PLPA-RA-0357 [pii]
86. Szabo A, Rajnavolgyi E (2013) Collaboration of Toll-like and RIG-I-like receptors in human dendritic cells: tRIGgering antiviral innate immune responses. Am J Clin Exp Immunol 2(3):195-207
87. Tugizov SM, Berline JW, Palefsky JM (2003) Epstein-Barr virus infection of polarized tongue and nasopharyngeal epithelial cells. Nat Med 9(3):307-314
88. Tugizov S, Herrera R, Veluppillai P, Greenspan J, Greenspan D, Palefsky JM (2007) Epstein-Barr virus (EBV)-infected monocytes facilitate dissemination of EBV within the oral mucosal epithelium. J Virol 81(11):5484-5496. doi:10.1128/JVI.00171-07, JVI.00171-07 [pii]
89. Tugizov SM, Herrera R, Palefsky JM (2013) Epstein-Barr virus transcytosis through polarized oral epithelial cells. J Virol 87(14):8179-8194. doi:10.1128/JVI.00443-13, JVI.00443-13 [pii]
90. Umbach JL, Cullen BR (2009) The role of RNAi and microRNAs in animal virus replication and antiviral immunity. Genes Dev 23(10):1151-1164. doi:10.1101/gad.1793309, 23/10/1151 [pii]
91. van derGrein SG, Nolte-'t Hoen EN (2014) "Small Talk" in the innate immune system via RNAcontaining extracellular vesicles. Front Immunol 5:542. doi:10.3389/fimmu.2014.00542
92. vanGent M, Griffin BD, Berkhoff EG, van Leeuwen D, Boer IG, Buisson M, Hartgers FC, Burmeister WP, Wiertz EJ, Ressing ME (2011) EBV lytic-phase protein BGLF5 contributes to TLR9 downregulation during productive infection. J Immunol 186(3):1694-1702. doi:10. 4049/jimmunol.0903120, jimmunol.0903120 [pii]
93. vanGent M, Braem SG, de Jong A, Delagic N, Peeters JG, Boer IG, Moynagh PN, Kremmer E, Wiertz EJ, Ovaa H, Griffin BD, Ressing ME (2014) Epstein-Barr virus large tegument protein BPLF1 contributes to innate immune evasion through interference with Toll-like receptor signaling. PLoS Pathog 10(2):e1003960. doi:10.1371/journal.ppat.1003960, PPATHOGENS-D-13-01814 [pii]
94. Waggoner SN, Cornberg M, Selin LK, Welsh RM (2012) Natural killer cells act as rheostats modulating antiviral T cells. Nature 481 (7381):394-398. doi:10.1038/nature10624, nature10624 [pii]
95. Weber F, Wagner V, Rasmussen SB, Hartmann R, Paludan SR (2006) Double-stranded RNA is produced by positive-strand RNA viruses and DNA viruses but not in detectable amounts by negative-strand RNA viruses. J Virol 80(10):5059-5064. doi:10.1128/ JVI.80.10.5059-5064.2006, 80/10/5059 [pii]
96. White MJ, Nielsen CM, McGregor RH, Riley EH, Goodier MR (2014) Differential activation of CD57-defined natural killer cell subsets during recall responses to vaccine antigens. Immunology 142(1):140-150
97. Williams H, McAulay K, Macsween KF, Gallacher NJ, Higgins CD, Harrison N, Swerdlow AJ, Crawford DH (2005) The immune response to primary EBV infection: a role for natural killer cells. Br J Haematol 129(2):266-274
98. Woellmer A, Arteaga-Salas JM, Hammerschmidt W (2012) BZLF1 governs CpG-methylated chromatin of Epstein-Barr Virus reversing epigenetic repression. PLoS Pathog 8(9):e1002902. doi:10.1371/journal.ppat.1002902, PPATHOGENS-D-12-00492 [pii]
99. Wurdinger T, Gatson NN, Balaj L, Kaur B, Breakefield XO, Pegtel DM (2012) Extracellular vesicles and their convergence with viral pathways. Adv Virol 2012:767694. doi:10.1155/2012/767694
100. Younesi V, Nikzamir H, Yousefi M, Khoshnoodi J, Arjmand M, Rabbani H, Shokri F (2010) Epstein Barr virus inhibits the stimulatory effect of TLR7/8 and TLR9 agonists but not CD40 ligand in human B lymphocytes. Microbiol Immunol 54(9):534-541. doi:10.1111/ j.1348-0421.2010.00248.x, MIM248 [pii]
101. Young LS, Rickinson AB (2004) Epstein-Barr virus: 40 years on. Nat Rev Cancer 4(10):757-768
102. Zauner L, Melroe GT, Sigrist JA, Rechsteiner MP, Dorner M, Arnold M, Berger C, Bernasconi M, Schaefer BW, Speck RF, Nadal D (2010) TLR9 triggering in Burkitt's lymphoma cell lines suppresses the EBV BZLF1 transcription via histone modification. Oncogene 29(32):4588-4598. doi:10.1038/onc.2010.203
103. Zomer A, Vendrig T, Hopmans ES, van Eijndhoven M, Middeldorp JM, Pegtel DM (2010) Exosomes: fit to deliver small RNA. Commun Integr Biol 3(5):447-450. doi:10.4161/ cib.3.5.12339