Multifunctional non-coding Epstein-Barr virus encoded RNAs (EBERs) contribute to viral pathogenesis

Virus Research

Volumn 212, Issue , 2016, Pages 30-38

  Iwakiri, Dai ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

Author keywords

EBER; Epstein Barr virus; Exosomes; Innate immunity; Micro RNA; Oncogenesis

Indexed keywords

CELL PROTEIN; EPSTEIN BARR VIRUS ENCODED RNA; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN D; L22 PROTEIN; LUPUS ANTIGEN; MICRORNA; PROTEIN KINASE R; RETINOIC ACID INDUCIBLE PROTEIN I; TOLL LIKE RECEPTOR 3; UNCLASSIFIED DRUG; UNTRANSLATED RNA; VIRUS RNA;

ARTICLE; CELL GROWTH; EPSTEIN BARR VIRUS; EXOSOME; GENE EXPRESSION; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN SECONDARY STRUCTURE; RNA STRUCTURE; RNA SYNTHESIS; SEQUENCE HOMOLOGY; VIRUS CARCINOGENESIS; VIRUS CELL TRANSFORMATION; VIRUS VIRULENCE; ANIMAL; EPSTEIN BARR VIRUS INFECTION; GENETICS; HUMAN; METABOLISM; PATHOGENICITY; VIROLOGY; VIRULENCE;

ANIMALS; EPSTEIN-BARR VIRUS INFECTIONS; HERPESVIRUS 4, HUMAN; HUMANS; RNA, UNTRANSLATED; RNA, VIRAL; VIRULENCE;

EID: 84957428655     PISSN: 01681702     EISSN: 18727492     Source Type: Journal    
DOI: 10.1016/j.virusres.2015.08.007     Document Type: Article

References (128)

1. Ahmed W., Phillip P.S., Taniq S., Khan G. Epstein-Barr virus-encoded small RNAs (EBERs) are present in fractions related to exosomes released by EBV-transformed cells. PLoS One 2014, 9:e99163.
2. Akira S., Takeda K. Toll-like receptor signaling. Nat. Rev. Immunol. 2004, 4:499-511.
3. Akusjärvi G., Mathews M.B., Andersson P., Vennström B., Pettersson U. Structure of genes for virus-associated RNAI and RNAII of adenovirus type 2. Proc. Natl. Acad. Sci. U. S. A. 1980, 77:2424-2428.
4. Alexopoulou L., Holt A.C., Medzhitov R., Flavell R.A. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 2001, 413:732-738.
5. Arrand J.R., Ryomo L. Characterization of the major Epstein-Barr virus-specific RNA in Burkitt lymphoma-derived cells. J. Virol. 1982, 41:376-389.
6. Arrand J.R., Young L.S., Tugwood J.D. Two families of sequences in the small RNA-encoding region of Epstein-Barr virus (EBV) correlate with EBV types A and B. J. Virol. 1989, 63:983-986.
7. Bachmann M., Pfeifer K., Schröder H.C., Müller W.E. The La antigen shuttles between the nucleus and the cytoplasm in CV-1 cells. Mol. Cell. Biochem. 1989, 85:103-114.
8. Bartel D.P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004, 116:281-297.
9. Bellare P., Ganem D. Regulation of KSHV lytic switch protein expression by a virus-encoded microRNA: an evolutionary adaptation that fine-tunes lytic reactivation. Cell Host Microbe 2009, 6:570-575.
10. Berezikov E., Plasterk R.H. Camels and zebrafish, viruses and cancer: a microRNA update. Hum. Mol. Genet. 2005, 14:R183-R190.
11. Bhat R.A., Thimmappaya B. Two small RNAs encoded by Epstein-Barr virus can functionally substitute for the virus-associated RNAs in the lytic growth of adenovirus 5. Proc. Natl. Acad. Sci. U. S. A. 1983, 80:4789-4793.
12. Cai X., Schafer A., Lu S., Bilello J.P., Desrosiers R.C., Edwards R., Raab-Traub N., Cullen B.R. Epstein-Barr virus microRNAs are evolutionarily conserved and differentially expressed. PLoS Pathog. 2006, 2:e23.
13. Cazalla D., Xie M., Steitz J.A. A primate herpesvirus uses the integrator complex to generate viral microRNAs. Mol. Cell 2011, 43:982-992.
14. Chang K.L., Chen Y.Y., Shibata D., Weiss L.M. Description of an in situ hybridization methodology for detection of Epstein-Barr virus RNA in paraffin-embedded tissues, with a survey of normal and neoplastic tissues. Diagn. Mol. Pathol. 1992, 1:246-255.
15. Chen S.J., Chen G.H., Chen Y.H., Liu C.Y., Chang K.P., Chang Y.S., Chen H.C. Characterization of Epstein-Barr virus miRNAome in nasopharyngeal carcinoma by deep sequencing. PLoS One 2010, 5:e12745.
16. Choy E.Y., Siu K.L., Kok K.H., Lung R.W., Tsang C.M., To K.F., Kwong D.L., Tsao S.W., Jin D.Y. An Epstein-Barr virus-encoded microRNA targets PUMA to promote host cell survival. J. Exp. Med. 2008, 205:2551-2560.
17. Clarke P.A., Schwemmle M., Schickinger J., Hilse K., Clemens M.J. Binding of Epstein-Barr virus small RNA EBER-1 to the double-stranded RNA-activated protein kinase DAI. Nucleic Acids Res. 1991, 19:243-248.
18. Clarke P.A., Sharp N.A., Clemens M.J. Expression of genes for the Epstein-Barr virus small RNAs EBER-1 and EBER-2 in Daudi Burkitt's lymphoma cells: effects of interferon treatment. J. Gen. Virol. 1992, 73:3169-3175.
19. Cole K., Cole K.E., Strick C.A., Paradis T.J., Ogborne K.T., Loetscher M., Gladue R.P., Lin W., Boyd J.G., Moser B., Wood D.E., Sahagan B.G. Curr. Opin. Virol. 2014, 7:61-65.
20. Cullen B.R. Viruses and microRNAs. Nat. Genet. 2006, 38:S25-S30.
21. Cullen B.R. MicroRNAs as mediators of viral immune evasion. Nat. Immunol. 2013, 14:205-210.
22. Dobbelstein M., Shenk T. In vitro selection of RNA ligands for the ribosomal L22 protein associated with Epstein-Barr virus-expressed RNA by using randomized and cDNA-derived RNA libraries. J. Virol. 1995, 69:8027-8034.
23. Dolken L., Malterer G., Erhard F., Kothe S., Friedel C.C., Suffert G., Marcinowski L., Motsch N., Barth S., Beitzinger M., Lieber D., Bailer S.M., Hoffmann R., Ruzsics Z., Kremmer E., Pfeffer S., Zimmer R., Koszinowski U.H., Grässer F., Meister G., Haas J. Systematic analysis of viral and cellular microRNA targets in cells latently infected with human gamma-herpesviruses by RISC immunoprecipitation assay. Cell Host Microbe 2010, 7:324-334.
24. Duan Y., Li Z., Cheng S., Chen Y., Zhang L., He J., Liao Q., Yang L., Gong Z., Sun L.Q. Nasopharyngeal carcinoma progression is mediated by EBER-triggered inflammation via the RIG-I pathway. Cancer Lett. 2015, 361:67-74.
25. Elia A., Vyas J., Laing K.G., Clemens M.J. Ribosomal protein L22 inhibits regulation of cellular activities by the Epstein-Barr virus small RNA EBER-1. Eur. J. Biochem. 2004, 27:1895-1905.
26. Feederle R., Linnstaedt S.D., Bannert H., Lips H., Bencun M., Cullen B.R., Delecluse H.J. A viral microRNA cluster strongly potentiates the transforming properties of a human herpesvirus. PLoS Pathog. 2011, 7:e1001294.
27. Feederle R., Haar J., Bernhardt K., Linnstaedt S.D., Bannert H., Lips H., Cullen B.R., Delecluse H.J. The members of an Epstein-Barr virus microRNA cluster cooperate to transform B lymphocytes. J. Virol. 2011, 85:9801-9810.
28. Fok V., Friend K., Steitz J.A. Epstein-Barr virus noncoding RNAs are confined to the nucleus, whereas their partner, the human La protein, undergoes nuclecytoplasmic shuttling. J. Cell Biol. 2006, 173:319-325.
29. Fok V., Mitton-Fry R.M., Grech A., Steitz J.A. Multiple domains of EBER 1, an Epstein-Barr virus noncoding RNA, recruit human ribosomal protein L22. RNA 2006, 12:872-882.
30. Gilligan K., Rajadurai P., Resnick L., Raab-Traub N. Epstein-Barr virus small nuclear RNAs are not expressed in permissively infected cells in AIDS-associated leukoplakia. Proc. Natl. Acad. Sci. U. S. A. 1990, 87:8790-8794.
31. Gratacós F.M., Brewer G. The role of AUF in regulated mRNA decay. Wiley Interdiscip. Rev. RNA 2010, 1:457-473.
32. Gregorovic G., Bosshard R., Karstegl C.E., White R.E., Pattle S., Chiang A.K., Dittrich-Breiholz O., Kracht M., Russ R., Farrell P.J. Cellular gene expression that correlates with EBER expression in Epstein-Barr virus-infected lymphoblastoid cell lines. J. Virol. 2011, 85:3535-3545.
33. Greifenegger N., Jäger M., Kunz-Schughart L.A., Wolf H., Schwarzmann F. Epstein-Barr virus small RNA (EBER) genes: differential regulation during lytic viral replication. J. Virol. 1998, 72:9323-9328.
34. Haneklaus M., Gerlic M., Kurowska-Stolarska M., Rainey A.-A., Pich D., McInnes I.B., Hammerschmidt W., O'Neill L.A.J., Masters S.L. Cutting edge: miR-223 and EBV miR-BART15 regulate the NLRP3 inflammasome and IL-1β production. J. Immunol. 2013, 189:3795-3799.
35. null mice. Blood 2003, 102:873-880.
36. Hornung V., Ellegast J., Kim S., Brzózka K., Jung A., Kato H., Poeck H., Akira S., Conzelmann K.K., Schlee M., Endres S., Hartman G. 5'-Triphosphate RNA is the ligand for RIG- I. Science 2006, 314:994-997.
37. Houmani J.L., Davis C.I., Ruf I.K. Growth-promoting properties of Epstein-Barr virus EBER-1 RNA correlate with ribosomal protein L22 binding. J. Virol. 2009, 83:9844-9853.
38. Howe J.G., Steitz J.A. Localization of Epstein-Barr virus-encoded small RNAs by in situ hybridization. Proc. Natl. Acad. Sci. U. S. A. 1986, 83:9006-9010.
39. Howe J.G., Shu M.D. Isolation and characterization of the genes for two small RNAs of herpesvirus papio and their comparison with Epstein-Barr virus-encoded EBER RNAs. J. Virol. 1988, 62:2790-2798.
40. Howe J.G., Shu M.D. Epstein-Barr virus small RNA (EBER) genes: unique transcription units that combine RNA polymerase II and III promoter elements. Cell 1989, 57:825-834.
41. Huang M., Ida H., Arima K., Nakamura H., Aramaki T., Fujikawa K., Tamai M., Kamachi M., Kawakami A., Yamasaki H., Origuchi T., Eguchi K. La autoantigen translocates to cytoplasm after cleavage during granzyme B-mediated cytotoxicity. Life Sci. 2007, 81:1461-1466.
42. Hutzinger R., Feederle R., Mrazek J., Schiefermeier N., Balwierz P.J., Zavolan M., Polacek N., Delecluse H.-J., Huttenhofer A. Expression and processing of a small nucleolar RNA from the Epstein-Barr virus genome. PLoS Pathog. 2009, 5:e1000547.
43. Iwakiri D., Eizuru Y., Tokunaga M., Takada K. Autocrine growth of Epstein-Barr virus-positive gastric carcinoma cells mediated by an Epstein-Barr virus-encoded small RNA. Cancer Res. 2003, 63:7062-7067.
44. Iwakiri D., Sheen T.S., Chen J.Y., Huang D.P., Takada K. Epstein-Barr virus-encoded small RNA induces insulin-like growth factor 1 and supports growth of nasopharyngeal carcinoma-derived cell lines. Oncogene 2005, 24:1767-1773.
45. Iwakiri D., Zhou L., Samanta M., Matsumoto M., Ebihara T., Seya T., Imai S., Fujieda M., Kawa K., Takada K. Epstein-Barr virus (EBV)-encoded small RNA is released from EBV-infected cells and activates signaling from Toll-like receptor 3. J. Exp. Med. 2009, 206:2091-2099.
46. Kang D.C., Gopalkrishnan R.V., Wu Q., Jankowsky E., Pyle A.M., Fisher P.B. mda-5: an interferon-inducible putative RNA helicase with double-stranded RNA-depen- dent ATPase activity and melanoma growth-suppressive properties. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:637-642.
47. Kasahara Y., Yachie A., Takei K., Kanegane C., Okada K., Ohta K., Seki H., Igarashi N., Maruhashi K., Katayama K., Katoh E., Terao G., Sakiyama Y., Koizumi S. Differential cellular targets of Epstein-Barr virus (EBV) infection between acute EBV-associated hemophagocytic lymphohistiocytosis and chronic active EBV infection. Blood 2001, 98:1882-1888.
48. Katze M.G., Wambach M., Wong M.L., Garfinkel M., Meurs E., Chong K., Williams B.R., Hovanessian A.G., Barber G.N. Functional expression and RNA binding analysis of the interferon-induced double-stranded RNA-activated, 68 000-Mr protein kinase in a cell-free system. Mol. Cell. Biol. 1991, 11:5497-5505.
49. Kawai T., Takahashi K., Sato S., Coban C., Kumar H., Kato H., Ishii K.J., Takeuchi O., Akira S. IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nat. Immunol. 2005, 11:1074-1076.
50. Kikuta H., Sakiyama Y., Matsumoto S., Oh-Ishi T., Nakano T., Nagashima T., Oka T., Hironaka T., Hirai K. Fatal Epstein-Barr virus-associated hemophagocytic syndrome. Blood 1993, 82:3259-3264.
51. Kincaid R.P., Sullivan C.S. Virus-encoded microRNAs: an overview and a look to the future. PLoS Pathog. 2012, 8:e1003018.
52. Kitagawa N., Goto M., Kurozumi K., Maruo S., Fukayama M., Naoe T., Yasukaswa M., Hino K., Suzuki T., Todo S., Takada K. Epstein-Barr virus-encoded poly(A)(-) RNA supports Burkitt's lymphoma growth through interleukin-10 induction. EMBO J. 2000, 19:6742-6750.
53. Komano J., Maruo S., Kurozumi K., Oda T., Takada K. Oncogenic role of Epstein-Barr virus-encoded RNAs in Burkitt's lymphoma cell line Akata. J. Virol. 1999, 73:9827-9831.
54. Krol J., Loedige I., Filipowicz W. The widespread regulation of microRNA biogenesis, function and decay. Nat. Rev. Genet. 2010, 11:597-610.
55. Lal A., Mazan-Mamczarz K., Kawai T., Yang X., Martindale J.L., Gorospe M. Concurrent versus individual binding of HuR and AUF1 to common labile target mRNAs. EMBO J. 2004, 23:3092-3102.
56. Landgraf P., Rusu M., Sheridan R., Sewer A., Iovino N., Aravin A., Pfeffer S., Rice A., Kamphorst A.O., Landthaler M., Lin C., Socci N.D., Hermida L., Fulci V., S Chiarettim, ' R., Schliwka J., Fuchs U., Novosel A., R- U., Schermer B., Bissels U., Inman J., Phan Q., Chien M., Weir D.B., Choksi R., De Vita G., Frezzetti D., H- I., Hornung V., Teng G., Hartmann G., Palkovits M., Di Lauro R., Wernet P., Macino G., Rogler C.E., Nagle J.W., Ju J., Papavasiliou F.N., Benzing T., Lichter P., Tam W., Brownstein M.J., Bosio A., Borkhardt A., Russo J.J., Sander C., Zavolan M., Tuschl T. A mammalian microRNA expression atlas based on small RNA library sequencing. Cell 2007, 129:1401-1414.
57. Le S., Sternglanz R., Greider C.W. Identification of two RNA-binding proteins associated with human telomerase RNA. Mol. Biol. Cell 2000, 11:999-1010.
58. Lee N., Pimienta G., Steitz J.A. AUF1/ hnRNP D is a novel protein partner of the EBER1 noncoding RNA of Epstein-Barr virus. RNA 2012, 18:2073-2082.
59. Lei X., Bai Z., Ye F., Xie J., Kim C.G., Huang Y., Gao S.J. Regulation of NF-kappaB inhibitor IkappaB alpha and viral replication by a KSHV microRNA. Nat. Cell Biol. 2010, 12:193-199.
60. Leopardi R., Ward P.L., Ogle W.O., Roizman B. Association of herpes simplex virus regulatory protein ICP22 with transcrip- tional complexes containing EAP, ICP4, RNA polymerase II, and viral DNA requires posttranslational modification by the U(L) 13 proteinkinase. J. Virol. 1997, 71:1133-1139.
61. Lerner M.R., Andrews N.C., Miller G., Steitz J.A. 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. U. S. A. 1981, 78:805-809.
62. Liu P., Tarlé S.A., Hajra A., Claxton D.F., Marlton P., Freedman M., Siciliano M.J., Collins F.S. Fusion between transcription factor CBF beta/PEBP2 beta and a myosin heavy chain in acute myeloid leukemia. Science 1993, 261:1041-1044.
63. Lu J.-Y., Sadri N., Schneider R.J. Endotoxic shock in AUF1 knockout mice mediated by failure to degrade proinflammatory cytokine mRNAs. Genes Dev. 2006, 20:3174-3184.
64. Mallory A., Vaucheret H. Functions of microRNAs and related small RNAs in plants. Nat. Genet. 2006, 38(Suppl 1):S31-S36.
65. Marquitz A.R., Mathu A., Nam C.S., Raab-Traub N. The Epstein-Barr virus BART microRNAs target the pro-apoptotic protein Bim. Virology 2011, 412:392-400.
66. Mckenna S.A., Lindhout D.A., Shimoike T., Aitken C.E., Puglisis J.D. Viral dsRNA inhibitors prevent self-association and autophosphorylation of PKR. J. Mol. Biol. 2007, 372:103-113.
67. Meckes D.G.J., r S., hair K.H.Y., Marquitz A.R., Kung C.-P., Edwards R.H., Raab-Traub N. Human tumor virus utilizes exosomes for intercellular communication. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:20370-20375.
68. Meerovitch K., Svitkin Y.V., Lee H.S., Lejbkowicz F., Kenan D.J., Chan E.K., Agol V.I., Keene J.D., Sonenberg N. La autoantigen enhances and corrects aberrant translation of poliovirus RNA in reticulocyte lysate. J. Virol. 1993, 67:3798-3807.
69. Meurs E., Chong K., Galabru J., Thomas N.S., Kerr I.M., Williams B.R., Hovanessian A.G. Molecular cloning and characterization of the human double-stranded RNA-activated protein kinase induced by interferon. Cell 1990, 62:379-390.
70. Meylan E., Tschopp J. Toll-like receptors and RNA helicases: two parallel ways to trigger antiviral responses. Mol. Cell 2006, 22:561-569.
71. Mizugaki Y., Sugawara Y., Shinozaki F., Takada K. Detection of Epstein-Barr virus in oral papilloma. Jpn. J. Cancer Res. 1998, 89:604-607.
72. Nachmani D., Stern-Ginossar N., Sarid R., Mandelboim O. Diverse herpesvirus microRNAs target the stress-induced immune ligand MICB to escape recognition by natural killer cells. Cell Host Microbe 2009, 5:376-385.
73. Nanbo A., Inoue K., Adachi-Takasawa K., Takada K. Epstein-Barr virus RNA confers resistance to interferon-alpha-induced apoptosis in Burkitt's lymphoma. EMBO J. 2002, 21:954-965.
74. Nanbo A., Kawanishi E., Yoshida R., Yoshiyama H. Exosomes derived from Epstein-Barr virus-infected cells are internalized via caveola-dependent endocytosis and promote phenotypic modulation in target cells. J. Virol. 2013, 87:10334-10347.
75. Nucifora G., Begy C.R., Erickson P., Drabkin H.A., Rowley J.D. The 3;21 translocation in myelodysplasia results in a fusion transcript between the AML1 gene and the gene for EAP, a highly conserved protein associated with the Epstein-Barr virus small RNA EBER 1. Proc. Natl. Acad. Sci. U. S. A. 1993, 90:7784-7788.
76. Pant S., Hilton H., Burczynski M.E. The multifaceted exosome: biogenesis, role in normal and aberrant cellular function, and frontiers for pharmacological and biomarker opportunities. Biochem. Pharmacol. 2012, 83:1484-1494.
77. Pegtel D.M., Cosmopoulos K., Thorley-Lawson D.A., van Eijndhoven M.A.J., Hopmans E.S., Lindenberg J.L., de Gruijl T.D., Würdinger T., Middeldorp J.M. Functional delivery of viral miRNAs via exoso mes. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:6328-6333.
78. Piper R.C., Katzmann D.J. Biogenesis and function of multivesicular bodies. Annu. Rev. Cell Dev. Biol. 2007, 23:519-547.
79. Pfeffer S., Sewer A., Lagos-Quintana M., Sheridan R., Sander C., Grasser A., van Dyk L.F., Ho C.K., Shuman S., Chien M., Russo J.J., Ju J., Randall G., Lindenbach B.D., Rice C.M., Simon V., Ho D.D., Zavolan M., Tuschl T. Identification of microRNAs of the herpesvirus family. Nat. Methods 2005, 2:269-276.
80. Pratt Z.L., Kuzembayeva M., Sengupta S., Sugden B. The microRNAs of Epstein-Barr virus are expressed at dramatically differing levels among cell lines. Virology 2009, 386:387-397.
81. Qiu J., Cosmopoulos K., Pegtel M., Hopmans E., Murray P., Middeldorp J., Shapiro M., Thorley-Lawson D.A. A novel persistence associated EBV miRNA expression profile is disrupted in neoplasia. PLoS Pathog. 2011, 7:e1002193.
82. Repellin C.E., Tsimbouri P.M., Philbey A.W., Wilson J.B. Lymphoid hyperplasia and lymphoma in transgenic mice expressing the small non-coding RNA, EBER1 of Epstein-Barr virus. PLoS One 2010, 5:e9092.
83. Rickinson A.B., Kieff E. Epstein-Barr virus. Fields Virol Walters 2007, 2655-2700. Kluwer/Lippincott, Philadelphia, USA. D.M. Knipe, P.M. Howley (Eds.).
84. Riley K.J., Rabinowitz G.S., Yario T.A., Luna J.M., Darnell R.B., Steitz J.A. EBV and human microRNAs co-target oncogenic and apoptotic viral and human genes during latency. EMBO J. 2012, 31:2207-2221.
85. Rosa M.D., Gottlieb E., Lerner M.R., Steitz J.A. Striking similarities are exhibited by two small Epstein-Barr virus-encoded ribonucleic acids and the adenovirus-associated ribonucleic acids VAI and VAII. Mol. Cell. Biol. 1981, 9:785-796.
86. Ruf I.K., Rhyne P.W., Yang C., Cleveland J.L., Sample J.T. Epstein-Barr virus small RNAs potentiate tumorigenicity of Burkitt lymphoma cells independently of an effect on apoptosis. J. Virol. 2000, 74:10223-10228.
87. Rymo L. Identification of transcribed regions of Epstein-Barr virus DNA in Burkitt lymphoma-derived cells. J. Virol. 1979, 32:8-18.
88. Samanta M., Iwakiri D., Kanda T., Imaizumi T., Takada K. EB virus-encoded RNAs are recognized by RIG-I and activate signaling to induce type I IFN. EMBO J. 2006, 25:4207-4214.
89. Samanta M., Iwakiri D., Takada K. Epstein-Barr virus-encoded small RNA induces IL-10 through RIG-I-mediated IRF-3 signaling. Oncogene 2008, 27:4150-4160.
90. Sato K., Misawa N., Nie C., Satou Y., Iwakiri D., Matsuoka M., Takahashi R., Kuzushima K., Ito M., Takada K., Koyanagi Y. A novel animal model of Epstein-Barr virus-associated hemophagocytic lymphohistiocytosis in humanized micse. Blood 2011, 117:5663-5673.
91. Schwemmle M., Clemens M.J., Hilse K., Pfeifer K., Tröster H., Müller W.E., Bachmann M. Localization of Epstein-Barr vi rus-encoded RNAs EBER-1 anEBER-2 in interphase and mitotic Burkitt lymphoma cells. Proc. Natl. Acad. Sci. U S A. 1992, 89:10292-10296.
92. Schmidt K.N., Leung B., Kwong M., Zarember K.A., Satyal S., Navas T.A., Wang F., Godowski P.J. APC-independent activation of NK cells by the Toll-like receptor 3 agonist double-stranded RNA. J. Immunol. 2004, 172:138-143.
93. Seto E., Moosmann A., Gromminger S., Walz N., Grundhoff A., Hammerschmidt W. Micro RNAs of Epstein-Barr virus promote cell cycle progression and prevent apoptosis of primary human B cells. PLoS Pathog. 2010, 6:e1001063.
94. Sharp T.V., Schwemmle M., Jeffrey I., Laing K., Mellor H., Proud C.G., Hilse K., Clemens M.J. Comparative analysis of the regulation of the interferon-inducible protein kinase PKR by Epstein-Barr virus RNAs EBER-1 and EBER-2 and adenovirus VAI RNA. Nucleic Acids Res. 1993, 21:4483-4490.
95. Shen Z.C., Luo B., Chen J.N., Chao Y., Shao C.K., Liu Q.Q., Wang Y. High prevalence of the EBER variant EB-8m in endemic nasopharyngeal carcinomas. PLoS One 2015, 10:e0121420.
96. Shimizu N., Tanabe-Tochikura A., Kuroiwa Y., Takada K. Isolation of Epstein-Barr virus (EBV)-negative cell clones from the EBV- positive Burkitt's lymphoma (BL) line Akata: malignant phenotypes of BL cells are dependent on EBV. J. Virol. 1994, 68:6069-6073.
97. Shiroki K., Isoyama T., Kuge S., Ishii T., Ohmi S., Hata S., Suzuki K., Takasaki Y., Nomoto A. Intracellular redistribution of truncated La protein produced by poliovirus 3Cpro- mediated cleavage. J. Virol. 1999, 73:2193-2200.
98. Skalsky R.L., Corcoran D.L., Gottwein E., Frank C.L., Kang D., Hafner M., Nusbaum J.D., Feederle R., Delecluse H.-J., Luftig M.A., Tuschl T., Ohler U., Cullen B.R. The viral and cellular microRNA targetome in lymphoblastoid cell lines. PLoS Pathog. 2012, 8:e1002484.
99. Swaminathan S., Tomkinson B., Kieff E. Recombinant Epstein-Barr virus with small RNA (EBER) genes deleted transforms lymphocytes and replicates in vitro. J. Virol. 1991, 66:5133-5136.
100. Tabiasco J., Devêvre E., Rufer N., Salaun B., Cerottini J.C., Speiser D., Romero D. Human effector CD8+ T lymphocytes express TLR3 as a functional coreceptor. J. Immunol. 2006, 177:8708-8713.
101. Toczyski D.P., Steitz J.A. EAP, a highly conserved cellular protein associated with Epstein-Barr virus small RNAs (EBERs). EMBO J. 1991, 10:459-466.
102. Toczyski D.P., Steitz J.A. The cellular RNA-binding protein EAP recognizes a conserved stem-loop in the Epstein-Barr virus small RNA EBER 1. Mol. Cell. Biol. 1993, 1:703-710.
103. Toczyski D.P., Matera A.G., Ward D.C., Steitz J.A. The Epstein-Barr virus (EBV) small RNA EBER1 binds and relocalizes ribosomal protein L22 in EBV-infected human B lymphocytes. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:3463-3467.
104. Tsang C.M., Zhang G., Seto E., Takada K., Deng W., Yip Y.L., Man C., Hau P.M., Chen H., Cao Y., Lo K.W., Middeldorp J.M., Cheung A.L., Tsao S.W. Epstein-Barr virus infection in immortalized nasopharyngeal epithelial cells: regulation of infection and phenotypic characterization. Int. J. Cancer 2010, 127:1570-1583.
105. Umbach J.L., Kramer M.F., Jurak I., Karnowski H.W., Coen D.M., Cullen B.R. MicroRNAs expressed by herpes simplex virus 1 during latent infection regulate viral mRNAs. Nature 2008, 454:780-783.
106. Umbach, JL, Nagel M.A., Cohrs R.J., Gilden D.H., Cullen B.R. Analysis of human alphaherpesvirus microRNA expression in latently infected human trigeminal ganglia. J. Virol. 2009, 83:10677-10683.
107. Vereide D.T., Seto E., Chiu Y.F., Hayes M., Tagawa T., Grundhoff A., Tagawa T., Grundhoff A., Hammerschmidt W., Sugden B. Epstein-Barr virus maintains lymphomas via its miRNAs. Oncogene 2013, 33:1258-1264.
108. Verweij F.J., van Eijndhoven M.A.J., Hopmans E.S., Vendrig T., Wurdinger T., Cahir-McFarland E., Kieff E., Geerts D., van der Kant R., Neefjes J., Middeldorp J.M., Pegtel D.M. LMP1 association with CD63 in endosomes and secretion via exosomes limits constitutive NF-kB activation. EMBO J. 2011, 30:2115-2129.
109. Vuyisich M., Spanggord R.J., Beal P.A. The binding site of the RNA-dependent protein kinase (PKR) on EBER1 RNA from Epstein-Barr virus. EMBO Rep. 2000, 3:622-627.
110. Wahl A., Linnstaedt S.D., Esoda C., Krisko J.F., Martinez-Torres F., Delecluse H.J., Cullen B.R., Garcia J.V. 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. 2013, 87:5437-5446.
111. Wang Y., Zhang X., Chao Y., Jia Y., Xing X., Luo B. New variations of Epstein-Barr virus-encoded small RNA genes in nasopharyngeal carcinomas, gastric carcinomas, and healthy donors in Northern China. J. Med. Virol. 2010, 82:829-836.
112. Wen S., Mizugaki Y., Shinozaki F., Takada K. Epstein-Barr virus (EBV) infection in salivary gland tumors: lytic EBV infection in nonmalignant epithelial cells surrounded by EBV-positive T-lymphoma cells. Virology 1997, 227:484-487.
113. Wen S., Shimizu N., Yoshiyama H., Mizugaki Y., Shinozaki F., Takada K. Association of Epstein-Barr virus (EBV) with Sjögren's syndrome: differential EBV expression between epithelial cells and lymphocytes in salivary glands. Am. J. Pathol. 1996, 149:1511-1517.
114. Wen W., Iwakir, i D., Yamamoto K., Maruo S., Kanda T., Takada K. Epstein-Barr Virus BZLF1 Gene, a switch from latency to lytic infection, is expressed as an immediate early gene following primary infection of B-lymphocytes. J. Virol. 2007, 81:1037-1042.
115. Wong H.L., Wang X., Chang R.C., Jin D.Y., Feng H., Wang Q., Lo K.W., Huang D.P., Yuen P.W., Takada K., Wong Y.C., Tsao S.W. table expression of EBERs in immortalized nasopharyngeal epithelial cells confers resis- tance to apoptotic stress. Mol. Carcinogenesis 2005, 44:92-101.
116. Wood J., Frederickson R.M., Fields S., Patel A.H. Hepatitis C virus 3!X region interacts with human ribosomal proteins. J. Virol. 2001, 75:1348-1358.
117. Wu Y., Maruo S., Yajima M., Kanda T., Takada K. Epstein-Barr virus (EBV)-encoded RNA 2 (EBER2) but not EBER1 plays a critical role in EBV-induced B-cell growth transformation. J. Virol. 2007, 80:11236-11245.
118. Xia T., O'Hara A., Araujo I., Barreto J., Carvalho E., Sapucaia J.B., Ramos J.C., Luz E., Pedroso C., Manrique M., Toomey N.L., Brites C., Dittmer, Harrington D.P., WJ EBV microRNAs in primary lymphomas and targeting of CXCL-11 by ebv-mir-BHRF1-3. Cancer Res. 2008, 68:1436-1442.
119. Yajima M., Kanda T., Takada K. Critical role of Epstein-Barr Virus (EBV)-encoded RNA in efficient EBV-induced B-lymphocyte growth transformation. J. Virol. 2005, 79:4298-4307.
120. Yajima M., Imadome K., Nakagawa A., Watanabe S., Terashima K., Nakamura H., Ito M., Shimizu N., Honda M., Yamamoto N., Fujiwara S. A new humanized mouse model of Epstein-Barr virus infection that reproduces persistent infection, lymphoproliferative disorder, and cel-mediated and humoral immune responses. J. Infect. Dis. 2008, 198:673-682.
121. Yamamoto N., Takizawa T., Iwanaga Y., Shimizu N., Yamamoto N. Malignant transformation of B lymphoma cell line BJAB by Epstein-Barr virus-encoded small RNAs. FEBS Lett. 2000, 484:153-158.
122. Yang L., Aozasa K., Oshimi K., Takada K. Epstein-Barr virus (EBV)-encoded RNA promotes growth of EBV-infected T cells through interleukin-9 induction. Cancer Res. 2004, 64:5332-5337.
123. Yao Y., Minter H.A., Chen X., Reynolds G.M., Bromley M., Arrand J.R. Heterogeneity of HLA and EBER expression in Epstein-Barr virus-associated nasopharyngeal carcinoma. Int. J. Cancer 2000, 88:949-955.
124. Yoneyama M., Kikuchi M., Natsukawa T., Shinobu N., Imaizumi T., Miyagishi M., Taira K., Akira S., Fujita T. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol. 2004, 5:730-737.
125. Yoneyama M., Fujita T. Function of RIG-I-like receptors in antiviral innate immunity. J. Biol. Chem. 2007, 282:15315-15318.
126. Yoshizaki T., Endo K., Ren Q., Wakisaka N., Murono S., Kondo S., Sato H., Furukawa M. Oncogenic role of Epstein-Barr virus-encoded small RNAs (EBERs) in nasopharyngeal carcinoma. Auris. Nasus. Larynx 2007, 34:73-78.
127. Zeng Z., Huang H., Huang L., Sun M., Yan Q., Song Y., Wei F., Bo H., Gong Z., Zeng Y., Li Q., Zhang W., Li X., Xiang B., Li X., Li Y., Xiong W., Li G. Regulation network and expression profiles of Epstein-Barr virus-encoded microRNAs and their potential target host genes in nasopharyngeal carcinomas. Sci. China Life Sci. 2014, 57:315-326.
128. Zhu J.Y., Pfuhl T., Motsch N., Barth S., Nicholls J., Grasser F., Meister G. Identification of novel Epstein-Barr virus microRNA genes from nasopharyngeal carcinomas. J. Virol. 2009, 83:3333-3341.