EBV noncoding RNAs

Current Topics in Microbiology and Immunology

Volumn 391, Issue , 2015, Pages 181-217

  Skalsky, Rebecca L ^a   Cullen, Bryan R ^b  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BAMHI A RIGHTWARD TRANSCRIPTS; EPSTEIN BARR VIRUS ENCODED RNA 1; EPSTEIN BARR VIRUS ENCODED RNA 2; EPSTEIN BARR VIRUS STABLE INTRONIC SEQUENCE RNA 1; MICRORNA; MICRORNA 7/106/20/93; MICRORNA BART1 5P; MICRORNA BART10 3P; MICRORNA BART14; MICRORNA BART16; MICRORNA BART17 3P; MICRORNA BART17 5P; MICRORNA BART18 5P; MICRORNA BART19 3P; MICRORNA BART2 5P; MICRORNA BART20 5P; MICRORNA BART22; MICRORNA BART3 3P; MICRORNA BART3 5P; MICRORNA BART5 5P; MICRORNA BART6; MICRORNA BART6 5P; MICRORNA BART7; MICRORNA BART8; MICRORNA BHRF1 1; MICRORNA BHRF1 2; SMALL NUCLEOLAR RNA; UNCLASSIFIED DRUG; UNINDEXED DRUG; UNTRANSLATED RNA; VIRUS RNA;

APOPTOSIS; BIOGENESIS; EPSTEIN BARR VIRUS; EXOSOME; GENE EXPRESSION; GENE REGULATORY NETWORK; HIGH THROUGHPUT SEQUENCING OF RNA ISOLATED BY CROSS LINKING AND IMMUNOPRECIPITATION; HUMAN; IMMUNE EVASION; IMMUNOPRECIPITATION; NF KB SIGNALING; NONHUMAN; PHOTOACTIVATABLE RIBONUCLEOSIDE ENHANCED CROSS LINKING AND IMMUNOPRECIPITATION; PRIORITY JOURNAL; RISC IMMUNOPRECIPITATION FOLLOWED BY MICROARRAY BASED TRANSCRIPTOME PROFILING; RNA SEQUENCE; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; VIRUS LATENCY; VIRUS PATHOGENESIS; VIRUS TRANSCRIPTION; WNT SIGNALING PATHWAY; ANIMAL; CHEMISTRY; EPSTEIN BARR VIRUS INFECTION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; VIROLOGY;

ANIMALS; EPSTEIN-BARR VIRUS INFECTIONS; GENE EXPRESSION REGULATION, VIRAL; HERPESVIRUS 4, HUMAN; HUMANS; RNA, UNTRANSLATED; RNA, VIRAL;

EID: 84943328675     PISSN: 0070217X     EISSN: 21969965     Source Type: Book Series    
DOI: 10.1007/978-3-319-22834-1_6     Document Type: Chapter

References (162)

1. Adams BD, Kasinski AL, Slack FJ (2014) Aberrant regulation and function of MicroRNAs in cancer. Curr Biol 24:R762-R776
2. Al-Mozaini M, Bodelon G, Karstegl CE, Jin B, Al-Ahdal M, Farrell PJ (2009) Epstein-Barr virus BART gene expression. J Gen Virol 90:307-316
3. Ambros V (2004) The functions of animal microRNAs. Nature 431:350-355
4. Ambros V, Bartel B, Bartel DP, Burge CB, Carrington JC, Chen X, Dreyfuss G, Eddy SR, Griffiths-Jones S, Marshall M, Matzke M, Ruvkun G, Tuschl T (2003) A uniform system for microRNA annotation. RNA 9:277-279
5. 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
6. Andersson MG, Haasnoot PC, Xu N, Berenjian S, Berkhout B, Akusjarvi G (2005) Suppression of RNA interference by adenovirus virus-associated RNA. J Virol 79:9556-9565
7. Aparicio O, Razquin N, Zaratiegui M, Narvaiza I, Fortes P (2006) Adenovirus virus-associated RNA is processed to functional interfering RNAs involved in virus production. J Virol 80:1376-1384
8. Aswad A, Katzourakis A (2014) The first endogenous herpesvirus, identified in the tarsier genome, and novel sequences from primate rhadinoviruses and lymphocryptoviruses. PLoS Genet 10:e1004332
9. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281-297
10. Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136:215-233
11. Barth S, Pfuhl T, Mamiani A, Ehses C, Roemer K, Kremmer E, Jaker C, Hock J, Meister G, Grasser FA (2008) Epstein-Barr virus-encoded microRNA miR-BART2 down-regulates the viral DNA polymerase BALF5. Nucleic Acids Res 36:666-675
12. Barth S, Meister G, Grasser FA (2011) EBV-encoded miRNAs. Biochim Biophys Acta 1809:631-640
13. Bhat RA, Thimmappaya B (1983) 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 USA 80:4789-4793
14. Bloom DC (2004) HSV LAT and neuronal survival. Int Rev Immunol 23:187-198
15. Boss IW, Nadeau PE, Abbott JR, Yang Y, Mergia A, Renne R (2011) A Kaposi's sarcoma-associated herpesvirus-encoded ortholog of microRNA miR-155 induces human splenic B-cell expansion in NOD/LtSz-scid IL2Rgammanull mice. J Virol 85:9877-9886
16. Bracken CP, Li X, Wright JA, Lawrence D, Pillman KA, Salmanidis M, Anderson MA, Dredge BK, Gregory PA, Tsykin A, Neilsen C, Thomson DW, Bert AG, Leerberg JM, Yap AS, Jensen KB, Khew-Goodall Y, Goodall GJ (2014) Genome-wide identification of miR-200 targets reveals a regulatory network controlling cell invasion. EMBO J 33:2040-2056
17. Burk U, Schubert J, Wellner U, Schmalhofer O, Vincan E, Spaderna S, Brabletz T (2008) A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells. EMBO Rep 9:582-589
18. Cahir-Mcfarland ED, Carter K, Rosenwald A, Giltnane JM, Henrickson SE, Staudt LM, Kieff E (2004) Role of NF-kappa B in cell survival and transcription of latent membrane protein 1-expressing or Epstein-Barr virus latency III-infected cells. J Virol 78:4108-4119
19. 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
20. Cai L, Ye Y, Jiang Q, Chen Y, Lyu X, Li J, Wang S, Liu T, Cai H, Yao K, Li JL, Li X (2015) Epstein-Barr virus-encoded microRNA BART1 induces tumour metastasis by regulating PTEN-dependent pathways in nasopharyngeal carcinoma. Nat Commun 6:7353
21. Calado DP, Sasaki Y, Godinho SA, Pellerin A, Kochert K, Sleckman BP, de Alboran IM, Janz M, Rodig S, Rajewsky K (2012) The cell-cycle regulator c-Myc is essential for the formation and maintenance of germinal centers. Nat Immunol 13:1092-1100
22. Cameron JE, Fewell C, Yin Q, McBride J, Wang X, Lin Z, Flemington EK (2008a) Epstein-Barr virus growth/latency III program alters cellular microRNA expression. Virology 382:257-266
23. Cameron JE, Yin Q, Fewell C, Lacey M, McBride J, Wang X, Lin Z, Schaefer BC, Flemington EK (2008b) Epstein-Barr virus latent membrane protein 1 induces cellular MicroRNA miR-146a, a modulator of lymphocyte signaling pathways. J Virol 82:1946-1958
24. Carthew RW, Sontheimer EJ (2009) Origins and mechanisms of miRNAs and siRNAs. Cell 136:642-655
25. Chen H, Huang J, Wu FY, Liao G, Hutt-Fletcher L, Hayward SD (2005) Regulation of expression of the Epstein-Barr virus BamHI-A rightward transcripts. J Virol 79:1724-1733
26. Chen SJ, Chen GH, Chen YH, Liu CY, Chang KP, Chang YS, Chen HC (2010) Characterization of Epstein-Barr virus miRNAome in nasopharyngeal carcinoma by deep sequencing. PLoS One 5:e12745
27. Chi SW, Zang JB, Mele A, Darnell RB (2009) Argonaute HITS-CLIP decodes microRNAmRNA interaction maps. Nature 460:479-486
28. Choy EY, Siu KL, Kok KH, Lung RW, Tsang CM, To KF, Kwong DL, Tsao SW, Jin DY (2008) An Epstein-Barr virus-encoded microRNA targets PUMA to promote host cell survival. J Exp Med 205:2551-2560
29. 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
30. Concha M, Wang X, Cao S, Baddoo M, Fewell C, Lin Z, Hulme W, Hedges D, McBride J, Flemington EK (2012) Identification of new viral genes and transcript isoforms during Epstein-Barr virus reactivation using RNA-Seq. J Virol 86:1458-1467
31. Corcoran DL, Georgiev S, Mukherjee N, Gottwein E, Skalsky RL, Keene JD, Ohler U (2011) PARalyzer: definition of RNA binding sites from PAR-CLIP short-read sequence data. Genome Biol 12:R79
32. deJesus O, Smith PR, Spender LC, Elgueta Karstegl C, Niller HH, Huang D, Farrell PJ (2003) Updated Epstein-Barr virus (EBV) DNA sequence and analysis of a promoter for the BART (CST, BARF0) RNAs of EBV. J Gen Virol 84:1443-1450
33. Ding Y, Xi Y, Chen T, Wang JY, Tao DL, Wu ZL, Li YP, Li C, Zeng R, Li L (2008) Caprin-2 enhances canonical Wnt signaling through regulating LRP5/6 phosphorylation. J Cell Biol 182:865-872
34. Dolken L, Malterer G, Erhard F, Kothe S, Friedel CC, Suffert G, Marcinowski L, Motsch N, Barth S, Beitzinger M, Lieber D, Bailer SM, Hoffmann R, Ruzsics Z, Kremmer E, Pfeffer S, Zimmer R, Koszinowski UH, Grasser F, Meister G, Haas J (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
35. Dominguez-Sola D, Victora GD, Ying CY, Phan RT, Saito M, Nussenzweig MC, Dalla-Favera R (2012) The proto-oncogene MYC is required for selection in the germinal center and cyclic reentry. Nat Immunol 13:1083-1091
36. Edwards RH, Marquitz AR, Raab-Traub N (2008) Epstein-Barr virus BART microRNAs are produced from a large intron prior to splicing. J Virol 82:9094-9106
37. Ellis-Connell AL, Iempridee T, Xu I, Mertz JE (2010) Cellular microRNAs 200b and 429 regulate the Epstein-Barr virus switch between latency and lytic replication. J Virol 84:10329-10343
38. Faumont N, Durand-Panteix S, Schlee M, Gromminger S, Schuhmacher M, Holzel M, Laux G, Mailhammer R, Rosenwald A, Staudt LM, Bornkamm GW, Feuillard J (2009) c-Myc and Rel/NF-kappaB are the two master transcriptional systems activated in the latency III program of Epstein-Barr virus-immortalized B cells. J Virol 83:5014-5027
39. Feederle R, Haar J, Bernhardt K, Linnstaedt SD, Bannert H, Lips H, Cullen BR, Delecluse HJ (2011a) The members of a viral miRNA cluster co-operate to transform B lymphocytes. J Virol 85:9801-9810
40. Feederle R, Linnstaedt SD, Bannert H, Lips H, Bencun M, Cullen BR, Delecluse HJ (2011b) A viral microRNA cluster strongly potentiates the transforming properties of a human herpesvirus. PLoS Pathog 7:e1001294
41. Fok V, Friend K, Steitz JA (2006a) Epstein-Barr virus noncoding RNAs are confined to the nucleus, whereas their partner, the human La protein, undergoes nucleocytoplasmic shuttling. J Cell Biol 173:319-325
42. Fok V, Mitton-Fry RM, Grech A, Steitz JA (2006b) Multiple domains of EBER 1, an Epstein-Barr virus noncoding RNA, recruit human ribosomal protein L22. RNA 12:872-882
43. Forte E, Luftig MA (2011) The role of microRNAs in Epstein-Barr virus latency and lytic reactivation. Microbes Infect 13:1156-1167
44. Friedman RC, Farh KK, Burge CB, Bartel DP (2009) Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19:92-105
45. Furuse Y, Ornelles DA, Cullen BR (2013) Persistently adenovirus-infected lymphoid cells express microRNAs derived from the viral VAI and especially VAII RNA. Virology 447:140-145
46. Gardner EJ, Nizami ZF, Talbot CC Jr, Gall JG (2012) Stable intronic sequence RNA (sisRNA), a new class of noncoding RNA from the oocyte nucleus of Xenopus tropicalis. Genes Dev 26:2550-2559
47. Germain C, Meier A, Jensen T, Knapnougel P, Poupon G, Lazzari A, Neisig A, Hakansson K, Dong T, Wagtmann N, Galsgaard ED, Spee P, Braud VM (2011) Induction of lectin-like transcript 1 (LLT1) protein cell surface expression by pathogens and interferon-gamma contributes to modulate immune responses. J Biol Chem 286:37964-37975
48. Gilligan K, Sato H, Rajadurai P, Busson P, Young L, Rickinson A, Tursz T, Raab-Traub N (1990) Novel transcription from the Epstein-Barr virus terminal EcoRI fragment, DIJhet, in a nasopharyngeal carcinoma. J Virol 64:4948-4956
49. Gilligan KJ, Rajadurai P, Lin JC, Busson P, Abdel-Hamid M, Prasad U, Tursz T, Raab-Traub N (1991) Expression of the Epstein-Barr virus BamHI A fragment in nasopharyngeal carcinoma: evidence for a viral protein expressed in vivo. J Virol 65:6252-6259
50. Goto M, Murakawa M, Kadoshima-Yamaoka K, Tanaka Y, Inoue H, Murafuji H, Hayashi Y, Miura K, Nakatsuka T, Nagahira K, Chamoto K, Fukuda Y, Nishimura T (2009) Phosphodiesterase 7A inhibitor ASB16165 suppresses proliferation and cytokine production of NKT cells. Cell Immunol 258:147-151
51. Gottwein E, Cai X, Cullen BR (2006) A novel assay for viral microRNA function identifies a single nucleotide polymorphism that affects Drosha processing. J Virol 80:5321-5326
52. Gottwein E, Mukherjee N, Sachse C, Frenzel C, Majoros WH, Chi JT, Braich R, Manoharan M, Soutschek J, Ohler U, Cullen BR (2007) A viral microRNA functions as an orthologue of cellular miR-155. Nature 450:1096-1099
53. Gottwein E, Corcoran DL, Mukherjee N, Skalsky RL, Hafner M, Nusbaum JD, Shamulailatpam P, Love CL, Dave SS, Tuschl T, Ohler U, Cullen BR (2011) Viral microRNA targetome of KSHV-infected primary effusion lymphoma cell lines. Cell Host Microbe 10:515-526
54. Gourzones C, Gelin A, Bombik I, Klibi J, Verillaud B, Guigay J, Lang P, Temam S, Schneider V, Amiel C, Baconnais S, Jimenez AS, Busson P (2010) Extra-cellular release and blood diffusion of BART viral micro-RNAs produced by EBV-infected nasopharyngeal carcinoma cells. Virol J 7:271
55. Gregorovic G, Bosshard R, Karstegl CE, White RE, Pattle S, Chiang AK, Dittrich-Breiholz O, Kracht M, Russ R, Farrell PJ (2011) Cellular gene expression that correlates with EBER expression in Epstein-Barr Virus-infected lymphoblastoid cell lines. J Virol 85:3535-3545
56. Grosswendt S, Filipchyk A, Manzano M, Klironomos F, Schilling M, Herzog M, Gottwein E, Rajewsky N (2014) Unambiguous identification of miRNA:target site interactions by different types of ligation reactions. Mol Cell 54:1042-1054
57. 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
58. Gurer C, Strowig T, Brilot F, Pack M, Trumpfheller C, Arrey F, Park CG, Steinman RM, Munz C (2008) Targeting the nuclear antigen 1 of Epstein-Barr virus to the human endocytic receptor DEC-205 stimulates protective T-cell responses. Blood 112:1231-1239
59. Haecker I, Gay LA, Yang Y, Hu J, Morse AM, McIntyre LM, Renne R (2012) Ago HITS-CLIP expands understanding of Kaposi's Sarcoma-associated herpesvirus miRNA function in primary effusion lymphomas. PLoS Pathog 8:e1002884
60. Hafner M, Landthaler M, Burger L, Khorshid M, Hausser J, Berninger P, Rothballer A, Ascano M Jr, Jungkamp AC, Munschauer M, Ulrich A, Wardle GS, Dewell S, Zavolan M, Tuschl T (2010) Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell 141:129-141
61. 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
62. Hitt MM, Allday MJ, Hara T, Karran L, Jones MD, Busson P, Tursz T, Ernberg I, Griffin BE (1989) EBV gene expression in an NPC-related tumour. EMBO J 8:2639-2651
63. Howe JG, Shu MD (1989) Epstein-Barr virus small RNA (EBER) genes: unique transcription units that combine RNA polymerase II and III promoter elements. Cell 57:825-834
64. Hsu CY, Yi YH, Chang KP, Chang YS, Chen SJ, Chen HC (2014) The Epstein-Barr virusencoded microRNA MiR-BART9 promotes tumor metastasis by targeting E-cadherin in nasopharyngeal carcinoma. PLoS Pathog 10:e1003974
65. Hutzinger R, Feederle R, Mrazek J, Schiefermeier N, Balwierz PJ, Zavolan M, Polacek N, Delecluse HJ, Huttenhofer A (2009) Expression and processing of a small nucleolar RNA from the Epstein-Barr virus genome. PLoS Pathog 5:e1000547
66. Iizasa H, Wulff BE, Alla NR, Maragkakis M, Megraw M, Hatzigeorgiou A, Iwakiri D, Takada K, Wiedmer A, Showe L, Lieberman P, Nishikura K (2010) Editing of EBV-encoded BART6 microRNAs controls their dicer targeting and consequently affects viral latency. J Biol Chem 285:33358-33370
67. Imig J, Motsch N, Zhu JY, Barth S, Okoniewski M, Reineke T, Tinguely M, Faggioni A, Trivedi P, Meister G, Renner C, Grasser FA (2011) microRNA profiling in Epstein-Barr virus-associated B-cell lymphoma. Nucleic Acids Res 39:1880-1893
68. Jin HY, Oda H, Lai M, Skalsky RL, Bethel K, Shepherd J, Kang SG, Liu WH, Sabouri-Ghomi M, Cullen BR, Rajewsky K, Xiao C (2013) MicroRNA-17 ~ 92 plays a causative role in lymphomagenesis by coordinating multiple oncogenic pathways. EMBO J 32:2377-2391
69. Jung YJ, Choi H, Kim H, Lee SK (2014) MicroRNA miR-BART20-5p stabilizes Epstein-Barr virus latency by directly targeting BZLF1 and BRLF1. J Virol 88:9027-9037
70. Kang D, Skalsky RL, Cullen BR (2015) EBV BART MicroRNAs target multiple pro-apoptotic cellular genes to promote epithelial cell survival. PLos Path 11:e1004979
71. Karran L, Gao Y, Smith PR, Griffin BE (1992) Expression of a family of complementary-strand transcripts in Epstein-Barr virus-infected cells. Proc Natl Acad Sci USA 89:8058-8062
72. Kieff E (2007) Epstein-Barr virus and its replication. In: Knipe DMaH PM (ed) Fields virology, 5 edn
73. Kienzle N, Sculley TB, Poulsen L, Buck M, Cross S, Raab-Traub N, Khanna R (1998) Identification of a cytotoxic T-lymphocyte response to the novel BARF0 protein of Epstein-Barr virus: a critical role for antigen expression. J Virol 72:6614-6620
74. Kienzle N, Buck M, Greco S, Krauer K, Sculley TB (1999) Epstein-Barr virus-encoded RKBARF0 protein expression. J Virol 73:8902-8906
75. Kim Do N, Song YJ, Lee SK (2011) The role of promoter methylation in Epstein-Barr virus (EBV) microRNA expression in EBV-infected B cell lines. Exp Mol Med 43:401-410
76. Kulesza CA, Shenk T (2004) Human cytomegalovirus 5-kilobase immediate-early RNA is a stable intron. J Virol 78:13182-13189
77. Kulesza CA, Shenk T (2006) Murine cytomegalovirus encodes a stable intron that facilitates persistent replication in the mouse. Proc Natl Acad Sci USA 103:18302-18307
78. Lee N, Pimienta G, Steitz JA (2012) AUF1/hnRNP D is a novel protein partner of the EBER1 noncoding RNA of Epstein-Barr virus. RNA 18:2073-2082
79. Lee N, Moss WN, Yario TA, Steitz JA (2015) EBV noncoding RNA binds nascent RNA to drive host PAX5 to viral DNA. Cell 160:607-618
80. Lei X, Bai Z, Ye F, Xie J, Kim CG, Huang Y, Gao SJ (2010) Regulation of NF-kappaB inhibitor IkappaBalpha and viral replication by a KSHV microRNA. Nat Cell Biol 12:193-199
81. Lei T, Yuen KS, Xu R, Tsao SW, Chen H, Li M, Kok KH, Jin DY (2013) Targeting of DICE1 tumor suppressor by Epstein-Barr virus-encoded miR-BART3 * microRNA in nasopharyngeal carcinoma. Int J Cancer 133:79-87
82. 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 78:805-809
83. Lewis BP, Burge CB, Bartel DP (2005) Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120:15-20
84. Lin Z, Wang X, Fewell C, Cameron J, Yin Q, Flemington EK (2010) Differential expression of the miR-200 family microRNAs in epithelial and B cells and regulation of Epstein-Barr virus reactivation by the miR-200 family member miR-429. J Virol 84:7892-7897
85. Lin TC, Liu TY, Hsu SM, Lin CW (2013a) 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
86. Lin Z, Wang X, Strong MJ, Concha M, Baddoo M, Xu G, Baribault C, Fewell C, Hulme W, Hedges D, Taylor CM, Flemington EK (2013b) Whole-genome sequencing of the Akata and Mutu Epstein-Barr virus strains. J Virol 87:1172-1182
87. Linnstaedt SD, Gottwein E, Skalsky RL, Luftig MA, Cullen BR (2010) Virally induced cellular miR-155 plays a key role in B-cell immortalization by EBV. J Virol 84:11670-11678
88. Lo AK, To KF, Lo KW, Lung RW, Hui JW, Liao G, Hayward SD (2007) Modulation of LMP1 protein expression by EBV-encoded microRNAs. Proc Natl Acad Sci USA 104:16164-16169
89. Lo AK, Dawson CW, Jin DY, Lo KW (2012) The pathological roles of BART miRNAs in nasopharyngeal carcinoma. J Pathol 227:392-403
90. Lu S, Cullen BR (2004) Adenovirus VA1 noncoding RNA can inhibit small interfering RNA and MicroRNA biogenesis. J Virol 78:12868-12876
91. Luftig M, Prinarakis E, Yasui T, Tsichritzis T, Cahir-Mcfarland E, Inoue J, Nakano H, Mak TW, Yeh WC, Li X, Akira S, Suzuki N, Suzuki S, Mosialos G, Kieff E (2003) Epstein-Barr virus latent membrane protein 1 activation of NF-kappaB through IRAK1 and TRAF6. Proc Natl Acad Sci USA 100:15595-15600
92. Lukas J, Mazna P, Valenta T, Doubravska L, Pospichalova V, Vojtechova M, Fafilek B, Ivanek R, Plachy J, Novak J, Korinek V (2009) Dazap2 modulates transcription driven by the Wnt effector TCF-4. Nucleic Acids Res 37:3007-3020
93. Lung RW, Tong JH, Sung YM, Leung PS, Ng DC, Chau SL, Chan AW, Ng EK, Lo KW, To KF (2009) Modulation of LMP2A expression by a newly identified Epstein-Barr virus-encoded microRNA miR-BART22. Neoplasia 11:1174-1184
94. Lung RW, Tong JH, To KF (2013) Emerging roles of small Epstein-Barr virus derived non-coding RNAs in epithelial malignancy. Int J Mol Sci 14:17378-17409
95. Majoros WH, Lekprasert P, Mukherjee N, Skalsky RL, Corcoran DL, Cullen BR, Ohler U (2013) MicroRNA target site identification by integrating sequence and binding information. Nat Methods 10:630-633
96. Marquitz AR, Raab-Traub N (2012) The role of miRNAs and EBV BARTs in NPC. Semin Cancer Biol 22:166-172
97. Marquitz AR, Mathur A, Nam CS, Raab-Traub N (2011) The Epstein-Barr Virus BART microRNAs target the pro-apoptotic protein Bim. Virology 412:392-400
98. Marquitz AR, Mathur A, Shair KH, Raab-Traub N (2012) Infection of Epstein-Barr virus in a gastric carcinoma cell line induces anchorage independence and global changes in gene expression. Proc Natl Acad Sci USA
99. Marquitz AR, Mathur A, Chugh PE, Dittmer DP, Raab-Traub N (2014) Expression profile of microRNAs in Epstein-Barr virus-infected AGS gastric carcinoma cells. J Virol 88:1389-1393
100. 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
101. Michaeli T, Pan ZQ, Prives C (1988) An excised SV40 intron accumulates and is stable in Xenopus laevis oocytes. Genes Dev 2:1012-1020
102. Moody R, Zhu Y, Huang Y, Cui X, Jones T, Bedolla R, Lei X, Bai Z, Gao SJ (2013) KSHV microRNAs mediate cellular transformation and tumorigenesis by redundantly targeting cell growth and survival pathways. PLoS Pathog 9:e1003857
103. Moss WN, Steitz JA (2013) Genome-wide analyses of Epstein-Barr virus reveal conserved RNA structures and a novel stable intronic sequence RNA. BMC Genom 14:543
104. Moynagh PN (2009) The Pellino family: IRAK E3 ligases with emerging roles in innate immune signalling. Trends Immunol 30:33-42
105. Mullokandov G, Baccarini A, Ruzo A, Jayaprakash AD, Tung N, Israelow B, Evans MJ, Sachidanandam R, Brown BD (2012) High-throughput assessment of microRNA activity and function using microRNA sensor and decoy libraries. Nat Methods 9:840-846
106. 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
107. 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
108. Nikitin PA, Yan CM, Forte E, Bocedi A, Tourigny JP, White RE, Allday MJ, Patel A, Dave SS, Kim W, Hu K, Guo J, Tainter D, Rusyn E, Luftig MA (2010) An ATM/Chk2-mediated DNA damage-responsive signaling pathway suppresses Epstein-Barr virus transformation of primary human B cells. Cell Host Microbe 8:510-522
109. O'Grady T, Cao S, Strong MJ, Concha M, Wang X, Splinter Bondurant S, Adams M, Baddoo M, Srivastav SK, Lin Z, Fewell C, Yin Q, Flemington EK (2014) Global bidirectional transcription of the Epstein-Barr virus genome during reactivation. J Virol 88:1604-1616
110. Parnas O, Corcoran DL, Cullen BR (2014) Analysis of the mRNA targetome of microRNAs expressed by Marek's disease virus. MBio 5:e01060-13
111. 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 107:6328-6333
112. Pekarsky Y, Croce CM (2010) Is miR-29 an oncogene or tumor suppressor in CLL? Oncotarget 1:224-227
113. Pfeffer S, Zavolan M, Grasser FA, Chien M, Russo JJ, Ju J, John B, Enright AJ, Marks D, Sander C, Tuschl T (2004) Identification of virus-encoded microRNAs. Science 304:734-736
114. Pillai RS, Bhattacharyya SN, Filipowicz W (2007) Repression of protein synthesis by miRNAs: how many mechanisms? Trends Cell Biol 17:118-126
115. Pratt ZL, Kuzembayeva M, Sengupta S, Sugden B (2009) The microRNAs of Epstein-Barr virus are expressed at dramatically differing levels among cell lines. Virology 386:387-397
116. Pratt ZL, Zhang J, Sugden B (2012) The latent membrane protein 1 (LMP1) oncogene of Epstein-Barr virus can simultaneously induce and inhibit apoptosis in B cells. J Virol 86:4380-4393
117. Price AM, Tourigny JP, Forte E, Salinas RE, Dave SS, Luftig MA (2012) Analysis of Epstein-Barr virus-regulated host gene expression changes through primary B-cell outgrowth reveals delayed kinetics of latent membrane protein 1-mediated NF-kappaB activation. J Virol 86:11096-11106
118. 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 111:11157-11162
119. 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
120. Ramachandran I, Ganapathy V, Gillies E, Fonseca I, Sureban SM, Houchen CW, Reis A, Queimado L (2014) Wnt inhibitory factor 1 suppresses cancer stemness and induces cellular senescence. Cell Death Dis 5:e1246
121. Rechavi O, Erlich Y, Amram H, Flomenblit L, Karginov FV, Goldstein I, Hannon GJ, Kloog Y (2009) Cell contact-dependent acquisition of cellular and viral nonautonomously encoded small RNAs. Genes Dev 23:1971-1979
122. Repellin CE, Tsimbouri PM, Philbey AW, Wilson JB (2010) Lymphoid hyperplasia and lymphoma in transgenic mice expressing the small non-coding RNA, EBER1 of Epstein-Barr virus. PLoS ONE 5:e9092
123. Riley KJ, Rabinowitz GS, Steitz JA (2010) Comprehensive analysis of Rhesus lymphocryptovirus microRNA expression. J Virol 84:5148-5157
124. 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
125. Robertson ES, Tomkinson B, Kieff E (1994) An Epstein-Barr virus with a 58-kilobase-pair deletion that includes BARF0 transforms B lymphocytes in vitro. J Virol 68:1449-1458
126. Rodriguez A, Vigorito E, Clare S, Warren MV, Couttet P, Soond DR, van Dongen S, Grocock RJ, Das PP, Miska EA, Vetrie D, Okkenhaug K, Enright AJ, Dougan G, Turner M, Bradley A (2007) Requirement of bic/microRNA-155 for normal immune function. Science 316:608-611
127. 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
128. 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 25:4207-4214
129. Sano M, Kato Y, Taira K (2006) Sequence-specific interference by small RNAs derived from adenovirus VAI RNA. FEBS Lett 580:1553-1564
130. 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
131. Shinozaki A, Sakatani T, Ushiku T, Hino R, Isogai M, Ishikawa S, Uozaki H, Takada K, Fukayama M (2010) Downregulation of microRNA-200 in EBV-associated gastric carcinoma. Cancer Res 70:4719-4727
132. Skalsky RL, Cullen BR (2010) Viruses, microRNAs, and host interactions. Annu Rev Microbiol 64:123-141
133. Skalsky RL, Hu J, Renne R (2007a) Analysis of viral cis elements conferring Kaposi's sarcomaassociated herpesvirus episome partitioning and maintenance. J Virol 81:9825-9837
134. Skalsky RL, Samols MA, Plaisance KB, Boss IW, Riva A, Lopez MC, Baker HV, Renne R (2007b) Kaposi's sarcoma-associated herpesvirus encodes an ortholog of miR-155. J Virol 81:12836-12845
135. Skalsky RL, Corcoran DL, Gottwein E, Frank CL, Kang D, Hafner M, Nusbaum JD, Feederle R, Delecluse HJ, Luftig MA, Tuschl T, Ohler U, Cullen BR (2012) The viral and cellular microRNA targetome in lymphoblastoid cell lines. PLoS Pathog 8:e1002484
136. Skalsky RL, Kang D, Linnstaedt SD, Cullen BR (2014) Evolutionary conservation of primate lymphocryptovirus microRNA targets. J Virol 88:1617-1635
137. Smith PR, de Jesus O, Turner D, Hollyoake M, Karstegl CE, Griffin BE, Karran L, Wang Y, Hayward SD, Farrell PJ (2000) Structure and coding content of CST (BART) family RNAs of Epstein-Barr virus. J Virol 74:3082-3092
138. Soni V, Cahir-Mcfarland E, Kieff E (2007) LMP1 TRAFficking activates growth and survival pathways. Adv Exp Med Biol 597:173-187
139. Swaminathan S, Tomkinson B, Kieff E (1991) Recombinant Epstein-Barr virus with small RNA (EBER) genes deleted transforms lymphocytes and replicates in vitro. Proc Natl Acad Sci USA 88:1546-1550
140. Talhouarne GJ, Gall JG (2014) Lariat intronic RNAs in the cytoplasm of Xenopus tropicalis oocytes. RNA 20:1476-1487
141. Tavalai N, Stamminger T (2009) Interplay between herpesvirus infection and host defense by PML nuclear bodies. Viruses 1:1240-1264
142. Thai TH, Calado DP, Casola S, Ansel KM, Xiao C, Xue Y, Murphy A, Frendewey D, Valenzuela D, Kutok JL, Schmidt-Supprian M, Rajewsky N, Yancopoulos G, Rao A, Rajewsky K (2007) Regulation of the germinal center response by microRNA-155. Science 316:604-608
143. Toczyski DP, Matera AG, Ward DC, Steitz JA (1994) The Epstein-Barr virus (EBV) small RNA EBER1 binds and relocalizes ribosomal protein L22 in EBV-infected human B lymphocytes. Proc Natl Acad Sci USA 91:3463-3467
144. Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO (2007) Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9:654-659
145. 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
146. 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
147. Walsh KB, Marsolais D, Welch MJ, Rosen H, Oldstone MB (2010) Treatment with a sphingosine analog does not alter the outcome of a persistent virus infection. Virology 397:260-269
148. Walz N, Christalla T, Tessmer U, Grundhoff A (2009) A global analysis of evolutionary conservation among known and predicted gammaherpesvirus microRNAs. J Virol 84:716-728
149. White EJ, Brewer G, Wilson GM (2013) Post-transcriptional control of gene expression by AUF1: mechanisms, physiological targets, and regulation. Biochim Biophys Acta 1829:680-688
150. Wong AM, Kong KL, Tsang JW, Kwong DL, Guan XY (2012) Profiling of Epstein-Barr virusencoded microRNAs in nasopharyngeal carcinoma reveals potential biomarkers and oncomirs. Cancer 118:698-710
151. Wu Y, Maruo S, Yajima M, Kanda T, Takada K (2007) Epstein-Barr virus (EBV)-encoded RNA 2 (EBER2) but not EBER1 plays a critical role in EBV-induced B-cell growth transformation. J Virol 81:11236-11245
152. Xia T, O'Hara A, Araujo I, Barreto J, Carvalho E, Sapucaia JB, Ramos JC, Luz E, Pedroso C, Manrique M, Toomey NL, Brites C, Dittmer DP, Harrington WJ Jr (2008) EBV microRNAs in primary lymphomas and targeting of CXCL-11 by ebv-mir-BHRF1-3. Cancer Res 68:1436-1442
153. Xiao C, Rajewsky K (2009) MicroRNA control in the immune system: basic principles. Cell 136:26-36
154. Xing L, Kieff E (2007) Epstein-Barr virus BHRF1 micro-and stable RNAs during latency III and after induction of replication. J Virol 81:9967-9975
155. Xing L, Kieff E (2011) cis-Acting effects on RNA processing and Drosha cleavage prevent Epstein-Barr virus latency III BHRF1 expression. J Virol 85:8929-8939
156. Yajima M, Kanda T, Takada K (2005) Critical role of Epstein-Barr Virus (EBV)-encoded RNA in efficient EBV-induced B-lymphocyte growth transformation. J Virol 79:4298-4307
157. Yang J, Yuan YA (2009) A structural perspective of the protein-RNA interactions involved in virus-induced RNA silencing and its suppression. Biochim Biophys Acta 1789:642-652
158. Yao Y, Zhao Y, Xu H, Smith LP, Lawrie CH, Watson M, Nair V (2008) MicroRNA profile of Marek's disease virus-transformed T-cell line MSB-1: predominance of virus-encoded microRNAs. J Virol 82:4007-4015
159. Young LS, Rickinson AB (2004) Epstein-Barr virus: 40 years on. Nat Rev Cancer 4:757-768
160. Zhang J, Chen H, Weinmaster G, Hayward SD (2001) Epstein-Barr virus BamHi-a rightward transcript-encoded RPMS protein interacts with the CBF1-associated corepressor CIR to negatively regulate the activity of EBNA2 and NotchIC. J Virol 75:2946-2956
161. Zhao Y, Xu H, Yao Y, Smith LP, Kgosana L, Green J, Petherbridge L, Baigent SJ, Nair V (2011) Critical role of the virus-encoded microRNA-155 ortholog in the induction of Marek's disease lymphomas. PLoS Pathog 7:e1001305
162. 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