Virus-encoded microRNAs

Virology

Volumn 411, Issue 2, 2011, Pages 325-343

  Grundhoff, Adam ^a   Sullivan, Christopher S ^b  

^a LEIBNIZ INSTITUTE FOR EXPERIMENTAL VIROLOGY   (Germany)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

BKV; EBV; HCMV; Herpesvirus; JCV; KSHV; MicroRNA; MiRNA; Polyomavirus; SV40

Indexed keywords

BCL2 ASSOCIATED FACTOR; COMPLEMENTARY RNA; CYTOKINE; MICRORNA; PROTEIN BCL 2; SMAD2 PROTEIN; THROMBOSPONDIN; TNF LIKE WEAK INDUCER OF APOPTOSIS RECEPTOR; UNCLASSIFIED DRUG; VIRUS RNA;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; AUTOREGULATION; BIOGENESIS; BIOINFORMATICS; DNA FINGERPRINTING; EPSTEIN BARR VIRUS; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; HERPES SIMPLEX VIRUS 1; HOST RESISTANCE; HUMAN HERPESVIRUS 8; IMMUNE EVASION; LATENT VIRUS INFECTION; MARDIVIRUS; MATHEMATICAL COMPUTING; NONHUMAN; PERSISTENT VIRUS INFECTION; PREDICTION; PRIORITY JOURNAL; REVIEW; RNA PROCESSING; VIRION; VIRUS CARCINOGENESIS; VIRUS CELL INTERACTION; VIRUS GENOME;

GENE EXPRESSION REGULATION, VIRAL; HUMANS; MICRORNAS; RNA, VIRAL; VIRUSES;

BK POLYOMAVIRUS; HERPESVIRIDAE; HUMAN HERPESVIRUS 4; HUMAN HERPESVIRUS 8; POLYOMAVIRUS;

EID: 79952070466     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2011.01.002     Document Type: Review

References (125)

1. Abend J.R., Uldrick T., Ziegelbauer J.M. Regulation of TWEAKR expression by KSHV microRNA prevents TWEAK-induced apoptosis and inflammatory cytokine expression. J. Virol. 2010, 84(23):12139-12151.
2. Andersson M.G., Haasnoot P.C., Xu N., Berenjian S., Berkhout B., Akusjarvi G. Suppression of RNA interference by adenovirus virus-associated RNA. J. Virol. 2005, 79:9556-9565.
3. Aparicio O., Razquin N., Zaratiegui M., Narvaiza I., Fortes P. Adenovirus virus-associated RNA is processed to functional interfering RNAs involved in virus production. J. Virol. 2006, 80:1376-1384.
4. Bartel D.P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004, 116:281-297.
5. Bartel D.P. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136:215-233.
6. Barth S., Pfuhl T., Mamiani A., Ehses C., Roemer K., Kremmer E., Jaker C., Hock J., Meister G., Grasser F.A. Epstein-Barr virus-encoded microRNA miR-BART2 down-regulates the viral DNA polymerase BALF5. Nucleic Acids Res. 2008, 36:666-675.
7. 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.
8. Bernstein E., Caudy A.A., Hammond S.M., Hannon G.J. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 2001, 409:363-366.
9. Bornkamm G.W. Epstein-Barr virus and its role in the pathogenesis of Burkitt's lymphoma: an unresolved issue. Semin. Cancer Biol. 2009, 19:351-365.
10. Buck A.H., Santoyo-Lopez J., Robertson K.A., Kumar D.S., Reczko M., Ghazal P. Discrete clusters of virus-encoded micrornas are associated with complementary strands of the genome and the 7.2-kilobase stable intron in murine cytomegalovirus. J. Virol. 2007, 81:13761-13770.
11. Cai X., Lu S., Zhang Z., Gonzalez C.M., Damania B., Cullen B.R. Kaposi's sarcoma-associated herpesvirus expresses an array of viral microRNAs in latently infected cells. Proc. Natl Acad. Sci. USA 2005, 102:5570-5575. (Epub 2005 Mar 5530).
12. Cai X., Li G., Laimins L.A., Cullen B.R. Human papillomavirus genotype 31 does not express detectable microRNA levels during latent or productive virus replication. J. Virol. 2006, 80:10890-10893.
13. 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.
14. Cantalupo P., Doering A., Sullivan C.S., Pal A., Peden K.W., Lewis A.M., Pipas J.M. Complete nucleotide sequence of polyomavirus SA12. J. Virol. 2005, 79:13094-13104.
15. Carroll P.A., Brazeau E., Lagunoff M. Kaposi's sarcoma-associated herpesvirus infection of blood endothelial cells induces lymphatic differentiation. Virology 2004, 328:7-18.
16. Carthew R.W., Sontheimer E.J. Origins and mechanisms of miRNAs and siRNAs. Cell 2009, 136:642-655.
17. Chandriani S., Xu Y., Ganem D. The lytic transcriptome of Kaposi's sarcoma-associated herpesvirus reveals extensive transcription of noncoding regions, including regions antisense to important genes. J. Virol. 2010, 84:7934-7942.
18. 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.
19. 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.
20. Clurman B.E., Hayward W.S. Multiple proto-oncogene activations in avian leukosis virus-induced lymphomas: evidence for stage-specific events. Mol. Cell. Biol. 1989, 9:2657-2664.
21. de Oliveira D.E., Ballon G., Cesarman E. NF-kappaB signaling modulation by EBV and KSHV. Trends Microbiol. 2010, 18:248-257.
22. Didiano D., Hobert O. Perfect seed pairing is not a generally reliable predictor for miRNA-target interactions. Nat. Struct. Mol. Biol. 2006, 13:849-851.
23. Dolken L., Perot J., Cognat V., Alioua A., John M., Soutschek J., Ruzsics Z., Koszinowski U., Voinnet O., Pfeffer S. Mouse cytomegalovirus microRNAs dominate the cellular small RNA profile during lytic infection and show features of posttranscriptional regulation. J. Virol. 2007, 81:13771-13782.
24. Dolken L., Krmpotic A., Kothe S., Tuddenham L., Tanguy M., Marcinowski L., Ruzsics Z., Elefant N., Altuvia Y., Margalit H., Koszinowski U.H., Jonjic S., Pfeffer S. Cytomegalovirus microRNAs facilitate persistent virus infection in salivary glands. PLoS Pathog. 2010, 6:e1001150.
25. Enright A.J., John B., Gaul U., Tuschl T., Sander C., Marks D.S. MicroRNA targets in Drosophila. Genome Biol. 2003, 5:R1.
26. Furnari F.B., Adams M.D., Pagano J.S. Unconventional processing of the 3' termini of the Epstein-Barr virus DNA polymerase mRNA. Proc. Natl Acad. Sci. USA 1993, 90:378-382.
27. Ganem D. KSHV and the pathogenesis of Kaposi sarcoma: listening to human biology and medicine. J. Clin. Invest. 2010, 120:939-949.
28. Gatto G., Rossi A., Rossi D., Kroening S., Bonatti S., Mallardo M. Epstein-Barr virus latent membrane protein 1 trans-activates miR-155 transcription through the NF-kappaB pathway. Nucleic Acids Res. 2008, 36:6608-6619.
29. Godshalk S.E., Bhaduri-McIntosh S., Slack F.J. Epstein-Barr virus-mediated dysregulation of human microRNA expression. Cell Cycle 2008, 7:3595-3600.
30. Gottwein E., Cullen B.R. A human herpesvirus microRNA inhibits p21 expression and attenuates p21-mediated cell cycle arrest. J. Virol. 2010, 84:5229-5237.
31. Gottwein E., Mukherjee N., Sachse C., Frenzel C., Majoros W.H., Chi J.T., Braich R., Manoharan M., Soutschek J., Ohler U., Cullen B.R. A viral microRNA functions as an orthologue of cellular miR-155. Nature 2007, 450:1096-1099.
32. Grey F., Nelson J. Identification and function of human cytomegalovirus microRNAs. J. Clin. Virol. 2008, 41:186-191.
33. Grey F., Antoniewicz A., Allen E., Saugstad J., McShea A., Carrington J.C., Nelson J. Identification and characterization of human cytomegalovirus-encoded microRNAs. J. Virol. 2005, 79:12095-12099.
34. Grey F., Meyers H., White E.A., Spector D.H., Nelson J. A human cytomegalovirus-encoded microRNA regulates expression of multiple viral genes involved in replication. PLoS Pathog. 2007, 3:e163.
35. Grey F., Tirabassi R., Meyers H., Wu G., McWeeney S., Hook L., Nelson J.A. A viral microRNA down-regulates multiple cell cycle genes through mRNA 5'UTRs. PLoS Pathog. 2010, 6:e1000967.
36. Griffiths-Jones S. miRBase: the microRNA sequence database. Meth. Mol. Biol. 2006, 342:129-138.
37. Grimson A., Farh K.K., Johnston W.K., Garrett-Engele P., Lim L.P., Bartel D.P. MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol. Cell 2007, 27:91-105.
38. Grundhoff A., Sullivan C.S., Ganem D. A combined computational and microarray-based approach identifies novel microRNAs encoded by human gamma-herpesviruses. RNA 2006, 12:733-750. (Epub 2006 Mar 2015).
39. Gunther T., Grundhoff A. The epigenetic landscape of latent Kaposi sarcoma-associated herpesvirus genomes. PLoS Pathog. 2010, 6:e1000935.
40. Hansen A., Henderson S., Lagos D., Nikitenko L., Coulter E., Roberts S., Gratrix F., Plaisance K., Renne R., Bower M., Kellam P., Boshoff C. KSHV-encoded miRNAs target MAF to induce endothelial cell reprogramming. Genes Dev. 2010, 24:195-205.
41. Hong Y.K., Foreman K., Shin J.W., Hirakawa S., Curry C.L., Sage D.R., Libermann T., Dezube B.J., Fingeroth J.D., Detmar M. Lymphatic reprogramming of blood vascular endothelium by Kaposi sarcoma-associated herpesvirus. Nat. Genet. 2004, 36:683-685.
42. Hussain M., Taft R.J., Asgari S. An insect virus-encoded microRNA regulates viral replication. J. Virol. 2008, 9:9.
43. Hutvagner G., McLachlan J., Pasquinelli A.E., Balint E., Tuschl T., Zamore P.D. A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA. Science 2001, 293:834-838.
44. Iizasa H., Wulff B.E., Alla N.R., Maragkakis M., Megraw M., Hatzigeorgiou A., Iwakiri D., Takada K., Wiedmer A., Showe L., Lieberman P., Nishikura K. Editing of Epstein-Barr virus-encoded BART6 microRNAs controls their dicer targeting and consequently affects viral latency. J. Biol. Chem. 2010, 285:33358-33370.
45. Johnston R.J., Hobert O. A microRNA controlling left/right neuronal asymmetry in Caenorhabditis elegans. Nature 2003, 426:845-849. (Epub 2003 Dec 2014).
46. Kedde M., van Kouwenhove M., Zwart W., Oude Vrielink J.A., Elkon R., Agami R. A Pumilio-induced RNA structure switch in p27-3' UTR controls miR-221 and miR-222 accessibility. Nat. Cell Biol. 2010, 12:1014-1020.
47. Kertesz M., Iovino N., Unnerstall U., Gaul U., Segal E. The role of site accessibility in microRNA target recognition. Nat. Genet. 2007, 39:1278-1284.
48. Kim V.N. MicroRNA biogenesis: coordinated cropping and dicing. Nat. Rev. Mol. Cell Biol. 2005, 15:15.
49. Kiriakidou M., Nelson P.T., Kouranov A., Fitziev P., Bouyioukos C., Mourelatos Z., Hatzigeorgiou A. A combined computational-experimental approach predicts human microRNA targets. Genes Dev. 2004, 18:1165-1178.
50. Krek A., Grun D., Poy M.N., Wolf R., Rosenberg L., Epstein E.J., MacMenamin P., da Piedade I., Gunsalus K.C., Stoffel M., Rajewsky N. Combinatorial microRNA target predictions. Nat. Genet. 2005, 37:495-500.
51. Kreuze J.F., Savenkov E.I., Cuellar W., Li X., Valkonen J.P. Viral class 1 RNase III involved in suppression of RNA silencing. J. Virol. 2005, 79:7227-7238.
52. Krutzfeldt J., Rajewsky N., Braich R., Rajeev K.G., Tuschl T., Manoharan M., Stoffel M. Silencing of microRNAs in vivo with 'antagomirs'. Nature 2005, 438:685-689.
53. Lagos-Quintana M., Rauhut R., Lendeckel W., Tuschl T. Identification of novel genes coding for small expressed RNAs. Science 2001, 294:853-858.
54. Lau N.C., Lim L.P., Weinstein E.G., Bartel D.P. An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science 2001, 294:858-862.
55. Lee R.C., Ambros V. An extensive class of small RNAs in Caenorhabditis elegans. Science 2001, 294:862-864.
56. Lee R.C., Feinbaum R.L., Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993, 75:843-854.
57. Lee Y., Ahn C., Han J., Choi H., Kim J., Yim J., Lee J., Provost P., Radmark O., Kim S., Kim V.N. The nuclear RNase III Drosha initiates microRNA processing. Nature 2003, 425:415-419.
58. Lei X., Bai Z., Ye F., Xie J., Kim C.G., Huang Y., Gao S.J. Regulation of NF-kappaB inhibitor IkappaBalpha and viral replication by a KSHV microRNA. Nat. Cell Biol. 2010, 12:193-199.
59. Lewis B.P., Shih I.H., Jones-Rhoades M.W., Bartel D.P., Burge C.B. Prediction of mammalian microRNA targets. Cell 2003, 115:787-798.
60. Lim L.P., Lau N.C., Garrett-Engele P., Grimson A., Schelter J.M., Castle J., Bartel D.P., Linsley P.S., Johnson J.M. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 2005, 433:769-773. (Epub 2005 Jan 2030).
61. Lin J., Cullen B.R. Analysis of the interaction of primate retroviruses with the human RNA interference machinery. J. Virol. 2007, 81:12218-12226.
62. Lin Y.T., Kincaid R.P., Arasappan D., Dowd S.E., Hunicke-Smith S.P., Sullivan C.S. Small RNA profiling reveals antisense transcription throughout the KSHV genome and novel small RNAs. RNA 2010, 16:1540-1558.
63. Lo A.K., To K.F., Lo K.W., Lung R.W., Hui J.W., Liao G., Hayward S.D. Modulation of LMP1 protein expression by EBV-encoded microRNAs. Proc. Natl. Acad. Sci. U.S.A. 2007, 104(41):16164-16169.
64. Lodish H.F., Zhou B., Liu G., Chen C.Z. Micromanagement of the immune system by microRNAs. Nat. Rev. Immunol. 2008, 8:120-130.
65. Lu S., Cullen B.R. Adenovirus VA1 noncoding RNA can inhibit small interfering RNA and microRNA biogenesis. J. Virol. 2004, 78:12868-12876.
66. Lu C.C., Li Z., Chu C.Y., Feng J., Sun R., Rana T.M. MicroRNAs encoded by Kaposi's sarcoma-associated herpesvirus regulate viral life cycle. EMBO Rep. 2010, 11:784-790.
67. Lu F., Stedman W., Yousef M., Renne R., Lieberman P.M. Epigenetic regulation of Kaposi's sarcoma-associated herpesvirus latency by virus-encoded microRNAs that target Rta and the cellular Rbl2-DNMT pathway. J. Virol. 2010, 84:2697-2706.
68. Lung R.W., Tong J.H., Sung Y.M., Leung P.S., Ng D.C., Chau S.L., Chan A.W., Ng E.K., Lo K.W., To K.F. Modulation of LMP2A expression by a newly identified Epstein-Barr virus-encoded microRNA miR-BART22. Neoplasia 2009, 11(11):1174-1184.
69. McClure L.V., Sullivan C.S. Kaposi's sarcoma herpes virus taps into a host microRNA regulatory network. Cell Host Microbe 2008, 3:1-3.
70. Medina P.P., Slack F.J. MicroRNAs and cancer: an overview. Cell Cycle 2008, 7:2485-2492.
71. Miranda K.C., Huynh T., Tay Y., Ang Y.S., Tam W.L., Thomson A.M., Lim B., Rigoutsos I. A pattern-based method for the identification of microRNA binding sites and their corresponding heteroduplexes. Cell 2006, 126:1203-1217.
72. Morgan R., Anderson A., Bernberg E., Kamboj S., Huang E., Lagasse G., Isaacs G., Parcells M., Meyers B.C., Green P.J., Burnside J. Sequence conservation and differential expression of Marek's disease virus microRNAs. J. Virol. 2008, 82:12213-12220.
73. Murphy E., Vanicek J., Robins H., Shenk T., Levine A.J. Suppression of immediate-early viral gene expression by herpesvirus-coded microRNAs: implications for latency. Proc. Natl Acad. Sci. USA 2008, 105:5453-5458.
74. Muylkens B., Coupeau D., Dambrine G., Trapp S., Rasschaert D. Marek's disease virus microRNA designated Mdv1-pre-miR-M4 targets both cellular and viral genes. Arch. Virol. 2010, 155(11):1823-1837.
75. 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.
76. Nair V., Zavolan M. Virus-encoded microRNAs: novel regulators of gene expression. Trends Microbiol. 2006, 14:169-175.
77. Okamura K., Hagen J.W., Duan H., Tyler D.M., Lai E.C. The mirtron pathway generates microRNA-class regulatory RNAs in Drosophila. Cell 2007, 130:89-100.
78. Pasquinelli A.E., Reinhart B.J., Slack F., Martindale M.Q., Kuroda M.I., Maller B., Hayward D.C., Ball E.E., Degnan B., Muller P., Spring J., Srinivasan A., Fishman M., Finnerty J., Corbo J., Levine M., Leahy P., Davidson E., Ruvkun G. Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA. Nature 2000, 408:86-89.
79. Pfeffer S., Zavolan M., Grasser F.A., Chien M., Russo J.J., Ju J., John B., Enright A.J., Marks D., Sander C., Tuschl T. Identification of virus-encoded microRNAs. Science 2004, 304:734-736.
80. Pfeffer S., Sewer A., Lagos-Quintana M., Sheridan R., Sander C., Grasser F.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. Meth. 2005, 2:269-276. (Epub 2005 Feb 2016).
81. Polic B., Jonjic S., Pavic I., Crnkovic I., Zorica I., Hengel H., Lucin P., Koszinowski U.H. Lack of MHC class I complex expression has no effect on spread and control of cytomegalovirus infection in vivo. J. Gen. Virol. 1996, 77(Pt 2):217-225.
82. Polic B., Hengel H., Krmpotic A., Trgovcich J., Pavic I., Luccaronin P., Jonjic S., Koszinowski U.H. Hierarchical and redundant lymphocyte subset control precludes cytomegalovirus replication during latent infection. J. Exp. Med. 1998, 188:1047-1054.
83. Qin Z., Kearney P., Plaisance K., Parsons C.H. Pivotal advance: Kaposi's sarcoma-associated herpesvirus (KSHV)-encoded microRNA specifically induce IL-6 and IL-10 secretion by macrophages and monocytes. J. Leukoc. Biol. 2010, 87:25-34.
84. Rehmsmeier M., Steffen P., Hochsmann M., Giegerich R. Fast and effective prediction of microRNA/target duplexes. RNA 2004, 10:1507-1517.
85. Reinhart B.J., Slack F.J., Basson M., Pasquinelli A.E., Bettinger J.C., Rougvie A.E., Horvitz H.R., Ruvkun G. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 2000, 403:901-906.
86. Riley K.J., Rabinowitz G.S., Steitz J.A. Comprehensive analysis of Rhesus lymphocryptovirus microRNA expression. J. Virol. 2010, 84:5148-5157.
87. Rodriguez A., Vigorito E., Clare S., Warren M.V., Couttet P., Soond D.R., van Dongen S., Grocock R.J., Das P.P., Miska E.A., Vetrie D., Okkenhaug K., Enright A.J., Dougan G., Turner M., Bradley A. Requirement of bic/microRNA-155 for normal immune function. Science 2007, 316:608-611.
88. Rouha H., Thurner C., Mandl C.W. Functional microRNA generated from a cytoplasmic RNA virus. Nucleic Acids Res. 2010, 38(22):8328-8337.
89. Ruby J.G., Jan C.H., Bartel D.P. Intronic microRNA precursors that bypass Drosha processing. Nature 2007, 448:83-86.
90. Samols M.A., Hu J., Skalsky R.L., Renne R. Cloning and identification of a microRNA cluster within the latency-associated region of Kaposi's sarcoma-associated herpesvirus. J. Virol. 2005, 79:9301-9305.
91. Samols M.A., Skalsky R.L., Maldonado A.M., Riva A., Lopez M.C., Baker H.V., Renne R. Identification of cellular genes targeted by KSHV-encoded microRNAs. PLoS Pathog. 2007, 3:e65.
92. Schratt G.M., Tuebing F., Nigh E.A., Kane C.G., Sabatini M.E., Kiebler M., Greenberg M.E. A brain-specific microRNA regulates dendritic spine development. Nature 2006, 439:283-289.
93. Seo G.J., Fink L.H., O'Hara B., Atwood W.J., Sullivan C.S. Evolutionarily conserved function of a viral microRNA. J. Virol. 2008, 82:9823-9828.
94. Seo G.J., Chen C.J., Sullivan C.S. Merkel cell polyomavirus encodes a microRNA with the ability to autoregulate viral gene expression. Virology 2009, 383:183-187.
95. 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.
96. Shapiro J.S., Varble A., Pham A.M., Tenoever B.R. Noncanonical cytoplasmic processing of viral microRNAs. RNA 2010, 16:2068-2074.
97. Singh J., Singh C.P., Bhavani A., Nagaraju J. Discovering microRNAs from Bombyx mori nucleopolyhedrosis virus. Virology 2010, 407:120-128.
98. Skalsky R.L., Samols M.A., Plaisance K.B., Boss I.W., Riva A., Lopez M.C., Baker H.V., Renne R. Kaposi's sarcoma-associated herpesvirus encodes an ortholog of miR-155. J. Virol. 2007, 81:12836-12845.
99. Stern-Ginossar N., Elefant N., Zimmermann A., Wolf D.G., Saleh N., Biton M., Horwitz E., Prokocimer Z., Prichard M., Hahn G., Goldman-Wohl D., Greenfield C., Yagel S., Hengel H., Altuvia Y., Margalit H., Mandelboim O. Host immune system gene targeting by a viral miRNA. Science 2007, 317:376-381.
100. Stern-Ginossar N., Saleh N., Goldberg M.D., Prichard M., Wolf D.G., Mandelboim O. Analysis of human cytomegalovirus-encoded microRNA activity during infection. J. Virol. 2009, 83:10684-10693.
101. Subramanian S., Steer C.J. MicroRNAs as gatekeepers of apoptosis. J. Cell. Physiol. 2010, 223:289-298.
102. Sullivan C.S. New roles for large and small viral RNAs in evading host defences. Nat. Rev. Genet. 2008, 20:20.
103. Sullivan C.S., Grundhoff A.T., Tevethia S., Pipas J.M., Ganem D. SV40-encoded microRNAs regulate viral gene expression and reduce susceptibility to cytotoxic T cells. Nature 2005, 435:682-686.
104. Sullivan C.S., Sung C.K., Pack C.D., Grundhoff A., Lukacher A.E., Benjamin T.L., Ganem D. Murine polyomavirus encodes a microRNA that cleaves early RNA transcripts but is not essential for experimental infection. Virology 2009, 7:7.
105. Tang S., Bertke A.S., Patel A., Wang K., Cohen J.I., Krause P.R. An acutely and latently expressed herpes simplex virus 2 viral microRNA inhibits expression of ICP34.5, a viral neurovirulence factor. Proc. Natl Acad. Sci. USA 2008, 105:10931-10936.
106. Tang S., Patel A., Krause P.R. Novel less-abundant viral microRNAs encoded by herpes simplex virus 2 latency-associated transcript and their roles in regulating ICP34.5 and ICP0 mRNAs. J. Virol. 2009, 83(3):1433-1442.
107. Teng G., Papavasiliou F.N. Shhh! Silencing by microRNA-155. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2009, 364:631-637.
108. Toth Z., Maglinte D.T., Lee S.H., Lee H.R., Wong L.Y., Brulois K.F., Lee S., Buckley J.D., Laird P.W., Marquez V.E., Jung J.U. Epigenetic analysis of KSHV latent and lytic genomes. PLoS Pathog. 2010, 6:e1001013.
109. Umbach J.L., Cullen B.R. In-depth analysis of Kaposi's sarcoma-associated herpesvirus microRNA expression provides insights into the mammalian microRNA-processing machinery. J. Virol. 2009, 84:695-703.
110. 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, 2:2.
111. Umbach J.L., 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.
112. Umbach J.L., Yen H.L., Poon L.L., Cullen B.R. Influenza A virus expresses high levels of an unusual class of small viral leader RNAs in infected cells. MBio 2010, 1.
113. Varble A., Chua M.A., Perez J.T., Manicassamy B., Garcia-Sastre A., tenOever B.R. Engineered RNA viral synthesis of microRNAs. Proc. Natl Acad. Sci. USA 2010, 107:11519-11524.
114. Waidner L.A., Morgan R.W., Anderson A.S., Bernberg E.L., Kamboj S., Garcia M., Riblet S.M., Ouyang M., Isaacs G.K., Markis M., Meyers B.C., Green P.J., Burnside J. MicroRNAs of Gallid and Meleagrid herpesviruses show generally conserved genomic locations and are virus-specific. Virology 2009, 388:128-136.
115. Walz N., Christalla T., Tessmer U., Grundhoff A. A global analysis of evolutionary conservation among known and predicted gammaherpesvirus microRNAs. J. Virol. 2010, 84:716-728.
116. Wang H.W., Trotter M.W., Lagos D., Bourboulia D., Henderson S., Makinen T., Elliman S., Flanagan A.M., Alitalo K., Boshoff C. Kaposi sarcoma herpesvirus-induced cellular reprogramming contributes to the lymphatic endothelial gene expression in Kaposi sarcoma. Nat. Genet. 2004, 36:687-693.
117. Wen K.W., Damania B. Kaposi sarcoma-associated herpesvirus (KSHV): molecular biology and oncogenesis. Cancer Lett. 2010, 289:140-150.
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 D.P., Harrington W.J. EBV microRNAs in primary lymphomas and targeting of CXCL-11 by ebv-mir-BHRF1-3. Cancer Res. 2008, 68:1436-1442.
119. Xu S., Xue C., Li J., Bi Y., Cao Y. MDV1-miR-M3 of Marek's disease virus suppresses Cisplatin-induced apoptosis by targeting SMAD2 of TGF-{beta} signal pathway. J. Virol. 2010, 85(1):276-285.
120. Yin Q., McBride J., Fewell C., Lacey M., Wang X., Lin Z., Cameron J., Flemington E.K. MicroRNA-155 is an Epstein-Barr virus-induced gene that modulates Epstein-Barr virus-regulated gene expression pathways. J. Virol. 2008, 82:5295-5306.
121. Yu F., Harada J.N., Brown H.J., Deng H., Song M.J., Wu T.T., Kato-Stankiewicz J., Nelson C.G., Vieira J., Tamanoi F., Chanda S.K., Sun R. Systematic identification of cellular signals reactivating Kaposi sarcoma-associated herpesvirus. PLoS Pathog. 2007, 3:e44.
122. Zeng Y., Yi R., Cullen B.R. Recognition and cleavage of primary microRNA precursors by the nuclear processing enzyme Drosha. EMBO J. 2005, 24:138-148. (Epub 2004 Nov 2025).
123. Zhao Y., Yao Y., Xu H., Lambeth L., Smith L.P., Kgosana L., Wang X., Nair V. A functional MicroRNA-155 ortholog encoded by the oncogenic Marek's disease virus. J. Virol. 2009, 83:489-492.
124. 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.
125. Ziegelbauer J.M., Sullivan C.S., Ganem D. Tandem array-based expression screens identify host mRNA targets of virus-encoded microRNAs. Nat. Genet. 2009, 41:130-134.