Roles and regulation of microRNAs in cytomegalovirus infection

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1809, Issue 11-12, 2011, Pages 613-622

  Tuddenham, Lee ^a   Pfeffer, Sébastien ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

Cytomegalovirus; HCMV; Herpesvirus; MCMV; miRNA; RCMV

Indexed keywords

MICRORNA; VIRUS RNA;

3' UNTRANSLATED REGION; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTION; EPSTEIN BARR VIRUS; GENE CONTROL; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE IDENTIFICATION; HERPES VIRUS; HUMAN; IMMUNE EVASION; INNATE IMMUNITY; LIFE CYCLE; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; REVIEW; VIRUS LATENCY;

3' UNTRANSLATED REGIONS; ANIMALS; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; GENE EXPRESSION REGULATION, VIRAL; HERPESVIRUS 4, HUMAN; HOST-PARASITE INTERACTIONS; HUMANS; MICRORNAS; RNA, VIRAL; VIRUS LATENCY;

CYTOMEGALOVIRUS; EUKARYOTA; HERPESVIRIDAE; HUMAN HERPESVIRUS 4; MAIZE CHLOROTIC MOTTLE VIRUS; RED CLOVER MOTTLE VIRUS;

EID: 80655149156     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2011.04.002     Document Type: Review

References (111)

1. 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.
2. Wightman B., Ha I., Ruvkun G. Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 1993, 75:855-862.
3. 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.
4. Lagos-Quintana M., Rauhut R., Lendeckel W., Tuschl T. Identification of novel genes coding for small expressed RNAs. Science 2001, 294:853-858.
5. 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.
6. Lee R.C., Ambros V. An extensive class of small RNAs in Caenorhabditis elegans. Science 2001, 294:862-864.
7. Reinhart B.J., Weinstein E.G., Rhoades M.W., Bartel B., Bartel D.P. MicroRNAs in plants. Genes Dev. 2002, 16:1616-1626.
8. 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.
9. 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. Methods 2005, 2:269-276.
10. Griffiths-Jones S., Saini H.K., van Dongen S., Enright A.J. miRBase: tools for microRNA genomics. Nucleic Acids Res. 2008, 36:D154-D158.
11. Winter J., Jung S., Keller S., Gregory R.I., Diederichs S. Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat. Cell Biol. 2009, 11:228-234.
12. Bartel D.P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004, 116:281-297.
13. 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.
14. Han J., Lee Y., Yeom K.H., Kim Y.K., Jin H., Kim V.N. The Drosha-DGCR8 complex in primary microRNA processing. Genes Dev. 2004, 18:3016-3027.
15. Yi R., Qin Y., Macara I.G., Cullen B.R. Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Dev. 2003, 17:3011-3016.
16. Lund E., Guttinger S., Calado A., Dahlberg J.E., Kutay U. Nuclear export of microRNA precursors. Science 2004, 303:95-98.
17. 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.
18. Ketting R.F., Fischer S.E., Bernstein E., Sijen T., Hannon G.J., Plasterk R.H. Dicer functions in RNA interference and in synthesis of small RNA involved in developmental timing in C. elegans. Genes Dev. 2001, 15:2654-2659.
19. Hammond S.M., Boettcher S., Caudy A.A., Kobayashi R., Hannon G.J. Argonaute2, a link between genetic and biochemical analyses of RNAi. Science 2001, 293:1146-1150.
20. Yekta S., Shih I.H., Bartel D.P. MicroRNA-directed cleavage of HOXB8 mRNA. Science 2004, 304:594-596.
21. Bartel D.P. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136:215-233.
22. Pillai R.S., Bhattacharyya S.N., Filipowicz W. Repression of protein synthesis by miRNAs: how many mechanisms?. Trends Cell Biol. 2007, 17:118-126.
23. Krol J., Loedige I., Filipowicz W. The widespread regulation of microRNA biogenesis, function and decay. Nat. Rev. Genet. 2010, 11:597-610.
24. Friedman R.C., Farh K.K., Burge C.B., Bartel D.P. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 2009, 19:92-105.
25. Lewis B.P., Burge C.B., Bartel D.P. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005, 120:15-20.
26. 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., Chiaretti S., Foa R., Schliwka J., Fuchs U., Novosel A., Muller R.U., Schermer B., Bissels U., Inman J., Phan Q., Chien M., Weir D.B., Choksi R., De Vita G., Frezzetti D., Trompeter 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.
27. Lagos-Quintana M., Rauhut R., Yalcin A., Meyer J., Lendeckel W., Tuschl T. Identification of tissue-specific microRNAs from mouse. Curr. Biol. 2002, 12:735-739.
28. Bushati N., Cohen S.M. microRNA functions. Annu. Rev. Cell Dev. Biol. 2007, 23:175-205.
29. Grimson A., Srivastava M., Fahey B., Woodcroft B.J., Chiang H.R., King N., Degnan B.M., Rokhsar D.S., Bartel D.P. Early origins and evolution of microRNAs and Piwi-interacting RNAs in animals. Nature 2008, 455:1193-1197.
30. Skalsky R.L., Cullen B.R. Viruses, microRNAs, and host interactions. Annu. Rev. Microbiol. 2010, 64:123-141.
31. Singh J., Singh C.P., Bhavani A., Nagaraju J. Discovering microRNAs from Bombyx mori nucleopolyhedrosis virus. Virology 2010, 407:120-128.
32. 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.
33. 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.
34. Hussain M., Taft R.J., Asgari S. An insect virus-encoded microRNA regulates viral replication. J. Virol. 2008, 82:9164-9170.
35. 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.
36. Omoto S., Ito M., Tsutsumi Y., Ichikawa Y., Okuyama H., Brisibe E.A., Saksena N.K., Fujii Y.R. HIV-1 nef suppression by virally encoded microRNA. Retrovirology 2004, 1:44.
37. Ouellet D.L., Plante I., Landry P., Barat C., Janelle M.E., Flamand L., Tremblay M.J., Provost P. Identification of functional microRNAs released through asymmetrical processing of HIV-1 TAR element. Nucleic Acids Res. 2008, 36:2353-2365.
38. Lin J., Cullen B.R. Analysis of the interaction of primate retroviruses with the human RNA interference machinery. J. Virol. 2007, 81:12218-12226.
39. Rouha H., Thurner C., Mandl C.W. Functional microRNA generated from a cytoplasmic RNA virus. Nucleic Acids Res. 2010, 38:8328-8337.
40. Shapiro J.S., Varble A., Pham A.M., Tenoever B.R. Noncanonical cytoplasmic processing of viral microRNAs. RNA 2010, 16:2068-2074.
41. 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.
42. 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.
43. 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.
44. Dunn W., Trang P., Zhong Q., Yang E., van Belle C., Liu F. Human cytomegalovirus expresses novel microRNAs during productive viral infection. Cell. Microbiol. 2005, 7:1684-1695.
45. 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.
46. Cannon M.J., Schmid D.S., Hyde T.B. Review of cytomegalovirus seroprevalence and demographic characteristics associated with infection. Rev. Med. Virol. 2010, 20:202-213.
47. Dolken L., Pfeffer S., Koszinowski U.H. Cytomegalovirus microRNAs. Virus Genes 2009, 38:355-364.
48. 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.
49. Powers C., Fruh K. Rhesus CMV: an emerging animal model for human CMV. Med. Microbiol. Immunol. 2008, 197:109-115.
50. Meyer C., Grey F., Kreklywich C.N., Andoh T.F., Tirabassi R.S., Orloff S.L., Streblow D.N. Cytomegalovirus microRNA expression is tissue specific and is associated with persistence. J. Virol. 2011, 85:378-389.
51. Kulesza C.A., Shenk T. Murine cytomegalovirus encodes a stable intron that facilitates persistent replication in the mouse. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:18302-18307.
52. 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.
53. John B., Enright A.J., Aravin A., Tuschl T., Sander C., Marks D.S. Human MicroRNA targets. PLoS Biol. 2004, 2:e363.
54. 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.
55. 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, 387:157-167.
56. 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.
57. 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.
58. 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.
59. 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.
60. 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. U.S.A. 2008, 105:5453-5458.
61. Ghazal P., Visser A.E., Gustems M., Garcia R., Borst E.M., Sullivan K., Messerle M., Angulo A. Elimination of ie1 significantly attenuates murine cytomegalovirus virulence but does not alter replicative capacity in cell culture. J. Virol. 2005, 79:7182-7194.
62. Stern-Ginossar N., Mandelboim O. An integrated view of the regulation of NKG2D ligands. Immunology 2009, 128:1-6.
63. Lenac T., Arapovic J., Traven L., Krmpotic A., Jonjic S. Murine cytomegalovirus regulation of NKG2D ligands. Med. Microbiol. Immunol. 2008, 197:159-166.
64. Powers C., DeFilippis V., Malouli D., Fruh K. Cytomegalovirus immune evasion. Curr. Top. Microbiol. Immunol. 2008, 325:333-359.
65. Wilkinson G.W., Tomasec P., Stanton R.J., Armstrong M., Prod'homme V., Aicheler R., McSharry B.P., Rickards C.R., Cochrane D., Llewellyn-Lacey S., Wang E.C., Griffin C.A., Davison A.J. Modulation of natural killer cells by human cytomegalovirus. J. Clin. Virol. 2008, 41:206-212.
66. Elefant N., Berger A., Shein H., Hofree M., Margalit H., Altuvia Y. RepTar: a database of predicted cellular targets of host and viral miRNAs. Nucleic Acids Res. 2011, 39:D188-D194.
67. 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.
68. Welte S.A., Sinzger C., Lutz S.Z., Singh-Jasuja H., Sampaio K.L., Eknigk U., Rammensee H.G., Steinle A. Selective intracellular retention of virally induced NKG2D ligands by the human cytomegalovirus UL16 glycoprotein. Eur. J. Immunol. 2003, 33:194-203.
69. Wu J., Chalupny N.J., Manley T.J., Riddell S.R., Cosman D., Spies T. Intracellular retention of the MHC class I-related chain B ligand of NKG2D by the human cytomegalovirus UL16 glycoprotein. J. Immunol. 2003, 170:4196-4200.
70. Stern-Ginossar N., Gur C., Biton M., Horwitz E., Elboim M., Stanietsky N., Mandelboim M., Mandelboim O. Human microRNAs regulate stress-induced immune responses mediated by the receptor NKG2D. Nat. Immunol. 2008, 9:1065-1073.
71. 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.
72. 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. U.S.A. 2005, 102:5570-5575.
73. 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.
74. Nachmani D., Lankry D., Wolf D.G., Mandelboim O. The human cytomegalovirus microRNA miR-UL112 acts synergistically with a cellular microRNA to escape immune elimination. Nat. Immunol. 2010, 11:806-813.
75. Keene J.D., Komisarow J.M., Friedersdorf M.B. RIP-Chip: the isolation and identification of mRNAs, microRNAs and protein components of ribonucleoprotein complexes from cell extracts. Nat. Protoc. 2006, 1:302-307.
76. Tan L.P., Seinen E., Duns G., de Jong D., Sibon O.C., Poppema S., Kroesen B.J., Kok K., van den Berg A. A high throughput experimental approach to identify miRNA targets in human cells. Nucleic Acids Res. 2009, 37:e137.
77. Malterer G., Dolken L., Haas J. The miRNA-targetome of KSHV and EBV in human B-cells. RNA Biol. 2011, 8.
78. Chi S.W., Zang J.B., Mele A., Darnell R.B. Argonaute HITS-CLIP decodes microRNA-mRNA interaction maps. Nature 2009, 460:479-486.
79. Licatalosi D.D., Mele A., Fak J.J., Ule J., Kayikci M., Chi S.W., Clark T.A., Schweitzer A.C., Blume J.E., Wang X., Darnell J.C., Darnell R.B. HITS-CLIP yields genome-wide insights into brain alternative RNA processing. Nature 2008, 456:464-469.
80. Hafner M., Landthaler M., Burger L., Khorshid M., Hausser J., Berninger P., Rothballer A., Ascano M., Jungkamp A.C., Munschauer M., Ulrich A., Wardle G.S., Dewell S., Zavolan M., Tuschl T. Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell 2010, 141:129-141.
81. Huang Y., Qi Y., Ruan Q., Ma Y., He R., Ji Y., Sun Z. A rapid method to screen putative mRNA targets of any known microRNA. Virol. J. 2011, 8:8.
82. 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.
83. Moretti F., Thermann R., Hentze M.W. Mechanism of translational regulation by miR-2 from sites in the 5' untranslated region or the open reading frame. RNA 2010, 16:2493-2502.
84. Schnall-Levin M., Zhao Y., Perrimon N., Berger B. Conserved microRNA targeting in Drosophila is as widespread in coding regions as in 3'UTRs. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:15751-15756.
85. Borst E.M., Hahn G., Koszinowski U.H., Messerle M. Cloning of the human cytomegalovirus (HCMV) genome as an infectious bacterial artificial chromosome in Escherichia coli: a new approach for construction of HCMV mutants. J. Virol. 1999, 73:8320-8329.
86. Messerle M., Crnkovic I., Hammerschmidt W., Ziegler H., Koszinowski U.H. Cloning and mutagenesis of a herpesvirus genome as an infectious bacterial artificial chromosome. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:14759-14763.
87. 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.
88. Smith H.R., Heusel J.W., Mehta I.K., Kim S., Dorner B.G., Naidenko O.V., Iizuka K., Furukawa H., Beckman D.L., Pingel J.T., Scalzo A.A., Fremont D.H., Yokoyama W.M. Recognition of a virus-encoded ligand by a natural killer cell activation receptor. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:8826-8831.
89. Arase H., Mocarski E.S., Campbell A.E., Hill A.B., Lanier L.L. Direct recognition of cytomegalovirus by activating and inhibitory NK cell receptors. Science 2002, 296:1323-1326.
90. Lecellier C.H., Dunoyer P., Arar K., Lehmann-Che J., Eyquem S., Himber C., Saib A., Voinnet O. A cellular microRNA mediates antiviral defense in human cells. Science 2005, 308:557-560.
91. Huang J., Wang F., Argyris E., Chen K., Liang Z., Tian H., Huang W., Squires K., Verlinghieri G., Zhang H. Cellular microRNAs contribute to HIV-1 latency in resting primary CD4+ T lymphocytes. Nat. Med. 2007, 13:1241-1247.
92. Otsuka M., Jing Q., Georgel P., New L., Chen J., Mols J., Kang Y.J., Jiang Z., Du X., Cook R., Das S.C., Pattnaik A.K., Beutler B., Han J. Hypersusceptibility to vesicular stomatitis virus infection in Dicer1-deficient mice is due to impaired miR24 and miR93 expression. Immunity 2007, 27:123-134.
93. Jopling C.L., Yi M., Lancaster A.M., Lemon S.M., Sarnow P. Modulation of hepatitis C virus RNA abundance by a liver-specific MicroRNA. Science 2005, 309:1577-1581.
94. Lanford R.E., Hildebrandt-Eriksen E.S., Petri A., Persson R., Lindow M., Munk M.E., Kauppinen S., Orum H. Therapeutic silencing of microRNA-122 in primates with chronic hepatitis C virus infection. Science 2010, 327:198-201.
95. Machlin E.S., Sarnow P., Sagan S.M. Masking the 5' terminal nucleotides of the hepatitis C virus genome by an unconventional microRNA-target RNA complex. Proc. Natl. Acad. Sci. U.S.A. 2011.
96. Cameron J.E., Yin Q., Fewell C., Lacey M., McBride J., Wang X., Lin Z., Schaefer B.C., Flemington E.K. Epstein-Barr virus latent membrane protein 1 induces cellular MicroRNA miR-146a, a modulator of lymphocyte signaling pathways. J. Virol. 2008, 82:1946-1958.
97. 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.
98. 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.
99. Anastasiadou E., Boccellato F., Vincenti S., Rosato P., Bozzoni I., Frati L., Faggioni A., Presutti C., Trivedi P. Epstein-Barr virus encoded LMP1 downregulates TCL1 oncogene through miR-29b. Oncogene 2010, 29:1316-1328.
100. Ellis-Connell A.L., Iempridee T., Xu I., Mertz J.E. Cellular microRNAs 200b and 429 regulate the Epstein-Barr virus switch between latency and lytic replication. J. Virol. 2010, 84:10329-10343.
101. Li G., Wu Z., Peng Y., Liu X., Lu J., Wang L., Pan Q., He M.L., Li X.P. MicroRNA-10b induced by Epstein-Barr virus-encoded latent membrane protein-1 promotes the metastasis of human nasopharyngeal carcinoma cells. Cancer Lett. 2010, 299:29-36.
102. 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.
103. 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.
104. Lagos D., Pollara G., Henderson S., Gratrix F., Fabani M., Milne R.S., Gotch F., Boshoff C. miR-132 regulates antiviral innate immunity through suppression of the p300 transcriptional co-activator. Nat. Cell Biol. 2010, 12:513-519.
105. Wang F.Z., Weber F., Croce C., Liu C.G., Liao X., Pellett P.E. Human cytomegalovirus infection alters the expression of cellular microRNA species that affect its replication. J. Virol. 2008, 82:9065-9074.
106. Santhakumar D., Forster T., Laqtom N.N., Fragkoudis R., Dickinson P., Abreu-Goodger C., Manakov S.A., Choudhury N.R., Griffiths S.J., Vermeulen A., Enright A.J., Dutia B., Kohl A., Ghazal P., Buck A.H. Combined agonist-antagonist genome-wide functional screening identifies broadly active antiviral microRNAs. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:13830-13835.
107. Buck A.H., Perot J., Chisholm M.A., Kumar D.S., Tuddenham L., Cognat V., Marcinowski L., Dolken L., Pfeffer S. Post-transcriptional regulation of miR-27 in murine cytomegalovirus infection. RNA 2010, 16:307-315.
108. Cazalla D., Yario T., Steitz J.A. Down-regulation of a host microRNA by a Herpesvirus saimiri noncoding RNA. Science 2010, 328:1563-1566.
109. Guttilla I.K., White B.A. Coordinate regulation of FOXO1 by miR-27a, miR-96, and miR-182 in breast cancer cells. J. Biol. Chem. 2009, 284:23204-23216.
110. Ameres S.L., Horwich M.D., Hung J.H., Xu J., Ghildiyal M., Weng Z., Zamore P.D. Target RNA-directed trimming and tailing of small silencing RNAs. Science 2010, 328:1534-1539.
111. Chatterjee S., Grosshans H. Active turnover modulates mature microRNA activity in Caenorhabditis elegans. Nature 2009, 461:546-549.