1887

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Volume 96, Issue 4

Role of microRNAs in herpesvirus latency and persistence Free

Abstract

The identification of virally encoded microRNAs (miRNAs) has had a major impact on the field of herpes virology. Given their ability to target cellular and viral transcripts, and the lack of immune response to small RNAs, miRNAs represent an ideal mechanism of gene regulation during viral latency and persistence. In this review, we discuss the role of miRNAs in virus latency and persistence, specifically focusing on herpesviruses. We cover the current knowledge on miRNAs in establishing and maintaining virus latency and promoting survival of infected cells through targeting of both viral and cellular transcripts, highlighting key publications in the field. We also discuss potential areas of future research and how novel technologies may aid in determining how miRNAs shape virus latency in the context of herpesvirus infections.

  • Received:
  • Accepted:
  • Published Online:
© 2015 The Author
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2015-04-01
2024-04-28
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References

  1. Abend J. R., Uldrick T., Ziegelbauer J. M. 2010; Regulation of tumor necrosis factor-like weak inducer of apoptosis receptor protein (TWEAKR) expression by Kaposi’s sarcoma-associated herpesvirus microRNA prevents TWEAK-induced apoptosis and inflammatory cytokine expression. J Virol 84:12139–12151 [View Article][PubMed]
     [Google Scholar]
  2. Abend J. R., Ramalingam D., Kieffer-Kwon P., Uldrick T. S., Yarchoan R., Ziegelbauer J. M. 2012; Kaposi’s sarcoma-associated herpesvirus microRNAs target IRAK1 and MYD88, two components of the toll-like receptor/interleukin-1R signaling cascade, to reduce inflammatory-cytokine expression. J Virol 86:11663–11674 [View Article][PubMed]
     [Google Scholar]
  3. Bartel D. P. 2009; MicroRNAs: target recognition and regulatory functions. Cell 136:215–233 [View Article][PubMed]
     [Google Scholar]
  4. Bellare P., Ganem D. 2009; Regulation of KSHV lytic switch protein expression by a virus-encoded microRNA: an evolutionary adaptation that fine-tunes lytic reactivation. Cell Host Microbe 6:570–575 [View Article][PubMed]
     [Google Scholar]
  5. Blaskovic D., Stanceková M., Svobodová J., Mistríková J. 1980; Isolation of five strains of herpesviruses from two species of free living small rodents. Acta Virol 24:468[PubMed]
     [Google Scholar]
  6. Bogerd H. P., Skalsky R. L., Kennedy E. M., Furuse Y., Whisnant A. W., Flores O., Schultz K. L., Putnam N., Barrows N. J.other authors 2014; Replication of many human viruses is refractory to inhibition by endogenous cellular microRNAs. J Virol 88:8065–8076 [View Article][PubMed]
     [Google Scholar]
  7. Boss I. W., Nadeau P. E., Abbott J. R., 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 IL2Rγnull mice. J Virol 85:9877–9886 [View Article][PubMed]
     [Google Scholar]
  8. Buck A. H., Santoyo-Lopez J., Robertson K. A., Kumar D. S., Reczko M., Ghazal P. 2007; 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 81:13761–13770 [View Article][PubMed]
     [Google Scholar]
  9. Cai X., Lu S., Zhang Z., Gonzalez C. M., Damania B., Cullen B. R. 2005; Kaposi’s sarcoma-associated herpesvirus expresses an array of viral microRNAs in latently infected cells. Proc Natl Acad Sci U S A 102:5570–5575 [View Article][PubMed]
     [Google Scholar]
  10. Cazalla D., Yario T., Steitz J. A. 2010; Down-regulation of a host microRNA by a Herpesvirus saimiri noncoding RNA. Science 328:1563–1566 [View Article][PubMed]
     [Google Scholar]
  11. 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. 2008; An Epstein–Barr virus-encoded microRNA targets PUMA to promote host cell survival. J Exp Med 205:2551–2560 [View Article][PubMed]
     [Google Scholar]
  12. Cosmopoulos K., Pegtel M., Hawkins J., Moffett H., Novina C., Middeldorp J., Thorley-Lawson D. A. 2009; Comprehensive profiling of Epstein–Barr virus microRNAs in nasopharyngeal carcinoma. J Virol 83:2357–2367 [View Article][PubMed]
     [Google Scholar]
  13. Costinean S., Zanesi N., Pekarsky Y., Tili E., Volinia S., Heerema N., Croce C. M. 2006; Pre-B cell proliferation and lymphoblastic leukemia/high-grade lymphoma in Eμ-miR155 transgenic mice. Proc Natl Acad Sci U S A 103:7024–7029 [View Article][PubMed]
     [Google Scholar]
  14. Dölken L., Malterer G., Erhard F., Kothe S., Friedel C. C., Suffert G., Marcinowski L., Motsch N., Barth S., Beitzinger M. 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 [View Article][PubMed]
     [Google Scholar]
  15. Ebert M. S., Sharp P. A. 2012; Roles for microRNAs in conferring robustness to biological processes. Cell 149:515–524 [View Article][PubMed]
     [Google Scholar]
  16. Eis P. S., Tam W., Sun L., Chadburn A., Li Z., Gomez M. F., Lund E., Dahlberg J. E. 2005; Accumulation of miR-155 and BIC RNA in human B cell lymphomas. Proc Natl Acad Sci U S A 102:3627–3632 [View Article][PubMed]
     [Google Scholar]
  17. Ellis A. L., Wang Z., Yu X., Mertz J. E. 2010; Either ZEB1 or ZEB2/SIP1 can play a central role in regulating the Epstein–Barr virus latent-lytic switch in a cell-type-specific manner. J Virol 84:6139–6152 [View Article][PubMed]
     [Google Scholar]
  18. Ellis-Connell A. L., Iempridee T., Xu I., Mertz J. E. 2010; Cellular microRNAs 200b and 429 regulate the Epstein–Barr virus switch between latency and lytic replication. J Virol 84:10329–10343 [View Article][PubMed]
     [Google Scholar]
  19. Feederle R., Linnstaedt S. D., Bannert H., Lips H., Bencun M., Cullen B. R., Delecluse H. J. 2011; A viral microRNA cluster strongly potentiates the transforming properties of a human herpesvirus. PLoS Pathog 7:e1001294 [View Article][PubMed]
     [Google Scholar]
  20. Feldman E. R., Kara M., Coleman C. B., Grau K. R., Oko L. M., Krueger B. J., Renne R., van Dyk L. F., Tibbetts S. A. 2014; Virus-encoded microRNAs facilitate gammaherpesvirus latency and pathogenesis in vivo. MBio 5:e00981-14 [View Article][PubMed]
     [Google Scholar]
  21. Feng P., Moses A., Früh K. 2013; Evasion of adaptive and innate immune response mechanisms by γ-herpesviruses. Curr Opin Virol 3:285–295 [View Article][PubMed]
     [Google Scholar]
  22. Frappier L. 2012; EBNA1 and host factors in Epstein–Barr virus latent DNA replication. Curr Opin Virol 2:733–739 [View Article][PubMed]
     [Google Scholar]
  23. Fu M., Gao Y., Zhou Q., Zhang Q., Peng Y., Tian K., Wang J., Zheng X. 2014; Human cytomegalovirus latent infection alters the expression of cellular and viral microRNA. Gene 536:272–278 [View Article][PubMed]
     [Google Scholar]
  24. Gallaher A. M., Das S., Xiao Z., Andresson T., Kieffer-Kwon P., Happel C., Ziegelbauer J. 2013; Proteomic screening of human targets of viral microRNAs reveals functions associated with immune evasion and angiogenesis. PLoS Pathog 9:e1003584 [View Article][PubMed]
     [Google Scholar]
  25. Goodrum F., Caviness K., Zagallo P. 2012; Human cytomegalovirus persistence. Cell Microbiol 14:644–655 [View Article][PubMed]
     [Google Scholar]
  26. Gottwein E., Mukherjee N., Sachse C., Frenzel C., Majoros W. H., Chi J. T., Braich R., Manoharan M., Soutschek J.other authors 2007; A viral microRNA functions as an orthologue of cellular miR-155. Nature 450:1096–1099 [View Article][PubMed]
     [Google Scholar]
  27. Gottwein E., Corcoran D. L., Mukherjee N., Skalsky R. L., Hafner M., Nusbaum J. D., Shamulailatpam P., Love C. L., Dave S. S.other authors 2011; Viral microRNA targetome of KSHV-infected primary effusion lymphoma cell lines. Cell Host Microbe 10:515–526 [View Article][PubMed]
     [Google Scholar]
  28. Grey F., Antoniewicz A., Allen E., Saugstad J., McShea A., Carrington J. C., Nelson J. 2005; Identification and characterization of human cytomegalovirus-encoded microRNAs. J Virol 79:12095–12099 [View Article][PubMed]
     [Google Scholar]
  29. Grey F., Meyers H., White E. A., Spector D. H., Nelson J. 2007; A human cytomegalovirus-encoded microRNA regulates expression of multiple viral genes involved in replication. PLoS Pathog 3:e163 [View Article][PubMed]
     [Google Scholar]
  30. 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 [View Article][PubMed]
     [Google Scholar]
  31. Grundhoff A., Sullivan C. S. 2011; Virus-encoded microRNAs. Virology 411:325–343 [View Article][PubMed]
     [Google Scholar]
  32. Haecker I., Gay L. A., Yang Y., Hu J., Morse A. M., McIntyre L. M., Renne R. 2012; Ago HITS-CLIP expands understanding of Kaposi’s sarcoma-associated herpesvirus miRNA function in primary effusion lymphomas. PLoS Pathog 8:e1002884 [View Article][PubMed]
     [Google Scholar]
  33. Hancock M. H., Tirabassi R. S., Nelson J. A. 2012; Rhesus cytomegalovirus encodes seventeen microRNAs that are differentially expressed in vitro and in vivo. Virology 425:133–142 [View Article][PubMed]
     [Google Scholar]
  34. Helwak A., Kudla G., Dudnakova T., Tollervey D. 2013; Mapping the human miRNA interactome by CLASH reveals frequent noncanonical binding. Cell 153:654–665 [View Article][PubMed]
     [Google Scholar]
  35. Hook L., Hancock M., Landais I., Grabski R., Britt W., Nelson J. A. 2014a; Cytomegalovirus microRNAs. Curr Opin Virol 7:40–46 [View Article][PubMed]
     [Google Scholar]
  36. Hook L. M., Grey F., Grabski R., Tirabassi R., Doyle T., Hancock M., Landais I., Jeng S., McWeeney S.other authors 2014b; Cytomegalovirus miRNAs target secretory pathway genes to facilitate formation of the virion assembly compartment and reduce cytokine secretion. Cell Host Microbe 15:363–373 [View Article][PubMed]
     [Google Scholar]
  37. Jones T., Ye F., Bedolla R., Huang Y., Meng J., Qian L., Pan H., Zhou F., Moody R.other authors 2012; Direct and efficient cellular transformation of primary rat mesenchymal precursor cells by KSHV. J Clin Invest 122:1076–1081 [View Article][PubMed]
     [Google Scholar]
  38. Jung Y. J., Choi H., Kim H., Lee S. K. 2014; MicroRNA miR-BART20-5p stabilizes Epstein–Barr virus latency by directly targeting BZLF1 and BRLF1. J Virol 88:9027–9037 [View Article][PubMed]
     [Google Scholar]
  39. Kim S., Lee S., Shin J., Kim Y., Evnouchidou I., Kim D., Kim Y. K., Kim Y. E., Ahn J. H.other authors 2011; Human cytomegalovirus microRNA miR-US4-1 inhibits CD8+ T cell responses by targeting the aminopeptidase ERAP1. Nat Immunol 12:984–991 [View Article][PubMed]
     [Google Scholar]
  40. Kim Y., Lee S., Kim S., Kim D., Ahn J. H., Ahn K. 2012; Human cytomegalovirus clinical strain-specific microRNA miR-UL148D targets the human chemokine RANTES during infection. PLoS Pathog 8:e1002577 [View Article][PubMed]
     [Google Scholar]
  41. Kincaid R. P., Burke J. M., Cox J. C., de Villiers E. M., Sullivan C. S. 2013; A human torque teno virus encodes a microRNA that inhibits interferon signaling. PLoS Pathog 9:e1003818 [View Article][PubMed]
     [Google Scholar]
  42. Kozomara A., Griffiths-Jones S. 2014; miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res 42:Database issueD68–D73 [View Article][PubMed]
     [Google Scholar]
  43. Kramer M. F., Jurak I., Pesola J. M., Boissel S., Knipe D. M., Coen D. M. 2011; Herpes simplex virus 1 microRNAs expressed abundantly during latent infection are not essential for latency in mouse trigeminal ganglia. Virology 417:239–247 [View Article][PubMed]
     [Google Scholar]
  44. Lee S. H., Kalejta R. F., Kerry J., Semmes O. J., O’Connor C. M., Khan Z., Garcia B. A., Shenk T., Murphy E. 2012; BclAF1 restriction factor is neutralized by proteasomal degradation and microRNA repression during human cytomegalovirus infection. Proc Natl Acad Sci U S A 109:9575–9580 [View Article][PubMed]
     [Google Scholar]
  45. Lee S., Song J., Kim S., Kim J., Hong Y., Kim Y., Kim D., Baek D., Ahn K. 2013; Selective degradation of host microRNAs by an intergenic HCMV noncoding RNA accelerates virus production. Cell Host Microbe 13:678–690 [View Article][PubMed]
     [Google Scholar]
  46. Lei X., Bai Z., Ye F., Xie J., Kim C. G., Huang Y., Gao S. J. 2010; Regulation of NF-kappaB inhibitor IkappaBalpha and viral replication by a KSHV microRNA. Nat Cell Biol 12:193–199 [View Article][PubMed]
     [Google Scholar]
  47. Libri V., Helwak A., Miesen P., Santhakumar D., Borger J. G., Kudla G., Grey F., Tollervey D., Buck A. H. 2012; Murine cytomegalovirus encodes a miR-27 inhibitor disguised as a target. Proc Natl Acad Sci U S A 109:279–284 [View Article][PubMed]
     [Google Scholar]
  48. Lin Z., Wang X., Fewell C., Cameron J., Yin Q., Flemington E. K. 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 [View Article][PubMed]
     [Google Scholar]
  49. Lin X., Liang D., He Z., Deng Q., Robertson E. S., Lan K. 2011; miR-K12-7-5p encoded by Kaposi’s sarcoma-associated herpesvirus stabilizes the latent state by targeting viral ORF50/RTA. PLoS One 6:e16224 [View Article][PubMed]
     [Google Scholar]
  50. Linnstaedt S. D., Gottwein E., Skalsky R. L., Luftig M. A., Cullen B. R. 2010; Virally induced cellular microRNA miR-155 plays a key role in B-cell immortalization by Epstein–Barr virus. J Virol 84:11670–11678 [View Article][PubMed]
     [Google Scholar]
  51. Lu F., Weidmer A., Liu C. G., Volinia S., Croce C. M., Lieberman P. M. 2008; Epstein–Barr virus-induced miR-155 attenuates NF-kappaB signaling and stabilizes latent virus persistence. J Virol 82:10436–10443 [View Article][PubMed]
     [Google Scholar]
  52. Lu C. C., Li Z., Chu C. Y., Feng J., Feng J., Sun R., Rana T. M. 2010a; MicroRNAs encoded by Kaposi’s sarcoma-associated herpesvirus regulate viral life cycle. EMBO Rep 11:784–790 [View Article][PubMed]
     [Google Scholar]
  53. Lu F., Stedman W., Yousef M., Renne R., Lieberman P. M. 2010b; Epigenetic regulation of Kaposi’s sarcoma-associated herpesvirus latency by virus-encoded microRNAs that target Rta and the cellular Rbl2–DNMT pathway. J Virol 84:2697–2706 [View Article][PubMed]
     [Google Scholar]
  54. Marcinowski L., Tanguy M., Krmpotic A., Rädle B., Lisnić V. J., Tuddenham L., Chane-Woon-Ming B., Ruzsics Z., Erhard F.other authors 2012; Degradation of cellular mir-27 by a novel, highly abundant viral transcript is important for efficient virus replication in vivo. PLoS Pathog 8:e1002510 [View Article][PubMed]
     [Google Scholar]
  55. Meyer C., Grey F., Kreklywich C. N., Andoh T. F., Tirabassi R. S., Orloff S. L., Streblow D. N. 2011; Cytomegalovirus microRNA expression is tissue specific and is associated with persistence. J Virol 85:378–389 [View Article][PubMed]
     [Google Scholar]
  56. Moody R., Zhu Y., Huang Y., Cui X., Jones T., Bedolla R., Lei X., Bai Z., Gao S. J. 2013; KSHV microRNAs mediate cellular transformation and tumorigenesis by redundantly targeting cell growth and survival pathways. PLoS Pathog 9:e1003857 [View Article][PubMed]
     [Google Scholar]
  57. Murphy E., Vanícek J., Robins H., Shenk T., Levine A. J. 2008; Suppression of immediate-early viral gene expression by herpesvirus-coded microRNAs: implications for latency. Proc Natl Acad Sci U S A 105:5453–5458 [View Article][PubMed]
     [Google Scholar]
  58. 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 [View Article][PubMed]
     [Google Scholar]
  59. Noriega V., Redmann V., Gardner T., Tortorella D. 2012; Diverse immune evasion strategies by human cytomegalovirus. Immunol Res 54:140–151 [View Article][PubMed]
     [Google Scholar]
  60. O’Connor C. M., Vanicek J., Murphy E. A. 2014; Host microRNA regulation of human cytomegalovirus immediate early protein translation promotes viral latency. J Virol 88:5524–5532 [View Article][PubMed]
     [Google Scholar]
  61. Pan D., Flores O., Umbach J. L., Pesola J. M., Bentley P., Rosato P. C., Leib D. A., Cullen B. R., Coen D. M. 2014; A neuron-specific host microRNA targets herpes simplex virus-1 ICP0 expression and promotes latency. Cell Host Microbe 15:446–456 [View Article][PubMed]
     [Google Scholar]
  62. Parnas O., Corcoran D. L., Cullen B. R. 2014; Analysis of the mRNA targetome of microRNAs expressed by Marek’s disease virus. MBio 5:e01060-13 [View Article][PubMed]
     [Google Scholar]
  63. Pavelin J., Reynolds N., Chiweshe S., Wu G., Tiribassi R., Grey F. 2013; Systematic microRNA analysis identifies ATP6V0C as an essential host factor for human cytomegalovirus replication. PLoS Pathog 9:e1003820 [View Article][PubMed]
     [Google Scholar]
  64. Pellet E. R., Roizman B. 2013; Herpesviridae. In Fields Virology, 6th edn. pp. 1803–1822 Edited by Knipe D. M., Howley P. M. Philadelphia, PA: Wolters Kluwer/Lippincott Williams & Wilkins;
     [Google Scholar]
  65. Pfeffer S., Sewer A., Lagos-Quintana M., Sheridan R., Sander C., Grässer F. A., van Dyk L. F., Ho C. K., Shuman S.other authors 2005; Identification of microRNAs of the herpesvirus family. Nat Methods 2:269–276 [View Article][PubMed]
     [Google Scholar]
  66. Poole E., McGregor Dallas S. R., Colston J., Joseph R. S., Sinclair J. 2011; Virally induced changes in cellular microRNAs maintain latency of human cytomegalovirus in CD34+ progenitors. J Gen Virol 92:1539–1549 [View Article][PubMed]
     [Google Scholar]
  67. Qiu J., Thorley-Lawson D. A. 2014; EBV microRNA BART 18-5p targets MAP3K2 to facilitate persistence in vivo by inhibiting viral replication in B cells. Proc Natl Acad Sci U S A 111:11157–11162 [View Article][PubMed]
     [Google Scholar]
  68. Riaz A., Dry I., Levy C. S., Hopkins J., Grey F., Shaw D. J., Dalziel R. G. 2014; Ovine herpesvirus-2-encoded microRNAs target virus genes involved in virus latency. J Gen Virol 95:472–480 [View Article][PubMed]
     [Google Scholar]
  69. Riley K. J., Rabinowitz G. S., Yario T. A., Luna J. M., Darnell R. B., Steitz J. A. 2012; EBV and human microRNAs co-target oncogenic and apoptotic viral and human genes during latency. EMBO J 31:2207–2221 [View Article][PubMed]
     [Google Scholar]
  70. Rodriguez A., Vigorito E., Clare S., Warren M. V., Couttet P., Soond D. R., van Dongen S., Grocock R. J., Das P. P.other authors 2007; Requirement of bic/microRNA-155 for normal immune function. Science 316:608–611 [View Article][PubMed]
     [Google Scholar]
  71. Roizman B., Whitley R. J. 2013; An inquiry into the molecular basis of HSV latency and reactivation. Annu Rev Microbiol 67:355–374 [View Article][PubMed]
     [Google Scholar]
  72. Seto E., Moosmann A., Grömminger 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:e1001063 [View Article][PubMed]
     [Google Scholar]
  73. Shen Z. Z., Pan X., Miao L. F., Ye H. Q., Chavanas S., Davrinche C., McVoy M., Luo M. H. 2014; Comprehensive analysis of human cytomegalovirus microRNA expression during lytic and quiescent infection. PLoS One 9:e88531 [View Article][PubMed]
     [Google Scholar]
  74. Sin S. H., Kim Y. B., Dittmer D. P. 2013; Latency locus complements microRNA 155 deficiency in vivo. J Virol 87:11908–11911 [View Article][PubMed]
     [Google Scholar]
  75. Sinclair J. H., Reeves M. B. 2013; Human cytomegalovirus manipulation of latently infected cells. Viruses 5:2803–2824 [View Article][PubMed]
     [Google Scholar]
  76. Skalsky R. L., Samols M. A., Plaisance K. B., Boss I. W., Riva A., Lopez M. C., Baker H. V., Renne R. 2007; Kaposi’s sarcoma-associated herpesvirus encodes an ortholog of miR-155. J Virol 81:12836–12845 [View Article][PubMed]
     [Google Scholar]
  77. Skalsky R. L., Corcoran D. L., Gottwein E., Frank C. L., Kang D., Hafner M., Nusbaum J. D., Feederle R., Delecluse H. J.other authors 2012; The viral and cellular microRNA targetome in lymphoblastoid cell lines. PLoS Pathog 8:e1002484 [View Article][PubMed]
     [Google Scholar]
  78. Smith M. S., Goldman D. C., Bailey A. S., Pfaffle D. L., Kreklywich C. N., Spencer D. B., Othieno F. A., Streblow D. N., Garcia J. V.other authors 2010; Granulocyte-colony stimulating factor reactivates human cytomegalovirus in a latently infected humanized mouse model. Cell Host Microbe 8:284–291 [View Article][PubMed]
     [Google Scholar]
  79. Stark T. J., Arnold J. D., Spector D. H., Yeo G. W. 2012; High-resolution profiling and analysis of viral and host small RNAs during human cytomegalovirus infection. J Virol 86:226–235 [View Article][PubMed]
     [Google Scholar]
  80. Stern-Ginossar N., Elefant N., Zimmermann A., Wolf D. G., Saleh N., Biton M., Horwitz E., Prokocimer Z., Prichard M.other authors 2007; Host immune system gene targeting by a viral miRNA. Science 317:376–381 [View Article][PubMed]
     [Google Scholar]
  81. Suffert G., Malterer G., Hausser J., Viiliäinen J., Fender A., Contrant M., Ivacevic T., Benes V., Gros F.other authors 2011; Kaposi’s sarcoma herpesvirus microRNAs target caspase 3 and regulate apoptosis. PLoS Pathog 7:e1002405 [View Article][PubMed]
     [Google Scholar]
  82. Sunil-Chandra N. P., Efstathiou S., Nash A. A. 1992; Murine gammaherpesvirus 68 establishes a latent infection in mouse B lymphocytes in vivo. J Gen Virol 73:3275–3279 [View Article][PubMed]
     [Google Scholar]
  83. Sunil-Chandra N. P., Arno J., Fazakerley J., Nash A. A. 1994; Lymphoproliferative disease in mice infected with murine gammaherpesvirus 68. Am J Pathol 145:818–826[PubMed]
     [Google Scholar]
  84. Tang S., Bertke A. S., Patel A., Wang K., Cohen J. I., Krause P. R. 2008; An acutely and latently expressed herpes simplex virus 2 viral microRNA inhibits expression of ICP34.5, a viral neurovirulence factor. Proc Natl Acad Sci U S A 105:10931–10936 [View Article][PubMed]
     [Google Scholar]
  85. Tang S., Patel A., Krause P. R. 2009; 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 83:1433–1442 [View Article][PubMed]
     [Google Scholar]
  86. Tang S., Bertke A. S., Patel A., Margolis T. P., Krause P. R. 2011; Herpes simplex virus 2 microRNA miR-H6 is a novel latency-associated transcript-associated microRNA, but reduction of its expression does not influence the establishment of viral latency or the recurrence phenotype. J Virol 85:4501–4509 [View Article][PubMed]
     [Google Scholar]
  87. Tarrant-Elorza M., Rossetto C. C., Pari G. S. 2014; Maintenance and replication of the human cytomegalovirus genome during latency. Cell Host Microbe 16:43–54 [View Article][PubMed]
     [Google Scholar]
  88. Umbach J. L., Kramer M. F., Jurak I., Karnowski H. W., Coen D. M., Cullen B. R. 2008; MicroRNAs expressed by herpes simplex virus 1 during latent infection regulate viral mRNAs. Nature 454:780–783[PubMed]
     [Google Scholar]
  89. Umbach J. L., Nagel M. A., Cohrs R. J., Gilden D. H., Cullen B. R. 2009; Analysis of human alphaherpesvirus microRNA expression in latently infected human trigeminal ganglia. J Virol 83:10677–10683 [View Article][PubMed]
     [Google Scholar]
  90. Umbach J. L., Wang K., Tang S., Krause P. R., Mont E. K., Cohen J. I., Cullen B. R. 2010; Identification of viral microRNAs expressed in human sacral ganglia latently infected with herpes simplex virus 2. J Virol 84:1189–1192 [View Article][PubMed]
     [Google Scholar]
  91. Vereide D. T., Seto E., Chiu Y. F., Hayes M., Tagawa T., Grundhoff A., Hammerschmidt W., Sugden B. 2014; Epstein–Barr virus maintains lymphomas via its miRNAs. Oncogene 33:1258–1264 [View Article][PubMed]
     [Google Scholar]
  92. Wahl A., Linnstaedt S. D., Esoda C., Krisko J. F., Martinez-Torres F., Delecluse H. J., Cullen B. R., Garcia J. V. 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 [View Article][PubMed]
     [Google Scholar]
  93. Xia T., O’Hara A., Araujo I., Barreto J., Carvalho E., Sapucaia J. B., Ramos J. C., Luz E., Pedroso C.other authors 2008; EBV microRNAs in primary lymphomas and targeting of CXCL-11 by ebv-mir-BHRF1-3. Cancer Res 68:1436–1442 [View Article][PubMed]
     [Google Scholar]
  94. Ye F. C., Zhou F. C., Xie J. P., Kang T., Greene W., Kuhne K., Lei X. F., Li Q. H., Gao S. J. 2008; Kaposi’s sarcoma-associated herpesvirus latent gene vFLIP inhibits viral lytic replication through NF-kappaB-mediated suppression of the AP-1 pathway: a novel mechanism of virus control of latency. J Virol 82:4235–4249 [View Article][PubMed]
     [Google Scholar]
  95. Yin Q., McBride J., Fewell C., Lacey M., Wang X., Lin Z., Cameron J., Flemington E. K. 2008; MicroRNA-155 is an Epstein–Barr virus-induced gene that modulates Epstein–Barr virus-regulated gene expression pathways. J Virol 82:5295–5306 [View Article][PubMed]
     [Google Scholar]
  96. Yin Q., Wang X., Fewell C., Cameron J., Zhu H., Baddoo M., Lin Z., Flemington E. K. 2010; MicroRNA miR-155 inhibits bone morphogenetic protein (BMP) signaling and BMP-mediated Epstein–Barr virus reactivation. J Virol 84:6318–6327 [View Article][PubMed]
     [Google Scholar]
  97. Zhao Y., Xu H., Yao Y., Smith L. P., Kgosana L., Green J., Petherbridge L., Baigent S. J., Nair V. 2011; Critical role of the virus-encoded microRNA-155 ortholog in the induction of Marek’s disease lymphomas. PLoS Pathog 7:e1001305 [View Article][PubMed]
     [Google Scholar]
  98. Zhu J. Y., Strehle M., Frohn A., Kremmer E., Höfig K. P., Meister G., Adler H. 2010; Identification and analysis of expression of novel microRNAs of murine gammaherpesvirus 68. J Virol 84:10266–10275 [View Article][PubMed]
     [Google Scholar]
  99. Ziegelbauer J. M., Sullivan C. S., Ganem D. 2009; Tandem array-based expression screens identify host mRNA targets of virus-encoded microRNAs. Nat Genet 41:130–134 [View Article][PubMed]
     [Google Scholar]
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Role of microRNAs in herpesvirus latency and persistence
J. Gen. Virol. 96, 739 (2015); https://doi.org/10.1099/vir.0.070862-0
/content/journal/jgv/10.1099/vir.0.070862-0
/content/journal/jgv/10.1099/vir.0.070862-0
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