1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Virology
  4. Volume 1, 2014
  5. Article

Annual Review of Virology

Volume 1, 2014

Balance and Stealth: The Role of Noncoding RNAs in the Regulation of Virus Gene Expression

Abstract

In the past two decades, our knowledge of gene regulation has been greatly expanded by the discovery of microRNAs (miRNAs). miRNAs are small (19–24 nt) noncoding RNAs (ncRNAs) found in metazoans, plants, and some viruses. They have been shown to regulate many cellular processes, including differentiation, maintenance of homeostasis, apoptosis, and the immune response. At present, there are over 300 known viral miRNAs encoded by diverse virus families. One well-characterized function of some viral miRNAs is the regulation of viral transcripts. Host miRNAs can also regulate viral gene expression. We propose that viruses take advantage of both host and viral ncRNA regulation to balance replication and infectious state (for example, latent versus lytic infection). As miRNA regulation can be reversed upon certain cellular stresses, we hypothesize that ncRNAs can serve viruses as barometers for cellular stress.

Keyword(s): autoregulation, latency, microRNAs, persistence, reactivation, stress
Loading

Article metrics loading...

/content/journals/10.1146/annurev-virology-031413-085439
2014-09-29
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/virology/1/1/annurev-virology-031413-085439.html?itemId=/content/journals/10.1146/annurev-virology-031413-085439&mimeType=html&fmt=ahah

Literature Cited

  1. Lee RC, Feinbaum RL, Ambros V. 1.  1993. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75:843–54 [Google Scholar]
  2. Ulitsky I, Bartel DP. 2.  2013. lincRNAs: genomics, evolution, and mechanisms. Cell 154:26–46 [Google Scholar]
  3. Wang KC, Chang HY. 3.  2011. Molecular mechanisms of long noncoding RNAs. Mol. Cell 43:904–14 [Google Scholar]
  4. Baltimore D. 4.  1971. Expression of animal virus genomes. Bacteriol. Rev. 35:235–41 [Google Scholar]
  5. Funk A, Truong K, Nagasaki T, Torres S, Floden N. 5.  et al. 2010. RNA structures required for production of subgenomic flavivirus RNA. J. Virol. 84:11407–17 [Google Scholar]
  6. Grundhoff A, Sullivan CS. 6.  2011. Virus-encoded microRNAs. Virology 411:325–43 [Google Scholar]
  7. Kincaid RP, Burke JM, Cox JC, de Villiers EM, Sullivan CS. 7.  2013. A human torque teno virus encodes a microRNA that inhibits interferon signaling. PLoS Pathog. 9:e1003818 [Google Scholar]
  8. Kincaid RP, Burke JM, Sullivan CS. 8.  2012. RNA virus microRNA that mimics a B-cell oncomiR. Proc. Natl. Acad. Sci. USA 109:3077–82 [Google Scholar]
  9. Yao Y, Smith LP, Nair V, Watson M. 9.  2014. An avian retrovirus uses canonical expression and processing mechanisms to generate viral microRNA. J. Virol. 88:2–9 [Google Scholar]
  10. Kincaid RP, Sullivan CS. 10.  2012. Virus-encoded microRNAs: an overview and a look to the future. PLoS Pathog. 8:e1003018 [Google Scholar]
  11. Sullivan CS. 11.  2008. New roles for large and small viral RNAs in evading host defences. Nat. Rev. Genet. 9:503–7 [Google Scholar]
  12. Umbach JL, Cullen BR. 12.  2009. The role of RNAi and microRNAs in animal virus replication and antiviral immunity. Genes Dev. 23:1151–64 [Google Scholar]
  13. Boss IW, Renne R. 13.  2010. Viral miRNAs: tools for immune evasion. Curr. Opin. Microbiol. 13:540–45 [Google Scholar]
  14. Sullivan CS, Cullen BR. 14.  2009. Non-coding regulatory RNAs of the DNA tumor viruses. DNA Tumor Viruses B Damania, JM Pipas 645–82 New York: Springer [Google Scholar]
  15. Sedger LM. 15.  2013. MicroRNA control of interferons and interferon induced anti-viral activity. Mol. Immunol. 56:781–93 [Google Scholar]
  16. Subramanian S, Steer CJ. 16.  2010. MicroRNAs as gatekeepers of apoptosis. J. Cell. Physiol. 223:289–98 [Google Scholar]
  17. Chen CZ, Schaffert S, Fragoso R, Loh C. 17.  2013. Regulation of immune responses and tolerance: the microRNA perspective. Immunol. Rev. 253:112–28 [Google Scholar]
  18. Farazi TA, Hoell JI, Morozov P, Tuschl T. 18.  2013. MicroRNAs in human cancer. Adv. Exp. Med. Biol. 774:1–20 [Google Scholar]
  19. Cullen BR. 19.  2004. Transcription and processing of human microRNA precursors. Mol. Cell 16:861–65 [Google Scholar]
  20. Flynt AS, Lai EC. 20.  2008. Biological principles of microRNA-mediated regulation: shared themes amid diversity. Nat. Rev. Genet. 9:831–42 [Google Scholar]
  21. Zisoulis DG, Lovci MT, Wilbert ML, Hutt KR, Liang TY. 21.  et al. 2010. Comprehensive discovery of endogenous Argonaute binding sites in Caenorhabditis elegans. Nat. Struct. Mol. Biol. 17:173–79 [Google Scholar]
  22. Lim LP, Lau NC, Garrett-Engele P, Grimson A, Schelter JM. 22.  et al. 2005. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 433:769–73 [Google Scholar]
  23. Seo GJ, Chen CJ, Sullivan CS. 23.  2009. Merkel cell polyomavirus encodes a microRNA with the ability to autoregulate viral gene expression. Virology 383:183–87 [Google Scholar]
  24. Seo GJ, Fink LHL, O'Hara B, Atwood WJ, Sullivan CS. 24.  2008. Evolutionarily conserved function of a viral microRNA. J. Virol. 82:9823–28 [Google Scholar]
  25. Sullivan CS, Grundhoff AT, Tevethia S, Pipas JM, Ganem D. 25.  2005. SV40-encoded microRNAs regulate viral gene expression and reduce susceptibility to cytotoxic T cells. Nature 435:682–86First demonstration of a viral miRNA target—the autoregulation of T antigen transcripts. [Google Scholar]
  26. Barth S, Pfuhl T, Mamiani A, Ehses C, Roemer K. 26.  et al. 2008. Epstein–Barr virus–encoded microRNA miR-BART2 down-regulates the viral DNA polymerase BALF5. Nucleic Acids Res. 36:666–75 [Google Scholar]
  27. Sullivan CS, Sung CK, Pack CD, Grundhoff A, Lukacher AE. 27.  et al. 2009. Murine polyomavirus encodes a microRNA that cleaves early RNA transcripts but is not essential for experimental infection. Virology 387:157–67 [Google Scholar]
  28. Bhattacharyya SN, Habermacher R, Martine U, Closs EI, Filipowicz W. 28.  2006. Stress-induced reversal of microRNA repression and mRNA P-body localization in human cells. Cold Spring Harb. Symp. Quant. Biol. 71:513–21 [Google Scholar]
  29. Leung AKL, Vyas S, Rood JE, Bhutkar A, Sharp PA, Chang P. 29.  2011. Poly(ADP-ribose) regulates stress responses and microRNA activity in the cytoplasm. Mol. Cell 42:489–99 [Google Scholar]
  30. Seo GJ, Kincaid RP, Phanaksri T, Burke JM, Pare JM. 30.  et al. 2013. Reciprocal inhibition between intracellular antiviral signaling and the RNAi machinery in mammalian cells. Cell Host Microbe 14:435–45 [Google Scholar]
  31. Bhattacharyya SN, Habermacher R, Martine U, Closs EI, Filipowicz W. 31.  2006. Relief of microRNA-mediated translational repression in human cells subjected to stress. Cell 125:1111–24 [Google Scholar]
  32. Vasudevan S, Tong Y, Steitz JA. 32.  2007. Switching from repression to activation: microRNAs can up-regulate translation. Science 318:1931–34 [Google Scholar]
  33. Vasudevan S, Steitz JA. 33.  2007. AU-rich-element-mediated upregulation of translation by FXR1 and Argonaute 2. Cell 128:1105–18 [Google Scholar]
  34. Ebert MS, Sharp PA. 34.  2012. Roles for microRNAs in conferring robustness to biological processes. Cell 149:515–24 [Google Scholar]
  35. Cassidy JJ, Jha AR, Posadas DM, Giri R, Venken KJT. 35.  et al. 2013. miR-9a minimizes the phenotypic impact of genomic diversity by buffering a transcription factor. Cell 155:1556–67 [Google Scholar]
  36. Mendell JT, Olson EN. 36.  2012. MicroRNAs in stress signaling and human disease. Cell 148:1172–87 [Google Scholar]
  37. Peláez N, Carthew RW. 37.  2012. Biological robustness and the role of microRNAs: a network perspective. Curr. Top. Dev. Biol. 99:237–55 [Google Scholar]
  38. Kozomara A, Griffiths-Jones S. 38.  2011. miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res. 39:D152–57 [Google Scholar]
  39. Grey F, Meyers H, White EA, Spector DH, Nelson J. 39.  2007. A human cytomegalovirus-encoded microRNA regulates expression of multiple viral genes involved in replication. PLoS Pathog. 3:e163Demonstrated that viral miRNAs can regulate several different viral transcripts. [Google Scholar]
  40. Murphy E, Vanícek J, Robins H, Shenk T, Levine AJ. 40.  2008. Suppression of immediate-early viral gene expression by herpesvirus-coded microRNAs: implications for latency. Proc. Natl. Acad. Sci. USA 105:5453–58First to suggest that miRNAs may regulate numerous viral transcripts in different herpesviruses. [Google Scholar]
  41. Forte E, Luftig MA. 41.  2011. The role of microRNAs in Epstein–Barr virus latency and lytic reactivation. Microbes Infect. 13:1156–67 [Google Scholar]
  42. Lieberman PM. 42.  2013. Keeping it quiet: chromatin control of gammaherpesvirus latency. Nat. Rev. Microbiol. 11:863–75 [Google Scholar]
  43. Wilson AC, Mohr I. 43.  2012. A cultured affair: HSV latency and reactivation in neurons. Trends Microbiol. 20:604–11 [Google Scholar]
  44. Umbach JL, Kramer MF, Jurak I, Karnowski HW, Coen DM, Cullen BR. 44.  2008. MicroRNAs expressed by herpes simplex virus 1 during latent infection regulate viral mRNAs. Nature 454:780–83Demonstrated that HSV-1 encodes autoregulatory miRNAs; implied a role in maintaining latency. [Google Scholar]
  45. Jurak I, Griffiths A, Coen DM. 45.  2011. Mammalian alphaherpesvirus miRNAs. Biochim. Biophys. Acta 1809:641–53 [Google Scholar]
  46. Boutell C, Everett RD. 46.  2013. Regulation of alphaherpesvirus infections by the ICP0 family of proteins. J. Gen. Virol. 94:465–81 [Google Scholar]
  47. Everett RD. 47.  2000. ICP0, a regulator of herpes simplex virus during lytic and latent infection. BioEssays 22:761–70 [Google Scholar]
  48. Everett RD, Parsy ML, Orr A. 48.  2009. Analysis of the functions of herpes simplex virus type 1 regulatory protein ICP0 that are critical for lytic infection and derepression of quiescent viral genomes. J. Virol. 83:4963–77 [Google Scholar]
  49. Smith MC, Boutell C, Davido DJ. 49.  2011. HSV-1 ICP0: paving the way for viral replication. Future Virol. 6:421–29 [Google Scholar]
  50. Flores O, Nakayama S, Whisnant AW, Javanbakht H, Cullen BR, Bloom DC. 50.  2013. Mutational inactivation of herpes simplex virus 1 microRNAs identifies viral mRNA targets and reveals phenotypic effects in culture. J. Virol. 87:6589–603An HSV-1 miRNA deletion mutant shows increased replication under only some experimental conditions. [Google Scholar]
  51. Dölken L, Pfeffer S, Koszinowski UH. 51.  2009. Cytomegalovirus microRNAs. Virus Genes 38:355–64 [Google Scholar]
  52. Huang Y, Qi Y, Ma Y, He R, Ji Y. 52.  et al. 2013. Down-regulation of human cytomegalovirus UL138, a novel latency-associated determinant, by hcmv-miR-UL36. J. Biosci. 38:479–85 [Google Scholar]
  53. Hancock MH, Tirabassi RS, Nelson JA. 53.  2012. Rhesus cytomegalovirus encodes seventeen microRNAs that are differentially expressed in vitro and in vivo. Virology 425:133–42 [Google Scholar]
  54. Stern-Ginossar N, Saleh N, Goldberg MD, Prichard M, Wolf DG, Mandelboim O. 54.  2009. Analysis of human cytomegalovirus–encoded microRNA activity during infection. J. Virol. 83:10684–93 [Google Scholar]
  55. Fu M, Gao Y, Zhou Q, Zhang Q, Peng Y. 55.  et al. 2014. Human cytomegalovirus latent infection alters the expression of cellular and viral microRNA. Gene 536:272–78 [Google Scholar]
  56. Dölken L, Krmpotic A, Kothe S, Tuddenham L, Tanguy M. 56.  et al. 2010. Cytomegalovirus microRNAs facilitate persistent virus infection in salivary glands. PLoS Pathog. 6:e1001150 [Google Scholar]
  57. Gottwein E, Corcoran DL, Mukherjee N, Skalsky RL, Hafner M. 57.  et al. 2011. Viral microRNA targetome of KSHV-infected primary effusion lymphoma cell lines. Cell Host Microbe 10:515–26 [Google Scholar]
  58. Grundhoff A, Sullivan CS, Ganem D. 58.  2006. A combined computational and microarray-based approach identifies novel microRNAs encoded by human gamma-herpesviruses. RNA 12:733–50 [Google Scholar]
  59. Haecker I, Gay LA, Yang Y, Hu J, Morse AM. 59.  et al. 2012. Ago HITS-CLIP expands understanding of Kaposi's sarcoma–associated herpesvirus miRNA function in primary effusion lymphomas. PLoS Pathog. 8:e1002884 [Google Scholar]
  60. Pfeffer S, Sewer A, Lagos-Quintana M, Sheridan R, Sander C. 60.  et al. 2005. Identification of microRNAs of the herpesvirus family. Nat. Methods 2:269–76 [Google Scholar]
  61. Zhu Y, Haecker I, Yang Y, Gao SJ, Renne R. 61.  2013. γ-Herpesvirus-encoded miRNAs and their roles in viral biology and pathogenesis. Curr. Opin. Virol. 3:266–75 [Google Scholar]
  62. Lukac DM, Kirshner JR, Ganem D. 62.  1999. Transcriptional activation by the product of open reading frame 50 of Kaposi's sarcoma–associated herpesvirus is required for lytic viral reactivation in B cells. J. Virol. 73:9348–61 [Google Scholar]
  63. Lin X, Liang D, He Z, Deng Q, Robertson ES, Lan K. 63.  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 [Google Scholar]
  64. Lu F, Stedman W, Yousef M, Renne R, Lieberman PM. 64.  2010. Epigenetic regulation of Kaposi's sarcoma–associated herpesvirus latency by virus-encoded microRNAs that target Rta and the cellular Rbl2-DNMT pathway. J. Virol. 84:2697–706Demonstrated that deletion of 10 of 12 KSHV pre-miRNAs results in increased lytic infection. [Google Scholar]
  65. Lei X, Bai Z, Ye F, Xie J, Kim CG. 65.  et al. 2010. Regulation of NF-κB inhibitor IκBα and viral replication by a KSHV microRNA. Nat. Cell Biol. 12:193–99Demonstrated that a KSHV miRNA can control viral replication through the NFκB pathway. [Google Scholar]
  66. Liang D, Gao Y, Lin X, He Z, Zhao Q. 66.  et al. 2011. A human herpesvirus miRNA attenuates interferon signaling and contributes to maintenance of viral latency by targeting IKKϵ. Cell Res. 21:793–806 [Google Scholar]
  67. Lu CC, Li Z, Chu CY, Feng J, Feng J. 67.  et al. 2010. MicroRNAs encoded by Kaposi's sarcoma–associated herpesvirus regulate viral life cycle. EMBO Rep. 11:784–90 [Google Scholar]
  68. Moody R, Zhu Y, Huang Y, Cui X, Jones T. 68.  et al. 2013. KSHV microRNAs mediate cellular transformation and tumorigenesis by redundantly targeting cell growth and survival pathways. PLoS Pathog. 9:e1003857 [Google Scholar]
  69. Ziegelbauer JM, Sullivan CS, Ganem D. 69.  2009. Tandem array–based expression screens identify host mRNA targets of virus-encoded microRNAs. Nat. Genet. 41:130–34 [Google Scholar]
  70. Umbach JL, Strelow LI, Wong SW, Cullen BR. 70.  2010. Analysis of rhesus rhadinovirus microRNAs expressed in virus-induced tumors from infected rhesus macaques. Virology 405:592–99 [Google Scholar]
  71. Bruce AG, Ryan JT, Thomas MJ, Peng X, Grundhoff A. 71.  et al. 2013. Next-generation sequence analysis of the genome of RFHVMn, the macaque homolog of Kaposi's sarcoma (KS)-associated herpesvirus, from a KS-like tumor of a pig-tailed macaque. J. Virol. 87:13676–93 [Google Scholar]
  72. Bai Z, Huang Y, Li W, Zhu Y, Jung JU. 72.  et al. 2014. Genomewide mapping and screening of Kaposi's sarcoma–associated herpesvirus (KSHV) 3′ untranslated regions identify bicistronic and polycistronic viral transcripts as frequent targets of KSHV microRNAs. J. Virol. 88:377–92 [Google Scholar]
  73. McClure LV, Kincaid RP, Burke JM, Grundhoff A, Sullivan CS. 73.  2013. Comprehensive mapping and analysis of Kaposi's sarcoma–associated herpesvirus 3′ UTRs identify differential posttranscriptional control of gene expression in lytic versus latent infection. J. Virol. 87:12838–49 [Google Scholar]
  74. Lin YT, Sullivan CS. 74.  2011. Expanding the role of Drosha to the regulation of viral gene expression. Proc. Natl. Acad. Sci. USA 108:11229–34 [Google Scholar]
  75. Cai X, Schäfer A, Lu S, Bilello JP, Desrosiers RC. 75.  et al. 2006. Epstein–Barr virus microRNAs are evolutionarily conserved and differentially expressed. PLoS Pathog. 2:e23 [Google Scholar]
  76. Pfeffer S, Zavolan M, Grässer FA, Chien M, Russo JJ. 76.  et al. 2004. Identification of virus-encoded microRNAs. Science 304:734–36First publication of viral miRNAs; suggested that miR-BART2 directly regulates the BALF5 polymerase transcript. [Google Scholar]
  77. Riley KJ, Rabinowitz GS, Yario TA, Luna JM, Darnell RB, Steitz JA. 77.  2012. EBV and human microRNAs co-target oncogenic and apoptotic viral and human genes during latency. EMBO J. 31:2207–21 [Google Scholar]
  78. Iizasa H, Wulff BE, Alla NR, Maragkakis M, Megraw M. 78.  et al. 2010. Editing of Epstein–Barr virus–encoded BART6 microRNAs controls their Dicer targeting and consequently affects viral latency. J. Biol. Chem. 285:33358–70 [Google Scholar]
  79. Seto E, Moosmann A, Grömminger S, Walz N, Grundhoff A, Hammerschmidt W. 79.  2010. Micro RNAs of Epstein–Barr virus promote cell cycle progression and prevent apoptosis of primary human B cells. PLoS Pathog. 6e1001063
  80. DeCaprio JA, Garcea RL. 80.  2013. A cornucopia of human polyomaviruses. Nat. Rev. Microbiol. 11:264–76 [Google Scholar]
  81. Korup S, Rietscher J, Calvignac-Spencer S, Trusch F, Hofmann J. 81.  et al. 2013. Identification of a novel human polyomavirus in organs of the gastrointestinal tract. PLoS ONE 8:e58021 [Google Scholar]
  82. Delbue S, Ferraresso M, Ghio L, Carloni C, Carluccio S. 82.  et al. 2013. A review on JC virus infection in kidney transplant recipients. Clin. Dev. Immunol. 2013:926391 [Google Scholar]
  83. Hirsch HH, Kardas P, Kranz D, Leboeuf C. 83.  2013. The human JC polyomavirus (JCPyV): virological background and clinical implications. APMIS 121:685–727 [Google Scholar]
  84. Rinaldo CH, Tylden GD, Sharma BN. 84.  2013. The human polyomavirus BK (BKPyV): virological background and clinical implications. APMIS 121:728–45 [Google Scholar]
  85. Kazem S, van der Meijden E, Feltkamp MCW. 85.  2013. The trichodysplasia spinulosa–associated polyomavirus: virological background and clinical implications. APMIS 121:770–82 [Google Scholar]
  86. Cole CN. 86.  1996. Polyomaviridae: the viruses and their replication. Fields Virology DM Knipe, PM Howley 1997–2043 Philadelphia: Lippincott-Raven, 3rd ed.. [Google Scholar]
  87. Cantalupo P, Doering A, Sullivan CS, Pal A, Peden KWC. 87.  et al. 2005. Complete nucleotide sequence of polyomavirus SA12. J. Virol. 79:13094–104 [Google Scholar]
  88. Chen CJ, Cox JE, Kincaid RP, Martinez A, Sullivan CS. 88.  2013. Divergent microRNA targetomes of closely related circulating strains of a polyomavirus. J. Virol. 87:11135–47 [Google Scholar]
  89. Chen CJ, Kincaid RP, Seo GJ, Bennett MD, Sullivan CS. 89.  2011. Insights into Polyomaviridae microRNA function derived from study of the bandicoot papillomatosis carcinomatosis viruses. J. Virol. 85:4487–500 [Google Scholar]
  90. Broekema NM, Imperiale MJ. 90.  2013. miRNA regulation of BK polyomavirus replication during early infection. Proc. Natl. Acad. Sci. USA 110:8200–5 [Google Scholar]
  91. Zhang S, Sroller V, Zanwar P, Chen CJ, Halvorson SJ. 91.  et al. 2014. Viral microRNA effects on pathogenesis of polyomavirus SV40 infections in Syrian golden hamsters. PLoS Pathogens 10:e1003912 [Google Scholar]
  92. Goff SP. 92.  2001. Retroviridae: the retroviruses and their replication. Fields Virology DM Knipe, PM Howley, DE Griffin, RA Lamb, MA Martin, B Roizman 1871–922 Philadelphia: Lippincott Williams & Wilkins, 4th ed.. [Google Scholar]
  93. Lin J, Cullen BR. 93.  2007. Analysis of the interaction of primate retroviruses with the human RNA interference machinery. J. Virol. 81:12218–26 [Google Scholar]
  94. Schmidt M, Herchenröder O, Heeney J, Rethwilm A. 94.  1997. Long terminal repeat U3 length polymorphism of human foamy virus. Virology 230:167–78 [Google Scholar]
  95. Rethwilm A, Baunach G, Netzer KO, Maurer B, Borisch B, ter Meulen V. 95.  1990. Infectious DNA of the human spumaretrovirus. Nucleic Acids Res. 18:733–38 [Google Scholar]
  96. Neves M, Périès J, Saïb A. 96.  1998. Study of human foamy virus proviral integration in chronically infected murine cells. Res. Virol. 149:393–401 [Google Scholar]
  97. Gregory SM, West JA, Dillon PJ, Hilscher C, Dittmer DP, Damania B. 97.  2009. Toll-like receptor signaling controls reactivation of KSHV from latency. Proc. Natl. Acad. Sci. USA 106:11725–30 [Google Scholar]
  98. Li X, Feng J, Sun R. 98.  2011. Oxidative stress induces reactivation of Kaposi's sarcoma–associated herpesvirus and death of primary effusion lymphoma cells. J. Virol. 85:715–24 [Google Scholar]
  99. Lu C, Zeng Y, Huang Z, Huang L, Qian C. 99.  et al. 2005. Human herpesvirus 6 activates lytic cycle replication of Kaposi's sarcoma–associated herpesvirus. Am. J. Pathol. 166:173–83 [Google Scholar]
  100. Palmisano I, Della Chiara G, D'Ambrosio RL, Huichalaf C, Brambilla P. 100.  et al. 2012. Amino acid starvation induces reactivation of silenced transgenes and latent HIV-1 provirus via down-regulation of histone deacetylase 4 (HDAC4). Proc. Natl. Acad. Sci. USA 109:E2284–93 [Google Scholar]
  101. Qin D, Zeng Y, Qian C, Huang Z, Lv Z. 101.  et al. 2008. Induction of lytic cycle replication of Kaposi's sarcoma–associated herpesvirus by herpes simplex virus type 1: involvement of IL-10 and IL-4. Cell Microbiol. 10:713–28 [Google Scholar]
  102. Taylor GM, Raghuwanshi SK, Rowe DT, Wadowsky RM, Rosendorff A. 102.  2011. Endoplasmic reticulum stress causes EBV lytic replication. Blood 118:5528–39 [Google Scholar]
  103. Vieira J, O'Hearn P, Kimball L, Chandran B, Corey L. 103.  2001. Activation of Kaposi's sarcoma–associated herpesvirus (human herpesvirus 8) lytic replication by human cytomegalovirus. J. Virol. 75:1378–86 [Google Scholar]
  104. Cai X, Li G, Laimins LA, Cullen BR. 104.  2006. Human papillomavirus genotype 31 does not express detectable microRNA levels during latent or productive virus replication. J. Virol. 80:10890–93 [Google Scholar]
  105. Gunasekharan V, Laimins LA. 105.  2013. Human papillomaviruses modulate microRNA 145 expression to directly control genome amplification. J. Virol. 87:6037–43 [Google Scholar]
  106. Crow JM. 106.  2012. HPV: the global burden. Nature 488:S2–3 [Google Scholar]
  107. Gu W, An J, Ye P, Zhao KN, Antonsson A. 107.  2011. Prediction of conserved microRNAs from skin and mucosal human papillomaviruses. Arch. Virol. 156:1161–71 [Google Scholar]
  108. Qian K, Pietilä T, Rönty M, Michon F, Frilander MJ. 108.  et al. 2013. Identification and validation of human papillomavirus encoded microRNAs. PLoS ONE 8:e70202 [Google Scholar]
  109. Doorbar J. 109.  2005. The papillomavirus life cycle. J. Clin. Virol. 32:Suppl. 1S7–15 [Google Scholar]
  110. Zacks MA, Paessler S. 110.  2010. Encephalitic alphaviruses. Vet. Microbiol. 140:281–86 [Google Scholar]
  111. Weaver SC. 111.  2005. Host range, amplification and arboviral disease emergence. Infectious Diseases from Nature: Mechanisms of Viral Emergence and Persistence CJ Peters, CH Calisher 33–44 Vienna: Springer [Google Scholar]
  112. Trobaugh DW, Gardner CL, Sun C, Haddow AD, Wang E. 112.  et al. 2013. RNA viruses can hijack vertebrate microRNAs to suppress innate immunity. Nature 506245–48Demonstrated that host miRNAs can restrict tissue tropism of virus infection in a nonengineered setting.
  113. Whisnant AW, Bogerd HP, Flores O, Ho P, Powers JG. 113.  et al. 2013. In-depth analysis of the interaction of HIV-1 with cellular microRNA biogenesis and effector mechanisms. mBio 4:e000193 [Google Scholar]
  114. Klase Z, Kale P, Winograd R, Gupta MV, Heydarian M. 114.  et al. 2007. HIV-1 TAR element is processed by Dicer to yield a viral micro-RNA involved in chromatin remodeling of the viral LTR. BMC Mol. Biol. 8:63 [Google Scholar]
  115. Omoto S, Ito M, Tsutsumi Y, Ichikawa Y, Okuyama H. 115.  et al. 2004. HIV-1 nef suppression by virally encoded microRNA. Retrovirology 1:44 [Google Scholar]
  116. Schopman NCT, Willemsen M, Liu YP, Bradley T, van Kampen A. 116.  et al. 2012. Deep sequencing of virus-infected cells reveals HIV-encoded small RNAs. Nucleic Acids Res. 40:414–27 [Google Scholar]
  117. Ahluwalia JK, Khan SZ, Soni K, Rawat P, Gupta A. 117.  et al. 2008. Human cellular microRNA hsa-miR-29a interferes with viral nef protein expression and HIV-1 replication. Retrovirology 5:117 [Google Scholar]
  118. Huang J, Wang F, Argyris E, Chen K, Liang Z. 118.  et al. 2007. Cellular microRNAs contribute to HIV-1 latency in resting primary CD4+ T lymphocytes. Nat. Med. 13:1241–47 [Google Scholar]
  119. Zhang Q, Chen CY, Yedavalli VSRK, Jeang KT. 119.  2013. NEAT1 long noncoding RNA and paraspeckle bodies modulate HIV-1 posttranscriptional expression. mBio 4:e00596–12 [Google Scholar]
  120. Skalsky RL, Cullen BR. 120.  2010. Viruses, microRNAs, and host interactions. Annu. Rev. Microbiol. 64:123–41 [Google Scholar]
  121. Huang T, Zhang X. 121.  2012. Functional analysis of a crustacean microRNA in host-virus interactions. J. Virol. 86:12997–3004 [Google Scholar]
  122. Kelly EJ, Nace R, Barber GN, Russell SJ. 122.  2010. Attenuation of vesicular stomatitis virus encephalitis through microRNA targeting. J. Virol. 84:1550–62 [Google Scholar]
  123. Pedersen IM, Cheng G, Wieland S, Volinia S, Croce CM. 123.  et al. 2007. Interferon modulation of cellular microRNAs as an antiviral mechanism. Nature 449:919–22 [Google Scholar]
  124. Cullen BR. 124.  2013. How do viruses avoid inhibition by endogenous cellular microRNAs?. PLoS Pathog. 9:e1003694 [Google Scholar]
  125. Sarasin-Filipowicz M, Krol J, Markiewicz I, Heim MH, Filipowicz W. 125.  2009. Decreased levels of microRNA miR-122 in individuals with hepatitis C responding poorly to interferon therapy. Nat. Med. 15:31–33 [Google Scholar]
  126. Berezikov E. 126.  2011. Evolution of microRNA diversity and regulation in animals. Nat. Rev. Genet. 12:846–60 [Google Scholar]
  127. Skalsky RL, Kang D, Linnstaedt SD, Cullen BR. 127.  2014. Evolutionary conservation of primate lymphocryptovirus microRNA targets. J. Virol. 88:1617–35 [Google Scholar]
  128. Lecellier C-H, Dunoyer P, Arar K, Lehmann-Che J, Eyquem S. 128.  et al. 2005. A cellular microRNA mediates antiviral defense in human cells. Science 308:557–60 [Google Scholar]
  129. Kamel W, Segerman B, Öberg D, Punga T, Akusjärvi G. 129.  2013. The adenovirus VA RNA–derived miRNAs are not essential for lytic virus growth in tissue culture cells. Nucleic Acids Res. 41:4802–12 [Google Scholar]
  130. Ma Y, Mathews MB. 130.  1996. Structure, function, and evolution of adenovirus-associated RNA: a phylogenetic approach. J. Virol. 70:5083–99 [Google Scholar]
  131. Maran A, Mathews MB. 131.  1988. Characterization of the double-stranded RNA implicated in the inhibition of protein synthesis in cells infected with a mutant adenovirus defective for VA RNA. Virology 164:106–13 [Google Scholar]
  132. Furuse Y, Ornelles DA, Cullen BR. 132.  2013. Persistently adenovirus-infected lymphoid cells express microRNAs derived from the viral VAI and especially VAII RNA. Virology 447:140–45 [Google Scholar]
  133. Garnett CT, Erdman D, Xu W, Gooding LR. 133.  2002. Prevalence and quantitation of species C adenovirus DNA in human mucosal lymphocytes. J. Virol. 76:10608–16 [Google Scholar]
  134. Aparicio O, Razquin N, Zaratiegui M, Narvaiza I, Fortes P. 134.  2006. Adenovirus virus-associated RNA is processed to functional interfering RNAs involved in virus production. J. Virol. 80:1376–84 [Google Scholar]
  135. Sun R, Lin SF, Gradoville L, Miller G. 135.  1996. Polyadenylylated nuclear RNA encoded by Kaposi sarcoma–associated herpesvirus. Proc. Natl. Acad. Sci. USA 93:11883–88 [Google Scholar]
  136. Mitton-Fry RM, DeGregorio SJ, Wang J, Steitz TA, Steitz JA. 136.  2010. Poly(A) tail recognition by a viral RNA element through assembly of a triple helix. Science 330:1244–47 [Google Scholar]
  137. Conrad NK, Mili S, Marshall EL, Shu MD, Steitz JA. 137.  2006. Identification of a rapid mammalian deadenylation-dependent decay pathway and its inhibition by a viral RNA element. Mol. Cell 24:943–53 [Google Scholar]
  138. Borah S, Darricarrère N, Darnell A, Myoung J, Steitz JA. 138.  2011. A viral nuclear noncoding RNA binds re-localized poly(A) binding protein and is required for late KSHV gene expression. PLoS Pathog. 7:e1002300 [Google Scholar]
  139. Rossetto CC, Tarrant-Elorza M, Verma S, Purushothaman P, Pari GS. 139.  2013. Regulation of viral and cellular gene expression by Kaposi's sarcoma–associated herpesvirus polyadenylated nuclear RNA. J. Virol. 87:5540–53 [Google Scholar]
  140. Rossetto CC, Pari G. 140.  2012. KSHV PAN RNA associates with demethylases UTX and JMJD3 to activate lytic replication through a physical interaction with the virus genome. PLoS Pathog. 8:e1002680 [Google Scholar]
  141. Arias C, Weisburd B, Stern-Ginossar N, Mercier A, Madrid AS. 141.  et al. 2014. KSHV 2.0: a comprehensive annotation of the Kaposi's sarcoma–associated herpesvirus genome using next-generation sequencing reveals novel genomic and functional features. PLoS Pathog. 10:e1003847 [Google Scholar]
  142. Haussecker D, Kay MA. 142.  2010. miR-122 continues to blaze the trail for microRNA therapeutics. Mol. Ther. 18:240–42 [Google Scholar]
  143. Jopling CL, Yi M, Lancaster AM, Lemon SM, Sarnow P. 143.  2005. Modulation of hepatitis C virus RNA abundance by a liver-specific microRNA. Science 309:1577–81 [Google Scholar]
  144. tenOever B. 144.  2009. MicroManipulating viral-based therapeutics. Discov. Med. 8:51–54 [Google Scholar]
  145. Ibrišimović M, Kneidinger D, Lion T, Klein R. 145.  2013. An adenoviral vector–based expression and delivery system for the inhibition of wild-type adenovirus replication by artificial microRNAs. Antiviral Res. 97:10–23 [Google Scholar]
  146. Ylösmäki E, Hakkarainen T, Hemminki A, Visakorpi T, Andino R, Saksela K. 146.  2008. Generation of a conditionally replicating adenovirus based on targeted destruction of E1A mRNA by a cell type–specific microRNA. J. Virol. 82:11009–15 [Google Scholar]
  147. Langlois RA, Albrecht RA, Kimble B, Sutton T, Shapiro JS. 147.  et al. 2013. MicroRNA-based strategy to mitigate the risk of gain-of-function influenza studies. Nat. Biotechnol. 31:844–47 [Google Scholar]
  148. Gall A, Palser A. 148.  2013. An elephantine viral problem. Nat. Rev. Microbiol. 11:512 [Google Scholar]
  149. Furuse Y, Dastjerdi A, Steinbach F, Cullen BR. 149.  2014. Analysis of viral microRNA expression by elephant endotheliotropic herpesvirus 1. Virology454–55:102–8
  150. Ross N, Gandhi MK, Nourse JP. 150.  2013. The Epstein–Barr virus microRNA BART11-5p targets the early B-cell transcription factor EBF1. Am. J. Blood Res. 3:210–24 [Google Scholar]
  151. Lung RW, Tong JH, Sung Y, Leung P, Ng DC. 151.  et al. 2009. Modulation of LMP2A expression by a newly identified Epstein–Barr virus–encoded microRNA miR-BART22. Neoplasia 11:1174–84 [Google Scholar]
  152. Tang S, Patel A, Krause PR. 152.  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. 83:1433–42 [Google Scholar]
  153. Tang S, Bertke AS, Patel A, Wang K, Cohen JI, Krause PR. 153.  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. USA 105:10931–36 [Google Scholar]
  154. Jaber T, Workman A, Jones C. 154.  2010. Small noncoding RNAs encoded within the bovine herpesvirus 1 latency-related gene can reduce steady-state levels of infected cell protein 0 (bICP0). J. Virol. 84:6297–307 [Google Scholar]
  155. Waidner LA, Burnside J, Anderson AS, Bernberg EL, German MA. 155.  et al. 2011. A microRNA of infectious laryngotracheitis virus can downregulate and direct cleavage of ICP4 mRNA. Virology 411:25–31 [Google Scholar]
  156. Muylkens B, Coupeau D, Dambrine G, Trapp S, Rasschaert D. 156.  2010. Marek's disease virus microRNA designated Mdv1-pre-miR-M4 targets both cellular and viral genes. Arch. Virol. 155:1823–37 [Google Scholar]
  157. Strassheim S, Stik G, Rasschaert D, Laurent S. 157.  2012. Mdv1-miR-M7-5p, located in the newly identified first intron of the latency-associated transcript of Marek's disease virus, targets the immediate-early genes ICP4 and ICP27. J. Gen. Virol. 93:1731–42 [Google Scholar]
  158. Singh CP, Singh J, Nagaraju J. 158.  2012. A baculovirus-encoded microRNA (miRNA) suppresses its host miRNA biogenesis by regulating the Exportin-5 cofactor Ran. J. Virol. 86:7867–79 [Google Scholar]
  159. Hussain M, Taft RJ, Asgari S. 159.  2008. An insect virus–encoded microRNA regulates viral replication. J. Virol. 82:9164–70 [Google Scholar]
  160. Wu YL, Wu CP, Liu CYY, Hsu PWC, Wu EC, Chao YC. 160.  2011. A non-coding RNA of insect HzNV-1 virus establishes latent viral infection through microRNA. Sci. Rep. 1:60 [Google Scholar]
  161. He Y, Yang K, Zhang X. 161.  2014. Viral microRNAs targeting virus genes promote virus infection in shrimp in vivo. J. Virol. 88:1104–12 [Google Scholar]
  162. Yanagawa-Matsuda A, Kitamura T, Higashino F, Yamano S, Totsuka Y, Shindoh M. 162.  2012. E1A expression might be controlled by miR-214 in cells with low adenovirus productivity. Virus Res. 170:85–90 [Google Scholar]
  163. Sagan SM, Sarnow P, Wilson JA. 163.  2013. Modulation of GB virus B RNA abundance by microRNA-122: dependence on and escape from microRNA-122 restriction. J. Virol. 87:7338–47 [Google Scholar]
  164. Zhang G, Li Y, Zheng S, Liu M, Li X, Tang H. 164.  2010. Suppression of hepatitis B virus replication by microRNA-199a-3p and microRNA-210. Antiviral Res. 88:169–75 [Google Scholar]
  165. Yan Q, Li W, Tang Q, Yao S, Lv Z. 165.  et al. 2013. Cellular microRNAs 498 and 320d regulate herpes simplex virus 1 induction of Kaposi's sarcoma–associated herpesvirus lytic replication by targeting RTA. PLoS ONE 8:e55832 [Google Scholar]
  166. Ma YJ, Yang J, Fan XL, Zhao HB, Hu W. 166.  et al. 2012. Cellular microRNA let-7c inhibits M1 protein expression of the H1N1 influenza A virus in infected human lung epithelial cells. J. Cell. Mol. Med. 16:2539–46 [Google Scholar]
  167. Sun JZ, Wang J, Yuan D, Wang S, Li Z. 167.  et al. 2013. Cellular microRNA miR-181b inhibits replication of mink enteritis virus by repression of non-structural protein 1 translation. PLoS ONE 8:e81515 [Google Scholar]
  168. Wen B, Dai H, Yang Y, Zhuang Y, Sheng R. 168.  2013. MicroRNA-23b inhibits enterovirus 71 replication through downregulation of EV71 VPL protein. Intervirology 56:195–200 [Google Scholar]
  169. Zheng Z, Ke X, Wang M, He S, Li Q. 169.  et al. 2013. Human microRNA hsa-miR-296-5p suppresses enterovirus 71 replication by targeting the viral genome. J. Virol. 87:5645–56 [Google Scholar]
  170. Wang L, Qin Y, Tong L, Wu S, Wang Q. 170.  et al. 2012. miR-342-5p suppresses coxsackievirus B3 biosynthesis by targeting the 2C-coding region. Antiviral Res. 93:270–79 [Google Scholar]
  171. Tong L, Lin L, Wu S, Guo Z, Wang T. 171.  et al. 2013. Mir-10a* up-regulates coxsackievirus B3 biosynthesis by targeting the 3D-coding sequence. Nucleic Acids Res. 41:3760–71 [Google Scholar]
  172. Sisk JM, Witwer KW, Tarwater PM, Clements JE. 172.  2013. SIV replication is directly downregulated by four antiviral miRNAs. Retrovirology 10:95 [Google Scholar]
/content/journals/10.1146/annurev-virology-031413-085439
Loading
Balance and Stealth: The Role of Noncoding RNAs in the Regulation of Virus Gene Expression
Annual Review of Virology 1, 89 (2014); https://doi.org/10.1146/annurev-virology-031413-085439
/content/journals/10.1146/annurev-virology-031413-085439
/content/journals/10.1146/annurev-virology-031413-085439
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error