Skip to main content

Current Knowledge of MicroRNAs and Noncoding RNAs in Virus-Infected Cells

  • Protocol
  • First Online:
RNA Interference

Part of the book series: Methods in Molecular Biology ((MIMB,volume 623))

Abstract

Within the past few years, microRNAs (miRNAs) and other noncoding RNAs (ncRNAs) have emerged as elements with critically high importance in posttranscriptional control of cellular and, more recently, viral processes. Endogenously produced by a component of the miRNA-guided RNA silencing machinery known as Dicer, miRNAs are known to control messenger RNA (mRNA) translation through recognition of specific binding sites usually located in their 3′ untranslated region. Recent evidences indicate that the host miRNA pathway may represent an adapted antiviral defense mechanism that can act either by direct miRNA-mediated modulation of viral gene expression or through recognition and inactivation of structured viral RNA species by the protein components of the RNA silencing machinery such as Dicer. This latter process, however, is a double-edge sword, as it may yield viral miRNAs exerting gene regulatory properties on both host and viral mRNAs. Our knowledge of the interaction between viruses and host RNA silencing machineries, and how this influences the course of infection, is becoming increasingly complex. This chapter aims to summarize our current knowledge about viral miRNAs/ncRNAs and their targets, as well as cellular miRNAs that are modulated by viruses upon infection.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Yekta, S., Shih, I.H. and Bartel, D.P. (2004) MicroRNA-directed cleavage of HOXB8 mRNA. Science 304, 594–596.

    Article  CAS  PubMed  Google Scholar 

  2. Mansfield, J.H., Harfe, B.D., Nissen, R., Obenauer, J., Srineel, J., Chaudhuri, A., et al. (2004) MicroRNA-responsive ‘sensor’ transgenes uncover Hox-like and other developmentally regulated patterns of vertebrate microRNA expression. Nat. Genet. 36, 1079–1083.

    Article  CAS  PubMed  Google Scholar 

  3. Vasudevan, S., Tong, Y. and Steitz, J.A. (2007) Switching from repression to activation: microRNAs can up-regulate translation. Science 318, 1931–1934.

    Article  CAS  PubMed  Google Scholar 

  4. Griffiths-Jones, S., Grocock, R.J., van Dongen, S., Bateman, A. and Enright, A.J. (2006) miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res. 34, D140–144.

    Article  CAS  PubMed  Google Scholar 

  5. Griffiths-Jones, S., Saini, H.K., van Dongen, S. and Enright, A.J. (2008) miRBase: tools for microRNA genomics. Nucleic Acids Res. 36, D154–158.

    Article  CAS  PubMed  Google Scholar 

  6. Aravin, A.A., Lagos-Quintana, M., Yalcin, A., Zavolan, M., Marks, D., Snyder, B., et al. (2003) The small RNA profile during Drosophila melanogaster development. Dev. Cell 5, 337–350.

    Article  CAS  PubMed  Google Scholar 

  7. Ambros, V., Lee, R.C., Lavanway, A., Williams, P.T. and Jewell, D. (2003) MicroRNAs and other tiny endogenous RNAs in C. elegans. Curr. Biol. 13, 807–818.

    Article  CAS  PubMed  Google Scholar 

  8. Swaminathan, S. (2008) Noncoding RNAs produced by oncogenic human herpesviruses. J. Cell Physiol. 216, 321–326.

    Article  CAS  PubMed  Google Scholar 

  9. Clemens, M.J., Laing, K.G., Jeffrey, I.W., Schofield, A., Sharp, T.V., Elia, A., et al. (1994) Regulation of the interferon-inducible eIF-2 alpha protein kinase by small RNAs. Biochimie 76, 770–778.

    Article  CAS  PubMed  Google Scholar 

  10. Kitajewski, J., Schneider, R.J., Safer, B., Munemitsu, S.M., Samuel, C.E., Thimmappaya, B. and Shenk, T. (1986) Adenovirus VAI RNA antagonizes the antiviral action of interferon by preventing activation of the interferon-induced eIF-2 alpha kinase. Cell 45, 195–200.

    Article  CAS  PubMed  Google Scholar 

  11. Furtado, M.R., Subramanian, S., Bhat, R.A., Fowlkes, D.M., Safer, B. and Thimmappaya, B. (1989) Functional dissection of adenovirus VAI RNA. J. Virol. 63, 3423–3434.

    CAS  PubMed  Google Scholar 

  12. Lu, S. and Cullen, B.R. (2004) Adenovirus VA1 noncoding RNA can inhibit small interfering RNA and microRNA biogenesis. J. Virol. 78, 12868–12876.

    Article  CAS  PubMed  Google Scholar 

  13. Cai, X., Hagedorn, C.H. and Cullen, B.R. (2004) Human microRNAs are processed from capped, polyadenylated transcripts that can also function as mRNAs. RNA 10, 1957–1966.

    Article  CAS  PubMed  Google Scholar 

  14. Lee, Y., Kim, M., Han, J., Yeom, K.H., Lee, S., Baek, S.H. and Kim, V.N. (2004) MicroRNA genes are transcribed by RNA polymerase II. EMBO J. 23, 4051–4060.

    Article  CAS  PubMed  Google Scholar 

  15. Lee, Y., Ahn, C., Han, J., Choi, H., Kim, J., Yim, J., et al. (2003) The nuclear RNase III Drosha initiates microRNA processing. Nature 425, 415–419.

    Article  CAS  PubMed  Google Scholar 

  16. Denli, A.M., Tops, B.B., Plasterk, R.H., Ketting, R.F. and Hannon, G.J. (2004) Processing of primary microRNAs by the Microprocessor complex. Nature 432, 231–235.

    Article  CAS  PubMed  Google Scholar 

  17. Gregory, R.I., Yan, K.P., Amuthan, G., Chendrimada, T., Doratotaj, B., Cooch, N. and Shiekhattar, R. (2004) The Micropro-cessor complex mediates the genesis of microRNAs. Nature 432, 235–240.

    Article  CAS  PubMed  Google Scholar 

  18. Han, J., Lee, Y., Yeom, K.H., Kim, Y.K., Jin, H. and Kim, V.N. (2004) The Drosha-DGCR8 complex in primary microRNA processing. Genes Dev. 18, 3016–3027.

    Article  CAS  PubMed  Google Scholar 

  19. Landthaler, M., Yalcin, A. and Tuschl, T. (2004) The human DiGeorge syndrome critical region gene 8 and its D. melanogaster homolog are required for miRNA biogenesis. Curr. Biol. 14, 2162–2167.

    Article  CAS  PubMed  Google Scholar 

  20. Ruby, J.G., Jan, C.H. and Bartel, D.P. (2007) Intronic microRNA precursors that bypass Drosha processing. Nature 448, 83–86.

    Article  CAS  PubMed  Google Scholar 

  21. Berezikov, E., Chung, W.J., Willis, J., Cuppen, E. and Lai, E.C. (2007) Mammalian mirtron genes. Mol. Cell 28, 328–336.

    Article  CAS  PubMed  Google Scholar 

  22. Bohnsack, M.T., Czaplinski, K. and Gorlich, D. (2004) Exportin 5 is a RanGTP-dependent dsRNA-binding protein that mediates nuclear export of pre-miRNAs. RNA 10, 185–191.

    Article  CAS  PubMed  Google Scholar 

  23. Brownawell, A.M. and Macara, I.G. (2002) Exportin-5, a novel karyopherin, mediates nuclear export of double-stranded RNA binding proteins. J. Cell Biol. 156, 53–64.

    Article  CAS  PubMed  Google Scholar 

  24. Lund, E., Guttinger, S., Calado, A., Dahlberg, J.E. and Kutay, U. (2004) Nuclear export of microRNA precursors. Science 303, 95–98.

    Article  CAS  PubMed  Google Scholar 

  25. Yi, R., Qin, Y., Macara, I.G. and Cullen, B.R. (2003) Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Dev. 17, 3011–3016.

    Article  CAS  PubMed  Google Scholar 

  26. Zhang, H., Kolb, F.A., Jaskiewicz, L., Westhof, E. and Filipowicz, W. (2004) Single processing center models for human Dicer and bacterial RNase III. Cell 118, 57–68.

    Article  CAS  PubMed  Google Scholar 

  27. Bernstein, E., Caudy, A.A., Hammond, S.M. and Hannon, G.J. (2001) Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature, 409, 363–366.

    Article  CAS  PubMed  Google Scholar 

  28. Provost, P., Dishart, D., Doucet, J., Frendewey, D., Samuelsson, B. and Radmark, O. (2002) Ribonuclease activity and RNA binding of recombinant human Dicer. EMBO J. 21, 5864–5874.

    Article  CAS  PubMed  Google Scholar 

  29. Zhang, H., Kolb, F.A., Brondani, V., Billy, E. and Filipowicz, W. (2002) Human Dicer preferentially cleaves dsRNAs at their termini without a requirement for ATP. EMBO J. 21, 5875–5885.

    Article  CAS  PubMed  Google Scholar 

  30. Gatignol, A., Buckler-White, A., Berkhout, B. and Jeang, K.T. (1991) Characterization of a human TAR RNA-binding protein that activates the HIV-1 LTR. Science 251, 1597–1600.

    Article  CAS  PubMed  Google Scholar 

  31. Haase, A.D., Jaskiewicz, L., Zhang, H., Laine, S., Sack, R., Gatignol, A. and Filipowicz, W. (2005) TRBP, a regulator of cellular PKR and HIV-1 virus expression, interacts with Dicer and functions in RNA silencing. EMBO Rep. 6, 961–967.

    Article  CAS  PubMed  Google Scholar 

  32. Chendrimada, T.P., Gregory, R.I., Kumaraswamy, E., Norman, J., Cooch, N., Nishikura, K. and Shiekhattar, R. (2005) TRBP recruits the Dicer complex to Ago2 for microRNA processing and gene silencing. Nature 436, 740–744.

    Article  CAS  PubMed  Google Scholar 

  33. Schwarz, D.S., Hutvagner, G., Du, T., Xu, Z., Aronin, N. and Zamore, P.D. (2003) Asymmetry in the assembly of the RNAi enzyme complex. Cell 115, 199–208.

    Article  CAS  PubMed  Google Scholar 

  34. Matranga, C., Tomari, Y., Shin, C., Bartel, D.P. and Zamore, P.D. (2005) Passenger-strand cleavage facilitates assembly of siRNA into Ago2-containing RNAi enzyme complexes. Cell 123, 607–620.

    Article  CAS  PubMed  Google Scholar 

  35. Plante, I., Davidovic, L., Ouellet, D.L., Gobeil, L.A., Tremblay, S., Khandjian, E.W. and Provost, P. (2006) Dicer-derived microRNAs are utilized by the fragile X mental retardation protein for assembly on target RNAs. J. Biomed. Biotechnol. 2006, 64347.

    PubMed  Google Scholar 

  36. Bagga, S., Bracht, J., Hunter, S., Massirer, K., Holtz, J., Eachus, R. and Pasquinelli, A.E. (2005) Regulation by let-7 and lin-4 miRNAs results in target mRNA degradation. Cell 122, 553–563.

    Article  CAS  PubMed  Google Scholar 

  37. Liu, J., Valencia-Sanchez, M.A., Hannon, G.J. and Parker, R. (2005) MicroRNA-dependent localization of targeted mRNAs to mammalian P-bodies. Nat. Cell Biol. 7, 719–723.

    Article  CAS  PubMed  Google Scholar 

  38. Teixeira, D., Sheth, U., Valencia-Sanchez, M.A., Brengues, M. and Parker, R. (2005) Processing bodies require RNA for assembly and contain nontranslating mRNAs. RNA 11, 371–382.

    Article  CAS  PubMed  Google Scholar 

  39. Eystathioy, T., Chan, E.K., Tenenbaum, S.A., Keene, J.D., Griffith, K. and Fritzler, M.J. (2002) A phosphorylated cytoplasmic autoantigen, GW182, associates with a unique population of human mRNAs within novel cytoplasmic speckles. Mol. Biol. Cell 13, 1338–1351.

    Article  CAS  PubMed  Google Scholar 

  40. Eulalio, A., Behm-Ansmant, I., Schweizer, D. and Izaurralde, E. (2007) P-body formation is a consequence, not the cause, of RNA-mediated gene silencing. Mol. Cell Biol. 27, 3970–3981.

    Article  CAS  PubMed  Google Scholar 

  41. Eystathioy, T., Jakymiw, A., Chan, E.K., Seraphin, B., Cougot, N. and Fritzler, M.J. (2003) The GW182 protein colocalizes with mRNA degradation associated proteins hDcp1 and hLSm4 in cytoplasmic GW bodies. RNA 9, 1171–1173.

    Article  CAS  PubMed  Google Scholar 

  42. Fukuhara, N., Ebert, J., Unterholzner, L., Lindner, D., Izaurralde, E. and Conti, E. (2005) SMG7 is a 14-3-3-like adaptor in the nonsense-mediated mRNA decay pathway. Mol. Cell 17, 537–547.

    Article  CAS  PubMed  Google Scholar 

  43. Unterholzner, L. and Izaurralde, E. (2004) SMG7 acts as a molecular link between mRNA surveillance and mRNA decay. Mol. Cell 16, 587–596.

    Article  CAS  PubMed  Google Scholar 

  44. Bartel, D.P. (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281–297.

    Article  CAS  PubMed  Google Scholar 

  45. Vella, M.C., Reinert, K. and Slack, F.J. (2004) Architecture of a validated microRNA:target interaction. Chem. Biol. 11, 1619–1623.

    Article  CAS  PubMed  Google Scholar 

  46. Pall, G.S., Codony-Servat, C., Byrne, J., Ritchie, L. and Hamilton, A. (2007) Carbodiimide-mediated cross-linking of RNA to nylon membranes improves the detection of siRNA, miRNA and piRNA by northern blot. Nucleic Acids Res. 35, e60.

    Article  PubMed  CAS  Google Scholar 

  47. Pall, G.S. and Hamilton, A.J. (2008) Improved Northern blot method for enhanced detection of small RNA. Nat. Protoc. 3, 1077–1084.

    Article  CAS  PubMed  Google Scholar 

  48. Ouellet, D.L., Plante, I., Landry, P., Barat, C., Janelle, M.E., Flamand, L., Tremblay, M.J. and Provost, P. (2008) Identification of functional microRNAs released through asymmetrical processing of HIV-1 TAR element. Nucleic Acids Res. 36, 2353–2365.

    Article  CAS  PubMed  Google Scholar 

  49. Friedlander, M.R., Chen, W., Adamidi, C., Maaskola, J., Einspanier, R., Knespel, S. and Rajewsky, N. (2008) Discovering microRNAs from deep sequencing data using miRDeep. Nat. Biotechnol. 26, 407–415.

    Article  PubMed  CAS  Google Scholar 

  50. Heldwein, E.E. and Krummenacher, C. (2008) Entry of herpesviruses into mammalian cells. Cell Mol. Life Sci. 65, 1653–1668.

    Article  CAS  PubMed  Google Scholar 

  51. Pfeffer, S., Sewer, A., Lagos-Quintana, M., Sheridan, R., Sander, C., Grasser, F.A., et al. (2005) Identification of microRNAs of the herpesvirus family. Nat. Methods 2, 269–276.

    Article  CAS  PubMed  Google Scholar 

  52. Pfeffer, S., Zavolan, M., Grasser, F.A., Chien, M., Russo, J.J., Ju, J., et al. (2004) Identification of virus-encoded microRNAs. Science 304, 734–736.

    Article  CAS  PubMed  Google Scholar 

  53. Buck, A.H., Santoyo-Lopez, J., Robertson, K.A., Kumar, D.S., Reczko, M. and 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.

    Article  CAS  PubMed  Google Scholar 

  54. Dolken, L., Perot, J., Cognat, V., Alioua, A., John, M., Soutschek, J., et al. (2007) Mouse cytomegalovirus microRNAs dominate the cellular small RNA profile during lytic infection and show features of posttranscriptional regulation. J. Virol. 81, 13771–13782.

    Article  PubMed  CAS  Google Scholar 

  55. Cui, C., Griffiths, A., Li, G., Silva, L.M., Kramer, M.F., Gaasterland, T., Wang, X.J. and Coen, D.M. (2006) Prediction and identification of herpes simplex virus 1-encoded microRNAs. J. Virol. 80, 5499–5508.

    Article  CAS  PubMed  Google Scholar 

  56. Bloom, D.C. (2004) HSV LAT and neuronal survival. Int. Rev. Immunol. 23, 187–198.

    Article  CAS  PubMed  Google Scholar 

  57. Cuchet, D., Ferrera, R., Lomonte, P. and Epstein, A.L. (2005) Characterization of antiproliferative and cytotoxic properties of the HSV-1 immediate-early ICPo protein. J. Gene Med. 7, 1187–1199.

    Article  CAS  PubMed  Google Scholar 

  58. La Frazia, S., Amici, C. and Santoro, M.G. (2006) Antiviral activity of proteasome inhibitors in herpes simplex virus-1 infection: role of nuclear factor-kappaB. Antivir. Ther. 11, 995–1004.

    PubMed  Google Scholar 

  59. Umbach, J.L., Kramer, M.F., Jurak, I., Karnowski, H.W., Coen, D.M. and Cullen, B.R. (2008) MicroRNAs expressed by herpes simplex virus 1 during latent infection regulate viral mRNAs. Nature 454, 780–783.

    CAS  PubMed  Google Scholar 

  60. Halford, W.P., Kemp, C.D., Isler, J.A., Davido, D.J. and Schaffer, P.A. (2001) ICP0, ICP4, or VP16 expressed from adenovirus vectors induces reactivation of latent herpes simplex virus type 1 in primary cultures of latently infected trigeminal ganglion cells. J. Virol. 75, 6143–6153.

    Article  CAS  PubMed  Google Scholar 

  61. Thompson, R.L. and Stevens, J.G. (1983) Biological characterization of a herpes simplex virus intertypic recombinant which is completely and specifically non-neurovirulent. Virology 131, 171–179.

    Article  CAS  PubMed  Google Scholar 

  62. Tang, S., Bertke, A.S., Patel, A., Wang, K., Cohen, J.I. and 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.

    Article  CAS  PubMed  Google Scholar 

  63. Brady, G., MacArthur, G.J. and Farrell, P.J. (2007) Epstein-Barr virus and Burkitt lymphoma. J. Clin. Pathol. 60, 1397–1402.

    CAS  PubMed  Google Scholar 

  64. Tao, Q., Young, L.S., Woodman, C.B. and Murray, P.G. (2006) Epstein-Barr virus (EBV) and its associated human cancers--genetics, epigenetics, pathobiology and novel therapeutics. Front. Biosci. 11, 2672–2713.

    Article  CAS  PubMed  Google Scholar 

  65. Young, L.S. and Rickinson, A.B. (2004) Epstein-Barr virus: 40 years on. Nat. Rev. Cancer 4, 757–768.

    Article  CAS  PubMed  Google Scholar 

  66. Grundhoff, A., Sullivan, C.S. and Ganem, D. (2006) A combined computational and microarray-based approach identifies novel microRNAs encoded by human gamma-herpesviruses. RNA 12, 733–750.

    Article  CAS  PubMed  Google Scholar 

  67. Edwards, R.H., Marquitz, A.R. and Raab-Traub, N. (2008) Epstein-Barr virus BART microRNAs are produced from a large intron prior to splicing. J. Virol. 82, 9094–9106.

    Article  CAS  PubMed  Google Scholar 

  68. Amon, W. and Farrell, P.J. (2005) Reactivation of Epstein-Barr virus from latency. Rev. Med. Virol. 15, 149–156.

    Article  PubMed  Google Scholar 

  69. Rickinson, A.B., Lee, S.P. and Steven, N.M. (1996) Cytotoxic T lymphocyte responses to Epstein-Barr virus. Curr. Opin. Immunol. 8, 492–497.

    Article  CAS  PubMed  Google Scholar 

  70. Cai, X., Schafer, A., Lu, S., Bilello, J.P., Desrosiers, R.C., Edwards, R., Raab-Traub, N. and Cullen, B.R. (2006) Epstein-Barr virus microRNAs are evolutionarily conserved and differentially expressed. PLoS Pathog 2, e23.

    Article  PubMed  CAS  Google Scholar 

  71. Xing, L. and Kieff, E. (2007) Epstein-Barr virus BHRF1 micro- and stable RNAs during latency III and after induction of replication. J. Virol. 81, 9967–9975.

    Article  CAS  PubMed  Google Scholar 

  72. Barth, S., Pfuhl, T., Mamiani, A., Ehses, C., Roemer, K., Kremmer, E., et al. (2008) Epstein-Barr virus-encoded microRNA miR-BART2 down-regulates the viral DNA polymerase BALF5. Nucleic Acids Res. 36, 666–675.

    Article  CAS  PubMed  Google Scholar 

  73. Lo, A.K., To, K.F., Lo, K.W., Lung, R.W., Hui, J.W., Liao, G. and Hayward, S.D. (2007) Modulation of LMP1 protein expression by EBV-encoded microRNAs. Proc. Natl. Acad. Sci. U S A 104, 16164–16169.

    Article  CAS  PubMed  Google Scholar 

  74. Zheng, H., Li, L.L., Hu, D.S., Deng, X.Y. and Cao, Y. (2007) Role of Epstein-Barr virus encoded latent membrane protein 1 in the carcinogenesis of nasopharyngeal carcinoma. Cell. Mol. Immunol. 4, 185–196.

    CAS  PubMed  Google Scholar 

  75. Mosialos, G., Birkenbach, M., Yalamanchili, R., VanArsdale, T., Ware, C. and Kieff, E. (1995) The Epstein-Barr virus transforming protein LMP1 engages signaling proteins for the tumor necrosis factor receptor family. Cell 80, 389–399.

    Article  CAS  PubMed  Google Scholar 

  76. Choy, E.Y., Siu, K.L., Kok, K.H., Lung, R.W., Tsang, C.M., To, K.F., et al. (2008) An Epstein-Barr virus-encoded microRNA targets PUMA to promote host cell survival. J. Exp. Med. 205, 2551–2560.

    Article  CAS  PubMed  Google Scholar 

  77. Xia, T., O’Hara, A., Araujo, I., Barreto, J., Carvalho, E., Sapucaia, J.B., et al. (2008) EBV microRNAs in primary lymphomas and targeting of CXCL-11 by ebv-mir-BHRF1-3. Cancer Res. 68, 1436–1442.

    Article  CAS  PubMed  Google Scholar 

  78. Reeves, M. and Sinclair, J. (2008) Aspects of human cytomegalovirus latency and reactivation. Curr. Top. Microbiol. Immunol. 325, 297–313.

    Article  CAS  PubMed  Google Scholar 

  79. Britt, W. (2008) Manifestations of human cytomegalovirus infection: proposed mechanisms of acute and chronic disease. Curr. Top. Microbiol. Immunol. 325, 417–470.

    Article  CAS  PubMed  Google Scholar 

  80. Grey, F., Antoniewicz, A., Allen, E., Saugstad, J., McShea, A., Carrington, J.C. and Nelson, J. (2005) Identification and characterization of human cytomegalovirus-encoded microRNAs. J. Virol,. 79, 12095–12099.

    Article  CAS  PubMed  Google Scholar 

  81. Dunn, W., Trang, P., Zhong, Q., Yang, E., van Belle, C. and Liu, F. (2005) Human cytomegalovirus expresses novel microRNAs during productive viral infection. Cell. Microbiol. 7, 1684–1695.

    Article  CAS  PubMed  Google Scholar 

  82. Grey, F., Meyers, H., White, E.A., Spector, D.H. and Nelson, J. (2007) A human cytomegalovirus-encoded microRNA regulates expression of multiple viral genes involved in replication. PLoS Pathog. 3, e163.

    Article  PubMed  CAS  Google Scholar 

  83. Murphy, E., Vanicek, J., Robins, H., Shenk, T. and 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.

    Article  CAS  PubMed  Google Scholar 

  84. Stern-Ginossar, N., Elefant, N., Zimmermann, A., Wolf, D.G., Saleh, N., Biton, M., Horwitz, E., et al. (2007) Host immune system gene targeting by a viral miRNA. Science 317, 376–381.

    Article  CAS  PubMed  Google Scholar 

  85. Spengler, M.L., Kurapatwinski, K., Black, A.R. and Azizkhan-Clifford, J. (2002) SUMO-1 modification of human cytomegalovirus IE1/IE72. J. Virol. 76, 2990–2996.

    Article  CAS  PubMed  Google Scholar 

  86. Grey, F. and Nelson, J. (2008) Identification and function of human cytomegalovirus microRNAs. J. Clin. Virol. 41, 186–191.

    Article  CAS  PubMed  Google Scholar 

  87. Wilkinson, G.W., Tomasec, P., Stanton, R.J., Armstrong, M., Prod’homme, V., Aicheler, R., et al. (2008) Modulation of natural killer cells by human cytomegalovirus. J. Clin. Virol. 41, 206–212.

    Article  CAS  PubMed  Google Scholar 

  88. Dunn, C., Chalupny, N.J., Sutherland, C.L., Dosch, S., Sivakumar, P.V., Johnson, D.C. and Cosman, D. (2003) Human cytomegalovirus glycoprotein UL16 causes intracellular sequestration of NKG2D ligands, protecting against natural killer cell cytotoxicity. J. Exp. Med. 197, 1427–1439.

    Article  CAS  PubMed  Google Scholar 

  89. Antman, K. and Chang, Y. (2000) Kaposi’s sarcoma. N. Engl. J. Med. 342, 1027–1038.

    Article  CAS  PubMed  Google Scholar 

  90. Aoki, Y., Yarchoan, R., Wyvill, K., Okamoto, S., Little, R.F. and Tosato, G. (2001) Detection of viral interleukin-6 in Kaposi sarcoma-associated herpesvirus-linked disorders. Blood 97, 2173–2176.

    Article  CAS  PubMed  Google Scholar 

  91. Cai, X., Lu, S., Zhang, Z., Gonzalez, C.M., Damania, B. and 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.

    Article  CAS  PubMed  Google Scholar 

  92. Samols, M.A., Hu, J., Skalsky, R.L. and Renne, R. (2005) Cloning and identification of a microRNA cluster within the latency-associated region of Kaposi’s sarcoma-associated herpesvirus. J. Virol. 79, 9301–9305.

    Article  CAS  PubMed  Google Scholar 

  93. Samols, M.A., Skalsky, R.L., Maldonado, A.M., Riva, A., Lopez, M.C., Baker, H.V. and Renne, R. (2007) Identification of cellular genes targeted by KSHV-encoded microRNAs. PLoS Pathog. 3, e65.

    Article  PubMed  CAS  Google Scholar 

  94. de Fraipont, F., Nicholson, A.C., Feige, J.J. and Van Meir, E.G. (2001) Thrombospondins and tumor angiogenesis. Trends Mol. Med. 7, 401–407.

    Article  PubMed  Google Scholar 

  95. Lawler, J. (2002) Thrombospondin-1 as an endogenous inhibitor of angiogenesis and tumor growth. J. Cell. Mol. Med. 6, 1–12.

    Article  CAS  PubMed  Google Scholar 

  96. Narizhneva, N.V., Razorenova, O.V., Podrez, E.A., Chen, J., Chandrasekharan, U.M., DiCorleto, P.E., et al. (2005) Thrombospondin-1 up-regulates expression of cell adhesion molecules and promotes monocyte binding to endothelium. FASEB J. 19, 1158–1160.

    CAS  PubMed  Google Scholar 

  97. Gottwein, E., Mukherjee, N., Sachse, C., Frenzel, C., Majoros, W.H., Chi, J.T., et al. (2007) A viral microRNA functions as an orthologue of cellular miR-155. Nature 450, 1096–1099.

    Article  CAS  PubMed  Google Scholar 

  98. Skalsky, R.L., Samols, M.A., Plaisance, K.B., Boss, I.W., Riva, A., Lopez, M.C., Baker, H.V. and Renne, R. (2007) Kaposi’s sarcoma-associated herpesvirus encodes an ortholog of miR-155. J. Virol. 81, 12836–12845.

    Article  CAS  PubMed  Google Scholar 

  99. Ochiai, S., Mizuno, T., Deie, M., Igarashi, K., Hamada, Y. and Ochi, M. (2008) Oxidative stress reaction in the meniscus of Bach 1 deficient mice: potential prevention of meniscal degeneration. J. Orthop. Res. 26, 894–898.

    Article  PubMed  Google Scholar 

  100. Randhawa, P., Vats, A. and Shapiro, R. (2006) The pathobiology of polyomavirus infection in man. Adv. Exp. Med. Biol. 577, 148–159.

    Article  CAS  PubMed  Google Scholar 

  101. Sullivan, C.S., Grundhoff, A.T., Tevethia, S., Pipas, J.M. and Ganem, D. (2005) SV40-encoded microRNAs regulate viral gene expression and reduce susceptibility to cytotoxic T cells. Nature 435, 682–686.

    Article  CAS  PubMed  Google Scholar 

  102. Cantalupo, P., Doering, A., Sullivan, C.S., Pal, A., Peden, K.W., Lewis, A.M. and Pipas, J.M. (2005) Complete nucleotide sequence of polyomavirus SA12. J. Virol. 79, 13094–13104.

    Article  CAS  PubMed  Google Scholar 

  103. Seo, G.J., Fink, L.H., O’Hara, B., Atwood, W.J. and Sullivan, C.S. (2008) Evolutionarily conserved function of a viral microRNA. J. Virol. 82, 9823–9828.

    Article  CAS  PubMed  Google Scholar 

  104. Mathews, M.B. and Shenk, T. (1991) Adenovirus virus-associated RNA and translation control. J. Virol. 65, 5657–5662.

    CAS  PubMed  Google Scholar 

  105. Reich, P.R., Forget, B.G. and Weissman, S.M. (1966) RNA of low molecular weight in KB cells infected with adenovirus type 2. J. Mol. Biol. 17, 428–439.

    Article  CAS  PubMed  Google Scholar 

  106. Maran, A. and Mathews, M.B. (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, 106–113.

    Article  CAS  PubMed  Google Scholar 

  107. Andersson, M.G., Haasnoot, P.C., Xu, N., Berenjian, S., Berkhout, B. and Akusjarvi, G. (2005) Suppression of RNA interference by adenovirus virus-associated RNA. J. Virol. 79, 9556–9565.

    Article  CAS  PubMed  Google Scholar 

  108. Sano, M., Kato, Y. and Taira, K. (2006) Sequence-specific interference by small RNAs derived from adenovirus VAI RNA. FEBS Lett. 580, 1553–1564.

    Article  CAS  PubMed  Google Scholar 

  109. Xu, N., Segerman, B., Zhou, X. and Akusjarvi, G. (2007) Adenovirus virus-associated RNAII-derived small RNAs are efficiently incorporated into the rna-induced silencing complex and associate with polyribosomes. J. Virol. 81, 10540–10549.

    Article  CAS  PubMed  Google Scholar 

  110. Aparicio, O., Razquin, N., Zaratiegui, M., Narvaiza, I. and Fortes, P. (2006) Adenovirus virus-associated RNA is processed to functional interfering RNAs involved in virus production. J. Virol. 80, 1376–1384.

    Article  CAS  PubMed  Google Scholar 

  111. Ghosh, S.S., Gopinath, P. and Ramesh, A. (2006) Adenoviral vectors: a promising tool for gene therapy. Appl. Biochem. Biotechnol. 133, 9–29.

    Article  CAS  PubMed  Google Scholar 

  112. Bennasser, Y., Le, S.Y., Yeung, M.L. and Jeang, K.T. (2004) HIV-1 encoded candidate micro-RNAs and their cellular targets. Retrovirology 1, 43.

    Article  PubMed  CAS  Google Scholar 

  113. Omoto, S., Ito, M., Tsutsumi, Y., Ichikawa, Y., Okuyama, H., Brisibe, E.A., Saksena, N.K. and Fujii, Y.R. (2004) HIV-1 nef suppression by virally encoded microRNA. Retrovirology 1, 44.

    Article  PubMed  CAS  Google Scholar 

  114. Omoto, S. and Fujii, Y.R. (2005) Regulation of human immunodeficiency virus 1 transcription by nef microRNA. J. Gen. Virol. 86, 751–755.

    Article  CAS  PubMed  Google Scholar 

  115. Bennasser, Y., Le, S.Y., Benkirane, M. and Jeang, K.T. (2005) Evidence that HIV-1 encodes an siRNA and a suppressor of RNA silencing. Immunity 22, 607–619.

    Article  CAS  PubMed  Google Scholar 

  116. Klase, Z., Kale, P., Winograd, R., Gupta, M.V., Heydarian, M., Berro, R., McCaffrey, T. and Kashanchi, F. (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.

    Article  PubMed  CAS  Google Scholar 

  117. Weinberg, M.S. and Morris, K.V. (2006) Are viral-encoded microRNAs mediating latent HIV-1 infection? DNA Cell Biol. 25, 223–231.

    Article  CAS  PubMed  Google Scholar 

  118. Purzycka, K.J. and Adamiak, R.W. (2008) The HIV-2 TAR RNA domain as a potential source of viral-encoded miRNA. A reconnaissance study. Nucleic Acids Symp. Ser. (Oxf.), 511–512.

    Google Scholar 

  119. Lin, J. and Cullen, B.R. (2007) Analysis of the interaction of primate retroviruses with the human RNA interference machinery. J. Virol. 81, 12218–12226.

    Article  CAS  PubMed  Google Scholar 

  120. Ebhardt, H.A., Thi, E.P., Wang, M.B. and Unrau, P.J. (2005) Extensive 3′ modification of plant small RNAs is modulated by helper component-proteinase expression. Proc. Natl. Acad. Sci. U S A 102, 13398–13403.

    Article  CAS  PubMed  Google Scholar 

  121. Hakim, S.T., Alsayari, M., McLean, D.C., Saleem, S., Addanki, K.C., Aggarwal, M., Mahalingam, K. and Bagasra, O. (2008) A large number of the human microRNAs target lentiviruses, retroviruses, and endogenous retroviruses. Biochem. Biophys. Res. Commun. 369, 357–362.

    Article  CAS  PubMed  Google Scholar 

  122. Lerner, M.R., Andrews, N.C., Miller, G. and Steitz, J.A. (1981) Two small RNAs encoded by Epstein-Barr virus and complexed with protein are precipitated by antibodies from patients with systemic lupus erythematosus. Proc. Natl. Acad. Sci. U S A 78, 805–809.

    Article  CAS  PubMed  Google Scholar 

  123. Rosa, M.D., Gottlieb, E., Lerner, M.R. and Steitz, J.A. (1981) Striking similarities are exhibited by two small Epstein-Barr virus-encoded ribonucleic acids and the adenovirus-associated ribonucleic acids VAI and VAII. Mol. Cell. Biol. 1, 785–796.

    CAS  PubMed  Google Scholar 

  124. Wolin, S.L. and Steitz, J.A. (1983) Genes for two small cytoplasmic Ro RNAs are adjacent and appear to be single-copy in the human genome. Cell 32, 735–744.

    Article  CAS  PubMed  Google Scholar 

  125. Bhat, R.A. and Thimmappaya, B. (1983) Two small RNAs encoded by Epstein-Barr virus can functionally substitute for the virus-associated RNAs in the lytic growth of adenovirus 5. Proc. Natl. Acad. Sci. U S A 80, 4789–4793.

    Article  CAS  PubMed  Google Scholar 

  126. Bhat, R.A. and Thimmappaya, B. (1985) Construction and analysis of additional adenovirus substitution mutants confirm the complementation of VAI RNA function by two small RNAs encoded by Epstein-Barr virus. J. Virol. 56, 750–756.

    CAS  PubMed  Google Scholar 

  127. Spector, D.H. (1996) Activation and regulation of human cytomegalovirus early genes. Intervirology 39, 361–377.

    CAS  PubMed  Google Scholar 

  128. Reeves, M.B., Davies, A.A., McSharry, B.P., Wilkinson, G.W. and Sinclair, J.H. (2007) Complex I binding by a virally encoded RNA regulates mitochondria-induced cell death. Science 316, 1345–1348.

    Article  CAS  PubMed  Google Scholar 

  129. Haussecker, D., Cao, D., Huang, Y., Parameswaran, P., Fire, A.Z. and Kay, M.A. (2008) Capped small RNAs and MOV10 in human hepatitis delta virus replication. Nat. Struct. Mol. Biol. 15, 714–721.

    Article  CAS  PubMed  Google Scholar 

  130. Miranda, K.C., Huynh, T., Tay, Y., Ang, Y.S., Tam, W.L., Thomson, A.M., Lim, B. and Rigoutsos, I. (2006) A pattern-based method for the identification of microRNA binding sites and their corresponding heteroduplexes. Cell 126, 1203–1217.

    Article  CAS  PubMed  Google Scholar 

  131. Jopling, C.L., Yi, M., Lancaster, A.M., Lemon, S.M. and Sarnow, P. (2005) Modulation of hepatitis C virus RNA abundance by a liver-specific microRNA. Science 309, 1577–1581.

    Article  CAS  PubMed  Google Scholar 

  132. Varnholt, H., Drebber, U., Schulze, F., Wedemeyer, I., Schirmacher, P., Dienes, H.P. and Odenthal, M. (2008) MicroRNA gene expression profile of hepatitis C virus-associated hepatocellular carcinoma. Hepatology 47, 1223–1232.

    Article  CAS  PubMed  Google Scholar 

  133. Lin, C.J., Gong, H.Y., Tseng, H.C., Wang, W.L. and Wu, J.L. (2008) miR-122 targets an anti-apoptotic gene, Bcl-w, in human hepatocellular carcinoma cell lines. Biochem. Biophys. Res. Commun. 375, 315–320.

    Article  CAS  PubMed  Google Scholar 

  134. Gottwein, E. and Cullen, B.R. (2008) Viral and cellular microRNAs as determinants of viral pathogenesis and immunity. Cell Host Microbe 3, 375–387.

    Article  CAS  PubMed  Google Scholar 

  135. Triboulet, R., Mari, B., Lin, Y.L., Chable-Bessia, C., Bennasser, Y., Lebrigand, K., et al. (2007) Suppression of microRNA-silencing pathway by HIV-1 during virus replication. Science 315, 1579–1582.

    Article  CAS  PubMed  Google Scholar 

  136. Huang, J., Wang, F., Argyris, E., Chen, K., Liang, Z., Tian, H., et al. (2007) Cellular microRNAs contribute to HIV-1 latency in resting primary CD4+ T lymphocytes. Nat. Med. 13, 1241–1247.

    Article  CAS  PubMed  Google Scholar 

  137. Tam, W. and Dahlberg, J.E. (2006) miR-155/BIC as an oncogenic microRNA. Genes Chromosomes Cancer 45, 211–212.

    Article  CAS  PubMed  Google Scholar 

  138. Hariharan, M., Scaria, V., Pillai, B. and Brahmachari, S.K. (2005) Targets for human encoded microRNAs in HIV genes. Biochem. Biophys. Res. Commun. 337, 1214–1218.

    Article  CAS  PubMed  Google Scholar 

  139. Yeung, M.L., Bennasser, Y., Myers, T.G., Jiang, G., Benkirane, M. and Jeang, K.T. (2005) Changes in microRNA expression profiles in HIV-1-transfected human cells. Retrovirology 2, 81.

    Article  PubMed  CAS  Google Scholar 

  140. Eletto, D., Russo, G., Passiatore, G., Del Valle, L., Giordano, A., Khalili, K., Gualco, E. and Peruzzi, F. (2008) Inhibition of SNAP25 expression by HIV-1 Tat involves the activity of mir-128a. J. Cell. Physiol. 216, 764–770.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We are grateful to the CHUQ Research Center Computer Graphics Department for the graphic illustrations. P. P. is a Senior Scholar from the Fonds de la Recherche en Santé du Québec. This work was supported by grant HOP-83069 from Health Canada/Canadian Institutes of Health Research (CIHR) to P.P.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Patrick Provost .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer Science+Business Media, LLC

About this protocol

Cite this protocol

Ouellet, D.L., Provost, P. (2010). Current Knowledge of MicroRNAs and Noncoding RNAs in Virus-Infected Cells. In: Min, WP., Ichim, T. (eds) RNA Interference. Methods in Molecular Biology, vol 623. Humana Press. https://doi.org/10.1007/978-1-60761-588-0_3

Download citation

  • DOI: https://doi.org/10.1007/978-1-60761-588-0_3

  • Published:

  • Publisher Name: Humana Press

  • Print ISBN: 978-1-60761-587-3

  • Online ISBN: 978-1-60761-588-0

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics