1932

Abstract

Like their host cells, many viruses express noncoding RNAs (ncRNAs). Despite the technical challenge of ascribing function to ncRNAs, diverse biological roles for virally expressed ncRNAs have been described, including regulation of viral replication, modulation of host gene expression, host immune evasion, cellular survival, and cellular transformation. Insights into conserved interactions between viral ncRNAs and host cell machinery frequently lead to novel findings concerning host cell biology. In this review, we discuss the functions and biogenesis of ncRNAs produced by animal viruses. Specifically, we describe noncanonical pathways of microRNA (miRNA) biogenesis and novel mechanisms used by viruses to manipulate miRNA and messenger RNA stability. We also highlight recent advances in understanding the function of viral long ncRNAs and circular RNAs.

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2019-09-29
2024-12-05
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Literature Cited

  1. 1. 
    Mathews MB, Shenk T. 1991. Adenovirus virus-associated RNA and translation control. J. Virol. 65:5657–62
    [Google Scholar]
  2. 2. 
    Wilson JL, Vachon VK, Sunita S, Schwartz SL, Conn GL 2014. Dissection of the adenoviral VA RNAI central domain structure reveals minimum requirements for RNA-mediated inhibition of PKR. J. Biol. Chem. 289:23233–45
    [Google Scholar]
  3. 3. 
    Lu S, Cullen BR. 2004. Adenovirus VA1 noncoding RNA can inhibit small interfering RNA and microRNA biogenesis. J. Virol. 78:12868–76
    [Google Scholar]
  4. 4. 
    Andersson MG, Haasnoot PC, Xu N, Berenjian S, Berkhout B, Akusjarvi G 2005. Suppression of RNA interference by adenovirus virus-associated RNA. J. Virol. 79:9556–65
    [Google Scholar]
  5. 5. 
    Lerner MR, Andrews NC, Miller G, Steitz JA 1981. Two small RNAs encoded by Epstein-Barr virus and complexed with protein are precipitated by antibodies from patients with systemic lupus erythematosus. PNAS 78:805–9
    [Google Scholar]
  6. 6. 
    Francoeur AM, Mathews MB. 1982. Interaction between VA RNA and the lupus antigen La: formation of a ribonucleoprotein particle in vitro. PNAS 79:6772–76
    [Google Scholar]
  7. 7. 
    Toczyski DP, Matera AG, Ward DC, Steitz JA 1994. The Epstein-Barr virus (EBV) small RNA EBER1 binds and relocalizes ribosomal protein L22 in EBV-infected human B lymphocytes. PNAS 91:3463–67
    [Google Scholar]
  8. 8. 
    Lee N, Pimienta G, Steitz JA 2012. AUF1/hnRNP D is a novel protein partner of the EBER1 noncoding RNA of Epstein-Barr virus. RNA 18:2073–82
    [Google Scholar]
  9. 9. 
    Lee N, Moss WN, Yario TA, Steitz JA 2015. EBV noncoding RNA binds nascent RNA to drive host PAX5 to viral DNA. Cell 160:607–18
    [Google Scholar]
  10. 10. 
    Tycowski KT, Guo YE, Lee N, Moss WN, Vallery TK et al. 2015. Viral noncoding RNAs: more surprises. Genes Dev 29:567–84
    [Google Scholar]
  11. 11. 
    Vachon VK, Conn GL. 2016. Adenovirus VA RNA: an essential pro-viral non-coding RNA. Virus Res 212:39–52
    [Google Scholar]
  12. 12. 
    Moss WN, Lee N, Pimienta G, Steitz JA 2014. RNA families in Epstein-Barr virus. RNA Biol 11:10–17
    [Google Scholar]
  13. 13. 
    Steil BP, Barton DJ. 2009. Cis-active RNA elements (CREs) and picornavirus RNA replication. Virus Res 139:240–52
    [Google Scholar]
  14. 14. 
    Firth AE, Brierley I. 2012. Non-canonical translation in RNA viruses. J. Gen. Virol. 93:1385–409
    [Google Scholar]
  15. 15. 
    Balvay L, Soto Rifo R, Ricci EP, Decimo D, Ohlmann T 2009. Structural and functional diversity of viral IRESes. Biochim. Biophys. Acta 1789:542–57
    [Google Scholar]
  16. 16. 
    Bartel DP. 2018. Metazoan microRNAs. Cell 173:20–51
    [Google Scholar]
  17. 17. 
    Ambros V, Bartel B, Bartel DP, Burge CB, Carrington JC et al. 2003. A uniform system for microRNA annotation. RNA 9:277–79
    [Google Scholar]
  18. 18. 
    Ha M, Kim VN. 2014. Regulation of microRNA biogenesis. Nat. Rev. Mol. Cell Biol. 15:509
    [Google Scholar]
  19. 19. 
    Pfeffer S, Zavolan M, Grässer FA, Chien M, Russo JJ et al. 2004. Identification of virus-encoded microRNAs. Science 304:734–36
    [Google Scholar]
  20. 20. 
    Kozomara A, Griffiths-Jones S. 2014. miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res 42:D68–73
    [Google Scholar]
  21. 21. 
    Kincaid RP, Sullivan CS. 2012. Virus-encoded microRNAs: an overview and a look to the future. PLOS Pathog 8:e1003018
    [Google Scholar]
  22. 22. 
    Bernier A, Sagan S. 2018. The diverse roles of microRNAs at the host–virus interface. Viruses 10:440
    [Google Scholar]
  23. 23. 
    Nguyen TA, Jo MH, Choi Y-G, Park J, Kwon SC et al. 2015. Functional anatomy of the human Microprocessor. Cell 161:1374–87
    [Google Scholar]
  24. 24. 
    Han J, Lee Y, Yeom K-H, Nam J-W, Heo I et al. 2006. Molecular basis for the recognition of primary microRNAs by the Drosha-DGCR8 complex. Cell 125:887–901
    [Google Scholar]
  25. 25. 
    Zeng Y, Cullen BR. 2005. Efficient processing of primary microRNA hairpins by Drosha requires flanking nonstructured RNA sequences. J. Biol. Chem. 280:27595–603
    [Google Scholar]
  26. 26. 
    Wilson RC, Tambe A, Kidwell MA, Noland CL, Schneider CP, Doudna JA 2015. Dicer-TRBP complex formation ensures accurate mammalian microRNA biogenesis. Mol. Cell 57:397–407
    [Google Scholar]
  27. 27. 
    Hutvágner G, McLachlan J, Pasquinelli AE, Bálint É, Tuschl T, Zamore PD 2001. A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA. Science 293:834–38
    [Google Scholar]
  28. 28. 
    Ketting RF, Fischer SEJ, Bernstein E, Sijen T, Hannon GJ, Plasterk RHA 2001. Dicer functions in RNA interference and in synthesis of small RNA involved in developmental timing in C. elegans. Genes Dev 15:2654–59
    [Google Scholar]
  29. 29. 
    Xie M, Steitz JA. 2014. Versatile microRNA biogenesis in animals and their viruses. RNA Biol 11:673–81
    [Google Scholar]
  30. 30. 
    Diebel KW, Smith AL, van Dyk LF 2010. Mature and functional viral miRNAs transcribed from novel RNA polymerase III promoters. RNA 16:170–85
    [Google Scholar]
  31. 31. 
    Reese TA, Xia J, Johnson LS, Zhou X, Zhang W, Virgin HW 2010. Identification of novel microRNA-like molecules generated from herpesvirus and host tRNA transcripts. J. Virol. 84:10344–53
    [Google Scholar]
  32. 32. 
    Bogerd HP, Karnowski HW, Cai X, Shin J, Pohlers M, Cullen BR 2010. A mammalian herpesvirus uses noncanonical expression and processing mechanisms to generate viral microRNAs. Mol. Cell 37:135–42
    [Google Scholar]
  33. 33. 
    Kincaid RP, Burke JM, Sullivan CS 2012. RNA virus microRNA that mimics a B-cell oncomiR. PNAS 109:3077–82
    [Google Scholar]
  34. 34. 
    Kincaid RP, Chen Y, Cox JE, Rethwilm A, Sullivan CS 2014. Noncanonical microRNA (miRNA) biogenesis gives rise to retroviral mimics of lymphoproliferative and immunosuppressive host miRNAs. mBio 5:e00074–14
    [Google Scholar]
  35. 35. 
    Cao W, Heit A, Hotz-Wagenblatt A, Löchelt M 2018. Functional characterization of the bovine foamy virus miRNA expression cassette and its dumbbell-shaped pri-miRNA. Virus Genes 54:550–60
    [Google Scholar]
  36. 36. 
    Whisnant AW, Kehl T, Bao Q, Materniak M, Kuzmak J et al. 2014. Identification of novel, highly expressed retroviral microRNAs in cells infected by bovine foamy virus. J. Virol. 88:4679–86
    [Google Scholar]
  37. 37. 
    Hussain M, Asgari S. 2014. microRNA-like viral small RNA from Dengue virus 2 autoregulates its replication in mosquito cells. PNAS 111:2746–51
    [Google Scholar]
  38. 38. 
    Hussain M, Torres S, Schnettler E, Funk A, Grundhoff A et al. 2012. West Nile virus encodes a microRNA-like small RNA in the 3′ untranslated region which up-regulates GATA4 mRNA and facilitates virus replication in mosquito cells. Nucleic Acids Res 40:2210–23
    [Google Scholar]
  39. 39. 
    Li X, Fu Z, Liang H, Wang Y, Qi X et al. 2018. H5N1 influenza virus-specific miRNA-like small RNA increases cytokine production and mouse mortality via targeting poly(rC)-binding protein 2. Cell Res 28:157
    [Google Scholar]
  40. 40. 
    Diebel KW, Claypool DJ, van Dyk LF 2014. A conserved RNA polymerase III promoter required for gammaherpesvirus TMER transcription and microRNA processing. Gene 544:8–18
    [Google Scholar]
  41. 41. 
    Cazalla D, Xie M, Steitz JA 2011. A primate herpesvirus uses the Integrator complex to generate viral microRNAs. Mol. Cell 43:982–92
    [Google Scholar]
  42. 42. 
    Harwig A, Jongejan A, van Kampen AHC, Berkhout B, Das AT 2016. Tat-dependent production of an HIV-1 TAR-encoded miRNA-like small RNA. Nucleic Acids Res 44:4340–53
    [Google Scholar]
  43. 43. 
    Lee Y, Ahn C, Han J, Choi H, Kim J et al. 2003. The nuclear RNase III Drosha initiates microRNA processing. Nature 425:415–19
    [Google Scholar]
  44. 44. 
    Conrad T, Marsico A, Gehre M, Orom UA 2014. Microprocessor activity controls differential miRNA biogenesis in vivo. Cell Rep 9:542–54
    [Google Scholar]
  45. 45. 
    Auyeung VC, Ulitsky I, McGeary SE, Bartel DP 2013. Beyond secondary structure: primary-sequence determinants license pri-miRNA hairpins for processing. Cell 152:844–58
    [Google Scholar]
  46. 46. 
    Yang JS, Maurin T, Robine N, Rasmussen KD, Jeffrey KL et al. 2010. Conserved vertebrate mir-451 provides a platform for Dicer-independent, Ago2-mediated microRNA biogenesis. PNAS 107:15163–68
    [Google Scholar]
  47. 47. 
    Cheloufi S, Dos Santos CO, Chong MM, Hannon GJ 2010. A Dicer-independent miRNA biogenesis pathway that requires Ago catalysis. Nature 465:584–89
    [Google Scholar]
  48. 48. 
    Cifuentes D, Xue H, Taylor DW, Patnode H, Mishima Y et al. 2010. A novel miRNA processing pathway independent of Dicer requires Argonaute2 catalytic activity. Science 328:1694–98
    [Google Scholar]
  49. 49. 
    Bennasser Y, Le S-Y, Yeung ML, Jeang K-T 2004. HIV-1 encoded candidate micro-RNAs and their cellular targets. Retrovirology 1:43
    [Google Scholar]
  50. 50. 
    Klase Z, Kale P, Winograd R, Gupta MV, Heydarian M 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]
  51. 51. 
    Ouellet DL, Plante I, Landry P, Barat C, Janelle ME et al. 2008. Identification of functional microRNAs released through asymmetrical processing of HIV-1 TAR element. Nucleic Acids Res 36:2353–65
    [Google Scholar]
  52. 52. 
    Feng S, Holland EC. 1988. HIV-1 tat trans-activation requires the loop sequence within tar. Nature 334:165–67
    [Google Scholar]
  53. 53. 
    Garcia JA, Harrich D, Soultanakis E, Wu F, Mitsuyasu R, Gaynor RB 1989. Human immunodeficiency virus type 1 LTR TATA and TAR region sequences required for transcriptional regulation. EMBO J 8:765–78
    [Google Scholar]
  54. 54. 
    Xie M, Zhang W, Shu M-D, Xu A, Lenis DA et al. 2015. The host Integrator complex acts in transcription-independent maturation of herpesvirus microRNA 3′ ends. Genes Dev 29:1552–64
    [Google Scholar]
  55. 55. 
    Feldman ER, Kara M, Oko LM, Grau KR, Krueger BJ et al. 2016. A gammaherpesvirus noncoding RNA is essential for hematogenous dissemination and establishment of peripheral latency. mSphere 1:e00105–15
    [Google Scholar]
  56. 56. 
    Diebel KW, Oko LM, Medina EM, Niemeyer BF, Warren CJ et al. 2015. Gammaherpesvirus small noncoding RNAs are bifunctional elements that regulate infection and contribute to virulence in vivo. mBio 6:e01670–14
    [Google Scholar]
  57. 57. 
    Schorn AJ, Martienssen R. 2018. Tie-break: host and retrotransposons play tRNA. Trends Cell Biol 28:793–806
    [Google Scholar]
  58. 58. 
    Kumar P, Kuscu C, Dutta A 2016. Biogenesis and function of transfer RNA related fragments (tRFs). Trends Biochem. Sci. 41:679–89
    [Google Scholar]
  59. 59. 
    Pfeffer S, Sewer A, Lagos-Quintana M, Sheridan R, Sander C et al. 2005. Identification of microRNAs of the herpesvirus family. Nat. Methods 2:269–76
    [Google Scholar]
  60. 60. 
    Chirayil R, Kincaid RP, Dahlke C, Kuny CV, Dälken N et al. 2018. Identification of virus-encoded microRNAs in divergent Papillomaviruses. PLOS Pathog 14:e1007156
    [Google Scholar]
  61. 61. 
    Friedländer MR, Mackowiak SD, Li N, Chen W, Rajewsky N 2012. miRDeep2 accurately identifies known and hundreds of novel microRNA genes in seven animal clades. Nucleic Acids Res 40:37–52
    [Google Scholar]
  62. 62. 
    Cazalla D, Yario T, Steitz JA 2010. Down-regulation of a host microRNA by a Herpesvirus saimiri noncoding RNA. Science 328:1563–66
    [Google Scholar]
  63. 63. 
    Guo YE, Riley KJ, Iwasaki A, Steitz JA 2014. Alternative capture of noncoding RNAs or protein-coding genes by herpesviruses to alter host T cell function. Mol. Cell 54:67–79
    [Google Scholar]
  64. 64. 
    Bitetti A, Mallory AC, Golini E, Carrieri C, Gutierrez HC et al. 2018. microRNA degradation by a conserved target RNA regulates animal behavior. Nat. Struct. Mol. Biol. 25:244–51
    [Google Scholar]
  65. 65. 
    Kleaveland B, Shi CY, Stefano J, Bartel DP 2018. A network of noncoding regulatory RNAs acts in the mammalian brain. Cell 174:350–62.e.17
    [Google Scholar]
  66. 66. 
    Ghini F, Rubolino C, Climent M, Simeone I, Marzi MJ, Nicassio F 2018. Endogenous transcripts control miRNA levels and activity in mammalian cells by target-directed miRNA degradation. Nat. Commun. 9:3119
    [Google Scholar]
  67. 67. 
    Haas G, Cetin S, Messmer M, Chane-Woon-Ming B, Terenzi O et al. 2016. Identification of factors involved in target RNA-directed microRNA degradation. Nucleic Acids Res 44:2873–87
    [Google Scholar]
  68. 68. 
    Pawlica P, Moss WN, Steitz JA 2016. Host miRNA degradation by Herpesvirus saimiri small nuclear RNA requires an unstructured interacting region. RNA 22:1181–89
    [Google Scholar]
  69. 69. 
    Lee S, Song J, Kim S, Kim J, Hong Y et al. 2013. Selective degradation of host microRNAs by an intergenic HCMV noncoding RNA accelerates virus production. Cell Host Microbe 13:678–90
    [Google Scholar]
  70. 70. 
    Gorbea C, Mosbruger T, Cazalla D 2017. A viral Sm-class RNA base-pairs with mRNAs and recruits microRNAs to inhibit apoptosis. Nature 550:275–79
    [Google Scholar]
  71. 71. 
    Cazalla D. 2018. Novel roles for Sm-class RNAs in the regulation of gene expression. RNA Biol 15:856–62
    [Google Scholar]
  72. 72. 
    Cech TR, Steitz JA. 2014. The noncoding RNA revolution—trashing old rules to forge new ones. Cell 157:77–94
    [Google Scholar]
  73. 73. 
    Mitton-Fry RM, DeGregorio SJ, Wang J, Steitz TA, Steitz JA 2010. Poly(A) tail recognition by a viral RNA element through assembly of a triple helix. Science 330:1244–47
    [Google Scholar]
  74. 74. 
    Brown JA, Valenstein ML, Yario TA, Tycowski KT, Steitz JA 2012. Formation of triple-helical structures by the 3′-end sequences of MALAT1 and MENβ noncoding RNAs. PNAS 109:19202–7
    [Google Scholar]
  75. 75. 
    Conrad NK, Steitz JA. 2005. A Kaposi's sarcoma virus RNA element that increases the nuclear abundance of intronless transcripts. EMBO J 24:1831–41
    [Google Scholar]
  76. 76. 
    Tycowski KT, Shu MD, Borah S, Shi M, Steitz JA 2012. Conservation of a triple-helix-forming RNA stability element in noncoding and genomic RNAs of diverse viruses. Cell Rep 2:26–32
    [Google Scholar]
  77. 77. 
    Borah S, Darricarrere N, Darnell A, Myoung J, Steitz JA 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]
  78. 78. 
    Rossetto CC, Pari GS. 2011. Kaposi's sarcoma-associated herpesvirus noncoding polyadenylated nuclear RNA interacts with virus- and host cell-encoded proteins and suppresses expression of genes involved in immune modulation. J. Virol. 85:13290–97
    [Google Scholar]
  79. 79. 
    Conrad NK. 2016. New insights into the expression and functions of the Kaposi's sarcoma-associated herpesvirus long noncoding PAN RNA. Virus Res 212:53–63
    [Google Scholar]
  80. 80. 
    Sztuba-Solinska J, Rausch JW, Smith R, Miller JT, Whitby D, Le Grice SFJ 2017. Kaposi's sarcoma-associated herpesvirus polyadenylated nuclear RNA: a structural scaffold for nuclear, cytoplasmic and viral proteins. Nucleic Acids Res 45:6805–21
    [Google Scholar]
  81. 81. 
    Vallery TK, Withers JB, Andoh JA, Steitz JA 2018. KSHV mRNA accumulation in nuclear foci is influenced by viral DNA replication and the viral noncoding polyadenylated nuclear RNA. J. Virol. 92:e00220–18
    [Google Scholar]
  82. 82. 
    Perng GC, Jones C, Ciacci-Zanella J, Stone M, Henderson G et al. 2000. Virus-induced neuronal apoptosis blocked by the herpes simplex virus latency-associated transcript. Science 287:1500–3
    [Google Scholar]
  83. 83. 
    Margolis TP, Imai Y, Yang L, Vallas V, Krause PR 2007. Herpes simplex virus type 2 (HSV-2) establishes latent infection in a different population of ganglionic neurons than HSV-1: role of latency-associated transcripts. J. Virol. 81:1872–78
    [Google Scholar]
  84. 84. 
    Watson ZL, Washington SD, Phelan DM, Lewin AS, Tuli SS et al. 2018. In vivo knockdown of the herpes simplex virus 1 latency-associated transcript reduces reactivation from latency. J. Virol. 92:e00812–18
    [Google Scholar]
  85. 85. 
    Leib DA, Bogard CL, Kosz-Vnenchak M, Hicks KA, Coen DM et al. 1989. A deletion mutant of the latency-associated transcript of herpes simplex virus type 1 reactivates from the latent state with reduced frequency. J. Virol. 63:2893–900
    [Google Scholar]
  86. 86. 
    Cliffe AR, Garber DA, Knipe DM 2009. Transcription of the herpes simplex virus latency-associated transcript promotes the formation of facultative heterochromatin on lytic promoters. J. Virol. 83:8182–90
    [Google Scholar]
  87. 87. 
    Kwiatkowski DL, Thompson HW, Bloom DC 2009. The polycomb group protein Bmi1 binds to the herpes simplex virus 1 latent genome and maintains repressive histone marks during latency. J. Virol. 83:8173–81
    [Google Scholar]
  88. 88. 
    Saayman S, Ackley A, Turner AW, Famiglietti M, Bosque A et al. 2014. An HIV-encoded antisense long noncoding RNA epigenetically regulates viral transcription. Mol. Ther. 22:1164–75
    [Google Scholar]
  89. 89. 
    Zapata JC, Campilongo F, Barclay RA, DeMarino C, Iglesias-Ussel MD et al. 2017. The Human Immunodeficiency Virus 1 ASP RNA promotes viral latency by recruiting the Polycomb Repressor Complex 2 and promoting nucleosome assembly. Virology 506:34–44
    [Google Scholar]
  90. 90. 
    Mbonye U, Karn J. 2017. The molecular basis for human immunodeficiency virus latency. Annu. Rev. Virol. 4:261–85
    [Google Scholar]
  91. 91. 
    Blackburn EH, Collins K. 2011. Telomerase: An RNP enzyme synthesizes DNA. Cold Spring Harb. Perspect. Biol. 3:a003558
    [Google Scholar]
  92. 92. 
    de Jesus BB, Blasco MA 2013. Telomerase at the intersection of cancer and aging. Trends Genet 29:513–20
    [Google Scholar]
  93. 93. 
    Hackett JA, Greider CW. 2002. Balancing instability: dual roles for telomerase and telomere dysfunction in tumorigenesis. Oncogene 21:619–26
    [Google Scholar]
  94. 94. 
    Van Doorslaer K, Burk RD 2012. Association between hTERT activation by HPV E6 proteins and oncogenic risk. Virology 433:216–19
    [Google Scholar]
  95. 95. 
    Greco A, Fester N, Engel AT, Kaufer BB 2014. Role of the short telomeric repeat region in Marek's disease virus replication, genomic integration, and lymphomagenesis. J. Virol. 88:14138–47
    [Google Scholar]
  96. 96. 
    Wallaschek N, Sanyal A, Pirzer F, Gravel A, Mori Y et al. 2016. The telomeric repeats of human herpesvirus 6A (HHV-6A) are required for efficient virus integration. PLOS Pathog 12:e1005666
    [Google Scholar]
  97. 97. 
    Kheimar A, Previdelli RL, Wight DJ, Kaufer BB 2017. Telomeres and telomerase: role in Marek's disease virus pathogenesis, integration and tumorigenesis. Viruses 9:173
    [Google Scholar]
  98. 98. 
    Fragnet L, Blasco MA, Klapper W, Rasschaert D 2003. The RNA subunit of telomerase is encoded by Marek's disease virus. J. Virol. 77:5985–96
    [Google Scholar]
  99. 99. 
    Brown AC, Nair V, Allday MJ 2012. Epigenetic regulation of the latency-associated region of Marek's disease virus in tumor-derived T-cell lines and primary lymphoma. J. Virol. 86:1683–95
    [Google Scholar]
  100. 100. 
    Fragnet L, Kut E, Rasschaert D 2005. Comparative functional study of the viral telomerase RNA based on natural mutations. J. Biol. Chem. 280:23502–15
    [Google Scholar]
  101. 101. 
    Trapp S, Parcells MS, Kamil JP, Schumacher D, Tischer BK et al. 2006. A virus-encoded telomerase RNA promotes malignant T cell lymphomagenesis. J. Exp. Med. 203:1307–17
    [Google Scholar]
  102. 102. 
    Kaufer BB, Arndt S, Trapp S, Osterrieder N, Jarosinski KW 2011. Herpesvirus telomerase RNA (vTR) with a mutated template sequence abrogates herpesvirus-induced lymphomagenesis. PLOS Pathog 7:e1002333
    [Google Scholar]
  103. 103. 
    Kaufer BB, Trapp S, Jarosinski KW, Osterrieder N 2010. Herpesvirus telomerase RNA(vTR)-dependent lymphoma formation does not require interaction of vTR with telomerase reverse transcriptase (TERT). PLOS Pathog 6:e1001073
    [Google Scholar]
  104. 104. 
    Le S, Sternglanz R, Greider CW 2000. Identification of two RNA-binding proteins associated with human telomerase RNA. Mol. Biol. Cell 11:999–1010
    [Google Scholar]
  105. 105. 
    Houmani JL, Davis CI, Ruf IK 2009. Growth-promoting properties of Epstein-Barr virus EBER-1 RNA correlate with ribosomal protein L22 binding. J. Virol. 83:9844–53
    [Google Scholar]
  106. 106. 
    Kheimar A, Kaufer BB. 2018. Epstein-Barr virus-encoded RNAs (EBERs) complement the loss of herpesvirus telomerase RNA (vTR) in virus-induced tumor formation. Sci. Rep. 8:209
    [Google Scholar]
  107. 107. 
    Jeck WR, Sorrentino JA, Wang K, Slevin MK, Burd CE et al. 2013. Circular RNAs are abundant, conserved, and associated with ALU repeats. RNA 19:141–57
    [Google Scholar]
  108. 108. 
    Falaleeva M, Stamm S. 2013. Processing of snoRNAs as a new source of regulatory non-coding RNAs: snoRNA fragments form a new class of functional RNAs. Bioessays 35:46–54
    [Google Scholar]
  109. 109. 
    Moss WN, Steitz JA. 2013. Genome-wide analyses of Epstein-Barr virus reveal conserved RNA structures and a novel stable intronic sequence RNA. BMC Genom 14:543
    [Google Scholar]
  110. 110. 
    Kulesza CA, Shenk T. 2006. Murine cytomegalovirus encodes a stable intron that facilitates persistent replication in the mouse. PNAS 103:18302–7
    [Google Scholar]
  111. 111. 
    Kulesza CA, Shenk T. 2004. Human cytomegalovirus 5-kilobase immediate-early RNA is a stable intron. J. Virol. 78:13182–89
    [Google Scholar]
  112. 112. 
    Farrell MJ, Dobson AT, Feldman LT 1991. Herpes simplex virus latency-associated transcript is a stable intron. PNAS 88:790–94
    [Google Scholar]
  113. 113. 
    Kelly GL, Milner AE, Tierney RJ, Croom-Carter DS, Altmann M et al. 2005. Epstein-Barr virus nuclear antigen 2 (EBNA2) gene deletion is consistently linked with EBNA3A, -3B, and -3C expression in Burkitt's lymphoma cells and with increased resistance to apoptosis. J. Virol. 79:10709–17
    [Google Scholar]
  114. 114. 
    Szymula A, Palermo RD, Bayoumy A, Groves IJ, Ba Abdullah M et al. 2018. Epstein-Barr virus nuclear antigen EBNA-LP is essential for transforming naïve B cells, and facilitates recruitment of transcription factors to the viral genome. PLOS Pathog 14:e1006890
    [Google Scholar]
  115. 115. 
    Tompkins VS, Valverde DP, Moss WN 2018. Human regulatory proteins associate with non-coding RNAs from the EBV IR1 region. BMC Res. Notes 11:139
    [Google Scholar]
  116. 116. 
    Fu XD, Ares M Jr 2014. Context-dependent control of alternative splicing by RNA-binding proteins. Nat. Rev. Genet. 15:689–701
    [Google Scholar]
  117. 117. 
    Toptan T, Abere B, Nalesnik MA, Swerdlow SH, Ranganathan S et al. 2018. Circular DNA tumor viruses make circular RNAs. PNAS 115:E8737–45
    [Google Scholar]
  118. 118. 
    Ungerleider N, Concha M, Lin Z, Roberts C, Wang X et al. 2018. The Epstein Barr virus circRNAome. PLOS Pathog 14:e1007206
    [Google Scholar]
  119. 119. 
    Rennekamp AJ, Lieberman PM. 2011. Initiation of Epstein-Barr virus lytic replication requires transcription and the formation of a stable RNA-DNA hybrid molecule at OriLyt. J. Virol. 85:2837–50
    [Google Scholar]
  120. 120. 
    Huang C, Liang D, Tatomer DC, Wilusz JE 2018. A length-dependent evolutionarily conserved pathway controls nuclear export of circular RNAs. Genes Dev 32:639–44
    [Google Scholar]
  121. 121. 
    Li X, Yang L, Chen LL 2018. The biogenesis, functions, and challenges of circular RNAs. Mol. Cell 71:428–42
    [Google Scholar]
  122. 122. 
    Bidet K, Garcia-Blanco MA. 2014. Flaviviral RNAs: weapons and targets in the war between virus and host. Biochem. J. 462:215–30
    [Google Scholar]
  123. 123. 
    Slonchak A, Khromykh AA. 2018. Subgenomic flaviviral RNAs: What do we know after the first decade of research. Antivir. Res. 159:13–25
    [Google Scholar]
  124. 124. 
    Fernandez-Sanles A, Rios-Marco P, Romero-Lopez C, Berzal-Herranz A 2017. Functional information stored in the conserved structural RNA domains of flavivirus genomes. Front. Microbiol. 8:546
    [Google Scholar]
  125. 125. 
    Kieft JS, Rabe JL, Chapman EG 2015. New hypotheses derived from the structure of a flaviviral Xrn1-resistant RNA: conservation, folding, and host adaptation. RNA Biol 12:1169–77
    [Google Scholar]
  126. 126. 
    Chapman EG, Moon SL, Wilusz J, Kieft JS 2014. RNA structures that resist degradation by Xrn1 produce a pathogenic Dengue virus RNA. eLife 3:e01892
    [Google Scholar]
  127. 127. 
    Chapman EG, Costantino DA, Rabe JL, Moon SL, Wilusz J et al. 2014. The structural basis of pathogenic subgenomic flavivirus RNA (sfRNA) production. Science 344:307–10
    [Google Scholar]
  128. 128. 
    MacFadden A, O'Donoghue Z, Silva P, Chapman EG, Olsthoorn RC et al. 2018. Mechanism and structural diversity of exoribonuclease-resistant RNA structures in flaviviral RNAs. Nat. Commun. 9:119
    [Google Scholar]
  129. 129. 
    Charley PA, Wilusz CJ, Wilusz J 2018. Identification of phlebovirus and arenavirus RNA sequences that stall and repress the exoribonuclease XRN1. J. Biol. Chem. 293:285–95
    [Google Scholar]
  130. 130. 
    Flobinus A, Chevigny N, Charley PA, Seissler T, Klein E et al. 2018. Beet necrotic yellow vein virus noncoding RNA production depends on a 5′→3′ Xrn exoribonuclease activity. Viruses 10:137
    [Google Scholar]
  131. 131. 
    Iwakawa HO, Mizumoto H, Nagano H, Imoto Y, Takigawa K et al. 2008. A viral noncoding RNA generated by cis-element-mediated protection against 5′→3′ RNA decay represses both cap-independent and cap-dependent translation. J. Virol. 82:10162–74
    [Google Scholar]
  132. 132. 
    Steckelberg AL, Akiyama BM, Costantino DA, Sit TL, Nix JC, Kieft JS 2018. A folded viral noncoding RNA blocks host cell exoribonucleases through a conformationally dynamic RNA structure. PNAS 115:6404–9
    [Google Scholar]
  133. 133. 
    Moon SL, Anderson JR, Kumagai Y, Wilusz CJ, Akira S et al. 2012. A noncoding RNA produced by arthropod-borne flaviviruses inhibits the cellular exoribonuclease XRN1 and alters host mRNA stability. RNA 18:2029–40
    [Google Scholar]
  134. 134. 
    Schnettler E, Sterken MG, Leung JY, Metz SW, Geertsema C et al. 2012. Noncoding flavivirus RNA displays RNA interference suppressor activity in insect and mammalian cells. J. Virol. 86:13486–500
    [Google Scholar]
  135. 135. 
    Moon SL, Dodd BJ, Brackney DE, Wilusz CJ, Ebel GD, Wilusz J 2015. Flavivirus sfRNA suppresses antiviral RNA interference in cultured cells and mosquitoes and directly interacts with the RNAi machinery. Virology 485:322–29
    [Google Scholar]
  136. 136. 
    Bidet K, Dadlani D, Garcia-Blanco MA 2014. G3BP1, G3BP2 and CAPRIN1 are required for translation of interferon stimulated mRNAs and are targeted by a dengue virus non-coding RNA. PLOS Pathog 10:e1004242
    [Google Scholar]
  137. 137. 
    Manokaran G, Finol E, Wang C, Gunaratne J, Bahl J et al. 2015. Dengue subgenomic RNA binds TRIM25 to inhibit interferon expression for epidemiological fitness. Science 350:217–21
    [Google Scholar]
  138. 138. 
    Wilhelm SW, Bird JT, Bonifer KS, Calfee BC, Chen T et al. 2017. A student's guide to giant viruses infecting small eukaryotes: from Acanthamoeba to Zooxanthellae. Viruses 9:46
    [Google Scholar]
  139. 139. 
    Yolken RH, Jones-Brando L, Dunigan DD, Kannan G, Dickerson F et al. 2014. Chlorovirus ATCV-1 is part of the human oropharyngeal virome and is associated with changes in cognitive functions in humans and mice. PNAS 111:16106–11
    [Google Scholar]
  140. 140. 
    Popgeorgiev N, Boyer M, Fancello L, Monteil S, Robert C et al. 2013. Marseillevirus-like virus recovered from blood donated by asymptomatic humans. J. Infect. Dis. 208:1042–50
    [Google Scholar]
  141. 141. 
    Jacob R, Zander S, Gutschner T 2017. The dark side of the epitranscriptome: chemical modifications in long non-coding RNAs. Int. J. Mol. Sci. 18:2387
    [Google Scholar]
  142. 142. 
    Aparicio O, Razquin N, Zaratiegui M, Narvaiza I, Fortes P 2006. Adenovirus virus-associated RNA is processed to functional interfering RNAs involved in virus production. J. Virol. 80:1376–84
    [Google Scholar]
  143. 143. 
    Stevens JG, Wagner EK, Devi-Rao GB, Cook ML, Feldman LT 1987. RNA complementary to a herpesvirus alpha gene mRNA is prominent in latently infected neurons. Science 235:1056–59
    [Google Scholar]
  144. 144. 
    Fok V, Friend K, Steitz JA 2006. Epstein-Barr virus noncoding RNAs are confined to the nucleus, whereas their partner, the human La protein, undergoes nucleocytoplasmic shuttling. J. Cell Biol. 173:319–25
    [Google Scholar]
  145. 145. 
    Lee SI, Murthy SC, Trimble JJ, Desrosiers RC, Steitz JA 1988. Four novel U RNAs are encoded by a herpesvirus. Cell 54:599–607
    [Google Scholar]
  146. 146. 
    Myer VE, Lee SI, Steitz JA 1992. Viral small nuclear ribonucleoproteins bind a protein implicated in messenger RNA destabilization. PNAS 89:1296–300
    [Google Scholar]
  147. 147. 
    Cook HL, Mischo HE, Steitz JA 2004. The Herpesvirus saimiri small nuclear RNAs recruit AU-rich element-binding proteins but do not alter host AU-rich element-containing mRNA levels in virally transformed T cells. Mol. Cell. Biol. 24:4522–33
    [Google Scholar]
  148. 148. 
    Albrecht JC, Fleckenstein B. 1992. Nucleotide sequence of HSUR 6 and HSUR 7, two small RNAs of herpesvirus saimiri. Nucleic Acids Res 20:1810
    [Google Scholar]
  149. 149. 
    Sun R, Lin SF, Gradoville L, Miller G 1996. Polyadenylylated nuclear RNA encoded by Kaposi sarcoma-associated herpesvirus. PNAS 93:11883–88
    [Google Scholar]
  150. 150. 
    Sahin BB, Patel D, Conrad NK 2010. Kaposi's sarcoma-associated herpesvirus ORF57 protein binds and protects a nuclear noncoding RNA from cellular RNA decay pathways. PLOS Pathog 6:e1000799
    [Google Scholar]
  151. 151. 
    Campbell M, Kim KY, Chang PC, Huerta S, Shevchenko B et al. 2014. A lytic viral long noncoding RNA modulates the function of a latent protein. J. Virol. 88:1843–48
    [Google Scholar]
  152. 152. 
    Bowden RJ, Simas JP, Davis AJ, Efstathiou S 1997. Murine gammaherpesvirus 68 encodes tRNA-like sequences which are expressed during latency. J. Gen. Virol. 78:1675–87
    [Google Scholar]
  153. 153. 
    Pijlman GP, Funk A, Kondratieva N, Leung J, Torres S et al. 2008. A highly structured, nuclease-resistant, noncoding RNA produced by flaviviruses is required for pathogenicity. Cell Host Microbe 4:579–91
    [Google Scholar]
  154. 154. 
    Roby JA, Pijlman GP, Wilusz J, Khromykh AA 2014. Noncoding subgenomic flavivirus RNA: multiple functions in West Nile virus pathogenesis and modulation of host responses. Viruses 6:404–27
    [Google Scholar]
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