MicroRNA Regulation of RNA Virus Replication and Pathogenesis

Trends in Molecular Medicine

Volumn 23, Issue 1, 2017, Pages 80-93

  Trobaugh, Derek W ^a   Klimstra, William B ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

innate immunity; miRNA; pathogenesis; RNA viruses

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; CASPASE 9; FURIN; INITIATION FACTOR 4E; INTERFERON REGULATORY FACTOR 1; INTERFERON REGULATORY FACTOR 9; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MATRIX PROTEIN; MICRORNA; MICRORNA 1; MICRORNA 122; MICRORNA 141; MICRORNA 146A; MICRORNA 155; MICRORNA 221; MICRORNA 223; MICRORNA 24; MICRORNA 29A; MICRORNA 29B; MICRORNA 9; PROTEIN VP1; RANTES; RNA; RNA POLYMERASE II; TOLL LIKE RECEPTOR 3; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; VIRAL PROTEIN; VIRUS VECTOR; TRANSCRIPTOME; VIRUS RNA;

ALPHAVIRUS; BINDING SITE; GENE REPRESSION; GENE THERAPY; HUMAN T-LYMPHOTROPIC VIRUS 1; INTERACTIONS WITH RNA; MUTATION RATE; NONHUMAN; ORTHOMYXOVIRIDAE; PICORNAVIRIDAE; PROTEIN EXPRESSION; RETROVIRIDAE; REVIEW; RNA BINDING; RNA STABILITY; RNA VIRUS; RNA VIRUS INFECTION; TRANSLATION REGULATION; VIRUS CELL INTERACTION; VIRUS GENOME; VIRUS INFECTION; VIRUS MUTATION; VIRUS PATHOGENESIS; VIRUS REPLICATION; VIRUS TRANSCRIPTION; ANIMAL; GENETICS; HOST PATHOGEN INTERACTION; HUMAN; METABOLISM; PATHOLOGY; PHYSIOLOGY; VIROLOGY;

ANIMALS; GENOME, VIRAL; HOST-PATHOGEN INTERACTIONS; HUMANS; MICRORNAS; RNA VIRUS INFECTIONS; RNA VIRUSES; RNA, VIRAL; TRANSCRIPTOME; VIRUS REPLICATION;

EID: 85007343217     PISSN: 14714914     EISSN: 1471499X     Source Type: Journal    
DOI: 10.1016/j.molmed.2016.11.003     Document Type: Review

References (110)

1. 1 Ding, S-W., Voinnet, O., Antiviral immunity directed by small RNAs. Cell 130 (2007), 413–426.
2. 2 Maillard, P.V., et al. Antiviral RNA interference in mammalian cells. Science 342 (2013), 235–238.
3. 3 Li, Y., et al. RNA interference functions as an antiviral immunity mechanism in mammals. Science 342 (2013), 231–234.
4. 4 Schneider, W.M., et al. Interferon-stimulated genes: a complex web of host defenses. Annu. Rev. Immunol. 32 (2014), 513–545.
5. 5 Ludwig, N., et al. Distribution of miRNA expression across human tissues. Nucleic Acids Res. 44 (2016), 3865–3877.
6. 6 Londin, E., et al. Analysis of 13 cell types reveals evidence for the expression of numerous novel primate- and tissue-specific microRNAs. Proc. Natl. Acad. Sci. U.S.A. 112 (2015), E1106–E1115.
7. 7 Lim, L.P., et al. The microRNAs of Caenorhabditis elegans. Genes Dev. 17 (2003), 991–1008.
8. 8 Grimson, A., et al. MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol. Cell 27 (2007), 91–105.
9. 9 Teterina, N.L., et al. Silencing of neurotropic Flavivirus replication in the central nervous system by combining multiple microRNA target insertions in two distinct viral genome regions. Virology 456 (2014), 247–258.
10. 10 Jopling, C.L., et al. Modulation of hepatitis C virus RNA abundance by a liver-specific microRNA. Science 309 (2005), 1577–1581.
11. 11 Trobaugh, D.W., et al. RNA viruses can hijack vertebrate microRNAs to suppress innate immunity. Nature 506 (2014), 245–248.
12. 12 Song, L., et al. Cellular microRNAs inhibit replication of the H1N1 influenza A virus in infected cells. J. Virol. 84 (2010), 8849–8860.
13. 13 Zheng, Z., et al. Human microRNA hsa-miR-296-5p suppresses enterovirus 71 replication by targeting the viral genome. J. Virol. 87 (2013), 5645–5656.
14. 14 Heiss, B.L., et al. MicroRNA targeting of neurotropic Flavivirus: effective control of virus escape and reversion to neurovirulent phenotype. J. Virol. 86 (2012), 5647–5659.
15. 15 Saetrom, P., et al. Distance constraints between microRNA target sites dictate efficacy and cooperativity. Nucleic Acids Res. 35 (2007), 2333–2342.
16. 16 Davis-Dusenbery, B.N., Hata, A., Mechanisms of control of microRNA biogenesis. J. Biochem. 148 (2010), 381–392.
17. 17 Gaur, A., et al. Characterization of microRNA expression levels and their biological correlates in human cancer cell lines. Cancer Res. 67 (2007), 2456–2468.
18. 18 Hwang, H-W., et al. Cell–cell contact globally activates microRNA biogenesis. Proc. Natl. Acad. Sci. U.S.A. 106 (2009), 7016–7021.
19. 19 Lu, J., et al. MicroRNA expression profiles classify human cancers. Nature 435 (2005), 834–838.
20. 20 Brackney, D.E., et al. C6/36 Aedes albopictus cells have a dysfunctional antiviral RNA interference response. PLoS Negl. Trop. Dis., 4, 2010, e856.
21. 21 Scott, J.C., et al. Comparison of dengue virus type 2-specific small RNAs from RNA interference-competent and -incompetent mosquito cells. PLoS Negl. Trop. Dis., 4, 2010, e848.
22. 22 Bogerd, H.P., et al. Replication of many human viruses is refractory to inhibition by endogenous cellular microRNAs. J. Virol. 88 (2014), 8065–8076.
23. 23 Scheel, T.K.H., et al. A broad RNA virus survey reveals both miRNA dependence and functional sequestration. Cell Host Microbe 19 (2016), 409–423.
24. 24 Shimakami, T., et al. Stabilization of hepatitis C virus RNA by an Ago2–miR-122 complex. Proc. Natl. Acad. Sci. U.S.A. 109 (2012), 941–946.
25. 25 Lauring, A.S., et al. The role of mutational robustness in RNA virus evolution. Nat. Rev. Microbiol. 11 (2013), 327–336.
26. 26 Deresiewicz, R.L., et al. Clinical and neuroradiographic manifestations of eastern equine encephalitis. N. Engl. J. Med. 336 (1997), 1867–1874.
27. 27 Gardner, C.L., et al. Eastern and Venezuelan equine encephalitis viruses differ in their ability to infect dendritic cells and macrophages: impact of altered cell tropism on pathogenesis. J. Virol. 82 (2008), 10634–10646.
28. 28 Lecellier, C-H., et al. A cellular microRNA mediates antiviral defense in human cells. Science 308 (2005), 557–560.
29. 29 Bai, X.T., Nicot, C., miR-28-3p is a cellular restriction factor that inhibits human T cell leukemia virus, type 1 (HTLV-1) replication and virus infection. J. Biol. Chem. 290 (2015), 5381–5390.
30. + T lymphocytes. Nat. Med. 13 (2007), 1241–1247.
31. 31 Nathans, R., et al. Cellular microRNA and P bodies modulate host-HIV-1 interactions. Mol. Cell 34 (2009), 696–709.
32. 32 Wen, B-P., et al. MicroRNA-23b inhibits enterovirus 71 replication through downregulation of EV71 VPl protein. Intervirology 56 (2013), 195–200.
33. 33 Khongnomnan, K., et al. Human miR-3145 inhibits influenza A viruses replication by targeting and silencing viral PB1 gene. Exp. Biol. Med. (Maywood) 240 (2015), 1630–1639.
34. 34 Ingle, H., et al. The microRNA miR-485 targets host and influenza virus transcripts to regulate antiviral immunity and restrict viral replication. Sci. Signal., 8, 2015, ra126.
35. 35 Ma, Y-J., et al. 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 (2012), 2539–2546.
36. 36 Zhang, H., et al. A computational method for predicting regulation of human microRNAs on the influenza virus genome. BMC Syst. Biol., 7, 2013, S3.
37. 37 He, T., et al. Identification of host encoded microRNAs interacting with novel swine-origin influenza A (H1N1) virus and swine influenza virus. Bioinformation 4 (2009), 112–118.
38. 38 Wang, Y-S., et al. Overexpression of microRNA gga-miR-21 in chicken fibroblasts suppresses replication of infectious bursal disease virus through inhibiting VP1 translation. Antiviral Res. 100 (2013), 196–201.
39. 39 Guo, X-K., et al. Increasing expression of microRNA 181 inhibits porcine reproductive and respiratory syndrome virus replication and has implications for controlling virus infection. J. Virol. 87 (2013), 1159–1171.
40. 40 Zhang, Q., et al. MicroRNA-23 inhibits PRRSV replication by directly targeting PRRSV RNA and possibly by upregulating type I interferons. Virology 450 (2014), 182–195.
41. 41 Weaver, S.C., et al. Genetic and fitness changes accompanying adaptation of an arbovirus to vertebrate and invertebrate cells. J. Virol. 73 (1999), 4316–4326.
42. 42 Pham, A.M., et al. Replication in cells of hematopoietic origin is necessary for dengue virus dissemination. PLoS Pathog., 8, 2012, e1002465.
43. 43 Janssen, H.L.A., et al. Treatment of HCV infection by targeting microRNA. N. Engl. J. Med. 368 (2013), 1685–1694.
44. 44 Wu, J., Chen, Z.J., Innate immune sensing and signaling of cytosolic nucleic acids. Annu. Rev. Immunol. 32 (2014), 461–488.
45. 45 Aguado, L.C., et al. microRNA function is limited to cytokine control in the acute response to virus infection. Cell Host Microbe 18 (2015), 714–722.
46. 46 Choi, E-J., et al. Differential microRNA expression following infection with a mouse-adapted, highly virulent avian H5N2 virus. BMC Microbiol., 14, 2014 1487–1413.
47. 47 Shin, O.S., et al. Hantaviruses induce cell type- and viral species-specific host microRNA expression signatures. Virology 446 (2013), 217–224.
48. 48 Luna, J.M., et al. Hepatitis C virus RNA functionally sequesters miR-122. Cell 160 (2015), 1099–1110.
49. 49 Beachboard, D.C., Horner, S.M., Innate immune evasion strategies of DNA and RNA viruses. Curr. Opin. Microbiol. 32 (2016), 113–119.
50. 50 Ho, B-C., et al. Inhibition of miR-146a prevents enterovirus-induced death by restoring the production of type I interferon. Nat. Commun., 5, 2014, 3344.
51. 51 Wu, S., et al. miR-146a facilitates replication of dengue virus by dampening interferon induction by targeting TRAF6. J. Infect. 67 (2013), 329–341.
52. 52 Sharma, N., et al. miR-146a suppresses cellular immune response during Japanese encephalitis virus JaOArS982 strain infection in human microglial cells. J. Neuroinflammation, 12, 2015, 30.
53. 53 Sharma, N., et al. Japanese encephalitis virus exploits the microRNA-432 to regulate the expression of suppressor of cytokine signaling (SOCS) 5. Sci. Rep., 6, 2016, 27685.
54. 54 Zhang, X., et al. Induction of the cellular miR-29c by influenza virus inhibits the innate immune response through protection of A20 mRNA. Biochem. Biophys. Res. Commun. 450 (2014), 755–761.
55. 55 Rosenberger, C.M., et al. miR-451 regulates dendritic cell cytokine responses to influenza infection. J. Immunol. 189 (2012), 5965–5975.
56. 56 Yang, Q., et al. Hepatitis C virus infection decreases the expression of Toll-like receptors 3 and 7 via upregulation of miR-758. Arch. Virol. 159 (2014), 2997–3003.
57. 57 Bhanja Chowdhury, J., et al. Hepatitis C virus infection modulates expression of interferon stimulatory gene IFITM1 by upregulating miR-130A. J. Virol. 86 (2012), 10221–10225.
58. 58 Mukherjee, A., et al. Hepatitis C virus-mediated enhancement of microRNA miR-373 impairs the JAK/STAT signaling pathway. J. Virol. 89 (2015), 3356–3365.
59. 59 Li, Z., et al. MicroRNA-23b promotes avian leukosis virus subgroup J (ALV-J) replication by targeting IRF1. Sci. Rep., 5, 2015, 10294.
60. 60 Li, S., et al. MicroRNA-130a inhibits HCV replication by restoring the innate immune response. J. Viral Hepat. 21 (2014), 121–128.
61. 61 Zhu, X., et al. MicroRNA-30e* suppresses dengue virus replication by promoting NF-κB-dependent IFN production. PLoS Negl. Trop. Dis., 8, 2014, e3088.
62. 62 Slonchak, A., et al. Human microRNA miR-532-5p exhibits antiviral activity against West Nile virus via suppression of host genes SESTD1 and TAB3 required for virus replication. J. Virol. 90 (2016), 2388–2402.
63. 63 Zhai, A., et al. Borna disease virus encoded phosphoprotein inhibits host innate immunity by regulating miR-155. Antiviral Res. 98 (2013), 66–75.
64. 64 Lai, F.W., et al. Human coronavirus OC43 nucleocapsid protein binds microRNA 9 and potentiates NF-κB activation. J. Virol. 88 (2014), 54–65.
65. 65 Thornburg, N.J., et al. Respiratory syncytial virus regulates human microRNAs by using mechanisms involving beta interferon and NF-κB. MBio 3 (2012), e00220–e312.
66. 66 Xu, C., et al. Downregulation of microRNA miR-526a by enterovirus inhibits RIG-I-dependent innate immune response. J. Virol. 88 (2014), 11356–11368.
67. 67 Bakre, A., et al. Respiratory syncytial virus modifies microRNAs regulating host genes that affect virus replication. J. Gen. Virol. 93 (2012), 2346–2356.
68. 68 Loveday, E-K., et al. Human microRNA-24 modulates highly pathogenic avian-origin H5N1 influenza A virus infection in A549 cells by targeting secretory pathway furin. J. Gen. Virol. 96 (2015), 30–39.
69. 69 Othumpangat, S., et al. Expression of non-structural-1A binding protein in lung epithelial cells is modulated by miRNA-548an on exposure to influenza A virus. Virology 447 (2013), 84–94.
70. 70 Ho, B-C., et al. Enterovirus-induced miR-141 contributes to shutoff of host protein translation by targeting the translation initiation factor eIF4E. Cell Host Microbe 9 (2011), 58–69.
71. 71 Bandiera, S., et al. Hepatitis C virus-induced upregulation of microRNA miR-146a-5p in hepatocytes promotes viral infection and deregulates metabolic pathways associated with liver disease pathogenesis. J. Virol. 90 (2016), 6387–6400.
72. 72 Othumpangat, S., et al. MicroRNA-221 modulates RSV replication in human bronchial epithelium by targeting NGF expression. PLoS One, 7, 2012, e30030.
73. 73 Shim, B-S., et al. MicroRNA-555 has potent antiviral properties against poliovirus. J. Gen. Virol. 97 (2016), 659–668.
74. 74 Wolf, S., et al. MicroRNA regulation of human genes essential for influenza A (H7N9) replication. PLoS One, 11, 2016, e0155104.
75. 75 Steinhauer, D.A., et al. Lack of evidence for proofreading mechanisms associated with an RNA virus polymerase. Gene 122 (1992), 281–288.
76. 76 Skalsky, R.L., et al. Identification of microRNAs expressed in two mosquito vectors, Aedes albopictus and Culex quinquefasciatus. BMC Genomics, 11, 2010, 119.
77. 77 Kelly, E.J., Russell, S.J., MicroRNAs and the regulation of vector tropism. Mol. Ther. 17 (2009), 409–416.
78. 78 Dunning, J., et al. Experimental treatment of Ebola virus disease with TKM-130803: a single-arm Phase 2 clinical trial. PLoS Med., 13, 2016, e1001997.
79. 79 Barnes, D., et al. Harnessing endogenous miRNAs to control virus tissue tropism as a strategy for developing attenuated virus vaccines. Cell Host Microbe 4 (2008), 239–248.
80. 80 Hussain, M., Asgari, S., MicroRNA-like viral small RNA from dengue virus 2 autoregulates its replication in mosquito cells. Proc. Natl. Acad. Sci. U.S.A. 111 (2014), 2746–2751.
81. 81 Weng, K-F., et al. A cytoplasmic RNA virus generates functional viral small RNAs and regulates viral IRES activity in mammalian cells. Nucleic Acids Res. 42 (2014), 12789–12805.
82. 82 Ha, M., Kim, V.N., Regulation of microRNA biogenesis. Nat. Immunol. 15 (2014), 509–524.
83. 83 Lee, Y., et al. The nuclear RNase III Drosha initiates microRNA processing. Nature 425 (2003), 415–419.
84. 84 Eichhorn, S.W., et al. mRNA destabilization is the dominant effect of mammalian microRNAs by the time substantial repression ensues. Mol. Cell 56 (2014), 104–115.
85. 85 Djuranovic, S., et al. miRNA-mediated gene silencing by translational repression followed by mRNA deadenylation and decay. Science 336 (2012), 237–240.
86. 86 Schwarz, D.S., et al. Asymmetry in the assembly of the RNAi enzyme complex. Cell 115 (2003), 199–208.
87. 87 Ameres, S.L., Zamore, P.D., Diversifying microRNA sequence and function. Nat. Immunol. 14 (2013), 475–488.
88. 88 Lim, L.P., et al. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 433 (2005), 769–773.
89. 89 Loeb, G.B., et al. Transcriptome-wide miR-155 binding map reveals widespread noncanonical microRNA targeting. Mol. Cell 48 (2012), 760–770.
90. 90 Agarwal, V., et al. Predicting effective microRNA target sites in mammalian mRNAs. Elife, 4, 2015, e05005.
91. 91 Haasnoot, J., et al. The Ebola virus VP35 protein is a suppressor of RNA silencing. PLoS Pathog., 3, 2007, e86.
92. 92 Fabozzi, G., et al. Ebolavirus proteins suppress the effects of small interfering RNA by direct interaction with the mammalian RNA interference pathway. J. Virol. 85 (2011), 2512–2523.
93. 93 Wang, Y., et al. Hepatitis C virus core protein is a potent inhibitor of RNA silencing-based antiviral response. Gastroenterology 130 (2006), 883–892.
94. 94 Bennasser, Y., et al. Evidence that HIV-1 encodes an siRNA and a suppressor of RNA silencing. Immunity 22 (2005), 607–619.
95. 95 Li, W-X., et al. Interferon antagonist proteins of influenza and vaccinia viruses are suppressors of RNA silencing. Proc. Natl. Acad. Sci. U. S. A. 101 (2004), 1350–1355.
96. 96 Langlois, R.A., et al. MicroRNA-based strategy to mitigate the risk of gain-of-function influenza studies. Nat. Biotechnol. 31 (2013), 844–847.
97. 97 Sanghvi, V.R., Steel, L.F., A re-examination of global suppression of RNA interference by HIV-1. PLoS One, 6, 2011, e17246.
98. 98 Gammon, D.B., Mello, C.C., RNA interference-mediated antiviral defense in insects. Curr. Opin. Insect Sci. 8 (2015), 111–120.
99. 99 Thounaojam, M.C., et al. MicroRNA 155 regulates Japanese encephalitis virus-induced inflammatory response by targeting Src homology 2-containing inositol phosphatase 1. J. Virol. 88 (2014), 4798–4810.
100. 100 Thounaojam, M.C., et al. MicroRNA-29b modulates Japanese encephalitis virus-induced microglia activation by targeting tumor necrosis factor alpha-induced protein 3. J. Neurochem. 129 (2014), 143–154.
101. 101 Zhu, B., et al. MicroRNA-15b modulates Japanese encephalitis virus-mediated inflammation via targeting RNF125. J. Immunol. 195 (2015), 2251–2262.
102. 102 Kumar, M., Nerurkar, V.R., Integrated analysis of microRNAs and their disease related targets in the brain of mice infected with West Nile virus. Virology 452 (2014), 143–151.
103. 103 Wu, Z., et al. MicroRNA expression profile of mouse lung infected with 2009 pandemic H1N1 influenza virus. PLoS One, 8, 2013, e74190.
104. 104 Buggele, W.A., et al. Influenza A virus infection of human respiratory cells induces primary microRNA expression. J. Biol. Chem. 287 (2012), 31027–31040.
105. 105 Lin, J., et al. MicroRNA-19b downregulates gap junction protein α1 and synergizes with microRNA-1 in viral myocarditis. Int. J. Mol. Sci., 17, 2016, 741.
106. 106 Xu, H-F., et al. MicroRNA-1 represses Cx43 expression in viral myocarditis. Mol. Cell. Biochem. 362 (2011), 141–148.
107. 107 Chang, Y-L., et al. miR-146a and miR-370 coordinate enterovirus 71-induced cell apoptosis through targeting SOS1 and GADD45β. Cell. Microbiol. 17 (2015), 802–818.
108. 108 Smith, J.L., et al. Induction of the cellular microRNA, Hs_154, by West Nile virus contributes to virus-mediated apoptosis through repression of antiapoptotic factors. J. Virol. 86 (2012), 5278–5287.
109. 109 Othumpangat, S., et al. Lung epithelial cells resist influenza A infection by inducing the expression of cytochrome c oxidase VIc which is modulated by miRNA 4276. Virology 468 (2014), 256–264.
110. 110 Stewart, C.R., et al. Promotion of Hendra virus replication by microRNA 146a. J. Virol. 87 (2013), 3782–3791.