1887

Abstract

Porcine reproductive and respiratory syndrome (PRRS) is one of the most important diseases in pigs. MicroRNAs (miRNAs) have emerged as an important regulator of virus–host cell interactions and miR-30c has been found to facilitate PRRSV replication. Here, we found that the interferon-alpha/beta receptor beta chain (IFNAR2) was down-regulated, while miR-30c was up-regulated during HV (a highly pathogenic type 2 PRRSV strain) and CH-1a (a classic type 2 PRRSV strain) infection. Subsequently, using bioinformatics analysis, we predicted that the IFNAR2 was targeted by miR-30c. A luciferase assay verified that the 3′ UTR of IFNAR2 was targeted by miR-30c, as a mutation on either the target sequence or the miR-30c seed sequence reversed the luciferase activity. In addition, miR-30c and IFNAR2 mRNA were physically co-localized in RNA-induced silencing complex (RISC). Importantly, we showed that miR-30c also impaired the induction of IFN-stimulated genes (ISGs) by targeting IFNAR2. Our findings further reveal the mechanism of miR-30c promoting PRRSV replication.

Keyword(s): IFN-I , IFNAR2 , miR-30c and PRRSV
Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.001166
2018-11-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/jgv/99/12/1671.html?itemId=/content/journal/jgv/10.1099/jgv.0.001166&mimeType=html&fmt=ahah

References

  1. Benfield DA, Nelson E, Collins JE, Harris L, Goyal SM et al. Characterization of swine infertility and respiratory syndrome (SIRS) virus (isolate ATCC VR-2332). J Vet Diagn Invest 1992; 4:127–133 [View Article][PubMed]
    [Google Scholar]
  2. Wensvoort G, Terpstra C, Pol JM, Ter Laak EA, Bloemraad M et al. Mystery swine disease in The Netherlands: the isolation of Lelystad virus. Vet Q 1991; 13:121–130 [View Article][PubMed]
    [Google Scholar]
  3. Han M, Yoo D. Engineering the PRRS virus genome: updates and perspectives. Vet Microbiol 2014; 174:279–295 [View Article][PubMed]
    [Google Scholar]
  4. Lunney JK, Fang Y, Ladinig A, Chen N, Li Y et al. Porcine reproductive and respiratory syndrome virus (PRRSV): pathogenesis and interaction with the immune system. Annu Rev Anim Biosci 2016; 4:129–154 [View Article][PubMed]
    [Google Scholar]
  5. Kappes MA, Faaberg KS. PRRSV structure, replication and recombination: Origin of phenotype and genotype diversity. Virology 2015; 479-480:475–486 [View Article][PubMed]
    [Google Scholar]
  6. Plagemann PG, Moennig V. Lactate dehydrogenase-elevating virus, equine arteritis virus, and simian hemorrhagic fever virus: a new group of positive-strand RNA viruses. Adv Virus Res 1992; 41:99–192[PubMed]
    [Google Scholar]
  7. Dunowska M, Biggs PJ, Zheng T, Perrott MR. Identification of a novel nidovirus associated with a neurological disease of the Australian brushtail possum (Trichosurus vulpecula). Vet Microbiol 2012; 156:418–424 [View Article][PubMed]
    [Google Scholar]
  8. Huang C, Zhang Q, Feng WH. Regulation and evasion of antiviral immune responses by porcine reproductive and respiratory syndrome virus. Virus Res 2015; 202:101–111 [View Article][PubMed]
    [Google Scholar]
  9. Morrison RB, Collins JE, Harris L, Christianson WT, Benfield DA et al. Serologic evidence incriminating a recently isolated virus (ATCC VR-2332) as the cause of swine infertility and respiratory syndrome (SIRS). J Vet Diagn Invest 1992; 4:186–188 [View Article][PubMed]
    [Google Scholar]
  10. Renukaradhya GJ, Alekseev K, Jung K, Fang Y, Saif LJ. Porcine reproductive and respiratory syndrome virus-induced immunosuppression exacerbates the inflammatory response to porcine respiratory coronavirus in pigs. Viral Immunol 2010; 23:457–466 [View Article][PubMed]
    [Google Scholar]
  11. Dwivedi V, Manickam C, Patterson R, Dodson K, Murtaugh M et al. Cross-protective immunity to porcine reproductive and respiratory syndrome virus by intranasal delivery of a live virus vaccine with a potent adjuvant. Vaccine 2011; 29:4058–4066 [View Article][PubMed]
    [Google Scholar]
  12. Albina E, Carrat C, Charley B. Interferon-alpha response to swine arterivirus (PoAV), the porcine reproductive and respiratory syndrome virus. J Interferon Cytokine Res 1998; 18:485–490 [View Article][PubMed]
    [Google Scholar]
  13. Koyama S, Ishii KJ, Coban C, Akira S. Innate immune response to viral infection. Cytokine 2008; 43:336–341 [View Article][PubMed]
    [Google Scholar]
  14. Feng W, Laster SM, Tompkins M, Brown T, Xu JS et al. In utero infection by porcine reproductive and respiratory syndrome virus is sufficient to increase susceptibility of piglets to challenge by Streptococcus suis type II. J Virol 2001; 75:4889–4895 [View Article][PubMed]
    [Google Scholar]
  15. Stetson DB, Medzhitov R. Type I interferons in host defense. Immunity 2006; 25:373–381 [View Article][PubMed]
    [Google Scholar]
  16. Le Bon A, Tough DF. Links between innate and adaptive immunity via type I interferon. Curr Opin Immunol 2002; 14:432–436 [View Article][PubMed]
    [Google Scholar]
  17. Content J. Mechanisms of induction and action of interferons. Verh K Acad Geneeskd Belg 2009; 71:51–71[PubMed]
    [Google Scholar]
  18. Tovey MG, Lallemand C, Thyphronitis G. Adjuvant activity of type I interferons. Biol Chem 2008; 389:541–545 [View Article][PubMed]
    [Google Scholar]
  19. Hoffmann HH, Schneider WM, Rice CM. Interferons and viruses: an evolutionary arms race of molecular interactions. Trends Immunol 2015; 36:124–138 [View Article][PubMed]
    [Google Scholar]
  20. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009; 136:215–233 [View Article][PubMed]
    [Google Scholar]
  21. Qiu J, Smith P, Leahy L, Thorley-Lawson DA. The Epstein-Barr virus encoded BART miRNAs potentiate tumor growth in vivo. PLoS Pathog 2015; 11:e1004561 [View Article][PubMed]
    [Google Scholar]
  22. Pasquinelli AE. MicroRNAs and their targets: recognition, regulation and an emerging reciprocal relationship. Nat Rev Genet 2012; 13:271–282 [View Article][PubMed]
    [Google Scholar]
  23. Eulalio A, Huntzinger E, Izaurralde E. Getting to the root of miRNA-mediated gene silencing. Cell 2008; 132:9–14 [View Article][PubMed]
    [Google Scholar]
  24. Nottrott S, Simard MJ, Richter JD. Human let-7a miRNA blocks protein production on actively translating polyribosomes. Nat Struct Mol Biol 2006; 13:1108–1114 [View Article][PubMed]
    [Google Scholar]
  25. Elton TS, Selemon H, Elton SM, Parinandi NL. Regulation of the MIR155 host gene in physiological and pathological processes. Gene 2013; 532:1–12 [View Article][PubMed]
    [Google Scholar]
  26. Wang Y, Sun HH, Sui MH, Ma JJ. miR-218 inhibits acute promyelocytic leukemia cell growth by targeting BMI-1. Oncol Lett 2017; 14:8078–8083 [View Article][PubMed]
    [Google Scholar]
  27. O'Connor CM, Vanicek J, Murphy EA. Host microRNA regulation of human cytomegalovirus immediate early protein translation promotes viral latency. J Virol 2014; 88:5524–5532 [View Article][PubMed]
    [Google Scholar]
  28. Liu F, du Y, Feng WH. New perspective of host microRNAs in the control of PRRSV infection. Vet Microbiol 2017; 209:48–56 [View Article][PubMed]
    [Google Scholar]
  29. Guo XK, Zhang Q, Gao L, Li N, Chen XX et al. Increasing expression of microRNA 181 inhibits porcine reproductive and respiratory syndrome virus replication and has implications for controlling virus infection. J Virol 2013; 87:1159–1171 [View Article][PubMed]
    [Google Scholar]
  30. Gao L, Guo XK, Wang L, Zhang Q, Li N et al. MicroRNA 181 suppresses porcine reproductive and respiratory syndrome virus (PRRSV) infection by targeting PRRSV receptor CD163. J Virol 2013; 87:8808–8812 [View Article][PubMed]
    [Google Scholar]
  31. Xiao S, Wang X, Ni H, Li N, Zhang A et al. MicroRNA miR-24-3p promotes porcine reproductive and respiratory syndrome virus replication through suppression of heme oxygenase-1 expression. J Virol 2015; 89:4494–4503 [View Article][PubMed]
    [Google Scholar]
  32. Zhang Q, Huang C, Yang Q, Gao L, Liu HC et al. MicroRNA-30c modulates type I IFN responses to facilitate porcine reproductive and respiratory syndrome virus infection by targeting JAK1. J Immunol 2016; 196:2272–2282 [View Article][PubMed]
    [Google Scholar]
  33. Qian X, Xu C, Fang S, Zhao P, Wang Y et al. Exosomal MicroRNAs derived from umbilical mesenchymal stem cells inhibit hepatitis C virus infection. Stem Cells Transl Med 2016; 5:1190–1203 [View Article][PubMed]
    [Google Scholar]
  34. Mizuguchi Y, Takizawa T, Uchida E. Host cellular microRNA involvement in the control of hepatitis B virus gene expression and replication. World J Hepatol 2015; 7:696–702 [View Article][PubMed]
    [Google Scholar]
  35. Kim S, Seo D, Kim D, Hong Y, Chang H et al. Temporal landscape of MicroRNA-mediated host-virus crosstalk during productive human cytomegalovirus infection. Cell Host Microbe 2015; 17:838–851 [View Article][PubMed]
    [Google Scholar]
  36. Sun Y, Han M, Kim C, Calvert JG, Yoo D. Interplay between interferon-mediated innate immunity and porcine reproductive and respiratory syndrome virus. Viruses 2012; 4:424–446 [View Article][PubMed]
    [Google Scholar]
  37. Huang C, Zhang Q, Guo XK, Yu ZB, Xu AT et al. Porcine reproductive and respiratory syndrome virus nonstructural protein 4 antagonizes beta interferon expression by targeting the NF-κB essential modulator. J Virol 2014; 88:10934–10945 [View Article][PubMed]
    [Google Scholar]
  38. Guo R, Katz BB, Tomich JM, Gallagher T, Fang Y. Porcine reproductive and respiratory syndrome virus utilizes nanotubes for intercellular spread. J Virol 2016; 90:5163–5175 [View Article][PubMed]
    [Google Scholar]
  39. Wang T, Fang L, Zhao F, Wang D, Xiao S. Exosomes mediate intercellular transmission of porcine reproductive and respiratory syndrome virus. J Virol 2018; 92:e01734-17 [View Article][PubMed]
    [Google Scholar]
  40. Chen J, Shi X, Zhang X, Wang A, Wang L et al. MicroRNA 373 facilitates the replication of porcine reproductive and respiratory syndrome virus by its negative regulation of type I interferon induction. J Virol 2017; 91:e01311-16 [View Article][PubMed]
    [Google Scholar]
  41. Zhang Q, Guo XK, Gao L, Huang C, Li N et al. MicroRNA-23 inhibits PRRSV replication by directly targeting PRRSV RNA and possibly by upregulating type I interferons. Virology 2014; 450-451:182–195 [View Article][PubMed]
    [Google Scholar]
  42. Li L, Wei Z, Zhou Y, Gao F, Jiang Y et al. Host miR-26a suppresses replication of porcine reproductive and respiratory syndrome virus by upregulating type I interferons. Virus Res 2015; 195:86–94 [View Article][PubMed]
    [Google Scholar]
  43. Uzé G, Schreiber G, Piehler J, Pellegrini S. The receptor of the type I interferon family. Curr Top Microbiol Immunol 2007; 316:71–95[PubMed]
    [Google Scholar]
  44. Duncan CJ, Mohamad SM, Young DF, Skelton AJ, Leahy TR et al. Human IFNAR2 deficiency: lessons for antiviral immunity. Sci Transl Med 2015; 7:307ra154 [View Article][PubMed]
    [Google Scholar]
  45. El Fiky A, Arch AE, Krolewski JJ. Intracellular domain of the IFNaR2 interferon receptor subunit mediates transcription via Stat2. J Cell Physiol 2005; 204:567–573 [View Article][PubMed]
    [Google Scholar]
  46. El Fiky A, Pioli P, Azam A, Yoo K, Nastiuk KL et al. Nuclear transit of the intracellular domain of the interferon receptor subunit IFNaR2 requires Stat2 and Irf9. Cell Signal 2008; 20:1400–1408 [View Article][PubMed]
    [Google Scholar]
  47. Usacheva A, Sandoval R, Domanski P, Kotenko SV, Nelms K et al. Contribution of the Box 1 and Box 2 motifs of cytokine receptors to Jak1 association and activation. J Biol Chem 2002; 277:48220–48226 [View Article][PubMed]
    [Google Scholar]
  48. Malakhova OA, Kim KI, Luo JK, Zou W, Kumar KG et al. UBP43 is a novel regulator of interferon signaling independent of its ISG15 isopeptidase activity. EMBO J 2006; 25:2358–2367 [View Article][PubMed]
    [Google Scholar]
  49. Akabayov SR, Biron Z, Lamken P, Piehler J, Anglister J. NMR mapping of the IFNAR1-EC binding site on IFNalpha2 reveals allosteric changes in the IFNAR2-EC binding site. Biochemistry 2010; 49:687–695 [View Article][PubMed]
    [Google Scholar]
  50. Piehler J, Schreiber G. Biophysical analysis of the interaction of human ifnar2 expressed in E. coli with IFNalpha2. J Mol Biol 1999; 289:57–67 [View Article][PubMed]
    [Google Scholar]
  51. Romporn S, Hirankarn N, Tangkijvanich P, Kimkong I. Association of IFNAR2 and IL10RB genes in chronic hepatitis B virus infection. Tissue Antigens 2013; 82:21–25 [View Article][PubMed]
    [Google Scholar]
  52. Rudnicki M, Perco P, D Haene B, Leierer J, Heinzel A et al. Renal microRNA- and RNA-profiles in progressive chronic kidney disease. Eur J Clin Invest 2016; 46:213–226 [View Article][PubMed]
    [Google Scholar]
  53. Chairatvit K, Wongnoppavich A, Choonate S. Up-regulation of interferon-stimulated gene15 and its conjugates by tumor necrosis factor-α via type I interferon-dependent and -independent pathways. Mol Cell Biochem 2012; 368:195–201 [View Article][PubMed]
    [Google Scholar]
  54. de Weerd NA, Nguyen T. The interferons and their receptors–distribution and regulation. Immunol Cell Biol 2012; 90:483–491 [View Article][PubMed]
    [Google Scholar]
  55. Schreiber G, Piehler J. The molecular basis for functional plasticity in type I interferon signaling. Trends Immunol 2015; 36:139–149 [View Article][PubMed]
    [Google Scholar]
  56. Hou J, Wang L, He W, Zhang H, Feng WH. Highly pathogenic porcine reproductive and respiratory syndrome virus impairs LPS- and poly(I:C)-stimulated tumor necrosis factor-alpha release by inhibiting ERK signaling pathway. Virus Res 2012; 167:106–111 [View Article][PubMed]
    [Google Scholar]
  57. Shi R, Sun YH, Zhang XH, Chiang VL. Poly(T) adaptor RT-PCR. Methods Mol Biol 2012; 822:53–66 [View Article][PubMed]
    [Google Scholar]
  58. Bookout AL, Cummins CL, Mangelsdorf DJ, Pesola JM, Kramer MF. High-throughput real-time quantitative reverse transcription PCR. Curr Protoc Mol Biol 2006; 73:15.8.1–15.8.28 [View Article][PubMed]
    [Google Scholar]
  59. Wang WX, Wilfred BR, Hu Y, Stromberg AJ, Nelson PT. Anti-Argonaute RIP-Chip shows that miRNA transfections alter global patterns of mRNA recruitment to microribonucleoprotein complexes. RNA 2010; 16:394–404 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.001166
Loading
/content/journal/jgv/10.1099/jgv.0.001166
Loading

Data & Media loading...

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