1887

Abstract

MicroRNAs (miRNAs) are a class of small regulatory non-coding RNAs that modulate gene expression at the post-transcriptional level, playing a crucial role in cell differentiation and development. Recently, some reports have demonstrated that a number of cellular miRNAs play a role during viral infection. In this study, a luciferase-reporter system carrying the 5′ untranslated region (5′ UTR) and 3′ UTR of avian leukosis virus subgroup J (ALV-J) was used to determine whether cellular miRNAs are involved in ALV-J infection. The miRNA gga-miR-1650 was screened for its potential interaction with the 5′ UTR of ALV-J and the ability to suppress luciferase-reporter activity. A mutational analysis of predicted gga-miR-1650-binding sites showed that the 5′ and 3′ ends of gga-miR-1650 contributed to the interaction between gga-miR-1650 and its target located at the 5′ UTR. Overexpression of miRNA gga-miR-1650 was shown to downregulate the expression of the Gag protein and influence the replication of ALV-J through binding to the 5′ UTR. Overall, this report provides the basis for the development of new strategies for anti-ALV-J intervention.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.054007-0
2013-10-01
2020-01-23
Loading full text...

Full text loading...

/deliver/fulltext/jgv/94/10/2287.html?itemId=/content/journal/jgv/10.1099/vir.0.054007-0&mimeType=html&fmt=ahah

References

  1. Ahluwalia J. K., Khan S. Z., Soni K., Rawat P., Gupta A., Hariharan M., Scaria V., Lalwani M., Pillai B.. & other authors ( 2008;). Human cellular microRNA hsa-miR-29a interferes with viral nef protein expression and HIV-1 replication. . Retrovirology 5:, 117. [CrossRef][PubMed]
    [Google Scholar]
  2. Ambros V.. ( 2004;). The functions of animal microRNAs. . Nature 431:, 350–355. [CrossRef][PubMed]
    [Google Scholar]
  3. Bagga S., Bracht J., Hunter S., Massirer K., Holtz J., Eachus R., Pasquinelli A. E.. ( 2005;). Regulation by let-7 and lin-4 miRNAs results in target mRNA degradation. . Cell 122:, 553–563. [CrossRef][PubMed]
    [Google Scholar]
  4. Bakre A., Mitchell P., Coleman J. K., Jones L. P., Saavedra G., Teng M., Tompkins S. M., Tripp R. A.. ( 2012;). Respiratory syncytial virus modifies microRNAs regulating host genes that affect virus replication. . J Gen Virol 93:, 2346–2356. [CrossRef][PubMed]
    [Google Scholar]
  5. Barnes D., Kunitomi M., Vignuzzi M., Saksela K., Andino R.. ( 2008;). Harnessing endogenous miRNAs to control virus tissue tropism as a strategy for developing attenuated virus vaccines. . Cell Host Microbe 4:, 239–248. [CrossRef][PubMed]
    [Google Scholar]
  6. Bartel D. P.. ( 2004;). MicroRNAs: genomics, biogenesis, mechanism, and function. . Cell 116:, 281–297. [CrossRef][PubMed]
    [Google Scholar]
  7. Berkhout B., Jeang K. T.. ( 2007;). RISCy business: MicroRNAs, pathogenesis, and viruses. . J Biol Chem 282:, 26641–26645. [CrossRef][PubMed]
    [Google Scholar]
  8. Bhattacharyya S. N., Habermacher R., Martine U., Closs E. I., Filipowicz W.. ( 2006;). Relief of microRNA-mediated translational repression in human cells subjected to stress. . Cell 125:, 1111–1124. [CrossRef][PubMed]
    [Google Scholar]
  9. Burnside J., Ouyang M., Anderson A., Bernberg E., Lu C., Meyers B. C., Green P. J., Markis M., Isaacs G.. & other authors ( 2008;). Deep sequencing of chicken microRNAs. . BMC Genomics 9:, 185. [CrossRef][PubMed]
    [Google Scholar]
  10. Carrington J. C., Ambros V.. ( 2003;). Role of microRNAs in plant and animal development. . Science 301:, 336–338. [CrossRef][PubMed]
    [Google Scholar]
  11. Davis S., Lollo B., Freier S., Esau C.. ( 2006;). Improved targeting of miRNA with antisense oligonucleotides. . Nucleic Acids Res 34:, 2294–2304. [CrossRef][PubMed]
    [Google Scholar]
  12. Deng X., Qi X., Wu G., Gao Y., Qin L., Wang Y., Gao H., Wang X.. ( 2012;). Construction and characterization of the infectious clone of Reticuloendotheliosis virus carrying a genetic marker. . Virus Res 167:, 146–151. [CrossRef][PubMed]
    [Google Scholar]
  13. Doria-Rose N. A., Vogt V. M.. ( 1998;). In vivo selection of Rous sarcoma virus mutants with randomized sequences in the packaging signal. . J Virol 72:, 8073–8082.[PubMed]
    [Google Scholar]
  14. Eulalio A., Huntzinger E., Izaurralde E.. ( 2008;). Getting to the root of miRNA-mediated gene silencing. . Cell 132:, 9–14. [CrossRef][PubMed]
    [Google Scholar]
  15. Finzi D., Hermankova M., Pierson T., Carruth L. M., Buck C., Chaisson R. E., Quinn T. C., Chadwick K., Margolick J.. & other authors ( 1997;). Identification of a reservoir for HIV-1 in patients on highly active antiretroviral therapy. . Science 278:, 1295–1300. [CrossRef][PubMed]
    [Google Scholar]
  16. Gao Y.-L., Qin L.-T., Pan W., Wang Y.-Q., Le Qi X.-L., Gao H.-L., Wang X.-M.. ( 2010;). Avian leukosis virus subgroup J in layer chickens, China. . Emerg Infect Dis 16:, 1637–1638. [CrossRef][PubMed]
    [Google Scholar]
  17. Gao Y., Yun B., Qin L., Pan W., Qu Y., Liu Z., Wang Y., Qi X., Gao H., Wang X.. ( 2012;). Molecular epidemiology of avian leukosis virus subgroup J in layer flocks in China. . J Clin Microbiol 50:, 953–960. [CrossRef][PubMed]
    [Google Scholar]
  18. Glazov E. A., Cottee P. A., Barris W. C., Moore R. J., Dalrymple B. P., Tizard M. L.. ( 2008;). A microRNA catalog of the developing chicken embryo identified by a deep sequencing approach. . Genome Res 18:, 957–964. [CrossRef][PubMed]
    [Google Scholar]
  19. Grimson A., Farh K. K., Johnston W. K., Garrett-Engele P., Lim L. P., Bartel D. P.. ( 2007;). MicroRNA targeting specificity in mammals: determinants beyond seed pairing. . Mol Cell 27:, 91–105. [CrossRef][PubMed]
    [Google Scholar]
  20. Ha I., Wightman B., Ruvkun G.. ( 1996;). A bulged lin-4/lin-14 RNA duplex is sufficient for Caenorhabditis elegans lin-14 temporal gradient formation. . Genes Dev 10:, 3041–3050. [CrossRef][PubMed]
    [Google Scholar]
  21. Himly M., Foster D. N., Bottoli I., Iacovoni J. S., Vogt P. K.. ( 1998;). The DF-1 chicken fibroblast cell line: transformation induced by diverse oncogenes and cell death resulting from infection by avian leukosis viruses. . Virology 248:, 295–304. [CrossRef][PubMed]
    [Google Scholar]
  22. Huang J., Wang F., Argyris E., Chen K., Liang Z., Tian H., Huang W., Squires K., Verlinghieri G., Zhang H.. ( 2007;). Cellular microRNAs contribute to HIV-1 latency in resting primary CD4+ T lymphocytes. . Nat Med 13:, 1241–1247. [CrossRef][PubMed]
    [Google Scholar]
  23. Hussain A. I., Johnson J. A., Da Silva Freire M., Heneine W.. ( 2003;). Identification and characterization of avian retroviruses in chicken embryo-derived yellow fever vaccines: investigation of transmission to vaccine recipients. . J Virol 77:, 1105–1111. [CrossRef][PubMed]
    [Google Scholar]
  24. Hussain M., Torres S., Schnettler E., Funk A., Grundhoff A., Pijlman G. P., Khromykh A. A., Asgari S.. ( 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:, 2210–2223. [CrossRef][PubMed]
    [Google Scholar]
  25. Jopling C. L., Yi M., Lancaster A. M., Lemon S. M., Sarnow P.. ( 2005;). Modulation of hepatitis C virus RNA abundance by a liver-specific microRNA. . Science 309:, 1577–1581. [CrossRef][PubMed]
    [Google Scholar]
  26. Kim Y. J., Bae S. W., Yu S. S., Bae Y. C., Jung J. S.. ( 2009;). miR-196a regulates proliferation and osteogenic differentiation in mesenchymal stem cells derived from human adipose tissue. . J Bone Miner Res 24:, 816–825. [CrossRef][PubMed]
    [Google Scholar]
  27. Kurihara Y., Takashi Y., Watanabe Y.. ( 2006;). The interaction between DCL1 and HYL1 is important for efficient and precise processing of pri-miRNA in plant microRNA biogenesis. . RNA 12:, 206–212. [CrossRef][PubMed]
    [Google Scholar]
  28. Lecellier C. H., Dunoyer P., Arar K., Lehmann-Che J., Eyquem S., Himber C., Saïb A., Voinnet O.. ( 2005;). A cellular microRNA mediates antiviral defense in human cells. . Science 308:, 557–560. [CrossRef][PubMed]
    [Google Scholar]
  29. Lee I., Ajay S. S., Yook J. I., Kim H. S., Hong S. H., Kim N. H., Dhanasekaran S. M., Chinnaiyan A. M., Athey B. D.. ( 2009;). New class of microRNA targets containing simultaneous 5′-UTR and 3′-UTR interaction sites. . Genome Res 19:, 1175–1183. [CrossRef][PubMed]
    [Google Scholar]
  30. Lewis B. P., Shih I. H., Jones-Rhoades M. W., Bartel D. P., Burge C. B.. ( 2003;). Prediction of mammalian microRNA targets. . Cell 115:, 787–798. [CrossRef][PubMed]
    [Google Scholar]
  31. Li K., Gao H., Gao L., Qi X., Qin L., Gao Y., Xu Y., Wang X.. ( 2012;). Development of TaqMan real-time PCR assay for detection and quantitation of reticuloendotheliosis virus. . J Virol Methods 179:, 402–408. [CrossRef][PubMed]
    [Google Scholar]
  32. Mahajan V. S., Drake A., Chen J.. ( 2009;). Virus-specific host miRNAs: antiviral defenses or promoters of persistent infection?. Trends Immunol 30:, 1–7. [CrossRef][PubMed]
    [Google Scholar]
  33. Ørom U. A., Nielsen F. C., Lund A. H.. ( 2008;). MicroRNA-10a binds the 5′UTR of ribosomal protein mRNAs and enhances their translation. . Mol Cell 30:, 460–471. [CrossRef][PubMed]
    [Google Scholar]
  34. Poole E., McGregor Dallas S. R., Colston J., Joseph R. S., Sinclair J.. ( 2011;). Virally induced changes in cellular microRNAs maintain latency of human cytomegalovirus in CD34+ progenitors. . J Gen Virol 92:, 1539–1549. [CrossRef][PubMed]
    [Google Scholar]
  35. Potenza N., Papa U., Mosca N., Zerbini F., Nobile V., Russo A.. ( 2011;). Human microRNA hsa-miR-125a-5p interferes with expression of hepatitis B virus surface antigen. . Nucleic Acids Res 39:, 5157–5163. [CrossRef][PubMed]
    [Google Scholar]
  36. Qin A., Lee L. F., Fadly A., Hunt H., Cui Z.. ( 2001;). Development and characterization of monoclonal antibodies to subgroup J avian leukosis virus. . Avian Dis 45:, 938–945. [CrossRef][PubMed]
    [Google Scholar]
  37. Qin L., Gao Y., Ni W., Sun M., Wang Y., Yin C., Qi X., Gao H., Wang X.. ( 2013;). Development and application of real-time PCR for detection of subgroup J avian leukosis virus. . J Clin Microbiol 51:, 149–154. [CrossRef][PubMed]
    [Google Scholar]
  38. Rajewsky N.. ( 2006;). microRNA target predictions in animals. . Nat Genet 38: (Suppl), S8–S13. [CrossRef][PubMed]
    [Google Scholar]
  39. Roberts A. P., Lewis A. P., Jopling C. L.. ( 2011;). miR-122 activates hepatitis C virus translation by a specialized mechanism requiring particular RNA components. . Nucleic Acids Res 39:, 7716–7729. [CrossRef][PubMed]
    [Google Scholar]
  40. Ronemus M., Vaughn M. W., Martienssen R. A.. ( 2006;). MicroRNA-targeted and small interfering RNA-mediated mRNA degradation is regulated by argonaute, dicer, and RNA-dependent RNA polymerase in Arabidopsis. . Plant Cell 18:, 1559–1574. [CrossRef][PubMed]
    [Google Scholar]
  41. Scaria V., Hariharan M., Maiti S., Pillai B., Brahmachari S. K.. ( 2006;). Host–virus interaction: a new role for microRNAs. . Retrovirology 3:, 68. [CrossRef][PubMed]
    [Google Scholar]
  42. Song L., Liu H., Gao S., Jiang W., Huang W.. ( 2010;). Cellular microRNAs inhibit replication of the H1N1 influenza A virus in infected cells. . J Virol 84:, 8849–8860. [CrossRef][PubMed]
    [Google Scholar]
  43. Stern-Ginossar N., Elefant N., Zimmermann A., Wolf D. G., Saleh N., Biton M., Horwitz E., Prokocimer Z., Prichard M.. & other authors ( 2007;). Host immune system gene targeting by a viral miRNA. . Science 317:, 376–381. [CrossRef][PubMed]
    [Google Scholar]
  44. Sullivan C. S., Grundhoff A. T., Tevethia S., Pipas J. M., Ganem D.. ( 2005;). SV40-encoded microRNAs regulate viral gene expression and reduce susceptibility to cytotoxic T cells. . Nature 435:, 682–686. [CrossRef][PubMed]
    [Google Scholar]
  45. Sun W., Julie Li Y. S., Huang H. D., Shyy J. Y., Chien S.. ( 2010;). microRNA: a master regulator of cellular processes for bioengineering systems. . Annu Rev Biomed Eng 12:, 1–27. [CrossRef][PubMed]
    [Google Scholar]
  46. Sun G., Li H., Wu X., Covarrubias M., Scherer L., Meinking K., Luk B., Chomchan P., Alluin J.. & other authors ( 2012;). Interplay between HIV-1 infection and host microRNAs. . Nucleic Acids Res 40:, 2181–2196. [CrossRef][PubMed]
    [Google Scholar]
  47. Vella M. C., Choi E. Y., Lin S. Y., Reinert K., Slack F. J.. ( 2004;). The C. elegans microRNA let-7 binds to imperfect let-7 complementary sites from the lin-41 3′UTR. . Genes Dev 18:, 132–137. [CrossRef][PubMed]
    [Google Scholar]
  48. Wang Q., Wang Y., Gao Y., Qin L., Qi X., Gao H., Wang X.. ( 2011;). Isolation and identification molecular characterization of a subgroup J avian leukosis virus isolate SD1009. . Chin J Prev Vet Med 33:, 593–597.
    [Google Scholar]
  49. Wang Q., Gao Y., Wang Y., Qin L., Qi X., Qu Y., Gao H., Wang X.. ( 2012;). A 205-nucleotide deletion in the 3′ untranslated region of avian leukosis virus subgroup J, currently emergent in China, contributes to its pathogenicity. . J Virol 86:, 12849–12860. [CrossRef][PubMed]
    [Google Scholar]
  50. Wu L., Fan J., Belasco J. G.. ( 2006;). MicroRNAs direct rapid deadenylation of mRNA. . Proc Natl Acad Sci U S A 103:, 4034–4039. [CrossRef][PubMed]
    [Google Scholar]
  51. Yao Y., Zhao Y., Smith L. P., Lawrie C. H., Saunders N. J., Watson M., Nair V.. ( 2009;). Differential expression of microRNAs in Marek’s disease virus-transformed T-lymphoma cell lines. . J Gen Virol 90:, 1551–1559. [CrossRef][PubMed]
    [Google Scholar]
  52. Yekta S., Shih I. H., Bartel D. P.. ( 2004;). MicroRNA-directed cleavage of HOXB8 mRNA. . Science 304:, 594–596. [CrossRef][PubMed]
    [Google Scholar]
  53. Yoon S., De Micheli G.. ( 2006;). Computational identification of microRNAs and their targets. . Birth Defects Res C Embryo Today 78:, 118–128. [CrossRef][PubMed]
    [Google Scholar]
  54. Yun B., Li D., Zhu H., Liu W., Qin L., Liu Z., Wu G., Wang Y., Qi X.. & other authors ( 2013;). Development of an antigen-capture ELISA for the detection of avian leukosis virus p27 antigen. . J Virol Methods 187:, 278–283. [CrossRef][PubMed]
    [Google Scholar]
  55. Zhang G. L., Li Y. X., Zheng S. Q., Liu M., Li X., Tang H.. ( 2010;). Suppression of hepatitis B virus replication by microRNA-199a-3p and microRNA-210. . Antiviral Res 88:, 169–175. [CrossRef][PubMed]
    [Google Scholar]
  56. Zhang X., Zhang E., Ma Z., Pei R., Jiang M., Schlaak J. F., Roggendorf M., Lu M.. ( 2011;). Modulation of hepatitis B virus replication and hepatocyte differentiation by MicroRNA-1. . Hepatology 53:, 1476–1485. [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.054007-0
Loading
/content/journal/jgv/10.1099/vir.0.054007-0
Loading

Data & Media loading...

Supplements

Supplementary material 

PDF

Most cited articles

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