Role of virus-encoded microRNAs in avian viral diseases

Viruses

Volumn 6, Issue 3, 2014, Pages 1379-1394

  Yao, Yongxiu ^a   Nair, Venugopal ^a  

^a INSTITUTE FOR ANIMAL HEALTH   (United Kingdom)

Author keywords

Avian leukosis virus; Avian viruses; DEV; ILTV; MDV; MicroRNAs

Indexed keywords

MICRORNA; VIRUS RNA;

BIRD DISEASE; CELL FUNCTION; CELLULAR IMMUNITY; DISEASE ASSOCIATION; HERPES VIRUS; ILTOVIRUS; IMMUNE RESPONSE; MARDIVIRUS; NONHUMAN; ORTHOLOGY; PATHOGENESIS; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVIEW; RNA EXTRACTION; SEQUENCE ANALYSIS; VACCINATION; VIRUS INFECTION;

ANIMALS; BIRDS; GENE EXPRESSION REGULATION; HOST-PATHOGEN INTERACTIONS; MICRORNAS; POULTRY; RNA, VIRAL; VIRUS DISEASES; VIRUS PHYSIOLOGICAL PHENOMENA; VIRUSES;

EID: 84897890777     PISSN: 19994915     EISSN: None     Source Type: Journal    
DOI: 10.3390/v6031379     Document Type: Review

References (69)

1. Lee, R.C.; Feinbaum, R.L.; Ambros, V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993, 75, 843-854.
2. Lagos-Quintana, M.; Rauhut, R.; Lendeckel, W.; Tuschl, T. Identification of novel genes coding for small expressed RNAs. Science 2001, 294, 853-858.
3. Lau, N.C.; Lim, L.P.; Weinstein, E.G.; Bartel, D.P. An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science 2001, 294, 858-862.
4. Lee, R.C.; Ambros, V. An extensive class of small RNAs in Caenorhabditis elegans. Science 2001, 294, 862-864.
5. Cullen, B.R. How do viruses avoid inhibition by endogenous cellular microRNAs. PLoS Pathog. 2013, 9, e1003694.
6. Libri, V.; Miesen, P.; van Rij, R.P.; Buck, A.H. Regulation of microRNA biogenesis and turnover by animals and their viruses. Cell. Mol. Life Sci. 2013, 70, 3525-3544.
7. Kincaid, R.P.; Sullivan, C.S. Virus-encoded microRNAs: An overview and a look to the future. PLoS Pathog. 2012, 8, e1003018.
8. Chen, C.J.; Cox, J.E.; Kincaid, R.P.; Martinez, A.; Sullivan, C.S. Divergent microrna targetomes of closely related circulating strains of a polyomavirus. J. Virol. 2013, 87, 11135-11147.
9. Kincaid, R.P.; Burke, J.M.; Cox, J.C.; de Villiers, E.M.; Sullivan, C.S. A human torque teno virus encodes a microRNA that inhibits interferon signaling. PLoS Pathog. 2013, 9, e1003818.
10. Lin, J.; Cullen, B.R. Analysis of the interaction of primate retroviruses with the human RNA interference machinery. J. Virol. 2007, 81, 12218-12226.
11. Kincaid, R.P.; Burke, J.M.; Sullivan, C.S. RNA virus microRNA that mimics a B-cell oncomiR. Proc. Natl. Acad. Sci. USA 2012, 109, 3077-3082.
12. Rosewick, N.; Momont, M.; Durkin, K.; Takeda, H.; Caiment, F.; Cleuter, Y.; Vernin, C.; Mortreux, F.; Wattel, E.; Burny, A. et al. Deep sequencing reveals abundant noncanonical retroviral microRNAs in B-cell leukemia/lymphoma. Proc. Natl. Acad. Sci. USA 2013, 110, 2306-2311.
13. Yao, Y.; Smith, L.P.; Nair, V.; Watson, M. An avian retrovirus uses canonical expression and processing mechanisms to generate viral microRNA. J. Virol. 2013, doi:10.1128/JVI.02921-13.
14. Legione, A.R.; Coppo, M.J.; Lee, S.W.; Noormohammadi, A.H.; Hartley, C.A.; Browning, G.F.; Gilkerson, J.R.; O'Rourke, D.; Devlin, J.M. Safety and vaccine efficacy of a glycoprotein G deficient strain of infectious laryngotracheitis virus delivered in vovo. Vaccine 2012, 30, 7193-7198.
15. Morrow, C.; Fehler, F. Marek's disease: A worldwide problem. In Marek's Disease: An Evolving Problem; Davison, F., Nair, V., Eds.; Elsevier Academic Press: Oxford, UK, 2004; pp. 49-61.
16. Bublot, M.; Sharma, J. Vaccination against Marek's disease. In Marek's Disease: An Evolving Problem; Davison, F., Nair, V., Eds.; Elsevier Academic Press: Amsterdam, The Netherlands, 2004; pp. 168-185.
17. Gimeno, I.M. Marek's disease vaccines: A solution for today but a worry for tomorrow? Vaccine 2008, 26, C31-C41.
18. Nair, V. Evolution of Marek's disease-A paradigm for incessant race between the pathogen and the host. Vet. J. 2005, 170, 175-183.
19. Wu, Y.; Cheng, A.; Wang, M.; Zhu, D.; Jia, R.; Chen, S.; Zhou, Y.; Chen, X. Comparative genomic analysis of duck enteritis virus strains. J. Virol. 2012, 86, 13841-13842.
20. Liu, J.; Chen, P.; Jiang, Y.; Deng, G.; Shi, J.; Wu, L.; Lin, Y.; Bu, Z.; Chen, H. Recombinant duck enteritis virus works as a single-dose vaccine in broilers providing rapid protection against H5N1 influenza infection. Antivir. Res. 2013, 97, 329-333.
21. Payne, L.N.; Howes, K.; Gillespie, A.M.; Smith, L.M. Host range of Rous sarcoma virus pseudotype RSV(HPRS-103) in 12 avian species: Support for a new avian retrovirus envelope subgroup, designated J. J. Gen. Virol. 1992, 73, 2995-2997.
22. Payne, L.N.; Brown, S.R.; Bumstead, N.; Howes, K.; Frazier, J.A.; Thouless, M.E. A novel subgroup of exogenous avian leukosis virus in chickens. J. Gen. Virol. 1991, 72, 801-807.
23. Gao, Y.; Yun, B.; Qin, L.; Pan, W.; Qu, Y.; Liu, Z.; Wang, Y.; Qi, X.; Gao, H.; Wang, X. Molecular epidemiology of avian leukosis virus subgroup J in layer flocks in China. J. Clin. Microbiol. 2012, 50, 953-960.
24. Burnside, J.; Bernberg, E.; Anderson, A.; Lu, C.; Meyers, B.C.; Green, P.J.; Jain, N.; Isaacs, G.; Morgan, R.W. Marek's disease virus encodes MicroRNAs that map to meq and the latency-associated transcript. J. Virol. 2006, 80, 8778-8786.
25. Yao, Y.; Zhao, Y.; Xu, H.; Smith, L.P.; Lawrie, C.H.; Watson, M.; Nair, V. MicroRNA profile of Marek's disease virus-transformed T-cell line MSB-1: Predominance of virus-encoded microRNAs. J. Virol. 2008, 82, 4007-4015.
26. Yao, Y.; Zhao, Y.; Xu, H.; Smith, L.P.; Lawrie, C.H.; Sewer, A.; Zavolan, M.; Nair, V. Marek's disease virus type 2 (MDV-2)-encoded microRNAs show no sequence conservation with those encoded by MDV-1. J. Virol. 2007, 81, 7164-7170.
27. Waidner, L.A.; Morgan, R.W.; Anderson, A.S.; Bernberg, E.L.; Kamboj, S.; Garcia, M.; Riblet, S.M.; Ouyang, M.; Isaacs, G.K.; Markis, M. et al. MicroRNAs of Gallid and Meleagrid herpesviruses show generally conserved genomic locations and are virus-specific. Virology 2009, 388, 128-136.
28. Yao, Y.; Zhao, Y.; Smith, L.P.; Watson, M.; Nair, V. Novel microRNAs (miRNAs) encoded by herpesvirus of Turkeys: Evidence of miRNA evolution by duplication. J. Virol. 2009, 83, 6969-6973.
29. Rachamadugu, R.; Lee, J.Y.; Wooming, A.; Kong, B.W. Identification and expression analysis of infectious laryngotracheitis virus encoding microRNAs. Virus Genes 2009, 39, 301-308.
30. Yao, Y.; Smith, L.P.; Petherbridge, L.; Watson, M.; Nair, V. Novel microRNAs encoded by duck enteritis virus. J. Gen. Virol. 2012, 93, 1530-1536.
31. Xu, S.; Xue, C.; Li, J.; Bi, Y.; Cao, Y. Marek's disease virus type 1 microRNA miR-M3 suppresses cisplatin-induced apoptosis by targeting Smad2 of the transforming growth factor beta signal pathway. J. Virol. 2011, 85, 276-285.
32. Zhao, Y.; Yao, Y.; Xu, H.; Lambeth, L.; Smith, L.P.; Kgosana, L.; Wang, X.; Nair, V. A functional MicroRNA-155 ortholog encoded by the oncogenic Marek's disease virus. J. Virol. 2009, 83, 489-492.
33. Muylkens, B.; Coupeau, D.; Dambrine, G.; Trapp, S.; Rasschaert, D. Marek's disease virus microRNA designated Mdv1-pre-miR-M4 targets both cellular and viral genes. Arch. Virol. 2010, 155, 1823-1837.
34. Parnas, O.; Corcoran, D.L.; Cullen, B.R. Analysis of the mRNA targetome of microRNAs expressed by Marek's disease virus. Am. Soc. Microbiol. 2014, 5, doi:10.1128/mBio.01060-13.
35. Strassheim, S.; Stik, G.; Rasschaert, D.; Laurent, S. Mdv1-miR-M7-5p, located in the newly identified first intron of the latency-associated transcript of Marek's disease virus, targets the immediate-early genes ICP4 and ICP27. J. Gen. Virol. 2012, 93, 1731-1742.
36. Waidner, L.A.; Burnside, J.; Anderson, A.S.; Bernberg, E.L.; German, M.A.; Meyers, B.C.; Green, P.J.; Morgan, R.W. A microRNA of infectious laryngotracheitis virus can downregulate and direct cleavage of ICP4 mRNA. Virology 2011, 411, 25-31.
37. Morgan, R.; Anderson, A.; Bernberg, E.; Kamboj, S.; Huang, E.; Lagasse, G.; Isaacs, G.; Parcells, M.; Meyers, B.C.; Green, P.J. et al. Sequence conservation and differential expression of Marek's disease virus microRNAs. J. Virol. 2008, 82, 12213-12220.
38. Burnside, J.; Morgan, R. Emerging roles of chicken and viral microRNAs in avian disease. BMC Proc. 2011, 5, doi:10.1186/1753-6561-5-S4-S2.
39. Coupeau, D.; Dambrine, G.; Rasschaert, D. Kinetic expression analysis of the cluster MDV1-mir-M9-M4, genes meq and vIL-8 differs between the lytic and latent phases of Marek's disease virus infection. J. Gen. Virol. 2012, 93, 1519-1529.
40. Zhao, Y.; Xu, H.; Yao, Y.; Smith, L.P.; Kgosana, L.; Green, J.; Petherbridge, L.; Baigent, S.J.; Nair, V. Critical role of the virus-encoded microRNA-155 ortholog in the induction of Marek's disease lymphomas. PLoS Pathog. 2011, 7, e1001305.
41. Yu, Z.H.; Teng, M.; Sun, A.J.; Yu, L.L.; Hu, B.; Qu, L.H.; Ding, K.; Cheng, X.C.; Liu, J.X.; Cui, Z.Z. et al. Virus-encoded miR-155 ortholog is an important potential regulator but not essential for the development of lymphomas induced by very virulent Marek's disease virus. Virology 2014, 448, 55-64.
42. Brown, A.C.; Nair, V.; Allday, M.J. Epigenetic regulation of the latency-associated region of Marek's disease virus in tumor-derived T-cell lines and primary lymphoma. J. Virol. 2012, 86, 1683-1695.
43. Stik, G.; Laurent, S.; Coupeau, D.; Coutaud, B.; Dambrine, G.; Rasschaert, D.; Muylkens, B. A p53-dependent promoter associated with polymorphic tandem repeats controls the expression of a viral transcript encoding clustered microRNAs. RNA 2010, 16, 2263-2276.
44. Yao, Y.; Zhao, Y.; Smith, L.P.; Lawrie, C.H.; Saunders, N.J.; Watson, M.; Nair, V. Differential expression of microRNAs in Marek's disease virus-transformed T-lymphoma cell lines. J. Gen. Virol. 2009, 90, 1551-1559.
45. Lujambio, A.; Lowe, S.W. The microcosmos of cancer. Nature 2012, 482, 347-355.
46. Xu, H.; Yao, Y.; Smith, L.P.; Nair, V. MicroRNA-26a-mediated regulation of interleukin-2 expression in transformed avian lymphocyte lines. Cancer Cell Int. 2010, 10, 15. doi:10.1186/ 1475-2867-10-15.
47. Hirai, K.; Yamada, M.; Arao, Y.; Kato, S.; Nii, S. Replicating Marek's disease virus (MDV) serotype 2 DNA with inserted MDV serotype 1 DNA sequences in a Marek's disease lymphoblastoid cell line MSB1-41C. Arch. Virol. 1990, 114, 153-165.
48. Xiang, J.; Cheng, A.; Wang, M.; Zhang, S.; Zhu, D.; Jia, R.; Chen, S.; Zhou, Y.; Wang, X.; Chen, X. Computational identification of microRNAs in anatid herpesvirus 1 genome. Virol. J. 2012, 9, e93.
49. Chesters, P.M.; Smith, L.P.; Nair, V. E (XSR) element contributes to the oncogenicity of Avian leukosis virus (subgroup J). J. Gen. Virol. 2006, 87, 2685-2692.
50. Zisoulis, D.G.; Lovci, M.T.; Wilbert, M.L.; Hutt, K.R.; Liang, T.Y.; Pasquinelli, A.E.; Yeo, G.W. Comprehensive discovery of endogenous Argonaute binding sites in Caenorhabditis elegans. Nat. Struct. Mol. Biol. 2010, 17, 173-179.
51. Gottwein, E.; Mukherjee, N.; Sachse, C.; Frenzel, C.; Majoros, W.H.; Chi, J.T.; Braich, R.; Manoharan, M.; Soutschek, J.; Ohler, U. et al. A viral microRNA functions as an orthologue of cellular miR-155. Nature 2007, 450, 1096-1099.
52. Skalsky, R.L.; Samols, M.A.; Plaisance, K.B.; Boss, I.W.; Riva, A.; Lopez, M.C.; Baker, H.V.; Renne, R. Kaposi's sarcoma-associated herpesvirus encodes an ortholog of miR-155. J. Virol. 2007, 81, 12836-12845.
53. McClure, L.V.; Sullivan, C.S. Kaposi's sarcoma herpes virus taps into a host microRNA regulatory network. Cell Host Microbe 2008, 3, 1-3.
54. Tili, E.; Croce, C.M.; Michaille, J.J. Mir-155: On the crosstalk between inflammation and cancer. Int. Rev. Immunol. 2009, 28, 264-284.
55. Faraoni, I.; Antonetti, F.R.; Cardone, J.; Bonmassar, E. Mir-155 gene: A typical multifunctional microRNA. Biochim. Biophys. Acta 2009, 1792, 497-505.
56. Rai, D.; Kim, S.W.; McKeller, M.R.; Dahia, P.L.; Aguiar, R.C. Targeting of SMAD5 links microRNA-155 to the TGF-beta pathway and lymphomagenesis. Proc. Natl. Acad. Sci. USA 2010, 107, 3111-3116.
57. Valeri, N.; Gasparini, P.; Fabbri, M.; Braconi, C.; Veronese, A.; Lovat, F.; Adair, B.; Vannini, I.; Fanini, F.; Bottoni, A. et al. Modulation of mismatch repair and genomic stability by miR-155. Proc. Natl. Acad. Sci. USA 2010, 107, 6982-6987.
58. Lu, F.; Weidmer, A.; Liu, C.G.; Volinia, S.; Croce, C.M.; Lieberman, P.M. Epstein-Barr virus-induced miR-155 attenuates NF-κB signaling and stabilizes latent virus persistence. J. Virol. 2008, 82, 10436-10443.
59. Bolisetty, M.T.; Dy, G.; Tam, W.; Beemon, K.L. Reticuloendotheliosis virus strain T induces miR-155, which targets JARID2 and promotes cell survival. J. Virol. 2009, 83, 12009-12017.
60. Fornari, F.; Gramantieri, L.; Ferracin, M.; Veronese, A.; Sabbioni, S.; Calin, G.A.; Grazi, G.L.; Giovannini, C.; Croce, C.M.; Bolondi, L. et al. MiR-221 controls CDKN1C/p57 and CDKN1B/p27 expression in human hepatocellular carcinoma. Oncogene 2008, 27, 5651-5661.
61. Galardi, S.; Mercatelli, N.; Giorda, E.; Massalini, S.; Frajese, G.V.; Ciafre, S.A.; Farace, M.G. Mir-221 and miR-222 expression affects the proliferation potential of human prostate carcinoma cell lines by targeting p27Kip1. J. Biol. Chem. 2007, 282, 23716-23724.
62. Lambeth, L.S.; Yao, Y.; Smith, L.P.; Zhao, Y.; Nair, V. MicroRNAs 221 and 222 target p27Kip1 in Marek's disease virus-transformed tumour cell line MSB-1. J. Gen. Virol. 2009, 90, 1164-1171.
63. Pekarsky, Y.; Croce, C.M. Is miR-29 an oncogene or tumor suppressor in CLL? Oncotarget 2010, 1, 224-227.
64. Carl, J.W., Jr.; Trgovcich, J.; Hannenhalli, S. Widespread evidence of viral miRNAs targeting host pathways. BMC Bioinform. 2013, 14, doi:10.1186/1471-2105-14-S2-S3.
65. Umbach, J.L.; Kramer, M.F.; Jurak, I.; Karnowski, H.W.; Coen, D.M.; Cullen, B.R. MicroRNAs expressed by herpes simplex virus 1 during latent infection regulate viral mRNAs. Nature 2008, 454, 780-783.
66. Brown, K.M.; Chu, C.Y.; Rana, T.M. Target accessibility dictates the potency of human RISC. Nat. Struct. Mol. Biol. 2005, 12, 469-470.
67. Grey, F.; Nelson, J. Identification and function of human cytomegalovirus microRNAs. J. Clin. Virol. 2008, 41, 186-191.
68. Boss, I.W.; Plaisance, K.B.; Renne, R. Role of virus-encoded microRNAs in herpesvirus biology. Trends Microbiol. 2009, 17, 544-553.
69. Murphy, E.; Vanicek, J.; Robins, H.; Shenk, T.; Levine, A.J. Suppression of immediate-early viral gene expression by herpesvirus-coded microRNAs: implications for latency. Proc. Natl. Acad. Sci. USA 2008, 105, 5453-5458.