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Abstract

Bovine herpesvirus 1 (BoHV-1) is a ubiquitous and important pathogen of cattle worldwide. This study reports the identification of 10 microRNA (miRNA) genes, Bhv1-mir-B1–Bhv1-mir-B10, encoded by the BoHV-1 genome that were processed into 12 detectable mature miRNAs as determined by ultra-high throughput sequencing bioinformatics analyses of small RNA libraries and expression studies. We found that four of the miRNA genes were present as two copies in the BoHV-1 genome, resulting in a total of 14 miRNA encoding loci. Unique features of the BoHV-1 miRNAs include evidence of bidirectional transcription and a close association of two miRNA genes with the origin of replication, including one miRNA that is encoded within the origin of replication. The miRNA gene Bhv1-mir-B5 was encoded on the opposite DNA strand to the latency associated transcript, potentially giving rise to antisense transcripts originating from this locus. The association of herpesvirus miRNAs with latency appears to be a common feature in the alphaherpesviruses. Analyses of the BoHV-5 genome for putative miRNA gene orthologues identified a high degree of evolutionary conservation for nine of the BoHV-1 miRNA genes. The possible roles for BoHV-1 miRNAs in the regulation of known BoHV-1 transcription units and the genetics of the BoHV-1 genotypes are also discussed.

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2010-01-01
2024-03-28
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References

  1. Ambros, V., Bartel, B., Bartel, D. P., Burge, C. B., Carrington, J. C., Chen, X., Dreyfuss, G., Eddy, S. R., Griffiths-Jones, S. & other authors(2003). A uniform system for microRNA annotation. RNA 9, 277–279.[CrossRef] [Google Scholar]
  2. Buck, A. H., Santoyo-Lopez, J., Robertson, K. A., Kumar, D. S., Reczko, M. & Ghazal, P.(2007). Discrete clusters of virus-encoded microRNAs are associated with complementary strands of the genome and the 7.2-kilobase stable intron in murine cytomegalovirus. J Virol 81, 13761–13770.[CrossRef] [Google Scholar]
  3. Bushati, N. & Cohen, S. M.(2007). MicroRNA functions. Annu Rev Cell Dev Biol 23, 175–205.[CrossRef] [Google Scholar]
  4. Darty, K., Denise, A. & Ponty, Y.(2009). VARNA: interactive drawing and editing of the RNA secondary structure. Bioinformatics 25, 1974–1975.[CrossRef] [Google Scholar]
  5. Delhon, G., Moraes, M. P., Lu, Z., Afonso, C. L., Flores, E. F., Weiblen, R., Kutish, G. F. & Rock, D. L.(2003). Genome of bovine herpesvirus 5. J Virol 77, 10339–10347.[CrossRef] [Google Scholar]
  6. Engels, M., Steck, F. & Wyler, R.(1981). Comparison of the genomes of infectious bovine rhinotracheitis and infectious pustular vulvovaginitis virus strains by restriction endonuclease analysis. Arch Virol 67, 169–174.[CrossRef] [Google Scholar]
  7. Esteves, P. A., Dellagostin, O. A., Pinto, L. S., Silva, A. D., Spilki, F. R., Ciacci-Zanella, J. R., Hubner, S. O., Puentes, R., Maisonnave, J. & other authors(2008). Phylogenetic comparison of the carboxy-terminal region of glycoprotein C (gC) of bovine herpesviruses (BoHV) 1.1, 1.2 and 5 from South America (SA). Virus Res 131, 16–22.[CrossRef] [Google Scholar]
  8. Ghosh, Z., Mallick, B. & Chakrabarti, J.(2009). Cellular versus viral microRNAs in host-virus interaction. Nucleic Acids Res 37, 1035–1048. [Google Scholar]
  9. 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] [Google Scholar]
  10. Glazov, E. A., Kongsuwan, K., Assavalapsakul, W., Horwood, P. F., Mitter, N. & Mahony, T. J.(2009). Repertoire of bovine miRNA and miRNA-like small regulatory RNAs expressed upon viral infection. PLoS One 4, e6349[CrossRef] [Google Scholar]
  11. Grey, F. & Nelson, J.(2008). Identification and function of human cytomegalovirus microRNAs. J Clin Virol 41, 186–191.[CrossRef] [Google Scholar]
  12. Grey, F., Meyers, H., White, E. A., Spector, D. H. & Nelson, J.(2007). A human cytomegalovirus-encoded microRNA regulates expression of multiple viral genes involved in replication. PLoS Pathog 3, e163[CrossRef] [Google Scholar]
  13. Griffiths-Jones, S., Grocock, R. J., van Dongen, S., Bateman, A. & Enright, A. J.(2006). miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res 34, D140–D144.[CrossRef] [Google Scholar]
  14. He, S., Yang, Z., Skogerbo, G., Ren, F., Cui, H., Zhao, H., Chen, R. & Zhao, Y.(2008). The properties and functions of virus encoded microRNA, siRNA, and other small noncoding RNAs. Crit Rev Microbiol 34, 175–188.[CrossRef] [Google Scholar]
  15. Hofacker, I. L.(2003). Vienna RNA secondary structure server. Nucleic Acids Res 31, 3429–3431.[CrossRef] [Google Scholar]
  16. Isler, J. A. & Schaffer, P. A.(2001). Origin binding protein-containing protein-DNA complex formation at herpes simplex virus type 1 oriS: role in oriS-dependent DNA replication. J Virol 75, 6808–6816.[CrossRef] [Google Scholar]
  17. Jones, C., Geiser, V., Henderson, G., Jiang, Y., Meyer, F., Perez, S. & Zhang, Y.(2006). Functional analysis of bovine herpesvirus 1 (BHV-1) genes expressed during latency. Vet Microbiol 113, 199–210.[CrossRef] [Google Scholar]
  18. Kent, W. J.(2002). BLAT – the blast-like alignment tool. Genome Res 12, 656–664.[CrossRef] [Google Scholar]
  19. Linsen, S. E. V., de Wit, E., Janssens, G., Heater, S., Chapman, L., Parkin, R. K., Fritz, B., Wyman, S. K., de Bruijn, E. & other authors(2009). Limitations and possibilities of small RNA digital gene expression profiling. Nat Methods 6, 474–476.[CrossRef] [Google Scholar]
  20. Livak, K. J. & Schmittgen, T. D.(2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔ C t method. Methods 25, 402–408.[CrossRef] [Google Scholar]
  21. Lodish, H. F., Zhou, B., Liu, G. & Chen, C. Z.(2008). Micromanagement of the immune system by microRNAs. Nat Rev Immunol 8, 120–130.[CrossRef] [Google Scholar]
  22. Lu, F., Weidmer, A., Liu, C. G., Volinia, S., Croce, C. M. & Lieberman, P. M.(2008). Epstein-Barr virus-induced miR-155 attenuates NF-κB signaling and stabilizes latent virus persistence. J Virol 82, 10436–10443.[CrossRef] [Google Scholar]
  23. Madin, S. H. & Darby, N. B., Jr(1958). Established kidney cell lines of normal adult bovine and ovine origin. Proc Soc Exp Biol Med 98, 574–576.[CrossRef] [Google Scholar]
  24. Mahony, T. J., McCarthy, F. M., Gravel, J. L., West, L. & Young, P. L.(2002). Construction and manipulation of an infectious clone of the bovine herpesvirus 1 genome maintained as a bacterial artificial chromosome. J Virol 76, 6660–6668.[CrossRef] [Google Scholar]
  25. Metzler, A. E., Matile, H., Gassmann, U., Engels, M. & Wyler, R.(1985). European isolates of bovine herpesvirus 1: a comparison of restriction endonuclease sites, polypeptides, and reactivity with monoclonal antibodies. Arch Virol 85, 57–69.[CrossRef] [Google Scholar]
  26. Mitter, N., Sulistyowati, E. & Dietzgen, R. G.(2003). Cucumber mosaic virus infection transiently breaks dsRNA-induced transgenic immunity to Potato virus Y in tobacco. Mol Plant Microbe Interact 16, 936–944.[CrossRef] [Google Scholar]
  27. Morgan, R., Anderson, A., Bernberg, E., Kamboj, S., Huang, E., Lagasse, G., Isaacs, G., Parcells, M., Meyers, B. C. & other authors(2008). Sequence conservation and differential expression of Marek's disease virus microRNAs. J Virol 82, 12213–12220.[CrossRef] [Google Scholar]
  28. Murphy, E., Vanicek, J., Robins, H., Shenk, T. & Levine, A. J.(2008). Suppression of immediate-early viral gene expression by herpesvirus-coded microRNAs: implications for latency. Proc Natl Acad Sci U S A 105, 5453–5458.[CrossRef] [Google Scholar]
  29. Nadin-Davis, S. A., Lutze-Wallace, C. & Zhong, X.(1996). Bovine herpesvirus 1 isolates contain variable copy numbers of GC-rich tandem repeats in the gI non-coding regions of their genomes. Virus Genes 13, 263–268.[CrossRef] [Google Scholar]
  30. Nguyen-Huynh, A. T. & Schaffer, P. A.(1998). Cellular transcription factors enhance herpes simplex virus type 1 oriS-dependent DNA replication. J Virol 72, 3635–3645. [Google Scholar]
  31. Pfeffer, S., Zavolan, M., Grasser, F. A., Chien, M., Russo, J. J., Ju, J., John, B., Enright, A. J., Marks, D. & other authors(2004). Identification of virus-encoded microRNAs. Science 304, 734–736.[CrossRef] [Google Scholar]
  32. Rijsewijk, F. A., Kaashoek, M. J., Langeveld, J. P., Meloen, R., Judek, J., Bienkowska-Szewczyk, K., Maris-Veldhuis, M. A. & van Oirschot, J. T.(1999). Epitopes on glycoprotein C of bovine herpesvirus-1 (BHV-1) that allow differentiation between BHV-1.1 and BHV-1.2 strains. J Gen Virol 80, 1477–1483. [Google Scholar]
  33. Snowdon, W. A.(1964). Infectious bovine rhinotracheitis and infectious pustular vulvovaginitis in Australian cattle. Aust Vet J 40, 277–288.[CrossRef] [Google Scholar]
  34. Tang, S., Patel, A. & Krause, P. R.(2009). Novel less-abundant viral microRNAs encoded by herpes simplex virus 2 latency-associated transcript and their roles in regulating ICP34.5 and ICP0 mRNAs. J Virol 83, 1433–1442.[CrossRef] [Google Scholar]
  35. Umbach, J. L. & Cullen, B. R.(2009). The role of RNAi and microRNAs in animal virus replication and antiviral immunity. Genes Dev 23, 1151–1164.[CrossRef] [Google Scholar]
  36. Umbach, J. L., Kramer, M. F., Jurak, I., Karnowski, H. W., Coen, D. M. & Cullen, B. R.(2008). MicroRNAs expressed by herpes simplex virus 1 during latent infection regulate viral mRNAs. Nature 454, 780–783. [Google Scholar]
  37. Varkonyi-Gasic, E., Wu, R., Wood, M., Walton, E. F. & Hellens, R. P.(2007). Protocol: a highly sensitive RT-PCR method for detection and quantification of microRNAs. Plant Methods 3, 12[CrossRef] [Google Scholar]
  38. Waidner, L. A., Morgan, R. W., Anderson, A. S., Bernberg, E. L., Kamboj, S., Garcia, M., Riblet, S. M., Ouyang, M., Isaacs, G. K. & other authors(2009). MicroRNAs of Gallid and Meleagrid herpesviruses show generally conserved genomic locations and are virus-specific. Virology 388, 128–136.[CrossRef] [Google Scholar]
  39. Winter, J., Jung, S., Keller, S., Gregory, R. I. & Diederichs, S.(2009). Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat Cell Biol 11, 228–234.[CrossRef] [Google Scholar]
  40. Wirth, U. V., Fraefel, C., Vogt, B., Vlcek, C., Paces, V. & Schwyzer, M.(1992). Immediate-early RNA 2.9 and early RNA 2.6 of bovine herpesvirus 1 are 3′ coterminal and encode a putative zinc finger transactivator protein. J Virol 66, 2763–2772. [Google Scholar]
  41. Wong, S. W. & Schaffer, P. A.(1991). Elements in the transcriptional regulatory region flanking herpes simplex virus type 1 oriS stimulate origin function. J Virol 65, 2601–2611. [Google Scholar]
  42. Xu, H., Yao, Y., Zhao, Y., Smith, L. P., Baigent, S. J. & Nair, V.(2008). Analysis of the expression profiles of Marek's disease virus-encoded microRNAs by real-time quantitative PCR. J Virol Methods 149, 201–208.[CrossRef] [Google Scholar]
  43. Yao, Y., Zhao, Y., Xu, H., Smith, L. P., Lawrie, C. H., Watson, M. & Nair, V.(2008). MicroRNA profile of Marek's disease virus-transformed T-cell line MSB-1: predominance of virus-encoded microRNAs. J Virol 82, 4007–4015.[CrossRef] [Google Scholar]
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vol. , part 1, pp. 32 - 41

Predicted secondary structures for five putative miRNA genes

Oligonucleotides used in this study [Single PDF file](49 KB)



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