1887

Abstract

Bovine herpesvirus type 5 (BoHV-5) and bovine herpesvirus 1 (BoHV-1) are two closely related viruses. However, BoHV-5 is responsible for fatal meningitis in calves, while BoHV-1 is associated with infectious rhinotracheitis in cattle, and the mechanism by which the two viruses cause different symptoms is not well understood. In this study, we identified 11 microRNA (miRNA) genes, encoded by the BoHV-5 genome, that were processed into 16 detectable mature miRNAs in productive infection as determined by deep sequencing. We found that 6 out of 16 miRNA genes were present as two copies in the internal repeat and terminal repeat regions, resulting in a total of 17 miRNA-encoding loci distributed in both DNA strands. Surprisingly, BoHV-5 shared only one conservative miRNA with BoHV-1, which was located upstream of the origin of replication. Furthermore, in contrast to BoHV-1, no miRNAs were detected in the unique short region and locus within or near the bovine infected-cell protein 0 and latency-related genes. Variations in both the 5′ and 3′ ends of the reference sequence were observed, resulting in more than one isoform for each miRNA. All of the 16 miRNAs were detectable by stem–loop reverse transcriptase-PCR. The miRNAs with high read numbers were subjected to Northern blot analysis, and all pre-miRNAs and one mature miRNA were detected. Collectively, the data suggest that BoHV-5 encodes a different pattern of miRNAs, which may regulate the life cycle of BoHV-5 and might account for the different pathogenesis of this virus compared with BoHV-1.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.061093-0
2014-03-01
2021-10-17
Loading full text...

Full text loading...

/deliver/fulltext/jgv/95/3/671.html?itemId=/content/journal/jgv/10.1099/vir.0.061093-0&mimeType=html&fmt=ahah

References

  1. Anziliero D., Santos C. M., Brum M. C., Weiblen R., Chowdhury S. I., Flores E. F. 2011; A recombinant bovine herpesvirus 5 defective in thymidine kinase and glycoprotein E is immunogenic for calves and confers protection upon homologous challenge and BoHV-1 challenge. Vet Microbiol 154:14–22 [View Article][PubMed]
    [Google Scholar]
  2. Barenfus M., Delliquadri C. A., McIntyre R. W., Schroeder R. J. 1963; Isolation of infectious bovine rhinotracheitis virus from calves with meningoencephalitis. J Am Vet Med Assoc 143:725–728[PubMed]
    [Google Scholar]
  3. Bartel D. P. 2004; MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297 [View Article][PubMed]
    [Google Scholar]
  4. Bartel D. P. 2009; MicroRNAs: target recognition and regulatory functions. Cell 136:215–233 [View Article][PubMed]
    [Google Scholar]
  5. Barth S., Pfuhl T., Mamiani A., Ehses C., Roemer K., Kremmer E., Jäker C., Höck J., Meister G., Grässer F. A. 2008; Epstein-Barr virus-encoded microRNA miR-BART2 down-regulates the viral DNA polymerase BALF5. Nucleic Acids Res 36:666–675 [View Article][PubMed]
    [Google Scholar]
  6. Bartha A., Hajdu G., Aldásy P., Paczolay G. 1969; Occurrence of encephalitis caused by infectious bovine rhinotracheitis virus in calves in hungary. Acta Vet Acad Sci Hung 19:145–151[PubMed]
    [Google Scholar]
  7. Belknap E. B., Collins J. K., Ayers V. K., Schultheiss P. C. 1994; Experimental infection of neonatal calves with neurovirulent bovine herpesvirus type 1.3. Vet Pathol 31:358–365 [View Article][PubMed]
    [Google Scholar]
  8. Cardoso T. C., Silva-Frade C., Táparo C. V., Okamura L. H., Flores E. F. 2013; Validation of a reference control for an SYBR-Green fluorescence assay-based real-time PCR for detection of bovine herpesvirus 5 in experimentally exposed bovine embryos. Mol Cell Probes 27:237–242 [View Article][PubMed]
    [Google Scholar]
  9. Carrillo B. J., Ambrogí A., Schudel A. A., Vazquez M., Dahme E., Pospischil A. 1983; Meningoencephalitis caused by IBR virus in calves in Argentina. Zentralbl Veterinarmed B 30:327–332 [View Article][PubMed]
    [Google Scholar]
  10. Chowdhury S. I., Lee B. J., Mosier D., Sur J. H., Osorio F. A., Kennedy G., Weiss M. L. 1997; Neuropathology of bovine herpesvirus type 5 (BHV-5) meningo-encephalitis in a rabbit seizure model. J Comp Pathol 117:295–310 [View Article][PubMed]
    [Google Scholar]
  11. Chowdhury S. I., Lee B. J., Ozkul A., Weiss M. L. 2000; Bovine herpesvirus 5 glycoprotein E is important for neuroinvasiveness and neurovirulence in the olfactory pathway of the rabbit. J Virol 74:2094–2106 [View Article][PubMed]
    [Google Scholar]
  12. Cui C., Griffiths A., Li G., Silva L. M., Kramer M. F., Gaasterland T., Wang X. J., Coen D. M. 2006; Prediction and identification of herpes simplex virus 1-encoded microRNAs. J Virol 80:5499–5508 [View Article][PubMed]
    [Google Scholar]
  13. d’Offay J. M., Fulton R. W., Eberle R. 2013; Complete genome sequence of the NVSL BoHV-1.1 Cooper reference strain. Arch Virol 158:1109–1113 [View Article][PubMed]
    [Google Scholar]
  14. Del Médico Zajac M. P., Puntel M., Zamorano P. I., Sadir A. M., Romera S. A. 2006; BHV-1 vaccine induces cross-protection against BHV-5 disease in cattle. Res Vet Sci 81:327–334 [View Article][PubMed]
    [Google Scholar]
  15. Del Médico Zajac M. P., Ladelfa M. F., Kotsias F., Muylkens B., Thiry J., Thiry E., Romera S. A. 2010; Biology of bovine herpesvirus 5. Vet J 184:138–145 [View Article][PubMed]
    [Google Scholar]
  16. 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 [View Article][PubMed]
    [Google Scholar]
  17. French E. L. 1962; A specific virus encephalitis in calves: isolation and characterization of the causal agent. Aust Vet J 38:216–221 [View Article]
    [Google Scholar]
  18. Glazov E. A., Horwood P. F., Assavalapsakul W., Kongsuwan K., Mitchell R. W., Mitter N., Mahony T. J. 2010; Characterization of microRNAs encoded by the bovine herpesvirus 1 genome. J Gen Virol 91:32–41 [View Article][PubMed]
    [Google Scholar]
  19. Jaber T., Workman A., Jones C. 2010; Small noncoding RNAs encoded within the bovine herpesvirus 1 latency-related gene can reduce steady-state levels of infected cell protein 0 (bICP0). J Virol 84:6297–6307 [View Article][PubMed]
    [Google Scholar]
  20. Jones L., Hamilton A. J., Voinnet O., Thomas C. L., Maule A. J., Baulcombe D. C. 1999; RNA–DNA interactions and DNA methylation in post-transcriptional gene silencing. Plant Cell 11:2291–2301[PubMed] [CrossRef]
    [Google Scholar]
  21. Jurak I., Griffiths A., Coen D. M. 2011; Mammalian alphaherpesvirus miRNAs. Biochim Biophys Acta 1809:641–653 [View Article][PubMed]
    [Google Scholar]
  22. Kim Y. K., Heo I., Kim V. N. 2010; Modifications of small RNAs and their associated proteins. Cell 143:703–709 [View Article][PubMed]
    [Google Scholar]
  23. Lee R. C., Feinbaum R. L., Ambros V. 1993; The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75:843–854 [View Article][PubMed]
    [Google Scholar]
  24. Lee B. J., Weiss M. L., Mosier D., Chowdhury S. I. 1999; Spread of bovine herpesvirus type 5 (BHV-5) in the rabbit brain after intranasal inoculation. J Neurovirol 5:474–484 [View Article][PubMed]
    [Google Scholar]
  25. Mahony T. J. 2010; Bovine herpesvirus: what is missing from our understanding of the relationship between BoHV-1 and BoHV-5?. Vet J 184:124–125 [View Article][PubMed]
    [Google Scholar]
  26. Maidana S. S., Ladelfa M. F., Pérez S. E., Lomónaco P. M., Del Médico Zajac M. P., Odeón A., Blanco Viera J., Combessies G., Fondevila N. other authors 2011; Characterization of BoHV-5 field strains circulation and report of transient specific subtype of bovine herpesvirus 5 in Argentina. BMC Vet Res 7:8 [View Article][PubMed]
    [Google Scholar]
  27. Meyer G., Lemaire M., Ros C., Belak K., Gabriel A., Cassart D., Coignoul F., Belak S., Thiry E. 2001; Comparative pathogenesis of acute and latent infections of calves with bovine herpesvirus types 1 and 5. Arch Virol 146:633–652 [View Article][PubMed]
    [Google Scholar]
  28. Morin R. D., O’Connor M. D., Griffith M., Kuchenbauer F., Delaney A., Prabhu A. L., Zhao Y., McDonald H., Zeng T. other authors 2008; Application of massively parallel sequencing to microRNA profiling and discovery in human embryonic stem cells. Genome Res 18:610–621 [View Article][PubMed]
    [Google Scholar]
  29. Pasquinelli A. E., Reinhart B. J., Slack F., Martindale M. Q., Kuroda M. I., Maller B., Hayward D. C., Ball E. E., Degnan B. other authors 2000; Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA. Nature 408:86–89 [View Article][PubMed]
    [Google Scholar]
  30. Pfeffer S., Zavolan M., Grässer 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 [View Article][PubMed]
    [Google Scholar]
  31. Pfeffer S., Sewer A., Lagos-Quintana M., Sheridan R., Sander C., Grässer F. A., van Dyk L. F., Ho C. K., Shuman S. other authors 2005; Identification of microRNAs of the herpesvirus family. Nat Methods 2:269–276 [View Article][PubMed]
    [Google Scholar]
  32. Rodríguez M., Barrera M., Sánchez O., Rodríguez E. C., Martínez N., Parra N. C., Toledo J. R. 2012; First report of bovine herpesvirus 5 in bull semen. Arch Virol 157:1775–1778 [View Article][PubMed]
    [Google Scholar]
  33. Roizmann B., Desrosiers R. C., Fleckenstein B., Lopez C., Minson A. C., Studdert M. J. The Herpesvirus Study Group of the International Committee on Taxonomy of Viruses 1992; The family Herpesviridae: an update. Arch Virol 123:425–449 [View Article][PubMed]
    [Google Scholar]
  34. Tang S., Bertke A. S., Patel A., Wang K., Cohen J. I., Krause P. R. 2008; An acutely and latently expressed herpes simplex virus 2 viral microRNA inhibits expression of ICP34.5, a viral neurovirulence factor. Proc Natl Acad Sci U S A 105:10931–10936 [View Article][PubMed]
    [Google Scholar]
  35. 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[PubMed]
    [Google Scholar]
  36. Varkonyi-Gasic E., Hellens R. P. 2011; Quantitative stem-loop RT-PCR for detection of microRNAs. Methods Mol Biol 744:145–157 [View Article][PubMed]
    [Google Scholar]
  37. Vogel F. S., Caron L., Flores E. F., Weiblen R., Winkelmann E. R., Mayer S. V., Bastos R. G. 2003; Distribution of bovine herpesvirus type 5 DNA in the central nervous systems of latently, experimentally infected calves. J Clin Microbiol 41:4512–4520 [View Article][PubMed]
    [Google Scholar]
  38. Wu Y. Q., Chen D. J., He H. B., Chen D. S., Chen L. L., Chen H. C., Liu Z. F. 2012; Pseudorabies virus infected porcine epithelial cell line generates a diverse set of host microRNAs and a special cluster of viral microRNAs. PLoS ONE 7:e30988 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.061093-0
Loading
/content/journal/jgv/10.1099/vir.0.061093-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited this month Most Cited RSS feed

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