1887

Abstract

The genus of the subfamily includes viruses that infect lymphoid cells of domestic and wild ruminants and swine, causing asymptomatic latent infections in reservoir hosts. Here, we describe the genome of bovine herpesvirus 6 (BoHV-6), a macavirus ubiquitous in healthy cattle populations. The BoHV-6 genome exhibited architecture conserved in macaviruses, including a repetitive H-DNA region and unique 141 kbp L-DNA region predicted to encode 77 genes. BoHV-6 encoded, in variable genomic regions, a novel complement of genes relative to other characterized macaviruses, probably contributing to distinctive aspects of BoHV-6 infection biology and host range. Most notably, BoHV-6 encoded the first herpesviral protein (Bov2.b2) similar to cellular ornithine decarboxylase, an enzyme that catalyses the first and rate-limiting step in the biosynthesis of polyamines. Bov2.b2 conceivably mediates a novel mechanism by which BoHV-6 promotes cell-cycle-dependent viral replication.

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2014-08-01
2024-04-28
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References

  1. Ackermann M. 2006; Pathogenesis of gammaherpesvirus infections. Vet Microbiol 113:211–222 [View Article][PubMed]
    [Google Scholar]
  2. Albrecht J.-C., Nicholas J., Biller D., Cameron K. R., Biesinger B., Newman C., Wittmann S., Craxton M. A., Coleman H.other authors 1992; Primary structure of the herpesvirus saimiri genome. J Virol 66:5047–5058[PubMed]
    [Google Scholar]
  3. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. 1990; Basic local alignment search tool. J Mol Biol 215:403–410 [View Article][PubMed]
    [Google Scholar]
  4. Auvinen M., Paasinen A., Andersson L. C., Hölttä E. 1992; Ornithine decarboxylase activity is critical for cell transformation. Nature 360:355–358 [View Article][PubMed]
    [Google Scholar]
  5. Banks M., Ibata G., Murphy A. M., Frossard J. P., Crawshaw T. R., Twomey D. F. 2008; Bovine lymphotropic herpesvirus and non-responsive post-partum metritis in dairy herds in the UK. Vet J 176:248–250 [View Article][PubMed]
    [Google Scholar]
  6. Bello-Fernandez C., Packham G., Cleveland J. L. 1993; The ornithine decarboxylase gene is a transcriptional target of c-Myc. Proc Natl Acad Sci U S A 90:7804–7808 [View Article][PubMed]
    [Google Scholar]
  7. Bellows D. S., Howell M., Pearson C., Hazlewood S. A., Hardwick J. M. 2002; Epstein-Barr virus BALF1 is a BCL-2-like antagonist of the herpesvirus antiapoptotic BCL-2 proteins. J Virol 76:2469–2479 [View Article][PubMed]
    [Google Scholar]
  8. Besemer J., Lomsadze A., Borodovsky M. 2001; GeneMarkS: a self-training method for prediction of gene starts in microbial genomes. Implications for finding sequence motifs in regulatory regions. Nucleic Acids Res 29:2607–2618 [View Article][PubMed]
    [Google Scholar]
  9. Betley J. N., Frith M. C., Graber J. H., Choo S., Deshler J. O. 2002; A ubiquitous and conserved signal for RNA localization in chordates. Curr Biol 12:1756–1761 [View Article][PubMed]
    [Google Scholar]
  10. Boisvert S., Laviolette F., Corbeil J. 2010; Ray: simultaneous assembly of reads from a mix of high-throughput sequencing technologies. J Comput Biol 17:1519–1533 [View Article][PubMed]
    [Google Scholar]
  11. Castresana J. 2000; Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552 [View Article][PubMed]
    [Google Scholar]
  12. Chmielewicz B., Goltz M., Ehlers B. 2001; Detection and multigenic characterization of a novel gammaherpesvirus in goats. Virus Res 75:87–94 [View Article][PubMed]
    [Google Scholar]
  13. Chmielewicz B., Goltz M., Franz T., Bauer C., Brema S., Ellerbrok H., Beckmann S., Rziha H.-J., Lahrmann K.-H.other authors 2003; A novel porcine gammaherpesvirus. Virology 308:317–329 [View Article][PubMed]
    [Google Scholar]
  14. Cobb S. P., Banks M., Russell C., Thorne M. 2006; Bovine lymphotrophic herpesvirus in a UK dairy herd. Vet Rec 158:807–808 [View Article][PubMed]
    [Google Scholar]
  15. Coffino P. 2001; Antizyme, a mediator of ubiquitin-independent proteasomal degradation. Biochimie 83:319–323 [View Article][PubMed]
    [Google Scholar]
  16. Cohen S. S. 1998 A Guide to the Polyamines New York: Oxford University Press;
    [Google Scholar]
  17. Collins J. K., Bruns C., Vermedahl T. L., Schiebel A. L., Jessen M. T., Schultheiss P. C., Anderson G. M., Dinsmore R. P., Callan R. J., DeMartini J. C. 2000; Malignant catarrhal fever: polymerase chain reaction survey for ovine herpesvirus 2 and other persistent herpesvirus and retrovirus infections of dairy cattle and bison. J Vet Diagn Invest 12:406–411 [View Article][PubMed]
    [Google Scholar]
  18. Ehlers B., Lowden S. 2004; Novel herpesviruses of Suidae: indicators for a second genogroup of artiodactyl gammaherpesviruses. J Gen Virol 85:857–862 [View Article][PubMed]
    [Google Scholar]
  19. Ehlers B., Ulrich S., Goltz M. 1999; Detection of two novel porcine herpesviruses with high similarity to gammaherpesviruses. J Gen Virol 80:971–978[PubMed]
    [Google Scholar]
  20. Ensser A., Pflanz R., Fleckenstein B. 1997; Primary structure of the alcelaphine herpesvirus 1 genome. J Virol 71:6517–6525[PubMed]
    [Google Scholar]
  21. Fischer M. G., Allen M. J., Wilson W. H., Suttle C. A. 2010; Giant virus with a remarkable complement of genes infects marine zooplankton. Proc Natl Acad Sci U S A 107:19508–19513 [View Article][PubMed]
    [Google Scholar]
  22. Gagnon C. A., Allam O., Drolet R., Tremblay D. 2010; Quebec: detection of bovine lymphotropic herpesvirus DNA in tissues of a bovine aborted fetus. Can Vet J 51:1021–1022[PubMed]
    [Google Scholar]
  23. Garigliany M.-M., Bayrou C., Cassart D., Jolly S., Desmecht D. 2013; Bovine lymphotropic herpesvirus detected in Belgium. Vet Rec 172:535–536 [View Article][PubMed]
    [Google Scholar]
  24. Gerner E. W., Meyskens F. L. Jr 2004; Polyamines and cancer: old molecules, new understanding. Nat Rev Cancer 4:781–792 [View Article][PubMed]
    [Google Scholar]
  25. Gesser B., Leffers H., Jinquan T., Vestergaard C., Kirstein N., Sindet-Pedersen S., Jensen S. L., Thestrup-Pedersen K., Larsen C. G. 1997; Identification of functional domains on human interleukin 10. Proc Natl Acad Sci U S A 94:14620–14625 [View Article][PubMed]
    [Google Scholar]
  26. Ghoda L., van Daalen Wetters T., Macrae M., Ascherman D., Coffino P. 1989; Prevention of rapid intracellular degradation of ODC by a carboxyl-terminal truncation. Science 243:1493–1495 [View Article][PubMed]
    [Google Scholar]
  27. Ghoda L., Sidney D., Macrae M., Coffino P. 1992; Structural elements of ornithine decarboxylase required for intracellular degradation and polyamine-dependent regulation. Mol Cell Biol 12:2178–2185[PubMed]
    [Google Scholar]
  28. Goltz M., Ericsson T., Patience C., Huang C. A., Noack S., Sachs D. H., Ehlers B. 2002; Sequence analysis of the genome of porcine lymphotropic herpesvirus 1 and gene expression during posttransplant lymphoproliferative disease of pigs. Virology 294:383–393 [View Article][PubMed]
    [Google Scholar]
  29. Gordon D., Green P. 2013; Consed: a graphical editor for next-generation sequencing. Bioinformatics 29:2936–2937 [View Article][PubMed]
    [Google Scholar]
  30. Guindon S., Gascuel O. 2003; A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704 [View Article][PubMed]
    [Google Scholar]
  31. Hart J., Ackermann M., Jayawardane G., Russell G., Haig D. M., Reid H., Stewart J. P. 2007; Complete sequence and analysis of the ovine herpesvirus 2 genome. J Gen Virol 88:28–39 [View Article][PubMed]
    [Google Scholar]
  32. Ivanov I. P., Firth A. E., Atkins J. F. 2010; Recurrent emergence of catalytically inactive ornithine decarboxylase homologous forms that likely have regulatory function. J Mol Evol 70:289–302 [View Article][PubMed]
    [Google Scholar]
  33. Katoh K., Misawa K., Kuma K., Miyata T. 2002; mafft: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30:3059–3066 [View Article][PubMed]
    [Google Scholar]
  34. Kubiś P., Materniak M., Kuźmak J. 2013; Comparison of nested PCR and qPCR for the detection and quantitation of BoHV6 DNA. J Virol Methods 194:94–101 [View Article][PubMed]
    [Google Scholar]
  35. Li X., Coffino P. 1992; Regulated degradation of ornithine decarboxylase requires interaction with the polyamine-inducible protein antizyme. Mol Cell Biol 12:3556–3562[PubMed]
    [Google Scholar]
  36. Li H., Gailbreath K., Flach E. J., Taus N. S., Cooley J., Keller J., Russell G. C., Knowles D. P., Haig D. M.other authors 2005; A novel subgroup of rhadinoviruses in ruminants. J Gen Virol 86:3021–3026 [View Article][PubMed]
    [Google Scholar]
  37. Lu Z., Li Y., Que Q., Kutish G. F., Rock D. L., Van Etten J. L. 1996; Analysis of 94 kb of the chlorella virus PBCV-1 330-kb genome: map positions 88 to 182. Virology 216:102–123 [View Article][PubMed]
    [Google Scholar]
  38. Machiels B., Lété C., de Fays K., Mast J., Dewals B., Stevenson P. G., Vanderplasschen A., Gillet L. 2011; The bovine herpesvirus 4 Bo10 gene encodes a nonessential viral envelope protein that regulates viral tropism through both positive and negative effects. J Virol 85:1011–1024 [View Article][PubMed]
    [Google Scholar]
  39. Machiels B., Stevenson P. G., Vanderplasschen A., Gillet L. 2013; A gammaherpesvirus uses alternative splicing to regulate its tropism and its sensitivity to neutralization. PLoS Pathog 9:e1003753 [View Article][PubMed]
    [Google Scholar]
  40. Macrae M., Coffino P. 1987; Complementation of a polyamine-deficient Escherichia coli mutant by expression of mouse ornithine decarboxylase. Mol Cell Biol 7:564–567[PubMed]
    [Google Scholar]
  41. Morehead T. A., Gurnon J. R., Adams B., Nickerson K. W., Fitzgerald L. A., Van Etten J. L. 2002; Ornithine decarboxylase encoded by chlorella virus PBCV-1. Virology 301:165–175 [View Article][PubMed]
    [Google Scholar]
  42. Nilsson J. A., Maclean K. H., Keller U. B., Pendeville H., Baudino T. A., Cleveland J. L. 2004; Mnt loss triggers Myc transcription targets, proliferation, apoptosis, and transformation. Mol Cell Biol 24:1560–1569 [View Article][PubMed]
    [Google Scholar]
  43. O’Toole D., Li H. 2014; The pathology of malignant catarrhal fever, with an emphasis on ovine herpesvirus 2. Vet Pathol 51:437–452 [View Article][PubMed]
    [Google Scholar]
  44. Osorio F. A., Reed D. E., Van der Maaten M. J., Metz C. A. 1985; Comparison of the herpesviruses of cattle by DNA restriction endonuclease analysis and serologic analysis. Am J Vet Res 46:2104–2109[PubMed]
    [Google Scholar]
  45. Paulsen S. J., Rosenkilde M. M., Eugen-Olsen J., Kledal T. N. 2005; Epstein-Barr virus-encoded BILF1 is a constitutively active G protein-coupled receptor. J Virol 79:536–546 [View Article][PubMed]
    [Google Scholar]
  46. Pearson W. R., Lipman D. J. 1988; Improved tools for biological sequence comparison. Proc Natl Acad Sci U S A 85:2444–2448 [View Article][PubMed]
    [Google Scholar]
  47. Pegg A. E. 2006; Regulation of ornithine decarboxylase. J Biol Chem 281:14529–14532 [View Article][PubMed]
    [Google Scholar]
  48. Rice P., Longden I., Bleasby A. 2000; emboss: the European molecular biology open software suite. Trends Genet 16:276–277 [View Article][PubMed]
    [Google Scholar]
  49. Rovnak J., Quackenbush S. L., Reyes R. A., Baines J. D., Parrish C. R., Casey J. W. 1998; Detection of a novel bovine lymphotropic herpesvirus. J Virol 72:4237–4242[PubMed]
    [Google Scholar]
  50. Russell G. C., Stewart J. P., Haig D. M. 2009; Malignant catarrhal fever: a review. Vet J 179:324–335 [View Article][PubMed]
    [Google Scholar]
  51. Shah R., Coleman C. S., Mir K., Baldwin J., Van Etten J. L., Grishin N. V., Pegg A. E., Stanley B. A., Phillips M. A. 2004; Paramecium bursaria chlorella virus-1 encodes an unusual arginine decarboxylase that is a close homolog of eukaryotic ornithine decarboxylases. J Biol Chem 279:35760–35767 [View Article][PubMed]
    [Google Scholar]
  52. Van der Maaten M. J., Boothe A. D. 1972; Isolation of a herpes-like virus from lymphosarcomatous cattle. Arch Gesamte Virusforsch 37:85–96 [View Article][PubMed]
    [Google Scholar]
  53. Wang M., Marín A. 2006; Characterization and prediction of alternative splice sites. Gene 366:219–227 [View Article][PubMed]
    [Google Scholar]
  54. Zhao G., Droit L., Tesh R. B., Popov V. L., Little N. S., Upton C., Virgin H. W., Wang D. 2011; The genome of Yoka poxvirus. J Virol 85:10230–10238 [View Article][PubMed]
    [Google Scholar]
  55. Zuo J., Currin A., Griffin B. D., Shannon-Lowe C., Thomas W. A., Ressing M. E., Wiertz E. J. H. J., Rowe M. 2009; The Epstein-Barr virus G-protein-coupled receptor contributes to immune evasion by targeting MHC class I molecules for degradation. PLoS Pathog 5:e1000255 [View Article][PubMed]
    [Google Scholar]
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