1887

Abstract

Equid herpesvirus 5 (EHV-5) is related to the human Epstein–Barr virus (human herpesvirus 4) and has frequently been observed in equine populations worldwide. EHV-5 was previously assumed to be low to non-pathogenic; however, studies have also related the virus to the severe lung disease equine multinodular pulmonary fibrosis (EMPF). Genetic information of EHV-5 is scanty: the whole genome was recently described and only limited nucleotide sequences are available. In this study, samples were taken twice 1 year apart from eight healthy horses at the same professional training yard and samples from a ninth horse that was diagnosed with EMPF with samples taken pre- and post-mortem to analyse partial glycoprotein B (gB) gene of EHV-5 by using next-generation sequencing. The analysis resulted in 27 partial gB gene sequences, 11 unique sequence types and five amino acid sequences. These sequences could be classified within four genotypes (I–IV) of the EHV-5 gB gene based on the degree of similarity of the nucleotide and amino acid sequences, and in this work horses were shown to be identified with up to three different genotypes simultaneously. The observations showed a range of interactions between EHV-5 and the host over time, where the same virus persists in some horses, whereas others have a more dynamic infection pattern including strains from different genotypes. This study provides insight into the genetic variation and dynamics of EHV-5, and highlights that further work is needed to understand the EHV-5 interaction with its host.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000332
2016-01-01
2020-01-19
Loading full text...

Full text loading...

/deliver/fulltext/jgv/97/1/169.html?itemId=/content/journal/jgv/10.1099/jgv.0.000332&mimeType=html&fmt=ahah

References

  1. Abdel-Hamid M., Chen J. J., Constantine N., Massoud M., Raab-Traub N.. 1992; EBV strain variation: geographical distribution and relation to disease state. Virology190:168–175 [CrossRef][PubMed]
    [Google Scholar]
  2. Achour A., Malet I., Le Gal F., Dehée A., Gautheret-Dejean A., Bonnafous P., Agut H.. 2008; Variability of gB and gH genes of human herpesvirus-6 among clinical specimens. J Med Virol80:1211–1221 [CrossRef][PubMed]
    [Google Scholar]
  3. Back H., Kendall A., Grandón R., Ullman K., Treiberg-Berndtsson L., Ståhl K., Pringle J.. 2012; Equine multinodular pulmonary fibrosis in association with asinine herpesvirus type 5 and equine herpesvirus type 5: a case report. Acta Vet Scand54:57 [CrossRef][PubMed]
    [Google Scholar]
  4. Back H., Ullman K., Treiberg Berndtsson L., Riihimäki M., Penell J., Ståhl K., Valarcher J.-F., Pringle J.. 2015; Viral load of equine herpesviruses 2 and 5 in nasal swabs of actively racing Standardbred trotters: temporal relationship of shedding to clinical findings and poor performance. Vet Microbiol179:142–148 [CrossRef][PubMed]
    [Google Scholar]
  5. Balfour H. H. Jr, Odumade O. A., Schmeling D. O., Mullan B. D., Ed J. A., Knight J. A., Vezina H. E., Thomas W., Hogquist K. A.. 2013; Behavioral, virologic, and immunologic factors associated with acquisition and severity of primary Epstein–Barr virus infection in university students. J Infect Dis207:80–88 [CrossRef][PubMed]
    [Google Scholar]
  6. Bell S. A., Balasuriya U. B. R., Gardner I. A., Barry P. A., Wilson W. D., Ferraro G. L., MacLachlan N. J.. 2006; Temporal detection of equine herpesvirus infections of a cohort of mares and their foals. Vet Microbiol116:249–257 [CrossRef][PubMed]
    [Google Scholar]
  7. Bolger A. M., Lohse M., Usadel B.. 2014; Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics30:2114–2120 [CrossRef][PubMed]
    [Google Scholar]
  8. Chantaraarphonkun S., Bhattarakosol P.. 2007; Intra- and intergenotypic variations among human cytomegalovirus gB genotypes. Intervirology50:78–84 [CrossRef][PubMed]
    [Google Scholar]
  9. Chesnokova L. S., Ahuja M. K., Hutt-Fletcher L. M.. 2014; Epstein-Barr virus glycoprotein gB and gHgL can mediate fusion and entry in trans, and heat can act as a partial surrogate for gHgL and trigger a conformational change in gB. J Virol88:12193–12201 [CrossRef][PubMed]
    [Google Scholar]
  10. Chou S. W., Dennison K. M.. 1991; Analysis of interstrain variation in cytomegalovirus glycoprotein B sequences encoding neutralization-related epitopes. J Infect Dis163:1229–1234 [CrossRef][PubMed]
    [Google Scholar]
  11. Coaquette A., Bourgeois A., Dirand C., Varin A., Chen W., Herbein G.. 2004; Mixed cytomegalovirus glycoprotein B genotypes in immunocompromised patients. Clin Infect Dis39:155–161 [CrossRef][PubMed]
    [Google Scholar]
  12. Dunowska M., Holloway S. A., Wilks C. R., Meers J.. 2000; Genomic variability of equine herpesvirus-5. Arch Virol145:1359–1371 [CrossRef][PubMed]
    [Google Scholar]
  13. Edgar R. C.. 2004; muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res32:1792–1797 [CrossRef][PubMed]
    [Google Scholar]
  14. Garcia N. J., Chen J., Longnecker R.. 2013; Modulation of Epstein-Barr virus glycoprotein B (gB) fusion activity by the gB cytoplasmic tail domain. MBio4:e00571-12 [CrossRef][PubMed]
    [Google Scholar]
  15. Hasegawa M., Kishino H., Yano T.. 1985; Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol22:160–174 [CrossRef][PubMed]
    [Google Scholar]
  16. Holloway S. A., Lindquester G. J., Studdert M. J., Drummer H. E.. 1999; Identification, sequence analysis and characterisation of equine herpesvirus 5 glycoprotein B. Arch Virol144:287–307 [CrossRef][PubMed]
    [Google Scholar]
  17. Humar A., Kumar D., Gilbert C., Boivin G.. 2003; Cytomegalovirus (CMV) glycoprotein B genotypes and response to antiviral therapy, in solid-organ-transplant recipients with CMV disease. J Infect Dis188:581–584 [CrossRef][PubMed]
    [Google Scholar]
  18. Jones D. T., Taylor W. R., Thornton J. M.. 1992; The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci8:275–282[PubMed]
    [Google Scholar]
  19. Kirchmeier M., Fluckiger A.-C., Soare C., Bozic J., Ontsouka B., Ahmed T., Diress A., Pereira L., Schödel F., other authors. 2014; Enveloped virus-like particle expression of human cytomegalovirus glycoprotein B antigen induces antibodies with potent and broad neutralizing activity. Clin Vaccine Immunol21:174–180 [CrossRef][PubMed]
    [Google Scholar]
  20. Kwok H., Wu C. W., Palser A. L., Kellam P., Sham P. C., Kwong D. L. W., Chiang A. K. S.. 2014; Genomic diversity of Epstein-Barr virus genomes isolated from primary nasopharyngeal carcinoma biopsy samples. J Virol88:10662–10672 [CrossRef][PubMed]
    [Google Scholar]
  21. Liu B., Yuan J., Yiu S.-M., Li Z., Xie Y., Chen Y., Shi Y., Zhang H., Li Y., other authors. 2012; cope: an accurate k-mer-based pair-end reads connection tool to facilitate genome assembly. Bioinformatics28:2870–2874 [CrossRef][PubMed]
    [Google Scholar]
  22. Marenzoni M. L., Coppola G., Maranesi M., Passamonti F., Cappelli K., Capomaccio S., Verini Supplizi A., Thiry E., Coletti M.. 2010; Age-dependent prevalence of equid herpesvirus 5 infection. Vet Res Commun34:703–708 [CrossRef][PubMed]
    [Google Scholar]
  23. Mechelli R., Manzari C., Policano C., Annese A., Picardi E., Umeton R., Fornasiero A., D'Erchia A. M., Buscarinu M. C., other authors. 2015; Epstein-Barr virus genetic variants are associated with multiple sclerosis. Neurology84:1362–1368 [CrossRef][PubMed]
    [Google Scholar]
  24. Mora A. L., Woods C. R., Garcia A., Xu J., Rojas M., Speck S. H., Roman J., Brigham K. L., Stecenko A. A.. 2005; Lung infection with gamma-herpesvirus induces progressive pulmonary fibrosis in Th2-biased mice. Am J Physiol Lung Cell Mol Physiol289:L711–L721 [CrossRef][PubMed]
    [Google Scholar]
  25. Neubauer A., Braun B., Brandmuller C., Kaaden O. R., Osterrieder N.. 1997; Analysis of the contributions of the equine herpesvirus 1 glycoprotein gB homolog to virus entry and direct cell-to-cell spread. Virology227:281–294 [CrossRef][PubMed]
    [Google Scholar]
  26. Palser A. L., Grayson N. E., White R. E., Corton C., Correia S., Ba Abdullah M. M., Watson S. J., Cotten M., Arrand J. R., other authors. 2015; Genome diversity of Epstein-Barr virus from multiple tumor types and normal infection. J Virol89:5222–5237 [CrossRef][PubMed]
    [Google Scholar]
  27. Parkin D. M.. 2006; The global health burden of infection-associated cancers in the year 2002. Int J Cancer118:3030–3044 [CrossRef][PubMed]
    [Google Scholar]
  28. Poth T., Niedermaier G., Hermanns W.. 2009; Equine multinodular pulmonary fibrosis in association with an EHV-5 infection in 5 horses. Wien Tierarztl Monatsschr96:203–208
    [Google Scholar]
  29. Rey F. A.. 2006; Molecular gymnastics at the herpesvirus surface. EMBO Rep7:1000–1005 [CrossRef][PubMed]
    [Google Scholar]
  30. 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 Virol123:425–449 [CrossRef][PubMed]
    [Google Scholar]
  31. Rushton J. O., Kolodziejek J., Tichy A., Nell B., Nowotny N.. 2013; Detection of equid herpesviruses 2 and 5 in a herd of 266 Lipizzaners in association with ocular findings. Vet Microbiol164:139–144 [CrossRef][PubMed]
    [Google Scholar]
  32. Ryckman B. J., Jarvis M. A., Drummond D. D., Nelson J. A., Johnson D. C.. 2006; Human cytomegalovirus entry into epithelial and endothelial cells depends on genes UL128 to UL150 and occurs by endocytosis and low-pH fusion. J Virol80:710–722 [CrossRef][PubMed]
    [Google Scholar]
  33. Sarcinella L., Mazzulli T., Willey B., Humar A.. 2002; Cytomegalovirus glycoprotein B genotype does not correlate with outcomes in liver transplant patients. J Clin Virol24:99–105 [CrossRef][PubMed]
    [Google Scholar]
  34. Sorem J., Longnecker R.. 2009; Cleavage of Epstein–Barr virus glycoprotein B is required for full function in cell–cell fusion with both epithelial and B cells. J Gen Virol90:591–595 [CrossRef][PubMed]
    [Google Scholar]
  35. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S.. 2011; mega5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol28:2731–2739 [CrossRef][PubMed]
    [Google Scholar]
  36. Tang Y. W., Johnson J. E., Browning P. J., Cruz-Gervis R. A., Davis A., Graham B. S., Brigham K. L., Oates J. A. Jr, Loyd J. E., Stecenko A. A.. 2003; Herpesvirus DNA is consistently detected in lungs of patients with idiopathic pulmonary fibrosis. J Clin Microbiol41:2633–2640 [CrossRef][PubMed]
    [Google Scholar]
  37. Telford E. A. R., Studdert M. J., Agius C. T., Watson M. S., Aird H. C., Davison A. J.. 1993; Equine herpesviruses 2 and 5 are gamma-herpesviruses. Virology195:492–499 [CrossRef][PubMed]
    [Google Scholar]
  38. Thorsteinsdóttir L., Torfason E. G., Torsteinsdóttir S., Svansson V.. 2010; Isolation and partial sequencing of Equid herpesvirus 5 from a horse in Iceland. J Vet Diagn Invest22:420–423 [CrossRef][PubMed]
    [Google Scholar]
  39. Torfason E. G., Thorsteinsdóttir L., Torsteinsdóttir S., Svansson V.. 2008; Study of equid herpesviruses 2 and 5 in Iceland with a type-specific polymerase chain reaction. Res Vet Sci85:605–611 [CrossRef][PubMed]
    [Google Scholar]
  40. Vannella K. M., Moore B. B.. 2008; Viruses as co-factors for the initiation or exacerbation of lung fibrosis. Fibrogenesis Tissue Repair1:2 [CrossRef][PubMed]
    [Google Scholar]
  41. Wilkie G. S., Kerr K., Stewart J. P., Studdert M. J., Davison A. J.. 2015; Genome sequences of equid herpesviruses 2 and 5. Genome Announc3:e00119-15 [CrossRef][PubMed]
    [Google Scholar]
  42. Williams K. J., Maes R., Del Piero F., Lim A., Wise A., Bolin D. C., Caswell J., Jackson C., Robinson N. E., other authors. 2007; Equine multinodular pulmonary fibrosis: a newly recognized herpesvirus-associated fibrotic lung disease. Vet Pathol44:849–862 [CrossRef][PubMed]
    [Google Scholar]
  43. Williams K. J., Robinson N. E., Lim A., Brandenberger C., Maes R., Behan A., Bolin S. R.. 2013; Experimental induction of pulmonary fibrosis in horses with the gammaherpesvirus equine herpesvirus 5. PLoS One8:e77754 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000332
Loading
/content/journal/jgv/10.1099/jgv.0.000332
Loading

Data & Media loading...

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