1887

Abstract

Bovine spongiform encephalopathy (BSE) in cattle and variant Creutzfeldt–Jakob disease in humans have previously been shown to be caused by the same strain of transmissible spongiform encephalopathy agent. It is hypothesized that the agent spread to humans following consumption of food products prepared from infected cattle. Despite evidence supporting zoonotic transmission, mouse models expressing human prion protein (HuTg) have consistently shown poor transmission rates when inoculated with cattle BSE. Higher rates of transmission have however been observed when these mice are exposed to BSE that has been experimentally transmitted through sheep or goats, indicating that humans may potentially be more susceptible to BSE from small ruminants. Here we demonstrate that increased transmissibility of small ruminant BSE to HuTg mice was not due to replication of higher levels of infectivity in sheep brain tissue, and is instead due to other specific changes in the infectious agent.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.065730-0
2014-08-01
2021-08-02
Loading full text...

Full text loading...

/deliver/fulltext/jgv/95/8/1855.html?itemId=/content/journal/jgv/10.1099/vir.0.065730-0&mimeType=html&fmt=ahah

References

  1. Asante E. A., Linehan J. M., Desbruslais M., Joiner S., Gowland I., Wood A. L., Welch J., Hill A. F., Lloyd S. E. other authors 2002; BSE prions propagate as either variant CJD-like or sporadic CJD-like prion strains in transgenic mice expressing human prion protein. EMBO J 21:6358–6366 [View Article][PubMed]
    [Google Scholar]
  2. Béringue V., Herzog L., Reine F., Le Dur A., Casalone C., Vilotte J. L., Laude H. 2008; Transmission of atypical bovine prions to mice transgenic for human prion protein. Emerg Infect Dis 14:1898–1901 [View Article][PubMed]
    [Google Scholar]
  3. Bishop M. T., Hart P., Aitchison L., Baybutt H. N., Plinston C., Thomson V., Tuzi N. L., Head M. W., Ironside J. W. other authors 2006; Predicting susceptibility and incubation time of human-to-human transmission of vCJD. Lancet Neurol 5:393–398 [View Article][PubMed]
    [Google Scholar]
  4. Bruce M. E., Will R. G., Ironside J. W., McConnell I., Drummond D., Suttie A., McCardle L., Chree A., Hope J. other authors 1997; Transmissions to mice indicate that ‘new variant’ CJD is caused by the BSE agent. Nature 389:498–501 [View Article][PubMed]
    [Google Scholar]
  5. Buschmann A., Groschup M. H. 2005; Highly bovine spongiform encephalopathy-sensitive transgenic mice confirm the essential restriction of infectivity to the nervous system in clinically diseased cattle. J Infect Dis 192:934–942 [View Article][PubMed]
    [Google Scholar]
  6. Caughey B. 2001; Interactions between prion protein isoforms: the kiss of death?. Trends Biochem Sci 26:235–242 [View Article][PubMed]
    [Google Scholar]
  7. de Marco M. F., Linehan J., Gill O. N., Clewley J. P., Brandner S. 2010; Large-scale immunohistochemical examination for lymphoreticular prion protein in tonsil specimens collected in Britain. J Pathol 222:380–387 [View Article][PubMed]
    [Google Scholar]
  8. Eloit M., Adjou K., Coulpier M., Fontaine J. J., Hamel R., Lilin T., Messiaen S., Andreoletti O., Baron T. other authors 2005; BSE agent signatures in a goat. Vet Rec 156:523–524[PubMed] [CrossRef]
    [Google Scholar]
  9. Espinosa J. C., Andréoletti O., Castilla J., Herva M. E., Morales M., Alamillo E., San-Segundo F. D., Lacroux C., Lugan S. other authors 2007; Sheep-passaged bovine spongiform encephalopathy agent exhibits altered pathobiological properties in bovine-PrP transgenic mice. J Virol 81:835–843 [View Article][PubMed]
    [Google Scholar]
  10. Espinosa J. C., Herva M. E., Andréoletti O., Padilla D., Lacroux C., Cassard H., Lantier I., Castilla J., Torres J. M. 2009; Transgenic mice expressing porcine prion protein resistant to classical scrapie but susceptible to sheep bovine spongiform encephalopathy and atypical scrapie. Emerg Infect Dis 15:1214–1221 [View Article][PubMed]
    [Google Scholar]
  11. Ferguson N. M., Ghani A. C., Donnelly C. A., Hagenaars T. J., Anderson R. M. 2002; Estimating the human health risk from possible BSE infection of the British sheep flock. Nature 415:420–424 [View Article][PubMed]
    [Google Scholar]
  12. Foster J. D., Hope J., Fraser H. 1993; Transmission of bovine spongiform encephalopathy to sheep and goats. Vet Rec 133:339–341 [View Article][PubMed]
    [Google Scholar]
  13. Foster J. D., Bruce M., McConnell I., Chree A., Fraser H. 1996; Detection of BSE infectivity in brain and spleen of experimentally infected sheep. Vet Rec 138:546–548 [View Article][PubMed]
    [Google Scholar]
  14. Fraser H., Dickinson A. G. 1967; Distribution of experimentally induced scrapie lesions in the brain. Nature 216:1310–1311 [View Article][PubMed]
    [Google Scholar]
  15. Gill O. N., Spencer Y., Richard-Loendt A., Kelly C., Dabaghian R., Boyes L., Linehan J., Simmons M., Webb P. other authors 2013; Prevalent abnormal prion protein in human appendixes after bovine spongiform encephalopathy epizootic: large scale survey. BMJ 347:f5675 [View Article][PubMed]
    [Google Scholar]
  16. González L., Martin S., Sisó S., Konold T., Ortiz-Peláez A., Phelan L., Goldmann W., Stewart P., Saunders G. other authors 2009; High prevalence of scrapie in a dairy goat herd: tissue distribution of disease-associated PrP and effect of PRNP genotype and age. Vet Res 40:65 [View Article][PubMed]
    [Google Scholar]
  17. Hamilton M. A., Russo R. C., Thurston R. V. 1977; Trimmed Spearman-Karber method for estimating median lethal concentrations in toxicity bioassays. Environ Sci Technol 11:714–719 [View Article]
    [Google Scholar]
  18. Hill A. F., Desbruslais M., Joiner S., Sidle K. C. L., Gowland I., Collinge J., Doey L. J., Lantos P. 1997; The same prion strain causes vCJD and BSE. Nature 389:448–450, 526 [View Article][PubMed]
    [Google Scholar]
  19. Hilton D. A., Ghani A. C., Conyers L., Edwards P., McCardle L., Penney M., Ritchie D., Ironside J. W. 2002; Accumulation of prion protein in tonsil and appendix: review of tissue samples. BMJ 325:633–634 [View Article][PubMed]
    [Google Scholar]
  20. Houston F., Foster J. D., Chong A., Hunter N., Bostock C. J. 2000; Transmission of BSE by blood transfusion in sheep. Lancet 356:999–1000 [View Article][PubMed]
    [Google Scholar]
  21. Jeffrey M., Martin S., González L., Foster J., Langeveld J. P., van Zijderveld F. G., Grassi J., Hunter N. 2006; Immunohistochemical features of PrP(d) accumulation in natural and experimental goat transmissible spongiform encephalopathies. J Comp Pathol 134:171–181 [View Article][PubMed]
    [Google Scholar]
  22. Jones M., Wight D., Barron R., Jeffrey M., Manson J., Prowse C., Ironside J. W., Head M. W. 2009; Molecular model of prion transmission to humans. Emerg Infect Dis 15:2013–2016 [View Article][PubMed]
    [Google Scholar]
  23. Padilla D., Béringue V., Espinosa J. C., Andreoletti O., Jaumain E., Reine F., Herzog L., Gutierrez-Adan A., Pintado B. other authors 2011; Sheep and goat BSE propagate more efficiently than cattle BSE in human PrP transgenic mice. PLoS Pathog 7:e1001319 [View Article][PubMed]
    [Google Scholar]
  24. Plinston C., Hart P., Chong A., Hunter N., Foster J., Piccardo P., Manson J. C., Barron R. M. 2011; Increased susceptibility of human-PrP transgenic mice to bovine spongiform encephalopathy infection following passage in sheep. J Virol 85:1174–1181 [View Article][PubMed]
    [Google Scholar]
  25. Priem J., Langeveld J. P., van Keulen L. J. M., van Zijderveld F. G., Andreoletti O., Bossers A. 2014; Enhanced virulence of sheep-passaged bovine spongiform encephalopathy agent is revealed by decreased polymorphism barriers in prion protein conversion studies. J Virol 88:2903–2912 [View Article][PubMed]
    [Google Scholar]
  26. Prusiner S. B. 1982; Novel proteinaceous infectious particles cause scrapie. Science 216:136–144 [View Article][PubMed]
    [Google Scholar]
  27. Safar J. G., Scott M., Monaghan J., Deering C., Didorenko S., Vergara J., Ball H., Legname G., Leclerc E. other authors 2002; Measuring prions causing bovine spongiform encephalopathy or chronic wasting disease by immunoassays and transgenic mice. Nat Biotechnol 20:1147–1150 [View Article][PubMed]
    [Google Scholar]
  28. Spiropoulos J., Lockey R., Sallis R. E., Terry L. A., Thorne L., Holder T. M., Beck K. E., Simmons M. M. 2011; Isolation of prion with BSE properties from farmed goat. Emerg Infect Dis 17:2253–2261 [View Article][PubMed]
    [Google Scholar]
  29. Will R. G., Ironside J. W., Zeidler M., Cousens S. N., Estibeiro K., Alperovitch A., Poser S., Pocchiari M., Hofman A., Smith P. G. 1996; A new variant of Creutzfeldt-Jakob disease in the UK. Lancet 347:921–925 [View Article][PubMed]
    [Google Scholar]
  30. Wilson R., Plinston C., Hunter N., Casalone C., Corona C., Tagliavini F., Suardi S., Ruggerone M., Moda F. other authors 2012; Chronic wasting disease and atypical forms of bovine spongiform encephalopathy and scrapie are not transmissible to mice expressing wild-type levels of human prion protein. J Gen Virol 93:1624–1629 [View Article][PubMed]
    [Google Scholar]
  31. Wilson R., King D., Hunter N., Goldmann W., Barron R. M. 2013; Characterization of an unusual transmissible spongiform encephalopathy in goat by transmission in knock-in transgenic mice. J Gen Virol 94:1922–1932 [View Article][PubMed]
    [Google Scholar]
  32. Zeidler M., Stewart G., Cousens S. N., Estibeiro K., Will R. G. 1997; Codon 129 genotype and new variant CJD. Lancet 350:668 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.065730-0
Loading
/content/journal/jgv/10.1099/vir.0.065730-0
Loading

Data & Media loading...

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