1887

Abstract

Multiple theories exist regarding the origin of bovine spongiform encephalopathy (BSE). An early and prominent theory proposed that BSE was the result of the adaptation of sheep scrapie to cattle. The reports to date indicate that the distribution of the pathological prion protein (PrP) in experimental bovine scrapie is largely restricted to the central nervous system (CNS). Here, we describe pathological findings in a calf intracerebrally inoculated with a Spanish classical scrapie isolate. While clinical disease was observed 30 months after inoculation and PrP was detected in the CNS, the corresponding phenotype differed from that of BSE. Immunohistochemistry and PMCA also revealed the presence of PrP in the peripheral nerves, lymphoid tissues, skeletal muscle and gastrointestinal tract, suggesting centrifugal spread of the scrapie agent from the brain. To the best of our knowledge, this is the first report describing the detection of PrP in tissues other than the CNS after experimental transmission of scrapie to cattle.

Keyword(s): bovine , BSE , ovine , peripheral tissues , prion and scrapie
Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000906
2017-10-01
2020-01-22
Loading full text...

Full text loading...

/deliver/fulltext/jgv/98/10/2628.html?itemId=/content/journal/jgv/10.1099/jgv.0.000906&mimeType=html&fmt=ahah

References

  1. Bruce ME, Will RG, Ironside JW, Mcconnell I, Drummond D et al. Transmissions to mice indicate that 'new variant' CJD is caused by the BSE agent. Nature 1997;389:498–501 [CrossRef][PubMed]
    [Google Scholar]
  2. Hill AF, Desbruslais M, Joiner S, Sidle KC, Gowland I et al. The same prion strain causes vCJD and BSE. Nature 1997;389:448–450 [CrossRef][PubMed]
    [Google Scholar]
  3. Wilesmith JW, Wells GA, Cranwell MP, Ryan JB. Bovine spongiform encephalopathy: epidemiological studies. Vet Rec 1988;123:638–644[PubMed]
    [Google Scholar]
  4. Konold T, Spiropoulos J, Chaplin MJ, Stack MJ, Hawkins SA et al. Unsuccessful oral transmission of scrapie from British sheep to cattle. Vet Rec 2013;173:118.1–11118 [CrossRef][PubMed]
    [Google Scholar]
  5. Cutlip RC, Miller JM, Hamir AN, Peters J, Robinson MM et al. Resistance of cattle to scrapie by the oral route. Can J Vet Res 2001;65:131–132[PubMed]
    [Google Scholar]
  6. Cutlip RC, Miller JM, Race RE, Jenny AL, Katz JB et al. Intracerebral transmission of scrapie to cattle. J Infect Dis 1994;169:814–820 [CrossRef][PubMed]
    [Google Scholar]
  7. Clark WW, Hourrigan JL, Hadlow WJ. Encephalopathy in cattle experimentally infected with the scrapie agent. Am J Vet Res 1995;56:606–612[PubMed]
    [Google Scholar]
  8. Cutlip RC, Miller JM, Lehmkuhl HD. Second passage of a US scrapie agent in cattle. J Comp Pathol 1997;117:271–275 [CrossRef][PubMed]
    [Google Scholar]
  9. Konold T, Lee YH, Stack MJ, Horrocks C, Green RB et al. Different prion disease phenotypes result from inoculation of cattle with two temporally separated sources of sheep scrapie from Great Britain. BMC Vet Res 2006;2:31 [CrossRef][PubMed]
    [Google Scholar]
  10. Robinson MM, Hadlow WJ, Knowles DP, Huff TP, Lacy PA et al. Experimental infection of cattle with the agents of transmissible mink encephalopathy and scrapie. J Comp Pathol 1995;113:241–251 [CrossRef][PubMed]
    [Google Scholar]
  11. Konold T, Nonno R, Spiropoulos J, Chaplin MJ, Stack MJ et al. Further characterisation of transmissible spongiform encephalopathy phenotypes after inoculation of cattle with two temporally separated sources of sheep scrapie from Great Britain. BMC Res Notes 2015;8:312 [CrossRef][PubMed]
    [Google Scholar]
  12. Andréoletti O, Berthon P, Marc D, Sarradin P, Grosclaude J et al. Early accumulation of PrPSc in gut-associated lymphoid and nervous tissues of susceptible sheep from a romanov flock with natural scrapie. J Gen Virol 2000;81:3115–3126 [CrossRef][PubMed]
    [Google Scholar]
  13. Andréoletti O, Berthon P, Levavasseur E, Marc D, Lantier F et al. Phenotyping of protein-prion (PrPsc)-accumulating cells in lymphoid and neural tissues of naturally scrapie-affected sheep by double-labeling immunohistochemistry. J Histochem Cytochem 2002;50:1357–1370 [CrossRef][PubMed]
    [Google Scholar]
  14. Andréoletti O, Simon S, Lacroux C, Morel N, Tabouret G et al. PrPSc accumulation in myocytes from sheep incubating natural scrapie. Nat Med 2004;10:591–593 [CrossRef][PubMed]
    [Google Scholar]
  15. Garza MC, Monzón M, Marín B, Badiola JJ, Monleón E. Distribution of peripheral PrPSc in sheep with naturally acquired scrapie. PLoS One 2014;9:e97768 [CrossRef][PubMed]
    [Google Scholar]
  16. Buschmann A, Groschup MH. Highly bovine spongiform encephalopathy-sensitive transgenic mice confirm the essential restriction of infectivity to the nervous system in clinically diseased cattle. J Infect Dis 2005;192:934–942 [CrossRef][PubMed]
    [Google Scholar]
  17. Wells GA, Hawkins SA, Green RB, Austin AR, Dexter I et al. Preliminary observations on the pathogenesis of experimental bovine spongiform encephalopathy (BSE): an update. Vet Rec 1998;142:103–106 [CrossRef][PubMed]
    [Google Scholar]
  18. Wells GA, Spiropoulos J, Hawkins SA, Ryder SJ. Pathogenesis of experimental bovine spongiform encephalopathy: preclinical infectivity in tonsil and observations on the distribution of lingual tonsil in slaughtered cattle. Vet Rec 2005;156:401–407 [CrossRef][PubMed]
    [Google Scholar]
  19. Espinosa JC, Morales M, Castilla J, Rogers M, Torres JM. Progression of prion infectivity in asymptomatic cattle after oral bovine spongiform encephalopathy challenge. J Gen Virol 2007;88:1379–1383 [CrossRef][PubMed]
    [Google Scholar]
  20. Kaatz M, Fast C, Ziegler U, Balkema-Buschmann A, Hammerschmidt B et al. Spread of classic BSE prions from the gut via the peripheral nervous system to the brain. Am J Pathol 2012;181:515–524 [CrossRef][PubMed]
    [Google Scholar]
  21. Saborio GP, Permanne B, Soto C. Sensitive detection of pathological prion protein by cyclic amplification of protein misfolding. Nature 2001;411:810–813 [CrossRef][PubMed]
    [Google Scholar]
  22. Franz M, Eiden M, Balkema-Buschmann A, Greenlee J, Schatzl H et al. Detection of PrPSc in peripheral tissues of clinically affected cattle after oral challenge with bovine spongiform encephalopathy. J Gen Virol 2012;93:2740–2748 [CrossRef][PubMed]
    [Google Scholar]
  23. Hedman C, Lyahyai J, Filali H, Marín B, Serrano C et al. Differential gene expression and apoptosis markers in presymptomatic scrapie affected sheep. Vet Microbiol 2012;159:23–32 [CrossRef][PubMed]
    [Google Scholar]
  24. Lacroux C, Vilette D, Fernández-Borges N, Litaise C, Lugan S et al. Prionemia and leukocyte-platelet-associated infectivity in sheep transmissible spongiform encephalopathy models. J Virol 2012;86:2056–2066 [CrossRef][PubMed]
    [Google Scholar]
  25. Laude H, Vilette D, Le Dur A, Archer F, Soulier S et al. New in vivo and ex vivo models for the experimental study of sheep scrapie: development and perspectives. C R Biol 2002;325:49–57 [CrossRef][PubMed]
    [Google Scholar]
  26. Moudjou M, Sibille P, Fichet G, Reine F, Chapuis J et al. Highly infectious prions generated by a single round of microplate-based protein misfolding cyclic amplification. MBio 2013;5:e00829-00813 [CrossRef][PubMed]
    [Google Scholar]
  27. Vilotte JL, Soulier S, Essalmani R, Stinnakre MG, Vaiman D et al. Markedly increased susceptibility to natural sheep scrapie of transgenic mice expressing ovine prp. J Virol 2001;75:5977–5984 [CrossRef][PubMed]
    [Google Scholar]
  28. Fukuda S, Onoe S, Nikaido S, Fujii K, Kageyama S et al. Neuroanatomical distribution of disease-associated prion protein in experimental bovine spongiform encephalopathy in cattle after intracerebral inoculation. Jpn J Infect Dis 2012;65:37–44[PubMed]
    [Google Scholar]
  29. Simmons MM, Harris P, Jeffrey M, Meek SC, Blamire IW et al. BSE in Great Britain: consistency of the neurohistopathological findings in two random annual samples of clinically suspect cases. Vet Rec 1996;138:175–177 [CrossRef][PubMed]
    [Google Scholar]
  30. Casalone C, Zanusso G, Acutis P, Ferrari S, Capucci L et al. Identification of a second bovine amyloidotic spongiform encephalopathy: molecular similarities with sporadic Creutzfeldt-Jakob disease. Proc Natl Acad Sci USA 2004;101:3065–3070 [CrossRef][PubMed]
    [Google Scholar]
  31. Bolea R, Monleón E, Schiller I, Raeber AJ, Acín C et al. Comparison of immunohistochemistry and two rapid tests for detection of abnormal prion protein in different brain regions of sheep with typical scrapie. J Vet Diagn Invest 2005;17:467–469 [CrossRef][PubMed]
    [Google Scholar]
  32. González L, Pitarch JL, Martin S, Thurston L, Simmons H et al. Influence of polymorphisms in the prion protein gene on the pathogenesis and neuropathological phenotype of sheep scrapie after oral infection. J Comp Pathol 2014;150:57–70 [CrossRef][PubMed]
    [Google Scholar]
  33. Iwamaru Y, Okubo Y, Ikeda T, Hayashi H, Imamura M et al. PrPSc distribution of a natural case of bovine spongiform encephalopathy. Prions: Food and Drug Safety 2005;179
    [Google Scholar]
  34. Iwata N, Sato Y, Higuchi Y, Nohtomi K, Nagata N et al. Distribution of PrPSc in cattle with bovine spongiform encephalopathy slaughtered at abattoirs in Japan. Jpn J Infect Dis 2006;59:100–107[PubMed]
    [Google Scholar]
  35. Hoffmann C, Eiden M, Kaatz M, Keller M, Ziegler U et al. BSE infectivity in jejunum, ileum and ileocaecal junction of incubating cattle. Vet Res 2011;42:21 [CrossRef][PubMed]
    [Google Scholar]
  36. Murayama Y, Yoshioka M, Masujin K, Okada H, Iwamaru Y et al. Sulfated dextrans enhance in vitro amplification of bovine spongiform encephalopathy PrP(Sc) and enable ultrasensitive detection of bovine PrPSc. PLoS One 2010;5:e13152 [CrossRef][PubMed]
    [Google Scholar]
  37. Sisó S, Jeffrey M, González L. Neuroinvasion in sheep transmissible spongiform encephalopathies: the role of the haematogenous route. Neuropathol Appl Neurobiol 2009;35:232–246 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000906
Loading
/content/journal/jgv/10.1099/jgv.0.000906
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