1887

Abstract

Feline spongiform encephalopathy (FSE) is a transmissible spongiform encephalopathy that affects domestic cats () and captive wild members of the family Felidae. In this report we describe a case of FSE in a captive cheetah from the zoological garden of Nuremberg. The biochemical examination revealed a BSE-like pattern. Disease-associated scrapie prion protein (PrP) was widely distributed in the central and peripheral nervous system, as well as in the lymphoreticular system and in other tissues of the affected animal, as demonstrated by immunohistochemistry and/or immunoblotting. Moreover, we report for the first time the use of the protein misfolding cyclic amplification technique for highly sensitive detection of PrP in the family Felidae. The widespread PrP deposition suggests a simultaneous lymphatic and neural spread of the FSE agent. The detection of PrP in the spleen indicates a potential for prion infectivity of cheetah blood.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.022103-0
2010-11-01
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/jgv/91/11/2874.html?itemId=/content/journal/jgv/10.1099/vir.0.022103-0&mimeType=html&fmt=ahah

References

  1. Andréoletti, O., Berthon, P., Marc, D., Sarradin, P., Grosclaude, J., van Keulen, L., Schelcher, F., Elsen, J. M. & Lantier, F.(2000). Early accumulation of PrPSc in gut-associated lymphoid and nervous tissues of susceptible sheep from a Romanov flock with natural scrapie. J Gen Virol 81, 3115–3126. [Google Scholar]
  2. Anonymous(2005). Swiss FSE cases raises questions. Animal Pharm 525, 4. [Google Scholar]
  3. Anonymous(2008). Bovine spongiform encephalopathy. In Manual of Diagnostic Tests and Vaccines for Terrestrial Animals (Mammals, Birds and Bees), 6th edn. Paris. : World Organisation for Animal Health (OIE). . [Google Scholar]
  4. Baron, T., Belli, P., Madec, J. Y., Moutou, F., Vitau, C. & Savey, M.(1997). Spongiform encephalopathy in an imported cheetah in France. Vet Rec 141, 270–271.[CrossRef] [Google Scholar]
  5. Baron, T., Madec, J. & Calavas, D.(1999). Similar signature of the prion protein in natural sheep scrapie and bovine spongiform encephalopathy-linked diseases. J Clin Microbiol 37, 3701–3704. [Google Scholar]
  6. Baron, T., Crozet, C., Biacabe, A. G., Philippe, S., Verchere, J., Bencsik, A., Madec, J. Y., Calavas, D. & Samarut, J.(2004). Molecular analysis of the protease-resistant prion protein in scrapie and bovine spongiform encephalopathy transmitted to ovine transgenic and wild-type mice. J Virol 78, 6243–6251.[CrossRef] [Google Scholar]
  7. Bencsik, A., Debeer, S., Petit, T. & Baron, T.(2009). Possible case of maternal transmission of feline spongiform encephalopathy in a captive cheetah. PLoS One 4, e6929.[CrossRef] [Google Scholar]
  8. Beringue, V., Mallinson, G., Kaisar, M., Tayebi, M., Sattar, Z., Jackson, G., Anstee, D., Collinge, J. & Hawke, S.(2003). Regional heterogeneity of cellular prion protein isoforms in the mouse brain. Brain 126, 2065–2073.[CrossRef] [Google Scholar]
  9. Bradshaw, J. M., Pearson, G. R. & Gruffydd-Jones, T. J.(2004). A retrospective study of 286 cases of neurological disorders of the cat. J Comp Pathol 131, 112–120.[CrossRef] [Google Scholar]
  10. Bratberg, B., Ueland, K. & Wells, G. A. H.(1995). Feline spongiform encephalopathy in a cat in Norway. Vet Rec 136, 444.[CrossRef] [Google Scholar]
  11. Bruce, M., Chree, A., McConnell, I., Foster, J., Pearson, G. & Fraser, H.(1994). Transmission of bovine spongiform encephalopathy and scrapie to mice: strain variation and the species barrier. Philos Trans R Soc Lond B Biol Sci 343, 405–411.[CrossRef] [Google Scholar]
  12. 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.[CrossRef] [Google Scholar]
  13. Castilla, J., Saa, P. & Soto, C.(2005a). Detection of prions in blood. Nat Med 11, 982–985. [Google Scholar]
  14. Castilla, J., Saa, P., Hetz, C. & Soto, C.(2005b).In vitro generation of infectious scrapie prions. Cell 121, 195–206.[CrossRef] [Google Scholar]
  15. Castilla, J., Saa, P., Morales, R., Abid, K., Maundrell, K. & Soto, C.(2006). Protein misfolding cyclic amplification for diagnosis and prion propagation studies. Methods Enzymol 412, 3–21. [Google Scholar]
  16. Castilla, J., Morales, R., Saa, P., Barria, M., Gambetti, P. & Soto, C.(2008). Cell-free propagation of prion strains. EMBO J 27, 2557–2566.[CrossRef] [Google Scholar]
  17. Collinge, J., Sidle, K. C., Meads, J., Ironside, J. & Hill, A. F.(1996). Molecular analysis of prion strain variation and the aetiology of ‘new variant' CJD. Nature 383, 685–690.[CrossRef] [Google Scholar]
  18. DEFRA(2009). Exotic species & domestic cats TSE surveillance statistics. http://www.defra.gov.uk/vla/science/sci_tse_stats_exotic.htm.
  19. Demierre, S., Botteron, C., Cizinauskas, S., Doherr, M. G., Fatzer, R. & Jaggy, A.(2002). Feline spongiforme Encephalopathie: erster klinischer Fall in der Schweiz. Schweiz Arch Tierheilkd 144, 550–557 (in German).[CrossRef] [Google Scholar]
  20. Gretzschel, A., Buschmann, A., Eiden, M., Ziegler, M., Lühken, G., Erhardt, G. & Groschup, M. H.(2005). Strain typing of German transmissible spongiform encephalopathies field cases in small ruminants by biochemical methods. J Vet Med B Infect Dis Vet Public Health 52, 55–63.[CrossRef] [Google Scholar]
  21. Harmeyer, S., Pfaff, E. & Groschup, M. H.(1998). Synthetic peptide vaccines yield monoclonal antibodies to cellular and pathological prion proteins of ruminants. J Gen Virol 79, 937–945. [Google Scholar]
  22. Hoffmann, C., Ziegler, U., Buschmann, A., Weber, A., Kupfer, L., Oelschlegel, A., Hammerschmidt, B. & Groschup, M. H.(2007). Prions spread via the autonomic nervous system from the gut to the CNS in cattle incubating BSE. J Gen Virol 88, 1048–1055.[CrossRef] [Google Scholar]
  23. Jeffrey, M., Martin, S., Thomson, J. R., Dingwall, W. S., Begara-McGorum, I. & Gonzalez, L.(2001). Onset and distribution of tissue PrP accumulation in scrapie-affected Suffolk sheep as demonstrated by sequential necropsies and tonsillar biopsies. J Comp Pathol 125, 48–57.[CrossRef] [Google Scholar]
  24. Jones, M., Peden, A. H., Prowse, C. V., Gröner, A., Manson, J. C., Turner, M. L., Ironside, J. W., MacGregor, I. R. & Head, M. W.(2007).In vitro amplification and detection of variant Creutzfeldt-Jakob disease PrPSc. J Pathol 213, 21–26.[CrossRef] [Google Scholar]
  25. Kuczius, T., Koch, R., Keyvani, K., Karch, H., Grassi, J. & Groschup, M. H.(2007). Regional and phenotype heterogeneity of cellular prion proteins in the human brain. Eur J Neurosci 25, 2649–2655.[CrossRef] [Google Scholar]
  26. Kupfer, L., Eiden, M., Buschmannm, A. & Groschup, M. H.(2007). Amino acid sequence and prion strain specific effects on the in vitro and in vivo convertibility of ovine/murine and bovine/murine prion protein chimeras. Biochim Biophys Acta 1772, 704–713.[CrossRef] [Google Scholar]
  27. Kurt, T. D., Perrott, M. R., Wilusz, C. J., Wilusz, J., Supattapone, S., Telling, G. C., Zabel, M. D. & Hoover, E. A.(2007). Efficient in vitro amplification of chronic wasting disease PrPRES. J Virol 81, 9605–9608.[CrossRef] [Google Scholar]
  28. Lezmi, S., Benczik, A., Monks, E., Petit, T. & Baron, T.(2003). First case of feline spongiform encephalopathy in a captive cheetah born in France: PrPSc analysis in various tissues revealed unexpected targeting of kidney and adrenal gland. Histochem Cell Biol 119, 415–422. [Google Scholar]
  29. Lezmi, S., Benczik, A. & Baron, T.(2006). PET-blot analysis contributes to BSE strain recognition in C57Bl/6 mice. J Histochem Cytochem 54, 1087–1094.[CrossRef] [Google Scholar]
  30. Ligios, C., Cancedda, G. M., Margalith, I., Santucciu, C., Madau, L., Maestrale, C., Basagni, M., Saba, M. & Heikenwalder, M.(2007). Intraepithelial and interstitial deposition of pathological prion protein in kidneys of scrapie-affected sheep. PLoS ONE 2, e859.[CrossRef] [Google Scholar]
  31. Richt, J. A., Kasinathan, P., Hamir, A. N., Castilla, J., Sathiyaseelan, T., Vargas, F., Sathiyaseelan, J., Wu, H., Matsushita, H. & other authors(2007). Production of cattle lacking prion protein. Nat Biotechnol 25, 132–138.[CrossRef] [Google Scholar]
  32. Ryder, S. J., Wells, G. A. H., Bradshaw, J. M. & Pearson, G. R.(2001). Inconsistent detection of PrP in extraneural tissues of cats with feline spongiform encephalopathy. Vet Rec 148, 437–441.[CrossRef] [Google Scholar]
  33. Saborio, G. P., Permann, B. & Soto, C.(2001). Sensitive detection of pathological prion protein by cyclic amplification of protein misfolding. Nature 411, 810–813.[CrossRef] [Google Scholar]
  34. Siso, S., Jeffrey, M., Steele, P., McGovern, G., Martin, S., Finlayson, J., Chianini, F. & Gonzalez, L.(2008). Occurrence and cellular localization of PrPd in kidneys of scrapie-affected sheep in the absence of inflammation. J Pathol 215, 126–134.[CrossRef] [Google Scholar]
  35. Stack, M. J., Chaplin, M. J. & Clark, J.(2002). Differentiation of prion protein glycoforms from naturally occurring sheep scrapie, sheep-passaged scrapie strains (CH1641 and SSBP1), bovine spongiform encephalopathy (BSE) cases and Romney and Cheviot breed sheep experimentally inoculated with BSE using two monoclonal antibodies. Acta Neuropathol 104, 279–286. [Google Scholar]
  36. Thorne, L. & Terry, L. A.(2008).In vitro amplification of PrPSc derived from the brain and blood of sheep infected with scrapie. J Gen Virol 89, 3177–3184.[CrossRef] [Google Scholar]
  37. Wyatt, J. M., Pearson, G. R., Smerdon, T., Gruffydd-Jones, T. J. & Wells, G. A. H.(1990). Spongiform encephalopathy in a cat. Vet Rec 126, 513. [Google Scholar]
  38. Wyatt, J. M., Pearson, G. R., Smerdon, T. N., Gruffydd-Jones, T. J., Wells, G. A. & Wilesmith, J. W.(1991). Naturally occurring scrapie-like spongiform encephalopathy in five domestic cats. Vet Rec 129, 233–236.[CrossRef] [Google Scholar]
  39. Young, S. & Slocombe, R. F.(2003). Prion-associated spongiform encephalopathy in an imported Asiatic golden cat (Catapuma temmincki). Aust Vet J 81, 295–296.[CrossRef] [Google Scholar]
  40. Zanusso, G., Nardelli, E., Rosati, A., Fabrizi, G., Ferrari, S., Carteri, A., De Simone, F., Rizzuto, N. & Monaco, S.(1998). Simultaneous occurrence of spongiform encephalopathy in a man and his cat in Italy. Lancet 352, 1116–1117.[CrossRef] [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.022103-0
Loading
/content/journal/jgv/10.1099/vir.0.022103-0
Loading

Data & Media loading...

Supplements

vol. , part 11, pp. 2874 –2883

Western blot analysis of PrP .

Glycoprofile of amplified feline spongiform encephalopathy samples after first and second rounds of protein misfolding cyclic amplification (PMCA).

Average incubation times, in days, of transgenic Tgshp XI mice that had accumulated PrP in their brains (detected by Western blot) after i.c. inoculation of feline spongiform encephalopathy material.

[ Single PDF file] (50 kB)

 



PDF
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