Prions in the peripheral nerves of bovine spongiform encephalopathy-affected cattle Free

Abstract

With the use of increasingly sensitive methods for detection of the abnormal isoform of prion protein (PrP) and infectivity in prion diseases, it has recently been shown that parts of the peripheral nervous system (PNS) of bovine spongiform encephalopathy (BSE)-affected cattle may become infected. It has been reported that prions spread to the central nervous system (CNS) via the PNS in sheep scrapie, but the pathogenesis of BSE in cattle is less well understood. To determine whether parts of the PNS other than those implicated directly in the hypothetical pathogenetic spread of agent from the intestine to the CNS become involved before or after the CNS is affected, PrP distribution was investigated by a highly sensitive Western blotting technique in dorsal root ganglia, stellate ganglion, phrenic, radial and sciatic nerves, adrenal gland and CNS of cattle that were inoculated orally with BSE-affected brain and culled sequentially. In experimentally BSE-affected cattle, PrP was first detected in the CNS and dorsal root ganglia; subsequently, PrP accumulation was detected in the peripheral nerve trunks. PrP was also detected in the adrenal glands of cattle that showed clinical signs. No PrP was detected in the PNS of BSE-negative cattle. This study shows that, with respect to dorsal root ganglia, a paravertebral sympathetic ganglion and the somatic nerves examined, PrP is detected in the PNS during the disease course at the same time as, or after, it accumulates in the CNS.

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2007-06-01
2024-03-28
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References

  1. Beekes M., McBride P. A., Baldauf E. 1998; Cerebral targeting indicates vagal spread of infection in hamsters fed with scrapie. J Gen Virol 79:601–607
    [Google Scholar]
  2. Bolton D. C., McKinley M. P., Prusiner S. B. 1982; Identification of a protein that purifies with the scrapie prion. Science 218:1309–1311 [CrossRef]
    [Google Scholar]
  3. 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]
  4. Chazot G., Broussolle E., Lapras C., Blattler T., Aguzzi A., Kopp N. 1996; New variant of Creutzfeldt–Jakob disease in a 26-year-old French man. Lancet 347:1181 [CrossRef]
    [Google Scholar]
  5. Cousens S. N., Vynnycky E., Zeidler M., Will R. G., Smith P. G. 1997; Predicting the CJD epidemic in humans. Nature 385:197–198 [CrossRef]
    [Google Scholar]
  6. Favereaux A., Quadrio I., Vital C., Perret-Liaudet A., Anne O., Laplanche J. L., Petry K. G., Vital A. 2004; Pathologic prion protein spreading in the peripheral nervous system of a patient with sporadic Creutzfeldt-Jakob disease. Arch Neurol 61:747–750 [CrossRef]
    [Google Scholar]
  7. Fraser H. 1979; Neuropathology of scrapie: precision of the lesions and their diversity. In Slow Transmissible Diseases of the Nervous System . pp 387–406 Edited by Prusiner S. B., Hadlow W. J. New York: Academic Press;
  8. Fraser H., Foster J. D. 1994; Transmission to mice, sheep and goat and bioassay of bovine tissues. In Transmissible Spongiform Encephalopathies pp 145–160 Edited by Bradley R., Marchant B. Brussels: European Commission Agriculture;
    [Google Scholar]
  9. Groschup M. H., Weiland F., Straub O. C., Pfaff E. 1996; Detection of scrapie agent in the peripheral nervous system of a diseased sheep. Neurobiol Dis 3:191–195 [CrossRef]
    [Google Scholar]
  10. Groschup M. H., Beekes M., McBride P. A., Hardt M., Hainfellner J. A., Budka H. 1999; Deposition of disease-associated prion protein involves the peripheral nervous system in experimental scrapie. Acta Neuropathol (Berl 98:453–457 [CrossRef]
    [Google Scholar]
  11. Haik S., Faucheux B. A., Sazdovitch V., Privat N., Kemeny J. L., Perret-Liaudet A., Hauw J. J. 2003; The sympathetic nervous system is involved in variant Creutzfeldt–Jakob disease. Nat Med 9:1121–1123 [CrossRef]
    [Google Scholar]
  12. Hayashi H., Takata M., Iwamaru Y., Ushiki Y., Kimura K.-M., Tagawa Y., Shinagawa M., Yokoyama T. 2004; Effect of tissue deterioration on postmortem BSE diagnosis by immunobiochemical detection of an abnormal isoform of prion protein. J Vet Med Sci 66:515–520 [CrossRef]
    [Google Scholar]
  13. Hayashi H.-K., Yokoyama T., Takata M., Iwamaru Y., Imamura M., Ushiki Y. K., Shinagawa M. 2005; The N-terminal cleavage site of PrPSc from BSE differs from that of PrPSc from scrapie. Biochem Biophys Res Commun 328:1024–1027 [CrossRef]
    [Google Scholar]
  14. Head M. W., Ritchie D., Smith N., McLoughlin V., Nailon W., Samad S., Masson S., Bishop M., McCardle L., Ironside J. W. 2004; Peripheral tissue involvement in sporadic, iatrogenic, and variant Creutzfeldt–Jakob disease: an immunohistochemical, quantitative, and biochemical study. Am J Pathol 164:143–153 [CrossRef]
    [Google Scholar]
  15. Ishida C., Okino S., Kitamoto T., Yamada M. 2005; Involvement of the peripheral nervous system in human prion diseases including dural graft associated Creutzfeldt–Jakob disease. J Neurol Neurosurg Psychiatry 76:325–329 [CrossRef]
    [Google Scholar]
  16. Iwamaru Y., Ookubo Y., Ikeda T., Hayashi H., Imamura M., Yokoyama T., Shinagawa M. 2005; PrPSc distribution of a natural case of bovine spongiform encephalopathy. In Prions: Food and Drug Safety p– 179 Edited by Kitamoto T. Tokyo: Springer;
    [Google Scholar]
  17. Iwata N., Sato Y., Higuchi Y., Nohtomi K., Nagata N., Hasegawa H., Tobiume M., Nakamura Y., Hagiwara K. other authors 2006; Distribution of PrPSc in cattle with bovine spongiform encephalopathy slaughtered at abattoirs in Japan. Jpn J Infect Dis 59:100–107
    [Google Scholar]
  18. MAFF 1995 Bovine Spongiform Encephalopathy in Great Britain – A Progress Report London: Ministry of Agriculture Fisheries and Food;
    [Google Scholar]
  19. Masters C. L., Richardson E. P. 1978; Subacute spongiform encephalopathy (Creutzfeldt–Jakob disease). The nature and progression of spongiform change. Brain 101:333–344 [CrossRef]
    [Google Scholar]
  20. McBride P. A., Beekes M. 1999; Pathological PrP is abundant in sympathetic and sensory ganglia of hamsters fed with scrapie. Neurosci Lett 265:135–138 [CrossRef]
    [Google Scholar]
  21. McBride P. A., Schulz-Schaeffer W. J., Donaldson M., Bruce M., Diringer H., Kretzschmar H. A., Beekes M. 2001; Early spread of scrapie from the gastrointestinal tract to the central nervous system involves autonomic fibers of the splanchnic and vagus nerves. J Virol 75:9320–9327 [CrossRef]
    [Google Scholar]
  22. Prusiner S. B. 1991; Molecular biology of prion diseases. Science 252:1515–1522 [CrossRef]
    [Google Scholar]
  23. Prusiner S. B., Bolton D. C., Groth D. F., Bowman K. A., Cochran S. P., McKinley M. P. 1982; Further purification and characterization of scrapie prions. Biochemistry 21:6942–6950 [CrossRef]
    [Google Scholar]
  24. 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 [CrossRef]
    [Google Scholar]
  25. Scott M. R., Safar J., Telling G., Nguyen O., Groth D., Torchia M., Koehler R., Tremblay P., Walther D. other authors 1997; Identification of a prion protein epitope modulating transmission of bovine spongiform encephalopathy prions to transgenic mice. Proc Natl Acad Sci U S A 94:14279–14284 [CrossRef]
    [Google Scholar]
  26. Shimada K., Hayashi H.-K., Ookubo Y., Iwamaru Y., Imamura M., Takata M., Schmerr M. J., Shinagawa M., Yokoyama T. 2005; Rapid PrPSc detection in lymphoid tissue and application to scrapie surveillance of fallen stock in Japan: variable PrPSc accumulation in palatal tonsil in natural scrapie. Microbiol Immunol 49:801–804 [CrossRef]
    [Google Scholar]
  27. Terry L. A., Marsh S., Ryder S. J., Hawkins S. A. C., Wells G. A. H., Spencer Y. I. 2003; Detection of disease-specific PrP in the distal ileum of cattle exposed orally to the agent of bovine spongiform encephalopathy. Vet Rec 152:387–392 [CrossRef]
    [Google Scholar]
  28. van Keulen L. J., Schreuder B. E., Vromans M. E., Langeveld J. P., Smits M. A. 2000; Pathogenesis of natural scrapie in sheep. Arch Virol Suppl 16:57–71
    [Google Scholar]
  29. Wells G. A. H., Hawkins S. A. C. 2004; Animal models of transmissible bovine spongiform encephalopathies: experimental infection, observation and tissue collection. In Techniques in Prion Research pp 37–71 Edited by Lehmann S., Grassi J. Basel: Birkhäuser Verlag;
    [Google Scholar]
  30. Wells G. A. H., Wilesmith J. W. 2004; Bovine spongiform encephalopathy and related diseases. In Prion Biology and Diseases , 2nd edn. pp 595–628 Edited by Prusiner S. B. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press;
    [Google Scholar]
  31. Wells G. A., Dawson M., Hawkins S. A., Green R. B., Dexter I., Francis M. E., Simmons M. M., Austin A. R., Horigan M. W. 1994; Infectivity in the ileum of cattle challenged orally with bovine spongiform encephalopathy. Vet Rec 135:40–41 [CrossRef]
    [Google Scholar]
  32. Wells G. A., Dawson M., Hawkins S. A., Austin A. R., Green R. B., Dexter I., Horigan M. W., Simmons M. M. 1996; Preliminary observations on the pathogenesis of experimental bovine spongiform encephalopathy. In Bovine Spongiform Encephalopathy: The BSE Dilemma pp 28–44 Edited by Gibbs C. J Jr. New York: Springer Verlag;
    [Google Scholar]
  33. Wells G. A., Hawkins S. A., Green R. B., Austin A. R., Dexter I., Spencer I., Chaplin M. J., Stack M. J., Dawson M. 1998; Preliminary observations on the pathogenesis of experimental bovine spongiform encephalopathy (BSE): an update. Vet Rec 142:103–106 [CrossRef]
    [Google Scholar]
  34. Wells G. A., Hawkins S. A., Green R. B., Spencer Y. I., Dexter I., Dawson M. 1999; Limited detection of sternal bone marrow infectivity in the clinical phase of experimental bovine spongiform encephalopathy (BSE). Vet Rec 144:292–294 [CrossRef]
    [Google Scholar]
  35. Wells G. A., Spiropoulos J., Hawkins S. A., Ryder S. J. 2005; Pathogenesis of experimental bovine spongiform encephalopathy: preclinical infectivity in tonsil and observations on the distribution of lingual tonsil in slaughtered cattle. Vet Rec 156:401–407 [CrossRef]
    [Google Scholar]
  36. Wells G. A. H., Konold T., Arnold M. E., Austin A. R., Hawkins S. A. C., Stack M., Simmons M. M., Lee Y. H., Gavier-Widén D. other authors 2007; Bovine spongiform encephalopathy: the effect of oral exposure dose on attack rate and incubation period in cattle. J Gen Virol 88:1363–1373 [CrossRef]
    [Google Scholar]
  37. 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 [CrossRef]
    [Google Scholar]
  38. Will R. G., Alperovitch A., Poser S., Pocchiari M., Hofman A., Mitrova E., de Silva R., D’Alessandro M., Delasnerie-Laupretre N. other authors 1998; Descriptive epidemiology of Creutzfeldt–Jakob disease in six European countries, 1993–1995. . EU Collaborative Study Group for CJD. . Ann Neurol 43:763–767 [CrossRef]
    [Google Scholar]
  39. Yokoyama T., Kimura K.-M., Ushiki Y., Yamada S., Morooka A., Nakashiba T., Sassa T., Itohara S. 2001; In vivo conversion of cellular prion protein to pathogenic isoforms, as monitored by conformation-specific antibodies. J Biol Chem 276:11265–11271 [CrossRef]
    [Google Scholar]
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