1887

Journal of General Virology header logo

Volume 82, Issue 10

PrP in the myenteric plexus, vagosympathetic trunk and endocrine glands of deer with chronic wasting disease Free

Abstract

Accumulated evidence in experimental and natural prion disease systems supports a neural route of infectious prion spread from peripheral sites of entry to the central nervous system. However, little is known about prion trafficking routes in cervids with a naturally occurring prion disease known as chronic wasting disease (CWD). In the brain, the pathogenic isoform of the prion protein (PrP) accumulates initially in the dorsal motor nucleus of the vagus nerve. To assess whether alimentary-associated neural pathways may play a role in prion trafficking, neural and endocrine tissues from mule deer naturally infected with CWD (=6) were examined by immunohistochemistry. PrP was detected in the myenteric plexus, vagosympathetic trunk, nodose ganglion, pituitary, adrenal medulla and pancreatic islets. No to scant PrP staining was detected in other nerves or ganglia (brachial plexus, sciatic nerve, gasserian ganglion, coeliac ganglion, cranial cervical ganglion, spinal nerve roots) of CWD-positive deer and no PrP was detected in nerves or endocrine tissues from 11 control deer. These findings suggest that: (i) transit of PrP in nerves, either centrifugally or centripetally, is one route of prion trafficking and organ invasion and (ii) endocrine organs may also be targets for cervid pathogenic prion accumulation.

  • Received:
  • Accepted:
  • Published Online:
© Microbiology Society
Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-82-10-2327
2001-10-01
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/jgv/82/10/0822327a.html?itemId=/content/journal/jgv/10.1099/0022-1317-82-10-2327&mimeType=html&fmt=ahah

References

  1. Beekes M., McBride P. A. 2000; Early accumulation of pathological PrP in the enteric nervous system and gut-associated lymphoid tissue of hamsters orally infected with scrapie. Neuroscience Letters 278:181–184
     [Google Scholar]
  2. Beekes M., McBride P. A., Baldauf E. 1998; Cerebral targeting indicates vagal spread of infection in hamsters fed with scrapie. Journal of General Virology 79:601–607
     [Google Scholar]
  3. Bons N., Mestre-Frances N., Belli P., Cathala F., Gajdusek D. C., Brown P. 1999; Natural and experimental oral infection of nonhuman primates by bovine spongiform encephalopathy agents. Proceedings of the National Academy of Sciences, USA 96:4046–4051
     [Google Scholar]
  4. Brown K. L., Stewart K., Ritchie D. L., Mabbott N. A., Williams A., Fraser H., Morrison W. I., Bruce M. E. 1999; Scrapie replication in lymphoid tissues depends on prion protein-expressing follicular dendritic cells. Nature Medicine 5:1308–1312
     [Google Scholar]
  5. Card J. P., Rinaman L., Schwaber J. S., Miselis R. R., Whealy M. E., Robbins A. K., Enquist L. W. 1990; Neurotropic properties of pseudorabies virus: uptake and transneuronal passage in the rat central nervous system. Journal of Neuroscience 10:1974–1994
     [Google Scholar]
  6. Glatzel M., Aguzzi A. 2000; PrPC expression in the peripheral nervous system is a determinant of prion neuroinvasion. Journal of General Virology 81:2813–2821
     [Google Scholar]
  7. Groschup M. H., Weiland F., Straub O. C., Pfaff E. 1996; Detection of scrapie agent in the peripheral nervous system of a diseased sheep. Neurobiology of Disease 3:191–195
     [Google Scholar]
  8. 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 Neuropathologica 98:453–457
     [Google Scholar]
  9. Hadlow W. J., Kennedy R. C., Race R. E. 1982; Natural infection of Suffolk sheep with scrapie virus. Journal of Infectious Diseases 146:657–664
     [Google Scholar]
  10. Hainfellner J. A., Budka H. 1999; Disease associated prion protein may deposit in the peripheral nervous system in human transmissible spongiform encephalopathies. Acta Neuropathologica 98:458–460
     [Google Scholar]
  11. Hill A. F., Butterworth R. J., Joiner S., Jackson G., Rossor M. N., Thomas D. J., Frosh A., Tolley N., Bell J. E., Spencer M., King A., Al-Sarraj S., Ironside J. W., Lantos P. L., Collinge J. 1999; Investigation of variant Creutzfeldt–Jakob disease and other human prion diseases with tonsil biopsy samples. Lancet 353:183–189
     [Google Scholar]
  12. Kimberlin R. H., Walker C. A. 1989; Pathogenesis of scrapie in mice after intragastric infection. Virus Research 12:213–220
     [Google Scholar]
  13. Kimberlin R. H., Hall S. M., Walker C. A. 1983; Pathogenesis of mouse scrapie. Evidence for direct neural spread of infection to the CNS after injection of sciatic nerve. Journal of Neurological Sciences 61:315–325
     [Google Scholar]
  14. Korth C., Stierli B., Streit P., Moser M., Schaller O., Fischer R., Schulz-Schaeffer W., Kretzschmar H., Raeber A., Braun U., Ehrensperger F., Hornemann S., Glockshuber R., Riek R., Billeter M., Wuthrich K., Oesch B. 1997; Prion (PrPSc)-specific epitope defined by a monoclonal antibody. Nature 390:74–77
     [Google Scholar]
  15. Loewy A. D., Franklin M. F., Haxhiu M. A. 1994; CNS monoamine cell groups projecting to pancreatic vagal motor neurons: a transneuronal labeling study using pseudorabies virus. Brain Research 638:248–260
     [Google Scholar]
  16. McBride P. A., Beekes M. 1999; Pathological PrP is abundant in sympathetic and sensory ganglia of hamsters fed with scrapie. Neuroscience Letters 265:135–138
     [Google Scholar]
  17. McBride P. A., Eikelenboom P., Kraal G., Fraser H., Bruce M. E. 1992; PrP protein is associated with follicular dendritic cells of spleens and lymph nodes in uninfected and scrapie-infected mice. Journal of Pathology 168:413–418
     [Google Scholar]
  18. McKinley M. P., Bolton D. C., Prusiner S. B. 1983; A protease-resistant protein is a structural component of the scrapie prion. Cell 35:57–62
     [Google Scholar]
  19. Miller M. W., Williams E. S., McCarty C. W., Spraker T. R., Kreeger T. J., Larsen C. T., Thorne E. T. 2000; Epidemiology of chronic wasting disease in free-ranging cervids. Journal of Wildlife Diseases 36:676–690
     [Google Scholar]
  20. Morrison L. A., Sidman R. L., Fields B. N. 1991; Direct spread of reovirus from the intestinal lumen to the central nervous system through vagal autonomic nerve fibers. Proceedings of the National Academy of Sciences, USA 88:3852–3856
     [Google Scholar]
  21. O’Rourke K. I., Baszler T. V., Besser T. E., Miller J. M., Cutlip R. C., Wells G. A., Ryder S. J., Parish S. M., Hamir A. N., Cockett N. E., Jenny A., Knowles D. P. 2000; Preclinical diagnosis of scrapie by immunohistochemistry of third eyelid lymphoid tissue. Journal of Clinical Microbiology 38:3254–3259
     [Google Scholar]
  22. Pattison I. H., Millson G. C. 1960; Further observations on the experimental production of scrapie in goats and sheep. Journal of Comparative Pathology 70:182–193
     [Google Scholar]
  23. Prusiner S. B. 1982; Novel proteinaceous infectious particles cause scrapie. Science 216:136–144
     [Google Scholar]
  24. Race R., Jenny A., Sutton D. 1998; Scrapie infectivity and proteinase K-resistant prion protein in sheep placenta, brain, spleen, and lymph node: implications for transmission and antemortem diagnosis. Journal of Infectious Diseases 178:949–953
     [Google Scholar]
  25. Race R., Oldstone M., Chesebro B. 2000; Entry versus blockade of brain infection following oral or intraperitoneal scrapie administration: role of prion protein expression in peripheral nerves and spleen. Journal of Virology 74:828–833
     [Google Scholar]
  26. Sigurdson C. J., Williams E. S., Miller M. W., Spraker T. R., O’Rourke K. I., Hoover E. A. 1999; Oral transmission and early lymphoid tropism of chronic wasting disease PrPres in mule deer fawns ( Odocoileus hemionus ). Journal of General Virology 80:2757–2764
     [Google Scholar]
  27. Spraker T. R., Miller M. W., Williams E. S., Getzy D. M., Adrian W. J., Schoonveld G. G., Spowart R. A., O’Rourke K. I., Miller J. M., Merz P. A. 1997; Spongiform encephalopathy in free-ranging mule deer ( Odocoileus hemionus ), white-tailed deer ( Odocoileus virginianus ) and Rocky Mountain elk ( Cervus elaphus nelsoni ) in northcentral Colorado. Journal of Wildlife Diseases 33:1–6
     [Google Scholar]
  28. Spraker T. R., Zink R. R., Cummings B. A., Sigurdson C. J., Miller M. W., O’Rourke K. I. 2001; Patterns of distribution of PrPres and spongiform encephalopathy in brain and PrPres in palatine tonsil of non-clinical mule deer ( Odocoileus hemionus ) with chronic wasting disease. Veterinary Pathology (in press)
    [Google Scholar]
  29. van Keulen L. J., Schreuder B. E., Vromans M. E., Langeveld J. P., Smits M. A. 1999; Scrapie-associated prion protein in the gastrointestinal tract of sheep with natural scrapie. Journal of Comparative Pathology 121:55–63
     [Google Scholar]
  30. van Keulen L. J., Schreuder B. E., Vromans M. E., Langeveld J. P., Smits M. A. 2000; Pathogenesis of natural scrapie in sheep. Archives of Virology Supplementum 16:57–71
     [Google Scholar]
  31. Williams E. S., Miller M. W. 2000; Pathogenesis of chronic wasting disease in orally exposed mule deer ( Odocoileus hemionus ): preliminary results. In Proceedings of the 49th Wildlife Disease Association Conference p 29 Jackson, WY, USA. 4–8 June 2000:
     [Google Scholar]
  32. Williams E. S., Young S. 1980; Chronic wasting disease of captive mule deer: a spongiform encephalopathy. Journal of Wildlife Diseases 16:89–98
     [Google Scholar]
  33. Williams E. S., Young S. 1982; Spongiform encephalopathy of Rocky Mountain elk. Journal of Wildlife Diseases 18:465–471
     [Google Scholar]
  34. Ye X., Carp R. I. 1996; Histopathological changes in the pituitary glands of female hamsters infected with the 139H strain of scrapie. Journal of Comparative Pathology 114:291–304
     [Google Scholar]
  35. Ye X., Carp R. I., Kascsak R. J. 1994a; Histopathological changes in the islets of Langerhans in scrapie 139H-affected hamsters. Journal of Comparative Pathology 110:153–167
     [Google Scholar]
  36. Ye X., Carp R. I., Yu Y., Kozielski R., Kozlowski P. 1994b; Hyperplasia and hypertrophy of B cells in the islets of Langerhans in hamsters infected with the 139H strain of scrapie. Journal of Comparative Pathology 110:169–183
     [Google Scholar]
  37. Ye X., Scallet A. C., Carp R. I. 1997; The 139H scrapie agent produces hypothalamic neurotoxicity and pancreatic islet histopathology: electron microscopic studies. Neurotoxicology 18:533–545
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-82-10-2327
Loading
PrPCWD in the myenteric plexus, vagosympathetic trunk and endocrine glands of deer with chronic wasting disease
J. Gen. Virol. 82, 2327 (2001); https://doi.org/10.1099/0022-1317-82-10-2327
/content/journal/jgv/10.1099/0022-1317-82-10-2327
/content/journal/jgv/10.1099/0022-1317-82-10-2327
Loading

Data & Media loading...

Most cited 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