1887

Abstract

A sensitive immunohistochemical procedure was used to investigate the presence of prion protein (PrP) in the ileal Peyer’s patch of PrP-genotyped lambs, including scrapie-free lambs and lambs naturally and experimentally exposed to the scrapie agent. The tyramide signal amplification system was used to enhance the sensitivity of conventional immunohistochemical procedures to show that PrP was widely distributed in the enteric nervous plexus supplying the gut wall. In scrapie-free lambs, PrP was also detected in scattered cells in the lamina propria and in the dome and interfollicular areas of the Peyer’s patch. In the follicles, staining for PrP was mainly confined to the capsule and cells associated with vascular structures in the light central zone. In lambs naturally exposed to the scrapie agent, staining was prominent in the dome and neck region of the follicles and was also found to be associated with the follicle-associated epithelium. Similar observations were made in lambs that had received a single oral dose of scrapie-infected brain material from sheep with a homologous and heterologous PrP genotype 1 and 5 weeks previously. These studies show that the ileal Peyer’s patch in young sheep may be an important site of uptake of the scrapie agent and that the biology of this major gut-associated lymphoid tissue may influence the susceptibility to oral infection in sheep. Furthermore, these studies suggest that homology or heterology between PrP genotypes or the presence of PrP genotypes seldom associated with disease does not impede uptake of PrP.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-81-9-2327
2000-09-01
2020-11-25
Loading full text...

Full text loading...

/deliver/fulltext/jgv/81/9/0812327a.html?itemId=/content/journal/jgv/10.1099/0022-1317-81-9-2327&mimeType=html&fmt=ahah

References

  1. Anon. 2000; Sauekontrollen (Norwegian Sheep Control System) Oslo, Norway: Norway Meat (Co-operative;
    [Google Scholar]
  2. 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 Letters278:181–184
    [Google Scholar]
  3. Beya M. F., Miyasaka M., Dudler L., Ezaki T., Trnka Z.. 1986; Studies on the differentiation of T lymphocytes in sheep. II. Two monoclonal antibodies that recognize all ovine T lymphocytes. Immunology57:115–121
    [Google Scholar]
  4. Blättler T., Brander S., Raeber A. J., Klein M. A., Voigtländer T., Weissmann C., Aguzzi A.. 1997; PrP-expression required for transfer of scrapie infectivity from spleen to brain. Nature389:69–73
    [Google Scholar]
  5. Bolton D. C., McKinley M. P., Prusiner S. B.. 1982; Identification of a protein that purifies with the scrapie protein. Science218:1309–1311
    [Google Scholar]
  6. Bosser A., Schreuder B. E. C., Muileman I. H., Belt P. B. G. M., Smits M. A.. 1996; PrP genotype contributes to determining survival times of sheep with natural scrapie. Journal of General Virology77:2669–2673
    [Google Scholar]
  7. Bratberg B., Benestad S. L., Knutsen G.. 2000; Resultater fra overvåkings- og kontrollprogrammet for skrapesjuke hos sau – histopatologi (Results from the surveillance- and control programme for scrapie in sheep – histopathology) In Husdyrforsøksmøtet 2000 pp173–176 Agricultural University of Norway; 15–16 February 2000 Edited by Kaurstad E.. (In Norwegian)
    [Google Scholar]
  8. Brotherson J. G., Renwick C. C., Stamp J. T., Zlotnik I., Pattison I. H.. 1968; Spread of scrapie by contact to goats and sheep. Journal of Comparative Pathology78:9–17
    [Google Scholar]
  9. Brown H. R., Goller N. L., Rudelli R. D., Merz G. S., Wolfe G. C., Wisniewski H. M., Robakis N. K.. 1990; The mRNA encoding the scrapie agent protein is present in a variety of non-neuronal cells. Acta Neuropathologica80:1–6
    [Google Scholar]
  10. 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 Medicine5:1308–1312
    [Google Scholar]
  11. Büeler H., Aguzzi A., Sailer A., Greiner R.-A., Autenried P., Aguet M., Weissmann C.. 1993; Mice devoid of PrP are resistant to scrapie. Cell73:1339–1347
    [Google Scholar]
  12. Carlens O.. 1928; Studien über das lymphatische Gewebe des Darmkanals bei einigen Haustieren, mit besonderer Berücksichtigung der embryonalen Entwicklung, der Mengenverhältnisse und der Altersinvolution dieses Gewebes im Dünndarm des Rindes. Zeitschrift für Anatomie und Entwicklüngsgeschichte86:393–493
    [Google Scholar]
  13. Clouscard C., Beaudry P., Elsen J. M., Milan D., Dussaucy M., Bounneau C., Schelcher F., Chatelain J., Launay J. M., Laplanche J. L.. 1995; Different allelic effects of the codons 136 and 171 of the prion protein gene in sheep with natural scrapie. Journal of Comparative Virology76:2097–2101
    [Google Scholar]
  14. Dickinson A. G.. 1974; Natural infection, ‘spontaneous generation’ and scrapie. Nature252:179–180
    [Google Scholar]
  15. Egan R. M., Yorkey C., Black R., Khan Loh W., Stevens J. L., Woodward J. G.. 1996; Peptide-specific T cell clonal expansion in vivo following immunization in the eye, an immune-privileged site. Journal of Immunology157:2262–2271
    [Google Scholar]
  16. Elsen J. M., Amigues Y., Schelcher F., Ducrocq V., Andreoletti O., Eychenne F., Khang J. V., Poivey J. P., Lantier F., Laplanche J. L.. 1999; Genetic susceptibility and transmission factors in scrapie: detailed analysis of an epidemic in a closed flock of Romanov. Archives of Virology144:431–445
    [Google Scholar]
  17. Fraser H., Brown K. L., Stewart K., McConnell I., McBride P., Williams A.. 1996; Replication of scrapie in spleens of SCID mice follows reconstitution with wild-type mouse bone marrow. Journal of General Virology77:1935–1940
    [Google Scholar]
  18. Gerber H. A., Morris B., Trevella W.. 1986; The role of gut-associated lymphoid tissues in the generation of immunoglobulin-bearing lymphocytes in sheep. Australian Journal of Experimental Biology and Medical Research64:201–213
    [Google Scholar]
  19. Goldmann W., O’Neill G., Cheung F., Charleson F., Ford P., Hunter N.. 1999; PrP (prion) gene expression in sheep may be modulated by alternative polyadenylation of its messenger RNA. Journal of General Virology80:2275–2283
    [Google Scholar]
  20. 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 Neuropathologica98:453–457
    [Google Scholar]
  21. Hadlow W. J., Kennedy R. C., Race R. E.. 1982; Natural infection of Suffolk sheep with scrapie virus. Journal of Infectious Diseases146:657–664
    [Google Scholar]
  22. Halleraker M., Landsverk T., Nicander L.. 1990; Organization of ruminant Peyer’s patches as seen with enzyme histochemical markers of stromal and accessory cells. Veterinary Immunology and Immunopathology26:93–104
    [Google Scholar]
  23. Hardt M., Baron T., Groschup M. H.. 2000; A comparative study on the immunohistochemical methods for detecting abnormal prion protein with monoclonal and polyclonal antibodies. Journal of Comparative Pathology122:43–53
    [Google Scholar]
  24. Harmeyer S., Pfaff E., Groschup M. H.. 1998; Synthetic peptide vaccines yield monoclonal antibodies to cellular and pathological prion proteins of ruminants. Journal of General Virology79:937–945
    [Google Scholar]
  25. Horiuchi M., Yamazaki N., Ikeda T., Ishiguro N., Shinagawa M.. 1995; A cellular form of prion protein (PrPC) exists in many non-neuronal tissues of sheep. Journal of General Virology76:2583–2587
    [Google Scholar]
  26. Hourrigan J. L., Klingsporn A., Clark W. W., Decamp M.. 1979; Epidemiology of scrapie in the United States. In Slow Transmissible Diseases of the Nervous System pp331–356 Edited by Prusiner S. B., Hadlow W. J.. New York: Academic Press;
    [Google Scholar]
  27. Hunter N., Foster J. D., Goldmann W., Stear M. J., Hope J., Bostock C.. 1996; Natural scrapie in a closed flock of Cheviot sheep occurs only in specific PrP genotypes. Archives of Virology141:809–824
    [Google Scholar]
  28. Hunyady B., Krempels K., Harta G., Mezey É.. 1996; Immunohistochemical signal amplification by catalyzed reporter deposition and its application in double immunostaining. Journal of Histochemistry and Cytochemistry44:1353–1362
    [Google Scholar]
  29. Jeffrey M., Goodsir C. M., Holliman A., Higgins R. J., Bruce M. A., McBride P. A., Fraser J. R.. 1998; Determination of the frequency and distribution of vascular and parenchymal amyloid with polyclonal and N-terminal-specific PrP antibodies in scrapie-affected sheep and mice. Veterinary Record142:534–537
    [Google Scholar]
  30. Kitamoto T., Muramoto T., Mohri S., Doh-Ura K., Tateishi J.. 1991; Abnormal isoform of prion protein accumulates in follicular dendritic cells in mice with Creutzfeldt–Jakob disease. Journal of Virology65:6292–6295
    [Google Scholar]
  31. Klein M. A., Frigg R., Flechsig E., Raeber A. J., Kalinke U., Bluethmann H., Bootz F., Suter M., Zinkernagel R. M., Aguzzi A.. 1997; A crucial role for B cells in neuroinvasive scrapie. Nature390:687–690
    [Google Scholar]
  32. Klein M. A., Frigg R., Raeber A. J., Flechsig E., Hegyi I., Zinkernagel R. M., Weissmann C., Aguzzi A.. 1998; PrP expression in B lymphocytes is not required for prion neuroinvasion. Nature Medicine4:1429–1433
    [Google Scholar]
  33. 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. Nature390:74–77
    [Google Scholar]
  34. Krammer H.-J., Kühnel W.. 1993; Topography of the enteric nervous system in Peyer’s patches of the porcine small intestine. Cell and Tissue Research272:267–272
    [Google Scholar]
  35. Landsverk T.. 1981; The epithelium covering Peyer’s patches in young milk-fed calves. An ultrastructural and enzyme histochemical investigation. Acta Veterinaria Scandinavia22:198–210
    [Google Scholar]
  36. Landsverk T.. 1987; The follicle-associated epithelium of the ileal Peyer’s patch in ruminants is distinguished by its shedding of 50 nm particles. Immunology and Cell Biology65:251–261
    [Google Scholar]
  37. Landsverk T.. 1988; Phagocytosis and transcytosis by the follicle-associated epithelium of the ileal Peyer’s patch in calves. Immunology and Cell Biology66:261–268
    [Google Scholar]
  38. Landsverk T., Press C. M.. 1998; Immune system. In Textbook of Veterinary Histology pp128–147 Edited by Dellman H. D., Eurell J. A. Baltimore: Williams & Wilkins;
    [Google Scholar]
  39. Landsverk T., Lium B., Matovelo J. A., Liven E., Nordstoga K.. 1990a; Peyer’s patches in experimental Salmonella dublin infection in calves. Microvascular and epithelial changes contributing to atrophy of lymphoid follicles. Acta Pathologica Microbiologica Immunologica Scandinavia98:255–268
    [Google Scholar]
  40. Landsverk T., Trevella W., Nicander L.. 1990b; Transfer of carbonic anhydrase-positive particles from the follicle-associated epithelium to lymphocytes of Peyer’s patches in foetal sheep and lambs. Cell and Tissue Research261:239–247
    [Google Scholar]
  41. Landsverk T., Halleraker M., Aleksandersen M., McClure S., Hein W., Nicander L.. 1991; The intestinal habitat for organized lymphoid tissues in ruminants; comparative aspects of structure, function and development. Veterinary Immunology and Immunopathology28:1–16
    [Google Scholar]
  42. Lasmézas C. I., Cesbron J.-Y., Deslys J.-P., Demaimay R., Adjou K. T., Rioux R., Lemarie C., Locht C., Dormont D.. 1996; Immune system-dependent and -independent replication of the scrapie agent. Journal of Virology70:1292–1295
    [Google Scholar]
  43. Lucier M. R., Thompson R. E., Waire J., Lin A. W., Osborne B. A., Goldsby R. A.. 1998; Multiple sites of V lambda diversification in cattle. Journal of Immunology161:5438–5444
    [Google Scholar]
  44. McBride P. A., Eikelenboom P., Kraal G., Fraser H., Bruce M. A.. 1992; PrP protein is associated with follicular dendritic cells of spleens and lymph nodes in uninfected and scrapie-infected mice. Journal of Pathology168:413–418
    [Google Scholar]
  45. Miller J. M., Jenny A. L., Talyor W. D., March R. F., Rubenstein R., Race R.. 1993; Immunohistochemical detection of prion protein in sheep with scrapie. Journal of Veterinary Diagnostic Investigation5:309–316
    [Google Scholar]
  46. Momotani E., Whipple D. L., Thiermann A. B., Cheville N. F.. 1988; Role of M cells and macrophages in the entrance of Mycobacterium paratuberculosis into domes of ileal Peyer’s patches in calves. Veterinary Pathology25:131–137
    [Google Scholar]
  47. Nicander L., Halleraker M., Landsverk T.. 1991; Ontogeny of reticular cells in the ileal Peyer’s patch of sheep and goats. American Journal of Anatomy191:237–249
    [Google Scholar]
  48. O’Rourke K. I., Holyoak G. R., Clark W. W., Mickelson J. R., Wang S., Melco R. P., Besser T. E., Foote W. C.. 1997; PrP genotypes and experimental scrapie in orally inoculated Suffolk sheep in the United States. Journal of General Virology78:975–978
    [Google Scholar]
  49. Press C. M., Halleraker M., Landsverk T.. 1992; Ontogeny of leukocyte populations in the ileal Peyer’s patch of sheep. Developmental and Comparative Immunology16:229–241
    [Google Scholar]
  50. Press C. M., Reynolds J. D., McClure S. J., Simpson-Morgan M. W., Landsverk T.. 1996; Fetal lambs are depleted of IgM+ cells following a single injection of an anti-IgM antibody early in gestation. Immunology88:28–34
    [Google Scholar]
  51. Reynaud C.-A., Mackay C. R., Müller R. G., Weill J.-C.. 1991; Somatic generation of diversity in a mammalian primary lymphoid organ: the sheep ileal Peyer’s patches. Cell64:995–1005
    [Google Scholar]
  52. Reynolds J. D., Morris B.. 1983; The evolution and involution of Peyer’s patches in fetal and postnatal sheep. European Journal of Immunology13:627–635
    [Google Scholar]
  53. Schreuder B. E. C., van Keulen L. J. M., Vromans M. E. W., Langeveld J. P. M., Smits M. A.. 1998; Tonsillar biopsy and PrPSc detection in the preclinical diagnosis of scrapie. Veterinary Record142:564–568
    [Google Scholar]
  54. Schulz-Schaeffer W. J., Tschoke S., Kranefuss N., Drose W., Hause-Reitner D., Giese A., Groschup M. H., Kretzschmar H. A.. 2000; The paraffin-embedded tissue blot detects PrP(Sc) early in the incubation time in prion diseases. American Journal of Pathology156:51–56
    [Google Scholar]
  55. 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 trophism of chronic wasting disease PrPres in mule deer fawns ( Odocoileus hemionus ). Journal of General Virology80:2757–2764
    [Google Scholar]
  56. Tranulis M. A., Osland A., Bratberg B., Ulvund M. J.. 1999; Prion protein gene polymorphisms in sheep with natural scrapie and healthy controls in Norway. Journal of General Virology80:1073–1077
    [Google Scholar]
  57. van Keulen L. J. M., Schreuder B. E. C., Meloen R. H., Poelen-van den Berg M., Mooij-Harkes G., Vromans M. E. W., Langeveld J. P. M.. 1995; Immunohistochemical detection and localization of prion protein in brain tissue of sheep with natural scrapie. Veterinary Pathology32:299–308
    [Google Scholar]
  58. van Keulen L. J. M., Schreuder B. E. C., Meloen R. H., Mooij-Harkes G., Vromans M. E. W., Langeveld J. P. M.. 1996; Immunohistochemical detection of prion protein in lymphoid tissues of sheep with natural scrapie. Journal of Clinical Microbiology34:1228–1231
    [Google Scholar]
  59. van Keulen L. J. M., Schreuder B. E. C., Vromans M. E. W., Langeveld J. P. M., Smits M. A.. 1999; Scrapie-associated prion protein in the gastrointestinal tract of sheep with natural scrapie. Journal of Comparative Pathology121:55–63
    [Google Scholar]
  60. Wolf J. L., Bye W. A.. 1984; The membranous epithelial (M) cell and the mucosal immune system. Annual Review of Medicine35:95–112
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-81-9-2327
Loading
/content/journal/jgv/10.1099/0022-1317-81-9-2327
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