1887

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Volume 93, Issue 1

Evidence for distinct chronic wasting disease (CWD) strains in experimental CWD in ferrets Free

Abstract

Chronic wasting disease (CWD) is an evolving prion disease of cervids (deer, elk and moose) that has been recognized in North America and Korea. Infection of non-cervid reservoir or transport species in nature is not reported. However, the ferret () is susceptible to CWD after experimental inoculation. Here, we report that infection of ferrets with either of two ferret CWD isolates by various routes of exposure has revealed biologically distinct strain-like properties distinguished by different clinical progression and survival period. The isolates of ferret CWD were also differentiated by the distribution of the infectious prion protein (PrP) in the brain and periphery, and by the proteinase K sensitivity of PrP. These findings suggest that diversity in prion conformers exists in CWD-infected cervids.

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© 2012 SGM
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2012-01-01
2024-04-20
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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[PubMed]
     [Google Scholar]
  2. Angers R. C., Kang H. E., Napier D., Browning S., Seward T., Mathiason C., Balachandran A., McKenzie D., Castilla J. other authors 2010; Prion strain mutation determined by prion protein conformational compatibility and primary structure. Science 328:1154–1158 [View Article][PubMed]
     [Google Scholar]
  3. Baeten L. A., Powers B. E., Jewell J. E., Spraker T. R., Miller M. W. 2007; A natural case of chronic wasting disease in a free-ranging moose (Alces alces shirasi). J Wildl Dis 43:309–314[PubMed] [CrossRef]
     [Google Scholar]
  4. Bartz J. C., Marsh R. F., McKenzie D. I., Aiken J. M. 1998; The host range of chronic wasting disease is altered on passage in ferrets. Virology 251:297–301 [View Article][PubMed]
     [Google Scholar]
  5. Bartz J. C., Bessen R. A., McKenzie D., Marsh R. F., Aiken J. M. 2000; Adaptation and selection of prion protein strain conformations following interspecies transmission of transmissible mink encephalopathy. J Virol 74:5542–5547 [View Article][PubMed]
     [Google Scholar]
  6. Bartz J. C., Dejoia C., Tucker T., Kincaid A. E., Bessen R. A. 2005; Extraneural prion neuroinvasion without lymphoreticular system infection. J Virol 79:11858–11863 [View Article][PubMed]
     [Google Scholar]
  7. Bartz J. C., Kramer M. L., Sheehan M. H., Hutter J. A., Ayers J. I., Bessen R. A., Kincaid A. E. 2007; Prion interference is due to a reduction in strain-specific PrPSc levels. J Virol 81:689–697 [View Article][PubMed]
     [Google Scholar]
  8. Benestad S. L., Sarradin P., Thu B., Schönheit J., Tranulis M. A., Bratberg B. 2003; Cases of scrapie with unusual features in Norway and designation of a new type, Nor98. Vet Rec 153:202–208 [View Article][PubMed]
     [Google Scholar]
  9. 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 [View Article][PubMed]
     [Google Scholar]
  10. Bessen R. A., Marsh R. F. 1992a; Identification of two biologically distinct strains of transmissible mink encephalopathy in hamsters. J Gen Virol 73:329–334 [View Article][PubMed]
     [Google Scholar]
  11. Bessen R. A., Marsh R. F. 1992b; Biochemical and physical properties of the prion protein from two strains of the transmissible mink encephalopathy agent. J Virol 66:2096–2101[PubMed]
     [Google Scholar]
  12. Bessen R. A., Marsh R. F. 1994; Distinct PrP properties suggest the molecular basis of strain variation in transmissible mink encephalopathy. J Virol 68:7859–7868[PubMed]
     [Google Scholar]
  13. Brayton K. A., O’Rourke K. I., Lyda A. K., Miller M. W., Knowles D. P. Jr 2004; A processed pseudogene contributes to apparent mule deer prion gene heterogeneity. Gene 326:167–173 [View Article][PubMed]
     [Google Scholar]
  14. Browning S. R., Mason G. L., Seward T., Green M., Eliason G. A., Mathiason C., Miller M. W., Williams E. S., Hoover E., Telling G. C. 2004; Transmission of prions from mule deer and elk with chronic wasting disease to transgenic mice expressing cervid PrP. J Virol 78:13345–13350 [View Article][PubMed]
     [Google Scholar]
  15. Bruce M. E., Fraser H. 1991; Scrapie strain variation and its implications. Curr Top Microbiol Immunol 172:125–138[PubMed]
     [Google Scholar]
  16. Bruce M. E., McConnell I., Fraser H., Dickinson A. G. 1991; The disease characteristics of different strains of scrapie in Sinc congenic mouse lines: implications for the nature of the agent and host control of pathogenesis. J Gen Virol 72:595–603 [View Article][PubMed]
     [Google Scholar]
  17. Bruce M., Chree A., Williams E., Fraser H. 2000; Perivascular PrP amyloid in the brains of mice infected with chronic wasting disease. Brain Pathol 10:662–663
     [Google Scholar]
  18. Buschmann A., Biacabe A. G., Ziegler U., Bencsik A., Madec J. Y., Erhardt G., Lühken G., Baron T., Groschup M. H. 2004; Atypical scrapie cases in Germany and France are identified by discrepant reaction patterns in BSE rapid tests. J Virol Methods 117:27–36 [View Article][PubMed]
     [Google Scholar]
  19. Casalone C., Zanusso G., Acutis P., Ferrari S., Capucci L., Tagliavini F., Monaco S., Caramelli M. 2004; Identification of a second bovine amyloidotic spongiform encephalopathy: molecular similarities with sporadic Creutzfeldt–Jakob disease. Proc Natl Acad Sci U S A 101:3065–3070 [View Article][PubMed]
     [Google Scholar]
  20. Everest S. J., Thorne L., Barnicle D. A., Edwards J. C., Elliott H., Jackman R., Hope J. 2006; Atypical prion protein in sheep brain collected during the British scrapie-surveillance programme. J Gen Virol 87:471–477 [View Article][PubMed]
     [Google Scholar]
  21. Farquhar C. F., Dornan J., Somerville R. A., Tunstall A. M., Hope J. 1994; Effect of Sinc genotype, agent isolate and route of infection on the accumulation of protease-resistant PrP in non-central nervous system tissues during the development of murine scrapie. J Gen Virol 75:495–504 [View Article][PubMed]
     [Google Scholar]
  22. Féraudet C., Morel N., Simon S., Volland H., Frobert Y., Créminon C., Vilette D., Lehmann S., Grassi J. 2005; Screening of 145 anti-PrP monoclonal antibodies for their capacity to inhibit PrPSc replication in infected cells. J Biol Chem 280:11247–11258 [View Article][PubMed]
     [Google Scholar]
  23. Fraser H., Dickinson A. G. 1973; Scrapie in mice. Agent-strain differences in the distribution and intensity of grey matter vacuolation. J Comp Pathol 83:29–40 [View Article][PubMed]
     [Google Scholar]
  24. Green K. M., Browning S. R., Seward T. S., Jewell J. E., Ross D. L., Green M. A., Williams E. S., Hoover E. A., Telling G. C. 2008; The elk PRNP codon 132 polymorphism controls cervid and scrapie prion propagation. J Gen Virol 89:598–608 [View Article][PubMed]
     [Google Scholar]
  25. Hamir A. N., Cutlip R. C., Miller J. M., Williams E. S., Stack M. J., Miller M. W., O’Rourke K. I., Chaplin M. J. 2001; Preliminary findings on the experimental transmission of chronic wasting disease agent of mule deer to cattle. J Vet Diagn Invest 13:91–96 [View Article][PubMed]
     [Google Scholar]
  26. Hamir A. N., Miller J. M., Cutlip R. C., Stack M. J., Chaplin M. J., Jenny A. L., Williams E. S. 2003; Experimental inoculation of scrapie and chronic wasting disease agents in raccoons (Procyon lotor). Vet Rec 153:121–123 [View Article][PubMed]
     [Google Scholar]
  27. Hamir A. N., Kunkle R. A., Cutlip R. C., Miller J. M., O’Rourke K. I., Williams E. S., Miller M. W., Stack M. J., Chaplin M. J., Richt J. A. 2005; Experimental transmission of chronic wasting disease agent from mule deer to cattle by the intracerebral route. J Vet Diagn Invest 17:276–281 [View Article][PubMed]
     [Google Scholar]
  28. Hamir A. N., Kunkle R. A., Miller J. M., Greenlee J. J., Richt J. A. 2006a; Experimental second passage of chronic wasting disease (CWDmule deer) agent to cattle. J Comp Pathol 134:63–69 [View Article][PubMed]
     [Google Scholar]
  29. Hamir A. N., Gidlewski T., Spraker T. R., Miller J. M., Creekmore L., Crocheck M., Cline T., O’Rourke K. I. 2006b; Preliminary observations of genetic susceptibility of elk (Cervus elaphus nelsoni) to chronic wasting disease by experimental oral inoculation. J Vet Diagn Invest 18:110–114 [View Article][PubMed]
     [Google Scholar]
  30. Hamir A. N., Kunkle R. A., Miller J. M., Cutlip R. C., Richt J. A., Kehrli M. E. Jr, Williams E. S. 2007; Age-related lesions in laboratory-confined raccoons (Procyon lotor) inoculated with the agent of chronic wasting disease of mule deer. J Vet Diagn Invest 19:680–686 [View Article][PubMed]
     [Google Scholar]
  31. Hecker R., Taraboulos A., Scott M., Pan K. M., Yang S. L., Torchia M., Jendroska K., DeArmond S. J., Prusiner S. B. 1992; Replication of distinct scrapie prion isolates is region specific in brains of transgenic mice and hamsters. Genes Dev 6:1213–1228 [View Article][PubMed]
     [Google Scholar]
  32. Heisey D. M., Mickelsen N. A., Schneider J. R., Johnson C. J., Johnson C. J., Langenberg J. A., Bochsler P. N., Keane D. P., Barr D. J. 2010; Chronic wasting disease (CWD) susceptibility of several North American rodents that are sympatric with cervid CWD epidemics. J Virol 84:210–215 [View Article][PubMed]
     [Google Scholar]
  33. Huson H. J., Happ G. M. 2006; Polymorphisms of the prion protein gene (PRNP) in Alaskan moose (Alces alces gigas). Anim Genet 37:425–426 [View Article][PubMed]
     [Google Scholar]
  34. Johnson C., Johnson J., Clayton M., McKenzie D., Aiken J. 2003; Prion protein gene heterogeneity in free-ranging white-tailed deer within the chronic wasting disease affected region of Wisconsin. J Wildl Dis 39:576–581[PubMed] [CrossRef]
     [Google Scholar]
  35. Johnson C., Johnson J., Vanderloo J. P., Keane D., Aiken J. M., McKenzie D. 2006; Prion protein polymorphisms in white-tailed deer influence susceptibility to chronic wasting disease. J Gen Virol 87:2109–2114 [View Article][PubMed]
     [Google Scholar]
  36. Kelly A. C., Mateus-Pinilla N. E., Diffendorfer J., Jewell E., Ruiz M. O., Killefer J., Shelton P., Beissel T., Novakofski J. 2008; Prion sequence polymorphisms and chronic wasting disease resistance in Illinois white-tailed deer (Odocoileus virginianus). Prion 2:28–36 [View Article][PubMed]
     [Google Scholar]
  37. Kim T. Y., Shon H. J., Joo Y. S., Mun U. K., Kang K. S., Lee Y. S. 2005; Additional cases of chronic wasting disease in imported deer in Korea. J Vet Med Sci 67:753–759 [View Article][PubMed]
     [Google Scholar]
  38. Kong Q., Huang S., Zou W., Vanegas D., Wang M., Wu D., Yuan J., Zheng M., Bai H. other authors 2005; Chronic wasting disease of elk: transmissibility to humans examined by transgenic mouse models. J Neurosci 25:7944–7949 [View Article][PubMed]
     [Google Scholar]
  39. Kurt T. D., Telling G. C., Zabel M. D., Hoover E. A. 2009; Trans-species amplification of PrPCWD and correlation with rigid loop 170N. Virology 387:235–243 [View Article][PubMed]
     [Google Scholar]
  40. LaFauci G., Carp R. I., Meeker H. C., Ye X., Kim J. I., Natelli M., Cedeno M., Petersen R. B., Kascsak R., Rubenstein R. 2006; Passage of chronic wasting disease prion into transgenic mice expressing Rocky Mountain elk (Cervus elaphus nelsoni) PrPC. J Gen Virol 87:3773–3780 [View Article][PubMed]
     [Google Scholar]
  41. Lawson V. A., Collins S. J., Masters C. L., Hill A. F. 2005; Prion protein glycosylation. J Neurochem 93:793–801 [View Article][PubMed]
     [Google Scholar]
  42. Marsh R. F., Kincaid A. E., Bessen R. A., Bartz J. C. 2005; Interspecies transmission of chronic wasting disease prions to squirrel monkeys (Saimiri sciureus). J Virol 79:13794–13796 [View Article][PubMed]
     [Google Scholar]
  43. Mathiason C. K., Powers J. G., Dahmes S. J., Osborn D. A., Miller K. V., Warren R. J., Mason G. L., Hays S. A., Hayes-Klug J. other authors 2006; Infectious prions in the saliva and blood of deer with chronic wasting disease. Science 314:133–136 [View Article][PubMed]
     [Google Scholar]
  44. Mathiason C. K., Hays S. A., Powers J., Hayes-Klug J., Langenberg J., Dahmes S. J., Osborn D. A., Miller K. V., Warren R. J. other authors 2009; Infectious prions in pre-clinical deer and transmission of chronic wasting disease solely by environmental exposure. PLoS ONE 4:e5916 [View Article][PubMed]
     [Google Scholar]
  45. McLean I. W., Nakane P. K. 1974; Periodate-lysine-paraformaldehyde fixative. A new fixation for immunoelectron microscopy. J Histochem Cytochem 22:1077–1083 [View Article][PubMed]
     [Google Scholar]
  46. O’Rourke K. I., Besser T. E., Miller M. W., Cline T. F., Spraker T. R., Jenny A. L., Wild M. A., Zebarth G. L., Williams E. S. 1999; PrP genotypes of captive and free-ranging Rocky Mountain elk (Cervus elaphus nelsoni) with chronic wasting disease. J Gen Virol 80:2765–2769[PubMed]
     [Google Scholar]
  47. O’Rourke K. I., Spraker T. R., Hamburg L. K., Besser T. E., Brayton K. A., Knowles D. P. 2004; Polymorphisms in the prion precursor functional gene but not the pseudogene are associated with susceptibility to chronic wasting disease in white-tailed deer. J Gen Virol 85:1339–1346 [View Article][PubMed]
     [Google Scholar]
  48. O’Rourke K. I., Spraker T. R., Zhuang D., Greenlee J. J., Gidlewski T. E., Hamir A. N. 2007; Elk with a long incubation prion disease phenotype have a unique PrPd profile. Neuroreport 18:1935–1938 [View Article][PubMed]
     [Google Scholar]
  49. Priola S. A., Lawson V. A. 2001; Glycosylation influences cross-species formation of protease-resistant prion protein. EMBO J 20:6692–6699 [View Article][PubMed]
     [Google Scholar]
  50. Race R. E., Raines A., Baron T. G., Miller M. W., Jenny A., Williams E. S. 2002; Comparison of abnormal prion protein glycoform patterns from transmissible spongiform encephalopathy agent-infected deer, elk, sheep, and cattle. J Virol 76:12365–12368 [View Article][PubMed]
     [Google Scholar]
  51. Raymond G. J., Raymond L. D., Meade-White K. D., Hughson A. G., Favara C., Gardner D., Williams E. S., Miller M. W., Race R. E., Caughey B. 2007; Transmission and adaptation of chronic wasting disease to hamsters and transgenic mice: evidence for strains. J Virol 81:4305–4314 [View Article][PubMed]
     [Google Scholar]
  52. Safar J. G., Lessard P., Tamgüney G., Freyman Y., Deering C., Letessier F., Dearmond S. J., Prusiner S. B. 2008; Transmission and detection of prions in feces. J Infect Dis 198:81–89 [View Article][PubMed]
     [Google Scholar]
  53. Schutt C. R., Bartz J. C. 2008; Prion interference with multiple prion isolates. Prion 2:61–63 [View Article][PubMed]
     [Google Scholar]
  54. Sigurdson C. J. 2008; A prion disease of cervids: chronic wasting disease. Vet Res 39:41 [View Article][PubMed]
     [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 tropism of chronic wasting disease PrPres in mule deer fawns (Odocoileus hemionus). J Gen Virol 80:2757–2764[PubMed]
     [Google Scholar]
  56. Sigurdson C. J., Mathiason C. K., Perrott M. R., Eliason G. A., Spraker T. R., Glatzel M., Manco G., Bartz J. C., Miller M. W., Hoover E. A. 2008; Experimental chronic wasting disease (CWD) in the ferret. J Comp Pathol 138:189–196 [View Article][PubMed]
     [Google Scholar]
  57. Sohn H. J., Kim J. H., Choi K. S., Nah J. J., Joo Y. S., Jean Y. H., Ahn S. W., Kim O. K., Kim D. Y., Balachandran A. 2002; A case of chronic wasting disease in an elk imported to Korea from Canada. J Vet Med Sci 64:855–858 [View Article][PubMed]
     [Google Scholar]
  58. Terry L. A., Marsh S., Ryder S. J., Hawkins S. A., Wells G. A., 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 [View Article][PubMed]
     [Google Scholar]
  59. Thielen C., Mélot F., Jolois O., Leclercq F., Tsunoda R., Frobert Y., Heinen E., Antoine N. 2001; Isolation of bovine follicular dendritic cells allows the demonstration of a particular cellular prion protein. Cell Tissue Res 306:49–55 [View Article][PubMed]
     [Google Scholar]
  60. Wadsworth J. D., Joiner S., Hill A. F., Campbell T. A., Desbruslais M., Luthert P. J., Collinge J. 2001; Tissue distribution of protease resistant prion protein in variant Creutzfeldt–Jakob disease using a highly sensitive immunoblotting assay. Lancet 358:171–180 [View Article][PubMed]
     [Google Scholar]
  61. Williams E. S. 2005; Chronic wasting disease. Vet Pathol 42:530–549 [View Article][PubMed]
     [Google Scholar]
  62. Williams E. S., Miller M. W. 2002; Chronic wasting disease in deer and elk in North America. Rev Sci Tech 21:305–316[PubMed]
     [Google Scholar]
  63. Williams E. S., Young S. 1980; Chronic wasting disease of captive mule deer: a spongiform encephalopathy. J Wildl Dis 16:89–98[PubMed] [CrossRef]
     [Google Scholar]
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Evidence for distinct chronic wasting disease (CWD) strains in experimental CWD in ferrets
J. Gen. Virol. 93, 212 (2012); https://doi.org/10.1099/vir.0.035006-0
/content/journal/jgv/10.1099/vir.0.035006-0
/content/journal/jgv/10.1099/vir.0.035006-0
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