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Volume 15, Number 9—September 2009
Research

Susceptibilities of Nonhuman Primates to Chronic Wasting Disease

Brent Race1Comments to Author , Kimberly D. Meade-White1, Michael W. Miller, Kent D. Barbian, Richard Rubenstein, Giuseppe LaFauci, Larisa Cervenakova, Cynthia Favara, Donald Gardner, Dan Long, Michael Parnell, James Striebel, Suzette A. Priola, Anne Ward, Elizabeth S. Williams2, Richard Race3, and Bruce Chesebro3
Author affiliations: Rocky Mountain Laboratories, Hamilton, Montana, USA (B. Race, K.D. Meade-White, K.D. Barbian, C. Favara, D. Gardner, D. Long, M. Parnell, J. Striebel, S.A. Priola, A. Ward, R. Race, B. Chesebro); Colorado Division of Wildlife, Fort Collins, Colorado, USA (M.W. Miller); State University of New York Downstate Medical Center, Brooklyn, New York, USA (R. Rubenstein); New York State Institute for Basic Research in Developmental Disabilities, Staten Island, New York, USA (G. LaFauci); American Red Cross, Rockville, Maryland, USA (L. Cervenakova); University of Wyoming, Laramie, Wyoming, USA (E.S. Williams)

Main Article

Table 4

PrP sequence variability in squirrel monkeys*

Genotype† No. monkeys PrP gene variations‡
Residue 19 No. octapeptide repeats Residue 164
A 16 Leu/Leu 5/5 Lys/Lys
B 5 ND 4/5 Lys/Lys
C 2 Val/Leu 5/5 Lys/Lys
Schätzl 1 Leu/Leu 5/5 Arg/Arg
Schneider 1 ND 4/4 Arg/Arg

*PrP, prion protein; ND, not determined.
†The PrP genes of 23 monkeys were sequenced, and 3 genotypes were found. For easy reference to Tables 1 and 2, they are designated types A, B, and C. Previous squirrel monkey PrP sequences were identified by Schätzl et al. (28) and Schneider et al. (31).
‡Compared with published sequences, PrP genotype variations were seen only at residue 19 (in the signal peptide), residue 164, and in the number of octapeptide repeats.

Main Article

References
  1. Williams  ES, Young  S. Chronic wasting disease of captive mule deer: a spongiform encephalopathy. J Wildl Dis. 1980;16:89–98.PubMedGoogle Scholar
  2. Williams  ES. Chronic wasting disease. Vet Pathol. 2005;42:530–49. DOIPubMedGoogle Scholar
  3. Miller  MW, Williams  ES. Chronic wasting disease of cervids. Curr Top Microbiol Immunol. 2004;284:193–214.PubMedGoogle Scholar
  4. Hamir  AN, Kunkle  RA, Cutlip  RC, Miller  JM, O’Rourke  KI, Williams  ES, Experimental transmission of chronic wasting disease agent from mule deer to cattle by the intracerebral route. J Vet Diagn Invest. 2005;17:276–81.PubMedGoogle Scholar
  5. Hamir  AN, Kunkle  RA, Cutlip  RC, Miller  JM, Williams  ES, Richt  JA. Transmission of chronic wasting disease of mule deer to Suffolk sheep following intracerebral inoculation. J Vet Diagn Invest. 2006;18:558–65.PubMedGoogle Scholar
  6. Sigurdson  CJ, Mathiason  CK, Perrott  MR, Eliason  GA, Spraker  TR, Glatzel  M, Experimental chronic wasting disease (CWD) in the ferret. J Comp Pathol. 2008;138:189–96. DOIPubMedGoogle Scholar
  7. Bartz  JC, Marsh  RF, McKenzie  DI, Aiken  JM. The host range of chronic wasting disease is altered on passage in ferrets. Virology. 1998;251:297–301. DOIPubMedGoogle Scholar
  8. Harrington  RD, Baszler  TV, O’Rourke  KI, Schneider  DA, Spraker  TR, Liggitt  HD, A species barrier limits transmission of chronic wasting disease to mink (Mustela vison). J Gen Virol. 2008;89:1086–96. DOIPubMedGoogle Scholar
  9. Raymond  GJ, Raymond  LD, Meade-White  KD, Hughson  AG, Favara  C, Gardner  D, Transmission and adaptation of chronic wasting disease to hamsters and transgenic mice: evidence for strains. J Virol. 2007;81:4305–14. DOIPubMedGoogle Scholar
  10. Sigurdson  CJ, Manco  G, Schwarz  P, Liberski  P, Hoover  EA, Hornemann  S, Strain fidelity of chronic wasting disease upon murine adaptation. J Virol. 2006;80:12303–11. DOIPubMedGoogle Scholar
  11. Kong  Q, Huang  S, Zou  W, Vanegas  D, Wang  M, Wu  D, Chronic wasting disease of elk: transmissibility to humans examined by transgenic mouse models. J Neurosci. 2005;25:7944–9. DOIPubMedGoogle Scholar
  12. Tamguney  G, Giles  K, Bouzamondo-Bernstein  E, Bosque  PJ, Miller  MW, Safar  J, Transmission of elk and deer prions to transgenic mice. J Virol. 2006;80:9104–14. DOIPubMedGoogle Scholar
  13. Marsh  RF, Kincaid  AE, Bessen  RA, Bartz  JC. Interspecies transmission of chronic wasting disease prions to squirrel monkeys (Saimiri sciureus). J Virol. 2005;79:13794–6. DOIPubMedGoogle Scholar
  14. Brown  P, Gibbs  CJ Jr, Rodgers-Johnson  P, Asher  DM, Sulima  MP, Bacote  A, Human spongiform encephalopathy: the National Institutes of Health series of 300 cases of experimentally transmitted disease. Ann Neurol. 1994;35:513–29. DOIPubMedGoogle Scholar
  15. Williams  L, Brown  P, Ironside  J, Gibson  S, Will  R, Ritchie  D, Clinical, neuropathologial and immunohistochemical features of sporadic and variant forms of Creutzfeldt-Jakob disease in the squirrel monkey (Saimiri scuireus). J Gen Virol. 2007;88:688–95. DOIPubMedGoogle Scholar
  16. Lasmezas  CI, Deslys  JP, Demaimay  R, Adjou  KT, Lamoury  F, Dormont  D, BSE transmission to macaques. Nature. 1996;381:743–4. DOIPubMedGoogle Scholar
  17. Hayasaka  K, Gojobori  T, Horai  S. Molecular phylogeny and evolution of primate mitochondrial DNA. Mol Biol Evol. 1988;5:626–44.PubMedGoogle Scholar
  18. Meade-White  K, Race  B, Trifilo  M, Bossers  A, Favara  C, Lacasse  R, Resistance to chronic wasting disease in transgenic mice expressing a naturally occurring allelic variant of deer prion protein. J Virol. 2007;81:4533–9. DOIPubMedGoogle Scholar
  19. Sigurdson  CJ, Williams  ES, Miller  MW, Spraker  TR, O’Rourke  KI, Hoover  EA. Oral transmission and early lymphoid trophism of chronic wasting disease PrPres in mule deer fawns (Odocoileus hemionus). J Gen Virol. 1999;80:2757–64.PubMedGoogle Scholar
  20. Raymond  GJ, Bossers  A, Raymond  LD, O’Rourke  KI, McHolland  LE, Bryant  PK III, Evidence of a molecular barrier limiting susceptibility of humans, cattle and sheep to chronic wasting disease. EMBO J. 2000;19:4425–30. DOIPubMedGoogle Scholar
  21. Scott  MR, Kohler  R, Foster  D, Prusiner  SB. Chimeric prion protein expression in cultured cells and transgenic mice. Protein Sci. 1992;1:986–97. DOIPubMedGoogle Scholar
  22. Race  BL, Meade-White  KD, Ward  A, Jewell  J, Miller  MW, Williams  ES, Levels of abnormal prion protein in deer and elk with chronic wasting disease. Emerg Infect Dis. 2007;13:824–30.PubMedGoogle Scholar
  23. Kascsak  RJ, Rubenstein  R, Merz  PA, Tonna-DeMasi  M, Fersko  R, Carp  RI, Mouse monoclonal and polyclonal antibody to scrapie-associated fibril proteins. J Virol. 1987;61:3688–93.PubMedGoogle Scholar
  24. Matsunaga  Y, Peretz  D, Williamson  A, Burton  D, Mehlhorn  I, Groth  D, Cryptic epitopes in N–terminally truncated prion protein are exposed in the full-length molecule: dependence of conformation on pH. Proteins. 2001;44:110–8. DOIPubMedGoogle Scholar
  25. Vorberg  I, Buschmann  A, Harmeyer  S, Saalmuller  A, Pfaff  E, Groschup  MH. A novel epitope for the specific detection of exogenous prion proteins in transgenic mice and transfected murine cell lines. Virology. 1999;255:26–31. DOIPubMedGoogle Scholar
  26. Race  B, Meade-White  K, Oldstone  MB, Race  R, Chesebro  B. Detection of prion infectivity in fat tissues of scrapie-infected mice. PLoS Pathog. 2008;4:e1000232. DOIPubMedGoogle Scholar
  27. Kercher  L, Favara  C, Striebel  JF, Lacasse  R, Chesebro  B. Prion protein expression differences in microglia and astroglia influence scrapie-induced neurodegenration in the retina and brain of transgenic mice. J Virol. 2007;81:10340–51. DOIPubMedGoogle Scholar
  28. Schätzl  HM, Da Costa  M, Taylor  L, Cohen  FE, Prusiner  SB. Prion protein variation among primates. J Mol Biol. 1995;245:362–74. DOIPubMedGoogle Scholar
  29. O’Rourke  KI, Spraker  TR, Hamburg  LK, Besser  TE, Brayton  KA, Knowles  DP. Polymorphisms in prion precursor functional gene but not the pseudogene are associated with susceptibility to chronic wasting disease in white-tailed deer. J Gen Virol. 2004;85:1339–46. DOIPubMedGoogle Scholar
  30. Fox  KA, Jewell  JE, Williams  ES, Miller  MW. Patterns of PrPCWD accumulation during the course of chronic wasting disease infection in orally inoculated mule deer (Odocoileus hemionus). J Gen Virol. 2006;87:3451–61. DOIPubMedGoogle Scholar
  31. Schneider  I, Schneider  H, Schneider  MP, Silva  A. The prion protein and New World primate phylogeny. Genet Mol Biol. 2004;27:505–10. DOIGoogle Scholar
  32. Gibbs  CJ Jr, Gajdusek  DC. Experimental subacute spongiform virus encephalopathies in primates and other laboratory animals. Science. 1973;182:67–8. DOIPubMedGoogle Scholar
  33. Spraker  TR, Zink  RR, Cummings  BA, Wild  MA, Miller  MW, O’Rourke  KI. Comparison of histological lesions and immunohistochemical staining of proteinease-resistant prion protein in a naturally occurring spongiform encephalopathy of free-ranging mule deer (Odocoileus hemionus) with those of chronic wasting disease of captive mule deer. Vet Pathol. 2002;39:110–9. DOIPubMedGoogle Scholar
  34. Herzog  C, Riviere  J, Lescoutra-Etchegaray  N, Charbonnier  A, Leblanc  V, Sales  N, PrPTSE distribution in a primate model of variant, sporadic, and iatrogenic Creutzfeldt-Jakob disease. J Virol. 2005;79:14339–45. DOIPubMedGoogle Scholar
  35. Lasmezas  CI, Comoy  E, Hawkins  S, Herzog  C, Mouthon  F, Konold  T, Risk of oral infection with bovine spongiform encephalopathy agent in primates. Lancet. 2005;365:781–3.PubMedGoogle Scholar
  36. Belay  ED, Maddox  RA, Williams  ES, Miller  MW, Gambetti  P, Schonberger  LB. Chronic wasting disease and potential transmission to humans. Emerg Infect Dis. 2004;10:977–84.PubMedGoogle Scholar
  37. Mawhinney  S, Pape  WJ, Forster  JE, Anderson  CA, Bosque  P, Miller  MW. Human prion disease and relative risk associated with chronic wasting disease. Emerg Infect Dis. 2006;12:1527–35.PubMedGoogle Scholar
  38. Anderson  CA, Bosque  P, Filley  CM, Arciniegas  DB, Kleinschmidt-Demasters  BK, Pape  WJ, Colorado surveillance program for chronic wasting disease transmission to humans: lessons from 2 highly suspicious but negative cases. Arch Neurol. 2007;64:439–41. DOIPubMedGoogle Scholar

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1These authors contributed equally to this article.

2Deceased.

3Co-senior authors.

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Page updated: December 07, 2010
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