Atypical scrapie prions from sheep and lack of disease in transgenic mice overexpressing human prion protein

Emerging Infectious Diseases

Volumn 19, Issue 11, 2013, Pages 1731-1739

  Wadsworth, Jonathan D F ^a   Joiner, Susan ^a   Linehan, Jacqueline M ^a   Balkema Buschmann, Anne ^b   Spiropoulos, John ^c   Simmons, Marion M ^c   Griffiths, Peter C ^c   Groschup, Martin H ^b   Hope, James ^c   Brandner, Sebastian ^a   Asante, Emmanuel A ^a   Collinge, John ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b Federal Research Institute for Animal Health   (Germany)

^c VETERINARY LABORATORIES AGENCY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

PRION PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; BOVINE SPONGIFORM ENCEPHALOPATHY; BOVINE SPONGIFORM ENCEPHALOPATHY AGENT; CATTLE; CONTROLLED STUDY; CREUTZFELDT JAKOB DISEASE; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; INOCULATION; MOUSE; NONHUMAN; SCRAPIE; SHEEP; SURVIVAL TIME; TRANSGENIC MOUSE; VARIANT CREUTZFELDT JAKOB DISEASE;

ATYPICAL SCRAPIE; BOVINE SPONGIFORM ENCEPHALOPATHY; BSE; NOR98 SCRAPIE; PRION DISEASE; PRION PROTEIN; PRIONS; SCRAPIE; SHEEP BSE; TRANSGENIC MICE; TRANSMISSIBLE SPONGIFORM ENCEPHALOPATHY (TSE); VARIANT CREUTZFELDT-JAKOB DISEASE; VCJD;

ANIMALS; BRAIN; CATTLE; ENCEPHALOPATHY, BOVINE SPONGIFORM; GENE EXPRESSION; HUMANS; MICE; MICE, TRANSGENIC; PRIONS; SCRAPIE; SHEEP; SPECIES SPECIFICITY;

EID: 84886997245     PISSN: 10806040     EISSN: 10806059     Source Type: Journal    
DOI: 10.3201/eid1911.121341     Document Type: Article

References (38)

1. Collinge J, Sidle KC, Meads J, Ironside J, Hill AF. Molecular analysis of prion strain variation and the aetiology of 'new variant' CJD. Nature. 1996; 383: 685-90. http://dx. doi. org/10. 1038/383685a0.
2. Hill AF, Desbruslais M, Joiner S, Sidle KCL, Gowland I, Collinge J. The same prion strain causes vCJD and BSE. Nature. 1997; 389: 448-50. http://dx. doi. org/10. 1038/38925.
3. Bruce ME, Will RG, Ironside JW, McConnell I, Drummond D, Suttie A, et al. Transmissions to mice indicate that 'new variant' CJD is caused by the BSE agent. Nature. 1997; 389: 498-501. http://dx. doi. org/10. 1038/39057.
4. Asante EA, Linehan J, Desbruslais M, Joiner S, Gowland I, Wood A, et al. BSE prions propagate as either variant CJD-like or sporadic CJD-like prion strains in transgenic mice expressing human prion protein. EMBO J. 2002; 21: 6358-66. http://dx. doi. org/10. 1093/emboj/cdf653.
5. Collinge J, Whitfield J, McKintosh E, Beck J, Mead S, Thomas DJ, et al. Kuru in the 21st century-an acquired human prion disease with very long incubation periods. Lancet. 2006; 367: 2068-74. http://dx. doi. org/10. 1016/S0140-6736(06)68930-7.
6. Hilton DA, Ghani AC, Conyers L, Edwards P, McCardle L, Ritchie D, et al. Prevalence of lymphoreticular prion protein accumulation in UK tissue samples. J Pathol. 2004; 203: 733-9. http://dx. doi. org/10. 1002/path. 1580.
7. Clewley JP, Kelly CM, Andrews N, Vogliqi K, Mallinson G, Kaisar M, et al. Prevalence of disease related prion protein in anonymous tonsil specimens in Britain: cross sectional opportunistic survey. BMJ. 2009; 338: b1442. http://dx. doi. org/10. 1136/bmj. b1442.
8. UK Health Protection Agency. Summary results of the second national survey of abnormal prion prevalence in archived appendix specimens. Heath Protection Agency Report. News Archives. 2012; 6: 32 [cited 2012 Aug 10]. http://www. hpa. org. uk/hpr/archives/2012/news3212. htm#bnrmlp.
9. Eloit M, Adjou K, Coulpier M, Fontaine JJ, Hamel R, Lilin T, et al. BSE agent signatures in a goat. Vet Rec. 2005; 156: 523-4.
10. Spiropoulos J, Lockey R, Sallis RE, Terry LA, Thorne L, Holder TM, et al. Isolation of prion with BSE properties from farmed goat. Emerg Infect Dis. 2011; 17: 2253-61. http://dx. doi. org/10. 3201/eid1712. 110333.
11. European Food Safety AuthorityPanel on Biological Hazards (BIOHAZ). Joint scientific opinion on any possible epidemiological or molecular association between TSEs in animals and humans. EFSA Journal. 2011; 9: 1945-2056 [cited 11 Sep 2013]. http://www. efsa. europa. eu/en/publications/efsajournal. htm.
12. Benestad SL, Sarradin P, Thu B, Schonheit J, Tranulis MA, Bratberg B. Cases of scrapie with unusual features in Norway and designation of a new type, Nor98. Vet Rec. 2003; 153: 202-8. http://dx. doi. org/10. 1136/vr. 153. 7. 202.
13. Benestad SL, Arsac JN, Goldmann W, Noremark M. Atypical/Nor98 scrapie: properties of the agent, genetics, and epidemiology. Vet Res. 2008; 39: 19. http://dx. doi. org/10. 1051/vetres: 2007056.
14. Webb PR, Powell L, Denyer M, Marsh S, Weaver C, Simmons MM, et al. A retrospective immunohistochemical study reveals atypical scrapie has existed in the United Kingdom since at least 1987. J Vet Diagn Invest. 2009; 21: 826-9. http://dx. doi. org/10. 1177/104063870902100609.
15. Bruce ME, Nonno R, Foster J, Goldmann W, Di Bari M, Esposito E, et al. Nor98-like sheep scrapie in the United Kingdom in 1989. Vet Rec. 2007; 160: 665-6. http://dx. doi. org/10. 1136/vr. 160. 19. 665.
16. Wadsworth JD, Asante EA, Collinge J. Contribution of transgenic models to understanding human prion disease. Neuropathol Appl Neurobiol. 2010; 36: 576-97. http://dx. doi. org/10. 1111/j. 1365-2990. 2010. 01129. x.
17. Padilla D, Beringue V, Espinosa JC, Andreoletti O, Jaumain E, Reine F, et al. Sheep and goat BSE propagate more efficiently than cattle BSE in human PrP transgenic mice. PLoS Pathog. 2011; 7: e1001319. http://dx. doi. org/10. 1371/journal. ppat. 1001319.
18. Kong Q, Huang S, Zou W, Vanegas D, Wang M, Wu D, et al. Chronic wasting disease of elk: transmissibility to humans examined by transgenic mouse models. J Neurosci. 2005; 25: 7944-9. http://dx. doi. org/10. 1523/JNEUROSCI. 2467-05. 2005.
19. Tamgüney G, Giles K, Bouzamondo-Bernstein E, Bosque PJ, Miller MW, Safar J, et al. Transmission of elk and deer prions to transgenic mice. J Virol. 2006; 80: 9104-14. http://dx. doi. org/10. 1128/JVI. 00098-06.
20. Sandberg MK, Al Doujaily H, Sigurdson CJ, Glatzel M, O'Malley C, Powell C, et al. Chronic wasting disease prions are not transmissible to transgenic mice overexpressing human prion protein. J Gen Virol. 2010; 91: 2651-7. http://dx. doi. org/10. 1099/vir. 0. 024380-0.
21. Thackray AM, Hopkins L, Spiropoulos J, Bujdoso R. Molecular and transmission characteristics of primary passaged ovine scrapie isolates in conventional and ovine PrP transgenic mice. J Virol. 2008; 82: 11197-207. http://dx. doi. org/10. 1128/JVI. 01454-08.
22. Griffiths PC, Spiropoulos J, Lockey R, Tout AC, Jayasena D, Plater JM, et al. Characterisation of atypical scrapie cases from Great Britain in transgenic ovine PrP mice. J Gen Virol. 2010; 91: 2132-8. http://dx. doi. org/10. 1099/vir. 0. 018986-0.
23. Lloyd SE, Linehan J, Desbruslais M, Joiner S, Buckell J, Brandner S, et al. Characterization of two distinct prion strains derived from bovine spongiform encephalopathy transmissions to inbred mice. J Gen Virol. 2004; 85: 2471-8. http://dx. doi. org/10. 1099/vir. 0. 79889-0.
24. Wadsworth JD, Asante EA, Desbruslais M, Linehan J, Joiner S, Gowland I, et al. Human prion protein with valine 129 prevents expression of variant CJD phenotype. Science. 2004; 306: 1793-6. http://dx. doi. org/10. 1126/science. 1103932.
25. Asante EA, Linehan J, Gowland I, Joiner S, Fox K, Cooper S, et al. Dissociation of pathological and molecular phenotype of variant Creutzfeldt-Jakob disease in transgenic human prion protein 129 heterozygous mice. Proc Natl Acad Sci U S A. 2006; 103: 10759-64. http://dx. doi. org/10. 1073/pnas. 0604292103.
26. Wadsworth JD, Joiner S, Linehan JM, Desbruslais M, Fox K, Cooper S, et al. Kuru prions and sporadic Creutzfeldt-Jakob disease prions have equivalent transmission properties in transgenic and wild-type mice. Proc Natl Acad Sci U S A. 2008; 105: 3885-90. http://dx. doi. org/10. 1073/pnas. 0800190105.
27. Wadsworth JD, Powell C, Beck JA, Joiner S, Linehan JM, Brandner S, et al. Molecular diagnosis of human prion disease. Methods Mol Biol. 2008; 459: 197-227. http://dx. doi. org/10. 1007/978-1-59745-234-2_14.
28. Wadsworth JD, Joiner S, Hill AF, Campbell TA, Desbruslais M, Luthert PJ, et al. Tissue distribution of protease resistant prion protein in variant CJD using a highly sensitive immuno-blotting assay. Lancet. 2001; 358: 171-80. http://dx. doi. org/10. 1016/S0140-6736(01)05403-4.
29. Kascsak RJ, Rubenstein R, Merz PA, Tonna DeMasi M, Fersko R, Carp RI, et al. Mouse polyclonal and monoclonal antibody to scrapie-associated fibril proteins. J Virol. 1987; 61: 3688-93.
30. Safar J, Wille H, Itri V, Groth D, Serban H, Torchia M, et al. Eight prion strains have PrPSc molecules with different conformations. Nat Med. 1998; 4: 1157-65. http://dx. doi. org/10. 1038/2654.
31. Gretzschel A, Buschmann A, Eiden M, Ziegler U, Luhken G, Erhardt G, et al. Strain typing of German transmissible spongiform encephalopathies field cases in small ruminants by biochemical methods. J Vet Med B Infect Dis Vet Public Health. 2005; 52: 55-63. http://dx. doi. org/10. 1111/j. 1439-0450. 2005. 00827. x.
32. Gretzschel A, Buschmann A, Langeveld J, Groschup MH. Immunological characterization of abnormal prion protein from atypical scrapie cases in sheep using a panel of monoclonal antibodies. J Gen Virol. 2006; 87: 3715-22. http://dx. doi. org/10. 1099/vir. 0. 81816-0.
33. Hill AF, Joiner S, Wadsworth JD, Sidle KC, Bell JE, Budka H, et al. Molecular classification of sporadic Creutzfeldt-Jakob disease. Brain. 2003; 126: 1333-46. http://dx. doi. org/10. 1093/brain/awg125.
34. Plinston C, Hart P, Chong A, Hunter N, Foster J, Piccardo P, et al. Increased susceptibility of human-PrP transgenic mice to bovine spongiform encephalopathy following passage in sheep. J Virol. 2011; 85: 1174-81. http://dx. doi. org/10. 1128/JVI. 01578-10.
35. Wilson R, Plinston C, Hunter N, Casalone C, Corona C, Tagliavini F, et al. Chronic wasting disease and atypical forms of BSE and scrapie are not transmissible to mice expressing wild-type levels of human PrP. J Gen Virol. 2012; 93: 1624-9. http://dx. doi. org/10. 1099/vir. 0. 042507-0.
36. Bishop MT, Hart P, Aitchison L, Baybutt HN, Plinston C, Thomson V, et al. Predicting susceptibility and incubation time of human-tohuman transmission of vCJD. Lancet Neurol. 2006; 5: 393-8. http://dx. doi. org/10. 1016/S1474-4422(06)70413-6.
37. Götte DR, Benestad SL, Laude H, Zurbriggen A, Oevermann A, Seuberlich T. Atypical scrapie isolates involve a uniform prion species with a complex molecular signature. PLoS ONE. 2011; 6: e27510. http://dx. doi. org/10. 1371/journal. pone. 0027510.
38. Béringue V, Herzog L, Jaumain E, Reine F, Sibille P, Le Dur A, et al. Facilitated cross-species transmission of prions in extraneural tissue. Science. 2012; 335: 472-5. http://dx. doi. org/10. 1126/science. 1215659.