Dissociation of prion protein amyloid seeding from transmission of a spongiform encephalopathy

Journal of Virology

Volumn 87, Issue 22, 2013, Pages 12349-12356

  Piccardo, Pedro ^a,b   King, Declan ^b   Telling, Glenn ^c   Manson, Jean C ^b   Barron, Rona M ^b  

^a CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c Veterinary Dentistry and Oral Surgery   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID; BRAIN EXTRACT; PRION PROTEIN; PRION PROTEIN 101L; PRION PROTEIN TSE; PROTEINASE K; UNCLASSIFIED DRUG; PRION;

AMYLOID PLAQUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASYMPTOMATIC DISEASE; BRAIN SPONGIOSIS; CONTROLLED STUDY; CORPUS CALLOSUM; DISEASE CARRIER; DISEASE SEVERITY; DISEASE TRANSMISSION; HOST; INFECTION SENSITIVITY; MOUSE; NONHUMAN; PATHOPHYSIOLOGY; PHENOTYPE; PRION DISEASE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN MISFOLDING; PROTEIN STRUCTURE; SURVIVAL; VALIDITY; ANIMAL; BRAIN; CHEMISTRY; ENZYME IMMUNOASSAY; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; HUMAN; METABOLISM; PATHOLOGY; PRION; TRANSGENIC MOUSE; VIROLOGY; WESTERN BLOTTING;

MUS; MUS MUSCULUS;

AMYLOID; ANIMALS; BLOTTING, WESTERN; BRAIN; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNOENZYME TECHNIQUES; MICE; MICE, TRANSGENIC; PHENOTYPE; PRION DISEASES; PRIONS;

EID: 84886256226     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00673-13     Document Type: Article

References (40)

1. Prusiner S. 1982. Novel proteinaceous infectious particles cause scrapie. Science 216:136-144.
2. McKinley MP, Bolton DC, Prusiner SB. 1983. A protease-resistant protein is a structural component of the scrapie prion. Cell 35:57-62.
3. Beekes M, Baldauf E, Diringer H. 1996. Sequential appearance and accumulation of pathognomonic markers in the central-nervous-system of hamsters orally infected with scrapie. J. Gen. Virol. 77:1925-1934.
4. Lasmezas CI, Deslys J, Robain O, Jaegly A, Beringue V, Peyrin J, Fournier J, Hauw J, Rossier J, Dormont D. 1997. Transmission of the BSE agent to mice in the absence of detectable abnormal prion protein. Science 275:402-405.
5. Chiesa R, Piccardo P, Quaglio E, Drisaldi B, Si-Hoe SL, Takao M, Ghetti B, Harris DA. 2003. Molecular distinction between pathogenic and infectious properties of the prion protein. J. Virol. 77:7611-7622.
6. Barron RM, Campbell SL, King D, Bellon A, Chapman KE, Williamson RA, Manson JC. 2007. High titres of TSE infectivity associated with extremely low levels of PrPSc in vivo. J. Biol. Chem. 282:35878-35886.
7. Piccardo P, Manson JC, King D, Ghetti B, Barron RM. 2007. Accumulation of prion protein in the brain that is not associated with transmissible disease. Proc. Natl. Acad. Sci. U. S. A. 104:4712-4717.
8. Balkema-Buschmann A, Eiden M, Hoffmann C, Kaatz M, Ziegler U, Keller M, Groschup MH. 2011. BSE infectivity in the absence of detectable PrPSc accumulation in the tongue and nasal mucosa of terminally diseased cattle. J. Gen. Virol. 92:467-476.
9. Jeffrey M, McGovern G, Chambers EV, King D, González L, Manson JC, Ghetti B, Piccardo P, Barron RM. 2012. Mechanism of PrP-amyloid formation in mice without transmissible spongiform encephalopathy. Brain Pathol. 22:58-66.
10. Miyazawa K, Emmerling K, Manuelidis L. 2011. High CJD infectivity remains after prion protein is destroyed. J. Cell Biochem. 112:3630-3637.
11. Frost B, Diamond MI. 2010. Prion-like mechanisms in neurodegenerative diseases. Nat. Rev. Neurosci. 11:155-159.
12. Saborio GP, Permanne B, Soto C. 2001. Sensitive detection of pathological prion protein by cyclic amplification of protein misfolding. Nature 411:810-813.
13. Colby DW, Zhang Q, Wang S, Groth D, Legname G, Riesner D, Prusiner SB. 2007. Prion detection by an amyloid seeding assay. Proc. Natl. Acad. Sci. U. S. A. 104:20914-20919.
14. Atarashi R, Wilham JM, Christensen L, Hughson AG, Moore RA, Johnson LM, Onwubiko HA, Priola SA, Caughey B. 2008. Simplified ultrasensitive prion detection by recombinant PrP conversion with shaking. Nat. Methods 5:211-212.
15. Klingeborn M, Race B, Meade-White KD, Chesebro B. 2011. Lower specific infectivity of protease-resistant prion protein generated in cellfree reactions. Proc. Natl. Acad. Sci. U. S. A. 108:E1244-E1253.
16. Makarava N, Kovacs GG, Bocharova O, Savtchenko R, Alexeeva I, Budka H, Rohwer RG, Baskakov IV. 2010. Recombinant prion protein induces a new transmissible prion disease in wild-type animals. Acta Neuropathol. 119:177-187.
17. Raymond GJ, Race B, Hollister JR, Offerdahl DK, Moore RA, Kodali R, Raymond LD, Hughson AG, Rosenke R, Long D, Dorward DW, Baron GS. 2012. Isolation of novel synthetic prion strains by amplification in transgenic mice coexpressing wild-type and anchorless prion proteins. J. Virol. 86:11763-11778.
18. Wang F, Wang X, Yuan C-G, Ma J. 2010. Generating a prion with bacterially expressed recombinant prion protein. Science 327:1132-1135.
19. Ghetti B, Tagliavini F, Kovacs GG, Piccardo P. 2011. Gerstmann-Straussler-Sheinker disease. In Dickinson DW, Weller RO (ed), Neurodegeneration: the molecular pathology of dementia and movement disorders, p 364-377. Blackwell Publishing Ltd., Oxford, United Kingdom.
20. Piccardo P, Dlouhy SR, Lievens PMJ, Young K, Thomas DP, Nochlin D, Dickson DW, Vinters HV, Zimmerman TR, Mackenzie IRA, Kish SJ, Ang LC, De Carli C, Pocchiari M, Brown P, Gibbs CJ, Gajdusek DC, Bugiani O, Ironside J, Tagliavini F, Ghetti B. 1998. Phenotypic variability of Gerstmann-Straussler-Scheinker disease is associated with prion protein heterogeneity. J. Neuropathol. Exp. Neurol. 57:979-988.
21. Parchi P, Chen SG, Brown P, Zou WQ, Capellari S, Budka H, Hainfellner J, Reyes PF, Golden GT, Hauw JJ, Gajdusek DC, Gambetti P. 1998. Different patterns of truncated prion protein fragments correlate with distinct phenotypes in P102L Gerstmann-Straussler-Scheinker disease. Proc. Natl. Acad. Sci. U. S. A. 95:8322-8327.
22. Manson JC, Jamieson E, Baybutt H, Tuzi NL, Barron R, McConnell I, Somerville R, Ironside J, Will R, Sy MS, Melton DW, Hope J, Bostock C. 1999. A single amino acid alteration (101L) introduced into murine PrP dramatically alters incubation time of transmissible spongiform encephalopathy. EMBO J. 18:6855-6864.
23. Nazor KE, Kuhn F, Seward T, Green M, Zwald D, Pürro M, Schmid J, Biffiger K, Power AM, Oesch B, Raeber A, Telling G. 2005. Immunodetection of disease-associated mutant PrP, which accelerates disease in GSS transgenic mice. EMBO J. 24:2472-2480.
24. Fraser H, Dickinson AG. 1967. Distribution of experimentally induced scrapie lesions in the brain. Nature 216:1310-1311.
25. Schmidt ML, Robinson KA, Lee VMY, Trojanowski JQ. 1995. Chemical and immunological heterogeneity of fibrillar amyloid in plaques of Alzheimer's disease and Downs Syndrome brains revealed by confocal microscopy. Am. J. Pathol. 147:503-515.
26. Plinston C, Hart P, Chong A, Hunter N, Foster J, Piccardo P, Manson JC, Barron RM. 2011. Increased susceptibility of human-PrP transgenic mice to bovine spongiform encephalopathy infection following passage in sheep. J. Virol. 85:1174-1181.
27. Tzaban S, Friedlander G, Schonberger O, Horonchik L, Yedidia Y, Shaked G, Gabizon R, Taraboulos A. 2002. Protease-sensitive scrapie prion protein in aggregates of heterogeneous sizes. Biochemistry 41: 12868-12875.
28. Beringue V, Herzog L, Jaumain E, Reine F, Sibille P, Le Dur A, Vilotte JL, Laude H. 2012. Facilitated cross-species transmission of prions in extraneural tissue. Science 335:472-475.
29. Westermark GT, Westermark P. 2010. Prion-like aggregates: infectious agents in human disease. Trends Mol. Med. 16:501-507.
30. Brundin P, Melki R, Kopito R. 2010. Prion-like transmission of protein aggregates in neurodegenerative diseases. Nat. Rev. Mol. Cell Biol. 11: 301-307.
31. de Calignon A, Polydoro M, Suarez-Calvet M, William C, Adamowicz DH, Kopeikina KJ, Pitstick R, Sahara N, Ashe KH, Carlson GA, Spires-Jones TL, Hyman BT. 2012. Propagation of tau pathology in a model of early Alzheimer's disease. Neuron 73:685-697. (Erratum, 76:461.)
32. Makarava N, Kovacs GG, Savtchenko R, Alexeeva I, Budka H, Rohwer RG, Baskakov IV. 2012. Stabilization of a prion strain of synthetic origin requires multiple serial passages. J. Biol. Chem. 287:30205-30214.
33. Chesebro B, Trifilo M, Race R, Meade-White K, Teng C, LaCasse R, Raymond L, Favara C, Baron G, Priola S, Caughey B, Masliah E, Oldstone M. 2005. Anchorless prion protein results in infectious amyloid disease without clinical scrapie. Science 308:1435-1439.
34. Race R, Meade-White K, Raines A, Raymond GJ, Caughey B, Chesebro B. 2002. Subclinical scrapie infection in a resistant species: persistence, replication, and adaptation of infectivity during four passages. J. Infect. Dis. 186:S166-S170.
35. Hill AF, Antoniou M, Collinge J. 1999. Protease-resistant prion protein produced in vitro lacks detectable infectivity. J. Gen. Virol. 80:11-14.
36. Deleault NR, Kascsak R, Geoghegan JC, Supattapone S. 2010. Speciesdependent differences in cofactor utilization for formation of the protease-resistant prion protein in vitro. Biochemistry 49:3928-3934.
37. Silveira JR, Raymond GJ, Hughson AG, Race R, Sim VL, Hayes SF, Caughey B. 2005. The most infectious prion protein particles. Nature 437:257-261.
38. Biasini E, Seegulam ME, Patti BN, Solforosi L, Medrano AZ, Christensen HM, Senatore A, Chiesa R, Williamson RA, Harris DA. 2008. Non-infectious aggregates of the prion protein react with several PrPScdirected antibodies. J. Neurochem. 105:2190-2204.
39. Miller MB, Geoghegan JC, Supattapone S. 2011. Dissociation of infectivity from seeding ability in prions with alternate docking mechanism. PLoS Pathog. 7:e1002128. doi:10.1371/journal.ppat.1002128.
40. Chiesa R, Piccardo P, Biasini E, Ghetti B, Harris DA. 2008. Aggregated, wild-type prion protein causes neurological dysfunction and synaptic abnormalities. J. Neurosci. 28:13258-13267.