Correlation of polydispersed prion protein and characteristic pathology in the thalamus in variant Creutzfeldt-Jakob disease: Implication of small oligomeric species

Brain Pathology

Volumn 21, Issue 3, 2011, Pages 298-307

  Choi, Young Pyo ^a   Gröner, Albrecht ^b   Ironside, James W ^a   Head, Mark W ^a,c  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b CSL BEHRING GMBH   (Germany)

^c WESTERN GENERAL HOSPITAL   (United Kingdom)

Author keywords

aggregation state; biochemistry; polydispersal; prion protein; thalamus; variant Creutzfeldt Jakob disease

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; OLIGOMER; PRION PROTEIN; PROTEASE RESISTANT PRION PROTEIN; PROTEINASE K; UNCLASSIFIED DRUG;

AMYLOID PLAQUE; ARTICLE; CELL LOSS; CELL VACUOLE; CEREBELLUM; CLINICAL ARTICLE; CONFORMATION DEPENDENT IMMUNOASSAY; CONTROLLED STUDY; CORRELATION ANALYSIS; FRONTAL CORTEX; GLIOSIS; HUMAN; HUMAN TISSUE; IMMUNOASSAY; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN FOLDING; SEDIMENTATION; SUCROSE DENSITY GRADIENT CENTRIFUGATION; THALAMUS; VARIANT CREUTZFELDT JAKOB DISEASE;

CASE-CONTROL STUDIES; CENTRIFUGATION, DENSITY GRADIENT; CEREBELLUM; CREUTZFELDT-JAKOB SYNDROME; FRONTAL LOBE; GENETIC VARIATION; HUMANS; PROTEIN CONFORMATION; PROTEIN ISOFORMS; PRPC PROTEINS; PRPSC PROTEINS; REFERENCE VALUES; THALAMUS; TISSUE DISTRIBUTION;

EID: 79954611509     PISSN: 10156305     EISSN: 17503639     Source Type: Journal    
DOI: 10.1111/j.1750-3639.2010.00446.x     Document Type: Article

References (60)

1. Aguzzi A, (2009) Cell biology. Beyond the prion principle. Nature 459: 924-925.
2. Bellinger-Kawahara CG, Kempner E, Groth D, Gabizon R, Prusiner SB, (1988) Scrapie prion liposomes and rods exhibit target sizes of 55 000 Da. Virology 164: 537-541.
3. Bellon A, Seyfert-Brandt W, Lang W, Baron H, Gröner A, Vey M, (2003) Improved conformation-dependent immunoassay: suitability for human prion detection with enhanced sensitivity. J Gen Virol 84: 1921-1925. (Pubitemid 36805928)
4. Cali I, Castellani R, Yuan J, Al-Shekhlee A, Cohen ML, Xiao X, et al, (2006) Classification of sporadic Creutzfeldt-Jakob disease revisited. Brain 129: 2266-2277. (Pubitemid 44522113)
5. Caughey B, Kocisko DA, Raymond GJ, Lansbury PT, (1995) Aggregates of scrapie-associated prion protein induce the cell-free conversion of protease-sensitive prion protein to the protease-resistant state. Chem Biol 2: 807-817. (Pubitemid 3014704)
6. DeMarco ML, Daggett V, (2004) From conversion to aggregation: protofibril formation of the prion protein. Proc Natl Acad Sci U S A 101: 2293-2298. (Pubitemid 38269305)
7. Gambetti P, Dong Z, Yuan J, Xiao X, Zheng M, Alshekhlee A, et al, (2008) A novel human disease with abnormal prion protein sensitive to protease. Ann Neurol 63: 697-708. (Pubitemid 351945529)
8. Govaerts C, Wille H, Prusiner SB, Cohen FE, (2004) Evidence for assembly of prions with left-handed beta-helices into trimers. Proc Natl Acad Sci U S A 101: 8342-8347. (Pubitemid 38736577)
9. Guentchev M, Hainfellner JA, Trabattoni GR, Budka H, (1997) Distribution of parvalbumin-immunoreactive neurons in brain correlates with hippocampal and temporal cortical pathology in Creutzfeldt-Jakob disease. J Neuropathol Exp Neurol 56: 1119-1124. (Pubitemid 27430473)
10. Guentchev M, Wanschitz J, Voigtlander T, Flicker H, Budka H, (1999) Selective neuronal vulnerability in human prion diseases. Fatal familial insomnia differs from other types of prion diseases. Am J Pathol 155: 1453-1457.
11. Haass C, Selkoe DJ, (2007) Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid beta-peptide. Nat Rev Mol Cell Biol 8: 101-112. (Pubitemid 46432529)
12. Head MW, Bunn TJ, Bishop MT, McLoughlin V, Lowrie S, McKimmie CS, et al, (2004) Prion protein heterogeneity in sporadic but not variant Creutzfeldt-Jakob disease: UK cases 1991-2002. Ann Neurol 55: 851-859. (Pubitemid 38702581)
13. Hetz CA, Soto C, (2006) Stressing out the ER: a role of the unfolded protein response in prion-related disorders. Curr Mol Med 6: 37-43.
14. Hill AF, Joiner S, Wadsworth JD, Sidle KC, Bell JE, Budka H, et al, (2003) Molecular classification of sporadic Creutzfeldt-Jakob disease. Brain 126: 1333-1346. (Pubitemid 36644379)
15. Ironside JW, Head MW, Bell JE, McCardle L, Will RG, (2000) Laboratory diagnosis of variant Creutzfeldt-Jakob disease. Histopathology 37: 1-9. (Pubitemid 30496729)
16. Ironside JW, Ghetti B, Head MW, Piccardo P, Will RG, (2008) Prion diseases. In: Greenfield's Neuropathology, 8th edn., S Love, DN Louis, DW Ellison, (eds), Chapter 16 pp. 1197-1274. Edward Arnold: London.
17. Kang SW, Rane NS, Kim SJ, Garrison JL, Taunton J, Hegde RS, (2006) Substrate-specific translocational attenuation during ER stress defines a pre-emptive quality control pathway. Cell 127: 999-1013. (Pubitemid 44803063)
18. Kaylor J, Bodner N, Edridge S, Yamin G, Hong DP, Fink AL, (2005) Characterization of oligomeric intermediates in alpha-synuclein fibrillation: FRET studies of Y125W/Y133F/Y136F alpha-synuclein. J Mol Biol 353: 357-372. (Pubitemid 41356722)
19. Kazlauskaite J, Sanghera N, Sylvester I, Venien-Bryan C, Pinheiro TJ, (2003) Structural changes of the prion protein in lipid membranes leading to aggregation and fibrillization. Biochemistry 42: 3295-3304. (Pubitemid 36348638)
20. Klein TR, Kirsch D, Kaufmann R, Riesner D, (1998) Prion rods contain small amounts of two host sphingolipids as revealed by thin-layer chromatography and mass spectrometry. Biol Chem 379: 655-666. (Pubitemid 28327564)
21. Korth C, Kaneko K, Groth D, Heye N, Telling G, Mastrianni J, et al, (2003) Abbreviated incubation times for human prions in mice expressing a chimeric mouse-human prion protein transgene. Proc Natl Acad Sci U S A 100: 4784-4789. (Pubitemid 36457806)
22. Kristiansen M, Deriziotis P, Dimcheff DE, Jackson GS, Ovaa H, Naumann H, et al, (2007) Disease-associated prion protein oligomers inhibit the 26S proteasome. Mol Cell 26: 175-188. (Pubitemid 46617340)
23. Levavasseur E, Laffont-Proust I, Morain E, Faucheux BA, Privat N, Peoc'h K, et al, (2008) Regulating factors of PrP glycosylation in Creutzfeldt-Jakob disease-implications for the dissemination and the diagnosis of human prion strains. PLoS ONE 3: e2786.
24. Llewelyn CA, Hewitt PE, Knight RK, Amar K, Cousins S, Mackenzie J, Will RG, (2004) Possible transmission of variant Creutzfeldt-Jakob disease by blood transmission. Lancet 363: 417-421. (Pubitemid 38210057)
25. Ma J, Lindquist S, (2001) Wild-type PrP and a mutant associated with prion disease are subject to retrograde transport and proteasome degradation. Proc Natl Acad Sci U S A 98: 14955-14960. (Pubitemid 34013951)
26. Ma J, Lindquist S, (2002) Conversion of PrP to a self-perpetuating PrPSc-like conformation in the cytosol. Science 298: 1785-1788. (Pubitemid 35404121)
27. McLean CA, Cherny RA, Fraser FW, Fuller SJ, Smith MJ, Beyreuther K, et al, (1999) Soluble pool of Abeta amyloid as a determinant of severity of neurodegeneration in Alzheimer's disease. Ann Neurol 46: 860-866.
28. Meier P, Genoud N, Prinz M, Maissen M, Rulicke T, Zurbriggen A, et al, (2003) Soluble dimeric prion protein binds PrP(Sc) in vivo and antagonizes prion disease. Cell 113: 49-60. (Pubitemid 36411959)
29. Notari S, Moleres FJ, Hunter SB, Belay ED, Schonberger LB, Cali I, et al, (2010) Multiorgan detection and characterization of protease-resistant prion protein in a case of variant CJD examined in the United States. PLoS ONE 5: e8765.
30. Orsi A, Fioriti L, Chiesa R, Sitia R, (2006) Conditions of endoplasmic reticulum stress favor the accumulation of cytosolic prion protein. J Biol Chem 281: 30431-30438. (Pubitemid 44582099)
31. Pan T, Li R, Kang SC, Wong BS, Wisniewski T, Sy MS, (2004) Epitope scanning reveals gain and loss of strain specific antibody binding epitopes associated with the conversion of normal cellular prion to scrapie prion. J Neurochem 90: 1205-1217. (Pubitemid 39167353)
32. Pan T, Chang B, Wong P, Li C, Li R, Kang SC, et al, (2005) An aggregation-specific enzyme-linked immunosorbent assay: detection of conformational differences between recombinant PrP protein dimers and PrP(Sc) aggregates. J Virol 79: 12355-12364. (Pubitemid 41346097)
33. Pan T, Wong P, Chang B, Li C, Li R, Kang SC, et al, (2005) Biochemical fingerprints of prion infection: accumulations of aberrant full-length and N-terminally truncated PrP species are common features in mouse prion disease. J Virol 79: 934-943. (Pubitemid 40053877)
34. Parchi P, Giese A, Capellari S, Brown P, Schulz-Schaeffer W, Windl O, et al, (1999) Classification of sporadic Creutzfeldt-Jakob disease based on molecular and phenotypic analysis of 300 subjects. Ann Neurol 46: 224-233. (Pubitemid 29382879)
35. Parchi P, Capellari S, Gambetti P, (2000) Intracerebral distribution of the abnormal isoform of the prion protein in sporadic Creutzfeldt-Jakob disease and fatal insomnia. Microsc Res Tech 50: 16-25. (Pubitemid 30497401)
36. Pastrana MA, Sajnani G, Onisko B, Castilla J, Morales R, Soto C, Requena JR, (2006) Isolation and characterization of a proteinase K-sensitive PrPSc fraction. Biochemistry 45: 15710-15717. (Pubitemid 46032491)
37. Peretz D, Williamson RA, Matsunaga Y, Serban H, Pinilla C, Bastidas RB, et al, (1997) A conformational transition at the N terminus of the prion protein features in formation of the scrapie isoform. J Mol Biol 273: 614-622. (Pubitemid 27488803)
38. Polymenidou M, Stoeck K, Glatzel M, Vey M, Bellon A, Aguzzi A, (2005) Coexistence of multiple PrPSc types in individuals with Creutzfeldt-Jakob disease. Lancet Neurol 4: 805-814. (Pubitemid 41619435)
39. Prusiner SB, (1998) Prions. Proc Natl Acad Sci U S A 95: 13363-13383. (Pubitemid 28525623)
40. Prusiner SB, Groth DF, Bildstein C, Masiarz FR, McKinley MP, Cochran SP, (1980) Electrophoretic properties of the scrapie agent in agarose gels. Proc Natl Acad Sci U S A 77: 2984-2988. (Pubitemid 10049862)
41. Prusiner SB, McKinley MP, Bowman KA, Bolton DC, Bendheim PE, Groth DF, Glenner GG, (1983) Scrapie prions aggregate to form amyloid-like birefringent rods. Cell 35: 349-358. (Pubitemid 14202913)
42. Prusiner SB, Scott M, Foster D, Pan KM, Groth D, Mirenda C, et al, (1990) Transgenetic studies implicate interactions between homologous PrP isoforms in scrapie prion replication. Cell 63: 673-686. (Pubitemid 120035041)
43. Rane NS, Kang SW, Chakrabarti O, Feigenbaum L, Hegde RS, (2008) Reduced translocation of nascent prion protein during ER stress contributes to neurodegeneration. Dev Cell 15: 359-370.
44. Ritchie DL, Boyle A, McConnell I, Head MW, Ironside JW, Bruce ME, (2009) Transmissions of variant Creutzfeldt-Jakob disease from brain and lymphoreticular tissue show uniform and conserved bovine spongiform encephalopathy-related phenotypic properties on primary and secondary passage in wild-type mice. J Gen Virol 90: 3075-3082.
45. Safar J, Wille H, Itri V, Groth D, Serban H, Torchia M, et al, (1998) Eight prion strains have PrP(Sc) molecules with different conformations. Nat Med 4: 1157-1165. (Pubitemid 28468829)
46. Safar JG, Geschwind MD, Deering C, Didorenko S, Sattavat M, Sanchez H, et al, (2005) Diagnosis of human prion disease. Proc Natl Acad Sci U S A 102: 3501-3506. (Pubitemid 40328074)
47. Safar JG, Wille H, Geschwind MD, Deering C, Latawiec D, Serban A, et al, (2006) Human prions and plasma lipoproteins. Proc Natl Acad Sci U S A 103: 11312-11317. (Pubitemid 44156514)
48. Silveira JR, Raymond GJ, Hughson AG, Race RE, Sim VL, Hayes SF, Caughey B, (2005) The most infectious prion protein particles. Nature 437: 257-261. (Pubitemid 41294488)
49. Simoneau S, Rezaei H, Sales N, Kaiser-Schulz G, Lefebvre-Roque M, Vidal C, et al, (2007) In vitro and in vivo neurotoxicity of prion protein oligomers. PLoS Pathog 3: e125.
50. Soto C, Estrada L, Castilla J, (2006) Amyloids, prions and the inherent infectious nature of misfolded protein aggregates. Trends Biochem Sci 31: 150-155. (Pubitemid 43357995)
51. Tixador P, Herzog L, Reine F, Jaumain E, Chapuis J, Le DA, et al, (2010) The physical relationship between infectivity and prion protein aggregates is strain-dependent. PLoS Pathog 6: e1000859.
52. Tomic JL, Pensalfini A, Head E, Glabe CG, (2009) Soluble fibrillar oligomer levels are elevated in Alzheimer's disease brain and correlate with cognitive dysfunction. Neurobiol Dis 35: 352-358.
53. Tzaban S, Friedlander G, Schonberger O, Horonchik L, Yedidia Y, Shaked G, et al, (2002) Protease-sensitive scrapie prion protein in aggregates of heterogeneous sizes. Biochemistry 41: 12868-12875. (Pubitemid 35192516)
54. Walsh DM, Klyubin I, Fadeeva JV, Cullen WK, Anwyl R, Wolfe MS, et al, (2002) Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416: 535-539. (Pubitemid 34288854)
55. Wang F, Yang F, Hu Y, Wang X, Wang X, Jin C, Ma J, (2007) Lipid interaction converts prion protein to a PrPSc-like proteinase K-resistant conformation under physiological conditions. Biochemistry 46: 7045-7053. (Pubitemid 46906433)
56. Wang F, Wang X, Yuan CG, Ma J, (2010) Generating a prion with bacterially expressed recombinant prion protein. Science 327: 1132-1135.
57. Will RG, Ironside JW, Zeidler M, Cousens SN, Estibeiro K, Alperovitch A, et al, (1996) A new variant of Creutzfeldt-Jakob disease in the UK. Lancet 347: 921-925. (Pubitemid 26102546)
58. Yuan J, Xiao X, McGeehan J, Dong Z, Cali I, Fujioka H, et al, (2006) Insoluble aggregates and protease-resistant conformers of prion protein in uninfected human brains. J Biol Chem 281: 34848-34858. (Pubitemid 46036524)
59. Yull HM, Ritchie DL, Langeveld JP, van Zijderveld FG, Bruce ME, Ironside JW, Head MW, (2006) Detection of type 1 prion protein in variant Creutzfeldt-Jakob disease. Am J Pathol 168: 151-157. (Pubitemid 43062568)
60. Zeidler M, Sellar RJ, Collie DA, Knight R, Stewart G, Macleod MA, et al, (2000) The pulvinar sign on magnetic resonance imaging in variant Creutzfeldt-Jakob disease. Lancet 355: 1412-1418. (Pubitemid 30215964)