Protease-sensitive conformers in broad spectrum of distinct prp sc structures in sporadic creutzfeldt-jakob disease are indicator of progression rate

PLoS Pathogens

Volumn 7, Issue 9, 2011, Pages

  Kim, Chae ^a   Haldiman, Tracy ^a   Cohen, Yvonne ^a   Chen, Wei ^a   Blevins, Janis ^a   Sy, Man Sun ^a   Cohen, Mark ^a   Safar, Jiri G ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

METHIONINE; PRION PROTEIN; PROTEINASE; PROTEINASE K; VALINE; EPITOPE; PEPTIDE HYDROLASE; PRNP PROTEIN, HUMAN;

ADULT; AGED; ARTICLE; CODON; CONFORMATION DEPENDENT IMMUNOASSAY; CONTROLLED STUDY; DISEASE COURSE; DISEASE DURATION; DNA POLYMORPHISM; ENZYME CONFORMATION; ENZYME STABILITY; FEMALE; HOMOZYGOSITY; HUMAN; HUMAN TISSUE; IMMUNOASSAY; MALE; PHENOTYPIC VARIATION; PRION; PROTEIN STRUCTURE; SPORADIC CREUTZFELDT JAKOB DISEASE; VIRUS STRAIN; WESTERN BLOTTING; BRAIN; CHEMISTRY; CREUTZFELDT JAKOB DISEASE; GENETICS; HOMOZYGOTE; METABOLISM; MIDDLE AGED; NONLINEAR SYSTEM; PATHOLOGY; PHENOTYPE; REGRESSION ANALYSIS;

AGED; AGED, 80 AND OVER; BRAIN; CODON; CREUTZFELDT-JAKOB SYNDROME; DISEASE PROGRESSION; EPITOPES; FEMALE; HOMOZYGOTE; HUMANS; MALE; METHIONINE; MIDDLE AGED; NONLINEAR DYNAMICS; PEPTIDE HYDROLASES; PHENOTYPE; PRIONS; PRPSC PROTEINS; REGRESSION ANALYSIS; VALINE;

EID: 80053451037     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002242     Document Type: Article

References (78)

1. Gajdusek DC, Gibbs CJ Jr, Alpers M, (1966) Experimental transmission of a kuru-like syndrome to chimpanzees. Nature 209: 794-796.
2. Prusiner SB, Scott MR, DeArmond SJ, Carlson G, (2004) Transmission and replication of prions. In: Prusiner SB, editors. Prion Biology and Diseases. 2nd ed Cold Spring Harbor Cold Spring Harbor Laboratory Press pp. 187-242.
3. Masters CL, Gajdusek DC, Gibbs CJ Jr, Bernouilli C, Asher DM, (1979) Familial Creutzfeldt-Jakob disease and other familial dementias: an inquiry into possible models of virus-induced familial diseases. In: Prusiner SB, Hadlow WJ, editors. Slow Transmissible Diseases of the Nervous System, Vol 1 New York Academic Press pp. 143-194.
4. Gibbs CJ Jr, Gajdusek DC, Asher DM, Alpers MP, Beck E, et al. (1968) Creutzfeldt-Jakob disease (spongiform encephalopathy): transmission to the chimpanzee. Science 161: 388-389.
5. Prusiner SB, (1982) Novel proteinaceous infectious particles cause scrapie. Science 216: 136-144.
6. Pan K-M, Baldwin M, Nguyen J, Gasset M, Serban A, et al. (1993) Conversion of α-helices into β-sheets features in the formation of the scrapie prion proteins. Proc Natl Acad Sci U S A 90: 10962-10966.
7. Safar J, Roller PP, Gajdusek DC, Gibbs CJ Jr, (1993) Conformational transitions, dissociation, and unfolding of scrapie amyloid (prion) protein. J Biol Chem 268: 20276-20284.
8. Caughey BW, Dong A, Bhat KS, Ernst D, Hayes SF, et al. (1991) Secondary structure analysis of the scrapie-associated protein PrP 27-30 in water by infrared spectroscopy. Biochemistry 30: 7672-7680.
9. Oesch B, Westaway D, Wälchli M, McKinley MP, Kent SBH, et al. (1985) A cellular gene encodes scrapie PrP 27-30 protein. Cell 40: 735-746.
10. Caughey B, Baron GS, Chesebro B, Jeffrey M, (2009) Getting a grip on prions: oligomers, amyloids, and pathological membrane interactions. Annu Rev Biochem 78: 177-204.
11. Cobb NJ, Surewicz WK, (2009) Prion diseases and their biochemical mechanisms. Biochemistry 48: 2574-2585.
12. Kim JI, Cali I, Surewicz K, Kong Q, Raymond GJ, et al. (2010) Mammalian prions generated from bacterially expressed prion protein in the absence of any mammalian cofactors. J Biol Chem 285: 14083-14087.
13. Bessen RA, Marsh RF, (1994) Distinct PrP properties suggest the molecular basis of strain variation in transmissible mink encephalopathy. J Virol 68: 7859-7868.
14. Telling GC, Parchi P, DeArmond SJ, Cortelli P, Montagna P, et al. (1996) Evidence for the conformation of the pathologic isoform of the prion protein enciphering and propagating prion diversity. Science 274: 2079-2082.
15. Safar J, Wille H, Itri V, Groth D, Serban H, et al. (1998) Eight prion strains have PrPSc molecules with different conformations. Nat Med 4: 1157-1165.
16. Peretz D, Scott M, Groth D, Williamson A, Burton D, et al. (2001) Strain-specified relative conformational stability of the scrapie prion protein. Protein Sci 10: 854-863.
17. Li J, Browning S, Mahal SP, Oelschlegel AM, Weissmann C, (2010) Darwinian evolution of prions in cell culture. Science 327: 869-872.
18. Telling GC, (2008) Transgenic mouse models of prion diseases. Methods Mol Biol 459: 249-263.
19. Aguzzi A, Heikenwalder M, (2006) Pathogenesis of prion diseases: current status and future outlook. Nat Rev Microbiol 4: 765-775.
20. Morales R, Abid K, Soto C, (2007) The prion strain phenomenon: molecular basis and unprecedented features. Biochim Biophys Acta 1772: 681-691.
21. Gambetti P, Kong Q, Zou W, Parchi P, Chen SG, (2003) Sporadic and familial CJD: classification and characterisation. Br Med Bull 66: 213-239.
22. Parchi P, Capellari S, Chen SG, Petersen RB, Gambetti P, et al. (1997) Typing prion isoforms. Nature 386: 232-233.
23. Collinge J, Sidle KCL, Meads J, Ironside J, Hill AF, (1996) Molecular analysis of prion strain variation and the aetiology of "new variant" CJD. Nature 383: 685-690.
24. Wadsworth JDF, Hill AF, Joiner S, Jackson GS, Clarke AR, et al. (1999) Strain-specific prion-protein conformation determined by metal ions. Nat Cell Biol 1: 55-59.
25. Zou WQ, Capellari S, Parchi P, Sy MS, Gambetti P, et al. (2003) Identification of novel proteinase K-resistant C-terminal fragments of PrP in Creutzfeldt-Jakob disease. J Biol Chem 278: 40429-40436.
26. Collinge J, Clarke AR, (2007) A general model of prion strains and their pathogenicity. Science 318: 930-936.
27. Hill AF, Desbruslais M, Joiner S, Sidle KCL, Gowland I, et al. (1997) The same prion strain causes vCJD and BSE. Nature 389: 448-450.
28. Monari L, Chen SG, Brown P, Parchi P, Petersen RB, et al. (1994) Fatal familial insomnia and familial Creutzfeldt-Jakob disease: different prion proteins determined by a DNA polymorphism. Proc Natl Acad Sci U S A 91: 2839-2842.
29. Parchi P, Castellani R, Capellari S, Ghetti B, Young K, et al. (1996) Molecular basis of phenotypic variability in sporadic Creutzfeldt-Jakob disease. Ann Neurol 39: 767-778.
30. Safar JG, Geschwind MD, Deering C, Didorenko S, Sattavat M, et al. (2005) Diagnosis of human prion disease. Proc Natl Acad Sci U S A 102: 3501-3506.
31. Uro-Coste E, Cassard H, Simon S, Lugan S, Bilheude JM, et al. (2008) Beyond PrP9res) type 1/type 2 dichotomy in Creutzfeldt-Jakob disease. PLoS Pathog 4: e1000029.
32. Polymenidou M, Stoeck K, Glatzel M, Vey M, Bellon A, et al. (2005) Coexistence of multiple PrPSc types in individuals with Creutzfeldt-Jakob disease. Lancet Neurol 4: 805-814.
33. Puoti G, Giaccone G, Rossi G, Canciani B, Bugiani O, et al. (1999) Sporadic Creutzfeldt-Jakob disease: co-occurrence of different types of PrP(Sc) in the same brain. Neurology 53: 2173-2176.
34. Kovacs GG, Head MW, Hegyi I, Bunn TJ, Flicker H, et al. (2002) Immunohistochemistry for the prion protein: comparison of different monoclonal antibodies in human prion disease subtypes. Brain Pathol 12: 1-11.
35. Head MW, Bunn TJ, Bishop MT, McLoughlin V, Lowrie S, et al. (2004) Prion protein heterogeneity in sporadic but not variant Creutzfeldt-Jakob disease: UK cases 1991-2002. Ann Neurol 55: 851-859.
36. Lewis V, Hill AF, Klug GM, Boyd A, Masters CL, et al. (2005) Australian sporadic CJD analysis supports endogenous determinants of molecular-clinical profiles. Neurology 65: 113-118.
37. Schoch G, Seeger H, Bogousslavsky J, Tolnay M, Janzer RC, et al. (2006) Analysis of prion strains by PrPSc profiling in sporadic Creutzfeldt-Jakob disease. PLoS Med 3: e14.
38. Cali I, Castellani R, Alshekhlee A, Cohen Y, Blevins J, et al. (2009) Co-existence of scrapie prion protein types 1 and 2 in sporadic Creutzfeldt-Jakob disease: its effect on the phenotype and prion-type characteristics. Brain 132: 2643-2658.
39. Cronier S, Gros N, Tattum MH, Jackson GS, Clarke AR, et al. (2008) Detection and characterization of proteinase K-sensitive disease-related prion protein with thermolysin. Biochem J 416: 297-305.
40. Safar JG, DeArmond SJ, Kociuba K, Deering C, Didorenko S, et al. (2005) Prion clearance in bigenic mice. J Gen Virol 86: 2913-2923.
41. Safar JG, Scott M, Monaghan J, Deering C, Didorenko S, et al. (2002) Measuring prions causing bovine spongiform encephalopathy or chronic wasting disease by immunoassays and transgenic mice. Nat Biotechnol 20: 1147-1150.
42. Shirley BA, eds. (1995) Protein Stability and Folding: Theory and Practice Totowa, New Jersey Humana Press.
43. Safar J, Roller PP, Gajdusek DC, Gibbs CJ Jr, (1994) Scrapie amyloid (prion) protein has the conformational characteristics of an aggregated molten globule folding intermediate. Biochemistry 33: 8375-8383.
44. Pocchiari M, Puopolo M, Croes EA, Budka H, Gelpi E, et al. (2004) Predictors of survival in sporadic Creutzfeldt-Jakob disease and other human transmissible spongiform encephalopathies. Brain 127: 2348-2359.
45. Kascsak RJ, Rubenstein R, Merz PA, Tonna-DeMasi M, Fersko R, et al. (1987) Mouse polyclonal and monoclonal antibody to scrapie-associated fibril proteins. J Virol 61: 3688-3693.
46. Zanusso G, Liu D, Ferrari S, Hegyi I, Yin X, et al. (1998) Prion protein expression in different species: Analysis with a panel of new mAbs. Proc Natl Acad Sci U S A 95: 8812-8816.
47. Choi EM, Geschwind MD, Deering C, Pomeroy K, Kuo A, et al. (2009) Prion proteins in subpopulations of white blood cells from patients with sporadic Creutzfeldt-Jakob disease. Lab Invest 89: 624-635.
48. Bellon A, Seyfert-Brandt W, Lang W, Baron H, Groner A, et al. (2003) Improved conformation-dependent immunoassay: suitability for human prion detection with enhanced sensitivity. J Gen Virol 84: 1921-1925.
49. Thackray AM, Hopkins L, Bujdoso R, (2007) Proteinase K-sensitive disease-associated ovine prion protein revealed by conformation-dependent immunoassay. Biochem J 401: 475-483.
50. Jones M, Peden AH, Yull H, Wight D, Bishop MT, et al. (2009) Human platelets as a substrate source for the in vitro amplification of the abnormal prion protein (PrP) associated with variant Creutzfeldt-Jakob disease. Transfusion 49: 376-384.
51. Tremblay P, Ball HL, Kaneko K, Groth D, Hegde RS, et al. (2004) Mutant PrPSc conformers induced by a synthetic peptide and several prion strains. J Virol 78: 2088-2099.
52. Peretz D, Williamson RA, Matsunaga Y, Serban H, Pinilla C, 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.
53. Glatzel M, Abela E, Maissen M, Aguzzi A, (2003) Extraneural pathologic prion protein in sporadic Creutzfeldt-Jakob disease. N Engl J Med 349: 1812-1820.
54. Wadsworth JD, Joiner S, Hill AF, Campbell TA, Desbruslais M, et al. (2001) Tissue distribution of protease resistant prion protein in variant Creutzfeldt-Jakob disease using a highly sensitive immunoblotting assay. Lancet 358: 171-180.
55. Wille H, Shanmugam M, Murugesu M, Ollesch J, Stubbs G, et al. (2009) Surface charge of polyoxometalates modulates polymerization of the scrapie prion protein. Proc Natl Acad Sci U S A 106: 3740-3745.
56. Notari S, Capellari S, Langeveld J, Giese A, Strammiello R, et al. (2007) A refined method for molecular typing reveals that co-occurrence of PrP(Sc) types in Creutzfeldt-Jakob disease is not the rule. Lab Invest 87: 1103-1112.
57. Wadsworth JD, Hill AF, Beck JA, Collinge J, (2003) Molecular and clinical classification of human prion disease. Br Med Bull 66: 241-254.
58. Notari S, Strammiello R, Capellari S, Giese A, Cescatti M, et al. (2008) Characterization of truncated forms of abnormal prion protein in Creutzfeldt-Jakob disease. J Biol Chem 283: 30557-65.
59. Parchi P, Giese A, Capellari S, Brown P, Schulz-Schaeffer W, et al. (1999) Classification of sporadic Creutzfeldt-Jakob disease based on molecular and phenotypic analysis of 300 subjects. Ann Neurol 46: 224-233.
60. Choi YP, Peden AH, Groner A, Ironside JW, Head MW, (2011) Distinct stability states of disease-associated human prion protein identified by conformation-dependent immunoassay. J Virol 84: 12030-12038.
61. Choi YP, Groner A, Ironside JW, Head MW, (2011) Comparison of the level, distribution and form of disease-associated prion protein in variant and sporadic Creutzfeldt-Jakob diseased brain using conformation-dependent immunoassay and Western blot. J Gen Virol 92: 727-732.
62. Tzaban S, Friedlander G, Schonberger O, Horonchik L, Yedidia Y, et al. (2002) Protease-sensitive scrapie prion protein in aggregates of heterogeneous sizes. Biochemistry 41: 12868-12875.
63. Pirisinu L, Di Bari M, Marcon S, Vaccari G, D'Agostino C, et al. (2011) A new method for the characterization of strain-specific conformational stability of protease-sensitive and protease-resistant PrP. PLoS ONE 5: e12723.
64. Bishop MT, Will RG, Manson JC, (2010) Defining sporadic Creutzfeldt-Jakob disease strains and their transmission properties. Proc Natl Acad Sci U S A 107: 12005-12010.
65. Pastrana MA, Sajnani G, Onisko B, Castilla J, Morales R, et al. (2006) Isolation and characterization of a proteinase K-sensitive PrP(Sc) fraction. Biochemistry 45: 15710-15717.
66. Colby DW, Wain R, Baskakov IV, Legname G, Palmer CG, et al. (2010) Protease-sensitive synthetic prions. PLoS Pathog 6: e1000736.
67. Prusiner SB, (2001) Shattuck Lecture - Neurodegenerative diseases and prions. N Engl J Med 344: 1516-1526.
68. Mallucci GR, White MD, Farmer M, Dickinson A, Khatun H, et al. (2007) Targeting cellular prion protein reverses early cognitive deficits and neurophysiological dysfunction in prion-infected mice. Neuron 53: 325-335.
69. Gambetti P, Dong Z, Yuan J, Xiao X, Zheng M, et al. (2008) A novel human disease with abnormal prion protein sensitive to protease. Ann Neurol 63: 697-708.
70. Jones M, Peden A, Prowse C, Groner A, Manson J, et al. (2007) In vitro amplification and detection of variant Creutzfeldt-Jakob disease PrP(Sc). J Pathol 213: 21-26.
71. Tanaka M, Collins SR, Toyama BH, Weissman JS, (2006) The physical basis of how prion conformations determine strain phenotypes. Nature 442: 585-589.
72. Legname G, Nguyen H-OB, Peretz D, Cohen FE, DeArmond SJ, et al. (2006) Continuum of prion protein structures enciphers a multitude of prion isolate-specified phenotypes. Proc Natl Acad Sci U S A 103: 19105-19110.
73. World Health Organization (1999) WHO infection control guidelines for transmissible spongiform encephalopathies. Geneva.
74. Collins SJ, Sanchez-Juan P, Masters CL, Klug GM, van Duijn C, et al. (2006) Determinants of diagnostic investigation sensitivities across the clinical spectrum of sporadic Creutzfeldt-Jakob disease. Brain 129: 2278-2287.
75. Geschwind MD, Shu H, Haman A, Sejvar JJ, Miller BL, (2008) Rapidly progressive dementia. Ann Neurol 64: 97-108.
76. Parchi P, Zou W, Wang W, Brown P, Capellari S, et al. (2000) Genetic influence on the structural variations of the abnormal prion protein. Proc Natl Acad Sci U S A 97: 10168-10172.
77. Swietnicki W, Morillas M, Chen SG, Gambetti P, Surewicz WK, (2000) Aggregation and fibrillization of the recombinant human prion protein huPrP90-231. Biochemistry 39: 424-431.
78. Safar JG, Wille H, Geschwind MD, Deering C, Latawiec D, et al. (2006) Human prions and plasma lipoproteins. Proc Natl Acad Sci U S A 103: 11312-11317.