The intriguing prion disorders

Cellular and Molecular Life Sciences

Volumn 63, Issue 19-20, 2006, Pages 2342-2351

  Abid, K ^a   Soto, C ^a  

^a UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

Author keywords

Cellular conversion factors; Creutzfeldt Jakob disease; Prion; Transmissible spongiform encephalopathies

Indexed keywords

PRION PROTEIN;

AMYLOIDOSIS; BIOMEDICINE; CARBOXY TERMINAL SEQUENCE; CELL FUNCTION; CELL MEMBRANE; DISEASE TRANSMISSION; ENDOCYTOSIS; HUMAN; INCIDENCE; MUTATION; NERVE DEGENERATION; NEUROPROTECTION; NUCLEAR MAGNETIC RESONANCE; PATHOGENESIS; PRION DISEASE; PROTEIN STRUCTURE; REVIEW;

ANIMALS; HUMANS; MODELS, BIOLOGICAL; PRION DISEASES; PRIONS; PROTEIN FOLDING; PROTEIN ISOFORMS;

EID: 33750442933     PISSN: 1420682X     EISSN: 15691632     Source Type: Journal    
DOI: 10.1007/s00018-006-6140-5     Document Type: Review

References (109)

1. Prusiner, S. B. (1998) Prions. Proc. Natl. Acad. Sci. USA 95, 13363-13383.
2. Collinge, J. (2001) Prion diseases of humans and animals: their causes and molecular basis. Annu. Rev. Neurosci. 24, 519-550.
3. Budka, H., Aguzzi, A., Brown, P., Brucher, J. M., Bugiani, O., Gullotta, F., Haltia, M., Hauw, J. J., Ironside, J. W. and Jellinger, K. (1995) Neuropathological diagnostic criteria for Creutzfeldt-Jakob disease (CJD) and other human spongiform encephalopathies (prion diseases). Brain Pathol. 5, 459-466.
4. Soto, C. (2003) Unfolding the role of protein misfolding in neurodegenerative diseases. Nat. Rev. Neurosci. 4, 49-60.
5. Johnson, R. T. and Gibbs, C. J. Jr (1998) Creutzfeldt-Jakob disease and related transmissible spongiform encephalopathies. N. Engl. J. Med. 339, 1994-2004.
6. Prusiner, S. B. and Scott, M. R. (1997) Genetics of prions. Annu. Rev. Genet. 31, 139-175.
7. Liberski, P. P. and Gajdusek, D. C. (1997) Kuru: forty years later, a historical note. Brain Pathol. 7, 555-560.
8. Goldfarb, L. G. (2002) Kuru: the old epidemic in a new mirror. Microbes. Infect. 4, 875-882.
9. Brown, P., Preece, M., Brandel, J. P., Sato, T., McShane, L., Zerr, I., Fletcher, A., Will, R. G., Pocchiari, M., Cashman, N. R. et al. (2000) Iatrogenic Creutzfeldt-Jakob disease at the millennium. Neurology 55, 1075-1081.
10. Brown, P., Preece, M. A. and Will, R. G. (1992) 'Friendly fire' in medicine: hormones, homografts, and Creutzfeldt-Jakob disease. Lancet 340, 24-27.
11. Will, R. G., Ironside, J. W., Zeidler, M., Cousens, S. N., Estibeiro, K., Alperovitch, A., Poser, S., Pocchiari, M., Hofman, A. and Smith, P. G. (1996) A new variant of Creutzfeldt-Jakob disease in the UK. Lancet 347, 921-925.
12. Cohen, C. H. and Valleron, A. J. (1999) When did bovine spongiform encephalopathy (BSE) start? Implications on the prediction of a new variant of Creutzfeldt-Jakob disease (nvCJD) epidemic. Int. J. Epidemiol. 28, 526-531.
13. Ghani, A. C., Ferguson, N. M., Donnelly, C. A., Hagenaars, T. J. and Anderson, R. M. (1998) Estimation of the number of people incubating variant CJD. Lancet 352, 1353-1354.
14. Will, R. (2004) Variant Creutzfeldt-Jakob disease. Folia Neuropathol. 42 Suppl. A, 77-83.
15. Soto, C. and Castilla, J. (2004) The controversial protein-only hypothesis of prion propagation. Nat. Med. 10, S63-S67.
16. Alper, T., Cramp, W. A., Haig, D. A. and Clarke, M. C. (1967) Does the agent of scrapie replicate without nucleic acid? Nature 214, 764-766.
17. Griffith, J. S. (1967) Self-replication and scrapie. Nature 215, 1043-1044.
18. Prusiner, S. B. (1982) Novel proteinaceous infectious particles cause scrapie. Science 216, 136-144.
19. Oesch, B., Westaway, D., Walchli, M., McKinley, M. P., Kent, S. B., Aebersold, R., Barry, R. A., Tempst, P., Teplow, D. B. and Hood, L. E. (1985) A cellular gene encodes scrapie PrP 27-30 protein. Cell 40, 735-746.
20. Chesebro, B., Race, R., Wehrly, K., Nishio, J., Bloom, M., Lechner, D., Bergstrom, S., Robbins, K., Mayer, L. and Keith, J. M. (1985) Identification of scrapie prion protein-specific mRNA in scrapie-infected and uninfected brain. Nature 315, 331-333.
21. Basler, K., Oesch, B., Scott, M., Westaway, D., Walchli, M., Groth, D. F., McKinley, M. P., Prusiner, S. B. and Weissmann, C. (1986) Scrapie and cellular PrP isoforms are encoded by the same chromosomal gene. Cell 46, 417-428.
22. Stahl, N., Baldwin, M. A., Teplow, D. B., Hood, L., Gibson, B. W., Burlingame, A. L. and Prusiner, S. B. (1993) Structural studies of the scrapie prion protein using mass spectrometry and amino acid sequencing. Biochemistry 32, 1991-2002.
23. Cohen, F. E. and Prusiner, S. B. (1998) Pathologic conformations of prion proteins. Annu. Rev. Biochem. 67, 793-819.
24. Caughey, B. W., Dong, A., Bhat, K. S., Ernst, D., Hayes, S. F. and Caughey, W. S. (1991) Secondary structure analysis of the scrapie-associated protein PrP 27-30 in water by infrared spectroscopy. Biochemistry 30, 7672-7680.
25. Pan, K. M., Baldwin, M., Nguyen, J., Gasset, M., Serban, A., Groth, D., Mehlhorn, I., Huang, Z., Fletterick, R. J., Cohen, F. E. and Prusiner, S. B. (1993) Conversion of alpha-helices into beta-sheets features in the formation of the scrapie prion proteins. Proc. Natl. Acad. Sci. USA 90, 10962-10966.
26. Riek, R., Hornemann, S., Wider, G., Billeter, M., Glockshuber, R. and Wuthrich, K. (1996) NMR structure of the mouse prion protein domain PrP(121-321). Nature 382, 180-182.
27. Hornemann, S., Schorn, C. and Wuthrich, K. (2004) NMR structure of the bovine prion protein isolated from healthy calf brains. EMBO Rep. 5, 1159-1164.
28. Lysek, D. A., Schorn, C., Nivon, L. G., Esteve-Moya, V., Christen, B., Calzolai, L., von Schroetter, C., Fiorito, F., Herrmann, T., Guntert, P. and Wuthrich, K. (2005) Prion protein NMR structures of cats, dogs, pigs, and sheep. Proc. Natl. Acad. Sci. USA 102, 640-645.
29. Gossert, A. D., Bonjour, S., Lysek, D. A., Fiorito, F. and Wuthrich, K. (2005) Prion protein NMR structures of elk and of mouse/elk hybrids. Proc. Natl. Acad. Sci. USA 102, 646-650.
30. Harris, D. A. (2003) Trafficking, turnover and membrane topology of PrP. Br. Med. Bull. 66, 71-85.
31. Zahn, R., Liu, A., Luhrs, T., Riek, R., von Schroetter, C., Lopez, G. F., Billeter, M., Calzolai, L., Wider, G. and Wuthrich, K. (2000) NMR solution structure of the human prion protein. Proc. Natl. Acad. Sci. USA 97, 145-150.
32. Endo, T., Groth, D., Prusiner, S. B. and Kobata, A. (1989) Diversity of oligosaccharide structures linked to asparagines of the scrapie prion protein. Biochemistry 28, 8380-8388.
33. Rudd, P. M., Endo, T., Colominas, C., Groth, D., Wheeler, S. F., Harvey, D. J., Wormald, M. R., Serban, H., Prusiner, S. B., Kobata, A. and Dwek, R. A. (1999) Glycosylation differences between the normal and pathogenic prion protein isoforms. Proc. Natl. Acad. Sci. USA 96, 13044-13049.
34. Lawson, V. A., Collins, S. J., Masters, C. L. and Hill, A. F. (2005) Prion protein glycosylation. J. Neurochem. 93, 793-801.
35. Russelakis-Carneiro, M., Saborio, G. P., Anderes, L. and Soto, C. (2002) Changes in the glycosylation pattern of prion protein in murine scrapie. Implications for the mechanism of neurodegeneration in prion diseases. J. Biol. Chem. 277, 36872-36877.
36. Stahl, N., Borchelt, D. R., Hsiao, K. and Prusiner, S. B. (1987) Scrapie prion protein contains a phosphatidylinositol glycolipid. Cell 51, 229-240.
37. Madore, N., Smith, K. L., Graham, C. H., Jen, A., Brady, K., Hall, S. and Morris, R. (1999) Functionally different GPI proteins are organized in different domains on the neuronal surface. EMBO J. 18, 6917-6926.
38. Vey, M., Pilkuhn, S., Wille, H., Nixon, R., DeArmond, S. J., Smart, E. J., Anderson, R. G., Taraboulos, A. and Prusiner, S. B. (1996) Subcellular colocalization of the cellular and scrapie prion proteins in caveolae-like membranous domains. Proc. Natl. Acad. Sci. USA 93, 14945-14949.
39. Taraboulos, A., Scott, M., Semenov, A., Avrahami, D., Laszlo, L., Prusiner, S. B. and Avraham, D. (1995) Cholesterol depletion and modification of COOH-terminal targeting sequence of the prion protein inhibit formation of the scrapie isoform. J. Cell Biol. 129, 121-132.
40. Sunyach, C., Jen, A., Deng, J., Fitzgerald, K. T., Frobert, Y., Grassi, J., McCaffrey, M. W. and Morris, R. (2003) The mechanism of internalization of glycosylphosphatidylinositol-anchored prion protein. EMBO J. 22, 3591-3601.
41. Harris, D. A., Gorodinsky, A., Lehmann, S., Moulder, K. and Shyng, S. L. (1996) Cell biology of the prion protein. Curr. Top. Microbiol. Immunol. 207, 77-93.
42. Arnold, J. E., Tipler, C., Laszlo, L., Hope, J., Landon, M. and Mayer, R. J. (1995) The abnormal isoform of the prion protein accumulates in late-endosome-like organelles in scrapie-infected mouse brain. J. Pathol. 176, 403-411.
43. McKinley, M. P., Taraboulos, A., Kenaga, L., Serban, D., Stieber, A., DeArmond, S. J., Prusiner, S. B. and Gonatas, N. (1991) Ultrastructural localization of scrapie prion proteins in cytoplasmic vesicles of infected cultured cells. Lab. Invest. 65, 622-630.
44. Bocharova, O. V., Breydo, L., Parfenov, A. S., Salnikov, V. V. and Baskakov, I. V. (2005) In vitro conversion of full-length mammalian prion protein produces amyloid form with physical properties of PrP(Sc). J. Mol. Biol. 346, 645-659.
45. Legname, G., Baskakov, I. V., Nguyen, H. O., Riesner, D., Cohen, F. E., DeArmond, S. J. and Prusiner, S. B. (2004) Synthetic mammalian prions. Science 305, 673-676.
46. Swietnicki, W., Morillas, M., Chen, S. G., Gambetti, P. and Surewicz, W. K. (2000) Aggregation and fibrillization of the recombinant human prion protein huPrP90-231. Biochemistry 39, 424-431.
47. Hetz, C., Maundrell, K. and Soto, C. (2003) Is loss of function of the prion protein the cause of prion disorders? Trends Mol. Med. 9, 237-243.
48. Martins, V. R., Linden, R., Prado, M. A., Walz, R., Sakamoto, A. C., Izquierdo, I. and Brentani, R. R. (2002) Cellular prion protein: on the road for functions. FEBS Lett. 512, 25-28.
49. Hugel, B., Martinez, M. C., Kunzelmann, C., Blattler, T., Aguzzi, A. and Freyssinet, J. M. (2004) Modulation of signal transduction through the cellular prion protein is linked to its incorporation in lipid rafts. Cell Mol. Life Sci. 61, 2998-3007.
50. Mouillet-Richard, S., Ermonval, M., Chebassier, C., Laplanche, J. L., Lehmann, S., Launay, J. M. and Kellermann, O. (2000) Signal transduction through prion protein. Science 289, 1925-1928.
51. Chiarini, L. B., Freitas, A. R., Zanata, S. M., Brentani, R. R., Martins, V. R. and Linden, R. (2002) Cellular prion protein transduces neuroprotective signals. EMBO J. 21, 3317-3326.
52. Brown, D. R. (2002) Copper and prion diseases. Biochem. Soc. Trans. 30, 742-745.
53. Kramer, M. L., Kratzin, H. D., Schmidt, B., Romer, A., Windl, O., Liemann, S., Hornemann, S. and Kretzschmar, H. (2001) Prion protein binds copper within the physiological concentration range. J. Biol. Chem. 276, 16711-16719.
54. Brown, D. R., Qin, K., Herms, J. W., Madlung, A., Manson, J., Strome, R., Fraser, P. E., Kruck, T., von Bohlen, A., Schulz-Schaeffer, W. et al. (1997) The cellular prion protein binds copper in vivo. Nature 390, 684-687.
55. Thackray, A. M., Knight, R., Haswell, S. J., Bujdoso, R. and Brown, D. R. (2002) Metal imbalance and compromised antioxidant function are early changes in prion disease. Biochem. J. 362, 253-258.
56. Wong, B. S., Chen, S. G., Colucci, M., Xie, Z., Pan, T., Liu, T., Li, R., Gambetti, P., Sy, M. S. and Brown, D. R. (2001) Aberrant metal binding by prion protein in human prion disease. J. Neurochem. 78, 1400-1408.
57. Bueler, H., Aguzzi, A., Sailer, A., Greiner, R. A., Autenried, P., Aguet, M. and Weissmann, C. (1993) Mice devoid of PrP are resistant to scrapie. Cell 73, 1339-1347.
58. Bueler, H., Fischer, M., Lang, Y., Bluethmann, H., Lipp, H. P., DeArmond, S. J., Prusiner, S. B., Aguet, M. and Weissmann, C. (1992) Normal development and behaviour of mice lacking the neuronal cell-surface PrP protein. Nature 356, 577-582.
59. Mallucci, G. R., Ratte, S., Asante, E. A., Linehan, J., Gowland, I., Jefferys, J. G. and Collinge, J. (2002) Post-natal knockout of prion protein alters hippocampal CA1 properties, but does not result in neurodegeneration. EMBO J. 21, 202-210.
60. Chesebro, B. (1998) BSE and prions: uncertainties about the agent. Science 279, 42-43.
61. Lehmann, S. and Harris, D. A. (1996) Mutant and infectious prion proteins display common biochemical properties in cultured cells. J. Biol. Chem. 271, 1633-1637.
62. Chiesa, R., Piccardo, P., Ghetti, B. and Harris, D. A. (1998) Neurological illness in transgenic mice expressing a prion protein with an insertional mutation. Neuron 21, 1339-1351.
63. Jackson, G. S., Hosszu, L. L., Power, A., Hill, A. F., Kenney, J., Saibil, H., Craven, C. J., Waltho, J. P., Clarke, A. R. and Collinge, J. (1999) Reversible conversion of monomeric human prion protein between native and fibrilogenic conformations. Science 283, 1935-1937.
64. Baskakov, I. V., Aagaard, C., Mehlhorn, I., Wille, H., Groth, D., Baldwin, M. A., Prusiner, S. B. and Cohen, F. E. (2000) Self-assembly of recombinant prion protein of 106 residues. Biochemistry 39, 2792-2804.
65. Zhang, H., Kaneko, K., Nguyen, J. T., Livshits, T. L., Baldwin, M. A., Cohen, F. E., James, T. L. and Prusiner, S. B. (1995) Conformational transitions in peptides containing two putative alpha-helices of the prion protein. J. Mol. Biol. 250, 514-526.
66. Lee, S. and Eisenberg, D. (2003) Seeded conversion of recombinant prion protein to a disulfide-bonded oligomer by a reduction-oxidation process. Nat. Struct. Biol. 10, 725-730.
67. Westaway, D., DeArmond, S. J., Cayetano-Canlas, J., Groth, D., Foster, D., Yang, S. L., Torchia, M., Carlson, G. A. and Prusiner, S. B. (1994) Degeneration of skeletal muscle, peripheral nerves, and the central nervous system in transgenic mice overexpressing wild-type prion proteins. Cell 76, 117-129.
68. Castilla, J., Gutierrez-Adan, A., Brun, A., Doyle, D., Pintado, B., Ramirez, M. A., Salguero, F. J., Parra, B., Diaz, S. S., Sanchez-Vizcaino, J. M., Rogers, M. and Torres, J. M. (2004) Subclinical bovine spongiform encephalopathy infection in transgenic mice expressing porcine prion protein. J. Neurosci. 24, 5063-5069.
69. Castilla, J., Saá, P., Hetz, C. and Soto, C. (2005) In vitro generation of infectious scrapie prions. Cell 121, 195-206.
70. Narang, H. (2002) A critical review of the nature of the spongiform encephalopathy agent: protein theory versus virus theory. Exp. Biol. Med. (Maywood) 227, 4-19.
71. Manuelidis, L., Sklaviadis, T., Akowitz, A. and Fritch, W. (1995) Viral particles are required for infection in neurodegenerative Creutzfeldt-Jakob disease. Proc. Natl. Acad. Sci. USA 92, 5124-5128.
72. Manuelidis, L., Murdoch, G. and Manuelidis, E. E. (1988) Potential involvement of retroviral elements in human dementias. Ciba Found. Symp. 135, 117-134.
73. Murdoch, G. H., Sklaviadis, T., Manuelidis, E. E. and Manuelidis, L. (1990) Potential retroviral RNAs in Creutzfeldt-Jakob disease. J. Virol. 64, 1477-1486.
74. Akowitz, A., Sklaviadis, T. and Manuelidis, L. (1994) Endogenous viral complexes with long RNA cosediment with the agent of Creutzfeldt-Jakob disease. Nucleic Acids Res. 22, 1101-1107.
75. Akowitz, A., Sklaviadis, T., Manuelidis, E. E. and Manuelidis, L. (1990) Nuclease-resistant polyadenylated RNAs of significant size are detected by PCR in highly purified Creutzfeldt-Jakob disease preparations. Microb. Pathog. 9, 33-45.
76. Weiss, S., Proske, D., Neumann, M., Groschup, M. H., Kretzschmar, H. A., Famulok, M. and Winnacker, E. L. (1997) RNA aptamers specifically interact with the prion protein PrP. J. Virol. 71, 8790-8797.
77. Derrington, E., Gabus, C., Leblanc, P., Chnaidermann, J., Grave, L., Dormont, D., Swietnicki, W., Morillas, M., Marck, D., Nandi, P. and Darlix, J. L. (2002) PrPC has nucleic acid chaperoning properties similar to the nucleocapsid protein of HIV-1. C. R. Acad. Sci. III 325, 17-23.
78. Gabus, C., Derrington, E., Leblanc, P., Chnaiderman, J., Dormont, D., Swietnicki, W., Morillas, M., Surewicz, W. K., Marc, D., Nandi, P. and Darlix, J. L. (2001) The prion protein has RNA binding and chaperoning properties characteristic of nucleocapsid protein NCP7 of HIV-1. J. Biol. Chem. 276, 19301-19309.
79. Safar, J. G., Kellings, K., Serban, A., Groth, D., Cleaver, J. E., Prusiner, S. B. and Riesner, D. (2005) Search for a prion-specific nucleic Acid. J. Virol. 79, 10796-10806.
80. Telling, G. C., Scott, M., Hsiao, K. K., Foster, D., Yang, S. L., Torchia, M., Sidle, K. C., Collinge, J., DeArmond, S. J. and Prusiner, S. B. (1994) Transmission of Creutzfeldt-Jakob disease from humans to transgenic mice expressing chimeric human-mouse prion protein. Proc. Natl. Acad. Sci. USA 91, 9936-9940.
81. Telling, G. C., Scott, M., Mastrianni, J., Gabizon, R., Torchia, M., Cohen, F. E., DeArmond, S. J. and Prusiner, S. B. (1995) Prion propagation in mice expressing human and chimeric PrP transgenes implicates the interaction of cellular PrP with another protein. Cell 83, 79-90.
82. Kaneko, K., Zulianello, L., Scott, M., Cooper, C. M., Wallace, A. C., James, T. L., Cohen, F. E. and Prusiner, S. B. (1997) Evidence for protein X binding to a discontinuous epitope on the cellular prion protein during scrapie prion propagation. Proc. Natl. Acad. Sci. USA 94, 10069-10074.
83. Stephenson, D. A., Chiotti, K., Ebeling, C., Groth, D., DeArmond, S. J., Prusiner, S. B. and Carlson, G. A. (2000) Quantitative trait loci affecting prion incubation time in mice. Genomics 69, 47-53.
84. Saborio, G. P., Soto, C., Kascsak, R. J., Levy, E., Kascsak, R., Harris, D. A. and Frangione, B. (1999) Cell-lysate conversion of prion protein into its protease-resistant isoform suggests the participation of a cellular chaperone. Biochem. Biophys. Res. Commun. 258, 470-475.
85. Deleault, N. R., Geoghegan, J. C., Nishina, K., Kascsak, R., Williamson, R. A. and Supattapone, S. (2005) Protease-resistant prion protein amplification reconstituted with partially purified substrates and synthetic polyanions. J. Biol. Chem. 280, 26873-26879.
86. Enari, M., Flechsig, E. and Weissmann, C. (2001) Scrapie prion protein accumulation by scrapie-infected neuroblastoma cells abrogated by exposure to a priori protein antibody. Proc. Natl. Acad. Sci. USA 98, 9295-9299.
87. Bosque, P. J. and Prusiner, S. B. (2000) Cultured cell sublines highly susceptible to prion infection. J. Virol. 74, 4377-4386.
88. Warner, R. G., Hundt, C., Weiss, S. and Turnbull, J. E. (2002) Identification of the heparan sulfate binding sites in the cellular prion protein. J. Biol. Chem. 277, 18421-18430.
89. Caughey, B. (1994) Protease-resistant PrP accumulation and scrapie agent replication: a role for sulphated glycosaminoglycans? Biochem. Soc. Trans. 22, 163-167.
90. McBride, P. A., Wilson, M. I., Eikelenboom, P., Tunstall, A. and Bruce, M. E. (1998) Heparan sulfate proteoglycan is associated with amyloid plaques and neuroanatomically targeted PrP pathology throughout the incubation period of scrapie-infected mice. Exp. Neurol. 149, 447-454.
91. Ben Zaken, O., Tzaban, S., Tal, Y., Horonchik, L., Esko, J. D., Vlodavsky, I. and Taraboulos, A. (2003) Cellular heparan sulfate participates in the metabolism of prions. J. Biol. Chem. 278, 40041-40049.
92. Adler, Y., Zeiler, B., Kryukov, V., Kascsak, R., Rubenstein, R. and Grossman, A. (2003) Small, highly structured RNAs participate in the conversion of human recombinant PrP(Sen) to PrP(Res) in vitro. J. Mol. Biol. 332, 47-57.
93. Deleault, N. R., Lucassen, R. W. and Supattapone, S. (2003) RNA molecules stimulate prion protein conversion. Nature 425, 717-720.
94. Cordeiro, Y., Machado, F., Juliano, L., Juliano, M. A., Brentani, R. R., Foguel, D. and Silva, J. L. (2001) DNA converts cellular prion protein into the beta-sheet conformation and inhibits prion peptide aggregation. J. Biol. Chem. 276, 49400-49409.
95. Kaneko, K., Vey, M., Scott, M., Pilkuhn, S., Cohen, F. E. and Prusiner, S. B. (1997) COOH-terminal sequence of the cellular prion protein directs subcellular trafficking and controls conversion into the scrapie isoform. Proc. Natl. Acad. Sci. USA 94, 2333-2338.
96. Chesebro, B., Trifilo, M., Race, R., Meade-White, K., Teng, C., LaCasse, R., Raymond, L., Favara, C., Baron, G., Priola, S. et al. (2005) Anchorless prion protein results in infectious amyloid disease without clinical scrapie. Science 308, 1435-1439.
97. McKenzie, D., Bartz, J., Mirwald, J., Olander, D., Marsh, R. and Aiken, J. (1998) Reversibility of scrapie inactivation is enhanced by copper. J. Biol. Chem. 273, 25545-25547.
98. Kuczius, T., Buschmann, A., Zhang, W., Karch, H., Becker, K., Peters, G. and Groschup, M. H. (2004) Cellular prion protein acquires resistance to proteolytic degradation following copper ion binding. Biol. Chem. 385, 739-747.
99. Sigurdsson, E. M., Brown, D. R., Alim, M. A., Scholtzova, H., Carp, R., Meeker, H. C., Prelli, F., Frangione, B. and Wisniewski, T. (2003) Copper chelation delays the onset of prion disease. J. Biol. Chem. 278, 46199-46202.
100. Hijazi, N., Shaked, Y., Rosenmann, H., Ben Hur, T. and Gabizon, R. (2003) Copper binding to PrPC may inhibit prion disease propagation. Brain Res. 993, 192-200.
101. Bocharova, O. V., Breydo, L., Salnikov, V. V. and Baskakov, I. V. (2005) Copper(II) inhibits in vitro conversion of prion protein into amyloid fibrils. Biochemistry 44, 6776-6787.
102. Orem, N. R., Geoghegan, J. C., Deleault, N. R., Kascsak, R. and Supattapone, S. (2006) Copper (II) ions potently inhibit purified PrPres amplification. J. Neurochem. 96, 1409-1415.
103. Jarrett, J. T. and Lansbury, P. T. Jr (1993) Seeding 'one-dimensional crystallization' of amyloid: a pathogenic mechanism in Alzheimer's disease and scrapie? Cell 73, 1055-1058.
104. Kocisko, D. A., Come, J. H., Priola, S. A., Chesebro, B., Raymond, G. J., Lansbury, P. T. and Caughey, B. (1994) Cell-free formation of protease-resistant prion protein. Nature 370, 471-474.
105. Silveira, J. R., Raymond, G. J., Hughson, A. G., Race, R. E., Sim, V. L., Hayes, S. F. and Caughey, B. (2005) The most infectious prion protein particles. Nature 437, 257-261.
106. Caughey, B. and Lansbury, P. T. (2003) Protofibrils, pores, fibrils, and neurodegeneration: separating the responsible protein aggregates from the innocent bystanders. Annu. Rev. Neurosci. 26, 267-298.
107. Apetri, A. C. and Surewicz, W. K. (2003) Atypical effect of salts on the thermodynamic stability of human prion protein. J. Biol. Chem. 278, 22187-22192.
108. Apetri, A. C. and Surewicz, W. K. (2002) Kinetic intermediate in the folding of human prion protein. J. Biol. Chem. 277, 44589-44592.
109. Glockshuber, R. (2001) Folding dynamics and energetics of recombinant prion proteins. Adv. Protein Chem. 57, 83-105.