Diagnosing prion diseases: Needs, challenges and hopes

Nature Reviews Microbiology

Volumn 2, Issue 10, 2004, Pages 809-819

  Soto, Claudio ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEIC ACID; PRION PROTEIN;

BRAIN BIOPSY; CLINICAL EXAMINATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUORESCENCE SPECTROSCOPY; GEL ELECTROPHORESIS; GENETIC SCREENING; HISTOPATHOLOGY; HUMAN; IMMUNOASSAY; INFRARED SPECTROSCOPY; INTERMETHOD COMPARISON; NUCLEAR MAGNETIC RESONANCE; PRION DISEASE; PRIORITY JOURNAL; RETROSPECTIVE STUDY; REVIEW; SENSITIVITY AND SPECIFICITY; WESTERN BLOTTING;

ANIMALS; CATTLE; DIAGNOSTIC TESTS, ROUTINE; ENCEPHALOPATHY, BOVINE SPONGIFORM; HUMANS; PRION DISEASES; PROTEIN FOLDING; PRPSC PROTEINS;

EID: 4844220510     PISSN: 17401526     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrmicro1003     Document Type: Review

References (124)

1. Collinge, J. Prion diseases of humans and animals: their causes and molecular basis. Annu. Rev. Neurosci. 24, 519-550 (2001).
2. Prusiner, S. B. Prions. Proc. Natl Acad. Sci. USA 95, 13363-13383 (1998).
3. Johnson, R. T. & Gibbs, C. J. Jr. Creutzfeldt-Jakob disease and related transmissible spongiform encephalopathies. N. Eng. J. Med. 339, 1994-2004 (1998).
4. Will, R. G. et al. A new variant of Creutzfeldt-Jakob disease in the UK. Lancet 347, 921-925 (1996).
5. Collinge, J. Variant Creutzfeldt-Jakob disease. Lancet 354, 317-323 (1999).
6. Bruce, M. E. 'New variant' Creutzfeldt-Jakob disease and bovine spongiform encephalopathy. Nature Med. 6, 258-259 (2000).
7. Scott, M. R. et al. Compelling transgenetic evidence for transmission of bovine spongiform encephalopathy prions to humans. Proc. Natl Acad. Sci. USA 96, 15137-15142 (1999).
8. Balter, M. Infectious diseases. Uncertainties plague projections of vCJD toll. Science 294, 770-771 (2001).
9. Aguzzi, A. Prions and the immune system: a journey through gut, spleen, and nerves. Adv. Immunol. 81, 123-171 (2003).
10. Kimberlin, R. H. & Walker, C. A. Pathogenesis of scrapie in mice after intragastric infection. Virus Res. 12, 213-220 (1989).
11. Banks, W. A., Niehoff, M. L., Adessi, C. & Soto, C. Passage of murine scrapie prion protein across the mouse vascular blood-brain barrier. Biochem. Biophys. Res. Commun. 318, 125-130 (2004).
12. Mestal, R. Putting prions to the test. Science 273, 184-189 (1996).
13. Chesebro, B. BSE and prions: uncertainties about the agent. Science 279, 42-43 (1998).
14. Soto, C. & Castilla, J. The controversial protein-only hypothesis of prion propagation. Nature Med. 10, S63-S67 (2004).
15. Cho, H. J. Is the scrapie agent a virus? Nature 262, 411-412 (1976).
16. Alper, T., Haig, D. A. & Clarke, M. C. The exceptionally small size of the scrapie agent. Biochem. Biophys. Res. Commun. 22, 278-284 (1966).
17. Alper, T. Scrapie agent unlike viruses in size and susceptibility to inactivation by ionizing or ultraviolet radiation. Nature 317, 750 (1985).
18. Bolton, D. C., McKinley, M. P. & Prusiner, S. B. Identification of a protein that purifies with the scrapie prion. Science 218, 1309-1311 (1982).
19. Gabizon, R., McKinley, M. P., Groth, D. & Prusiner, S. B. Immunoaffinity purification and neutralization of scrapie prion infectivity. Proc. Natl Acad. Sci. USA 85, 6617-6621 (1988).
20. Basler, K. et al. Scrapie and cellular PrP isoforms are encoded by the same chromosomal gene. Cell 46, 417-428 (1986).
21. Stahl, N. et al. Structural studies of the scrapie prion protein using mass spectrometry and amino acid sequencing. Biochemistry 32, 1991-2002 (1993).
22. Pan, K. M. et al. Conversion of α-helices into β-sheets features in the formation of scrapie prion poteins. Proc. Natl Acad. Sci. USA 90, 10962-10966 (1993).
23. Cohen, F. E. & Prusiner, S. B. Pathologic conformations of prion proteins. Annu. Rev. Biochem. 67, 793-819 (1998).
24. Caughey, B. et al. Interactions and conversions of prion protein isoforms. Adv. Protein Chem. 57, 139-169 (2001).
25. Kocisko, D. A. et al. Cell-free formation of protease-resistant prion protein. Nature 370, 471-474 (1994).
26. Saborio, G. P., Permanne, B., & Soto, C, Sensitive detection of pathological prion protein by cyclic amplification of protein misfolding. Nature 411, 810-813 (2001).
27. Soto, C., Saborio, G. P. & Anderes, L. Cyclic amplification of protein misfolding: application to prion-related disorders and beyond. Trends Neurosci. 25, 390-394 (2002).
28. Legname, G. et al. Synthetic mammalian prions. Science 305, 673-676 (2004).
29. Brown, P., Cervenakova, L. & Diringer, H. Blood infectivity and the prospects for a diagnostic screening test in Creutzfeldt-Jakob disease. J. Lab. Clin, Med. 137, 5-13 (2001).
30. Collins, S. et al. Recent advances in the pre-mortem diagnosis of Creutzfeldt-Jakob disease. J. Clin. Neurosci. 7, 195-202 (2000).
31. Ingrosso, L., Vetrugno, V., Cardone, F. & Pocchiari, M. Molecular diagnostics of transmissible spongiform encephalopathies. Trends Mol. Med. 8, 273-280 (2002).
32. Kordek, R. The diagnosis of human prion diseases. Folia Neuropathol. 38, 151-160 (2000).
33. Weber, T., Otto, M., Bodemer, M. & Zerr, I. Diagnosis of Creutzfeld-Jakob disease and related human spongiform encephalopathies. Biomed. Pharmacother. 51, 381-387 (1997).
34. Henry, C. & Knight, R. Clinical features of variant Creutzfeldt-Jakob disease. Rev. Med. Virol. 12, 143-150 (2002).
35. Coulthard, A. et al. Quantitative analysis of MRI signal intensity in new variant Crautzfeldt-Jakob disease. Br. J. Radiol. 72, 742-748 (1999).
36. Hill, A. F. et al. Investigation of variant Creutzfeldt-Jakob disease and other human prion diseases with tonsil biopsy samples. Lancet 353, 183-189 (1999).
37. Boellaard, J. W., Brown, P. & Tateishi, J. Gerstmann-Straussler-Scheinker disease - the dilemma of molecular and clinical correlations. Clin. Neuropathol. 18, 271-285 (1999).
38. Ghetti, B. et al. Gerstmann-Straussler-Scheinker disease and the Indiana kindred. Brain Pathol. 5, 61-75 (1995).
39. Cortelli, P., Gambetti, P., Montagna, P. & Lugaresi, E. Fatal familial insomnia: clinical features and molecular genetics. J. Sleep Res. 8, S23-S29 (1999).
40. Jimi, T. et al. High levels of nervous system specific protein in the cerebrospinal fluid in patients with early stage Creutzfeldt-Jakob disease. Clin. Chim. Acta 211, 37 (1992).
41. Hsich, G., Kenney, K., Gibbs, C. J. Jr, Lee, K. H. & Harrington, M. G. The 14-3-3 brain protein in cerebrospinal fluid as a marker for transmissible spongiform encephalopathies. N. Eng. J. Med. 335, 924 (1996).
42. Will, R. G. et al. Diagnosis of new variant Creutzfeldt-Jakob disease. Ann. Neurol. 47, 575-582 (2000).
43. Miele, G., Manson, J. & Clinton, M. A novel erythroid-specific marker of transmissible spongiform encephalopathies. Nature Med. 7, 361-364 (2001).
44. Glock, B. et al. Transcript level of erythroid differentiation-related factor, a candidate surrogate marker for transmissible spongiform encephalopathy diseases in blood, shows a broad range of variation in healthy individuals. Transfusion 43, 1706-1710 (2003).
45. Bird, S. M. European Union's rapid TSE testing in adult cattle and sheep: implementation and results in 2001 and 2002. Stat. Methods Med. Res. 12, 261-278 (2003).
46. Butler, D. Brussels seeks BSE diagnostic test to screen European cattle. Nature 395, 205-206 (1998).
47. Heim, D. & Wilesmirth, J. W. Surveillance of BSE. Arch. Virol. Suppl. 127-133 (2000).
48. Moynagh, J. & Schimmel, H. Tests for BSE evaluated. Bovine spongiform encephalopathy. Nature 400, 105 (1999).
49. Moynagh, J. & Schimmel, H. The evaluation of tests for the diagnosis of transmissible spongiform encephalopathy in bovines. July 8, 1999. Report from the European Commission. [online], (1999).
50. Schimmel, H. et al. The evaluation of five rapid tests for the diagnosis of transmissible spongiform encephalopathy in bovines (2nd study). March 27, 2002. Report from the European Commission. [online], (2002).
51. Sc detection and its use as a rapid surveillance method for the diagnosis of bovine spongiform encephalopathy (BSE). Acta Neuropathol. (Berl.) 98, 437-443 (1999).
52. Oesch, B. et al. Application of prionics Western blotting procedure to screen for BSE in cattle regularly slaughtered at Swiss abattoirs. Arch. Virol. Suppl. 189-195 (2000).
53. Grassi, J. et al. Rapid test for the preclinical postmortem diagnosis of BSE in central nervous system tissue. Vet. Rec. 149, 577-582 (2001).
54. Deslys, J. P. et al. Screening slaughtered cattle for BSE. Nature 409, 476-478 (2001).
55. Sc in brain homogenate. J. Virol. Methods 101, 79-84 (2002).
56. Sc molecules with different conformations. Nature Med. 4, 1157-1165 (1998).
57. Safer, J. G. et al. Measuring prions causing bovine spongiform encephalopathy or chronic wasting disease by immunoassays and transgenic mice. Nature Biotechnol. 20, 1147-1150 (2002).
58. Cousens, S. N., Vynnycky, E., Zeidler, M., Will, R. G. & Smith, P. G. Predicting the CJD epidemic in humans. Nature 385, 197-198 (1997).
59. Schiermeier, Q. Testing times for BSE. Nature 409, 658-659 (2001).
60. Donnelly, C. A., Ferguson, N. M., Ghani, A. C. & Anderson, R. M. Extending backcalculation to analyse BSE data. Stat. Methods Med. Res. 12, 177-190 (2003).
61. Nolen, R. S. Washington state dairy cow nation's first case of BSE. J. Am. Vet. Med. Assoc. 224, 345-346 (2004).
62. Wadsworth, J. D. et al. Tissue distribution of protease resistant prion protein in variant Creutzfeldt-Jakob disease using a highly sensitive immunoblotting assay. Lancet 358, 171-180 (2001).
63. Brown,P. et al. Iatrogenic, Creutzfeldt-Jakob disease at the millennium. Neurology 55, 1075-1081 (2000).
64. Llewelyn,C. A. et al. Possible transmission of variant Creutzfeldt-Jakob disease by blood transfusion. Lancet 363, 417-421 (2004).
65. Houston, F., Foster, J. D., Chong, A., Hunter, N. & Bostock, C. J. Transmission of BSE by blood transfusion in sheep. Lancet 356, 999-1000 (2000).
66. Hunter, N. et al. Transmission of prion diseases by blood transfusion. J. Gen. Virol. 83, 2897-2905 (2002).
67. Brown, P. et al. Further studies of blood infectivity in an experimental model of transmissible spongiform encephalopathy, with an explanation of why blood components do not transmit Creutzfeldt-Jakob disease in humans. Transfusion 39, 1169-1178 (1999).
68. Aguzzi, A., Glatzel, M., Montrasio, F., Prinz, M. & Heppner, F. L. Interventional strategies against prion diseases. Nature Rev. Neurosci. 2, 745-749 (2001).
69. Dormont, D. Approaches to prophylaxis and therapy. Br. Med. Bull. 66, 281-292 (2003).
70. Rossi, G., Salmona, M., Forloni, G., Bugiani, O. & Tagliavini, F. Therapeutic approaches to prion diseases. Clin. Lab. Men. 23, 187-208 (2003).
71. Field, E. J. & Shenton, B. K. Rapid diagnosis of scrapie in the mouse. Nature 240, 104-106 (1972).
72. Baron, T. Mouse models of prion disease transmission. Trends Mol. Med. 8, 495-500 (2002).
73. res in BSE-infected bovine PrP transgenic mice. Arch. Virol 148, 677-691 (2003).
74. c. Arch. Virol. Suppl. 75-86 (2000).
75. Sc in scrapie-infected hamster brain is spatially and temporally related to histopathology and infectivity titer. Prog. Clin. Biol. Res. 317, 601-618 (1989).
76. Aguzzi, A. Prion diseases, blood and the immune system: concerns and reality. Haematologica 85, 3-10 (2000).
77. Brown, P. The risk of blood-borne Creutzfeldt-Jakob disease. Dev. Biol. Stand. 102, 53-59 (2000).
78. Hill, A. F., Zeidler, M., Ironside, J. & Collinge, J. Diagnosis of new variant Creutzfeldt-Jakob disease by tonsil biopsy. Lancet 349, 99-100 (1997).
79. Schreuder, B. E., van Keulen, L. J., Vromans, M. E., Langeveld, J. P. & Smits, M. A. Preclinical test for prion diseases. Nature 381, 563 (1996).
80. Hilton, D. A., Fathers, E., Edwards, P., Ironside, J. W. & Zajicek. J. Prion immunoreactivity in appendix before clinical onset of variant Creutzfeldt-Jakob disease. Lancet 352, 703-704 (1998).
81. Hilton, D. A. et al. Prevalence of lymphoreticular prion protein accumulation in UK tissue samples. J. Pathol. 203, 733-739 (2004).
82. Glatzel, M., Abela, E., Maissen, M. & Aguzzi, A. Extraneural pathologic prion protein in sporadic Creutzfeldt-Jakob disease. N. Engl. J. Med. 349, 1812-1820 (2003).
83. Zanusso, G. et al. Detection of pathologic prion protein in the olfactory epithelium in sporadic Creutzfeldt-Jakob disease. N. Engl. J. Med. 348, 711-719 (2003).
84. Shaked, G. M. et al. A protease-resistant prion protein isoform is present in urine of animals and humans affected with prion diseases. J. Biol. Chem. 276, 31479-31482 (2001).
85. Furukawa, H. et al. A pitfall in diagnosis of human prion diseases using detection of protease-resistant prion protein in urine: contamination with bacterial outer membrane proteins. J. Biol. Chem. 279, 23661-23667 (2004).
86. Groschup, M. H., Harmeyer, S. & Pfaff, E. Antigenic features of prion proteins of sheep and of other mammalian species. J. Immunol. Methods 207, 89-101 (1997).
87. Demart, S. et al. New insight into abnormal prion protein using monoclonal antibodies. Biochem. Biophys. Res. Commun. 265, 652-657 (1999).
88. Kascsak, R. J., Fersko, R., Pulgiano, D., Rubenstein, R. & Carp, R. I. Immunodiagnosis of prion disease. Immunol. Invest. 26, 259-268 (1997).
89. Sc)-specific epitope defined by a monoclonal antibody. Nature 390, 74-77 (1997).
90. Korth, C., Streit, P. & Oesch, B. Monoclonal antibodies specific for the native, disease-associated isoform of the prion protein. Methods Enzymol. 309, 106-122 (1999).
91. Paramithiotis, E. et al. A prion protein epitope selective for the pathologically misfolded conformation. Nature Med. 9, 893-699 (2003).
92. Curin,S. et al. Monoclonal antibody against a peptide of human prion protein discriminates between Creutzfeldt-Jacob's disease-affected and normal brain tissue. J. Biol. Chem. 279, 3694-3698 (2004).
93. Zou, W. Q., Zheng, J., Gray, D. M., Gambetti, P., & Chen, S. G. Antibody to DNA detects scrapie but not normal prion protein. Proc. Natl Acad. Sci. USA 101, 1380-1385 (2004).
94. Sc by multi-spectral ultraviolet fluorescence. Biochem. Biophys. Res. Commun. 246, 100-106 (1998).
95. Bieschke, J. et al. Ultrasensitive detection of pathological prion protein aggregates by dual-color scanning for intensely fluorescent targets. Proc. Natl Acad. Sci. USA 97, 5468-5473 (2000).
96. Lasch, P. et al. Ante-mortem identification of bovine spongiform encephalopathy from serum using infrared spectroscopy. Anal. Chem. 75, 6673-6678 (2003).
97. Kneipp, J., Lasch, P., Baldauf, E., Beekes, M. & Naumann, D. Detection of pathological molecular alterations in scrapie-infected hamster brain by Fourier transform infrared (FT-IR) spectroscopy. Biochim. Biophys. Acta 1501, 189-199 (2000).
98. Kneipp, J., Beekes, M., Lasch, P. & Naumann, D. Molecular changes of preclinical scrapie can be detected by infrared spectroscopy J. Neurosci. 22, 2989-2997 (2002).
99. Schmerr, M. J. & Jenny, A. A diagnostic test for scrapie-infected sheep using a capillary electrophoresis immunoassay with fluorescent-labeled peptides. Electrophoresis 19, 409-414 (1998).
100. Schmerr, M. J. et al. Use of capillary electrophoresis and fluorescent labeled peptides to detect the abnormal prion protein in the blood of animals that are infected with a transmissible spongiform encephalopathy. J. Chromatogr. A 853, 207-214 (1999).
101. Jackman, R. & Schmerr, M. J. Analysis of the performance of antibody capture methods using fluorescent peptides with capillary zone electrophoresis with laser-induced fluorescence. Electrophoresis 24, 892-896 (2003).
102. Cervenakova, L. et al. Failure of immunocompetitive capillary electrophoresis assay to detect disease-specific prion protein in buffy coat from humans and chimpanzees with Creutzfeldt-Jakob disease. Electrophoresis 24, 853-859 (2003).
103. Fischer, M. B., Roeckl, C., Parizek, P., Schwarz, H. P. & Aguzzi, A. Binding of disease-associated prion protein to plasminogen. Nature 408, 479-483 (2000).
104. Maissen, M., Roeckl, C., Glatzel, M., Goldmann, W. & Aguzzi, A. Plasminogen binds to disease-associated prion protein of multiple species. Lancet 357, 2026-2028 (2001).
105. Kornblatt, J. A. et al. The fate of the prion protein in the prior/plasminogen complex. Biochem. Biophys. Res. Commun. 305, 518-522 (2003).
106. Shaked, Y., Engelstein, R. & Gabizon, R. The binding of prion proteins to serum components is affected by detergent extraction conditions. J. Neurochem. 82, 1-5 (2002).
107. 2-terminal fragment PrP 23-110. Thromb. Haemost. 89, 812-819 (2003).
108. Akowitz, A., Sklaviadis, T. & Manuelidis, L. Endogenous viral complexes with long RNA cosediment with the agent of Creutzfeldt-Jakob disease. Nucleic Acids Res. 22, 1101-1107 (1994).
109. Deleault, N. R., Lucassen, R. W. & Supattapone, S. RNA molecules stimulate prion protein conversion. Nature 425, 717-720 (2003).
110. Gabus, C. et al. The prion protein has RNA binding and chaperoning properties characteristic of nucleocapsid protein NCP7 of HIV-1. J. Biol. Chem. 276, 19301-19309 (2001).
111. Weiss, S. et al. RNA aptamers specifically interact with the prion protein PrP. J. Virol. 71, 8790-8797 (1997).
112. Rhie, A. et al. Characterization of 2′-fluoro-RNA aptamers that bind preferentially to disease-associated conformations of prion protein and inhibit conversion. J. Biol. Chem. 278, 39697-39705 (2003).
113. Sc formation. Chemibiochem 3, 717-725 (2002).
114. Sayer, N. M. et al. Structural determinants of conformationally selective, prion-binding aptamers. J. Biol. Chem. (2004).
115. Klohn, P. C., Stoltze, L., Flechsig, E., Enari, M. & Weissmann, C. A quantitative, highly sensitive cell-based infectivity assay for mouse scraple prions. Proc. Natl Acad. Sci. USA 100, 11666-11671 (2003).
116. Enari, M., Flechsig, E. & Weissmann, C. Scrapie prion protein accumulation by scrapie-infected neuroblastoma cells abrogated by exposure to a prion protein antibody. Proc. Natl Acad. Sci. USA 98, 9295-9299 (2001).
117. Bosque, P. J. & Prusiner, S. B. Cultured cell sublines highly susceptible to prion infection. J. Virol. 74, 4377-4386 (2000).
118. Vorberg, I., Raines, A., Story, B. & Priola, S. A. Susceptibility of common fibroblast cell lines to transmissible spongiform encephalopathy agents. J. Infect. Dis. 189, 431-439 (2004).
119. Jarrett, J. T. & Lansbury, P. T. Jr. Seeding 'one-dimensional crystallization' of amyloid: a pathogenic mechanism in Alzheimer's disease and scrapie? Cell 73, 1055-1058 (1993).
120. Brown, P. Creutzfeldt-Jakob disease: blood infectivity and screening tests. Semin. Hematol, 38, 2-6 (2001).
121. Brown, P. et al. The distribution of infectivity in blood components and plasma derivatives in experimental models of transmissible spongiform encephalopathy. Transfusion 38, 810-816 (1998).
122. Holada, K. et al. Scrapie infectivity in hamster blood is not associated with platelets. J. Virol. 76, 4649-4650 (2002).
123. Soto, C. Protein misfolding and disease; protein refolding and therapy. FEBS Lett. 498, 204-207 (2001).
124. Carrell, R. W. & Lomas, D. A. Conformational disease. Lancet 350, 134-138 (1997).