Co-existence of distinct prion types enables conformational evolution of human PrPSc by competitive selection

Journal of Biological Chemistry

Volumn 288, Issue 41, 2013, Pages 29846-29861

  Haldiman, Tracy ^a   Kim, Chae ^a   Cohen, Yvonne ^a   Chen, Wei ^a   Blevins, Janis ^a   Qing, Liuting ^a   Cohen, Mark L ^a   Langeveld, Jan ^b   Telling, Glenn C ^c   Kong, Qingzhong ^a   Safar, Jiri G ^a  

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

^b WAGENINGEN UNIVERSITY   (Netherlands)

^c Veterinary Dentistry and Oral Surgery   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGGREGATE SIZE; BIOPHYSICAL TECHNIQUES; CONFORMATIONAL STABILITIES; CREUTZFELDT-JAKOB DISEASE; MOLECULAR MECHANISM; NATURAL SELECTION; PRION PROTEIN; PROTEIN MISFOLDING;

MAMMALS; NEURODEGENERATIVE DISEASES; POPULATION STATISTICS;

PROTEINS;

PRION PROTEIN;

ADULT; AGED; ARTICLE; CREUTZFELDT JAKOB DISEASE; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOASSAY; MALE; MOLECULAR MECHANICS; NATURAL SELECTION; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STABILITY; VIRUS REPLICATION;

MOLECULAR EVOLUTION; NEUROBIOLOGY; NEURODEGENERATION; PRIONS; PROTEIN CONFORMATION; SPORADIC CREUTZFELDT-JAKOB DISEASE;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BLOTTING, WESTERN; BRAIN; CREUTZFELDT-JAKOB SYNDROME; EVOLUTION, MOLECULAR; HUMANS; IMMUNOASSAY; MUTATION; PRIONS; PROTEIN CONFORMATION; PROTEIN STABILITY; PRPSC PROTEINS; SELECTION, GENETIC;

EID: 84885597502     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.500108     Document Type: Article

References (66)

1. 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
2. Deleault, N. R., Harris, B. T., Rees, J. R., and Supattapone, S. (2007) Formation of native prions from minimal components in vitro. Proc. Natl. Acad. Sci. U.S.A. 104, 9741-9746
3. Wang, F., Wang, X., Yuan, C. G., and Ma, J. (2010) Generating a prion with bacterially expressed recombinant prion protein. Science 327, 1132-1135
4. Prusiner, S. B. (1982) Novel proteinaceous infectious particles cause scrapie. Science 216, 136-144
5. Safar, J. G. (2012) Molecular pathogenesis of sporadic prion diseases in man. Prion 6, 108-115
6. Safar, J. G. (2012) in Prions and Diseases (Gambetti, P., ed) pp. 161-179, Springer-Verlag, New York
7. Bessen, R. A., and Marsh, R. F. (1994) Distinct PrP properties suggest the molecular basis of strain variation in transmissible mink encephalopathy. J. Virol. 68, 7859-7868
8. Telling, G. C., Parchi, P., DeArmond, S. J., Cortelli, P., Montagna, P., Gabizon, R., Mastrianni, J., Lugaresi, E., Gambetti, P., and Prusiner, S. B. (1996) Evidence for the conformation of the pathologic isoform of the prion protein enciphering and propagating prion diversity. Science 274, 2079-2082
9. Safar, J., and Prusiner, S. B. (1998) Molecular studies of prion diseases. Prog. Brain Res. 117, 421-434
10. Li, J., Browning, S., Mahal, S. P., Oelschlegel, A. M., and Weissmann, C. (2010) Darwinian evolution of prions in cell culture. Science 327, 869-872
11. Makarava, N., Savtchenko, R., and Baskakov, I. V. (2013) Selective amplification of classical and atypical prions using modified protein misfolding cyclic amplification. J. Biol. Chem. 288, 33-41
12. Ghaemmaghami, S., Colby, D. W., Nguyen, H. O., Hayashi, S., Oehler, A., DeArmond, S. J., and Prusiner, S. B. (2013) Convergent replication of mouse synthetic prion strains. Am. J. Pathol. 182, 866-874
13. Colby, D. W., Wain, R., Baskakov, I. V., Legname, G., Palmer, C. G., Nguyen, H. O., Lemus, A., Cohen, F. E., DeArmond, S. J., and Prusiner, S. B. (2010) Protease-sensitive synthetic prions. PLoS Pathog. 6, e1000736
14. Puoti, G., Bizzi, A., Forloni, G., Safar, J. G., Tagliavini, F., and Gambetti, P. (2012) Sporadic human prion diseases: molecular insights and diagnosis. Lancet Neurol. 11, 618-628
15. Kim,C., Haldiman, T., Surewicz, K., Cohen, Y., Chen, W., Blevins, J., Sy, M. S., Cohen, M., Kong, Q., Telling, G. C., Surewicz, W. K., and Safar, J. G. (2012) Small protease-sensitive oligomers of PrP(Sc) in distinct human prions determine conversion rate of PrP(C). PLoS Pathog. 8, e1002835
16. Kim, C., Haldiman, T., Cohen, Y., Chen, W., Blevins, J., Sy, M. S., Cohen, M., and Safar, J. G. (2011) Protease-sensitive conformers in broad spectrum of distinct PrP structures in sporadic Creutzfeldt-Jakob disease are indicators of progression rate. PLoS Pathog. 7, e1002242
17. Uro-Coste, E., Cassard, H., Simon, S., Lugan, S., Bilheude, J. M., Perret-Liaudet, A., Ironside, J. W., Haik, S., Basset-Leobon, C., Lacroux, C., Peoch, K., Streichenberger, N., Langeveld, J., Head, M. W., Grassi, J., Hauw, J. J., Schelcher, F., Delisle, M. B., and Andreoletti, O. (2008) Beyond PrP9res type 1/type 2 dichotomy in Creutzfeldt-Jakob disease. PLoS Pathog. 4, e1000029
18. Yull, H. M., Ritchie, D. L., Langeveld, J. P., van Zijderveld, F. G., Bruce, M. E., Ironside, J. W., and Head, M. W. (2006) Detection of type 1 prion protein in variant Creutzfeldt-Jakob disease. Am. J. Pathol. 168, 151-157
19. Schoch, G., Seeger, H., Bogousslavsky, J., Tolnay, M., Janzer, R. C., Aguzzi, A., and Glatzel, M. (2006) Analysis of prion strains by PrPSc profiling in sporadic Creutzfeldt-Jakob disease. PLoS Med. 3, e14
20. Cali, I., Castellani, R., Alshekhlee, A., Cohen, Y., Blevins, J., Yuan, J., Langeveld, J. P., Parchi, P., Safar, J. G., Zou, W. Q., and Gambetti, P. (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
21. Kobayashi, A., Mizukoshi, K., Iwasaki, Y., Miyata, H., Yoshida, Y., and Kitamoto, T. (2011) Co-occurrence of types 1 and 2 PrP(res) in sporadic Creutzfeldt-Jakob disease MM1. Am. J. Pathol. 178, 1309-1315
22. Parchi, P., Giese, A., Capellari, S., Brown, P., Schulz-Schaeffer, W., Windl, O., Zerr, I., Budka, H., Kopp, N., Piccardo, P., Poser, S., Rojiani, A., Streichemberger, N., Julien, J., Vital, C., Ghetti, B., Gambetti, P., and Kretzschmar, H. (1999) Classification of sporadic Creutzfeldt-Jakob disease based on molecular and phenotypic analysis of 300 subjects. Ann. Neurol. 46, 224-233
23. World Health Organization (1999) in WHO Infection Control Guidelines for Transmissible Spongiform Encephalopathies (Asher, D., and Pocchiari, M., eds) pp. 1-38, World Health Organization Emerging and Other Communicable Diseases, Geneva
24. Collins, S. J., Sanchez-Juan, P., Masters, C. L., Klug, G. M., van Duijn, C., Poleggi, A., Pocchiari, M., Almonti, S., Cuadrado-Corrales, N., de Pedro-Cuesta, J., Budka, H., Gelpi, E., Glatzel, M., Tolnay, M., Hewer, E., Zerr, I., Heinemann, U., Kretszchmar, H. A., Jansen, G. H., Olsen, E., Mitrova, E., Alpérovitch, A., Brandel, J. P., Mackenzie, J., Murray, K., and Will, R. G. (2006) Determinants of diagnostic investigation sensitivities across the clinical spectrum of sporadic Creutzfeldt-Jakob disease. Brain 129, 2278-2287
25. Geschwind, M. D., Shu, H., Haman, A., Sejvar, J. J., and Miller, B. L. (2008) Rapidly progressive dementia. Ann. Neurol. 64, 97-108
26. Parchi, P., Zou, W., Wang, W., Brown, P., Capellari, S., Ghetti, B., Kopp, N., Schulz-Schaeffer, W. J., Kretzschmar, H. A., Head, M. W., Ironside, J. W., Gambetti, P., and Chen, S. G. (2000) Genetic influence on the structural variations of the abnormal prion protein. Proc. Natl. Acad. Sci. U.S.A. 97, 10168-10172
27. Parchi, P., Castellani, R., Capellari, S., Ghetti, B., Young, K., Chen, S. G., Farlow, M., Dickson, D. W., Sima, A. A., Trojanowski, J. Q., Petersen, R. B., and Gambetti, P. (1996) Molecular basis of phenotypic variability in sporadic Creutzfeldt-Jakob disease. Ann. Neurol. 39, 767-778
28. Safar, J. G., Geschwind, M. D., Deering, C., Didorenko, S., Sattavat, M., Sanchez, H., Serban, A., Vey, M., Baron, H., Giles, K., Miller, B. L., Dearmond, S. J., and Prusiner, S. B. (2005) Diagnosis of human prion disease. Proc. Natl. Acad. Sci. U.S.A. 102, 3501-3506
29. Langeveld, J. P., Jacobs, J. G., Erkens, J. H., Bossers, A., van Zijderveld, F. G., and van Keulen, L. J. (2006) Rapid and discriminatory diagnosis of scrapie and BSE in retro-pharyngeal lymph nodes of sheep. BMC Vet. Res. 2, 19
30. Yuan, J., Xiao, X., McGeehan, J., Dong, Z., Cali, I., Fujioka, H., Kong, Q., Kneale, G., Gambetti, P., and Zou, W. Q. (2006) Insoluble aggregates and protease-resistant conformers of prion protein in uninfected human brains. J. Biol. Chem. 281, 34848-34858
31. Choi, E. M., Geschwind, M. D., Deering, C., Pomeroy, K., Kuo, A., Miller, B. L., Safar, J. G., and Prusiner, S. B. (2009) Prion proteins in subpopulations of white blood cells from patients with sporadic Creutzfeldt-Jakob disease. Lab. Invest. 89, 624-635
32. Zanusso, G., Liu, D., Ferrari, S., Hegyi, I., Yin, X., Aguzzi, A., Hornemann, S., Liemann, S., Glockshuber, R., Manson, J. C., Brown, P., Petersen, R. B., Gambetti, P., and Sy, M.-S. (1998) Prion protein expression in different species: Analysis with a panel of new mAbs. Proc. Natl. Acad. Sci. U.S.A. 95, 8812-8816
33. Kascsak, R. J., Rubenstein, R., Merz, P. A., Tonna-DeMasi, M., Fersko, R., Carp, R. I., Wisniewski, H. M., and Diringer, H. (1987) Mouse polyclonal and monoclonal antibody to scrapie-associated fibril proteins. J. Virol. 61, 3688-3693
34. 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
35. Safar, J. G., Lessard, P., Tamgüney, G., Freyman, Y., Deering, C., Letessier, F., Dearmond, S. J., and Prusiner, S. B. (2008) Transmission and detection of prions in feces. J. Infect. Dis. 198, 81-89
36. Safar, J. G., Scott, M., Monaghan, J., Deering, C., Didorenko, S., Vergara, J., Ball, H., Legname, G., Leclerc, E., Solforosi, L., Serban, H., Groth, D., Burton, D. R., Prusiner, S. B., and Williamson, R. A. (2002) Measuring prions causing bovine spongiform encephalopathy or chronic wasting disease by immunoassays and transgenic mice. Nat. Biotechnol. 20, 1147-1150
37. Safar, J., Wille, H., Itri, V., Groth, D., Serban, H., Torchia, M., Cohen, F. E., and Prusiner, S. B. (1998) Eight prion strains have PrPSc molecules with different conformations. Nat. Med. 4, 1157-1165
38. Thackray, A. M., Hopkins, L., and Bujdoso, R. (2007) Proteinase K-sensitive disease-associated ovine prion protein revealed by conformation-dependent immunoassay. Biochem. J. 401, 475-483
39. Bellon, A., Seyfert-Brandt, W., Lang, W., Baron, H., Gröner, A., and Vey, M. (2003) Improved conformation-dependent immunoassay: suitability for human prion detection with enhanced sensitivity. J. Gen. Virol. 84, 1921-1925
40. Choi, Y. P., Gröner, A., Ironside, J. W., and Head, M. W. (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
41. McCutcheon, S., Hunter, N., and Houston, F. (2005) Use of a new immunoassay to measure PrP Sc levels in scrapie-infected sheep brains reveals PrP genotype-specific differences. J. Immunol. Methods 298, 119-128
42. Safar, J. G., Wille, H., Geschwind, M. D., Deering, C., Latawiec, D., Serban, A., King, D. J., Legname, G., Weisgraber, K. H., Mahley, R. W., Miller, B. L., Dearmond, S. J., and Prusiner, S. B. (2006) Human prions and plasma lipoproteins. Proc. Natl. Acad. Sci. U.S.A. 103, 11312-11317
43. Safar, J., Roller, P. P., Gajdusek, D. C., and Gibbs, C. J., Jr. (1993) Conformational transitions, dissociation, and unfolding of scrapie amyloid (prion) protein. J. Biol. Chem. 268, 20276-20284
44. Kong, Q., Huang, S., Zou, W., Vanegas, D., Wang, M., Wu, D., Yuan, J., Zheng, M., Bai, H., Deng, H., Chen, K., Jenny, A. L., O'Rourke, K., Belay, E. D., Schonberger, L. B., Petersen, R. B., Sy, M. S., Chen, S. G., and Gambetti, P. (2005) Chronic wasting disease of elk: transmissibility to humans examined by transgenic mouse models. J. Neurosci. 25, 7944-7999
45. Fischer, M., Rülicke, T., Raeber, A., Sailer, A., Moser, M., Oesch, B., Brandner, S., Aguzzi, A., and Weissmann, C. (1996) Prion protein (PrP) with amino-proximal deletions restoring susceptibility of PrP knockout mice to scrapie. EMBO J. 15, 1255-1264
46. Castilla, J., Morales, R., Saá, P., Barria, M., Gambetti, P., and Soto, C. (2008) Cell-free propagation of prion strains. EMBO J. 27, 2557-2566
47. Notari, S., Capellari, S., Langeveld, J., Giese, A., Strammiello, R., Gambetti, P., Kretzschmar, H. A., and Parchi, P. (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
48. Pocchiari, M., Puopolo, M., Croes, E. A., Budka, H., Gelpi, E., Collins, S., Lewis, V., Sutcliffe, T., Guilivi, A., Delasnerie-Laupretre, N., Brandel, J. P., Alperovitch, A., Zerr, I., Poser, S., Kretzschmar, H. A., Ladogana, A., Rietvald, I., Mitrova, E., Martinez-Martin, P., de Pedro-Cuesta, J., Glatzel, M., Aguzzi, A., Cooper, S., Mackenzie, J., van Duijn, C. M., and Will, R. G. (2004) Predictors of survival in sporadic Creutzfeldt-Jakob disease and other human transmissible spongiform encephalopathies. Brain 127, 2348-2359
49. Gambetti, P., Kong, Q., Zou, W., Parchi, P., and Chen, S. G. (2003) Sporadic and familial CJD: classification and characterisation. Br. Med. Bull. 66, 213-239
50. 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
51. Steensgaard, J., Humphries, S., and Spragg, S. P. (1992) in Preparative Centrifugation: A Practical Approach (Rickwood, D., ed) pp. 187-232, IRL Press at Oxford University Press, Oxford
52. Kimberlin, R. H., and Walker, C. A. (1978) Evidence that the transmission of one source of scrapie agent to hamsters involves separation of agent strains from a mixture. J. Gen. Virol. 39, 487-496
53. Bruce, M. E., and Fraser, H. (1991) Scrapie strain variation and its implications. Curr. Top. Microbiol. Immunol. 172, 125-138
54. Bruce, M. E. (1993) Scrapie strain variation and mutation. Br. Med. Bull. 49, 822-838
55. Bessen, R. A., and Marsh, R. F. (1992) Identification of two biologically distinct strains of transmissible mink encephalopathy in hamsters. J. Gen. Virol. 73, 329-334
56. Bessen, R. A., and Marsh, R. F. (1992) Biochemical and physical properties of the prion protein from two strains of the transmissible mink encephalopathy agent. J. Virol. 66, 2096-2101
57. Scott, M. R., Peretz, D., Nguyen, H.-O., Dearmond, S. J., and Prusiner, S. B. (2005) Transmission barriers for bovine, ovine, and human prions in transgenic mice. J. Virol. 79, 5259-5271
58. Scott,M., Peretz, D., Ridley, R. M., Baker, H. F., DeArmond, S. J., and Prusiner, S. B. (2004) in Prion Biology and Diseases (Prusiner, S. B., ed) 2nd Ed., pp. 435-482, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
59. Bishop, M. T., Will, R. G., and Manson, J. C. (2010) Defining sporadic Creutzfeldt-Jakob disease strains and their transmission properties. Proc. Natl. Acad. Sci. U.S.A. 107, 12005-12010
60. Korth, C., Kaneko, K., Groth, D., Heye, N., Telling, G., Mastrianni, J., Parchi, P., Gambetti, P., Will, R., Ironside, J., Heinrich, C., Tremblay, P., DeArmond, S. J., and Prusiner, S. B. (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
61. Manuelidis, L., and Lu, Z. Y. (2003) Virus-like interference in the latency and prevention of Creutzfeldt-Jakob disease. Proc. Natl. Acad. Sci. U.S.A. 100, 5360-5365
62. Bartz, J. C., Kramer, M. L., Sheehan, M. H., Hutter, J. A., Ayers, J. I., Bessen, R. A., and Kincaid, A. E. (2007) Prion interference is due to a reduction in strain-specific PrPSc levels. J. Virol. 81, 689-697
63. Shikiya, R. A., Ayers, J. I., Schutt, C. R., Kincaid, A. E., and Bartz, J. C. (2010) Coinfecting prion strains compete for a limiting cellular resource. J. Virol. 84, 5706-5714
64. Piro, J. R., Harris, B. T., Nishina, K., Soto, C., Morales, R., Rees, J. R., and Supattapone, S. (2009) Prion protein glycosylation is not required for strain-specific neurotropism. J. Virol. 83, 5321-5328
65. Prusiner, S. B. (2001) Shattuck Lecture-Neurodegenerative diseases and prions. N. Engl. J. Med. 344, 1516-1526
66. Oelschlegel, A. M., and Weissmann, C. (2013) Acquisition of drug resistance and dependence by prions. PLoS Pathog. 9, e1003158