Stabilization of a prion strain of synthetic origin requires multiple serial passages

Journal of Biological Chemistry

Volumn 287, Issue 36, 2012, Pages 30205-30214

  Makarava, Natallia ^a   Kovacs, Gabor G ^b   Savtchenko, Regina ^a   Alexeeva, Irina ^c   Budka, Herbert ^b   Rohwer, Robert G ^a,c   Baskakov, Ilia V ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b MEDICAL UNIVERSITY OF VIENNA   (Austria)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION PROCESS; CLINICAL SIGNS; HIGH DOSE; INCUBATION PERIODS; INOCULA; KEY ATTRIBUTES; LOW DOSE; NEUROPATHOLOGICAL FEATURES; SERIAL TRANSMISSION; TERMINALLY ILL;

TISSUE;

ANIMALS;

PRION PROTEIN;

ADAPTATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN LEVEL; CONTROLLED STUDY; MOLECULAR EVOLUTION; NONHUMAN; PRION; PRION DISEASE; PRIORITY JOURNAL; PROTEIN STRUCTURE; VIRUS CELL INTERACTION; VIRUS STRAIN; VIRUS TRANSMISSION;

ANIMALS; BRAIN; CRICETINAE; PRION DISEASES; PROTEIN STABILITY; PRPSC PROTEINS;

ANIMALIA;

EID: 84865740820     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.392985     Document Type: Article

References (50)

1. Prusiner, S. B. (1998) Prions. Proc. Natl. Acad. Sci. U.S.A. 95, 13363-13383
2. Prusiner, S. B. (1982) Novel proteinaceous infectious particles cause scrapie. Science 216, 136-144
3. 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
4. Wang, F., Wang, X., Yuan, C. G., and Ma, J. (2010) Generating a prion with bacterially expressed recombinant prion protein. Science 327, 1132-1135
5. Ayers, J. I., Schutt, C. R., Shikiya, R. A., Aguzzi, A., Kincaid, A. E., and Bartz, J. C. (2011) The strain-encoded relationship between PrP replication, stability, and processing in neurons is predictive of the incubation period of disease. PLOS Pathog. 7, e1001317
6. Kimberlin, R. H., and Walker, C. (1977) Characteristics of a short incubation model of scrapie in the golden hamster. J. Gen. Virol. 34, 295-304
7. Dickinson, A. G. (1976) Scrapie in sheep and goats. in Slow Virus Diseases of Animals and Man (Kimberlin, R. H. ed.), pp 209-241, North-Holland Publishing, Amsterdam
8. Zlotnik, I. (1963) Experimental transmission of scrapie to golden hamsters. Lancet 282, 1072
9. 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
10. Chandler, R. L. (1963) Experimental scrapie in the mouse. Res. Vet. Sci. 4, 276-285
11. Chandler, R. L., and Fisher, J. (1963) Experimental transmission of scrapie to rats. Lancet 282, 1165
12. Chandler, R. L., and Turfrey, B. A. (1972) Inoculation of voles, Chinese hamsters, gerbils, and guinea pigs with scrapie brain material. Res. Vet. Sci. 13, 219-224
13. 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
14. Kimberlin, R. H., Cole, S., and Walker, C. A. (1987) Temporary and permanent modifications to a single strain of mouse scrapie on transmission to rats and hamsters. J. Gen. Virol. 68, 1875-1881
15. Bartz, J. C., Bessen, R. A., McKenzie, D., Marsh, R. F., and Aiken, J. M. (2000) Adaptation and selection of prion protein strain conformations following interspecies transmission of transmissible mink encephalopathy. J. Virol. 74 5542-5547
16. Bruce, M. E., and Dickinson, A. G. (1987) Biological evidence that scrapie agent has an independent genome. J. Gen. Virol. 68, 79-89
17. Thackray, A. M., Lockey, R., Beck, K. E., Spiropoulos, J., and Bujdoso, R. (2012) Evidence for co-infection of ovine prion strains in classical scrapie isolates. J. Comp. Path. 147, 316-329
18. Kimberlin, R. H., Walker, C. A., and Fraser, H. (1989) The genomic identity of different strains of mouse scrapie is expressed in hamsters and preserved on reisolation in mice. J. Gen. Virol. 70, 2017-2025
19. Barria, M. A., Mukherjee, A., Gonzalez-Romero, D., Morales, R., and Soto, C. (2009) De novo generation of infectious prions in vitro produces a new disease phenotype. PLOS Pathog. 5, e1000421
20. Diaz-Espinoza, R., and Soto, C. (2010) Generation of prions in vitro and the protein-only hypothesis. Prion 4, 53-59
21. Baskakov, I. V., Legname, G., Baldwin, M. A., Prusiner, S. B., and Cohen, F. E. (2002) Pathway complexity of prion protein assembly into amyloid. J. Biol. Chem. 277, 21140-21148
22. 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
23. Colby, D. W., Giles, K., Legname, G., Wille, H., Baskakov, I. V., De-Armond, S. J., and Prusiner, S. B. (2009) Design and construction of diverse mammalian prion strains. Proc. Natl. Acad. Sci. U.S.A. 106, 20417-20422
24. 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
25. Makarava, N., Kovacs, G. G., Bocharova, O., Savtchenko, R., Alexeeva, I., Budka, H., Rohwer, R. G., and Baskakov, I. V. (2010) Recombinant prion protein induces a new transmissible prion disease in wild-type animals. Acta Neuropathol. 119, 177-187
26. Makarava, N., Kovacs, G. G., Savtchenko, R., Alexeeva, I., Budka, H., Rohwer, R. G., and Baskakov, I. V. (2011) Genesis of mammalian prions: from noninfectious amyloid fibrils to a transmissible prion disease. PLoS Pathog. 7, e1002419
27. Makarava, N., Kovacs, G. G., Savtchenko, R., Alexeeva, I., Ostapchenko, V. G., Budka, H., Rohwer, R. G., and Baskakov, I. V. (2012) A new mechanism for transmissible prion diseases. J. Neurosci. 32, 7345-7355
28. Sandberg, M. K., Al-Doujaily, H., Sharps, B., Clarke, A. R., and Collinge, J. (2011) Prion propagation and toxicity in vivo occur in two distinct mechanistic phases. Nature 470, 540-542
29. Makarava, N., Savtchenko, R., Alexeeva, I., Rohwer, R. G., and Baskakov, I. V. (2012) Fast and ultrasensitive method for quantitating prion infectivity titer. Nat. Commun. 3, 741
30. Gonzalez-Montalban, N., Makarava, N., Ostapchenko, V. G., Savtchenk, R., Alexeeva, I., Rohwer, R. G., and Baskakov, I. V. (2011) Highly efficient protein misfolding cyclic amplification. PLoS Pathog. 7, e1001277
31. Somerville, R. A., and Carp, R. I. (1983) Altered scrapie infectivity estimates by titration and incubation period in the presence of detergents. J. Gen. Virol. 64, 2045-2050
32. Bailey, J. D., Berardinelli, J. G., Rocke, T. E., and Bessen, R. A. (2008) Prominent pancreatic endocrinopathy and altered control of food intake disrupt energy homeostasis in prion diseases. J. Endocrinol. 197, 251-263
33. Gonzalez-Montalban, N., Makarava, N., Savtchenko, R., and Baskakov, I. V. (2011) Relationship between conformational stability and amplification efficiency of prions. Biochemistry 50, 7933-7940
34. Béringue, V., Herzog, L., Jaumain, E., Reine, F., Sibille, P., Le Dur, A., Vilotte, J. L., and Laude, H. (2012) Facilitated cross-species transmission of prions in extraneural tissue. Science 335, 472-475
35. Pattison, I. H., and Jones, K. M. (1968) Modification of a strain of mouse-adapted scrapie by passage through rats. Res. Vet. Sci. 9, 408-410
36. Deleault, N. R., Kascsak, R., Geoghegan, J. C., and Supattapone, S. (2010) Species-dependent differences in co-factor utilization for formation of the protease-resistant prion protein in vitro. Biochemistry 49, 3928-3934
37. Deleault, N. R., Lucassen, R. W., and Supattapone, S. (2003) RNA molecules stimulate prion protein conversion. Nature 425 717-720
38. Deleault, N. R., Walsh, D. J., Piro, J. R., Wang, F., Wang, X., Ma, J., Rees, J. R., and Supattapone, S. (2012) Co-factor molecules maintain infectious conformation and restrict strain properties in purified prions. Proc. Natl. Acad. Sci. U.S.A. 109, E1938-E1946
39. Deleault, N. R., Piro, J. R., Walsh, D. J., Wang, F., Ma, J., Geoghegan, J. C., and Supattapone, S. (2012) Isolation of phosphatidylethanolamine as a solitary co-factor for prion formation in the absence of nucleic acids. Proc. Natl. Acad. Sci. U.S.A.. 109, 8546-8551
40. Prusiner, S. B., Cochran, S. P., Groth, D. F., Downey, D. E., Bowman, K. A., and Martinez, H. M. (1982) Measurement of the scrapie agent using an incubation time interval assay. Ann. Neurol. 11, 353-358
41. Thackray, A. M., Klein, M. A., Aguzzi, A., and Bujdoso, R. (2002) Chronic subclinical prion disease induced by low dose inoculum. J. Virol. 76, 2510-2517
42. Safar, J. G., DeArmond, S. J., Kociuba, K., Deering, C., Didorenko, S., Bouzamondo-Bernstein, E., Prusiner, S. B., and Tremblay, P. (2005) Prion clearance in bigenic mice. J. Gen. Virol. 86, 2913-2923
43. Collins, S. J., Lewis, V., Brazier, M. W., Hill, A. F., Lawson, V. A., Klug, G. M., and Masters, C. L. (2005) Extended period of asymptomatic prion disease after low dose inoculation: assessment of detection methods and implications for infection control. Neurobiol. Dis. 20, 336-346
44. Race, R., Raines, A., Raymond, G. J., Caughey, B., and Chesebro, B. (2001) Long-term subclinical carrier state precedes scrapie replication and adaptation in a resistant species: analogies to bovine spongiform encephalopathy and variant Creutzfeldt-Jakob disease in humans. J. Virol. 75, 10106-10112
45. Kimberlin, R. H., and Walker, C. A. (1979) Pathogenesis of scrapie: agent multiplication in brain at the first and second passage of hamster scrapie in mice. J. Gen. Virol. 42, 107-117
46. Hill, A. F., Joiner, S., Linehan, J., Desbruslais, M., Lantos, P. L., and Collinge, J. (2000) Species-barrier-independent prion replication in apparently resistant species. Proc. Natl. Acad. Sci. U.S.A. 97, 10248-10253
47. Peretz, D., Williamson, R. A., Kaneko, K., Vergara, J., Leclerc, E., Schmitt-Ulms, G., Mehlhorn, I. R., Legname, G., Wormald, M. R., Rudd, P. M., Dwek, R. A., Burton, D. R., and Prusiner, S. B. (2001) Antibodies inhibit prion propagation and clear cell cultures of prion infectivity. Nature 412, 739-743
48. Collinge, J., and Clarke, A. R. (2007) A general model of prion strains and their pathogenicity. Science 318, 930-936
49. 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
50. Legname, G., Nguyen, H. O., Baskakov, I. V., Cohen, F. E., Dearmond, S. J., and Prusiner, S. B. (2005) Strain-specified characteristics of mouse synthetic prions. Proc. Natl. Acad. Sci. U.S.A. 102, 2168-2173