Infrared Microspectroscopy Detects Protein Misfolding Cyclic Amplification (PMCA)-induced conformational alterations in hamster scrapie progeny seeds

Journal of Biological Chemistry

Volumn 288, Issue 49, 2013, Pages 35068-35080

  Daus, Martin L ^a   Wagenführ, Katja ^a   Thomzig, Achim ^a   Boerner, Susann ^a   Hermann, Peter ^a   Hermelink, Antje ^a   Beekes, Michael ^a   Lasch, Peter ^a  

^a ROBERT KOCH INSTITUTE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANALYTICAL APPROACH; INFRARED MICRO-SPECTROSCOPY; PROTEIN MISFOLDING; SCRAPIE PRIONS; STRAIN PROPERTIES;

BIOASSAY; MICROOPTICS; NEURODEGENERATIVE DISEASES; PROTEINS;

AMPLIFICATION;

PRION PROTEIN; PROTEINASE K;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOASSAY; BIOCHEMISTRY; COMPARATIVE STUDY; CONTROLLED STUDY; GENE AMPLIFICATION; HAMSTER; INFRARED MICROSPECTROSCOPY; INFRARED SPECTROSCOPY; NONHUMAN; PRIORITY JOURNAL; PROGENY; PROTEIN ASSEMBLY; PROTEIN DEFECT; PROTEIN MISFOLDING CYCLIC AMPLIFICATION; PROTEIN MODIFICATION; SCRAPIE; SCRAPIE AGENT; SENSITIVITY AND SPECIFICITY; STRUCTURE ANALYSIS; ULTRACENTRIFUGATION; VIRUS REPLICATION; VIRUS STRAIN;

AMYLOID; BIOPHYSICS; INFRARED MICROSPECTROSCOPY (IR-MSP); NEURODEGENERATIVE DISEASES; PRION STRAINS; PRION STRUCTURE; PRIONS; PROTEIN MISFOLDING; PROTEIN MISFOLDING CYCLIC AMPLIFICATION (PMCA); SEEDING ACTIVITY;

ANIMALS; BRAIN CHEMISTRY; CRICETINAE; ENDOPEPTIDASE K; MESOCRICETUS; MICROSCOPY, ATOMIC FORCE; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STABILITY; PRP 27-30 PROTEIN; PRPSC PROTEINS; SCRAPIE; SPECTROSCOPY, FOURIER TRANSFORM INFRARED;

EID: 84890282801     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.497131     Document Type: Article

References (49)

1. Weissmann, C. (2009) Thoughts on mammalian prion strains. Folia Neuropathol. 47, 104-113
2. Prusiner, S. B. (1982) Novel proteinaceous infectious particles cause scrapie. Science 216, 136-144
3. Colby, D. W., and Prusiner, S. B. (2011) Prions. Cold Spring Harb. Perspect. Biol. 3, a006833
4. Prusiner, S. B. (1998) Prions. Proc. Natl. Acad. Sci. U.S.A. 95, 13363-13383
5. Gill, A. C., Agarwal, S., Pinheiro, T. J., and Graham, J. F. (2010) Structural requirements for efficient prion protein conversion. Cofactors may promote a conversion-competent structure for PrP(C). Prion 4, 235-242
6. Wang, F., Wang, X., Yuan, C. G., and Ma, J. (2010) Generating a prion with bacterially expressed recombinant prion protein. Science 327, 1132-1135
7. Kim, J. I., Cali, I., Surewicz, K., Kong, Q., Raymond, G. J., Atarashi, R., Race, B., Qing, L., Gambetti, P., Caughey, B., and Surewicz, W. K. (2010) Mammalian prions generated from bacterially expressed prion protein in the absence of any mammalian cofactors. J. Biol. Chem. 285, 14083-14087
8. Wang, F., Zhang, Z., Wang, X., Li, J., Zha, L., Yuan, C. G., Weissmann, C., and Ma, J. (2012) Genetic informational RNA is not required for recombinant prion infectivity. J. Virol. 86, 1874-1876
9. Collinge, J., and Clarke, A. R. (2007) A general model of prion strains and their pathogenicity. Science 318, 930-936
10. Aguzzi, A., Heikenwalder, M., and Polymenidou, M. (2007) Insights into prion strains and neurotoxicity. Nat. Rev. Mol. Cell Biol. 8, 552-561
11. Castilla, J., Gonzalez-Romero, D., Saá, P., Morales, R., De Castro, J., and Soto, C. (2008) Crossing the species barrier by PrP(Sc) replication in vitro generates unique infectious prions. Cell 134, 757-768
12. Thomzig, A., Spassov, S., Friedrich, M., Naumann, D., and Beekes, M. (2004) Discriminating scrapie and bovine spongiform encephalopathy isolates by infrared spectroscopy of pathological prion protein. J. Biol. Chem. 279, 33847-33854
13. Spassov, S., Beekes, M., and Naumann, D. (2006) Structural differences between TSEs strains investigated by FT-IR spectroscopy. Biochim. Biophys. Acta 1760, 1138-1149
14. 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
15. Daus, M. L., and Beekes, M. (2012) Chronic wasting disease. Fingerprinting the culprit in risk assessments. Prion 6, 17-22
16. Caughey, B., Raymond, G. J., and Bessen, R. A. (1998) Strain-dependent differences in beta-sheet conformations of abnormal prion protein. J. Biol. Chem. 273, 32230-32235
17. Krimm, S., and Bandekar, J. (1986) Vibrational spectroscopy and conformation of peptides, polypeptides, and proteins. Adv. Protein Chem. 38, 181-364
18. Bandekar, J. (1992) Amide modes and protein conformation. Biochim. Biophys. Acta 1120, 123-143
19. Barth, A., and Zscherp, C. (2002) What vibrations tell us about proteins. Q. Rev. Biophys. 35, 369-430
20. Barria, M. A., Gonzalez-Romero, D., and Soto, C. (2012) Cyclic amplification of prion protein misfolding. Methods Mol. Biol. 849, 199-212
21. Castilla, J., Saá, P., Hetz, C., and Soto, C. (2005) In vitro generation of infectious scrapie prions. Cell 121, 195-206
22. Gonzalez-Montalban, N., and Baskakov, I. V. (2012) Assessment of strainspecific PrP(Sc) elongation rates revealed a transformation of PrP(Sc) properties during protein misfolding cyclic amplification. PloS One 7, e41210
23. Gonzalez-Montalban, N., Lee, Y. J., Makarava, N., Savtchenko, R., and Baskakov, I. V. (2013) Changes in prion replication environment cause prion strain mutation. FASEB J. 27, 3702-3710
24. 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
25. Lemmer, K., Mielke, M., Kratzel, C., Joncic, M., Oezel, M., Pauli, G., and Beekes, M. (2008) Decontamination of surgical instruments from prions. II. In vivo findings with a model system for testing the removal of scrapie infectivity from steel surfaces. J. Gen. Virol. 89, 348-358
26. Pritzkow, S., Wagenfuhr, K., Daus, M. L., Boerner, S., Lemmer, K., Thomzig, A., Mielke, M., and Beekes, M. (2011) Quantitative detection and biological propagation of scrapie seeding activity in vitro facilitate use of prions as model pathogens for disinfection. PloS One 6, e20384
27. Oakley, B. R., Kirsch, D. R., and Morris, N. R. (1980) A simplified ultrasensitive silver stain for detecting proteins in polyacrylamide gels. Anal. Biochem. 105, 361-363
28. 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
29. Tixador, P., Herzog, L., Reine, F., Jaumain, E., Chapuis, J., Le Dur, A., Laude, H., and Béringue, V. (2010) The physical relationship between infectivity and prion protein aggregates is strain-dependent. PLoS Pathog. 6, e1000859
30. Diringer, H., Beekes, M., Ozel, M., Simon, D., Queck, I., Cardone, F., Pocchiari, M., and Ironside, J. W. (1997) Highly infectious purified preparations of disease-specific amyloid of transmissible spongiform encephalopathies are not devoid of nucleic acids of viral size. Intervirology 40, 238-246
31. Fabian, H., Schultz, C., Backmann, J., Hahn, U., Saenger, W., Mantsch, H. H., and Naumann, D. (1994) Impact of point mutations on the structure and thermal stablility of ribonuclease T1 in aqueous solution probed by Fourier transform infrared spectroscopy. Biochemistry 33, 10725-10730
32. Lasch, P., Schultz, C., and Naumann, D. (1998) The influence of poly-(Llysine) and porin on the domain structure of mixed vesicles composed of lipopolysaccharide and phospholipid. An infrared spectroscopic study. Biophys. J. 75, 840-852
33. Everest, S. J., Ramsay, A. M., Chaplin, M. J., Everitt, S., Stack, M. J., Neale, M. H., Jeffrey, M., Moore, S. J., Bellworthy, S. J., and Terry, L. A. (2011) Detection and localisation of PrP(Sc) in the liver of sheep infected with scrapie and bovine spongiform encephalopathy. PloS One 6, e19737
34. 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
35. Weber, P., Giese, A., Piening, N., Mitteregger, G., Thomzig, A., Beekes, M., and Kretzschmar, H. A. (2006) Cell-free formation of misfolded prion protein with authentic prion infectivity. Proc. Natl. Acad. Sci. U.S.A. 103, 15818-15823
36. Deleault, N. R., Walsh, D. J., Piro, J. R., Wang, F., Wang, X., Ma, J., Rees, J. R., and Supattapone, S. (2012) Cofactor molecules maintain infectious conformation and restrict strain properties in purified prions. Proc. Natl. Acad. Sci. U.S.A. 109, E1938-E1946
37. Beekes, M., Lasch, P., and Naumann, D. (2007) Analytical applications of Fourier transform-infrared (FT-IR) spectroscopy in microbiology and prion research. Vet. Microbiol. 123, 305-319
38. Surewicz, W. K., and Mantsch, H. H. (1988) New insight into protein secondary structure from resolution-enhanced infrared spectra. Biochim. Biophys. Acta 952, 115-130
39. Surewicz, W. K., and Apostol, M. I. (2011) Prion protein and its conformational conversion. A structural perspective. Top. Curr. Chem. 305, 135-167
40. Cobb, N. J., Sonnichsen, F. D., McHaourab, H., and Surewicz, W. K. (2007) Molecular architecture of human prion protein amyloid. A parallel, inregister -structure. Proc. Natl. Acad. Sci. U.S.A. 104, 18946-18951
41. Xue, W. F., Hellewell, A. L., Gosal, W. S., Homans, S. W., Hewitt, E. W., and Radford, S. E. (2009) Fibril fragmentation enhances amyloid cytotoxicity. J. Biol. Chem. 284, 34272-34282
42. Fabian, H., Gast, K., Laue, M., Misselwitz, R., Uchanska-Ziegler, B., Ziegler, A., and Naumann, D. (2008) Early stages of misfolding and association of -2-microglobulin. Insights from infrared spectroscopy and dynamic light scattering. Biochemistry 47, 6895-6906
43. Debelouchina, G. T., Platt, G. W., Bayro, M. J., Radford, S. E., and Griffin, R. G. (2010) Intermolecular alignment in -2-microglobulin amyloid fibrils. J. Am. Chem. Soc. 132, 17077-17079
44. Suzuki, S. Y., Takata, M., Teruya, K., Shinagawa, M., Mohri, S., and Yokoyama, T. (2008) Conformational change in hamster scrapie prion protein (PrP27-30) associated with proteinase K resistance and prion infectivity. J. Vet. Med. Sci. 70, 159-165
45. Klingeborn, M., Race, B., Meade-White, K. D., and Chesebro, B. (2011) Lower specific infectivity of protease-resistant prion protein generated in cell-free reactions. Proc. Natl. Acad. Sci. U.S.A. 108, E1244-E1253
46. Saá, P., Sferrazza, G. F., Ottenberg, G., Oelschlegel, A. M., Dorsey, K., and Lasmézas, C. I. (2012) Strain-specific role of RNAs in prion replication. J. Virol. 86, 10494-10504
47. Makarava, N., Ostapchenko, V. G., Savtchenko, R., and Baskakov, I. V. (2009) Conformational switching within individual amyloid fibrils. J. Biol. Chem. 284, 14386-14395
48. Baskakov, I. V. (2009) Switching in amyloid structure within individual fibrils. Implication for strain adaptation, species barrier and strain classification. FEBS Lett. 583, 2618-2622
49. Weissmann, C., Li, J., Mahal, S. P., and Browning, S. (2011) Prions on the move. EMBO Rep. 12, 1109-1117