Identification and removal of proteins that co-purify with infectious prion protein improves the analysis of its secondary structure

Proteomics

Volumn 11, Issue 19, 2011, Pages 3853-3865

  Moore, Roger A ^a   Timmes, Andrew G ^a   Wilmarth, Phillip A ^b   Safronetz, David ^a   Priola, Suzette A ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Animal proteomics; Apolipoprotein E; Ferritin; Infrared spectroscopy; Prion protein purification; Prion strains

Indexed keywords

ACTIN; APOLIPOPROTEIN E; CLAUDIN 11; COLLAGEN; COLLAPSIN RESPONSE MEDIATOR PROTEIN 2; EXOCYST; FERRITIN; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GUANINE NUCLEOTIDE BINDING PROTEIN BETA SUBUNIT; HELIX LOOP HELIX PROTEIN; HEMOGLOBIN CHAIN; MYOSIN VA; POLYUBIQUITIN; PRION PROTEIN; PROTEOLIPID PROTEIN; SYNTAXIN 1; TUBULIN;

ABSORPTION; ALPHA HELIX; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BETA SHEET; CONTROLLED STUDY; HAMSTER; INFRARED SPECTROSCOPY; LIQUID CHROMATOGRAPHY; MOUSE; NONHUMAN; PRION; PRION DISEASE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN PURIFICATION; PROTEIN SECONDARY STRUCTURE; TANDEM MASS SPECTROMETRY;

ANIMALS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CRICETINAE; FERRITINS; HUMANS; MICE; PRION DISEASES; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEINS; PROTEOMICS; PRPSC PROTEINS; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; TANDEM MASS SPECTROMETRY;

ANIMALIA; CRICETINAE; MAMMALIAN PRION;

EID: 80052976271     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201100253     Document Type: Article

References (55)

1. Chesebro, B., Introduction to the transmissible spongiform encephalopathies or prion diseases. Br. Med. Bull. 2003, 66, 1-20.
2. Moore, R. A., Taubner, L. M., Priola, S. A., Prion protein misfolding and disease. Curr. Opin. Struct. Biol. 2009, 19, 14-22.
3. Safar, J., Wille, H., Itri, V., Groth, D. et al., Eight prion strains have PrP(Sc) molecules with different conformations. Nat. Med. 1998, 4, 1157-1165.
4. Thomzig, A., Spassov, S., Friedrich, M., Naumann, D., Beekes, M., Discriminating scrapie and bovine spongiform encephalopathy isolates by infrared spectroscopy of pathological prion protein. J. Biol. Chem. 2004, 279, 33847-33854.
5. Spassov, S., Beekes, M., Naumann, D., Structural differences between TSEs strains investigated by FT-IR spectroscopy. Biochim. Biophys. Acta 2006, 1760, 1138-1149.
6. Caughey, B., Raymond, G. J., Bessen, R. A., Strain-dependent differences in beta-sheet conformations of abnormal prion protein. J. Biol. Chem. 1998, 273, 32230-32235.
7. Wiltzius, J. J., Landau, M., Nelson, R., Sawaya, M. R. et al., Molecular mechanisms for protein-encoded inheritance. Nat. Struct. Mol. Biol. 2009, 16, 973-978.
8. Caughey, B., Baron, G. S., Chesebro, B., Jeffrey, M., Getting a grip on prions: oligomers, amyloids, and pathological membrane interactions. Annu. Rev. Biochem. 2009, 78, 177-204.
9. Riek, R., Hornemann, S., Wider, G., Billeter, M. et al., NMR structure of the mouse prion protein domain PrP(121-231). Nature 1996, 382, 180-182.
10. Zahn, R., Liu, A., Luhrs, T., Riek, R. et al., NMR solution structure of human prion protein. Proc. Natl. Acad. Sci. USA 2000, 97, 145-150.
11. Lysek, D. A., Schorn, C., Nivon, L. G., Esteve-Moya, V. et al., Prion protein NMR structures of cats, dogs, pigs, and sheep. Proc. Natl. Acad. Sci. USA 2005, 102, 640-645.
12. Knaus, K. J., Morillas, M., Swietnicki, W., Malone, M. et al., Crystal structure of the human prion protein reveals a mechanism for oligomerization. Nat. Struct. Biol. 2001, 8, 770-774.
13. Safar, J., Roller, P. P., Gajdusek, D. C., Gibbs, C. J., Jr., Conformational transitions, dissociation, and unfolding of scrapie amyloid (prion) protein. J. Biol. Chem. 1993, 268, 20276-20284.
14. Caughey, B. W., Dong, A., Bhat, K. S., Ernst, D. et al., Secondary structure-analysis of the scrapie-associated protein Prp 27-30 in water by infrared-spectroscopy. Biochemistry 1991, 30, 7672-7680.
15. Pan, K.-M., Baldwin, M., Nguyen, J., Gasset, M. et al., Conversion of alpha-helices into beta-sheets features in the formation of the scrapie prion protein. Proc. Natl. Acad. Sci. USA 1993, 90, 10962-10966.
16. Baron, G. S., Hughson, A. G., Raymond, G. J., Offerdahl, D. K. et al., Effect of glycans and the glycophosphatidylinositol anchor on strain dependent conformations of scrapie prion protein: improved purifications and infrared spectra. Biochemistry 2011, 50, 4479-4490.
17. Smirnovas, V., Baron, G. S., Offerdahl, D. K., Raymond, G. J. et al., Structural organization of brain-derived mammalian prions examined by hydrogen-deuterium exchange. Nat. Struct. Mol. Biol. 2011, 18, 504-506.
18. Demarco, M. L., Silveira, J., Caughey, B., Daggett, V., Structural properties of prion protein protofibrils and fibrils: an experimental assessment of atomic models. Biochemistry 2006, 45, 15573-15582.
19. Govaerts, C., Wille, H., Prusiner, S. B., Cohen, F. E., Evidence for assembly of prions with left-handed beta-helices into trimers. Proc. Natl. Acad. Sci. USA 2004, 101, 8342-8347.
20. Diringer, H., Hilmert, H., Simon, D., Werner, E., Ehlers, B., Towards purification of the scrapie agent. Eur. J. Biochem. 1983, 134, 555-560.
21. Bolton, D. C., McKinley, M. P., Prusiner, S. B., Identification of a protein that purifies with the scrapie prion. Science 1982, 218, 1309-1311.
22. Gabizon, R., McKinley, M. P., Groth, D., Prusiner, S. B., Immunoaffinity purification and neutralization of scrapie prion infectivity. Proc. Natl. Acad. Sci. USA 1988, 85, 6617-6621.
23. Raymond, G. J., Chabry, J., Purification of the pathological isoform of prion protein (PrPSc or PrPres) from transmissible spongiform encephalopathy-affected brain tissue. In: Lehmann, S., Grassi, J. (Eds), Techniques in Prion Research, Birkhauser Verlag, Basel 2004, pp. 16-26.
24. Prusiner, S. B., Bolton, D. C., Groth, D. F., Bowman, K. A. et al., Further purification and characterization of scrapie prions. Biochemistry 1982, 21, 6942-6950.
25. Appel, T. R., Dumpitak, C., Matthiesen, U., Riesner, D., Prion rods contain an inert polysaccharide scaffold. Biol. Chem. 1999, 380, 1295-1306.
26. Stahl, N., Borchelt, D. R., Hsiao, K., Prusiner, S. B., Scrapie prion protein contains a phosphatidylinositol glycolipid. Cell 1987, 51, 229-240.
27. Diringer, H., Beekes, M., Ozel, M., Simon, D. et al., Highly infectious purified preparations of disease-specific amyloid of transmissible spongiform encephalopathies are not devoid of nucleic acids of viral size. Intervirology 1997, 40, 238-246.
28. Giorgi, A., Di, F. L., Principe, S., Mignogna, G. et al., Proteomic profiling of PrP27-30-enriched preparations extracted from the brain of hamsters with experimental scrapie. Proteomics 2009, 9, 3802-3814.
29. Moore, R. A., Timmes, A., Wilmarth, P. A., Priola, S. A., Comparative profiling of highly enriched 22L and Chandler mouse scrapie prion protein preparations. Proteomics 2010, 10, 2858-2869.
30. Wadsworth, J. D., Hill, A. F., Joiner, S., Jackson, G. S. et al., Strain-specific prion-protein conformation determined by metal ions. Nat. Cell Biol. 1999, 1, 55-59.
31. Crichton, R. R., Declercq, J. P., X-ray structures of ferritins and related proteins. Biochim. Biophys. Acta 2010, 1800, 706-718.
32. Perkins, D. N., Pappin, D. J., Creasy, D. M., Cottrell, J. S., Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 1999, 20, 3551-3567.
33. Weatherly, D. B., Atwood, J. A., III, Minning, T. A., Cavola, C. et al., A Heuristic method for assigning a false-discovery rate for protein identifications from Mascot database search results. Mol. Cell. Proteomics 2005, 4, 762-772.
34. Silveira, J. R., Raymond, G. J., Hughson, A. G., Race, R. E. et al., The most infectious prion protein particles. Nature 2005, 437, 257-261.
35. Bruce, M. E., Scrapie strain variation and mutation. Br. Med. Bull. 1993, 49, 822-838.
36. Cunningham, C., Deacon, R. M., Chan, K., Boche, D. et al., Neuropathologically distinct prion strains give rise to similar temporal profiles of behavioral deficits. Neurobiol. Dis. 2005, 18, 258-269.
37. Bruce, M. E., McConnell, I., Fraser, H., Dickinson, A. G., The disease characteristics of different strains of scrapie in Sinc congenic mouse lines: implications for the nature of the agent and host control of pathogenesis. J. Gen. Virol. 1991, 72, 595-603.
38. Kimberlin, R. H., Walker, C. A., Fraser, H., The genomic identity of different strains of mouse scrapie is expressed in hamsters and preserved on reisolation in mice. J. Gen. Virol. 1989, 70, 2017-2025.
39. Seshadri, S., Khurana, R., Fink, A. L., Fourier transform infrared spectroscopy in analysis of protein deposits. Methods Enzymol. 1999, 309, 559-576.
40. Haris, P. I., Can infrared spectroscopy provide information on protein-protein interactions? Biochem. Soc. Trans. 2010, 38, 940-946.
41. Surewicz, W. K., Mantsch, H. H., Chapman, D., Determination of protein secondary structure by Fourier transform infrared spectroscopy: a critical assessment. Biochemistry 1993, 32, 389-394.
42. Wilder, C. L., Friedrich, A. D., Potts, R. O., Daumy, G. O., Francoeur, M. L., Secondary structural analysis of two recombinant murine proteins, interleukins 1 alpha and 1 beta: is infrared spectroscopy sufficient to assign structure? Biochemistry 1992, 31, 27-31.
43. Barth, A., Infrared spectroscopy of proteins. Biochim. Biophys. Acta Bioenerg. 2007, 1767, 1073-1101.
44. Susi, H., Byler, D. M., Protein structure by Fourier transform infrared spectroscopy: second derivative spectra. Biochem. Biophys. Res. Commun. 1983, 115, 391-397.
45. Lundgren, D. H., Hwang, S. I., Wu, L., Han, D. K., Role of spectral counting in quantitative proteomics. Exp. Rev. Proteomics 2010, 7, 39-53.
46. Gasset, M., Baldwin, M. A., Fletterick, R. J., Prusiner, S. B., Perturbation of the secondary structure of the scrapie prion protein under conditions that alter infectivity. Proc. Natl. Acad. Sci. USA 1993, 90, 1-5.
47. Huzarewich, R. L., Siemens, C. G., Booth, S. A., Application of "omics" to prion biomarker discovery. J. Biomed. Biotechnol. 2010, 2010, 613504.
48. Skinner, P. J., Abbassi, H., Chesebro, B., Race, R. E. et al., Gene expression alterations in brains of mice infected with three strains of scrapie. BMC Genomics 2006, 7, 114.
49. Sorensen, G., Medina, S., Parchaliuk, D., Phillipson, C. et al., Comprehensive transcriptional profiling of prion infection in mouse models reveals networks of responsive genes. BMC Genomics 2008, 9, 114.
50. Twine, N. A., Janitz, K., Wilkins, M. R., Janitz, M., Whole transcriptome sequencing reveals gene expression and splicing differences in brain regions affected by Alzheimer's disease. PLoS ONE 2011, 6, e16266.
51. Choe, L. H., Green, A., Knight, R. S., Thompson, E. J., Lee, K. H., Apolipoprotein E and other cerebrospinal fluid proteins differentiate ante mortem variant Creutzfeldt-Jakob disease from ante mortem sporadic Creutzfeldt-Jakob disease. Electrophoresis 2002, 23, 2242-2246.
52. Hochstrasser, D. F., Frutiger, S., Wilkins, M. R., Hughes, G., Sanchez, J. C., Elevation of apolipoprotein E in the CSF of cattle affected by BSE. FEBS Lett. 1997, 416, 161-163.
53. Kim, J., Basak, J. M., Holtzman, D. M., The role of apolipoprotein E in Alzheimer's disease. Neuron 2009, 63, 287-303.
54. Baumann, M. H., Kallijarvi, J., Lankinen, H., Soto, C., Haltia, M., Apolipoprotein E includes a binding site which is recognized by several amyloidogenic polypeptides. Biochem. J. 2000, 349, 77-84.
55. Nakamura, S., Ono, F., Hamano, M., Odagiri, K. et al., Immunohistochemical detection of apolipoprotein E within prion-associated lesions in squirrel monkey brains. Acta Neuropathol. 2000, 100, 365-370.