Conformational stability of mammalian prion protein amyloid fibrils is dictated by a packing polymorphism within the core region

Journal of Biological Chemistry

Volumn 289, Issue 5, 2014, Pages 2643-2650

  Cobb, Nathan J ^a   Apostol, Marcin I ^a   Chen, Shugui ^a,c   Smirnovas, Vytautas ^a,d   Surewicz, Witold K ^a,b  

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

^b CASE WESTERN RESERVE UNIVERSITY   (United States)

^c KBI Biopharma   (United States)

^d GLAXOSMITHKLINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID; NEURODEGENERATIVE DISEASES; PRIONS; PROTEIN AGGREGATION; PROTEIN MISFOLDING;

AMYLOID; ANIMALS; HUMANS; MAMMALS; POLYMORPHISM, GENETIC; PRION DISEASES; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY; PROTEOSTASIS DEFICIENCIES; PRPSC PROTEINS; RECOMBINANT PROTEINS;

EID: 84893499249     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.520718     Document Type: Article

References (60)

1. Prusiner, S. B. (1998) Prions. Proc. Natl. Acad. Sci. U. S. A. 95, 13363-13383
2. Aguzzi, A., and Polymenidou, M. (2004) Mammalian prion biology: one century of evolving concepts. Cell 116, 313-327
3. Collinge, J. (2001) Prion diseases of humans and animals: their causes and molecular basis. Annu. Rev. Neurosci. 24, 519-550
4. Cobb, N. J., and Surewicz, W. K. (2009) Prion diseases and their biochemical mechanisms. Biochemistry 48, 2574-2585
5. Kraus, A., Groveman, B. R., and Caughey, B. (2013) Prions and the potential transmissibility of protein misfolding diseases. Annu. Rev. Microbiol. 67, 543-564
6. Castilla, J., Saá, P., Hetz, C, and Soto, C. (2005) In vitro generation of infectious scrapie prions. Cell 121, 195-206
7. Wang, F., Wang, X., Yuan, C. G., and Ma, J. (2010) Generating a prion with bacterially expressed recombinant prion protein. Science 327, 1132-1135
8. Legname, G., Baskakov, I. V., Nguyen, H. O., Riesner, D., Cohen, F. E., De Armond, S. J., and Prusiner, S. B. (2004) Synthetic mammalian prions. Science 305, 673-676
9. 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
10. 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
11. 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 cofactor for prion formation in the absence of nucleic acids. Proc. Natl. Acad. Sci. U. S. A. 109, 8546-8551
12. Collinge, J., and Clarke, A. R. (2007) A general model of prion strains and their pathogenicity. Science 318, 930-936
13. Caughey, B., Raymond, G. J., and Bessen, R. A. (1998) Strain-dependent differences in β-sheet conformations of abnormal prion protein. J. Biol. Chem. 273, 32230-32235
14. Baron, G. S., Hughson, A. G., Raymond, G. J., Offerdahl, D. K., Barton, K. A., Raymond, L. D., Dorward, D. W., and Caughey, B. (2011) Effect of glycans and the glycophosphatidylinositol anchor on strain-dependent conformations of scrapie prion protein: improved purifications and infrared spectra. Biochemistry 50, 4479-4490
15. 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
16. Kuczius, T., and Groschup, M. H. (1999) Differences in proteinase K resistance and neuronal deposition of abnormal prion proteins characterize bovine spongiform encephalopathy (BSE) and scrapie strains. Mol. Med. 5, 406-418
17. 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
18. Bett, C, Kurt, T. D., Lucero, M., Trejo, M., Rozemuller, A. J., Kong, Q., Nilsson, K. P., Masliah, E., Oldstone, M. B., and Sigurdson, C. J. (2013) Defining the conformational features of anchorless, poorly neuroinvasive prions. PLoS Pathog. 9, e1003280
19. 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
20. Peretz, D., Williamson, R. A., Legname, G., Matsunaga, Y., Vergara, J., Burton, D. R., De Armond, S. J., Prusiner, S. B., and Scott, M. R. (2002) A change in the conformation of prions accompanies the emergence of a new prion strain. Neuron 34, 921-932
21. Legname, G., Nguyen, H. O., Peretz, D., Cohen, F. E., De Armond, S. J., and Prusiner, S. B. (2006) Continuum of prion protein structures enciphers a multitude of prion isolate-specified phenotypes. Proc. Natl. Acad. Sci. U. S. A. 103, 19105-19110
22. 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
23. Bett, C., Joshi-Barr, S., Lucero, M., Trejo, M., Liberski, P., Kelly, J. W., Masliah, E., and Sigurdson, C. J. (2012) Biochemical properties of highly neuroinvasive prion strains. PLoS Pathog. 8, e1002522
24. Tanaka, M., Chien, P., Naber, N., Cooke, R., and Weissman, J. S. (2004) Conformational variations in an infectious protein determine prion strain differences. Nature 428, 323-328
25. Toyama, B. H., Kelly, M. J., Gross, J. D., and Weissman, J. S. (2007) The structural basis of yeast prion strain variants. Nature 449, 233-237
26. Apetri, A. C, Vanik, D. L., and Surewicz, W. K. (2005) Polymorphism at residue 129 modulates the conformational conversion of the D178N variant of human prion protein 90-231. Biochemistry 44, 15880-15888
27. Naiki, H., Higuchi, K., Hosokawa, M., and Takeda, T. (1989) Fluorometric determination of amyloid fibrils in vitro using the fluorescent dye, thioflavin T1. Anal. Biochem. 177, 244-249
28. Lu, X., Wintrode, P. L., and Surewicz, W. K. (2007) β-Sheet core of human prion protein amyloid fibrils as determined by hydrogen/deuterium exchange. Proc. Natl. Acad. Sci. U. S. A. 104, 1510-1515
29. Smirnovas, V., Kim, J. I., Lu, X., Atarashi, R., Caughey, B., and Surewicz, W. K. (2009) Distinct structures of scrapie prion protein (PrPSc)-seeded versus spontaneous recombinant prion protein fibrils revealed by hydrogen/deuterium exchange. J. Biol. Chem. 284, 24233-24241
30. Miyagi, M., and Nakazawa, T. (2008) Determination of pKa values of individual histidine residues in proteins using mass spectrometry. Anal. Chem. 80, 6481-6487
31. Miyagi, M., Wan, Q., Ahmad, M. F., Gokulrangan, G., Tomechko, S. E., Bennett, B., and Dealwis, C. (2011) Histidine hydrogen-deuterium exchange mass spectrometry for probing the microenvironment of histidine residues in dihydrofolate reductase. PLoS ONE 6, e17055
32. Bocharova, O. V., Breydo, L., Parfenov, A. S., Salnikov, V. V., and Baskakov, I. V. (2005) In vitro conversion of full-length mammalian prion protein produces amyloid form with physical properties of PrPSc. J. Mol. Biol. 346, 645-659
33. Cobb, N. J., Sönnichsen, F. D., McHaourab, H., and Surewicz, W. K. (2007) Molecular architecture of human prion protein amyloid: a parallel, inregister β-structure. Proc. Natl. Acad. Sci. U. S. A. 104, 18946-18951
34. Smirnovas, V., Baron, G. S., Offerdahl, D. K., Raymond, G. J., Caughey, B., and Surewicz, W. K. (2011) Structural organization of brain-derived mammalian prions examined by hydrogen-deuterium exchange. Nat. Struct. Mol. Biol. 18, 504-506
35. Toyama, B. H., and Weissman, J. S. (2011) Amyloid structure: conformational diversity and consequences. Annu. Rev. Biochem. 80, 557-585
36. Surewicz, W. K., Mantsch, H. H., and Chapman, D. (1993) Determination of protein secondary structure by Fourier transform infrared spectroscopy: a critical assessment. Biochemistry 32, 389-394
37. Zandomeneghi, G., Krebs, M. R., McCammon, M. G., and Fändrich, M. (2004) FTIR reveals structural differences between native β-sheet proteins and amyloid fibrils. Protein Sci. 13, 3314-3321
38. Serpell, L. C, Fraser, P. E., and Sunde, M. (1999) X-ray fiber diffraction of amyloid fibrils. Methods Enzymol. 309, 526-536
39. Tran, D. T., Banerjee, S., Alayash, A. I., Crumbliss, A. L., and Fitzgerald, M. C. (2012) Slow histidine H/D exchange protocol for thermodynamic analysis of protein folding and stability using mass spectrometry. Anal. Chem. 84, 1653-1660
40. Nelson, R., Sawaya, M. R., Balbirnie, M., Madsen, A. Ø., Riekel, C, Grothe, R., and Eisenberg, D. (2005) Structure of thecross-β spine of amyloid-like fibrils. Nature 435, 773-778
41. Sawaya, M. R., Sambashivan, S., Nelson, R., Ivanova, M. I., Sievers, S. A., Apostol, M. I., Thompson, M. J., Balbirnie, M., Wiltzius, J. J., McFarlane, H. T., Madsen, A. Ø., Riekel, C, and Eisenberg, D. (2007) Atomic structures of amyloid cross-β spines reveal varied steric zippers. Nature 447, 453-457
42. Chiti, F., and Dobson, CM. (2006) Proteinmisfolding, functional amyloid, and human disease. Annu. Rev. Biochem. 75, 333-366
43. Shewmaker, F., McGlinchey, R. P., and Wickner, R. B. (2011) Structural insights into functional and pathological amyloid. J. Biol. Chem. 286, 16533-16540
44. Petkova, A. T., Leapman, R. D., Guo, Z., Yau, W. M., Mattson, M. P., and Tycko, R. (2005) Self-propagating, molecular-level polymorphism in Alzheimer's β-amyloid fibrils. Science 307, 262-265
45. Paravastu, A. K., Leapman, R. D., Yau, W. M., and Tycko, R. (2008) Molecular structural basis for polymorphism in Alzheimer's β-amyloid fibrils. Proc. Natl. Acad. Sci. U. S. A. 105, 18349-18354
46. Heise, H., Hoyer, W., Becker, S., Andronesi, O. C, Riedel, D., and Baldus, M. (2005) Molecular-level secondary structure, polymorphism, and dynamics of full-length a-synuclein fibrils studied by solid-state NMR. Proc. Natl. Acad. Sci. U. S. A. 102, 15871-15876
47. Dinkel, P. D., Siddiqua, A., Huynh, H., Shah, M., and Margittai, M. (2011) Variations in filament conformation dictate seeding barrier between three- and four-repeat tau. Biochemistry 50, 4330-4336
48. Yamaguchi, K., Katou, H., Hoshino, M., Hasegawa, K., Naiki, H., and Goto, Y. (2004) Core and heterogeneity of β2-microglobulin amyloid fibrils as revealed by H/D exchange. J. Mol. Biol. 338, 559-571
49. Chatani, E., Yagi, H., Naiki, H., and Goto, Y. (2012) Polymorphism of β2-microglobulin amyloid fibrils manifested by ultrasonication-enhanced fibril formation in trifluoroethanol. J. Biol. Chem. 287, 22827-22837
50. Debelouchina, G. T., Platt, G. W., Bayro, M. J., Radford, S. E., and Griffin, R. G. (2010) Magic angle spinning NMR analysis of β2-microglobulin amyloid fibrils in two distinct morphologies. J. Am. Chem. Soc. 132, 10414-10423
51. Anderson, M., Bocharova, O. V., Makarava, N, Breydo, L., Salnikov, V. V., and Baskakov, I. V. (2006) Polymorphism and ultrastructural organization of prion protein amyloid fibrils: an insight from high resolution atomic force microscopy. J. Mol. Biol. 358, 580-596
52. Jones, E. M., and Surewicz, W. K. (2005) Fibril conformation as the basis of species- and strain-dependent seeding specificity of mammalian prion amyloids. Cell 121, 63-72
53. Jones, E. M., Wu, B., Surewicz, K., Nadaud, P. S., Helmus, J. J., Chen, S., Jaroniec, C. P., and Surewicz, W. K. (2011) Structural polymorphism in amyloids. New insights from studies with Y145Stop prion protein fibrils. J. Biol. Chem. 286, 42777-42784
54. Dzwolak, W., Smirnovas, V., Jansen, R., and Winter, R. (2004) Insulin forms amyloid in a strain-dependent manner: an FT-IR spectroscopic study. Protein Sci. 13, 1927-1932
55. Chien, P., Weissman, J. S., and De Pace, A. H. (2004) Emerging principles of conformation-based prion inheritance. Annu. Rev. Biochem. 73, 617-656
56. Wiltzius, J. J., Landau, M., Nelson, R., Sawaya, M. R., Apostol, M. I., Goldschmidt, L., Soriaga, A. B., Cascio, D., Rajashankar, K., and Eisenberg, D. (2009) Molecular mechanisms for protein-encoded inheritance. Nat. Struct. Mol. Biol. 16, 973-978
57. Tanaka, M., Collins, S. R., Toyama, B. H., and Weissman, J. S. (2006) The physical basis of how prion conformations determine strain phenotypes. Nature 442, 585-589
58. Surewicz, W. K., and Apostol, M. I. (2011) Prion protein and its conformational conversion: a structural perspective. Top. Curr. Chem. 305, 135-167
59. Hosszu, L. L., Wells, M. A., Jackson, G. S., Jones, S., Batchelor, M., Clarke, A. R., Craven, C. J., Waltho, J. P., and Collinge, J. (2005) Definable equilibrium states in the folding of human prion protein. Biochemistry 44, 16649-16657
60. Apetri, A. C, Maki, K., Roder, H., and Surewicz, W. K. (2006) Early intermediate in human prion protein folding as evidenced by ultrarapid mixing experiments. J. Am. Chem. Soc. 128, 11673-11678