High-resolution structure of infectious prion protein: The final frontier

Nature Structural and Molecular Biology

Volumn 19, Issue 4, 2012, Pages 370-377

  Diaz Espinoza, Rodrigo ^a   Soto, Claudio ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROGEN; POLYMER; PRION PROTEIN;

AGGREGATIBACTER; ALPHA HELIX; BETA SHEET; CIRCULAR DICHROISM; CRYSTALLIZATION; DIFFRACTION; DISEASE TRANSMISSION; DNA STRUCTURE; HUMAN; IN VITRO STUDY; IN VIVO STUDY; INFRARED SPECTROPHOTOMETRY; INFRARED SPECTROSCOPY; MOLECULAR INTERACTION; MUTATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRION DISEASE; PRIORITY JOURNAL; PROPAGANDA; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; REVIEW; TRANSMISSION ELECTRON MICROSCOPY; X RAY CRYSTALLOGRAPHY; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; PROTEIN SECONDARY STRUCTURE;

PRIONS (INFECTIVE AGENTS);

ANIMALS; HUMANS; MODELS, MOLECULAR; PRION DISEASES; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; PRPSC PROTEINS;

EID: 84861315209     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2266     Document Type: Review

References (108)

1. Delez, A.L., Gustafson, D.P. & Luttrell, C.N. Some clinical and histological observations on scrapie in sheep. J. Am. Vet. Med. Assoc. 131, 439-446 (1957).
2. Collinge, J. Prion diseases of humans and animals: their causes and molecular basis. Annu. Rev. Neurosci. 24, 519-550 (2001). (Pubitemid 32695238)
3. Alper, T. Scrapie agent unlike viruses in size and susceptibility to inactivation by ionizing or ultraviolet radiation. Nature 317, 750 (1985).
4. Gajdusek, D.C., Gibbs, C.J. & Alpers, M. Experimental transmission of a Kuru-like syndrome to chimpanzees. Nature 209, 794-796 (1966).
5. Hope, J., Ritchie, L., Farquhar, C., Somerville, R. & Hunter, N. Bovine spongiform encephalopathy: a scrapie-like disease of British cattle. Prog. Clin. Biol. Res. 317, 659-667 (1989).
6. Will, R.G. et al. A new variant of Creutzfeldt-Jakob disease in the UK. Lancet 347, 921-925 (1996). (Pubitemid 26102546)
7. Collinge, J. Variant Creutzfeldt-Jakob disease. Lancet 354, 317-323 (1999). (Pubitemid 29348751)
8. Soto, C. & Castilla, J. The controversial protein-only hypothesis of prion propagation. Nat. Med. 10, S63-S67 (2004). (Pubitemid 38901869)
9. Griffith, J.S. Self-replication and scrapie. Nature 215, 1043-1044 (1967).
10. Bolton, D.C., McKinley, M.P. & Prusiner, S.B. Identification of a protein that purifies with the scrapie prion. Science 218, 1309-1311 (1982).
11. McKinley, M.P., Bolton, D.C. & Prusiner, S.B. A protease-resistant protein is a structural component of the scrapie prion. Cell 35, 57-62 (1983). (Pubitemid 14240218)
12. Stahl, N. et al. Structural studies of the scrapie prion protein using mass spectrometry and amino acid sequencing. Biochemistry 32, 1991-2002 (1993). (Pubitemid 23086050)
13. Pan, K.M. et al. Conversion of alpha-helices into beta-sheets features in the formation of the scrapie prion proteins. Proc. Natl. Acad. Sci. USA 90, 10962-10966 (1993).
14. Prusiner, S.B. Prions. Proc. Natl. Acad. Sci. USA 95, 13363-13383 (1998).
15. Soto, C. Prion hypothesis: the end of the controversy? Trends Biochem. Sci. 36, 151-158 (2011).
16. Büeler, H. et al. Mice devoid of PrP are resistant to scrapie. Cell 73, 1339-1347 (1993). (Pubitemid 23201147)
17. Jackson, W.S. et al. Spontaneous generation of prion infectivity in fatal familial insomnia knockin mice. Neuron 63, 438-450 (2009).
18. Sigurdson, C.J. et al. De novo generation of a transmissible spongiform encephalopathy by mouse transgenesis. Proc. Natl. Acad. Sci. USA 106, 304-309 (2009).
19. Castilla, J., Saá, P., Hetz, C. & Soto, C. In vitro generation of infectious scrapie prions. Cell 121, 195-206 (2005). (Pubitemid 40546388)
20. Deleault, N.R., Harris, B.T., Rees, J.R. & Supattapone, S. From the cover: formation of native prions from minimal components in vitro. Proc. Natl. Acad. Sci. USA 104, 9741-9746 (2007). (Pubitemid 47175337)
21. Wang, F., Wang, X., Yuan, C.-G. & Ma, J. Generating a prion with bacterially expressed recombinant prion protein. Science 327, 1132-1135 (2010).
22. Castilla, J. et al. Cell-free propagation of prion strains. EMBO J. 27, 2557-2566 (2008).
23. Chiti, F. & Dobson, C.M. Protein misfolding, functional amyloid, and human disease. Annu. Rev. Biochem. 75, 333-366 (2006). (Pubitemid 44118036)
24. Silveira, J.R. et al. The most infectious prion protein particles. Nature 437, 257-261 (2005). (Pubitemid 41294488)
25. Tixador, P. et al. The physical relationship between infectivity and prion protein aggregates is strain-dependent. PLoS Pathog. 6, e1000859 (2010).
26. Riek, R. et al. NMR structure of the mouse prion protein domain PrP(121-321). Nature 382, 180-182 (1996). (Pubitemid 26242887)
27. Jarrett, J.T. & Lansbury, P.T. Jr. Seeding "one-dimensional crystallization" of amyloid: a pathogenic mechanism in Alzheimer's disease and scrapie? Cell 73, 1055-1058 (1993). (Pubitemid 23180480)
28. Soto, C., Estrada, L. & Castilla, J. Amyloids, prions and the inherent infectious nature of misfolded protein aggregates. Trends Biochem. Sci. 31, 150-155 (2006). (Pubitemid 43357995)
29. Caughey, B., Baron, G.S., Chesebro, B. & Jeffrey, M. Getting a grip on prions: oligomers, amyloids, and pathological membrane interactions. Annu. Rev. Biochem. 78, 177-204 (2009).
30. McKinley, M.P., Braunfeld, M.B., Bellinger, C.G. & Prusiner, S.B. Molecular characteristics of prion rods purified from scrapie-infected hamster brains. J. Infect. Dis. 154, 110-120 (1986). (Pubitemid 16088309)
31. Gabizon, R., McKinley, M.P. & Prusiner, S.B. Purified prion proteins and scrapie infectivity copartition into liposomes. Proc. Natl. Acad. Sci. USA 84, 4017-4021 (1987). (Pubitemid 17090866)
32. Riesner, D. et al. Disruption of prion rods generates 10-nm spherical particles having high alpha-helical content and lacking scrapie infectivity. J. Virol. 70, 1714-1722 (1996). (Pubitemid 26062931)
33. Wille, H., Zhang, G.F., Baldwin, M.A., Cohen, F.E. & Prusiner, S.B. Separation of scrapie prion infectivity from PrP amyloid polymers. J. Mol. Biol. 259, 608-621 (1996). (Pubitemid 26226002)
34. Pastrana, M.A. et al. Isolation and characterization of a proteinase K-sensitive PrPSc fraction. Biochemistry 45, 15710-15717 (2006). (Pubitemid 46032491)
35. Cobb, N.J. & Surewicz, W.K. Prion diseases and their biochemical mechanisms. Biochemistry 48, 2574-2585 (2009).
36. Diringer, H. et al. 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 (1997). (Pubitemid 28230819)
37. Leffers, K.W. et al. Assembly of natural and recombinant prion protein into fibrils. Biol. Chem. 386, 569-580 (2005).
38. Cobb, N.J., Apetri, A.C. & Surewicz, W.K. Prion protein amyloid formation under native-like conditions involves refolding of the C-terminal alpha-helical domain. J. Biol. Chem. 283, 34704-34711 (2008).
39. Baskakov, I.V., Legname, G., Baldwin, M.A., Prusiner, S.B. & Cohen, F.E. Pathway complexity of prion protein assembly into amyloid. J. Biol. Chem. 277, 21140-21148 (2002). (Pubitemid 34952249)
40. Bocharova, O.V., Breydo, L., Parfenov, A.S., Salnikov, V.V. & Baskakov, I.V. In vitro conversion of full-length mammalian prion protein produces amyloid form with physical properties of PrPSc. J. Mol. Biol. 346, 645-659 (2005).
41. Jackson, G.S. et al. Reversible conversion of monomeric human prion protein between native and fibrilogenic conformations. Science 283, 1935-1937 (1999).
42. May, B.C., Govaerts, C., Prusiner, S.B. & Cohen, F.E. Prions: so many fibers, so little infectivity. Trends Biochem. Sci. 29, 162-165 (2004). (Pubitemid 38472018)
43. Legname, G. et al. Synthetic mammalian prions. Science 305, 673-676 (2004). (Pubitemid 39006757)
44. Westaway, D. et al. Degeneration of skeletal muscle, peripheral nerves, and the central nervous system in transgenic mice overexpressing wild-type prion proteins. Cell 76, 117-129 (1994). (Pubitemid 24035286)
45. Chiesa, R., Piccardo, P., Ghetti, B. & Harris, D.A. Neurological illness in transgenic mice expressing a prion protein with an insertional mutation. Neuron 21, 1339-1351 (1998). (Pubitemid 29022536)
46. Nazor, K.E. et al. Immunodetection of disease-associated mutant PrP, which accelerates disease in GSS transgenic mice. EMBO J. 24, 2472-2480 (2005). (Pubitemid 41032597)
47. Colby, D.W. et al. Design and construction of diverse mammalian prion strains. Proc. Natl. Acad. Sci. USA 106, 20417-20422 (2009).
48. Colby, D.W. et al. Protease-sensitive synthetic prions. PLoS Pathog. 6, e1000736 (2010).
49. Makarava, N. et al. Recombinant prion protein induces a new transmissible prion disease in wild-type animals. Acta Neuropathol. 119, 177-187 (2010).
50. Wille, H. et al. Natural and synthetic prion structure from X-ray fiber diffraction. Proc. Natl. Acad. Sci. USA 106, 16990-16995 (2009).
51. Piro, J.R. et al. Seeding specificity and ultrastructural characteristics of infectious recombinant prions. Biochemistry 50, 7111-7116 (2011).
52. Smirnovas, V. et al. Structural organization of brain-derived mammalian prions examined by hydrogen-deuterium exchange. Nat. Struct. Mol. Biol. 18, 504-506 (2011).
53. Kocisko, D.A. et al. Cell-free formation of protease-resistant prion protein. Nature 370, 471-474 (1994). (Pubitemid 24263553)
54. Saborio, G.P., Permanne, B. & Soto, C. Sensitive detection of pathological prion protein by cyclic amplification of protein misfolding. Nature 411, 810-813 (2001). (Pubitemid 32588105)
55. Castilla, J. et al. Crossing the species barrier by PrPSc replication in vitro generates unique infectious prions. Cell 134, 757-768 (2008).
56. Meyerett, C. et al. In vitro strain adaptation of CWD prions by serial protein misfolding cyclic amplification. Virology 382, 267-276 (2008).
57. Kim, J.I., Surewicz, K., Gambetti, P. & Surewicz, W.K. The role of glycophosphatidylinositol anchor in the amplification of the scrapie isoform of prion protein in vitro. FEBS Lett. 583, 3671-3675 (2009).
58. Wang, F. et al. Genetic informational RNA is not required for recombinant prion infectivity. J. Virol. 86, 1874-1876 (2012).
59. Kim, J.I. et al. Mammalian prions generated from bacterially expressed prion protein in the absence of any mammalian cofactors. J. Biol. Chem. 285, 14083-14087 (2010).
60. Supattapone, S. Biochemistry. What makes a prion infectious? Science 327, 1091-1092 (2010).
61. Abid, K., Morales, R. & Soto, C. Cellular factors implicated in prion replication. FEBS Lett. 584, 2409-2414 (2010).
62. Deleault, N.R., Lucassen, R.W. & Supattapone, S. RNA molecules stimulate prion protein conversion. Nature 425, 717-720 (2003). (Pubitemid 37314314)
63. Cordeiro, Y. & Silva, J.L. The hypothesis of the catalytic action of nucleic acid on the conversion of prion protein. Protein Pept. Lett. 12, 251-255 (2005). (Pubitemid 40428415)
64. Caughey, B. Protease-resistant PrP accumulation and scrapie agent replication: a role for sulphated glycosaminoglycans? Biochem. Soc. Trans. 22, 163-167 (1994). (Pubitemid 24072410)
65. Cordeiro, Y. et al. DNA converts cellular prion protein into the beta-sheet conformation and inhibits prion peptide aggregation. J. Biol. Chem. 276, 49400-49409 (2001).
66. Adler, V. et al. Small, highly structured RNAs participate in the conversion of human recombinant PrP(Sen) to PrP(Res) in vitro. J. Mol. Biol. 332, 47-57 (2003). (Pubitemid 36999730)
67. Geoghegan, J.C. et al. Selective incorporation of polyanionic molecules into hamster prions. J. Biol. Chem. 282, 36341-36353 (2007).
68. Piro, J.R., Harris, B.T. & Supattapone, S. In situ photodegradation of incorporated polyanion does not alter prion infectivity. PLoS Pathog. 7, e1002001 (2011).
69. Nelson, R. & Eisenberg, D. Structural models of amyloid-like fibrils. Adv. Protein Chem. 73, 235-282 (2006). (Pubitemid 44960406)
70. Nelson, R. et al. Structure of the cross-β spine of amyloid-like fibrils. Nature 435, 773-778 (2005). (Pubitemid 40839722)
71. Wasmer, C. et al. Amyloid fibrils of the HET-s(218-289) prion form a β solenoid with a triangular hydrophobic core. Science 319, 1523-1526 (2008). (Pubitemid 351398180)
72. 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. 268, 20276-20284 (1993). (Pubitemid 23278933)
73. Caughey, B.W. et al. Secondary structure analysis of the scrapie-associated protein PrP 27-30 in water by infrared spectroscopy. Biochemistry 30, 7672-7680 (1991).
74. Baldwin, M.A. et al. Spectroscopic characterization of conformational differences between PrPC and PrPSc: an α-helix to β-sheet transition. Phil. Trans. R. Soc. Lond. B 343, 435-441 (1994).
75. Aucouturier, P., Kascsak, R.J., Frangione, B. & Wisniewski, T. Biochemical and conformational variability of human prion strains in sporadic Creutzfeldt-Jakob disease. Neurosci. Lett. 274, 33-36 (1999). (Pubitemid 29458972)
76. Caughey, B., Raymond, G.J. & Bessen, R.A. Strain-dependent differences in β-sheet conformations of abnormal prion protein. J. Biol. Chem. 273, 32230-32235 (1998). (Pubitemid 29177169)
77. Chesebro, B. et al. Anchorless prion protein results in infectious amyloid disease without clinical scrapie. Science 308, 1435-1439 (2005). (Pubitemid 40791292)
78. Baron, G.S. et al. Effect of glycans and the glycophosphatidylinositol anchor on strain dependent conformations of scrapie prion protein: improved purifications and infrared spectra. Biochemistry 50, 4479-4490 (2011).
79. Parchi, P. et al. Molecular basis of phenotypic variability in sporadic Creutzfeldt-Jakob disease. Ann. Neurol. 39, 767-778 (1996). (Pubitemid 26183813)
80. Cronier, S. et al. Detection and characterization of proteinase K-sensitive disease-related prion protein with thermolysin. Biochem. J. 416, 297-305 (2008).
81. Supattapone, S. et al. Prion protein of 106 residues creates an artifical transmission barrier for prion replication in transgenic mice. Cell 96, 869-878 (1999). (Pubitemid 29165089)
82. Bessen, R.A. & Marsh, R.F. Distinct PrP properties suggest the molecular basis of strain variation in transmissible mink encephalopathy. J. Virol. 68, 7859-7868 (1994). (Pubitemid 24362673)
83. Peretz, D. et al. A conformational transition at the N terminus of the prion protein features in formation of the scrapie isoform. J. Mol. Biol. 273, 614-622 (1997). (Pubitemid 27488803)
84. Williamson, R.A. et al. Mapping the prion protein using recombinant antibodies. J. Virol. 72, 9413-9418 (1998). (Pubitemid 28471899)
85. Merz, P.A., Somerville, R.A., Wisniewski, H.M., Manuelidis, L. & Manuelidis, E.E. Scrapie-associated fibrils in Creutzfeldt-Jakob disease. Nature 306, 474-476 (1983). (Pubitemid 14235567)
86. Sim, V.L. & Caughey, B. Ultrastructures and strain comparison of under-glycosylated scrapie prion fibrils. Neurobiol. Aging 30, 2031-2042 (2009).
87. Ayers, J.I. et al. The strain-encoded relationship between PrP replication, stability and processing in neurons is predictive of the incubation period of disease. PLoS Pathog. 7, e1001317 (2011).
88. Deleault, A.M., Deleault, N.R., Harris, B.T., Rees, J.R. & Supattapone, S. The effects of prion protein proteolysis and disaggregation on the strain properties of hamster scrapie. J. Gen. Virol. 89, 2642-2650 (2008).
89. Eanes, E.D. & Glenner, G.G. X-ray diffraction studies on amyloid filaments. J. Histochem. Cytochem. 16, 673-677 (1968).
90. Govaerts, C., Wille, H., Prusiner, S.B. & Cohen, F.E. Evidence for assembly of prions with left-handed β-helices into trimers. Proc. Natl. Acad. Sci. USA 101, 8342-8347 (2004). (Pubitemid 38736577)
91. Serag, A.A., Altenbach, C., Gingery, M., Hubbell, W.L. & Yeates, T.O. Arrangement of subunits and ordering of β-strands in an amyloid sheet. Nat. Struct. Biol. 9, 734-739 (2002).
92. Cobb, N.J., Sonnichsen, F.D., McHaourab, H. & Surewicz, W.K. Molecular architecture of human prion protein amyloid: a parallel, in-register β-structure. Proc. Natl. Acad. Sci. USA 104, 18946-18951 (2007).
93. Schuler, B., Rachel, R. & Seckler, R. Formation of fibrous aggregates from a non-native intermediate: the isolated P22 tailspike β-helix domain. J. Biol. Chem. 274, 18589-18596 (1999).
94. Junker, M. et al. Pertactin β-helix folding mechanism suggests common themes for the secretion and folding of autotransporter proteins. Proc. Natl. Acad. Sci. USA 103, 4918-4923 (2006).
95. DeMarco, M.L. & Daggett, V. From conversion to aggregation: protofibril formation of the prion protein. Proc. Natl. Acad. Sci. USA 101, 2293-2298 (2004). (Pubitemid 38269305)
96. Surewicz, W.K., Mantsch, H.H. & Chapman, D. Determination of protein secondary structure by Fourier transform infrared spectroscopy: a critical assessment. Biochemistry 32, 389-394 (1993). (Pubitemid 23034873)
97. 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 31, 27-31 (1992).
98. Brundin, P., Melki, R. & Kopito, R. Prion-like transmission of protein aggregates in neurodegenerative diseases. Nat. Rev. Mol. Cell Biol. 11, 301-307 (2010).
99. Frost, B. & Diamond, M.I. Prion-like mechanisms in neurodegenerative diseases. Nat. Rev. Neurosci. 11, 155-159 (2010).
100. Aguzzi, A. Cell biology: beyond the prion principle. Nature 459, 924-925 (2009).
101. Westermark, G.T. & Westermark, P. Prion-like aggregates: infectious agents in human disease. Trends Mol. Med. 16, 501-507 (2010).
102. Soto, C. & Estrada, L.D. Protein misfolding and neurodegeneration. Arch. Neurol. 65, 184-189 (2008). (Pubitemid 351240778)
103. Wickner, R.B. et al. Prions: proteins as genes and infectious entities. Genes Dev. 18, 470-485 (2004). (Pubitemid 38372804)
104. Uptain, S.M. & Lindquist, S. Prions as protein-based genetic elements. Annu. Rev. Microbiol. 56, 703-741 (2002). (Pubitemid 35217472)
105. Halfmann, R., Alberti, S. & Lindquist, S. Prions, protein homeostasis, and phenotypic diversity. Trends Cell Biol. 20, 125-133 (2010).
106. Halfmann, R. et al. Prions are a common mechanism for phenotypic inheritance in wild yeasts. Nature 482, 363-368 (2012).
107. Toyama, B.H., Kelly, M.J., Gross, J.D. & Weissman, J.S. The structural basis of yeast prion strain variants. Nature 449, 233-237 (2007). (Pubitemid 47402368)
108. Collinge, J. & Clarke, A.R. A general model of prion strains and their pathogenicity. Science 318, 930-936 (2007). (Pubitemid 350098981)