Parallel in-register intermolecular β-sheet architectures for prion-seeded prion protein (PrP) amyloids

Journal of Biological Chemistry

Volumn 289, Issue 35, 2014, Pages 24129-24142

  Groveman, Bradley R ^a   Dolan, Michael A ^b   Taubner, Lara M ^a,d   Kraus, Allison ^a   Wickner, Reed B ^c   Caughey, Byron ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^c NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^d Analytical 360 LLC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARCHITECTURE; MAMMALS; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEINS;

CELLULAR PRION PROTEINS; CONFORMATIONAL CONSTRAINTS; DETAILED MODELS; MOLECULAR DYNAMICS SIMULATIONS; SHEET STRUCTURE; SOLID STATE NMR; STRUCTURAL MODELS; TEMPLATE-DRIVEN;

GLYCOPROTEINS;

AMYLOID PROTEIN; PRION PROTEIN; RECOMBINANT PROTEIN; AMYLOID; DISULFIDE; POLYSACCHARIDE; PRION;

AMINO TERMINAL SEQUENCE; ARTICLE; BETA SHEET; CARBOXY TERMINAL SEQUENCE; MOLECULAR DYNAMICS; MOLECULAR MODEL; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN STRUCTURE; VIRUS REPLICATION; VIRUS STRAIN; CARBON NUCLEAR MAGNETIC RESONANCE; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; PROTEIN DEGRADATION; SCANNING TRANSMISSION ELECTRON MICROSCOPY;

AMYLOID; CARBON-13 MAGNETIC RESONANCE SPECTROSCOPY; DISULFIDES; MICROSCOPY, ELECTRON, SCANNING TRANSMISSION; MODELS, MOLECULAR; POLYSACCHARIDES; PRIONS; PROTEOLYSIS;

EID: 84906861755     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.578344     Document Type: Article

References (68)

1. Prusiner, S. B. (1998) Prions. Proc. Natl. Acad. Sci. U.S.A. 95, 13363-13383
2. Kraus, A., Groveman, B. R., and Caughey, B. (2013) Prions and the potential transmissibility of protein misfolding diseases. Annu. Rev. Microbiol. 67, 543-564
3. Caughey, B., Baron, G. S., Chesebro, B., and Jeffrey, M. (2009) Getting a grip on prions: oligomers, amyloids, anchors and pathological membrane interactions. Annu. Rev. Biochem. 78, 177-204
4. Caughey, B., and Baron, G. S. (2006) Prions and their partners in crime. Nature 443, 803-810 (Pubitemid 44622685)
5. Linden, R., Martins, V. R., Prado, M. A., Cammarota, M., Izquierdo, I., and Brentani, R. R. (2008) Physiology of the prion protein. Physiol. Rev. 88, 673-728 (Pubitemid 351520090)
6. Wüthrich, K., and Riek, R. (2001) Three-dimensional structures of prion proteins. Adv. Protein Chem. 57, 55-82 (Pubitemid 32622680)
7. McKinley, M. P., Taraboulos, A., Kenaga, L., Serban, D., Stieber, A., DeArmond, S. J., Prusiner, S. B., and Gonatas, N. (1991) Ultrastructural localization of scrapie prion proteins in cytoplasmic vesicles of infected cultured cells. Lab. Invest. 65, 622-630
8. Gabizon, R., McKinley, M. P., Groth, D. F., Kenaga, L., and Prusiner, S. B. (1988) Properties of scrapie prion protein liposomes. J. Biol. Chem. 263, 4950-4955
9. Govaerts, C., Wille, H., Prusiner, S. B., and Cohen, F. E. (2004) Evidence for assembly of prions with left-handed β-helices into trimers. Proc. Natl. Acad. Sci. U.S.A. 101, 8342-8347 (Pubitemid 38736577)
10. Silveira, J. R., Raymond, G. J., Hughson, A. G., Race, R. E., Sim, V. L., Hayes, S. F., and Caughey, B. (2005) The most infectious prion protein particles. Nature 437, 257-261 (Pubitemid 41294488)
11. 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
12. Piro, J. R., Wang, F., Walsh, D. J., Rees, J. R., Ma, J., and Supattapone, S. (2011) Seeding specificity and ultrastructural characteristics of infectious recombinant prions. Biochemistry 50, 7111-7116
13. Merz, P. A., Somerville, R. A., Wisniewski, H. M., and Iqbal, K. (1981) Abnormal fibrils from scrapie-infected brain. Acta Neuropathol. 54, 63-74 (Pubitemid 11047598)
14. Sim, V. L., and Caughey, B. (2009) Ultrastructures and strain comparison of under-glycosylated scrapie prion fibrils. Neurobiol. Aging 30, 2031-2042
15. 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
16. Pan, K.-M., Baldwin, M., Nguyen, J., Gasset, M., Serban, A., Groth, D., Mehlhorn, I., Huang, Z., Fletterick, R. J., Cohen, F. E., and Prusiner, S. B. (1993) Conversion of α-helices into β-sheets features in the formation of the scrapie prion protein. Proc. Natl. Acad. Sci. U.S.A. 90, 10962-10966
17. Safar, J., Roller, P. P., Gajdusek, D. C., and Gibbs, C. J., Jr. (1993) Conformational transitions, dissociation, and unfolding of scrapie amyloid (prion) protein. J. Biol. Chem. 268, 20276-20284 (Pubitemid 23278933)
18. Oesch, B., Westaway, D., Wälchli, M., McKinley, M. P., Kent, S. B., Aebersold, R., Barry, R. A., Tempst, P., Teplow, D. B., and Hood, L. E. (1985) A cellular gene encodes scrapie PrP 27-30 protein. Cell 40, 735-746 (Pubitemid 15240279)
19. McKinley, M. P., Bolton, D. C., and Prusiner, S. B. (1983) A protease-resistant protein is a structural component of the scrapie prion. Cell 35, 57-62 (Pubitemid 14240218)
20. Hope, J., Multhaup, G., Reekie, L. J., Kimberlin, R. H., and Beyreuther, K. (1988) Molecular pathology of scrapie-associated fibril protein (PrP) in mouse brain affected by the ME7 strain of scrapie. Eur. J. Biochem. 172, 271-277
21. Basler, K., Oesch, B., Scott, M., Westaway, D., Wälchli, M., Groth, D. F., McKinley, M. P., Prusiner, S. B., and Weissmann, C. (1986) Scrapie and cellular PrP isoforms are encoded by the same chromosomal gene. Cell 46, 417-428 (Pubitemid 16031678)
22. 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
23. 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
24. Wang, F., Wang, X., Yuan, C. G., and Ma, J. (2010) Generating a prion with bacterially expressed recombinant prion protein. Science 327, 1132-1135
25. 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
26. 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
27. 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
28. 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
29. Tycko, R., Savtchenko, R., Ostapchenko, V. G., Makarava, N., and Baskakov, I. V. (2010) The α-helical C-terminal domain of full-length recombinant PrP converts to an in-register parallel β-sheet structure in PrP fibrils: evidence from solid state nuclear magnetic resonance. Biochemistry 49, 9488-9497
30. Helmus, J. J., Surewicz, K., Nadaud, P. S., Surewicz, W. K., and Jaroniec, C. P. (2008) Molecular conformation and dynamics of the Y145Stop variant of human prion protein in amyloid fibrils. Proc. Natl. Acad. Sci. U.S.A. 105, 6284-6289 (Pubitemid 351758338)
31. Helmus, J. J., Surewicz, K., Apostol, M. I., Surewicz, W. K., and Jaroniec, C. P. (2011) Intermolecular alignment in Y145Stop human prion protein amyloid fibrils probed by solid-state NMR spectroscopy. J. Am. Chem. Soc. 133, 13934-13937
32. Adrover, M., Pauwels, K., Prigent, S., de Chiara, C., Xu, Z., Chapuis, C., Pastore, A., and Rezaei, H. (2010) Prion fibrillization is mediated by a native structural element that comprises helices H2 and H3. J. Biol. Chem. 285, 21004-21012
33. Wickner, R. B., Edskes, H. K., Bateman, D. A., Kelly, A. C., Gorkovskiy, A., Dayani, Y., and Zhou, A. (2013) Amyloids and yeast prion biology. Biochemistry 52, 1514-1527
34. Toyama, B. H., and Weissman, J. S. (2011) Amyloid structure: conformational diversity and consequences. Annu. Rev. Biochem. 80, 557-585
35. Shewmaker, F., Wickner, R. B., and Tycko, R. (2006) Amyloid of the prion domain of Sup35p has an in-register parallel β-sheet structure. Proc. Natl. Acad. Sci. U.S.A. 103, 19754-19759 (Pubitemid 46037503)
36. Baxa, U., Wickner, R. B., Steven, A. C., Anderson, D. E., Marekov, L. N., Yau, W. M., and Tycko, R. (2007) Characterization of β-sheet structure in Ure2p1-89 yeast prion fibrils by solid-state nuclear magnetic resonance. Biochemistry 46, 13149-13162 (Pubitemid 350086233)
37. Wickner, R. B., Dyda, F., and Tycko, R. (2008) Amyloid of Rnq1p, the basis of the [PIN+] prion, has a parallel in-register β-sheet structure. Proc. Natl. Acad. Sci. U.S.A. 105, 2403-2408 (Pubitemid 351520526)
38. Antzutkin, O. N., Balbach, J. J., Leapman, R. D., Rizzo, N. W., Reed, J., and Tycko, R. (2000) Multiple quantum solid-state NMR indicates a parallel, not antiparallel, organization of β-sheets in Alzheimer's β-amyloid fibrils. Proc. Natl. Acad. Sci. U.S.A. 97, 13045-13050
39. Tycko, R. (2011) Solid-state NMR studies of amyloid fibril structure. Annu. Rev. Phys. Chem. 62, 279-299
40. Benzinger, T. L., Gregory, D. M., Burkoth, T. S., Miller-Auer, H., Lynn, D. G., Botto, R. E., and Meredith, S. C. (1998) Propagating structure of Alzheimer's β-amyloid(10-35) is parallel β-sheet with residues in exact register. Proc. Natl. Acad. Sci. U.S.A. 95, 13407-13412
41. Tycko, R. (2007) Symmetry-based constant-time homonuclear dipolar recoupling in solid state NMR. J. Chem. Phys. 126, 064506
42. Wilham, J. M., Orrú, C. D., Bessen, R. A., Atarashi, R., Sano, K., Race, B., Meade-White, K. D., Taubner, L. M., Timmes, A., and Caughey, B. (2010) Rapid end-point quantitation of prion seeding activity with sensitivity comparable to bioassays. PLoS Pathog. 6, e1001217
43. Atarashi, R., Wilham, J. M., Christensen, L., Hughson, A. G., Moore, R. A., Johnson, L. M., Onwubiko, H. A., Priola, S. A., and Caughey, B. (2008) Simplified ultrasensitive prion detection by recombinant PrP conversion with shaking. Nat. Methods 5, 211-212
44. Caughey, B., Raymond, G. J., Ernst, D., and Race, R. E. (1991) N-terminal truncation of the scrapie-associated form of PrP by lysosomal protease(s): implications regarding the site of conversion of PrP to the protease-resistant state. J. Virol. 65, 6597-6603
45. Petkova, A. T., and Tycko, R. (2002) Sensitivity enhancement in structural measurements by solid state NMR through pulsed spin locking. J. Magn. Reson. 155, 293-299
46. Hafner-Bratkovic, I., Bester, R., Pristovsek, P., Gaedtke, L., Veranic, P., Gaspersic, J., Mancek-Keber, M., Avbelj, M., Polymenidou, M., Julius, C., Aguzzi, A., Vorberg, I., and Jerala, R. (2011) Globular domain of the prion protein needs to be unlocked by domain swapping to support prion protein conversion. J. Biol. Chem. 286, 12149-12156
47. Klose, D. P., Wallace, B. A., and Janes, R. W. (2010) 2Struc: the secondary structure server. Bioinformatics 26, 2624-2625
48. Atarashi, R., Moore, R. A., Sim, V. L., Hughson, A. G., Dorward, D. W., Onwubiko, H. A., Priola, S. A., and Caughey, B. (2007) Ultrasensitive detection of scrapie prion protein using seeded conversion of recombinant prion protein. Nat. Methods 4, 645-650 (Pubitemid 47202476)
49. 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
50. Wishart, D. S., Sykes, B. D., and Richards, F. M. (1991) Relationship between nuclear-magnetic-resonance chemical-shift and protein secondary structure. J. Mol. Biol. 222, 311-333 (Pubitemid 121004009)
51. Welker, E., Raymond, L. D., Scheraga, H. A., and Caughey, B. (2002) Intramolecular versus intermolecular disulfide bonds in prion proteins. J. Biol. Chem. 277, 33477-33481 (Pubitemid 34984871)
52. Herrmann, L. M., and Caughey, B. (1998) The importance of the disulfide bond in prion protein conversion. Neuroreport 9, 2457-2461 (Pubitemid 28387130)
53. Turk, E., Teplow, D. B., Hood, L. E., and Prusiner, S. B. (1988) Purification and properties of the cellular and scrapie hamster prion proteins. Eur. J. Biochem. 176, 21-30
54. Eisenberg, D., and Jucker, M. (2012) The amyloid state of proteins in human diseases. Cell 148, 1188-1203
55. Shewmaker, F., Ross, E. D., Tycko, R., and Wickner, R. B. (2008) Amyloids of shuffled prion domains that form prions have a parallel in-register β-sheet structure. Biochemistry 47, 4000-4007 (Pubitemid 351458114)
56. Paramithiotis, E., Pinard, M., Lawton, T., LaBoissiere, S., Leathers, V. L., Zou, W. Q., Estey, L. A., Lamontagne, J., Lehto, M. T., Kondejewski, L. H., Francoeur, G. P., Papadopoulos, M., Haghighat, A., Spatz, S. J., Head, M., Will, R., Ironside, J., O'Rourke, K., Tonelli, Q., Ledebur, H. C., Chakrabartty, A., and Cashman, N. R. (2003) A prion protein epitope selective for the pathologically misfolded conformation. Nat. Med. 9, 893-899 (Pubitemid 36889932)
57. Kocisko, D. A., Lansbury, P. T., Jr., and Caughey, B. (1996) Partial unfolding and refolding of scrapie-associated prion protein: evidence for a critical 16-kDa C-terminal domain. Biochemistry 35, 13434-13442 (Pubitemid 26349439)
58. Vázquez-Fernández, E., Alonso, J., Pastrana, M. A., Ramos, A., Stitz, L., Vidal, E., Dynin, I., Petsch, B., Silva, C. J., and Requena, J. R. (2012) Structural organization of mammalian prions as probed by limited proteolysis. PLoS ONE 7, e50111
59. Sajnani, G., Pastrana, M. A., Dynin, I., Onisko, B., and Requena, J. R. (2008) Scrapie prion protein structural constraints obtained by limited proteolysis and mass spectrometry. J. Mol. Biol. 382, 88-98
60. Supattapone, S., Bosque, P., Muramoto, T., Wille, H., Aagaard, C., Peretz, D., Nguyen, H. O., Heinrich, C., Torchia, M., Safar, J., Cohen, F. E., DeArmond, S. J., Prusiner, S. B., and Scott, M. (1999) Prion protein of 106 residues creates an artificial transmission barrier for prion replication in transgenic mice. Cell 96, 869-878 (Pubitemid 29165089)
61. DeMarco, M. L., and Daggett, V. (2004) From conversion to aggregation: protofibril formation of the prion protein. Proc. Natl. Acad. Sci. U.S.A. 101, 2293-2298 (Pubitemid 38269305)
62. 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 (Pubitemid 47175337)
63. Deleault, N. R., Geoghegan, J. C., Nishina, K., Kascsak, R., Williamson, R. A., and Supattapone, S. (2005) Protease-resistant prion protein amplification reconstituted with partially purified substrates and synthetic polyanions. J. Biol. Chem. 280, 26873-26879 (Pubitemid 41040721)
64. Onisko, B., Fernández, E. G., Freire, M. L., Schwarz, A., Baier, M., Camiña, F., García, J. R., Rodríguez-Segade Villamarín, S., and Requena, J. R. (2005) Probing PrPSc structure using chemical cross-linking and mass spectrometry: evidence of the proximity of Gly-90 amino termini in the PrP 27-30 aggregate. Biochemistry 44, 10100-10109 (Pubitemid 41076805)
65. Wickner, R. B., Shewmaker, F., Edskes, H., Kryndushkin, D., Nemecek, J., McGlinchey, R., Bateman, D., and Winchester, C. L. (2010) Prion amyloid structure explains templating: how proteins can be genes. FEMS Yeast Res. 10, 980-991
66. DebBurman, S. K., Raymond, G. J., Caughey, B., and Lindquist, S. (1997) Chaperone-supervised conversion of prion protein to its protease-resistant form. Proc. Natl. Acad. Sci. U.S.A. 94, 13938-13943
67. Horiuchi, M., Priola, S. A., Chabry, J., and Caughey, B. (2000) Interactions between heterologous forms of prion protein: binding, inhibition of conversion, and species barriers. Proc. Natl. Acad. Sci. U.S.A. 97, 5836-5841 (Pubitemid 30367485)
68. Orrú, C. D., Wilham, J. M., Raymond, L. D., Kuhn, F., Schroeder, B., Raeber, A. J., and Caughey, B. (2011) Prion disease blood test using immunoprecipitation and improved quaking-induced conversion. MBio. 2, e00078-e00011