Evaluating prion models based on comprehensive mutation data of mouse PrP

Structure

Volumn 22, Issue 4, 2014, Pages 560-571

  Shirai, Tsuyoshi ^a,b   Saito, Mihoko ^a,b,e   Kobayashi, Atsushi ^c   Asano, Masahiro ^c   Hizume, Masaki ^c   Ikeda, Shino ^c   Teruya, Kenta ^c,f   Morita, Masanori ^c,d,g   Kitamoto, Tetsuyuki ^c  

^a NAGAHAMA INSTITUTE OF BIO SCIENCE AND TECHNOLOGY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d Research and Development Division Benesis Corporation   (Japan)

^e UNIVERSITY OF TOKYO   (Japan)

^f KYOTO PREFECTURAL UNIVERSITY OF MEDICINE   (Japan)

^g Japan Blood Products Organization   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; PRION PROTEIN; RECOMBINANT PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; MOUSE; NONHUMAN; POINT MUTATION; PRION; PRIORITY JOURNAL; PROTEIN STRUCTURE; STRUCTURE ANALYSIS; AMINO ACID SEQUENCE; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; CYTOLOGY; GENE EXPRESSION; GENETIC TRANSFECTION; GENETICS; METABOLISM; MOLECULAR GENETICS; NERVE CELL; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SITE DIRECTED MUTAGENESIS; TUMOR CELL LINE; ANIMAL CELL; BETA SHEET; GENE CONVERSION; MOLECULAR MODEL; PROTEIN MODIFICATION;

AMINO ACID SEQUENCE; ANIMALS; CELL LINE, TUMOR; GENE EXPRESSION; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; NEURONS; POINT MUTATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PRPSC PROTEINS; RECOMBINANT PROTEINS; TRANSFECTION;

EID: 84898431660     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2013.12.019     Document Type: Article

References (66)

1. M. Asano, S. Mohri, J.W. Ironside, M. Ito, N. Tamaoki, and T. Kitamoto vCJD prion acquires altered virulence through trans-species infection Biochem. Biophys. Res. Commun. 342 2006 293 299
2. G.S. Baron, A.G. Hughson, G.J. Raymond, D.K. Offerdahl, K.A. Barton, L.D. Raymond, D.W. Dorward, and B. Caughey Effect of glycans and the glycophosphatidylinositol anchor on strain dependent conformations of scrapie prion protein: improved purifications and infrared spectra Biochemistry 50 2011 4479 4490
3. I.V. Baskakov, and L. Breydo Converting the prion protein: what makes the protein infectious Biochim. Biophys. Acta 1772 2007 692 703
4. E. Biasini, M.E. Seegulam, B.N. Patti, L. Solforosi, A.Z. Medrano, H.M. Christensen, A. Senatore, R. Chiesa, R.A. Williamson, and D.A. Harris et al. Non-infectious aggregates of the prion protein react with several PrPSc-directed antibodies J. Neurochem. 105 2008 2190 2204
5. D.A. Butler, M.R. Scott, J.M. Bockman, D.R. Borchelt, A. Taraboulos, K.K. Hsiao, D.T. Kingsbury, and S.B. Prusiner Scrapie-infected murine neuroblastoma cells produce protease-resistant prion proteins J. Virol. 62 1988 1558 1564
6. B.W. Caughey, A. Dong, K.S. Bhat, D. Ernst, S.F. Hayes, and W.S. Caughey Secondary structure analysis of the scrapie-associated protein PrP 27-30 in water by infrared spectroscopy Biochemistry 30 1991 7672 7680
7. B. Caughey, G.J. Raymond, and R.A. Bessen Strain-dependent differences in beta-sheet conformations of abnormal prion protein J. Biol. Chem. 273 1998 32230 32235
8. B. Caughey, G.S. Baron, B. Chesebro, and M. Jeffrey Getting a grip on prions: oligomers, amyloids, and pathological membrane interactions Annu. Rev. Biochem. 78 2009 177 204
9. CCP4 Collaborative Computational Project, Number 4 The CCP4 suite: programs for protein crystallography Acta Crystallogr. D Biol. Crystallogr. 50 1994 760 763
10. B. Chesebro, M. Trifilo, R. Race, K. Meade-White, C. Teng, R. LaCasse, L. Raymond, C. Favara, G. Baron, and S. Priola et al. Anchorless prion protein results in infectious amyloid disease without clinical scrapie Science 308 2005 1435 1439
11. N.J. Cobb, F.D. Sönnichsen, H. McHaourab, and W.K. Surewicz Molecular architecture of human prion protein amyloid: a parallel, in-register beta-structure Proc. Natl. Acad. Sci. USA 104 2007 18946 18951
12. J. Collinge, and A.R. Clarke A general model of prion strains and their pathogenicity Science 318 2007 930 936
13. M.L. DeMarco, and V. Daggett From conversion to aggregation: protofibril formation of the prion protein Proc. Natl. Acad. Sci. USA 101 2004 2293 2298
14. R. Diaz-Espinoza, and C. Soto Generation of prions in vitro and the protein-only hypothesis Prion 4 2010 53 59
15. R. Diaz-Espinoza, and C. Soto High-resolution structure of infectious prion protein: the final frontier Nat. Struct. Mol. Biol. 19 2012 370 377
16. F. Eghiaian, T. Daubenfeld, Y. Quenet, M. van Audenhaege, A.P. Bouin, G. van der Rest, J. Grosclaude, and H. Rezaei Diversity in prion protein oligomerization pathways results from domain expansion as revealed by hydrogen/deuterium exchange and disulfide linkage Proc. Natl. Acad. Sci. USA 104 2007 7414 7419
17. P. Emsley, B. Lohkamp, W.G. Scott, and K. Cowtan Features and development of Coot Acta Crystallogr. D Biol. Crystallogr. 66 2010 486 501
18. A.R. Fersht, and V. Daggett Protein folding and unfolding at atomic resolution Cell 108 2002 573 582
19. M. Gasset, M.A. Baldwin, R.J. Fletterick, and S.B. Prusiner Perturbation of the secondary structure of the scrapie prion protein under conditions that alter infectivity Proc. Natl. Acad. Sci. USA 90 1993 1 5
20. C. Govaerts, H. Wille, S.B. Prusiner, and F.E. Cohen Evidence for assembly of prions with left-handed beta-helices into trimers Proc. Natl. Acad. Sci. USA 101 2004 8342 8347
21. H. Hara, Y. Okemoto-Nakamura, F. Shinkai-Ouchi, K. Hanada, Y. Yamakawa, and K. Hagiwara Mouse prion protein (PrP) segment 100 to 104 regulates conversion of PrP(C) to PrP(Sc) in prion-infected neuroblastoma cells J. Virol. 86 2012 5626 5636
22. L.M. Herrmann, and B. Caughey The importance of the disulfide bond in prion protein conversion Neuroreport 9 1998 2457 2461
23. C. Hiraga, A. Kobayashi, and T. Kitamoto The number of octapeptide repeat affects the expression and conversion of prion protein Biochem. Biophys. Res. Commun. 382 2009 715 719
24. M. Hizume, A. Kobayashi, H. Mizusawa, and T. Kitamoto Amino acid conditions near the GPI anchor attachment site of prion protein for the conversion and the GPI anchoring Biochem. Biophys. Res. Commun. 391 2010 1681 1686
25. S. Ikeda, A. Kobayashi, and T. Kitamoto Thr but Asn of the N-glycosylation sites of PrP is indispensable for its misfolding Biochem. Biophys. Res. Commun. 369 2008 1195 1198
26. K. Kaneko, L. Zulianello, M. Scott, C.M. Cooper, A.C. Wallace, T.L. James, F.E. Cohen, and S.B. Prusiner Evidence for protein X binding to a discontinuous epitope on the cellular prion protein during scrapie prion propagation Proc. Natl. Acad. Sci. USA 94 1997 10069 10074
27. R.J. Kascsak, R. Rubenstein, P.A. Merz, M. Tonna-DeMasi, R. Fersko, R.I. Carp, H.M. Wisniewski, and H. Diringer Mouse polyclonal and monoclonal antibody to scrapie-associated fibril proteins J. Virol. 61 1987 3688 3693
28. K.C. Kunes, S.C. Clark, D.L. Cox, and R.R. Singh Left handed beta helix models for mammalian prion fibrils Prion 2 2008 81 90
29. J.P. Langedijk, G. Fuentes, R. Boshuizen, and A.M. Bonvin Two-rung model of a left-handed beta-helix for prions explains species barrier and strain variation in transmissible spongiform encephalopathies J. Mol. Biol. 360 2006 907 920
30. X. Lu, P.L. Wintrode, and W.K. Surewicz Beta-sheet core of human prion protein amyloid fibrils as determined by hydrogen/deuterium exchange Proc. Natl. Acad. Sci. USA 104 2007 1510 1515
31. T. Lührs, C. Ritter, M. Adrian, D. Riek-Loher, B. Bohrmann, H. Döbeli, D. Schubert, and R. Riek 3D structure of Alzheimer's amyloid-beta(1-42) fibrils Proc. Natl. Acad. Sci. USA 102 2005 17342 17347
32. R. Lüthy, J.U. Bowie, and D. Eisenberg Assessment of protein models with three-dimensional profiles Nature 356 1992 83 85
33. N. Makarava, G.G. Kovacs, O. Bocharova, R. Savtchenko, I. Alexeeva, H. Budka, R.G. Rohwer, and I.V. Baskakov Recombinant prion protein induces a new transmissible prion disease in wild-type animals Acta Neuropathol. 119 2010 177 187
34. N. Mizuno, U. Baxa, and A.C. Steven Structural dependence of HET-s amyloid fibril infectivity assessed by cryoelectron microscopy Proc. Natl. Acad. Sci. USA 108 2011 3252 3257
35. G. Moroncini, N. Kanu, L. Solforosi, G. Abalos, G.C. Telling, M. Head, J. Ironside, J.P. Brockes, D.R. Burton, and R.A. Williamson Motif-grafted antibodies containing the replicative interface of cellular PrP are specific for PrPSc Proc. Natl. Acad. Sci. USA 101 2004 10404 10409
36. T. Muramoto, T. Tanaka, N. Kitamoto, C. Sano, Y. Hayashi, T. Kutomi, C. Yutani, and T. Kitamoto Analyses of Gerstmann-Straussler syndrome with 102Leu219Lys using monoclonal antibodies that specifically detect human prion protein with 219Glu Neurosci. Lett. 288 2000 179 182
37. G.N. Murshudov, A.A. Vagin, and E.J. Dodson Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr. D Biol. Crystallogr. 53 1997 240 255
38. J.T. Nguyen, H. Inouye, M.A. Baldwin, R.J. Fletterick, F.E. Cohen, S.B. Prusiner, and D.A. Kirschner X-ray diffraction of scrapie prion rods and PrP peptides J. Mol. Biol. 252 1995 412 422
39. M. Ota, Y. Isogai, and K. Nishikawa Knowledge-based potential defined for a rotamer library to design protein sequences Protein Eng. 14 2001 557 564
40. V. Perrier, K. Kaneko, J. Safar, J. Vergara, P. Tremblay, S.J. DeArmond, F.E. Cohen, S.B. Prusiner, and A.C. Wallace Dominant-negative inhibition of prion replication in transgenic mice Proc. Natl. Acad. Sci. USA 99 2002 13079 13084
41. E.F. Pettersen, T.D. Goddard, C.C. Huang, G.S. Couch, D.M. Greenblatt, E.C. Meng, and T.E. Ferrin UCSF Chimera - a visualization system for exploratory research and analysis J. Comput. Chem. 25 2004 1605 1612
42. S.B. Prusiner Molecular biology of prion diseases Science 252 1991 1515 1522
43. S.B. Prusiner Prions Proc. Natl. Acad. Sci. USA 95 1998 13363 13383
44. R.E. Race, B. Caughey, K. Graham, D. Ernst, and B. Chesebro Analyses of frequency of infection, specific infectivity, and prion protein biosynthesis in scrapie-infected neuroblastoma cell clones J. Virol. 62 1988 2845 2849
45. R. Riek, S. Hornemann, G. Wider, M. Billeter, R. Glockshuber, and K. Wüthrich NMR structure of the mouse prion protein domain PrP(121-231) Nature 382 1996 180 182
46. A. Rigter, J.P. Langeveld, D. Timmers-Parohi, J.G. Jacobs, P.L. Moonen, and A. Bossers Mapping of possible prion protein self-interaction domains using peptide arrays BMC Biochem. 8 2007 6
47. A. Rigter, J. Priem, D. Timmers-Parohi, J.P. Langeveld, F.G. van Zijderveld, and A. Bossers Prion protein self-peptides modulate prion interactions and conversion BMC Biochem. 10 2009 29
48. M. Rogers, F. Yehiely, M. Scott, and S.B. Prusiner Conversion of truncated and elongated prion proteins into the scrapie isoform in cultured cells Proc. Natl. Acad. Sci. USA 90 1993 3182 3186
49. J. Safar, H. Wille, V. Itri, D. Groth, H. Serban, M. Torchia, F.E. Cohen, and S.B. Prusiner Eight prion strains have PrP(Sc) molecules with different conformations Nat. Med. 4 1998 1157 1165
50. G. Sajnani, M.A. Pastrana, I. Dynin, B. Onisko, and J.R. Requena Scrapie prion protein structural constraints obtained by limited proteolysis and mass spectrometry J. Mol. Biol. 382 2008 88 98
51. K. Sasaki, J. Gaikwad, S. Hashiguchi, T. Kubota, K. Sugimura, W. Kremer, H.R. Kalbitzer, and K. Akasaka Reversible monomer-oligomer transition in human prion protein Prion 2 2008 118 122
52. M.R. Sawaya, S. Sambashivan, R. Nelson, M.I. Ivanova, S.A. Sievers, M.I. Apostol, M.J. Thompson, M. Balbirnie, J.J. Wiltzius, and H.T. McFarlane et al. Atomic structures of amyloid cross-beta spines reveal varied steric zippers Nature 447 2007 453 457
53. M.R. Scott, R. Köhler, D. Foster, and S.B. Prusiner Chimeric prion protein expression in cultured cells and transgenic mice Protein Sci. 1 1992 986 997
54. R.A. Shikiya, and J.C. Bartz In vitro generation of high-titer prions J. Virol. 85 2011 13439 13442
55. S.S. Sidhu, and A.A. Kossiakoff Exploring and designing protein function with restricted diversity Curr. Opin. Chem. Biol. 11 2007 347 354
56. V.L. Sim, and B. Caughey Ultrastructures and strain comparison of under-glycosylated scrapie prion fibrils Neurobiol. Aging 30 2009 2031 2042
57. V. Smirnovas, G.S. Baron, D.K. Offerdahl, G.J. Raymond, B. Caughey, and W.K. Surewicz Structural organization of brain-derived mammalian prions examined by hydrogen-deuterium exchange Nat. Struct. Mol. Biol. 18 2011 504 506
58. L. Solforosi, A. Bellon, M. Schaller, J.T. Cruite, G.C. Abalos, and R.A. Williamson Toward molecular dissection of PrPC-PrPSc interactions J. Biol. Chem. 282 2007 7465 7471
59. A.R. Spevacek, E.G. Evans, J.L. Miller, H.C. Meyer, J.G. Pelton, and G.L. Millhauser Zinc drives a tertiary fold in the prion protein with familial disease mutation sites at the interface Structure 21 2013 236 246
60. E. Stimson, J. Hope, A. Chong, and A.L. Burlingame Site-specific characterization of the N-linked glycans of murine prion protein by high-performance liquid chromatography/electrospray mass spectrometry and exoglycosidase digestions Biochemistry 38 1999 4885 4895
61. J. Stöhr, N. Weinmann, H. Wille, T. Kaimann, L. Nagel-Steger, E. Birkmann, G. Panza, S.B. Prusiner, M. Eigen, and D. Riesner Mechanisms of prion protein assembly into amyloid Proc. Natl. Acad. Sci. USA 105 2008 2409 2414
62. M.H. Tattum, S. Cohen-Krausz, K. Thumanu, C.W. Wharton, A. Khalili-Shirazi, G.S. Jackson, E.V. Orlova, J. Collinge, A.R. Clarke, and H.R. Saibil Elongated oligomers assemble into mammalian PrP amyloid fibrils J. Mol. Biol. 357 2006 975 985
63. E. Vázquez-Fernández, J. Alonso, M.A. Pastrana, A. Ramos, L. Stitz, E. Vidal, I. Dynin, B. Petsch, C.J. Silva, and J.R. Requena Structural organization of mammalian prions as probed by limited proteolysis PLoS ONE 7 2012 e50111
64. C. Wasmer, A. Lange, H. Van Melckebeke, A.B. Siemer, R. Riek, and B.H. Meier Amyloid fibrils of the HET-s(218-289) prion form a beta solenoid with a triangular hydrophobic core Science 319 2008 1523 1526
65. H. Wille, M.D. Michelitsch, V. Guenebaut, S. Supattapone, A. Serban, F.E. Cohen, D.A. Agard, and S.B. Prusiner Structural studies of the scrapie prion protein by electron crystallography Proc. Natl. Acad. Sci. USA 99 2002 3563 3568
66. H. Wille, W. Bian, M. McDonald, A. Kendall, D.W. Colby, L. Bloch, J. Ollesch, A.L. Borovinskiy, F.E. Cohen, S.B. Prusiner, and G. Stubbs Natural and synthetic prion structure from X-ray fiber diffraction Proc. Natl. Acad. Sci. USA 106 2009 16990 16995