Two-rung Model of a Left-handed β-Helix for Prions Explains Species Barrier and Strain Variation in Transmissible Spongiform Encephalopathies

Journal of Molecular Biology

Volumn 360, Issue 4, 2006, Pages 907-920

  Langedijk, J P M ^a   Fuentes, G ^b   Boshuizen, R ^a   Bonvin, A M J J ^b  

^a Pepscan Systems   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

Author keywords

BSE; CJD; prion; strain; helix

Indexed keywords

METHIONINE; PRION PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BETA HELIX; BETA SHEET; BRAIN SPONGIOSIS; FIBER; HYDROGEN BOND; MODEL; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STRUCTURE; SEQUENCE HOMOLOGY; SIMULATION;

EID: 33745620145     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.05.042     Document Type: Article

References (79)

1. Collinge J. Prion diseases of humans and animals: their causes and molecular basis. Annu. Rev. Neurosci. 24 (2001) 519-550
2. Riek R., Hornemann S., Wider G., Billeter M., Glockshuber R., and Wuthrich K. NMR structure of the mouse prion protein domain PrP(121-321). Nature 382 (1996) 180-182
3. Donne D.G., Viles J.H., Groth D., Mehlhorn I., James T.L., Cohen F.E., Prusiner S.B., Wright P.E., and Dyson H.J. Structure of the recombinant full-length hamster prion protein PrP(29-231): the N terminus is highly flexible. Proc. Natl Acad. Sci. USA 94 (1997) 13452-13457
4. Knaus K.J., Morillas M., Swietnicki W., Malone M., Surewicz W.K., and Yee V.C. Crystal structure of the human prion protein reveals a mechanism for oligomerization. Nature Struct. Biol. 8 (2001) 770-774
5. Zahn R., Liu A., Luhrs T., Riek R., von Schroetter C., Lopez F., et al. NMR solution structure of the human prion protein. Proc. Natl Acad. Sci. USA 97 (2000) 145-150
6. Zahn R. The octapeptide repeats in mammalian prion protein constitute a pH-dependent folding and aggregation site. J. Mol. Biol. 334 (2003) 477-488
7. Peretz D., Williamson R.A., Matsunaga Y., Serban H., Pinilla C., Bastidas R.B., et al. A conformational transition at the N terminus of the prion protein features in formation of the scrapie isoform. J. Mol. Biol. 273 (1997) 614-622
8. Speare J.O., Rush III T.S., Bloom M.E., and Caughey B. The role of helix 1 aspartates and salt bridges in the stability and conversion of prion protein. J. Biol. Chem. 278 (2003) 12522-12529
9. Torrent J., Alvarez-Martinez M.T., Liautard J.P., Balny C., and Lange R. The role of the 132-160 region in prion protein conformational transitions. Protein Sci. 14 (2005) 956-967
10. Viles J.H., Donne D., Kroon G., Prusiner S.B., Cohen F.E., Dyson H.J., and Wright P.E. Local structural plasticity of the prion protein. Analysis of NMR relaxation dynamics. Biochemistry 40 (2001) 2743-2753
11. Caughey B.W., Dong A., Bhat K.S., Ernst D., Hayes S.F., and Caughey W.S. Secondary structure analysis of the scrapie-associated protein PrP 27-30 in water by infrared spectroscopy. Biochemistry 30 (1991) 7672-7680
12. Pan K.M., Baldwin M., Nguyen J., Gasset M., Serban A., Groth D., et al. Conversion of alpha-helices into beta-sheets features in the formation of the scrapie prion proteins. Proc. Natl Acad. Sci. USA 90 (1993) 10962-10966
13. Jenkins J., and Pickersgill R. The architecture of parallel beta-helices and related folds. Prog. Biophys. Mol. Biol. 77 (2001) 111-175
14. McColl I.H., Blanch E.W., Gill A.C., Rhie A.G., Ritchie M.A., Hecht L., et al. A new perspective on beta-sheet structures using vibrational Raman optical activity: from poly(L-lysine) to the prion protein. J. Am. Chem. Soc. 125 (2003) 10019-10026
15. DeMarco M.L., and Daggett V. From conversion to aggregation: protofibril formation of the prion protein. Proc. Natl Acad. Sci. USA 101 (2004) 2293-2298
16. Diaz-Avalos R., Long C., Fontano E., Balbirnie M., Grothe R., Eisenberg D., and Caspar D.L. Cross-beta order and diversity in nanocrystals of an amyloid-forming peptide. J. Mol. Biol. 330 (2003) 1165-1175
17. Balbirnie M., Grothe R., and Eisenberg D.S. An amyloid-forming peptide from the yeast prion Sup35 reveals a dehydrated beta-sheet structure for amyloid. Proc. Natl Acad. Sci. USA 98 (2001) 2375-2380
18. Benzinger T.L., Gregory D.M., Burkoth T.S., Miller-Auer H., Lynn D.G., Botto R.E., and Meredith S.C. Propagating structure of Alzheimer's beta-amyloid(10-35) is parallel beta-sheet with residues in exact register. Proc. Natl Acad. Sci. USA 95 (1998) 13407-13412
19. Jaroniec C.P., MacPhee C.E., Astrof N.S., Dobson C.M., and Griffin R.G. Molecular conformation of a peptide fragment of transthyretin in an amyloid fibril. Proc. Natl Acad. Sci. USA 99 (2002) 16748-51673
20. Tanaka M., Chien P., Yonekura K., and Weissman J.S. Mechanism of cross-species prion transmission: an infectious conformation compatible with two highly divergent yeast prion proteins. Cell 121 (2005) 49-62
21. Krishnan R., and Lindquist S.L. Structural insights into a yeast prion illuminate nucleation and strain diversity. Nature 435 (2005) 765-772
22. Ritter C., Maddelein M.L., Siemer A.B., Luhrs T., Ernst M., Meier B.H., Saupe S.J., and Riek R. Correlation of structural elements and infectivity of the HET-s prion. Nature 435 (2005) 844-848
23. Nelson R., Sawaya M.R., Balbirnie M., Madsen A.O., Riekel C., Grothe R., and Eisenberg D. Structure of the cross-beta spine of amyloid-like fibrils. Nature 435 (2005) 773-778
24. Perutz M.F., Finch J.T., Berriman J., and Lesk A. Amyloid fibers are water-filled nanotubes. Proc. Natl Acad. Sci. USA 99 (2002) 5591-5595
25. Lazo N.D., and Downing D.T. Amyloid fibrils may be assembled from beta-helical protofibrils. Biochemistry 37 (1998) 1731-1735
26. Wetzel R. Ideas of order for amyloid fibril structure. Structure (Camb) 10 (2002) 1031-1036
27. Wille H., Michelitsch M.D., Guenebaut V., Supattapone S., Serban A., Cohen F.E., et al. Structural studies of the scrapie prion protein by electron crystallography. Proc. Natl Acad. Sci. USA 99 (2002) 3563-3568
28. Govaerts C., Wille H., Prusiner S.B., and Cohen F.E. Evidence for assembly of prions with left-handed beta-helices into trimers. Proc. Natl Acad. Sci. USA 101 (2004) 8342-8347
29. Parisi G., Fornasari M.S., and Echave J. Dynactins p25 and p27 are predicted to adopt the LbetaH fold. FEBS Letters 562 (2004) 1-4
30. Bradley P., Cowen L., Menke M., King J., and Berger B. BETAWRAP: successful prediction of parallel beta -helices from primary sequence reveals an association with many microbial pathogens. Proc. Natl Acad. Sci. USA 98 (2001) 14819-14824
31. Barducci A., Chelli R., Procacci P., and Schettino V. Misfolding pathways of the prion protein probed by molecular dynamics simulations. Biophys. J. 88 (2005) 1334-1343
32. Ziegler J., Sticht H., Marx U.C., Muller W., Rosch P., and Schwarzinger S. CD and NMR studies of prion protein (PrP) helix 1. Novel implications for its role in the PrPC->PrPSc conversion process. J. Biol. Chem. 278 (2003) 50175-50181
33. Laws D.D., Bitter H.M., Liu K., Ball H.L., Kaneko K., Wille H., et al. Solid-state NMR studies of the secondary structure of a mutant prion protein fragment of 55 residues that induces neurodegeneration. Proc. Natl Acad. Sci. USA 98 (2001) 11686-11690
34. Salmona M., Morbin M., Massignan T., Colombo L., Mazzoleni G., Capobianco R., et al. Structural properties of Gerstmann-Straussler-Scheinker disease amyloid protein. J. Biol. Chem. 278 (2003) 48146-48153
35. Tagliavini F., Prelli F., Porro M., Rossi G., Giaccone G., Farlow M.R., et al. Amyloid fibrils in Gerstmann-Straussler-Scheinker disease (Indiana and Swedish kindreds) express only PrP peptides encoded by the mutant allele. Cell 79 (1994) 695-703
36. Boshuizen R.S., Langeveld J.P., Salmona M., Williams A., Meloen R.H., and Langedijk J.P. An in vitro screening assay based on synthetic prion protein peptides for identification of fibril-interfering compounds. Anal. Biochem. 333 (2004) 372-380
37. De Gioia L., Selvaggini C., Ghibaudi E., Diomede L., Bugiani O., Forloni G., et al. Conformational polymorphism of the amyloidogenic and neurotoxic peptide homologous to residues 106-126 of the prion protein. J. Biol. Chem. 269 (1994) 7859-7862
38. Forloni G., Angeretti N., Chiesa R., Monzani E., Salmona M., Bugiani O., and Tagliavini F. Neurotoxicity of a prion protein fragment. Nature 362 (1993) 543-546
39. Gasset M., Baldwin M.A., Lloyd D.H., Gabriel J.M., Holtzman D.M., Cohen F., et al. Predicted alpha-helical regions of the prion protein when synthesized as peptides form amyloid. Proc. Natl Acad. Sci. USA 89 (1992) 10940-10944
40. Schwede T., Kopp J., Guex N., and Peitsch M.C. SWISS-MODEL: An automated protein homology-modeling server. Nucl. Acids Res. 31 (2003) 3381-3385
41. Jing H., Takagi J., Liu J.H., Lindgren S., Zhang R.G., Joachimiak A., et al. Archaeal surface layer proteins contain beta propeller, PKD, and beta helix domains and are related to metazoan cell surface proteins. Structure (Camb) 10 (2002) 1453-1464
42. Freiberg A., Morona R., Van den Bosch L., Jung C., Behlke J., Carlin N., et al. The tailspike protein of Shigella phage Sf6. A structural homolog of Salmonella phage P22 tailspike protein without sequence similarity in the beta-helix domain. J. Biol. Chem. 278 (2003) 1542-1548
43. Guex N., and Peitsch M.C. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18 (1997) 2714-2723
44. Raetz C.R., and Roderick S.L. A left-handed parallel beta helix in the structure of UDP-N-acetylglucosamine acyltransferase. Science 270 (1995) 997-1000
45. Sulzenbacher G., Gal L., Peneff C., Fassy F., and Bourne Y. Crystal structure of Streptococcus pneumoniae N-acetylglucosamine-1-phosphate uridyltransferase bound to acetyl-coenzyme A reveals a novel active site architecture. J. Biol. Chem. 276 (2001) 11844-11851
46. Beaman T.W., Sugantino M., and Roderick S.L. Structure of the hexapeptide xenobiotic acetyltransferase from Pseudomonas aeruginosa. Biochemistry 37 (1998) 6689-6696
47. Pickersgill R., Smith D., Worboys K., and Jenkins J. Crystal structure of polygalacturonase from Erwinia carotovora ssp. carotovora. J. Biol. Chem. 273 (1998) 24660-24664
48. Huang W., Matte A., Li Y., Kim Y.S., Linhardt R.J., Su H., and Cygler M. Crystal structure of chondroitinase B from Flavobacterium heparinum and its complex with a disaccharide product at 1.7 Å resolution. J. Mol. Biol. 294 (1999) 1257-1269
49. Breydo L., Bocharova O.V., Makarava N., Salnikov V.V., Anderson M., and Baskakov I.V. Methionine oxidation interferes with conversion of the prion protein into the fibrillar proteinase K-resistant conformation. Biochemistry 44 (2005) 15534-15543
50. Kabsch W., and Sander C. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22 (1983) 2577-2637
51. Hun Lim K., Nguyen T.N., Damo S.M., Mazur T., Ball H.L., Prusiner S.B., et al. Solid-state NMR structural studies of the fibril form of a mutant mouse prion peptide PrP(89-143)(P101L). Solid State Nucl. Magn. Reson. 29 (2006) 183-190
52. Dominguez C., Boelens R., and Bonvin A.M. HADDOCK: a protein-protein docking approach based on biochemical or biophysical information. J. Am. Chem. Soc. 125 (2003) 1731-1737
53. Zhang C., Liu S., and Zhou Y.Q. Accurate and efficient loop selections by the DFIRE-based all-atom statistical potential. Protein Sci. 13 (2004) 391-399
54. Williamson R.A., Peretz D., Pinilla C., Ball H., Bastidas R.B., Rozenshteyn R., et al. Mapping the prion protein using recombinant antibodies. J. Virol. 72 (1998) 9413-9418
55. Prusiner S.B., Scott M., Foster D., Pan K.M., Groth D., Mirenda C., et al. Transgenetic studies implicate interactions between homologous PrP isoforms in scrapie prion replication. Cell 63 (1990) 673-686
56. Cartoni C., Schinina M.E., Maras B., Nonno R., Vaccari G., Di M., et al. Identification of the pathological prion protein allotypes in scrapie-infected heterozygous bank voles (Clethrionomys glareolus) by high-performance liquid chromatography-mass spectrometry. J. Chromatog. A 1081 (2005) 122-126
57. Supattapone S., Muramoto T., Legname G., Mehlhorn I., Cohen F.E., De Armond S.J., et al. Identification of two prion protein regions that modify scrapie incubation time. J. Virol. 75 (2001) 1408-1413
58. Hill A.F., Desbruslais M., Joiner S., Sidle K.C., Gowland I., Collinge J., et al. The same prion strain causes vCJD and BSE. Nature 389 (1997) 448-450
59. Telling G.C., Scott M., Hsiao K.K., Foster D., Yang S.L., Torchia M., et al. Transmission of Creutzfeldt-Jakob disease from humans to transgenic mice expressing chimeric human-mouse prion protein. Proc. Natl Acad. Sci. USA 91 (1994) 9936-9940
60. Bossers A., Belt P., Raymond G.J., Caughey B., de Vries R., and Smits M.A. Scrapie susceptibility-linked polymorphisms modulate the in vitro conversion of sheep prion protein to protease-resistant forms. Proc. Natl Acad. Sci. USA 94 (1997) 4931-4936
61. Goldmann W., Hunter N., Smith G., Foster J., and Hope J. PrP genotype and agent effects in scrapie: change in allelic interaction with different isolates of agent in sheep, a natural host of scrapie. J. Gen. Virol. 75 (1994) 989-995
62. Kocisko D.A., Priola S.A., Raymond G.J., Chesebro B., Lansbury Jr. P.T., and Caughey B. Species specificity in the cell-free conversion of prion protein to protease-resistant forms: a model for the scrapie species barrier. Proc. Natl Acad. Sci. USA 92 (1995) 3923-3927
63. Thuring C.M., Erkens J.H., Jacobs J.G., Bossers A., Van Keulen L.J., Garssen G.J., et al. Discrimination between scrapie and bovine spongiform encephalopathy in sheep by molecular size, immunoreactivity, and glycoprofile of prion protein. J. Clin. Microbiol. 42 (2004) 972-980
64. Tremblay P., Ball H.L., Kaneko K., Groth D., Hegde R.S., Cohen F.E., et al. Mutant PrPSc conformers induced by a synthetic peptide and several prion strains. J. Virol. 78 (2004) 2088-2099
65. Manson J.C., Jamieson E., Baybutt H., Tuzi N.L., Barron R., McConnell I., et al. A single amino acid alteration (101L) introduced into murine PrP dramatically alters incubation time of transmissible spongiform encephalopathy. EMBO J. 18 (1999) 6855-6864
66. Chien P., Weissman J.S., and De Pace A.H. Emerging principles of conformation-based prion inheritance. Annu. Rev. Biochem. 73 (2004) 617-656
67. Rost B. TOPITS: threading one-dimensional predictions into three-dimensional structures. Proc. Int. Conf. Intell. Syst. Mol. Biol. 3 (1995) 314-321
68. Rost B. PHD: predicting one-dimensional protein structure by profile-based neural networks. Methods Enzymol. 266 (1996) 525-539
69. Peitsch M.C. ProMod and Swiss-Model: Internet-based tools for automated comparative protein modelling. Biochem. Soc. Trans. 24 (1996) 274-279
70. Hooft R.W., Vriend G., Sander C., and Abola E.E. Errors in protein structures. Nature 381 (1996) 272
71. Lindahl E., Hess B., and van der Spoel D. GROMACS 3.0: A package for molecular simulation and trajectory analisys. J. Mol. Modeling 7 (2001) 306-317
72. Daura X., Mark A.E., and van Gunsteren W.F. Parametrization of aliphatic CHn united atoms of GROMOS96 force field. J. Comput. Chem. 19 (1998) 535-547
73. Berendsen H.J.C., Postma J.P.M., van Gunsteren W.F., and Hermans J. Interaction models for water in relation to protein hydration. In: Pullman B. (Ed). Intermolecular Forces (1981), Reidel Publishing Company, Dordrecht 331-342
74. Berendsen H.J.C., Postma J.P.M., van Gunsteren W.F., Di Nola A., and Haak J.R. Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81 (1984) 3684-3690
75. Hess B., Bekker H., Berendsen H.J.C., and Fraaije J.G.E.M. LINCS: a linear constraint solver for molecular simulations. J. Comput. Chem. 18 (1997) 1463-1472
76. van Gunsteren W.F., and Berendsen H.J.C. Computer-simulation of molecular-dynamics-methodology, applications, and perspectives in chemistry. Angew. Chem.-Int. Ed, English 29 (1990) 992-1023
77. Tironi I.G., Sperb R., Smith P.E., and Vangunsteren W.F. A generalized reaction field method for molecular-dynamics simulations. J. Chem. Phys. 102 (1995) 5451-5459
78. Hsu S.-T.D., and Bonvin A.M.J.J. Atomic insight into the CD4 binding-induced conformational changes in HIV-1 gp120. Proteins: Struct. Funct. Genet. 55 (2004) 582-593
79. Jorgensen W.L., and Tirado-Rives J. The OPLS potential functions for proteins. Energy minimizations for crystals of cyclin peptides and crambin. J. Am. Chem. Soc. 110 (1988) 1657-1666