Spontaneous β-helical fold in prion protein: The case of PrP(82-146)

Proteins: Structure, Function and Bioinformatics

Volumn 75, Issue 4, 2009, Pages 964-976

  Saracino, Gloria A A ^a   Villa, Alessandra ^b   Moro, Giorgio ^a   Cosentino, Ugo ^a   Salmona, Mario ^c  

^a UNIVERSITY OF MILANO BICOCCA   (Italy)

^b GOETHE UNIVERSITY   (Germany)

^c MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

Author keywords

Conformational flexibility; Fibrils; Molecular dynamics; Prion peptide; Right handed helix

Indexed keywords

AMYLOID; PRION PROTEIN;

ARTICLE; BETA SHEET; CONTROLLED STUDY; HUMAN; KINETICS; MOLECULAR DYNAMICS; PRION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN FOLDING; SEQUENCE ANALYSIS; SIMULATION;

AMINO ACID SEQUENCE; CLUSTER ANALYSIS; COMPUTER SIMULATION; HYDROGEN BONDING; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PRIONS; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY;

RUMEX;

EID: 66149179016     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.22306     Document Type: Article

References (73)

1. Prusiner SB. Molecular biology of prion disease. Science 1991;252:1515-1522.
2. Prusiner SB, Scott MR, De Armond SJ, Cohen FE. Prion protein biology. Cell 1998;93:337-348. (Pubitemid 28232079)
3. Caughey BW, Dong A, Bhat KS, Ernst D, Hayes SF, Caughey WS. Secondary structure analysis of the scrapie-associated protein PrP 27-30 in water by infrared spectroscopy. Biochemistry 1991;30:7672-7680.
4. Pan KM, Baldwin M, Nguyen J, Gasset M, Serban A, Groth D, Mehlhorn I, Huang Z, Fletterick RJ, Cohen FE, Prusiner SB. Conversion of alpha-helices into beta-sheets features in the formation of the scrapie prion proteins. Proc Natl Acad Sci USA 1993;90:10962-10966. (Pubitemid 2007975)
5. De Armond SJ, Yang SL, Lee A, Bowler R, Tarabolous A, Groth D, Prusiner SB. Three scrapie prion isolates exhibit different accumulation patterns of the prion protein scrapie isoform. Proc Natl Acad Sci USA 1993;90:6449-6453. (Pubitemid 23207230)
6. Williams A, Lucassen PJ, Ritchie D, Bruce M. PrP deposition, microglial activation, and neuronal apoptosis in murine scrapie. Expt Neurol 1997;144:433-438. (Pubitemid 27224571)
7. James TL, Liu H, Ulyanov NB, Farr-Jones S, Zhang H, Donne DG, Kaneko K, Groth D, Mehlhorn I, Prusiner SB, Cohen FE. Solution structure of a 142-residue recombinant prion protein corresponding to the infectious fragment of the scrapie isoform. Proc Natl Acad Sci USA 1997;94:10086-10091. (Pubitemid 27406998)
8. Donne DG, Viles JH, Groth D, Mehlhorn I, James TL, Cohen FE, Prusiner SB, Wright PE, Dyson HJ. Structure of the recombinant full-length hamster prion protein PrP(29-231): the N terminus is highly flexible. Proc Natl Acad Sci USA 1997;94:13452-13457.
9. Zhan R, Liu H, Lührs T, Riek R, von Schroetter C, Garcia L, Billiter M, Calzolai L, Wider G, Wüthrich K. NMR solution structure of the human prion protein. Proc Natl Acad Sci USA 2000;97:145-150. (Pubitemid 30055798)
10. Wille H, Zhang GF, Baldwin MA, Cohen FE, Prusiner SB. Separation of scrapie prion infectivity from PrP amyloid polymers. J Mol Biol 1996;259:608-621. (Pubitemid 26226002)
11. Laws DD, Bitter HML, Liu K, Bell HL, Kaneko K, Wille H, Cohen FE, Prusiner SB, Pines A, Wemmer DE. 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 2001;98:11686-11690.
12. Wille H, Michelitsch MD, Guènebaut V, Supattopone S, Serban A, Cohen FE, Agard DA, Prusiner SB. Structural studies of the scrapie prion protein by electron crystallography. Proc Natl Acad Sci USA 2002;99:3563-3568. (Pubitemid 34252147)
13. Peretz D, Williamson RA, Matsunaga Y, Serban H, Pinilla C, Bastidas RB, Rozenhsteyn R, James TL, Houghten RA, Cohen FE. A conformational transition at the N terminus of the prion protein features in formation of the scrapie isoform. J Mol Biol 1997;273:614-622. (Pubitemid 27488803)
14. Williamson RA, Peretz D, Pinilla C, Ball H, Bastidas RB, Rozenshteyn R, Houghten RA, Prusiner SB, Burton DR. Mapping the prion protein using recombinant antibodies. J Virol 1998;72:9413-9418. (Pubitemid 28471899)
15. Muramoto T, Scott M, Cohen FE, Prusiner SB. Recombinant scrapie-like prion protein of 106 amino acids is soluble. Proc Natl Acad Sci USA 1996;93:15457-15462. (Pubitemid 27009621)
16. Taylor JP, Hardy J, Fischbeck KH. Toxic proteins in neurodegenerative disease. Science 2002;296:1991-1995. (Pubitemid 34627514)
17. Bucciantini M, Giannoni E, Chiti F, Baroni F, Formigli L, Zurdo J, Taddei N, Ramponi G, Dobson CM, Stefani M. Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases Nature 2002;416:507-511.
18. Kayed R, Head E, Thompson JL,McIntire TM, Milton SC, Cotman CW, Glabe CG. Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 2003;300: 486-489. (Pubitemid 36444329)
19. Caughey B, Lansbury PT. Protofibrils, pores, fibrils, and neurodegeneration: separating the responsible protein aggregates from the innocent bystanders. Annu Rev Neurosci 2003;26:267-298. (Pubitemid 37064935)
20. Dobson CM. Protein folding and misfolding. Nature 2003;426:884-890. (Pubitemid 38056880)
21. Fändrich M, Dobson C. The behavior of poly amino acids reveals an inverse side chain effect in amyloid structure formation. EMBO J 2002;21:5682-5690. (Pubitemid 35315268)
22. Sunde M, Serpell LC, Bartlam M, Fraser PE, Pepys MB, Blake CC. Common core structure of amyloid fibrils by synchrotron X-ray diffraction. J Mol Biol 1997;273:729-739. (Pubitemid 27488813)
23. Chiti F, Stefani M, Taddei N, Ramponi G, Dobson CM. Rationalization mutational effects on protein aggregation rates. Nature 2003;424:805-808.
24. Forloni G, Angeretti N, Chiesa R, Monzani E, Salmona M, Bugiani O, Tagliavini F. Neurotoxicity of a prion protein fragment. Nature 1993;362:543-546. (Pubitemid 23113029)
25. Brown DR, Schmidt B, Kretzschmar HA. Role of microglia and host prion protein in neurotoxicity of a prion protein fragment. Nature 1996;380:345-347. (Pubitemid 26097115)
26. Tagliavini F, Prelli F, Verga L, Giaccone G, Sarma R, Gorevic P, Ghetti B, Passerini F, Ghibaudi E, Forloni G, Salmona M, Bugiani O, Frangioni B. Synthetic peptides homologous to prion protein residues 106-147 form amyloid-like fibrils in vitro. Proc Natl Acad Sci USA 1993;90:9678-9682. (Pubitemid 23315849)
27. Selvaggini C, De Gioa L, Cantù L, Ghibaudi E, Diomede L, Passerini F, Forloni G, Bugiani O, Tagliavini F, Salmona M. Molecular characteristics of a protease-resistant, amyloidogenic and neurotoxic peptide homologous to residues 106-126 of the prion protein. Biochem Biophys Res Commun 1993;194:1380-1386. (Pubitemid 23255035)
28. De Gioia L, Selvaggini C, Ghibaudi E, Diomede L, Bugiani O, Forloni G, Tagliavini F, Salmona M. Conformational polymorphism of the amyloidogenic and neurotoxic peptide homologous to residues 106-126 of the prion protein. J Biol Chem 1994;269:7859-7862. (Pubitemid 24200181)
29. Salmona M, Malesani P, De Gioia L, Gorla S, Bruschi M, Molinari A, DellaVedova R, Pedrotti B, Marrari MA, Awan T, Bugiani O, Forloni G, Tagliavini F. Molecular determinants of the physicochemical properties of a critical prion protein region comprising residues 106-126. Biochem J 1999;342:207-214. (Pubitemid 29410867)
30. Ragg E, Tagliavini F, Malesani P, Monticelli L, Bugiani O, Forloni G, Salmona M. Determination of solution conformations of PrP106-126, a neurotoxic fragment of prion protein, by 1H NMR and restrained molecular dynamics. Eur J Biochem 1999;266:1192-1201. (Pubitemid 30010139)
31. Kuwata K, Matumoto T, Cheng H, Nagayama K, James TL, Roder H. NMR-detected hydrogen exchange and molecular dynamics simulations provide structural insight into fibril formation of prion protein fragment 106-126. Proc Natl Acad Sci USA 2003;100: 14790-14795. (Pubitemid 37517969)
32. Villa A, Mark AE, Saracino GAA, Cosentino U, Pitea D, Moro G, Salmona M. Conformational polymorphism of the PrP106-126 peptide in different environments: a molecular dynamics study. J Phys Chem B 2006;110:1423-1428. (Pubitemid 43301145)
33. C delta114-121 in scrapie-infected mouse neuroblastoma cells leads to trans-dominant inhibition of wild-type PrP(Sc) accumulation. J Virol 1998;72:1153-1159.
34. C complex that leads to prion propagation. J Biol Chem 2005;280:27236-27243.
35. Brown DR. Prion protein peptides: optimal toxicity and peptide blockade of toxicity. Mol Cell Neurosci 2000;15:66-78. (Pubitemid 30090381)
36. Tagliavini F, Lievens PM, Tranchant C, Warter JM, Mohr M, Giaccone G, Perini F, Rossi G, Salmona M, Piccardo P, Ghetti B, Beavis RC, Bugiano O, Frangione B, Prelli F. A 7-kDa prion protein (PrP) fragment, an integral component of the PrP region required for infectivity, is the major amyloid protein in Gerstmann-Sträussler-Scheinker disease. A117V. J Biol Chem 2001;276:6009-6015. (Pubitemid 37385759)
37. Salmona M, Morbin M, Massignan T, Colombo L, Mazzoleni G, Capobianco R, Diomede L, Thaler F, Mollica L, Musco G, Kourie JJ, Bugiani O, Sharma D, Inouye H, Kirschner DA, Forloni G, Tagliavini F. Structural properties of Gerstmann-Straüssler-Scheinker disease amyloid protein. J Biol Chem 2003;278:48146-48153. (Pubitemid 37523267)
38. Govaerts C, Wille H, Prusiner SB, Cohen FE. Evidence for assembly of prions with left-handed beta-helices into trimers. Proc Natl Acad Sci 2004;101:8342-8347. (Pubitemid 38736577)
39. Lee SW, Mou Y, Lin SY, Chou FC, Tseng WH, Chen Ch, Lu CYD, Yu SSF, Chan JCC. Steric zipper of the amyloid fibrils formed by residues 109-122 of the Syrian hamster prion protein. J Mol Biol 2008;378:1142-1145.
40. van Gunsteren WF, Bakowies D, Baron R, Chandrasekhar I, Christen M, Daura X, Gee P, Geerke DP, Glättli A, Hünenberger PH, Kastenholz MA, Oostenbrink C, Schenk M, Trzesniak D, van der Vegt NF, Yu HB. Biomolecular modeling: goals, problems, perspectives. Angew Chem Int Ed Engl 2006;45:4064-4092. (Pubitemid 44105659)
41. Karplus M, McCammon JA. Molecular dynamics simulations of biomolecules. Nat Struct Biol 2002;9:646-652.
42. Kazmirski SL, Alonso DOV, Cohen FE, Prusiner SB, Daggett V. Theoretical studies of sequence effects on the conformational properties of a fragment of the prion protein: implications for scrapie formation. Chem Biol 1995;2:305-315.
43. Daidone I, Simona F, Roccatano D, Broglia RA, Tiana G, Colombo G, Di Nola A. Beta-hairpin conformation of fibrillogenic peptides: structure and alpha-beta transition mechanism revealed by molecular dynamics simulations. Proteins 2004;57:198-204. (Pubitemid 39195893)
44. Ma B, Nussinov R. Molecular dynamics simulations of alanine rich beta-sheet oligomers: insight into amyloid formation. Prot Sci 2002;11:2335-2350.
45. Levy Y, Hanan E, Solomon B, Becker OM. Helix-coil transition of PrP106-126: molecular dynamic study. Proteins 2001;45:382-396. (Pubitemid 33108073)
46. Langedijk JPM, Fuentes G, Boshuizen R, Bonvin AMJJ. Two-rung model of a left-handed beta-helix for prions explains species barrier and strain variation in transmissible spongiform encephalopathies. J Mol Biol 2006;360:907-920. (Pubitemid 43993917)
47. Sugita Y, Okamoto Y. Replica-exchange molecular dynamics method for protein folding. Chem Phys Lett 1999;314:141-151. (Pubitemid 129556751)
48. Okabe T, Kawata M, Okamoto Y, Mikami M. Replica-exchange Monte Carlo method for the isobaric-isothermal ensemble. Chem Phys Lett 2001;335:435-439. (Pubitemid 33628069)
49. van Gunsteren WF, Billeter SR, Eising AA, Hünenberger PH, Krüger P, Mark AE, Scott WRP, Tironi IG. Biomolecular simulation: the GROMOS96 manual and user guide. Zürich: Vdf Hochschulverlag AG an der ETH Zürich; 1996.
50. Berendsen HJC, Postma JPM, van Gunsteren WF, Hermans J. Intermolecular forces. In: Pulman B, editor. D. Reidel Publishing Company: Dordrecht 1981. pp 331.
51. Lindahl E, Hess B, van der Spoel D. GROMACS 3.0: a package for molecular simulation and trajectory analysis. JMolModel 2001;7:306-317. (Pubitemid 36153547)
52. van der Spoel D, Lindahl E, Hess B, Groenhof G, Mark AE, Berendsen HJC. GROMACS: fast, flexible, and free. J Comput Chem 2005;26:1701-1718.
53. Tironi IG, Sperb R, Smith PE, van Gunsteren WF. A generalized reaction field method for molecular dynamics simulations. J Chem Phys 1995;102:5451-5459.
54. Berendsen HJC, Postma JPM, van Gunsteren WF, Di Nola A, Haak JR. Molecular dynamics with coupling to an external bath. J Chem Phys 1984;81:3684-3690.
55. Miyamoto S, Kollman PA. Settle: an analytical version of the SHAKE and RATTLE algorithm for rigid water models. J Comput Chem 1992;13:952-962.
56. Hess B, Bekker H, Berendsen HJC, Fraaije JGEM. LINCS: a linear constraint solver for molecular simulations. J Comput Chem 1997;18:1463-1472. (Pubitemid 127637344)
57. Daura X, Gademann K, Jaun B, Seebach D, van Gunsteren WF, Mark AE. Peptide folding: when simulation meets experiment. Angew Chem Int Ed 1999;38:236-240. (Pubitemid 29051239)
58. Kabsch W, Sander C. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 1983;22:2577-2637.
59. Eisenhaber F, Lijnzaad P, Argos P, Sander C, Scharf M. The double cubic lattice method: efficient approaches to numerical integration of surface area and volume and to dot surface contouring of molecular assemblies. J Comput Chem 1995;16:273-284.
60. Eisenberg D, McLachlan AD. Solvation energy in protein folding and binding. Nature 1986;319:199-203. (Pubitemid 16128783)
61. Amadei A, Linssen ABM, Berendsen HJC. Essential dynamics of proteins. Proteins 1993;17:412-425. (Pubitemid 23358549)
62. Taraboulos A, Scott M, Semenov A, Avraham D, Laszlo L, Prusiner SB. Cholesterol depletion and modification of COOH-terminal targeting sequence of the prion protein inhibit formation of the scrapie isoform. J Cell Biol 1995;129:121-132.
63. Vey M, Pilkuhn S, Wille H, Nixon R, De Armond SJ, Smart EJ, Anderson RGW, Taraboulos A, Prusiner SB. Subcellular colocalization of the cellular and scrapie prion proteins in caveolae-like membranous domains. Proc Natl Acad Sci USA 1996;93:14945-14949. (Pubitemid 26419075)
64. Nguyen JT, Inouye H, Baldwin MA, Fleeterick RJ, Cohen FE, Prusiner SB, Kirschner DA. X-ray diffraction of scrapie prion rods and PrP peptides. J Mol Biol 1995;252:412-422.
65. Daley ME, Spyracopoulos L, Jia Z, Davies PL, Sykes BD. Structure and dynamics of a beta-helical antifreeze protein. Biochemistry 2002;41:5515-5525.
66. Zhang H, Kaneko K, Nguyen JT, Livshits TL, Baldwin MA, Cohen FE, James TL, Prusiner SB. Conformational transitions in peptides containing two putative alpha-helices of the prion protein. J Mol Biol 1995;250:514-526.
67. Chabry J, Caughey B, Chesebro B. Specific inhibition of in vitro formation of protease-resistant prion protein by synthetic peptides. J Biol Chem 1998;273:13203-13207. (Pubitemid 28246891)
68. Ziegler J, Viehrig C, Geimer S, Rösh P, Schwarzinger S. Putative aggregation initiation sites in prion protein. FEBS Letters 2006;580:2033-2040.
69. Alonso DOV, De Armond SJ, Cohen FE, Daggett V. Mapping the early steps in the pH-induced conformational conversion of the prion protein. Proc Natl Acad Sci USA 2001;98:2985-2989. (Pubitemid 32220786)
70. De Marco ML, Daggett V. From conversion to aggregation: protofibril formation of the prion protein. Proc Natl Acad Sci USA 2004;101:2293-2298. (Pubitemid 38269305)
71. Inouye H, Kirshner DA. Polypeptide chain folding in the hydrophobic core of hamster scrapie prion: analysis by X-ray diffraction. J Struct Biol 1998;122:247-255. (Pubitemid 28411205)
72. C. Proc Natl Acad Sci USA 2007;104:11551-11556.
73. Gobbi M, Colombo L, Morbin M, Mazzoleni G, Accardo E, Vanoni M, Del favero E, Cantù L, Kirshner DA, Manzoni C, Beeg M, Ceci P, Ubezio P, Forloni G, Tagliavini F, Salmona M. Gerstmann-Sträussler-Scheinker disease amyloid protein polymerizes according to the "dock-and-lock" model. J Biol Chem 2006;281:843-849.