A cylinder-shaped double ribbon structure formed by an amyloid hairpin peptide derived from the β-sheet of murine PrP: An X-ray and molecular dynamics simulation study

Journal of Structural Biology

Volumn 150, Issue 3, 2005, Pages 284-299

  Croixmarie, Vincent ^a   Briki, Fatma ^d   David, Gabriel ^d   Coïc, Yves Marie ^b   Ovtracht, Ludmila ^c,e   Doucet, Jean ^d   Jamin, Nadège ^c   Sanson, A ^c  

^a CEA DIF   (France)

^b INSTITUT PASTEUR   (France)

^c CEA SACLAY   (France)

^d UNIVERSITÉ PARIS SUD   (France)

^e SORBONNE UNIVERSITÉ   (France)

Author keywords

Amyloid fibrils; MD simulation; Modeling; Peptide aggregation; X ray diffraction

Indexed keywords

AMYLOID; ARGINYLGLYCYLTYROSYLMETHIONYLLEUCYLGLYCYLSERYLALANYLASPARTYLPROLYL ASPARAGINYLGLYCYLASPARAGINYLGLUTAMINYLVALYLTYROSYLTYROSYLARGINYLGLYCINE; PRION PROTEIN; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO ACID SEQUENCE; ARTICLE; BETA SHEET; ELECTRON MICROSCOPY; MOLECULAR DYNAMICS; NONHUMAN; PEPTIDE SYNTHESIS; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN STRUCTURE; X RAY DIFFRACTION;

AMINO ACID SEQUENCE; AMYLOID; AMYLOID BETA-PROTEIN; ANIMALS; DNA MUTATIONAL ANALYSIS; MAGNETIC RESONANCE SPECTROSCOPY; MICE; MICROSCOPY, ELECTRON; MICROSCOPY, ELECTRON, TRANSMISSION; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDES; PRIONS; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; SOFTWARE; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; TIME FACTORS; X-RAY DIFFRACTION;

MURINAE;

EID: 18844387881     PISSN: 10478477     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jsb.2005.03.003     Document Type: Article

References (52)

1. O.N. Antzutkin, J.J. Balbach, R.D. Leapman, N.W. Rizzo, J. Reed, and R. Tycko Multiple quantum solid state NMR indicates a parallel, not antiparallel, organization of β-sheets in Alzheimer's β-amyloid fibrils Proc. Natl. Acad. Sci. USA 97 2000 13045 13050
2. O.N. Antzutkin, R.D. Leapman, J.J. Balbach, and R. Tycko Supramolecular structural constraints on Alzheimer's β-amyloid fibrils from electron microscopy and solid state nuclear magnetic resonance Biochemistry 41 2002 15436 15450
3. R.S. Armen, M.L. DeMarco, D.O.V. Alonso, and V. Daggett Pauling and Corey's α-pleated sheet structure may define the prefibrillar amyloidogenic intermediate in amyloid disease Proc. Natl. Acad. Sci. USA 101 2004 11622 11627
4. J.J. Balbach, A.T. Petkova, N.A. Oyler, O.N. Antzutkin, D.J. Gordon, S.C. Meredith, and R. Tycko Supramolecular structure in full-length Alzheimer's β-amyloid fibrils: evidence for a parallel beta-sheet organization from solid-state nuclear magnetic resonance Biophys. J. 83 2002 1205 1216
5. J. Bandekar Amide modes and protein conformation Biochim. Biophys. Acta 1120 1992 123 143
6. A. Barth The infrared absorption of amino acid side chains Prog. Biophys. Mol. Biol. 74 2000 141 173
7. C. Blake, and L. Serpell Synchrotron X-ray studies suggest that the core of the transthyretin amyloid fibril is a continuous β-sheet helix Structure 4 1996 989 998
8. L. Bousset, F. Briki, J. Doucet, and R. Melki The native-like conformation of Ure2p in fibrils assembled under physiologically relevant conditions switches to an amyloid-like conformation upon heat-treatment of the fibrils J. Struct. Biol. 141 2003 132 142
9. F. Briki, B. Busson, and J. Doucet Organization of microfibrils in keratin fibers studied by X-ray scattering modelling using the paracrystal concept Biochim. Biophys. Acta 1429 1998 57 68
10. B.R. Brooks, R.E. Bruccoleri, B.D. Olafson, D.J. States, S. Swaminathan, and M. Karplus CHARMM: a program for macromolecular energy, minimization, and dynamics calculations J. Comp. Chem. 4 1983 187 217
11. W.C. Chan, and P.D. White Fmoc Solid Phase Peptide Synthesis: A Practical Approach 2000 Oxford University Press Oxford
12. J.P. Cleary, D.M. Walsh, J.J. Hofmeister, G.M. Shankar, M.A. Kuskowski, D.J. Selkoe, and K.H. Ashe Natural oligomers of the amyloid-B protein specifically disrupt cognitive function Nat. Neurosci. 8 2005 79 84
13. P. Derreumaux Evidence that the 127-164 region of prion proteins has two equi-energetic conformations with β or α features Biophys. J. 81 2001 1657 1665
14. C.M. Dobson Protein misfolding, evolution and disease Trends Biochem. Sci. 24 1999 329 332
15. J. Doucet, and J.P. Benoit Molecular dynamics studied by analysis of the X-ray diffuse scattering from lysozyme crystals Nature 325 1987 643 646
16. C. Govaerts, H. Wille, S.B. Prusiner, and F.E. Cohen Evidence for assembly of prions with left-handed β-helices into trimers Proc. Natl. Acad. Sci. USA 101 2004 8342 8347
17. J. Gsponer, U. Haberthür, and A. Caflisch The role of side-chain interactions in the early steps of aggregation: molecular dynamics simulations of an amyloid-forming peptide from the yeast prion Sup35 Proc. Natl. Acad. Sci. USA 100 2003 5154 5159
18. J. Guo, R. Wetzel, and Y. Xu Molecular modeling of the core of Aβ amyloid fibrils Proteins 57 2004 357 364
19. L.F. Haire, S.M. Whyte, N. Vasisht, A.C. Gill, C. Verma, E.J. Dodson, G.G. Dodson, and P.M. Bayley The crystal structure of the globular domain of sheep prion protein J. Mol. Biol. 336 2004 1175 1183
20. W. Humphrey, A. Dalke, and K. Schulten VMD-visual molecular dynamics J. Mol. Graphics 14 1996 33 38
21. E.G. Hutchinson, and J.M. Thornton A revised set of potentials for β-turn formation in protein Protein Sci. 3 1994 2207 2216
22. T. Huynh, J.C. Smith, and A. Sanson Protein unfolding transitions in an intrinsically unstable annexing domain: molecular dynamics simulation and comparison with nuclear magnetic resonance data Biophys. J. 83 2002 681 698
23. W. Hwang, S. Zhang, R.D. Kamm, and M. Karplus Kinetic control of dimer structure formation in amyloid fibrillogenesis Proc. Natl. Acad. Sci. USA 101 2004 12916 12921
24. H. Inouye, J.E. Bond, S.P. Deverin, A. Lim, C.E. Costello, and D.A. Kirschner Molecular organizaation of amyloid protofilament-like assembly of betabellin 15D: helical array of beta-sandwiches Biophys. J. 83 2002 1716 1727
25. M.I. Ivanova, M.R. Sawaya, M. Gingery, A. Attinger, and D. Eisenberg An amyloid-forming segment of β 2-microglobulin suggests a molecular model for the fibril Proc. Natl. Acad. Sci. USA 101 2004 10584 10589
26. N. Jamin, Y.-M. Coic, C. Landon, L. Ovtracht, F. Baleux, J.-M. Neumann, and A. Sanson Most of the structural elements of the globular domain of murine prion protein form fibrils with predominant β-sheet structure FEBS Lett. 529 2002 256 260
27. R. Kahn, R. Fourme, A. Gadet, J. Janin, C. Dumas, and D. André Macromolecular crystallography with synchrotron radiation: photographic data collection and polarization correction J. Appl. Cryst. 15 1982 330 337
28. 16-22 amyloid peptides into antiparallel β sheets Structure 11 2002 295 307
29. J. Kubelka, and T.A. Keiderling Differentiation of β-sheet-forming structures: ab initio-based simulations of IR absorption and vibrational CD for model peptide and protein β-sheets J. Am. Chem. Soc. 123 2001 12048 12058
30. M. Lopez de la Paz, K. Goldie, J. Zurdo, E. Lacroix, C.M. Dobson, A. Hoenger, and L. Serrano De novo designed peptide-based amyloid fibrils Proc. Natl. Acad. Sci. USA 99 2002 16052 16057
31. M. Lopez de la Paz, and L. Serrano Sequence determinants of amyloid fibril formation Proc. Natl. Acad. Sci. USA 101 2004 87 92
32. B. Ma, and R. Nussinov Molecular dynamics simulations of a β-hairpin fragment of protein G: balance between side-chain and backbone forces J. Mol. Biol. 296 2000 1091 1104
33. B. Ma, and R. Nussinov Molecular dynamics simulation of alanine rich β-sheet oligomers: insight into amyloid formation Protein Sci. 11 2002 2335 2350
34. B. Ma, and R. Nussinov Energy landscape and dynamics of the β-hairpin G peptide and isomers: topology and sequences Protein Sci. 12 2003 1882 1893
35. E. Paci, J. Gsponer, X. Salvatella, and M. Vendruscolo Molecular dynamics studies of the process of amyloid aggregation of peptide fragments of transthyretin J. Mol. Biol. 340 2004 555 569
36. M.F. Perutz, J.T. Finch, J. Berriman, and A. Lesk Amyloid fibers are water-filled nanotubes Proc. Natl. Acad. Sci. USA 99 2002 5591 5595
37. A.T. Petkova, Y. Ishii, J.J. Balbach, O.J. Antzutkin, R.D. Leapman, F. Delaglio, and R. Tycko A structural model for Alzheimer's β-amyloid fibrils based on experimental constraints from solid state NMR Proc. Natl. Acad. Sci. USA 99 2002 16742 16747
38. C.A. Ross, and M.A. Poirier Protein aggregation and neurodegenerative disease Nat. Med. 10 2004 S7 S10
39. K.S. Satheeshkumar, and R. Jayakumar Conformational polymorphism of the amyloidogenic peptide homologous to residues 113-127 of the prion protein Biophys. J. 85 2003 473 483
40. K.S. Satheeshkumar, J. Murali, and R. Jayakumar Assemblages of prion fragments: novel model systems for understanding amyloid toxicity J. Struct. Biol. 148 2004 176 193
41. 16-22 peptide into β-sheets J. Am. Chem. Soc. 126 2004 11509 11516
42. M. Schaefer, C. Bartels, F. Leclerc, and M. Karplus Effective atom volumes for implicit solvent models: comparison between Voronoi volumes and minimum fluctuation volumes J. Comp. Chem. 22 2001 1857 1879
43. M. Schaefer, and M. Karplus A comprehensive analytical treatment of continuum electrostatics J. Phys. Chem. 100 1996 1578 1599
44. 11-25 peptide fragment Structure 11 2003 915 926
45. Stefani, M., Dobson, C.M., 2003. J. Mol. Med. 81, 678-699
46. M. Sunde, L.C. Serpell, M. Bartlam, P.E. Fraser, M.B. Pepys, and C.C.F. Blake Common core structure of amyloid fibrils by synchrotron X-ray diffraction J. Mol. Biol. 273 1997 729 739
47. F. Tagliavini, G. Forloni, P. D'Ursi, O. Bugiani, and M. Salmona Studies on peptide fragments of prion proteins Adv. Protein Chem. 57 2001 171 201
48. F. Tagliavini, F. Prelli, L. Verga, G. Giaccone, R. Sarma, P. Gorevic, B. Ghetti, F. Passerini, E. Ghibaudi, G. Forloni, M. Salmona, O. Bugiani, and B. Frangione Synthetic peptides homologous to prion protein residues 106-147 form amyloid-like fibrils in vitro Proc. Natl. Acad. Sci. USA 90 1993 9678 9682
49. R. Tycko Progress towards a molecular-level structural understanding of amyloid fibrils Curr. Opin. Struct. Biol. 14 2004 96 103
50. P. Westermark, S. Araki, M.D. Benson, A.S. Cohen, B. Frangione, C.L. Masters, M.J. Saraiva, J.D. Sipe, G. Husby, R.A. Kyle, and D. Selkoe Nomenclature of amyloid fibril proteins. Report from the meeting of the International Nomenclature Committee on Amyloidosis, Aug 8-9, 1998. Part 1 Amyloid 6 1999 63 66
51. P. Westermark, M.D. Benson, J.N. Buxvaum, A.S. Cohen, B. Frangione, S.-I. Ikeada, C.L. Masters, G. Merlini, M.J. Saraiva, and J.D. Sipe Amyloid fibril protein nomenclature. Amyloid J. Protein Folding Disord. 9 2002 197 200
52. D. Zanuy, and R. Nussinov The sequence dependence of fiber organization. A comparative molecular dynamics study of the islet amyloid polypeptide segments 22-27 and 22-29 J. Mol. Biol. 329 2003 565 584