Probing the mechanism of amyloidogenesis through a tandem repeat of the PI3-SH3 domain suggests a generic model for protein aggregation and fibril formation

Journal of Molecular Biology

Volumn 356, Issue 1, 2006, Pages 189-208

  Bader, Reto ^a   Bamford, Richard ^a   Zurdo, Jesús ^a   Luisi, Ben F ^a   Dobson, Christopher M ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Amyloid fibrils; Assembly mechanism; Nucleation; PI3 SH3 domain; Protofibrils

Indexed keywords

AMYLOID; GLYCINE; OLIGOMER; PROTEIN SH3; SERINE; THIOFLAVINE;

ARTICLE; BETA SHEET; CONTROLLED STUDY; ISOELECTRIC POINT; MORPHOLOGICAL TRAIT; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DOMAIN;

EID: 30344457011     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2005.11.034     Document Type: Article

References (71)

1. R. Lumry, and H. Eyring Conformation changes of proteins J. Phys. Chem. 58 1954 110 120
2. E.Y. Chi, S. Krishnan, T.W. Randolph, and J.F. Carpenter Physical stability of proteins in aqueous solution: mechanism and driving forces in nonnative protein aggregation Pharm. Res. 20 2003 1325 1336
3. C.M. Dobson Protein folding and misfolding Nature 426 2003 884 890
4. J.D. Harper, and P.T. Lansbury Jr Models of amyloid seeding in Alzheimer's disease and scrapie: mechanistic truths and physiological consequences of the time-dependent solubility of amyloid proteins Annu. Rev. Biochem. 66 1997 385 407
5. R.L. Hull, G.T. Westermark, P. Westermark, and S.E. Kahn Islet amyloid: a critical entity in the pathogenesis of type 2 diabetes J. Clin. Endocrinol. Metab. 89 2004 3629 3643
6. D.J. Selkoe Folding proteins in fatal ways Nature 426 2003 900 904
7. D. Canet, M. Sunde, A.M. Last, A. Miranker, A. Spencer, C.V. Robinson, and C.M. Dobson Mechanistic studies of the folding of human lysozyme and the origin of amyloidogenic behavior in its disease-related variants Biochemistry 38 1999 6419 6427
8. M. Sunde, and C. Blake The structure of amyloid fibrils by electron microscopy and X-ray diffraction Advan Protein Chem. 50 1997 123 159
9. J.T. Jarrett, and P.T. Lansbury Jr Seeding "one-dimensional crystallization" of amyloid: a pathogenic mechanism in Alzheimer's disease and scrapie? Cell 73 1993 1055 1058
10. M. Eigen Prionics or the kinetic basis of prion diseases Biophys. Chem. 63 1996 A1-18
11. Z. Kam, H.B. Shore, and G. Feher On the crystallization of proteins J. Mol. Biol. 123 1978 539 555
12. S.D. Durbin, and G. Feher Protein crystallization Annu. Rev. Phys. Chem. 47 1996 171 204
13. G.W. Booker, I. Gout, A.K. Downing, P.C. Driscoll, J. Boyd, M.D. Waterfield, and I.D. Campbell Solution structure and ligand-binding site of the SH3 domain of the p85 alpha subunit of phosphatidylinositol 3-kinase Cell 73 1993 813 822
14. J.I. Guijarro, M. Sunde, J.A. Jones, I.D. Campbell, and C.M. Dobson Amyloid fibril formation by an SH3 domain Proc. Natl Acad. Sci. USA 95 1998 4224 4228
15. C.M. Dobson The structural basis of protein folding and its links with human disease Phil. Trans. Roy. Soc. ser. B 356 2001 133 145
16. J. Zurdo, J.I. Guijarro, J.L. Jimenez, H.R. Saibil, and C.M. Dobson Dependence on solution conditions of aggregation and amyloid formation by an SH3 domain J. Mol. Biol. 311 2001 325 340
17. J.L. Jimenez, J.I. Guijarro, E. Orlova, J. Zurdo, C.M. Dobson, M. Sunde, and H.R. Saibil Cryo-electron microscopy structure of an SH3 amyloid fibril and model of the molecular packing EMBO J. 18 1999 815 821
18. R. Nelson, M.R. Sawaya, M. Balbirnie, A.O. Madsen, C. Riekel, R. Grothe, and D. Eisenberg Structure of the cross-beta spine of amyloid-like fibrils Nature 435 2005 773 778
19. J. Zurdo, J.I. Guijarro, and C.M. Dobson Preparation and characterization of purified amyloid fibrils J. Am. Chem. Soc. 123 2001 8141 8142
20. A.T. Petkova, Y. Ishii, J.J. Balbach, O.N. Antzutkin, R.D. Leapman, F. Delaglio, and R. Tycko A structural model for Alzheimer's beta -amyloid fibrils based on experimental constraints from solid state NMR Proc. Natl Acad. Sci. USA 99 2002 16742 16747
21. A.T. Petkova, G. Buntkowsky, F. Dyda, R.D. Leapman, W.M. Yau, and R. Tycko Solid state NMR reveals a pH-dependent antiparallel beta-sheet registry in fibrils formed by a beta-amyloid peptide J. Mol. Biol. 335 2004 247 260
22. Y. Liu, and D. Eisenberg 3D domain swapping: as domains continue to swap Protein Sci. 11 2002 1285 1299
23. A. Sanders, C. Jeremy Craven, L.D. Higgins, S. Giannini, M.J. Conroy, and A.M. Hounslow Cystatin forms a tetramer through structural rearrangement of domain-swapped dimers prior to amyloidogenesis J. Mol. Biol. 336 2004 165 178
24. C.M. Eakin, F.J. Attenello, C.J. Morgan, and A.D. Miranker Oligomeric assembly of native-like precursors precedes amyloid formation by beta-2 microglobulin Biochemistry 43 2004 7808 7815
25. K.V. Kishan, G. Scita, W.T. Wong, P.P. Di Fiore, and M.E. Newcomer The SH3 domain of Eps8 exists as a novel intertwined dimer Nature Struct. Biol. 4 1997 739 743
26. Cantor, C. R. & Schimmel, P. R. (1980). Ultracentrifugation. In Techniques for the Study of Biological Structures and Function, 12th edit., pp. 591-641, Freeman, New York.
27. J. Lebowitz, M.S. Lewis, and P. Schuck Modern analytical ultracentrifugation in protein science: a tutorial review Protein Sci. 11 2002 2067 2079
28. P. Schuck Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and Lamm equation modeling Biophys. J. 78 2000 1606 1619
29. S. Koyama, H. Yu, D.C. Dalgarno, T.B. Shin, L.D. Zydowsky, and S.L. Schreiber 1H and 15N assignments and secondary structure of the PI3K SH3 domain FEBS Letters 324 1993 93 98
30. J.I. Guijarro, C.J. Morton, K.W. Plaxco, I.D. Campbell, and C.M. Dobson Folding kinetics of the SH3 domain of PI3 kinase by real-time NMR combined with optical spectroscopy J. Mol. Biol. 276 1998 657 667
31. C.S. Goldsbury, G.J. Cooper, K.N. Goldie, S.A. Muller, E.L. Saafi, and W.T. Gruijters Polymorphic fibrillar assembly of human amylin J. Struct. Biol. 119 1997 17 27
32. A.J. Geddes, K.D. Parker, E.D. Atkins, and E. Beighton "Cross-beta" conformation in proteins J. Mol. Biol. 32 1968 343 358
33. M. Sunde, L.C. Serpell, M. Bartlam, P.E. Fraser, M.B. Pepys, and C.C. Blake Common core structure of amyloid fibrils by synchrotron X-ray diffraction J. Mol. Biol. 273 1997 729 739
34. M. Fandrich, and C.M. Dobson The behaviour of polyamino acids reveals an inverse side chain effect in amyloid structure formation EMBO J. 21 2002 5682 5690
35. P. Polverino de Laureto, N. Taddei, E. Frare, C. Capanni, S. Costantini, and J. Zurdo Protein aggregation and amyloid fibril formation by an SH3 domain probed by limited proteolysis J. Mol. Biol. 334 2003 129 141
36. D.K. Wilkins, C.M. Dobson, and M. Gross Biophysical studies of the development of amyloid fibrils from a peptide fragment of cold shock protein B Eur. J. Biochem. 267 2000 2609 2616
37. S. Ventura, J. Zurdo, S. Narayanan, M. Parreno, R. Mangues, and B. Reif Short amino acid stretches can mediate amyloid formation in globular proteins: the Src homology 3 (SH3) case Proc. Natl Acad. Sci. USA 101 2004 7258 7263
38. M.F. Perutz Glutamine repeats and neurodegenerative diseases: molecular aspects Trends Biochem. Sci. 24 1999 58 63
39. Bamford, R. (2004). Folding and misfolding of a PI3-SH3 domain variant,. Part III thesis, University of Cambridge.
40. L.A. Morozova-Roche, V. Zamotin, M. Malisauskas, A. Ohman, R. Chertkova, and M.A. Lavrikova Fibrillation of carrier protein albebetin and its biologically active constructs. Multiple oligomeric intermediates and pathways Biochemistry 43 2004 9610 9619
41. J.R. Silveira, G.J. Raymond, A.G. Hughson, R.E. Race, V.L. Sim, S.F. Hayes, and B. Caughey The most infectious prion protein particles Nature 437 2005 257 261
42. J.W. Kelly The alternative conformations of amyloidogenic proteins and their multi-step assembly pathways Curr. Opin. Struct. Biol. 8 1998 101 106
43. H.X. Zhou Polymer models of protein stability, folding, and interactions Biochemistry 43 2004 2141 2154
44. W.P. Jencks On the attribution and addivity of binding-energies Proc. Natl Acad. Sci. USA 4046 1981 4050
45. S.B. Shuker, P.J. Hajduk, R.P. Meadows, and S.W. Fesik Discovering high-affinity ligands for proteins: SAR by NMR Science 274 1996 1531 1534
46. A.K. Chamberlain, C.E. MacPhee, J. Zurdo, L.A. Morozova-Roche, H.A. Hill, C.M. Dobson, and J.J. Davis Ultrastructural organization of amyloid fibrils by atomic force microscopy Biophys. J. 79 2000 3282 3293
47. A.R. Hurshman, J.T. White, E.T. Powers, and J.W. Kelly Transthyretin aggregation under partially denaturing conditions is a downhill polymerization Biochemistry 43 2004 7365 7381
48. J.T. Jarrett, and P.T. Lansbury Jr Amyloid fibril formation requires a chemically discriminating nucleation event: studies of an amyloidogenic sequence from the bacterial protein OsmB Biochemistry 31 1992 12345 12352
49. D.P. Smith, S. Jones, L.C. Serpell, M. Sunde, and S.E. Radford A systematic investigation into the effect of protein destabilisation on beta 2-microglobulin amyloid formation J. Mol. Biol. 330 2003 943 954
50. P.L. San Biagio, V. Martorana, A. Emanuele, S.M. Vaiana, M. Manno, and D. Bulone Interacting processes in protein coagulation Proteins: Struct. Funct. Genet. 37 1999 116 120
51. A.J. Modler, K. Gast, G. Lutsch, and G. Damaschun Assembly of amyloid protofibrils via critical oligomers-a novel pathway of amyloid formation J. Mol. Biol. 325 2003 135 148
52. R. Carrotta, M. Manno, D. Bulone, V. Martorana, and P.L. San Biagio Protofibril formation of amyloid beta-protein at low pH via a non-cooperative elongation mechanism J. Biol. Chem. 280 2005 30001 30008
53. F. Chiti, M. Stefani, N. Taddei, G. Ramponi, and C.M. Dobson Rationalization of the effects of mutations on peptide and protein aggregation rates Nature 424 2003 805 808
54. D.F. Waugh, D.F. Wilhelmson, S.L. Commerford, and M.L. Sackler Studies of the nucleation and growth reactions of selected types of insulin fibrils J. Am. Chem. Soc. 75 1953 2592 2600
55. A. Lomakin, D.S. Chung, G.B. Benedek, D.A. Kirschner, and D.B. Teplow On the nucleation and growth of amyloid beta-protein fibrils: detection of nuclei and quantitation of rate constants Proc. Natl Acad. Sci. USA 93 1996 1125 1129
56. L.O. Tjernberg, A. Pramanik, S. Bjorling, P. Thyberg, J. Thyberg, and C. Nordstedt Amyloid beta-peptide polymerization studied using fluorescence correlation spectroscopy Chem. Biol. 6 1999 53 62
57. T.R. Serio, A.G. Cashikar, A.S. Kowal, G.J. Sawicki, J.J. Moslehi, and L. Serpell Nucleated conformational conversion and the replication of conformational information by a prion determinant Science 289 2000 1317 1321
58. N.M. Kad, S.L. Myers, D.P. Smith, D.A. Smith, S.E. Radford, and N.H. Thomson Hierarchical assembly of beta2-microglobulin amyloid in vitro revealed by atomic force microscopy J. Mol. Biol. 330 2003 785 797
59. R. Krishnan, and S.L. Lindquist Structural insights into a yeast prion illuminate nucleation and strain diversity Nature 435 2005 765 772
60. E.J. Nettleton, P. Tito, M. Sunde, M. Bouchard, C.M. Dobson, and C.V. Robinson Characterization of the oligomeric states of insulin in self-assembly and amyloid fibril formation by mass spectrometry Biophys. J. 79 2000 1053 1065
61. G. Plakoutsi, N. Taddei, M. Stefani, and F. Chiti Aggregation of the Acylphosphatase from Sulfolobus solfataricus: the folded and partially unfolded states can both be precursors for amyloid formation J. Biol. Chem. 279 2004 14111 14119
62. G. Plakoutsi, F. Bemporad, M. Calamai, N. Taddei, C.M. Dobson, and F. Chiti Evidence for a mechanism of amyloid formation involving molecular reorganisation within native-like precursor aggregates J. Mol. Biol. 351 2005 910 922
63. F. Oosawa, and M. Kasai A theory of linear and helical aggregations of macromolecules J. Mol. Biol. 4 1962 10 21
64. J. Liang, J.K. Chen, S.T. Schreiber, and J. Clardy Crystal structure of PI3K SH3 domain at 20 Å resolution J. Mol. Biol. 257 1996 632 643
65. V.A. Parsegian, R.P. Rand, and D.C. Rau Osmotic stress, crowding, preferential hydration, and binding: a comparison of perspectives Proc. Natl Acad. Sci. USA 97 2000 3987 3992
66. 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
67. B. Caughey, and P.T. Lansbury Protofibrils, pores, fibrils, and neurodegeneration: separating the responsible protein aggregates from the innocent bystanders Annu. Rev. Neurosci. 26 2003 267 298
68. R.M. Horton, H.D. Hunt, S.N. Ho, J.K. Pullen, and L.R. Pease Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension Gene 77 1989 61 68
69. F. Delaglio, S. Grzesiek, G.W. Vuister, G. Zhu, J. Pfeifer, and A. Bax NMRPipe: a multidimensional spectral processing system based on UNIX pipes J. Biomol. NMR 6 1995 277 293
70. T. Laue, B.D. Shaw, T.M. Ridgeway, and S.L. Pelletier Computer-aided interpretation of analytical sedimentation data for proteins S.E. Harding A.J. Rowe J.C. Horton Analytical Ultracentrifugation in Biochemistry and Polymer Science 1992 The Royal Society of Chemistry Cambridge, UK 90 125
71. D.H. Spackman, W.H. Stein, and S. Moore Automatic recording apparatus for use in chromatography of amino acids Anal. Chem. 30 1958 1190 1206