Evidence of fibril-like β-sheet structures in a neurotoxic amyloid intermediate of Alzheimer's β-amyloid

Nature Structural and Molecular Biology

Volumn 14, Issue 12, 2007, Pages 1157-1164

  Chimon, Sandra ^a   Shaibat, Medhat A ^a   Jones, Christopher R ^a   Calero, Diana C ^a   Aizezi, Buzulagu ^a   Ishii, Yoshitaka ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA SECRETASE;

ALZHEIMER DISEASE; AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; BETA SHEET; CONTROLLED STUDY; ELECTRON MICROSCOPY; FIBER; NEUROTOXICITY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STRUCTURE; RAT;

AMYLOID; AMYLOID BETA-PEPTIDES; ANIMALS; FLUORESCENT DYES; HUMANS; MICROSCOPY, FLUORESCENCE; MODELS, CHEMICAL; NEUROTOXINS; PC12 CELLS; PEPTIDE FRAGMENTS; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; RATS; THIAZOLES;

EID: 36849084640     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb1345     Document Type: Article

References (50)

1. Selkoe, D.J. Cell biology of protein misfolding: the examples of Alzheimer's and Parkinson's diseases. Nat. Cell Biol. 6, 1054-1061 (2004).
2. Caughey, B. & Lansbury, P.T. Protofibrils, pores, fibrils, and neurodegeneration: Separating the responsible protein aggregates from the innocent bystanders. Annu. Rev. Neurosci. 26, 267-298 (2003).
3. Sunde, M. & Blake, C.C.F. From the globular to the fibrous state: protein structure and structural conversion in amyloid formation. Q. Rev. Biophys. 31, 1-39 (1998).
4. Dobson, C.M. Protein folding and misfolding. Nature 426, 884-890 (2003).
5. Bucciantini, M. et al. Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases. Nature 416, 507-511 (2002).
6. Lorenzo, A. & Yankner, B.A. β-amyloid neurotoxicity requires fibril formation and is inhibited by Congo red. Proc. Natl. Acad. Sci. USA 91, 12243-12247 (1994).
7. Walsh, D.M., Lomakin, A., Benedek, G.B., Condron, M.M. & Teplow, D.B. Amyloid β-protein fibrillogenesis - detection of a protofibrillar intermediate. J. Biol. Chem. 272, 22364-22372 (1997).
8. 1-42 are potent central nervous system neurotoxins. Proc. Natl. Acad. Sci. USA 95, 6448-6453 (1998).
9. Hoshi, M. et al. Spherical aggregates of (β-amyloid (amylospheroid) show high neurotoxicity and activate tau protein kinase I/glycogen synthase kinase-3β. Proc. Natl. Acad. Sci. USA 100, 6370-6375 (2003).
10. Nilsberth, C. et al. The 'Arctic' APP mutation (E693G) causes Alzheimer's disease by enhanced Aβ protofibril formation. Nat. Neurosci. 4, 887-893 (2001).
11. Lashuel, H.A. et al. Mixtures of wild-type and a pathogenic (E22G) form of Aβ40 in vitro accumulate protofibrils, including amyloid pores. J. Mol. Biol. 332, 795-808 (2003).
12. Conway, K.A. et al. Acceleration of oligomerization, not fibrillization, is a shared property of both α-synuclein mutations linked to early-onset Parkinson's disease: Implications for pathogenesis and therapy. Proc. Natl. Acad. Sci. USA 97, 571-576 (2000).
13. McLean, C.A. et al. Soluble pool of Aβ amyloid as a determinant of severity of neurodegeneration in Alzheimer's disease. Ann. Neurol. 46, 860-866 (1999).
14. Lue, L.F. et al. Soluble amyloid β peptide concentration as a predictor of synaptic change in Alzheimer's disease. Am. J. Pathol. 155, 853-862 (1999).
15. Hsia, A.Y. et al. Plaque-independent disruption of neural circuits in Alzheimer's disease mouse models. Proc. Natl. Acad. Sci. USA 96, 3228-3233 (1999).
16. Walsh, D.M. et al. Naturally secreted oligomers of amyloid β protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416, 535-539 (2002).
17. Lesne, S. et al. A specific amyloid-β protein assembly in the brain impairs memory. Nature 440, 352-357 (2006).
18. Kirkitadze, M.D., Condron, M.M. & Teplow, D.B. Identification and characterization of key kinetic intermediate in amyloid β-protein fibrillogenesis. J. Mol. Biol. 312, 1103-1119 (2001).
19. Krishnan, R. & Lindquist, S.L. Structural insights into a yeast prion illuminate nucleation and strain diversity. Nature 435, 765-772 (2005).
20. Liu, K., Cho, H.S., Lashuel, H.A., Kelly, J.W. & Wemmer, D.E. A glimpse of a possible amyloidogenic intermediate of transthyretin. Nat. Struct. Biol. 7, 754-757 (2000).
21. Jahn, T.R., Parker, M.J., Homans, S.W. & Radford, S.E. Amyloid formation under physiological conditions proceeds via a native-like folding intermediate. Nat. Struct. Mol. Biol. 13, 195-201 (2006).
22. Eakin, C.M., Berman, A.J. & Miranker, A.D. A native to amyloidogenic transition regulated by a backbone trigger. Nat. Struct. Mol. Biol. 13, 202-208 (2006).
23. Dobson, C.M. An accidental breach of a protein's natural defenses. Nat. Struct. Mol. Biol. 13, 295-297 (2006).
24. Chromy, B.A. et al. Self-assembly of Aβ(1-42) into globular neurotoxins. Biochemistry 42, 12749-12760 (2003).
25. Chimon, S. & Ishii, Y. Capturing intermediate structures of Alzheimer's β-amyloid, Aβ(1-40), by solid-state NMR spectroscopy. J. Am. Chem. Soc. 127, 13472-13473 (2005).
26. Shearman, M.S. Toxicity of protein aggregates in PC12 cells: 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide assay. Methods Enzymol. 309, 716-723 (1999).
27. Kayed, R. et al. Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300, 486-489 (2003).
28. Lansbury, P.T. et al. Structural model for the β-amyloid fibril based on interstrand alignment of an antiparellel-sheet comprising a c-terminal peptide. Nat. Struct. Biol. 2, 990-998 (1995).
29. Petkova, A.T. et al. A structural model for Alzheimer's β-amyloid peptide fibrils based on experimental constraints from solid-state NMR spectroscopy. Proc. Natl. Acad. Sci. USA 99, 16742-16747 (2002).
30. Jaroniec, C.P., MacPhee, C.E., Astrof, N.S., Dobson, C.M. & Griffin, R.G. Molecular conformation of a peptide fragment of transthyretin in an amyloid fibril. Proc. Natl. Acad. Sci. USA 99, 16748-16753 (2002).
31. Heise, H. et al. Molecular-level secondary structure, polymorphism, and dynamics of full-length α-synuclein fibrils studied by solid-state NMR. Proc. Natl. Acad. Sci. USA 102, 15871-15876 (2005).
32. Ritter, C. et al. Correlation of structural elements and infectivity of the HET-s prion. Nature 435, 844-848 (2005).
33. Benzinger, T.L.S. et al. Propagating structure of Alzheimer's β-amyloid(10-35) is parallel β-sheet with residues in exact register. Proc. Natl. Acad. Sci. USA 95, 13407-13412 (1998).
34. Weliky, D.P. et al. Solid-state NMR evidence for an antibody-dependent conformation of the V3 loop of HIV-1 gp120. Nat. Struct. Biol. 6, 141-145 (1999).
35. Igumenova, T.I. et al. Assignments of carbon NMR resonances for microcrystalline ubiquitin. J. Am. Chem. Soc. 126, 6720-6727 (2004).
36. Castellani, F. et al. Structure of a protein determined by solid-state magic-angle-spinning NMR spectroscopy. Nature 420, 98-102 (2002).
37. Lange, A. et al. Toxin-induced conformational changes in a potassium channel revealed by solid-state NMR. Nature 440, 959-962 (2006).
38. Studelska, D.R., McDowell, L.M., Espe, M.P., Klug, C.A. & Schaefer, J. Slowed enzymatic turnover allows characterization of intermediates by solid-state NMR. Biochemistry 36, 15555-15560 (1997).
39. 13C chemical shifts: a new means of conformational characterization as obtained by high-resolution solid-state NMR. Magn. Reson. Chem. 24, 835-852 (1986).
40. Spera, S. & Bax, A. Empirical correlation between protein backbone conformation and C-α and C-β C-13 nuclear-magnetic-resonance chemical shifts. J. Am. Chem. Soc. 113, 5490-5492 (1991).
41. 13C dipolar recoupling under very fast magic angle spinning in solidstate NMR: Applications to distance measurements, spectral assignments, and high-throughput secondary-structure elucidation. J. Chem. Phys. 114, 8473-8483 (2001).
42. Petkova, A.T. et al. Self-propagating, molecular-level polymorphism in Alzheimer's β-amyloid fibrils. Science 307, 262-265 (2005).
43. 15N random coil NMR chemical shifts of the common amino acids. I. Investigations of nearest-neighbor effects. J. Biomol. NMR 5, 67-81 (1995).
44. Cornilescu, G., Delaglio, F. & Bax, A. Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR 13, 289-302 (1999).
45. Petkova, A.T., Yau, W.M. & Tycko, R. Experimental constraints on quaternary structure in Alzheimer's β-amyloid fibrils. Biochemistry 45, 498-512 (2006).
46. Levine, H., III Quantification of β-sheet amyloid fibril structures with thioflavin T. Methods Enzymol. 309, 274-284 (1999).
47. Naiki, H., Gejyo, F. & Nakakuki, K. Concentration-dependent inhibitory effects of apolipoprotein E on Alzheimer's β-amyloid fibril formation in vitro. Biochemistry 36, 6243-6250 (1997).
48. Reches, M. & Gazit, E. Casting metal nanowires within discrete self-assembled peptide nanotubes. Science 300, 625-627 (2003).
49. Zhang, S. Fabrication of novel biomaterials through molecular self-assembly. Nat. Biotechnol. 21, 1171-1178 (2003).
50. Lambert, M.P. et al. Vaccination with soluble Aβ oligomers generates toxicity-neutralizing antibodies. J. Neurochem. 79, 595-605 (2001).