Amyloid-β forms fibrils by nucleated conformational conversion of oligomers

Nature Chemical Biology

Volumn 7, Issue 9, 2011, Pages 602-609

  Lee, Jiyong ^a   Culyba, Elizabeth K ^a   Powers, Evan T ^a   Kelly, Jeffery W ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN[1-40]; CYSTEINE; ETHANOLAMINE; OLIGOMER; PLASMALOGEN; THIOFLAVINE;

ALZHEIMER DISEASE; ARTICLE; BINDING SITE; CONCENTRATION (PARAMETERS); FIBER; FLUORESCENCE ANALYSIS; FLUORESCENCE RESONANCE ENERGY TRANSFER; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN SYNTHESIS; PROTEOTOXICITY; TOXICITY;

EID: 84860389674     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.624     Document Type: Article

References (51)

1. Selkoe, D.J. Te molecular pathology of Alzheimer's disease. Neuron 6, 487-498 (1991).
2. Hardy, J. Te Alzheimer family of diseases: many etiologies, one pathogenesis? Proc. Natl. Acad. Sci. USA 94, 2095-2097 (1997). (Pubitemid 27136831)
3. Holtzman, D.M., Morris, J.C. & Goate, A.M. Alzheimer's disease: the challenge of the second century. Sci. Transl. Med. 3, 77sr71 (2011).
4. Klein, W.L., Kraf, G.A. & Finch, C.E. Targeting small Aβ oligomers: the solution to an Alzheimer's disease conundrum? Trends Neurosci. 24, 219-224 (2001). (Pubitemid 32204378)
5. Walsh, D.M. & Selkoe, D.J. Aβ oligomers - a decade of discovery. J. Neurochem. 101, 1172-1184 (2007).
6. Shankar, G.M. et al. Amyloid-β protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat. Med. 14, 837-842 (2008).
7. Shoji, M. et al. Production of the Alzheimer amyloid β protein by normal proteolytic processing. Science 258, 126-129 (1992).
8. Garzon-Rodriguez, W., Sepulveda-Becerra, M., Milton, S. & Glabe, C.G. Soluble amyloid Aβ-(1-40) exists as a stable dimer at low concentrations. J. Biol. Chem. 272, 21037-21044 (1997). (Pubitemid 27373960)
9. Ono, K., Condron, M.M. & Teplow, D.B. Structure-neurotoxicity relationships of amyloid β-protein oligomers. Proc. Natl. Acad. Sci. USA 106, 14745-14750 (2009).
10. Bernstein, S.L. et al. Amyloid-β protein oligomerization and the importance of tetramers and dodecamers in the aetiology of Alzheimer's disease. Nat. Chem. 1, 326-331 (2009).
11. Lesné, S. et al. A specifc amyloid-β protein assembly in the brain impairs memory. Nature 440, 352-357 (2006).
12. Lambert, M.P. et al. Difusible, nonfbrillar ligands derived from Aβ1-42 are potent central nervous system neurotoxins. Proc. Natl. Acad. Sci. USA 95, 6448-6453 (1998).
13. Lomakin, A., Teplow, D.B., Kirschner, D.A. & Benedek, G.B. Kinetic theory of fbrillogenesis of amyloid-β protein. Proc. Natl. Acad. Sci. USA 94, 7942-7947 (1997). (Pubitemid 27343754)
14. Sabaté, R. & Estelrich, J. Evidence of the existence of micelles in the fbrillogenesis of β-amyloid peptide. J. Phys. Chem. B 109, 11027-11032 (2005). (Pubitemid 40844540)
15. Tomiyama, T. et al. A mouse model of amyloid β oligomers: their contribution to synaptic alteration, abnormal tau phosphorylation, glial activation, and neuronal loss in vivo. J. Neurosci. 30, 4845-4856 (2010).
16. Harper, J.D. & Lansbury, P.T. 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, 385-407 (1997). (Pubitemid 27274662)
17. Jarrett, J.T. & Lansbury, P.T. Jr. Seeding "one-dimensional crystallization" of amyloid: A pathogenic mechanism in Alzheimer's disease and scrapie? Cell 73, 1055-1058 (1993). (Pubitemid 23180480)
18. Roychaudhuri, R., Yang, M., Hoshi, M.M. & Teplow, D.B. Amyloid β-protein assembly and Alzheimer disease. J. Biol. Chem. 284, 4749-4753 (2009).
19. Wetzel, R. Kinetics and thermodynamics of amyloid fbril assembly. Acc. Chem. Res. 39, 671-679 (2006).
20. LeVine, H. III. Tiofavin T interaction with synthetic Alzheimer's disease β-amyloid peptides: detection of amyloid aggregation in solution. Protein Sci. 2, 404-410 (1993).
21. Bieschke, J., Zhang, Q., Powers, E.T., Lerner, R.A. & Kelly, J.W. Oxidative metabolites accelerate Alzheimer's amyloidogenesis by a two-step mechanism, eliminating the requirement for nucleation. Biochemistry 44, 4977-4983 (2005). (Pubitemid 40471214)
22. Kayed, R. et al. Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300, 486-489 (2003). (Pubitemid 36444329)
23. Grifn, B.A., Adams, S.R. & Tsien, R.Y. Specifc covalent labeling of recombinant protein molecules inside live cells. Science 281, 269-272 (1998). (Pubitemid 28334512)
24. Coleman, B.M. et al. Conformational detection of prion protein with biarsenical labeling and FlAsH fuorescence. Biochem. Biophys. Res. Commun. 380, 564-568 (2009).
25. Luedtke, N.W., Dexter, R.J., Fried, D.B. & Schepartz, A. Surveying polypeptide and protein domain conformation and association with FlAsH and ReAsH. Nat. Chem. Biol. 3, 779-784 (2007). (Pubitemid 350126876)
26. Krishnan, B. & Gierasch, L.M. Cross-strand split tetra-Cys motifs as structure sensors in a β-sheet protein. Chem. Biol. 15, 1104-1115 (2008).
27. Goodman, J.L., Fried, D.B. & Schepartz, A. Bipartite tetracysteine display requires site fexibility for ReAsH coordination. ChemBioChem 10, 1644-1647 (2009).
28. Webber, T.M. et al. Conformational detection of p53's oligomeric state by FlAsH fuorescence. Biochem. Biophys. Res. Commun. 384, 66-70 (2009).
29. Petkova, A.T. et al. A structural model for Alzheimer's β-amyloid fbrils based on experimental constraints from solid state NMR. Proc. Natl. Acad. Sci. USA 99, 16742-16747 (2002). (Pubitemid 36034043)
30. Lührs, T. et al. 3D structure of Alzheimer's amyloid-β(1-42) fbrils. Proc. Natl. Acad. Sci. USA 102, 17342-17347 (2005).
31. Porat, Y., Abramowitz, A. & Gazit, E. Inhibition of amyloid fbril formation by polyphenols: structural similarity and aromatic interactions as a common inhibition mechanism. Chem. Biol. Drug Des. 67, 27-37 (2006). (Pubitemid 43881385)
32. Yang, F. et al. Curcumin inhibits formation of amyloid β oligomers and fbrils, binds plaques, and reduces amyloid in vivo. J. Biol. Chem. 280, 5892-5901 (2005). (Pubitemid 40280072)
33. Maezawa, I. et al. Congo red and thiofavin-T analogs detect Aβ oligomers. J. Neurochem. 104, 457-468 (2008). (Pubitemid 350293869)
34. Serio, T.R. et al. Nucleated conformational conversion and the replication of conformational information by a prion determinant. Science 289, 1317-1321 (2000). (Pubitemid 30656041)
35. Takur, A.K. et al. Polyglutamine disruption of the huntingtin exon 1 N terminus triggers a complex aggregation mechanism. Nat. Struct. Mol. Biol. 16, 380-389 (2009).
36. Wei, L. et al. Temolecular basis of distinct aggregation pathways of islet amyloid polypeptide. J. Biol. Chem. 286, 6291-6300 (2011).
37. Chimon, S. et al. Evidence of fbril-like β-sheet structures in a neurotoxic amyloid intermediate of Alzheimer's β-amyloid. Nat Struct. Mol. Biol 14, 1157-1164 (2007). (Pubitemid 350223342)
38. Ahmed, M. et al. Structural conversion of neurotoxic amyloid-β (1-42) oligomers to fbrils. Nat Struct. Mol. Biol 17, 561-567 (2010).
39. Nilsberth, C. et al. Te Arctic' APP mutation (E693G) causes Alzheimer's disease by enhanced Aβ protofbril formation. Nat Neurosci. 4, 887-893 (2001). (Pubitemid 32801591)
40. Lashuel, H.A. et al. Mixtures of wild-type and a pathogenic (E22G) form of Aβ40 in vitro accumulate protofbrils, including amyloid pores. J. Mol. Biol. 332, 795-808 (2003). (Pubitemid 37101368)
41. Tomiyama, T. et al. A new amyloid β variant favoring oligomerization in Alzheimer's-type dementia. Ann. Neurol 63, 377-387 (2008). (Pubitemid 351499867)
42. 1-39. Biochemistry 50, 2026-2039 (2011).
43. Wells, K., Farooqui, A.A., Liss, L. & Horrocks, L.A. Neural membrane phospholipids in Alzheimer disease. Neurochem. Res. 20, 1329-1333 (1995). (Pubitemid 26003436)
44. Goodenowe, D.B. et al. Peripheral ethanolamine plasmalogen defciency: a logical causative factor in Alzheimer's disease and dementia. J. Lipid Res. 48, 2485-2498 (2007). (Pubitemid 350058760)
45. Han, X., Holtzman, D.M. & McKeel, DW. Jr. Plasmalogen defciency in early Alzheimer's disease subjects and in animal models: molecular characterization using electrospray ionization mass spectrometry. J. Neurochem. 77, 1168-1180 (2001). (Pubitemid 32467071)
46. Martins, I.C. et al. Lipids revert inert Aβ amyloid fbrils to neurotoxic protofbrils that afect learning in mice. EMBO J. 27, 224-233 (2008).
47. Kim, S., Nollen, E.A., Kitagawa, K., Bindokas, V.P. & Morimoto, R.I. Polyglutamine protein aggregates are dynamic. Nat. Cell Biol. 4, 826-831 (2002).
48. Outeiro, T.F. et al. Formation of toxic oligomeric α-synuclein species in living cells. PLoS One 3, e1867 (2008).
49. Yushchenko, D.A., Fauerbach, J.A., Tirunavukkuarasu, S., Jares-Erijman, E.A. & Jovin, T.M. Fluorescent ratiometric MFC probe sensitive to early stages of α-synuclein aggregation. J. Am. Chem. Soc. 132, 7860-7861 (2010).
50. Roberti, M.J., Bertoncini, C.W, Klement, R., Jares-Erijman, E.A. & Jovin, T.M. Fluorescence imaging of amyloid formation in living cells by a functional, tetracysteine-tagged α-synuclein. Nat. Methods 4, 345-351 (2007). (Pubitemid 46766980)
51. Sunde, M. & Blake, C. Te structure of amyloid fbrils by electron microscopy and X-ray difraction. Adv. Protein Chem. 50, 123-159 (1997). (Pubitemid 27449487)