Molecular basis for amyloid-β polymorphism

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 41, 2011, Pages 16938-16943

  Colletier, Jacques Philippe ^a,c,d   Laganowsky, Arthur ^a,e   Landau, Meytal ^a   Zhao, Minglei ^a   Soriaga, Angela B ^a   Goldschmidt, Lukasz ^a   Flot, David ^b   Cascio, Duilio ^a   Sawaya, Michael R ^a   Eisenberg, David ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b EUROPEAN SYNCHROTRON RADIATION FACILITY   (France)

^c INSTITUT DE BIOLOGIE STRUCTURALE   (France)

^d SHANGHAI INSTITUTE OF MATERIA MEDICA   (China)

^e UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

3D profile; Amyloid aggregation; Heterotypic zipper; Protofilaments

Indexed keywords

AMYLOID BETA PROTEIN;

ARTICLE; CRYSTAL STRUCTURE; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN POLYMORPHISM; PROTEIN STRUCTURE;

ALZHEIMER DISEASE; AMINO ACID SEQUENCE; AMYLOID BETA-PEPTIDES; CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; HUMANS; MICROSCOPY, ELECTRON, TRANSMISSION; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDE FRAGMENTS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY;

EID: 80054752317     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1112600108     Document Type: Article

References (67)

1. Hardy JA, Higgins GA (1992) Alzheimer's disease: The amyloid cascade hypothesis. Science 256:184-185.
2. Selkoe DJ (1991) Alzheimer's disease. In the beginning. Nature 354:432-433.
3. Glenner GG, Wong CW, Quaranta V, Eanes ED (1984) The amyloid deposits in Alzheimer's disease: Their nature and pathogenesis. Appl Pathol 2:357-369. (Pubitemid 16028900)
4. Selkoe DJ (1994) Alzheimer's disease: A central role for amyloid. J Neuropathol Exp Neurol 53:438-447.
5. Ashe KH, Zahs KR (2010) Probing the biology of Alzheimer's disease in mice. Neuron 66:631-645.
6. Van Nostrand WE, Melchor JP, Cho HS, Greenberg SM, Rebeck GW (2001) Pathogenic effects of D23N Iowa mutant amyloid beta-protein. J Biol Chem 276:32860-32866.
7. Tycko R, Sciarretta KL, Orgel JP, Meredith SC (2009) Evidence for novel beta-sheet structures in Iowa mutant beta-amyloid fibrils. Biochemistry 48:6072-6084.
8. Lambert MP, et al. (1998) Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc Natl Acad Sci USA 95:6448-6453.
9. Lesne S, et al. (2006) A specific amyloid-beta protein assembly in the brain impairs memory. Nature 440:352-357.
10. Xue WF, Hellewell AL, Hewitt EW, Radford SE (2010) Fibril fragmentation in amyloid assembly and cytotoxicity: When size matters. Prion 4:20-25.
11. Collins SR, Douglass A, Vale RD, Weissman JS (2004) Mechanism of prion propagation: Amyloid growth occurs by monomer addition. PLoS Biol 2:e321.
12. Chimon S, et al. (2007) Evidence of fibril-like beta-sheet structures in a neurotoxic amyloid intermediate of Alzheimer's beta-amyloid. Nat Struct Mol Biol.
13. Ono K, Condron MM, Teplow DB (2009) Structure-neurotoxicity relationships of amyloid β-protein oligomers. Proc Natl Acad Sci USA 106:14745-14750.
14. Maezawa I, et al. (2008) Congo red and thioflavin-T analogs detect Abeta oligomers. J Neurochem 104:457-468. (Pubitemid 350293869)
15. Necula M, Kayed R, Milton S, Glabe CG (2007) Small molecule inhibitors of aggregation indicate that amyloid beta oligomerization and fibrillization pathways are independent and distinct. J Biol Chem 282:10311-10324. (Pubitemid 47093410)
16. Hong HS, et al. (2007) Combining the rapid MTT formazan exocytosis assay and the MC65 protection assay led to the discovery of carbazole analogs as small molecule inhibitors of Abeta oligomer-induced cytotoxicity. Brain Res 1130:223-234.
17. Yang F, et al. (2005) Curcumin inhibits formation of amyloid beta oligomers and fibrils, binds plaques, and reduces amyloid in vivo. J Biol Chem 280:5892-5901. (Pubitemid 40280072)
18. Steiner B, et al. (1990) Phosphorylation of microtubule-associated protein tau: Identification of the site for Ca2(+)-calmodulin dependent kinase and relationship with tau phosphorylation in Alzheimer tangles. EMBO J 9:3539-3544.
19. Luhrs T, et al. (2005) 3D structure of Alzheimer's amyloid-beta(1-42) fibrils. Proc Natl Acad Sci USA 102:17342-17347.
20. Nelson R, Eisenberg D (2006) Recent atomic models of amyloid fibril structure. Curr Opin Struct Biol 16:260-265.
21. Petkova AT, et al. (2002) A structural model for Alzheimer's beta-amyloid fibrils based on experimental constraints from solid state NMR. Proc Natl Acad Sci USA 99:16742-16747. (Pubitemid 36034043)
22. Bayro MJ, et al. (2010) High-resolution MAS NMR analysis of PI3-SH3 amyloid fibrils: Backbone conformation and implications for protofilament assembly and structure. Biochemistry 49:7474-7484.
23. Greenwald J, et al. (2010) The mechanism of prion inhibition by HET-S. Mol Cell 38:889-899.
24. Shewmaker F, Wickner RB, Tycko R (2006) Amyloid of the prion domain of Sup35p has an in-register parallel beta-sheet structure. Proc Natl Acad Sci USA 103:19754-19759. (Pubitemid 46037503)
25. Antzutkin ON, et al. (2000) Multiple quantum solid-state NMR indicates a parallel, not antiparallel, organization of beta-sheets in Alzheimer's beta-amyloid fibrils. Proc Natl Acad Sci USA 97:13045-13050.
26. Balbach JJ, et al. (2000) Amyloid fibril formation by A beta 16-22, a seven-residue fragment of the Alzheimer's beta-amyloid peptide, and structural characterization by solid state NMR. Biochemistry 39:13748-13759.
27. Goldsbury C, et al. (2000) Amyloid fibril formation from full-length and fragments of amylin. J Struct Biol 130:352-362.
28. Kodali R, Williams AD, Chemuru S, Wetzel R (2010) Abeta(1-40) forms five distinct amyloid structures whose beta-sheet contents and fibril stabilities are correlated. J Mol Biol 401:503-517.
29. Paravastu AK, Leapman RD, Yau WM, Tycko R (2008) Molecular structural basis for polymorphism in Alzheimer's beta-amyloid fibrils. Proc Natl Acad Sci USA 105:18349-18354.
30. Petkova AT, et al. (2004) Solid state NMR reveals a pH-dependent antiparallel betasheet registry in fibrils formed by a beta-amyloid peptide. J Mol Biol 335:247-260. (Pubitemid 37494976)
31. Petkova AT, et al. (2005) Self-propagating, molecular-level polymorphism in Alzheimer's beta-amyloid fibrils. Science 307:262-265. (Pubitemid 40116242)
32. Sachse C, FandrichM, Grigorieff N (2008) Paired beta-sheet structure of an Abeta(1-40) amyloid fibril revealed by electron microscopy. Proc Natl Acad Sci USA 105:7462-7466. (Pubitemid 351830040)
33. Wasmer C, et al. (2008) Amyloid fibrils of the HET-s(218-289) prion form a beta solenoid with a triangular hydrophobic core. Science 319:1523-1526. (Pubitemid 351398180)
34. Petkova AT, Yau WM, Tycko R (2006) Experimental constraints on quaternary structure in Alzheimer's beta-amyloid fibrils. Biochemistry 45:498-512. (Pubitemid 43100415)
35. Paravastu AK, Qahwash I, Leapman RD, Meredith SC, Tycko R (2009) Seeded growth of beta-amyloid fibrils from Alzheimer's brain-derived fibrils produces a distinct fibril structure. Proc Natl Acad Sci USA 106:7443-7448.
36. Gazit E (2005) Mechanisms of amyloid fibril self-assembly and inhibition. Model short peptides as a key research tool. FEBS J 272:5971-5978.
37. Kirschner DA, Abraham C, Selkoe DJ (1986) X-ray diffraction from intraneuronal paired helical filaments and extraneuronal amyloid fibers in Alzheimer disease indicates cross-beta conformation. Proc Natl Acad Sci USA 83:503-507. (Pubitemid 16080042)
38. Astbury WT, Beighton E, Parker KD (1959) The cross-beta configuration in supercontracted proteins. Biochim Biophys Acta 35:17-25.
39. Sunde M, et al. (1997) Common core structure of amyloid fibrils by synchrotron X-ray diffraction. J Mol Biol 273:729-739. (Pubitemid 27488813)
40. Ivanova MI, Thompson MJ, Eisenberg D (2006) A systematic screen of beta(2)-microglobulin and insulin for amyloid-like segments. Proc Natl Acad Sci USA 103:4079-4082.
41. Thompson MJ, et al. (2006) The 3D profile method for identifying fibril-forming segments of proteins. Proc Natl Acad Sci USA 103:4074-4078.
42. Gazit E (2002) Mechanistic studies of the process of amyloid fibrils formation by the use of peptide fragments and analogues: Implications for the design of fibrillization inhibitors. Curr Med Chem 9:1725-1735.
43. Balbirnie M, Grothe R, Eisenberg DS (2001) An amyloid-forming peptide from the yeast prion Sup35 reveals a dehydrated beta-sheet structure for amyloid. Proc Natl Acad Sci USA 98:2375-2380. (Pubitemid 32209490)
44. Nelson R, et al. (2005) Structure of the cross-beta spine of amyloid-like fibrils. Nature 435:773-778. (Pubitemid 40839722)
45. Sawaya MR, et al. (2007) Atomic structures of amyloid cross-beta spines reveal varied steric zippers. Nature 447:453-457. (Pubitemid 46816731)
46. Wiltzius JJ, et al. (2008) Atomic structure of the cross-β spine of islet amyloid polypeptide (amylin). Protein Sci 17:1467-1474.
47. Apostol MI, Sawaya MR, Cascio D, Eisenberg D (2010) Crystallographic studies of prion protein (PrP) segments suggest how structural changes encoded by polymorphism at residue 129 modulate susceptibility to human prion disease. J Biol Chem 285:29671-29675.
48. Wiltzius JJ, et al. (2009) Molecular mechanisms for protein-encoded inheritance. Nat Struct Mol Biol 16:973-978.
49. Ivanova MI, Sievers SA, Sawaya MR, Wall JS, Eisenberg D (2009) Molecular basis for insulin fibril assembly. Proc Natl Acad Sci USA 106:18990-18995.
50. Sambashivan S, Liu Y, Sawaya MR, Gingery M, Eisenberg D (2005) Amyloid-like fibrils of ribonuclease A with three-dimensional domain-swapped and native-like structure. Nature 437:266-269. (Pubitemid 41294490)
51. Meinhardt J, Sachse C, Hortschansky P, Grigorieff N, Fandrich M (2009) Abeta(1-40) fibril polymorphism implies diverse interaction patterns in amyloid fibrils. J Mol Biol 386:869-877.
52. Andrews ME, Inayathullah NM, Jayakumar R, Malar EJ (2009) Conformational polymorphism and cellular toxicity of IAPP and beta AP domains. J Struct Biol 166:116-125.
53. Komatsu H, Feingold-Link E, Sharp KA, Rastogi T, Axelsen PH (2010) Intrinsic linear heterogeneity of amyloid β protein fibrils revealed by higher resolution mass-perlength determinations. J Biol Chem 285:41843-41851.
54. Schmidt M, et al. (2009) Comparison of Alzheimer Abeta(1-40) and Abeta(1-42) amyloid fibrils reveals similar protofilament structures. Proc Natl Acad Sci USA 106:19813-19818.
55. Zhang R, et al. (2009) Interprotofilament interactions between Alzheimer's Abeta1-42 peptides in amyloid fibrils revealed by cryoEM. Proc Natl Acad Sci USA 106:4653-4658.
56. Yoshiike Y, Akagi T, Takashima A (2007) Surface structure of amyloid-beta fibrils contributes to cytotoxicity. Biochemistry 46:9805-9812. (Pubitemid 47328586)
57. Kirkitadze MD, Bitan G, Teplow DB (2002) Paradigm shifts in Alzheimer's disease and other neurodegenerative disorders: The emerging role of oligomeric assemblies. J Neurosci Res 69:567-577. (Pubitemid 34966869)
58. Kuhlman B, Baker D (2000) Native protein sequences are close to optimal for their structures. Proc Natl Acad Sci USA 97:10383-10388.
59. Goldschmidt L, Teng PK, Riek R, Eisenberg D (2010) Identifying the amylome, proteins capable of forming amyloid-like fibrils. Proc Natl Acad Sci USA 107:3487-3492.
60. Takano K, et al. (2006) Structure of amyloid beta fragments in aqueous environments. FEBS J 273:150-158.
61. Lansbury PT, Jr, et al. (1995) Structural model for the beta-amyloid fibril based on interstrand alignment of an antiparallel-sheet comprising a C-terminal peptide. Nat Struct Biol 2:990-998.
62. Cerf E, et al. (2009) Antiparallel beta-sheet: A signature structure of the oligomeric amyloid beta-peptide. Biochem J 421:415-423.
63. Yu L, et al. (2009) Structural characterization of a soluble amyloid beta-peptide oligomer. Biochemistry 48:1870-1877.
64. Eckert A, et al. (2008) Oligomeric and fibrillar species of beta-amyloid (A beta 42) both impair mitochondrial function in P301L tau transgenic mice. J Mol Med 86:1255-1267.
65. Habicht G, et al. (2007) Directed selection of a conformational antibody domain that prevents mature amyloid fibril formation by stabilizing Abeta protofibrils. Proc Natl Acad Sci USA 104:19232-19237.
66. Crick FH (1952) Is alpha-keratin a coiled coil? Nature 170:882-883.
67. Rousseau F, Schymkowitz J, Serrano L (2006) Protein aggregation and amyloidosis: confusion of the kinds? Curr Opin Struct Biol 16:118-126. (Pubitemid 43221880)