Progress towards a molecular-level structural understanding of amyloid fibrils

Current Opinion in Structural Biology

Volumn 14, Issue 1, 2004, Pages 96-103

  Tycko, Robert ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

A m n; Electron microscopy; Electron paramagnetic resonance; EM; EPR; H D; Hydrogen deuterium; Magic angle spinning; MAS; Mass per length; MPL; Residues m n of the Alzheimer's amyloid peptide; TTR 105 115

Indexed keywords

ALPHA SYNUCLEIN; AMYLIN; AMYLOID; AMYLOID BETA PROTEIN; BIOMATERIAL; CHYMOTRYPSIN; CYSTEINE; DEUTERIUM; GOLD; HUNTINGTIN; HYBRID PROTEIN; HYDROGEN; INSULIN; LYASE; PERTACTIN; PREALBUMIN; PRION PROTEIN; SILVER; TRYPSIN;

ALKYLATION; ALZHEIMER DISEASE; AMINO TERMINAL SEQUENCE; BETA SHEET; CARBON NUCLEAR MAGNETIC RESONANCE; CARBOXY TERMINAL SEQUENCE; COGNITIVE DEFECT; CRYSTAL STRUCTURE; ELECTRON MICROSCOPY; ELECTRON SPIN RESONANCE; ENZYME ACTIVITY; GENETIC POLYMORPHISM; HUMAN; HYDRATION; HYDROPHOBICITY; MOLECULAR DYNAMICS; NITROGEN NUCLEAR MAGNETIC RESONANCE; NONHUMAN; PARKINSON DISEASE; PH MEASUREMENT; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; REVIEW; SITE DIRECTED MUTAGENESIS; SOLID STATE; TEMPERATURE DEPENDENCE;

EID: 1342324027     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.sbi.2003.12.002     Document Type: Review

References (63)

1. Astbury W.T., Dickinson S., Bailey K. The X-ray interpretation of denaturation and the structure of the seed globulins. Biochem. J. 29:1935;2351.
2. Eanes E.D., Glenner G.G. X-ray diffraction studies on amyloid filaments. J. Histochem. Cytochem. 16:1968;673-677.
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. 31:1998;1-39.
4. Lansbury P.T., Costa P.R., Griffiths J.M., Simon E.J., Auger M., Halverson K.J., Kocisko D.A., Hendsch Z.S., Ashburn T.T., Spencer R.G.S.et al. Structural model for the β-amyloid fibril based on interstrand alignment of an antiparallel sheet comprising a C-terminal peptide. Nat. Struct. Biol. 2:1995;990-998.
5. Benzinger T.L.S., Gregory D.M., Burkoth T.S., Miller-Auer H., Lynn D.G., Botto R.E., Meredith S.C. Propagating structure of Alzheimer's β-amyloid(10-35) is parallel β-sheet with residues in exact register. Proc. Natl. Acad. Sci. USA. 95:1998;13407-13412.
6. Balbach J.J., Petkova A.T., Oyler N.A., Antzutkin O.N., Gordon D.J., Meredith S.C., Tycko R. Supramolecular structure in full-length Alzheimer's β-amyloid fibrils: evidence for a parallel β-sheet organization from solid-state nuclear magnetic resonance. Biophys. J. 83:2002;1205-1216.
7. 1-40 fibrils, in conjunction with constraints on fibril diameters and MPL from EM.
8. 1-40 fibrils.
9. 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. 99:2002;16748-16753.
10. Jaroniec CP, MacPhee CE, Bajaj VS, McMahon MT, Dobson CM, Griffin RG: High resolution molecular structure of a peptide in an amyloid fibril determined by magic angle spinning NMR spectroscopy. Proc Natl Acad Sci USA 2003, in press.
11. Antzutkin O.N., Balbach J.J., Tycko R. Site-specific identification of non-β-strand conformations in Alzheimer's β-amyloid fibrils by solid-state NMR. Biophys. J. 84:2003;3326-3335.
12. Tycko R. Insights into the amyloid folding problem from solid-state NMR. Biochemistry. 42:2003;3151-3159 A recent, detailed review of structural issues and experimental approaches based on solid-state NMR.
13. Tycko R., Ishii Y. Constraints on supramolecular structure in amyloid fibrils from two-dimensional solid-state NMR spectroscopy with uniform isotopic labeling. J. Am. Chem. Soc. 125:2003;6606-6607.
14. Serag A.A., Altenbach C., Gingery M., Hubbell W.L., Yeates T.O. Identification of a subunit interface in transthyretin amyloid fibrils: evidence for self-assembly from oligomeric building blocks. Biochemistry. 40:2001;9089-9096.
15. Serag A.A., Altenbach C., Gingery M., Hubbell W.L., Yeates T.O. Arrangement of subunits and ordering of β-strands in an amyloid sheet. Nat. Struct. Biol. 9:2002;734-739 Constraints on the β-sheet organization in TTR fibrils from EPR measurements on samples with site-directed spin labeling.
16. 1-42 fibrils.
17. Der-Sarkissian A., Jao C.C., Chen J., Langen R. Structural organization of α-synuclein fibrils studied by site-directed spin labeling. J. Biol. Chem. 278:2003;37530-37535.
18. Jimenez J.L., Guijarro J.L., Orlova E., Zurdo J., Dobson C.M., Sunde M., Saibil H.R. Cryo-electron microscopy structure of an SH3 amyloid fibril and model of the molecular packing. EMBO J. 18:1999;815-821.
19. Serpell L.C., Smith J.M. Direct visualisation of the β-sheet structure of synthetic Alzheimer's amyloid. J. Mol. Biol. 299:2000;225-231.
20. 1-40: implications for the search for Aβ fibril formation inhibitors. J. Struct. Biol. 130:2000;217-231.
21. Goldsbury C., Goldie K., Pellaud J., Seelig J., Frey P., Muller S.A., Kistler J., Cooper G.J.S., Aebi U. Amyloid fibril formation from full-length and fragments of amylin. J. Struct. Biol. 130:2000;352-362.
22. Wille H., Michelitsch M.D., Guenebaut V., Supattapone S., Serban A., Cohen F.E., Agard D.A., Prusiner S.B. Structural studies of the scrapie prion protein by electron crystallography. Proc. Natl. Acad. Sci. USA. 99:2002;3563-3568 Variants of a mammalian prion protein are reported to form ordered two-dimensional arrays of aggregates, for which an electron density distribution was determined. A parallel β-helical structural model was found to fit the electron density distribution.
23. Jimenez J.L., Nettleton E.J., Bouchard M., Robinson C.V., Dobson C.M., Saibil H.R. The protofilament structure of insulin amyloid fibrils. Proc. Natl. Acad. Sci. USA. 99:2002;9196-9201 Cryo-EM was used to construct models of electron density in insulin amyloid fibrils with several different morphologies. The possibility that the observed morphologies share a common protofilament structure is investigated.
24. Balbirnie M., Grothe R., Eisenberg D.S. An amyloid-forming peptide from the yeast prion Sup35 reveals a dehydrated β-sheet structure for amyloid. Proc. Natl. Acad. Sci. USA. 98:2001;2375-2380.
25. 11-25 fibrils that are nearly crystalline, leading to an antiparallel β-sheet model.
26. Diaz-Avalos R., Long C., Fontano E., Balbirnie M., Grothe R., Eisenberg D., Caspar D.L.D. Cross-β order and diversity in nanocrystals of an amyloid-forming peptide. J. Mol. Biol. 330:2003;1165-1175 Detailed analyses of X-ray and electron diffraction from microcrystalline forms of the seven-residue peptide GNNQQNY from the N-terminal region of Sup35, leading to a parallel β-sheet model.
27. 16-22 forms hollow, tubular fibrils at low pH. A model for the supramolecular organization within these fibrils is proposed that differs qualitatively from, but is nonetheless related to, a standard cross-β structure.
28. Kheterpal I., Williams A., Murphy C., Bledsoe B., Wetzel R. Structural features of the Aβ amyloid fibril elucidated by limited proteolysis. Biochemistry. 40:2001;11757-11767.
29. 2-microglobulin amyloid fibril by H/D exchange. Nat. Struct. Biol. 9:2002;332-336.
30. Kheterpal I., Wetzel R., Cook K.D. Enhanced correction methods for hydrogen exchange-mass spectrometric studies of amyloid fibrils. Protein Sci. 12:2003;635-643.
31. Nazabal A., Dos Reis S., Bonneu M., Saupe S.J., Schmitter J.M. Conformational transition occurring upon amyloid aggregation of the HET-s prion protein of Podospora anserina analyzed by hydrogen/deuterium exchange and mass spectrometry. Biochemistry. 42:2003;8852-8861.
32. Ippel J.H., Olofsson A., Schleucher J., Lundgren E., Wijmenga S.S. Probing solvent accessibility of amyloid fibrils by solution NMR spectroscopy. Proc. Natl. Acad. Sci. USA. 99:2002;8648-8653.
33. Iwata K., Eyles S.J., Lee J.P. Exposing asymmetry between monomers in Alzheimer's amyloid fibrils via reductive alkylation of lysine residues. J. Am. Chem. Soc. 123:2001;6728-6729.
34. Burkoth T.S., Benzinger T.L.S., Urban V., Morgan D.M., Gregory D.M., Thiyagarajan P., Botto R.E., Meredith S.C., Lynn D.G. Structure of the β-amyloid(10-35) fibril. J. Am. Chem. Soc. 122:2000;7883-7889.
35. 16-22, a seven-residue fragment of the Alzheimer's beta-amyloid peptide, and structural characterization by solid state NMR. Biochemistry. 39:2000;13748-13759.
36. Petkova AT, Buntkowsky G, Dyda F, Leapman RD, Yau W-M, Tycko R: Solid state NMR reveals a pH-dependent antiparallel β-sheet registry in fibrils formed by a β-amyloid peptide. J Mol Biol 2003, in press.
37. Iwatsubo T. Amyloid beta peptides and presenilins in the pathogenesis of Alzheimer's disease. Acta Histochem. et Cytochem. 32:1999;13-15.
38. Harper J.D., Wong S.S., Lieber C.M., Lansbury P.T. Observation of metastable Aβ amyloid protofibrils by atomic force microscopy. Chem. Biol. 4:1997;119-125.
39. 1-42 levels with Alzheimer's disease.
40. Baxa U., Speransky V., Steven A.C., Wickner R.B. Mechanism of inactivation on prion conversion of the Saccharomyces cerevisiae Ure2 protein. Proc. Natl. Acad. Sci. USA. 99:2002;5253-5260 Amyloid fibrils formed by fusion proteins composed of the N-terminal 'prion domain' of Ure2 and several enzymes with globular structures are found to retain nearly full enzymatic activity. This demonstrates retention of the globular structure in the amyloid form and may place steric constraints on the amyloid structure.
41. Roher A.E., Lowenson J.D., Clarke S., Wolkow C., Wang R., Cotter R.J., Reardon I.M., Zurcherneely H.A., Heinrikson R.L., Ball M.J., Greenberg B.D. Structural alterations in the peptide backbone of β-amyloid core protein may account for its deposition and stability in Alzheimer's disease. J. Biol. Chem. 268:1993;3072-3083.
42. Dearmond S.J., Yang S.L., Lee A., Bowler R., Taraboulos A., Groth D., Prusiner S.B. Three scrapie prion isolates exhibit different accumulation patterns of the prion protein scrapie isoform. Proc. Natl. Acad. Sci. USA. 90:1993;6449-6453.
43. Uptain S.M., Sawicki G.J., Caughey B., Lindquist S. Strains of [PSI+] are distinguished by their efficiencies of prion-mediated conformational conversion. EMBO J. 20:2001;6236-6245.
44. Schlumpberger M., Prusiner S.B., Herskowitz I. Induction of distinct [URE3] yeast prion strains. Mol. Cell. Biol. 21:2001;7035-7046.
45. Derkatch I.L., Chernoff Y.O., Kushnirov V.V., Inge-Vechtomov S.G., Liebman S.W. Genesis and variability of [PSI] prion factors in Saccharomyces cerevisiae. Genetics. 144:1996;1375-1386.
46. Prusiner S.B. Molecular biology of prion diseases. Science. 252:1991;1515-1522.
47. Peretz D., Scott M.R., Groth D., Williamson R.A., Burton D.R., Cohen F.E., Prusiner S.B. Strain-specified relative conformational stability of the scrapie prion protein. Protein Sci. 10:2001;854-863.
48. Kirkitadze M.D., Bitan G., Teplow D.B. Paradigm shifts in Alzheimer's disease and other neurodegenerative disorders: the emerging role of oligomeric assemblies. J. Neurosci. Res. 69:2002;567-577.
49. Perutz M.F., Johnson T., Suzuki M., Finch J.T. Glutamine repeats as polar zippers: their possible role in inherited neurodegenerative diseases. Proc. Natl. Acad. Sci. USA. 91:1994;5355-5358.
50. Perutz M.F., Pope B.J., Owen D., Wanker E.E., Scherzinger E. Aggregation of proteins with expanded glutamine and alanine repeats of the glutamine-rich and asparagine-rich domains of Sup35 and of the amyloid β-peptide of amyloid plaques. Proc. Natl. Acad. Sci. USA. 99:2002;5596-5600.
51. Bevivino A.E., Loll P.J. An expanded glutamine repeat destabilizes native ataxin-3 structure and mediates parallel β-fibrils. Proc. Natl. Acad. Sci. USA. 98:2001;11955-11960.
52. Perutz M.F., Finch J.T., Berriman J., Lesk A. Amyloid fibers are water-filled nanotubes. Proc. Natl. Acad. Sci. USA. 99:2002;5591-5595 The authors describe a β-helix-like tubular structural model for amyloid fibrils, especially those formed by polyglutamine peptides. Evidence from EM that the experimentally observed fibrils may be bundles of three tubular structures is discussed.
53. Liu Y.S., Gotte G., Libonati M., Eisenberg D. A domain-swapped RNase A dimer with implications for amyloid formation. Nat. Struct. Biol. 8:2001;211-214.
54. Thakur A.K., Wetzel R. Mutational analysis of the structural organization of polyglutamine aggregates. Proc. Natl. Acad. Sci. USA. 99:2002;17014-17019 Measurements of the aggregation kinetics of synthetic polyglutamine peptides with proline-glycine inserts, suggesting a molecular conformation with repeated β-hairpins in the amyloid fibril state.
55. Liu Y., Eisenberg D. 3D domain swapping: as domains continue to swap. Protein Sci. 11:2002;1285-1299.
56. Staniforth R.A., Giannini S., Higgins L.D., Conroy M.J., Hounslow A.M., Jerala R., Craven C.J., Waltho J.P. Three-dimensional domain swapping in the folded and molten-globule states of cystatins, an amyloid-forming structural superfamily. EMBO J. 20:2001;4774-4781.
57. Yoder M.D., Keen N.T., Jurnak F. New domain motif: the structure of pectate lyase C, a secreted plant virulence factor. Science. 260:1993;1503-1507.
58. Emsley P., Charles I.G., Fairweather N.F., Isaacs N.W. Structure of Bordetella pertussis virulence factor P.69 pertactin. Nature. 381:1996;90-92.
59. Lazo N.D., Downing D.T. Amyloid fibrils may be assembled from β-helical protofibrils. Biochemistry. 37:1998;1731-1735.
60. 1-40 fibrils bind to a variety of amyloid fibrils, but not to nonamyloid controls.
61. Reches M., Gazit E. Casting metal nanowires within discrete self-assembled peptide nanotubes. Science. 300:2003;625-627.
62. Scheibel T., Parthasarathy R., Sawicki G., Lin X.M., Jaeger H., Lindquist S.L. Conducting nanowires built by controlled self-assembly of amyloid fibers and selective metal deposition. Proc. Natl. Acad. Sci. USA. 100:2003;4527-4532.
63. Koradi R., Billeter M., Wuthrich K. MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph. 14:1996;51-55.