Common core structure of amyloid fibrils by synchrotron X-ray diffraction

Journal of Molecular Biology

Volumn 273, Issue 3, 1997, Pages 729-739

  Sunde, Margaret ^a,b   Serpell, Louise C ^a,c   Bartlam, Mark ^a   Fraser, Paul E ^a,c   Pepys, Mark B ^a,d   Blake, Colin C F ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF TORONTO   (Canada)

^d HAMMERSMITH HOSPITAL   (United Kingdom)

Author keywords

Amyloid; Fibre; Protofilament; Structure; X ray diffraction

Indexed keywords

AMYLOID; PROTEIN PRECURSOR;

ARTICLE; HUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN STRUCTURE; SEQUENCE HOMOLOGY; SYNCHROTRON; X RAY DIFFRACTION;

EID: 0031592945     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1997.1348     Document Type: Article

References (67)

1. Adams M. J., Blundell T. L., Dodson E. J., Dodson G. G., Vijayan M., Baker E. N., Harding M. M., Hodgkin D. C., Rimmer B., Sheat S. The structure of rhombohedral 2 zinc insulin crystals. Nature. 224:1969;491-495.
2. Arnott S., Dover S., Elliot A. Structure of β-poly-L. J. Mol. Biol. 30:1967;201-208.
3. Barrow C. J., Yasuda A., Kenny P. T. M., Zagorski M. G. Solution conformations and aggregational properties of synthetic amyloid β-peptides of Alzheimer's disease. J. Mol. Biol. 225:1992;1075-1093.
4. 2. Proc. Natl Acad. Sci USA. 82:1985;4225-4229.
5. Blake C. C. F., Serpell L. C. Synchrotron X-ray studies suggest that the core of the transthyretin amyloid fibril is a continuous β-sheet helix. Structure. 4:1996;989-998.
6. Blake C. C. F., Geisow M. J., Oatley S. J., Rerat B., Rerat C. Structure of prealbumin: secondary, tertiary and quaternary interactions determined by Fourier refinement at 1.8 Å J. Mol. Biol. 121:1978;339-356.
7. Blake C. C. F., Serpell L. C., Sunde M., Lundgren E. A molecular model of the amyloid fibril. CIBA Symposium No. 199, The Nature and origin of Amyloid Fibrils. 1996;John Wiley & Sons Ltd, Chichester.
8. Bode W., Engh R., Musil D., Thiele U., Huber R., Karshikov A., Brzin J., Kos J., Turk V. The 2.0 Å X-ray crystal structure of chicken egg white cystatin and its possible mode of interaction with cysteine proteinases. EMBO J. 7:1988;2593-2599.
9. Bonar L., Cohen A. S., Skinner M. Characterization of the amyloid fibril as a cross-β Protein. Proc. Soc. Expt. Biol. Med. 131:1967;1373-1375.
10. Booth D. R., Soutar A. K., Hawkins P. N., Reilly M., Harding A., Pepys M. B. Three new amyloidogenic transthyretin gene mutations: advantages of direct sequencing. Amyloid and Amyloidosis 1993. 1994;Parthenon Publishing, New York.
11. Booth D. R., Sunde M., Bellotti V., Robinson C. V., Hutchinson W. L., Fraser P. E. Instability, unfolding and fibrillogenesis in amyloidogenic lysozyme variants. Nature. 385:1997;787-793.
12. Bradbury E. M., Brown L., Downie A. R., Elliott A., Fraser R. D. B., Hanby W. E., Macdonald T. R. R. The "cross-beta" structure in polypeptides of low molecular weight. J. Mol. Biol. 2:1960;276.
13. Burge R. E. X-ray scattering by bundles of cylinders. Acta Crystallog. 12:1959;285-289.
14. Burge R. E. Equatorial X-ray diffraction by fibrous proteins: short range order in collagen, feather keratin and f-actin. J. Mol. Biol. 7:1963;213-224.
15. Burke M. J., Rougvie M. A. Cross-β protein structures I. Insulin fibrils. Biochemistry. 11:1972;2435-2439.
16. Burtnick L. D., Robinson R. C., Koepf E. K. The structure of horse plasma gelsolin to 2.5 Å Biophys. J. 70:1996;Pt. 2,-pSUA12.
17. Chothia C. Conformations of twisted β-sheets in proteins. J. Mol. Biol. 75:1973;295-302.
18. Cohen A. S., Shirahama T., Skinner M. Electron microscopy of amyloid. Harriss I. Electron Microscopy of Protein. 1981;Academic Press, London.
19. Colon W., Kelly J. W. Partial denaturation of transthyretin is sufficient for amyloid fibril formation in vitro. Biochemistry. 31:1992;8654-8660.
20. Come J. H., Fraser P. E., Lansbury P. T. A kinetic model for amyloid formation in the prion diseases: importance of seeding. Proc. Natl Acad. Sci. USA. 90:1993;5959-5963.
21. Damas A., Sebastião M. P., Domingues F. S., Costa P. P., Saraiva M. J. Structural studies on FAP fibrils: removal of contaminants is essential for the interpretation of X-ray data. Amyloid: Int. J. Exp. Clin. Invest. 2:1995;173-1278.
22. Eanes E. D., Glenner G. G. X-ray diffraction studies on amyloid filaments. J. Histochem. Cytochem. 16:1968;673-677.
23. Filshie B. K., Fraser R. D. B., MacRae T. P., Rogers G. E. X-ray diffraction and electron microscope observations on soluble derivatives of keratin. Biochem. J. 92:1964;19-26.
24. Fraser P. E., Nguyen J. T., Surewicz W. K., Kirschner D. A. pH dependent structural transitions of Alzheimer's amyloid peptides. Biophys. J. 60:1991;1190-1201.
25. Gasset M., Baldwin M. A., Lloyd D. H., Gabriel J.-M., Holtzman D. M., Cohen F. E., Fletterick R., Prusiner S. B. Predicted α-helical regions of the prion protein, when synthesized as peptides, form amyloid. Proc. Natl Acad. Sci. USA. 89:1992;10940-10944.
26. Gasset M., Baldwin M., Fletterick R., Prusiner S. Perturbation of secondary structure of the scrapie prion protein under conditions that alter infectivity. Proc. Natl Acad. Sci. USA. 90:1993;1-5.
27. Geddes A. J., Parker K. D., Atkins E. D. T., Beighton E. "Cross β" conformation in protein. J. Mol. Biol. 32:1968;343-358.
28. Gilchrist P., Bradshaw J. Amyloid formation by salmon calcitonin. Biochim. Biophys. Acta. 1993;111-114.
29. Glenner G. G. Amyloid deposits and amyloidosis. The beta-fibrilloses (part one). New Eng. J. Med. 302:1080a;1283-1292.
30. Glenner G. G. Amyloid deposits and amyloidosis. The bea-fibrilloses (part two). New Eng. J. Med. 302:1980b;1333-1343.
31. Glenner G. G., Wong C. W. Alzheimer's disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein. Biochem. Biophys. Res. Commun. 120:1984;885-890.
32. Gorevic P., Castano E., Sarma R., Frangione B. Ten to fourteen residue peptides of Alzheimer's disease protein are sufficient for amyloid fibril formation and its characteristic X-ray diffraction pattern. Biochem. Biophys. Res. Commun. 147:1987;854-862.
33. Hamilton J., Steinrauf L., Braden B., Liepnieks J., Benson M., Holmgren G., Sandgren O., Steen L. The X-ray crystal structure refinements of normal human transthyretin and the amyloidogenic Val-30-Met variant to 1.7 Å resolution. J. Biol. Chem. 268:1993;2416-2424.
34. Harrison P. M., Bamborough P., Daggett V., Prusiner S. B., Cohen F. E. The prion folding problem. Curr. Opin. Struct. Biol. 7:1997;53-59.
35. Hilbich C., Kisters-Woike B., Reed J., Masters C., Beyreuther K. Aggregation and secondary structure of synthetic amyloid βA4 peptides of Alzheimer's disease. J. Mol. Biol. 218:1991;149-163.
36. Inouye H., Fraser P. E., Kirschner D. A. Structure of β-crystallite assemblies by Alzheimer β-amyloid protein analogues: analysis by X-ray diffraction. Biopys. J. 64:1993;502-519.
37. Jarvis J. A., Craik D. J., Wilce M. C. J. X-ray diffraction studies of fibrils formed from peptide fragments of transthyretin. Biochem. Biophys. Res. Commun. 192:1993;991-998.
38. Kelly J. W. Alternative conformations of amyloidogenic proteins govern their behaviour. Curr. Opin. Struct. Biol. 6:1996;11-17.
39. Kelly J. W. Amyloid fibril formation and protein misassembly: a structural quest for insights into amyloid and prion diseases. Structure. 5:1997;595-600.
40. Kirschner D. A., Abraham C., Selkoe D. A. X-ray diffraction from intraneuronal paired helical filaments and extra-neuronal amyloid fibres in Alzheimer's disease indicates crossβ conformation. Proc. Natl Acad. Sci. USA. 83:1986;503-507.
41. Kirschner D. A., Inouye H., Duffy L., Sinclair A., Lind M., Selkoe D. A. Synthetic peptide homologous to β-protein from Alzheimer's disease forms amyloid-like fibrilsin vitro. Proc. Natl Acad. Sci. USA. 84:1987;6953-6957.
42. Lorenz M., Holmes K. C. Computer processing and analysis of X-ray diffraction data. J. Appl. Crystallog. 26:1993;82-91.
43. McCutchen S., Colon W., Kelly J. W. Transthyretin mutation Leu-55-Pro significantly alters tetramer stability and increases amyloidogenicity. Biochemistry. 32:1993;12119-12127.
44. McCutchen S. L., Lai Z., Miroy G. J., Kelly J. W., Colon W. Comparison of lethal and nonlethal transthyretin variants and their relationship to amyloid disease. Biochemistry. 34:1995;13527-13536.
45. Nelson S., Lyon M., Gallager J., Johnson E., Pepys M. B. Isolation and characterisation of the integral glycosaminoglycan constitutents of human amyloid A and monoclonal light-chain amyloid fibrils. Biochem. J. 275:1991;67-74.
46. Nguyen J. T., Inouye H., Baldwin M. A., Fletterick R., Cohen F. E., Prusiner S. B., Kirschner D. A. X-ray diffraction from scrapie prion rod and PrP peptides. J. Mol. Biol. 252:1995;412-422.
47. Nolte R. T., Atkinson D. Conformational analysis of apolipoprotein A-1 and E-3 based on primary sequence and circular dichroism. Biophys. J. 63:1992;1221-1239.
48. Pan K.-M., Baldwin M. A., Nguyen J. T., Gaseet M., Serban A., Groth D., Mehlhorn I., Huang Z., Fletterick R. J., Cohen F. E., Prusiner S. B. Conversion of α-helices into β-sheets features in the formation of the scrapie prion proteins. Proc. Natl Acad. Sci. USA. 90:1993;10962-10966.
49. Pauling L., Corey R. Configuration of polypeptide chains with favoured orientation around single bonds: two new pleated sheets. Proc. Natl Acad. Sci. USA. 37:1951;729-739.
50. Pepys M. B. Amyloidosi. Weatherall D. J., Ledingham J. G. G., Warell D. A. The Oxford Textbook of Medicine. 1996;Oxford University Press, Oxford.
51. Pepys M. B., Hawkins P. N., Booth D. R., Vigushin D. M., Tennet G. A., Soutar A. K., Totty N., Nguyen O., Blake C. C. F., Terry C. J., Feest T. G., Zalin A. M., Hsuan J. J. Human lysozyme gene mutations cause hereditary systemic amyloidosis. Nature. 362:1993;553-557.
52. Riek R., Hornemann S., Wider G., Billeter M., Glockshuber R., Wüthrich K. NMR structure of the mouse prion protein domain PrP(121-231). Nature. 382:1996;180-182.
53. Schormann N., Murrell J. R., Liepnieks J., Benson M. Tertiary structure of an amyloid immunoglobulin light chain protein: a proposed model for amyloid fibril formation. Proc. Natl Acad. Sci. USA. 92:1995;9490-9494.
54. Sebastião P., Dauter Z., Saraiva M. J., Damas A. M. Crystallization and preliminary X-ray diffraction studies of Leu55Pro variant transthyretin. Acta Crystallog. sect. D. 52:1996;566-568.
55. Serpell L. C., Sunde M., Fraser P. E., Luther P. K., Morris E., Sandgren O., Lundgren E., Blake C. C. F. The examination of the structure of the transthyretin amyloid fibril by image reconstruction from electron micrographs. J. Mol. Biol. 254:1995;113-118.
56. Shirahama T., Cohen A. S. High resolution electron microscopic analysis of the amyloid fibril. J. Cell Biol. 33:1967;679-706.
57. Shirahama T., Benson M. D., Cohen A. S., Tanaka A. Fibrillar assemblage of variable segments of immunoglobulin light chains: an electron microscopic study. J. Immunol. 110:1973;21-30.
58. Soto C., Castano E., Frangione B., Inestrosa N. The α-helical to β-sheet transition in the amino-terminal fragment of the amyloid β-peptide modulates amyloid formation. J. Biol. Chem. 270:1995;3063-3067.
59. Sticht H. P., Bayer P., Willbold D., Dames S., Hilbich C., Beyreuther K., Frank R., Rosch P. Structure of amyloid A4(1-40)-peptide of Alzheimer's disease. Eur. J. Biochem. 233:1995;293-298.
60. Soutar A. K., Hawkins P. N., Vigushin D. M., Tennent G. A., Booth S., Hutton T., Nguyen O., Totty N., Feest T. G., Hsuan J. J., Pepys M. B. Apolipoprotein A-1 mutation Arg-60 causes autosomal dominant amyloidosis. Proc. Natl Acad. Sci. USA. 89:1992;7389-7393.
61. Tagliavini F., Prelli F., Verga L., Giaccone G., Jarma R., Gorevic P., Ghetti B., Passerini F., Ghibaudi E., Forloni G., Salmona M., Bugiani O., Frangione B. Synthetic peptides homologous to prion protein residues 106-147 form amyloid-like fibrilsin vitro. Proc. Natl Acad. Sci. USA. 90:1993;9678-9682.
62. Talafous J., Marcinowski K., Klopman G., Zagorski M. Solution structure of residues 1-28 of the amyloid β-peptide. Biochemistry. 33:1994;7788-7796.
63. Tan S. Y., Pepys M. B., Hawkins P. N. Treatment of amyloidosis. Am. J. Kidney Dis. 26:1995;267-285.
64. Terry C. J., Damas A. M., Oliviera P., Saraiva M. J. M., Alves A. L., Costa P. P., Matias P. M., Sakaki Y., Blake C. C. F. Structure of Met30 variant of transthyretin and its amyloidogenic variations. EMBO J. 12:1993;735-741.
65. Turnell W., Sarra R., Baum J. O., Caspi D., Baltz M. L., Pepys M. B. X-Ray scattering and diffraction by wet gels of AA amyloid fibrils. Mol. Biol. Med. 3:1986a;409-424.
66. 1. Mol. Biol. Med. 3:1986b;387-407.
67. Worcester D. L. Structural origins of diamagnetic anisotropy in proteins. Proc. Natl Acad. Sci. USA. 75:1978;5475-5477.