The structural biology of protein aggregation diseases: Fundamental questions and some answers

Accounts of Chemical Research

Volumn 39, Issue 9, 2006, Pages 568-575

  Eisenberg, David ^a   Nelson, Rebecca ^a   Sawaya, Michael R ^a   Balbirnie, Melinda ^a   Sambashivan, Shilpa ^a   Ivanova, Magdalena I ^a   Madsen, Anders Ø ^b,c   Riekel, Christian ^c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c EUROPEAN SYNCHROTRON RADIATION FACILITY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID; PROTEIN;

CHEMISTRY; METABOLISM; PROTEIN CONFORMATION; REVIEW; X RAY CRYSTALLOGRAPHY;

AMYLOID; CRYSTALLOGRAPHY, X-RAY; PROTEIN CONFORMATION; PROTEINS;

EID: 33749818217     PISSN: 00014842     EISSN: None     Source Type: Journal    
DOI: 10.1021/ar0500618     Document Type: Review

References (65)

1. Sikorski, P.; Atkins, E. New model for crystalline polyglutamine assemblies and their connection with amyloid fibrils. Biomacromolecules 2005, 6, 425-432.
2. Makin, O. S.; Serpell, L. C. Structures for amyloid fibrils. FEBS J. 2005, 272, 5950-5961.
3. Janowski, R.; Kozak, M.; Jankowska, E.; Grzonka, Z.; Grubb, A.; Abrahamson, M.; Jaskolski, M. Human cystatin C, an amyloidogenic protein, dimerizes through three-dimensional domain swapping. Nat. Struct. Biol. 2001, 8, 316-320.
4. Kishimoto, A.; Hasegawa, K.; Suzuki, H.; Taguchi, H.; Namba, K.; Yoshida, M. β-Helix is a likely core structure of yeast prion Sup35 amyloid fibers. Biochem. Biophys. Res. Commun. 2004, 315, 739-745.
5. Krishnan, R.; Lindquist, S. L. Structural insights into a yeast prion illuminate nucleation and strain diversity. Nature 2005, 435, 765-772.
6. Kajava, A. V.; Baxa, U.; Wickner, R. B.; Steven, A. C. A model for Ure2p prion filaments and other amyloids: the parallel superpleated β-structure. Proc. Natl. Acad. Sci. U.S.A. 2004, 101, 7885-7890.
7. Kajava, A. V.; Aebi, U.; Steven, A. C. The parallel superpleated β-structure as a model for amyloid fibrils of human amylin. J. Mol. Biol. 2005, 348, 247-252.
8. Petkova, A. T.; Buntkowsky, G.; Dyda, F.; Leapman, R. D.; Yau, W. M.; Tycko, R. Solid state NMR reveals a pH-dependent antiparallel -sheet registry in fibrils formed by a β-amyloid peptide. J. Mol. Biol. 2004, 335, 247-260.
9. Ritter, C.; Maddelein, M. L.; Siemer, A. B.; Lührs, T.; Ernst, M.; Meier, B. H.; Saupe, S. J.; Riek, R. Correlation of structural elements and infectivity of the HET-s prion. Nature 2005, 435, 844-848.
10. Lührs, T.; Ritter, C.; Adrian, M.; Riek-Loher, D.; Bohrmann, B.; Döbeli, H.; Schubert, D.; Riek, R. 3D structure of Alzheimer's amyloid-β(1-42) fibrils. Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 17342-17347.
11. Williams, A. D.; Portelius, E.; Kheterpal, I.; Guo, J. T.; Cook, K. D.; Xu, Y.; Wetzel, R. Mapping Aβ amyloid fibril secondary structure using scanning proline mutagenesis. J. Mol. Biol. 2004, 335, 833-842.
12. Westermark, P. Aspects on human amyloid forms and their fibril polypeptides. FEBS J. 2005, 272, 5942-5949.
13. Astbury, W. T.; Dickinson, S.; Bailey, K. The X-ray interpretation of denaturation and the structure of the seed globulins. Biochem. J. 1935, 29, 2351-2360.
14. Eanes, E. D.; Glenner, G. G. X-ray diffraction studies on amyloid filaments. J. Histochem. Cytochem. 1968, 16, 673-677.
15. Sunde, M.; Serpell, L. C.; Bartlam, M.; Fraser, P. E.; Pepys, M. B.; Blake, C. C. Common core structure of amyloid fibrils by synchrotron X-ray diffraction. J. Mol. Biol. 1997, 273, 729-739.
16. Rochet, J. C.; Lansbury, P. T., Jr. Amyloid fibrillogenesis: themes and variations. Curr. Opin. Struct. Biol. 2000, 10, 60-68.
17. Westermark, P.; Benson, M. D.; Buxbaum, J. N.; Cohen, A. S.; Frangione, B.; Ikeda, S.; Masters, C. L.; Merlini, G.; Saraiva, M. J.; Sipe, J. D. Amyloid fibril protein nomenclature - 2002. Amyloid 2002, 9, 197-200.
18. Guijarro, J. I.; Sunde, M.; Jones, J. A.; Campbell, I. D.; Dobson, C. M. Amyloid fibril formation by an SH3 domain. Proc. Natl. Acad. Sci. U.S.A. 1998, 95, 4224-4228.
19. Fändrich, M.; Fletcher, M. A.; Dobson, C. M. Amyloid fibrils from muscle myoglobin. Nature 2001, 410, 165-166.
20. Fändrich, M.; Dobson, C. M. The behaviour of polyamino acids reveals an inverse side chain effect in amyloid structure formation. EMBO J. 2002, 21, 5682-5690.
21. Fändrich, M.; Forge, V.; Buder, K.; Kittler, M.; Dobson, C. M.; Diekmann, S. Myoglobin forms amyloid fibrils by association of unfolded polypeptide segments. Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 15463-15468.
22. Dobson, C. M. Protein misfolding, evolution and disease. Trends Biochem. Sci. 1999, 24, 329-332.
23. Wickner, R. B. [URE3] as an altered URE2 protein: evidence for a prion analog in Saccharomyces cerevisiae. Science 1994, 264, 566-569.
24. Patino, M. M.; Liu, J. J.; Glover, J. R.; Lindquist, S. Support for the prion hypothesis for inheritance of a phenotypic trait in yeast. Science 1996, 273, 622-626.
25. Serio, T. R.; Cashikar, A. G.; Kowal, A. S.; Sawicki, G. J.; Moslehi, J. J.; Serpell, L.; Arnsdorf, M. F.; Lindquist, S. L. Nucleated conformational conversion and the replication of conformational information by a prion determinant. Science 2000, 289, 1317-1321.
26. King, C. Y.; Diaz-Avalos, R. Protein-only transmission of three yeast prion strains. Nature 2004, 428, 319-323.
27. Tanaka, M.; Chien, P.; Naber, N.; Cooke, R.; Weissman, J. S. Conformational variations in an infectious protein determine prion strain differences. Nature 2004, 428, 323-328.
28. DePace, A. H.; Santoso, A.; Hillner, P.; Weissman, J. S. A critical role for amino-terminal glutamine/asparagine repeats in the formation and propagation of a yeast prion. Cell 1998, 93, 1241-1252.
29. Santoso, A.; Chien, P.; Osherovich, L. Z.; Weissman, J. S. Molecular basis of a yeast prion species barrier. Cell 2000, 100, 277-288.
30. 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. U.S.A. 2001, 98, 2375-2380.
31. Riekel, C. Recent developments in micro-diffraction on protein crystals. J. Synchrotron Radiat. 2004, 11, 4-6.
32. Nelson, R.; Sawaya, M. R.; Balbirnie, M.; Madsen, A. O.; Riekel, C.; Grothe, R.; Eisenberg, D. Structure of the cross-β spine of amyloid-like fibrils. Nature 2005, 435, 773-778.
33. Jaroniec, C. P.; MacPhee, C. E.; Bajaj, V. S.; McMahon, M. T.; Dobson, C. M.; Griffin, R. G. High-resolution molecular structure of a peptide in an amyloid fibril determined by magic angle spinning NMR spectroscopy. Proc. Natl. Acad. Sci. U.S.A. 2004, 101, 711-716.
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. 2000, 122, 7883-7889.
35. Petkova, A. T.; Ishii, Y.; Balbach, J. J.; Antzutkin, O. N.; Leapman, R. D.; Delaglio, F.; Tycko, R. A structural model for Alzheimer's β-amyloid fibrils based on experimental constraints from solid state NMR. Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 16742-16747.
36. Paravastu, A. K.; Petkova, A. T.; Tycko, R. Polymorphic fibril formation by residues 10-40 of the Alzheimer's β-amyloid peptide. Biophys. J. 2006, 90, 4618-4629.
37. Siemer, A. B.; Ritter, C.; Steinmetz, M. O.; Ernst, M.; Riek, R.; Meier, B. H. 13C, 15N resonance assignment of parts of the HET-s prion protein in its amyloid form. J. Biomol. NMR 2006, 34, 75-87.
38. 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. 2002, 9, 734-739.
39. Török, M.; Milton, S.; Kayed, R.; Wu, P.; McIntire, T.; Glabe, C. G.; Langen, R. Structural and dynamic features of Alzheimer's Aβ peptide in amyloid fibrils studied by site-directed spin labeling. J. Biol. Chem. 2002, 277, 40810-40815.
40. Hoshino, M.; Katou, H.; Hagihara, Y.; Hasegawa, K.; Naiki, H.; Goto, Y. Mapping the core of the β(2)-microglobulin amyloid fibril by H/D exchange. Nat. Struct. Biol. 2002, 9, 332-336.
41. Thakur, A. K.; Wetzel, R. Mutational analysis of the structural organization of polyglutamine aggregates. Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 17014-17019.
42. Jiménez, J. L.; Guijarro, J. I.; 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. 1999, 18, 815-821.
43. Jiménez, 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. U.S.A. 2002, 99, 9196-9201.
44. Goldsbury, C.; Goldie, K.; Pellaud, J.; Seelig, J.; Frey, P.; Muller, S. A.; Kistler, J.; Cooper, G. J.; Aebi, U. Amyloid fibril formation from full-length and fragments of amylin. J. Struct. Biol. 2000, 130, 352-362.
45. McParland, V. J.; Kalverda, A. P.; Homans, S. W.; Radford, S. E. Structural properties of an amyloid precursor of β(2)-microglobulin. Nat. Struct. Biol. 2002, 9, 326-331.
46. Lopez de la Paz, M.; Serrano, L. Sequence determinants of amyloid fibril formation. Proc. Natl. Acad. Sci. U.S.A. 2004, 101, 87-92.
47. Nelson, R.; Eisenberg, D. Structural models of amyloid-like fibrils. Adv. Protein Chem., in press.
48. Lawrence, M. C.; Colman, P. M. Shape complementarity at protein/protein interfaces. J. Mol. Biol. 1993, 234, 946-950.
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. U.S.A. 1994, 91, 5355-5358.
50. Perutz, M. F.; Finch, J. T.; Berriman, J.; Lesk, A. Amyloid fibers are water-filled nanotubes. Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 5591-5595.
51. Varley, P.; Gronenborn, A. M.; Christensen, H.; Wingfield, P. T.; Pain, R. H.; Clore, G. M. Kinetics of folding of the all-β sheet protein interleukin-1 β. Science 1993, 260, 1110-1113.
52. Sivaraman, T.; Kumar, T. K.; Chang, D. K.; Lin, W. Y.; Yu, C. Events in the kinetic folding pathway of a small, all β-sheet protein. J. Biol. Chem. 1998, 273, 10181-10189.
53. Liu, Y.; Gotte, G.; Libonati, M.; Eisenberg, D. A domain-swapped RNase A dimer with implications for amyloid formation. Nat. Struct. Biol. 2001, 8, 211-214.
54. Crestfield, A. M.; Stein, W. H.; Moore, S. Properties and conformation of the histidine residues at the active site of ribonuclease. J. Biol. Chem. 1963, 238, 2421-2428.
55. Gotte, G.; Bertoldi, M.; Libonati, M. Structural versatility of bovine ribonuclease A. Distinct conformers of trimeric and tetrameric aggregates of the enzyme. Eur. J. Biochem. 1999, 265, 680-687.
56. Sambashivan, S.; Liu, Y.; Sawaya, M. R.; Gingery, M.; Eisenberg, D. Amyloid-like fibrils of ribonuclease A with three-dimensional domain-swapped and native-like structure. Nature 2005, 437, 266-269.
57. Baxa, U.; Cheng, N.; Winkler, D. C.; Chiu, T. K.; Davies, D. R.; Sharma, D.; Inouye, H.; Kirschner, D. A.; Wickner, R. B.; Steven, A. C. Filaments of the Ure2p prion protein have a cross-β core structure. J. Struct. Biol. 2005, 150, 170-179.
58. Bousset, L.; Briki, F.; Doucet, J.; Melki, R. The native-like conformation of Ure2p in fibrils assembled under physiologically relevant conditions switches to an amyloid-like conformation upon heat-treatment of the fibrils. J. Struct. Biol. 2003, 141, 132-142.
59. Bousset, L.; Redeker, V.; Decottignies, P.; Dubois, S.; Le Marechal, P.; Melki, R. Structural characterization of the fibrillar form of the yeast Saccharomyces cerevisiae prion Ure2p. Biochemistry 2004, 43, 5022-5032.
60. Eakin, C. M.; Attenello, F. J.; Morgan, C. J.; Miranker, A. D. Oligomeric assembly of native-like precursors precedes amyloid formation by β-2 microglobulin. Biochemistry 2004, 43, 7808-7815.
61. Baxa, U.; Taylor, K. L.; Wall, J. S.; Simon, M. N.; Cheng, N.; Wickner, R. B.; Steven, A. C. Architecture of Ure2p prion filaments: the N-terminal domains form a central core fiber. J. Biol. Chem. 2003, 278, 43717-43727.
62. Thompson, M. J.; Sievers, S. A.; Karanicolas, J.; Ivanova, M. I.; Baker, D.; Eisenberg, D. The 3D profile method for identifying fibril-forming segments of proteins. Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 4074-4078.
63. Ivanova, M. I.; Sawaya, M. R.; Gingery, M.; Attinger, A.; Eisenberg, D. An amyloid-forming segment of β2-microglobulin suggests a molecular model for the fibril. Proc. Natl. Acad. Sci. U.S.A. 2004, 101, 10584-10589.
64. Ivanova, M. I.; Thompson, M. J.; Eisenberg, D. A systematic screen of β(2)-microglobulin and insulin for amyloid-like segments. Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 4079-4082.
65. 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. 2001, 20, 4774-4781.