Polymorphic fibril formation by residues 10-40 of the Alzheimer's β-amyloid peptide

Biophysical Journal

Volumn 90, Issue 12, 2006, Pages 4618-4629

  Paravastu, Anant K ^a   Petkova, Aneta T ^a,c   Tycko, Robert ^a,b  

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

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c University of Florida ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN;

ALZHEIMER DISEASE; AMINO ACID SEQUENCE; ARTICLE; ATOMIC FORCE MICROSCOPY; CHEMICAL STRUCTURE; ELECTRON MICROSCOPY; FIBER; FREEZE DRYING; GENETIC POLYMORPHISM; HYDRATION; NUCLEAR MAGNETIC RESONANCE;

EID: 33744831968     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.105.076927     Document Type: Article

References (45)

1. Booth, D. R., M. Sunde, V. Bellotti, C. V. Robinson, W. L. Hutchinson, P. E. Fraser, P. N. Hawkins, C. M. Dobson, S. E. Radford, C. C. Blake, and A. M. Pepys. 1997. Instability, unfolding and aggregation of human lysozyme variants underlying amyloid fibrillogenesis. Nature. 385:787-793.
2. Chiti, F., P. Webster, N. Taddei, A. Clark, M. Stefani, G. Ramponi, and C. M. Dobson. 1999. Designing conditions for in vitro formation of amyloid protofilaments and fibrils. Proc. Natl. Acad. Sci. USA. 96:3590-3594.
3. Dobson, C. M. 2003. Protein folding and misfolding. Nature. 426:884-890.
4. Sunde, M., and C. C. F. Blake. 1998. From the globular to the fibrous state: protein structure and structural conversion in amyloid formation. Q. Rev. Biophys. 31:1-39.
5. Sipe, J. D. 1992. Amyloidosis. Annu. Rev. Biochem. 61:947-975.
6. Balbach, J. J., A. T. Petkova, N. A. Oyler, O. N. Antzutkin, D. J. Gordon, S. C. Meredith, and R. Tycko. 2002. 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. 83:1205-1216.
7. 16-22, a seven-residue fragment of the Alzheimer's β-amyloid peptide, and structural characterization by solid state NMR. Biochemistry. 39:13748-13759.
8. Petkova, A. T., Y. Ishii, J. J. Balbach, O. N. Antzutkin, R. D. Leapman, F. Delaglio, and R. Tycko. 2002. A structural model for Alzheimer's β-amyloid fibrils based on experimental constraints from solid state NMR. Proc. Natl. Acad. Sci. USA. 99:16742-16747.
9. Petkova, A. T., R. D. Leapman, Z. H. Guo, W. M. Yau, M. P. Mattson, and R. Tycko. 2005. Self-propagating, molecular-level polymorphism in Alzheimer's β-amyloid fibrils. Science. 307:262-265.
10. Jaroniec, C. P., C. E. MacPhee, V. S. Bajaj, M. T. McMahon, C. M. Dobson, and R. G. Griffin. 2004. High-resolution molecular structure of a peptide in an amyloid fibril determined by magic angle spinning NMR spectroscopy. Proc. Natl. Acad. Sci. USA. 101:711-716.
11. Antzutkin, O. N., J. J. Balbach, R. D. Leapman, N. W. Rizzo, J. Reed, and R. Tycko. 2000. Multiple quantum solid-state NMR indicates a parallel, not antiparallel, organization of β-sheets in Alzheimer's β-amyloid fibrils. Proc. Natl. Acad. Sci. USA. 97:13045-13050.
12. Petkova, A. T., G. Buntkowsky, F. Dyda, R. D. Leapman, W. M. Yau, and R. Tycko. 2004. Solid state NMR reveals a pH-dependent antiparallel β-sheet registry in fibrils formed by a β-amyloid peptide. J. Mol. Biol. 335:247-260.
13. Torok, M., S. Milton, R. Kayed, P. Wu, T. McIntire, C. G. Glabe, and R. Langen. 2002. Structural and dynamic features of Alzheimer's Aβ peptide in amyloid fibrils studied by site-directed spin labeling. J. Biol. Chem. 277:40810-40815.
14. Der-Sarkissian, A., C. C. Jao, J. Chen, and R. Langen. 2003. Structural organization of α-synuclein fibrils studied by site-directed spin labeling. J. Biol. Chem. 278:37530-37535.
15. Jayasinghe, S. A., and R. Langen. 2004. Identifying structural features of fibrillar islet amyloid polypeptide using site-directed spin labeling. J. Biol. Chem. 279:48420-48425.
16. 1-40 amyloid fibril secondary structure using nuclear magnetic resonance spectroscopy. Biochemistry. 44:4434-4441.
17. Wang, S. S. S., S. A. Tobler, T. A. Good, and E. J. Fernandez. 2003. Hydrogen exchange-mass spectrometry analysis of β-amyloid peptide structure. Biochemistry. 42:9507-9514.
18. Ritter, C., M. L. Maddelein, A. B. Siemer, T. Luhrs, M. Ernst, B. H. Meier, S. J. Saupe, and R. Riek. 2005. Correlation of structural elements and infectivity of the HET-s prion. Nature. 435:844-848.
19. Williams, A. D., E. Portelius, I. Kheterpal, J. T. Guo, K. D. Cook, Y. Xu, and R. Wetzel. 2004. Mapping Aβ amyloid fibril secondary structure using scanning proline mutagenesis. J. Mol. Biol. 335:833-842.
20. Shivaprasad, S., and R. Wetzel. 2004. An intersheet packing interaction in Aβ fibrils mapped by disulfide cross-linking. Biochemistry. 43:15310-15317.
21. Gordon, D. J., J. J. Balbach, R. Tycko, and S. C. Meredith. 2004. Increasing the amphiphilicity of an amyloidogenic peptide changes the β-sheet structure in the fibrils from antiparallel to parallel. Biophys. J. 86:428-434.
22. Lansbury, P. T., P. R. Costa, J. M. Griffiths, E. J. Simon, M. Auger, K. J. Halverson, D. A. Kocisko, Z. S. Hendsch, T. T. Ashburn, R. G. S. Spencer, B. Tidor, and R. G. Griffin. 1995. Structural model for the β-amyloid fibril based on interstrand alignment of an antiparallel-sheet comprising a C-terminal peptide. Nat. Struct. Biol. 2:990-998.
23. (10-35) fibril. J. Am. Chem. Soc. 122:7883-7889.
24. Kammerer, R. A., D. Kostrewa, J. Zurdo, A. Detken, C. Garcia-Echeverria, J. D. Green, S. A. Muller, B. H. Meier, F. K. Winkler, C. M. Dobson, and M. O. Steinmetz. 2004. Exploring amyloid formation by a de novo design. Proc. Natl. Acad. Sci. USA. 101:4435-4440.
25. Goldsbury, C. S., S. Wirtz, S. A. Muller, S. Sunderji, P. Wicki, U. Aebi, and P. Frey. 2000. Studies on the in vitro assembly of Aβ 1-40: implications for the search for Aβ fibril formation inhibitors. J. Struct. Biol. 130:217-231.
26. Jimenez, J. L., E. J. Nettleton, M. Bouchard, C. V. Robinson, C. M. Dobson, and H. R. Saibil. 2002. The protofilament structure of insulin amyloid fibrils. Proc. Natl. Acad. Sci. USA. 99:9196-9201.
27. Harper, J. D., S. S. Wong, C. M. Lieber, and P. T. Lansbury. 1997. Observation of metastable Aβ amyloid protofibrils by atomic force microscopy. Chem. Biol. 4:119-125.
28. Bessen, R. A., and R. F. Marsh. 1992. Biochemical and physical properties of the prion protein from 2 strains of the transmissible mink encephalopathy agent. J. Virol. 66:2096-2101.
29. Telling, G. C., P. Parchi, S. J. DeArmond, P. Cortelli, P. Montagna, R. Gabizon, J. Mastrianni, E. Lugaresi, P. Gambetti, and S. B. Prusiner. 1996. Evidence for the conformation of the pathologic isoform of the prion protein enciphering and propagating prion diversity. Science. 274:2079-2082.
30. Safar, J., H. Wille, V. Itrri, D. Groth, H. Serban, M. Torchia, F. E. Cohen, and S. B. Prusiner. 1998. Eight prion strains have PrPSc molecules with different conformations. Nat. Med. 4:1157-1165.
31. Chien, P., and J. S. Weissman. 2001. Conformational diversity in a yeast prion dictates its seeding specificity. Nature. 410:223-227.
32. Kheterpal, I., A. Williams, C. Murphy, B. Bledsoe, and R. Wetzel. 2001. Structural features of the Aβ amyloid fibril elucidated by limited proteolysis. Biochemistry. 40:11757-11767.
33. Hilbich, C., B. Kisterswoike, J. Reed, C. L. Masters, and K. Beyreuther. 1991. Aggregation and secondary structure of synthetic amyloid βA4 peptides of Alzheimer's. J. Mol. Biol. 218:149-163.
34. Perutz, M. F., J. T. Finch, J. Berriman, and A. Lesk. 2002. Amyloid fibers are water-filled nanotubes. Proc. Natl. Acad. Sci. USA. 99:5591-5595.
35. Kishimoto, A., K. Hasegawa, H. Suzuki, H. Taguchi, K. Namba, and M. Yoshida. 2004. β-Helix is a likely core structure of yeast prion Sup35 amyloid fibers. Biochem. Biophys. Res. Commun. 315:739-745.
36. Bennett, A. E., C. M. Rienstra, M. Auger, K. V. Lakshmi, and R. G. Griffin. 1995. Heteronuclear decoupling in rotating solids. J. Chem. Phys. 103:6951-6958.
37. 13C dipolar recoupling under very fast magic angle spinning in solid-state nuclear magnetic resonance: applications to distance measurements, spectral assignments, and high-throughput secondary-structure determination. J. Chem. Phys. 114:8473-8483.
38. Morcombe, C. R., V. Gaponenko, R. A. Byrd, and K. W. Zilm. 2004. Diluting abundant spins by isotope edited radio frequency field assisted diffusion. J. Am. Chem. Soc. 126:7196-7197.
39. 1H dipolar-assisted rotational resonance in magic-angle spinning NMR. Chem. Phys. Lett. 344:631-637.
40. Wishart, D. S., B. D. Sykes, and F. M. Richards. 1991. Relationship between nuclear magnetic resonance chemical shift and protein secondary structure. J. Mol. Biol. 222:311-333.
41. Lomakin, A., D. B. Teplow, D. A. Kirschner, and G. B. Benedek. 1997. Kinetic theory of fibrillogenesis of amyloid β-protein. Proc. Natl. Acad. Sci. USA. 94:7942-7947.
42. Collins, S. R., A. Douglass, R. D. Vale, and J. S. Weissman. 2004. Mechanism of prion propagation: amyloid growth occurs by monomer addition. PLoS Biol. 2:1582-1590.
43. Chan, J. C. C., N. A. Oyler, W. M. Yau, and R. Tycko. 2005. Parallel β-sheets and polar zippers in amyloid fibrils formed by residues 10-39 of the yeast prion protein Ure2p. Biochemistry. 44:10669-10680.
44. Roher, A. E., J. D. Lowenson, S. Clarke, C. Wolkow, R. Wang, R. J. Cotter, I. M. Reardon, H. A. Zurcher-Neely, R. L. Heinrikson, and M. J. Ball. 1993. 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. 268:3072-3083.
45. 15N random coil NMR chemical shifts of the common amino acids. I. Investigations of nearest-neighbor effects. J. Biomol. NMR. 5:67-81.