Modeling the Alzheimer Aβ17-42 fibril architecture: Tight intermolecular sheet-sheet association and intramolecular hydrated cavities

Biophysical Journal

Volumn 93, Issue 9, 2007, Pages 3046-3057

  Zheng, Jie ^a,c   Jang, Hyunbum ^a   Ma, Buyong ^a   Tsai, Chung Jun ^a   Nussinov, Ruth ^a,b  

^a NATIONAL CANCER INSTITUTE   (United States)

^b TEL AVIV UNIVERSITY   (Israel)

^c The University of Akron   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID; AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN (17 42); AMYLOID BETA-PROTEIN (17-42); PEPTIDE FRAGMENT; UNCLASSIFIED DRUG; WATER;

ALZHEIMER DISEASE; AMINO TERMINAL SEQUENCE; ARTICLE; BETA SHEET; CARBOXY TERMINAL SEQUENCE; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN MOTIF; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER SIMULATION; HUMAN; METABOLISM; PROTEIN CONFORMATION; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; THERMODYNAMICS;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; COMPUTER SIMULATION; HUMANS; MODELS, MOLECULAR; PEPTIDE FRAGMENTS; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; THERMODYNAMICS; WATER;

EID: 36148983867     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.107.110700     Document Type: Article

References (59)

1. Buxbaum, J. D., E. H. Koo, and P. Greengard. 1993. Protein phosphorylation inhibits production of Alzheimer amyloid beta/A4 peptide. Proc. Natl. Acad. Sci. USA. 90:9195-9198.
2. Lin, H., R. Bhatia, and R. Lal. 2001. Amyloid beta protein forms ion channels: implications for Alzheimer's disease pathophysiology. FASEB J. 15:2433-2444.
3. Fraser, P. E., L. Levesque, and D. R. McLachlan. 1993. Biochemistry of Alzheimer's disease amyloid plaques. Clin. Biochem. 26:339-349.
4. Wertkin, A. M., R. S. Turner, S. J. Pleasure, T. E. Golde, S. G. Younkin, J. Q. Trojanowski, and V. M. Lee. 1993. Human neurons derived from a teratocarcinoma cell line express solely the 695-amino acid amyloid precursor protein and produce intracellular beta-amyloid or A4 peptides. Proc. Natl. Acad. Sci. USA. 90:9513-9517.
5. Lamour, Y. 1994. Alzheimer's disease: a review of recent findings. Biomedecine & Pharmacotherapy. 48:312-318.
6. Kayed, R., E. Head, J. L. Thompson, T. M. McIntire, S. C. Milton, C. W. Cotman, and C. G. Glabe. 2003. Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science. 300:486-489.
7. Bucciantini, M., E. Giannoni, F. Chiti, F. Baroni, L. Formigli, J. Zurdo, N. Taddei, G. Ramponi, C. M. Dobson, and M. Stefani. 2002. Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases. Nature. 416:507-511.
8. Cleary, J. P., D. M. Walsh, J. J. Hofmeister, G. M. Shankar, M. A. Kuskowski, D. J. Selkoe, and K. H. Ashe. 2005. Natural oligomers of the amyloid-beta protein specifically disrupt cognitive function. Nat. Neurosci. 8:79-84.
9. Mousseau, N., and P. Derreumaux. 2005. Exploring the early steps of amyloid peptide aggregation by computers. Acc. Chem. Res. 38:885-891.
10. Makabe, K., D. McElheny, V. Tereshko, A. Hilyard, G. Gawlak, S. Yan, A. Koide, and S. Koide. 2006. Atomic structures of peptide self-assembly mimics. Proc. Natl. Acad. Sci. USA. 103:17753-17758.
11. Petkova, A. T., R. D. Leapman, Z. Guo, W.-M. Yau, M. P. Mattson, and R. Tycko. 2005. Self-propagating, molecular-level polymorphism in Alzheimer's beta-amyloid fibrils. Science. 307:262-265.
12. 13C solid-state NMR spectroscopy. Magn. Reson. Chem. 42:247-257.
13. Luhrs, T., C. Ritter, M. Adrian, D. Riek-Loher, B. Bohrmann, H. Dobeli, D. Schubert, and R. Riek. 2005. 3D structure of Alzheimer's amyloid-beta (1-42) fibrils. Proc. Natl. Acad. Sci. USA. 102:17342-17347.
14. Ma, B., and R. Nussinov. 2002. Stabilities and conformations of Alzheimer's beta-amyloid peptide oligomers (Abeta 16-22, Abeta 16-35, and Abeta 10-35): sequence effects. Proc. Natl. Acad. Sci. USA. 99:14126-14131.
15. Petkova, A. T., W. M. Yau, and R. Tycko. 2006. Experimental constraints on quaternary structure in Alzheimer's beta-amyloid fibrils. Biochemistry. 45:498-512.
16. Butterfield, D. A., and A. I. Bush. 2004. Alzheimer's amyloid betapeptide (1-42): involvement of methionine residue 35 in the oxidative stress and neurotoxicity properties of this peptide. Neurobiol. Aging. 25:563-568.
17. Ciccotosto, G. D., D. Tew, C. C. Curtain, D. Smith, D. Carrington, C. L. Masters, A. I. Bush, R. A. Cherny, R. Cappai, and K. J. Barnham. 2004. Enhanced toxicity and cellular binding of a modified amyloid fbetag peptide with a methionine to valine substitution. J. Biol. Chem. 279:42528-42534.
18. Hou, L., I. Kang, R. E. Marchant, and M. G. Zagorski. 2002. Methionine 35 oxidation reduces fibril assembly of the amyloid A[beta]-(1-42) peptide of Alzheimer's disease. J. Biol. Chem. 277:40173-40176.
19. Palmblad, M., A. Westlind-Danielsson, and J. Bergquist. 2002. Oxidation of methionine 35 attenuates formation of amyloid beta-peptide 1-40 oligomers. J. Biol. Chem. 277:19506-19510.
20. Sato, T., P. Kienlen-Campard, M. Ahmed, W. Liu, H. Li, J. I. Elliott, S. Aimoto, S. N. Constantinescu, J. N. Octave, and S. O. Smith. 2006. Inhibitors of amyloid toxicity based on beta-sheet packing of Abeta40 and Abeta42. Biochemistry. 45:5503-5516.
21. Zheng, J., B. Ma, C.-J. Tsai, and R. Nussinov. 2006. Structural stability and dynamics of an amyloid-forming peptide GNNQQNY from the yeast prion sup-35. Biophys. J. 91:824-833.
22. Tsai, H.-H., M. Reches, C.-J. Tsai, K. Gunasekaran, E. Gazit, and R. Nussinov. 2005. Energy landscape of amyloidogenic peptide oligomerization by parallel-tempering molecular dynamics simulation: significant role of Asn ladder. Proc. Natl. Acad. Sci. USA. 102:8174-8179.
23. Nguyen, H. D., and C. K. Hall. 2006. Spontaneous fibril formation by polyalanines: discontinuous molecular dynamics simulations. J. Am. Chem. Soc. 128:1890-1901.
24. Kale, L., R. Skeel, M. Bhandarkar, R. Brunner, A. Gursoy, N. Krawetz, J. Phillips, A. Shinozaki, K. Varadarajan, and K. Schulten. 1999. NAMD2: greater scalability for parallel molecular dynamics. J. Comput. Phys. 151:283-312.
25. Brooks, B. R., R. E. Bruccoleri, B. D. Olafson, D. J. States, S. Swaminathan, and M. Karplus. 1983. CHARMM: a program for macromolecular energy, minimization, and dynamics calculations. J. Comput. Chem. 4:187-217.
26. Lee, M. S., M. Feig, F. R. Salsbury Jr., and C. L. Brooks III. 2003. New analytic approximation to the standard molecular volume definition and its application to generalized Born calculations. J. Comput. Chem. 24:1348-1356.
27. Lawrence, M. C., and P. M. Colman. 1993. Shape complementarity at protein/protein interfaces. J. Mol. Biol. 234:946-950.
28. Buchete, N.-V., R. Tycko, and G. Hummer. 2005. Molecular dynamics simulations of Alzheimer's beta-amyloid protofilaments. J. Mol. Biol. 353:804-821.
29. Bitan, G., B. Tarus, S. S. Vollers, H. A. Lashuel, M. M. Condron, J. E. Straub, and D. B. Teplow. 2003. A molecular switch in amyloid assembly: Met35-protein and amyloid beta-protein oligomerization. J. Am. Chem. Soc. 125:15359-15365.
30. Nilsberth, C., A. Westlind-Danielsson, C. B. Eckman, M. M. Condron, K. Axelman, C. Forsell, C. Stenh, J. Luthman, D. B. Teplow, S. G. Younkin, J. Naslund, and L. Lannfelt. 2001. The 'Arctic' APP mutation (E693G) causes Alzheimer's disease by enhanced Abeta protofibril formation. Nat. Neurosci. 4:887-893.
31. Murakami, K., K. Irie, A. Morimoto, H. Ohigashi, M. Shindo, M. Nagao, T. Shimizu, and T. Shirasawa. 2003. Neurotoxicity and physicochemical properties of Abeta mutant peptides from cerebral amyloid angiopathy: implication for the pathogenesis of cerebral amyloid angiopathy and Alzheimer's disease. J. Biol. Chem. 278:46179-46187.
32. Klimov, D. K., and D. Thirumalai. 2003. Dissecting the assembly of Abeta16-22 amyloid peptides into antiparallel beta sheets. Structure. 11:295-307.
33. Baumketner, A., S. L. Bernstein, T. Wyttenbach, N. D. Lazo, D. B. Teplow, M. T. Bowers, and J.-E. Shea. 2006. Structure of the 21-30 fragment of amyloid beta-protein. Protein Sci. 15:1239-1247.
34. Buchete, N.-V., and G. Hummer. 2007. Structure and dynamics of parallel beta-sheets, hydrophobic core, and loops in Alzheimer's Abeta fibrils. Biophys. J. 92:3032-3039.
35. Makhatadze, G., and P. Privalov. 1995. Energetics of protein structure. Adv. Protein Chem. 47:307-425.
36. Iwata, K., T. Fujiwara, Y. Matsuki, H. Akutsu, S. Takahashi, H. Naiki, and Y. Goto. 2006. 3D structure of amyloid protofilaments of beta2-microglobulin fragment probed by solid-state NMR. Proc. Natl. Acad. Sci. USA. 103:18119-18124.
37. Michael, W. M., and L. J. William. 2001. Diffusion constant of the TIP5P model of liquid water. J. Chem. Phys. 114:363-366.
38. Makin, O. S., and L. C. Serpell. 2005. Structures for amyloid fibrils. FEBS J. 272:5950-5961.
39. Ferguson, N., J. Becker, H. Tidow, S. Tremmel, T. D. Sharpe, G. Krause, J. Flinders, M. Petrovich, J. Berriman, H. Oschkinat, and A. R. Fersht. 2006. General structural motifs of amyloid protofilaments. Proc. Natl. Acad. Sci. USA. 103:16248-16253.
40. Zheng, J., B. Ma, and R. Nussinov. 2006. Consensus features in amyloid fibrils: sheet-sheet recognition via a (polar or nonpolar) zipper structure. Physical Biology. 3:P1-P4.
41. Zanuy, D., B. Ma, and R. Nussinov. 2003. Short peptide amyloid organization: stabilities and conformations of the islet amyloid peptide NFGAIL. Biophys. J. 84:1884-1894.
42. Zanuy, D., and R. Nussinov. 2003. The sequence dependence of fiber organization. a comparative molecular dynamics study of the islet amyloid polypeptide segments 22-27 and 22-29. J. Mol. Biol. 329:565-584.
43. Nelson, R., M. R. Sawaya, M. Balbirnie, A. O. Madsen, C. Riekel, R. Grothe, and D. Eisenberg. 2005. Structure of the cross-beta spine of amyloid-like fibrils. Nature. 435:773-778.
44. Esposito, L., C. Pedone, and L. Vitagliano. 2006. Molecular dynamics analyses of cross-beta-spine steric zipper models: beta-sheet twisting and aggregation. Proc. Natl. Acad. Sci. USA. 103:11533-11538.
45. Sawaya, M. R., S. Sambashivan, R. Nelson, M. I. Ivanova, S. A. Sievers, M. I. Apostol, M. J. Thompson, M. Balbirnie, J. J. W. Wiltzius, H. T. McFarlane, A. O. Madsen, C. Riekel, and D. Eisenberg. 2007. Atomic structures of amyloid cross-beta spines reveal varied steric zippers. Nature. 447:453-457.
46. Chan, J. C. C., N. A. Oyler, W. M. Yau, and R. Tycko. 2005. Parallel beta-sheets and polar zippers in amyloid fibrils formed by residues 10-39 of the yeast prion protein Ure2p. Biochemistry. 44:10669-10680.
47. 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.
48. Jao, C. C., A. Der-Sarkissian, J. Chen, and R. Langen. 2004. Structure of membrane-bound alpha-synuclein studied by site-directed spin labeling. Proc. Natl. Acad. Sci. USA. 101:8331-8336.
49. Tsai, H.-H., K. Gunasekaran, and R. Nussinov. 2006. Sequence and structure analysis of parallel beta helices: implication for constructing amyloid structural models. Structure. 14:1059-1072.
50. Ross, E. D., A. Minton, and R. B. Wickner. 2005. Prion domains: sequences, structures and interactions. Nat. Cell Biol. 7:1039-1044.
51. 13C solid-state NMR spectroscopy. Magn. Reson. Chem. 42:247-257.
52. Petty, S. A., and S. M. Decatur. 2005. Intersheet rearrangement of polypeptides during nucleation of beta-sheet aggregates. Proc. Natl. Acad. Sci. USA. 102:14272-14277.
53. Tamburro, A. M., A. Pepe, B. Bochicchio, D. Quaglino, and I. P. Ronchetti. 2005. Supramolecular amyloid-like assembly of the polypeptide sequence coded by exon 30 of human tropoelastin. J. Biol. Chem. 280:2682-2690.
54. Bu, Z., Y. Shi, D. J. E. Callaway, and R. Tycko. 2007. Molecular alignment within beta-sheets in Abeta14-23 fibrils: solid-state NMR experiments and theoretical predictions. Biophys. J. 92:594-602.
55. 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 beta-amyloid fibrils based on experimental constraints from solid state NMR. Proc. Natl. Acad. Sci. USA. 99:16742-16747.
56. Saiki, M., T. Konakahara, and H. Morii. 2006. Interaction-based evaluation of the propensity for amyloid formation with cross-beta structure. Biochem. Biophys. Res. Commun. 343:1262-1271.
57. Han, W., and Y. D. Wu. 2005. A strand-loop-strand structure is a possible intermediate in fibril elongation: long time simulations of amyloid-beta peptide (10-35). J. Am. Chem. Soc. 127:15408-15416.
58. Wei, G., N. Mousseau, and P. Derreumaux. 2004. Sampling the self-assembly pathways of KFFE hexamers. Biophys. J. 87:3648-3656.
59. Makin, O. S., P. Sikorski, and L. C. Serpell. 2006. Diffraction to study protein and peptide assemblies. Curr. Opin. Chem. Biol. 10:417-422.