Atomic-scale simulations confirm that soluble β-sheet-rich peptide self-assemblies provide amyloid mimics presenting similar conformational properties

Biophysical Journal

Volumn 98, Issue 1, 2010, Pages 27-36

  Yu, Xiang ^a   Wang, Jingdai ^c   Yang, Jui Chen ^a   Wang, Qiuming ^a   Cheng, Stephen Z D ^b   Nussinov, Ruth ^d,e   Zheng, Jie ^a  

^a Department of Chemical and Biomolecular Engineering ^*  (United States)

^b The University of Akron   (United States)

^c ZHEJIANG UNIVERSITY   (China)

^d SAIC FREDERICK INC   (United States)

^e TEL AVIV UNIVERSITY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID; AMYLOID BETA PROTEIN; GLYCOPROTEIN; OUTER SURFACE PROTEIN A; PEPTIDE SELF ASSEMBLY MIMIC; UNCLASSIFIED DRUG;

ARTICLE; ATOM; BETA SHEET; HYDROGEN BOND; MOLECULAR DYNAMICS; NOCICEPTION; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN STRUCTURE; SIMULATION;

EID: 74049165050     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2009.10.003     Document Type: Article

References (42)

1. Hill, D. J., M. J. Mio, ..., J. S. Moore. 2001. A field guide to foldamers. Chem. Rev. 101:3893-4012.
2. Alemán, C., D. Zanuy, ..., R. Nussinov. 2006. Concepts and schemes for the re-engineering of physical protein modules: generating nanodevices via targeted replacements with constrained amino acids. Phys. Biol. 3:S54-S62.
3. Schafmeister, C. E., Z. Z. Brown, and S. Gupta. 2008. Shape-programmable macromolecules. Acc. Chem. Res. 41:1387-1398.
4. McCullagh, M., T. Prytkova, ..., G. C. Schatz. 2008. Modeling self-assembly processes driven by nonbonded interactions in soft materials. J. Phys. Chem. B. 112:10388-10398.
5. Makabe, K., M. Biancalana, ..., S. Koide. 2008. High-resolution structure of a self-assembly-competent form of a hydrophobic peptide captured in a soluble β-sheet scaffold. J. Mol. Biol. 378:459-467.
6. Dobson, C. M. 2004. Experimental investigation of protein folding and misfolding. Methods. 34:4-14.
7. Lamour, Y. 1994. Alzheimer's disease: a review of recent findings. Biomed. Pharmacother. 48:312-318.
8. Lashuel, H. A., and P. T. Lansbury, Jr. 2006. Are amyloid diseases caused by protein aggregates that mimic bacterial pore-forming toxins? Q. Rev. Biophys. 39:167-201.
9. Selkoe, D. J. 2001. Alzheimer's disease: genes, proteins, and therapy. Physiol. Rev. 81:741-766.
10. Makabe, K., D. McElheny, ..., S. Koide. 2006. Atomic structures of peptide self-assembly mimics. Proc. Natl. Acad. Sci. USA. 103:17753-17758.
11. Benseny-Cases, N., M. Cócera, and J. Cladera. 2007. Conversion of non-fibrillar β-sheet oligomers into amyloid fibrils in Alzheimer's disease amyloid peptide aggregation. Biochem. Biophys. Res. Commun. 361:916-921.
12. Fändrich, M., G. Zandomeneghi, ..., S. Diekmann. 2006. Apomyoglobin reveals a random-nucleation mechanism in amyloid protofibril formation. Acta Histochem. 108:215-219.
13. Guo, Z., and D. Eisenberg. 2008. The structure of a fibril-forming sequence, NNQQNY, in the context of a globular fold. Protein Sci. 17:1617-1623.
14. Takano, K., S. Endo, ..., S. Kanaya. 2006. Structure of amyloid β fragments in aqueous environments. FEBS J. 273:150-158.
15. Stott, K., J. M. Blackburn, ..., M. Perutz. 1995. Incorporation of glutamine repeats makes protein oligomerize: implications for neurodegenerative diseases. Proc. Natl. Acad. Sci. USA. 92:6509-6513.
16. Hosia, W., N. Bark, ..., L. Tjernberg. 2004. Folding into a β-hairpin can prevent amyloid fibril formation. Biochemistry. 43:4655-4661.
17. Nelson, R., M. R. Sawaya, ..., D. Eisenberg. 2005. Structure of the cross-β spine of amyloid-like fibrils. Nature. 435:773-778.
18. Esposito, L., C. Pedone, and L. Vitagliano. 2006. Molecular dynamics analyses of cross-β-spine steric zipper models: β-sheet twisting and aggregation. Proc. Natl. Acad. Sci. USA. 103:11533-11538.
19. Zheng, J., B. Ma, ..., R. Nussinov. 2006. Structural stability and dynamics of an amyloid-forming peptide GNNQQNY from the yeast prion sup-35. Biophys. J. 91:824-833.
20. Wang, J., C. Tan, ..., R. Luo. 2008. All-atom computer simulations of amyloid fibrils disaggregation. Biophys. J. 95:5037-5047.
21. Biancalana, M., K. Makabe, ..., S. Koide. 2008. Aromatic cross-strand ladders control the structure and stability of β-rich peptide self-assembly mimics. J. Mol. Biol. 383:205-213.
22. Zheng, J., H. Jang, ..., R. Nussinov. 2007. Modeling the Alzheimer Aβ 17-42 fibril architecture: tight intermolecular sheet-sheet association and intramolecular hydrated cavities. Biophys. J. 93:3046-3057.
23. Zheng, J., H. Jang, .., R. Nussinov. 2008. Annular structures as intermediates in fibril formation of Alzheimer Aβ 17-42. J. Phys. Chem. B. 112:6856-6865.
24. Zheng, J., B. Ma, ..., R. Nussinov. 2008. Molecular dynamics simulations of Alzheimer Aβ40 elongation and lateral association. Front. Biosci. 13:3919-3930.
25. Zheng, J., H. Jang, and R. Nussinov. 2008. β2-microglobulin amyloid fragment organization and morphology and its comparison to Aβ suggests that amyloid aggregation pathways are sequence specific. Biochemistry. 47:2497-2509.
26. Kabsch, W., and C. Sander. 1983. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers. 22:2577-2637.
27. Im, W., M. S. Lee, and C. L. Brooks, 3rd. 2003. Generalized Born model with a simple smoothing function. J. Comput. Chem. 24:1691-1702.
28. Takeda, T., and D. K. Klimov. 2009. Replica exchange simulations of the thermodynamics of Aβ fibril growth. Biophys. J. 96:442-452.
29. Chebaro, Y., N. Mousseau, and P. Derreumaux. 2009. Structures and thermodynamics of Alzheimer's amyloid-β Aβ (16-35) monomer and dimer by replica exchange molecular dynamics simulations: implication for full-length Aβ fibrillation. J. Phys. Chem. B. 113:7668-7675.
30. Periole, X., A. Rampioni, ..., A. E. Mark. 2009. Factors that affect the degree of twist in β-sheet structures: a molecular dynamics simulation study of a cross-β filament of the GNNQQNY peptide. J. Phys. Chem. B. 113:1728-1737.
31. Berryman, J. T., S. E. Radford, and S. A. Harris. 2009. Thermodynamic description of polymorphism in Q- and N-rich peptide aggregates revealed by atomistic simulation. Biophys. J. 97:1-11.
32. Bu, Z., Y. Shi, ..., R. Tycko. 2007. Molecular alignment within β-sheets in Aβ (14-23) fibrils: solid-state NMR experiments and theoretical predictions. Biophys. J. 92:594-602.
33. Wei, G., N. Mousseau, and P. Derreumaux. 2004. Sampling the self-assembly pathways of KFFE hexamers. Biophys. J. 87:3648-3656.
34. Bellesia, G., and J.-E. Shea. 2009. What determines the structure and stability of KFFE monomers, dimers, and protofibrils? Biophys. J. 96:875-886.
35. Zheng, J., B. Ma, and R. Nussinov. 2006. Consensus features in amyloid fibrils: sheet-sheet recognition via a (polar or nonpolar) zipper structure. Phys. Biol. 3:P1-P4.
36. Tsai, H.-H., K. Gunasekaran, and R. Nussinov. 2006. Sequence and structure analysis of parallel β helices: implication for constructing amyloid structural models. Structure. 14:1059-1072.
37. Ferguson, N., J. Becker, ..., A. R. Fersht. 2006. General structural motifs of amyloid protofilaments. Proc. Natl. Acad. Sci. USA. 103:16248-16253.
38. Iwata, K., T. Fujiwara, ..., Y. Goto. 2006. 3D structure of amyloid protofilaments of β2-microglobulin fragment probed by solid-state NMR. Proc. Natl. Acad. Sci. USA. 103:18119-18124.
39. Sasahara, K., H. Yagi, ..., Y. Goto. 2007. Heat-triggered conversion of protofibrils into mature amyloid fibrils of β2-microglobulin. Biochemistry. 46:3286-3293.
40. Naito, A., and I. Kawamura. 2007. Solid-state NMR as a method to reveal structure and membrane-interaction of amyloidogenic proteins and peptides. Biochim. Biophys. Acta. 1768:1900-1912.
41. Ma, B., and R. Nussinov. 2002. Stabilities and conformations of Alzheimer's β-amyloid peptide oligomers (Aβ 16-22, Aβ 16-35, and Aβ 10-35): sequence effects. Proc. Natl. Acad. Sci. USA. 99:14126-14131.
42. Petkova, A. T., W. M. Yau, and R. Tycko. 2006. Experimental constraints on quaternary structure in Alzheimer's β-amyloid fibrils. Biochemistry. 45:498-512.