Investigating the mechanism of peptide aggregation: Insights from mixed monte carlo-molecular dynamics simulations

Biophysical Journal

Volumn 94, Issue 11, 2008, Pages 4414-4426

  Meli, Massimiliano ^a   Morra, Giulia ^a   Colombo, Giorgio ^a  

^a CNR   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

MULTIPROTEIN COMPLEX; PEPTIDE;

ARTICLE; BINDING SITE; CHEMICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER SIMULATION; DIMERIZATION; MONTE CARLO METHOD; PROTEIN BINDING; ULTRASTRUCTURE;

BINDING SITES; COMPUTER SIMULATION; DIMERIZATION; MODELS, CHEMICAL; MODELS, MOLECULAR; MONTE CARLO METHOD; MULTIPROTEIN COMPLEXES; PEPTIDES; PROTEIN BINDING;

EID: 44849096158     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1529/biophysj.107.121061     Document Type: Article

References (63)

1. Chiti, F., and C. M. Dobson. 2006. Protein misfolding, functional amyloid, and human disease. Annu. Rev. Biochem. 75:333-366.
2. Berriman, J., L. C. Serpell, K. A. Oberg, A. L. Fink, M. Goedert, and R. A. Crowther. 2003. Tau filaments from human brain and from in vitro assembly of recombinant protein show cross-β structure. Proc. Natl. Acad. Sci. USA. 100:9034-9038.
3. Serpell, L. C. 2000. Alzheimer's amyloid fibrils: structure and assembly. Biochim. Biophys. Acta. 1502:16-30.
4. Makin, O. S., and L. C. Serpell. 2005. Structures for amyloid fibrils. FEBS J. 272:5950-5961.
5. Lansbury, P. T., and H. A. Lashuel. 2006. A century-old debate on protein aggregation and neurodegeneration enters the clinic. Nature. 443:774-779.
6. Cohen, E., J. Bieschke, R. M. Perciavalle, J. W. Kelly, and A. Dillin. 2006. Opposing activities protect against age-onset proteotoxicity. Science. 313:1604-1610.
7. Jarrett, J. T., and P. T. L. Jr. 1992. Amyloid fibril formation requires a chemically discriminating nucleation event: studies of an amyloido-genic sequence from the bacterial protein OsmB. Biochemistry. 31: 12345-12352.
8. Guijarro, J. I., M. Sunde, J. A. Jones, I. D. Campbell, and C. M. Dobson. 1998. Amyloid fibril formation by an SH3 domain. Proc. Natl. Acad. Sci. USA. 95:4224-4228.
9. Zurdo, J., J. I. Guijarro, and C. M. Dobson. 2001. Preparation and characterization of purified amyloid fibrils. J. Am. Chem. Soc. 123: 8141-8142.
10. Ellis-Behnke, R. G., Y. X. Liang, S. W. You, D. K. Tay, S. Zhang, K. F. So, and G. E. Schneider. 2006. Nano neuro knitting: peptide nanofiber scaffold for brain repair and axon regeneration with functional return of vision. Proc. Natl. Acad. Sci. USA. 103:5054-5059.
11. Smith, J. F., T. P. Knowles, C. M. Dobson, C. E. Macphee, and M. E. Welland. 2006. Characterization of the nanoscale properties of individual amyloid fibrils. Proc. Natl. Acad. Sci. USA. 103:15806-15811.
12. Nilsson, M. R. 2004. Techniques to study amyloid fibril formation in vitro. Methods. 34:151-160.
13. Walsh, D. M., I. Klyubin, J. V. Fadeeva, W. K. Cullen, R. Anwyl, M. S. Wolfe, R. J. Rowan, and D. J. Selkoe. 2002. Naturally secreted oligomers of amyloid βprotein potently inhibit hippocampal long-term potentiation in vivo. Nature. 416:535-539.
14. Colombo, G., P. Soto, and E. Gazit. 2007. Peptide self-assembly at the nanoscale: a challenging target for computational and experimental biotechnology. Trends Biotechnol. 25:211-218.
15. Holmes, T. C., S. de Lacalle, X. Su, G. Liu, A. Rich, and S. Zhang. 2000. Extensive neurite outgrowth and active synapse formation on self-assembling peptide scaffolds. Proc. Natl. Acad. Sci. USA. 97:6728-6733.
16. Silva, G. A., C. Czeisler, K. L. Niece, E. Beniash, D. A. Harrington, J. A. Kessler, andS. I. Stupp. 2004. Selectivedifferentiationofneuralprogenitor cells by high-epitope density nanofibers. Science. 303:1352-1355.
17. Baumketner, A., and J. E. Shea. 2007. The structure of the Alzheimer amyloid β1035 peptide probed through replica-exchange molecular dynamics simulations in explicit solvent. J. Mol. Biol. 366:275-285.
18. Kamiya, N., D. Mitomo, J. E. Shea, and J. Higo. 2007. Folding of the 25 residue Aβ (12-36) peptide in TFE/water: temperature-dependent transition from a funneled free-energy landscape to a rugged one. J. Phys. Chem. B. 111:5351-5356.
19. Daidone, I., F. Simona, D. Roccatano, R. A. Broglia, G. Tiana, G. Colombo, and A. D. Nola. 2004.β-hairpin conformation of fibrillo- genic peptides: structure and α-β transition mechanism revealed by molecular dynamics simulation. Proteins. 57:198-204.
20. Lopez de la Paz, M., G. M. S. de Mori, L. Serrano, and G. Colombo. 2005.Sequence dependence of amyloid fibril formation: insights from molecular dynamics simulations. J. Mol. Biol. 349:583-596.
21. Colombo, G., I. Daidone, E. Gazit, A. Amadei, and A. Di Nola. 2005. Molecular dynamics simulation of the aggregation of the core-recognition motif of the islet amyloid polypeptide in explicit water. Proteins. 59:519-527.
22. Zanuy, D., Y. Porat, E. Gazit, and R. Nussinov. 2004. Peptide sequence, molecular assembly and amyloid formation: molecular simulations and experimental study of a human islet amyloid poly-peptide fragment and its analogues. Structure. 12:439-455.
23. 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.
24. 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.
25. Klimov, D. K., J. E. Straub, and D. Thirumalai. 2004. Aqueous urea solution destabilizes Aβ (16-22) oligomers. Proc. Natl. Acad. Sci. USA. 101:14760-14765.
26. Nguyen,P. H., M. S. Li, G. Stock, J. E. Straub, and D. Thirumalai. 2007. Monomer adds to preformed structured oligomers of A β-peptides by a two-stage dock-lock mechanism. Proc. Natl. Acad. Sci. USA. 104:111-116.
27. Tarus, B., J. E. Straub, and D. Thirumalai. 2005. Probing the initial stage of aggregation of the A β(10-35)-protein: assessing the propensity for peptide dimerization. J. Mol. Biol. 345:1141-1156.
28. 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: met(35) and amyloid β-protein oligomerization. J. Am. Chem. Soc. 125:15359-15365.
29. Thirumalai, D., D. K. Klimov, and R. I. Dima. 2003. Emerging ideas on the molecular basis of protein and peptide aggregation. Curr. Opin. Struct. Biol. 13:146-159.
30. Klimov, D. K., and D. Thirumalai. 2003. Dissecting the assembly of A (16-22) amyloid peptides into antiparallel / sheets. Structure. 11:295-307.
31. Caflisch, A. 2006. Computational models for the prediction of poly-peptide aggregation propensity. Curr. Opin. Chem. Biol. 10:437-444.
32. Cecchini, M., R. Curcio, M. Pappalardo, R. Melki, and A. Caflisch. 2006.A molecular dynamics approach to the structural characterization of amyloid aggregation. J. Mol. Biol. 357:1306-1321.
33. Marchut, A. J., and C. K. Hall. 2007. Effects of chain length on the aggregation of model polyglutamine peptides: molecular dynamics simulations. Proteins. 66:96-109.
34. Dokholyan, N. V. 2006. Studies of folding and misfolding using simplified models. Curr. Opin. Struct. Biol. 16:79-85.
35. Nguyen, H. D., and C. K. Hall. 2004. Molecular dynamics simulations of spontaneous fibril formation by random-coil peptides. Proc. Natl. Acad. Sci. USA. 101:16180-16185.
36. Cecchini, M., F. Rao, M. Seeber, and A. Caflisch. 2004. Replica exchange molecular dynamics simulations of amyloid peptide aggregation. J. Chem. Phys. 121:10748-10756.
37. Baumketner, A., and J. E. Shea. 2006. Folding landscapes of the Alzheimer amyloid-b (12-28) peptide. J. Mol. Biol. 362:567-579.
38. Tsai, H. T., C. 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.
39. Mousseau, N., and P. Derreumaux. 2005. Exploring the early steps of amyloid peptide aggregation by computers. Acc. Chem. Res. 38:885-891.
40. Melquiond, A., J. C. Gelly, N. Mousseau, and P. Derreumaux. 2007. Probing amyloid fibril formation of the NFGAIL peptide by computer simulations. J. Chem. Phys. 126:065101.
41. De Mori, G. M. S., C. Micheletti, and G. Colombo. 2004. All-atom folding simulations of the villin headpiece from stochastically selected coarse-grained structures. J. Phys. Chem. B. 108:12267-12270.
42. De Mori, G. M. S., G. Colombo, and C. Micheletti. 2005. Study of the villin headpiece folding dynamics by combining coarse-grained Monte Carlo evolution and all-atom molecular dynamics. Proteins. 58:459-471.
43. Colombo, G., and C. Micheletti. 2006. Protein folding simulations: combining coarse-grained models and all-atom molecular dynamics. Theor. Chem. Acc. 116:75-86.
44. Esposito, L., C. Pedone, and L. Vitagliano. 2006. Molecular dynamics analyses of cross-β-spine zipper models: β-sheet twisting and aggregation. Proc. Natl. Acad. Sci. USA. 103:11533-11538.
45. Gsponer, J., U. Haberthuer, and A. Caflisch. 2003. The role of side chain interactions in the early steps of aggregation: molecular dynamics simulations of an amyloid-forming peptide from yeast prion Sup35. Proc. Natl. Acad. Sci. USA. 100:5154-5159.
46. Zhang, Z. Q., H. Chen, H. J. Bai, and L. H. Lai. 2007. Molecular dynamics simulations on the oligomer-formation process of the GNNQQNY peptide from yeast prion protein Sup35. Biophys. J. 93:1484-1492.
47. Nelson, R., M. R. Sawaya, M. Balbirnie, A. O. Madsen, C. Riekel, R. Grothe, and D. Eisenberg. 2005. Structure of the cross-β spine of amyloid-like fibrils. Nature. 435:773-778.
48. 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-β spines reveal varied steric zippers. Nature. 447:453-457.
49. Daura, X., K. Gademann, B. Jaun, D. Seebach, W. F. van Gunsteren, and A. E. Mark. 1999. Peptide folding: when simulation meets experiment. Angew. Chemie. Intl. Ed. 38:236-240.
50. Berendsen, H. J. C., J. R. Grigera, and P. R. Straatsma. 1987. The missing term in effective pair potentials. J. Phys. Chem. 91:6269-6271.
51. Hess, B., H. Bekker, J. G. E. M. Fraaije, and H. J. C. Berendsen. 1997. A linear constraint solver for molecular simulations. J. Comput. Chem. 18:1463-1472.
52. Miyamoto, S., and P. A. Kollman. 1992. SETTLE: an analytical version of the SHAKE and RATTLE algorithms for rigid water models. J. Comput. Chem. 13:952-962.
53. Berendsen, H. J. C., J. P. M. Postma, W. F. van Gunsteren, A. Di Nola, and J. R. Haak. 1984. Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81:3684.
54. van der Spoel, D., E. Lindahl, B. Hess, A. R. van Buuren, E. Apol, P. J. Meulenhoff, D. P. Tieleman, A. L. T. M. Sijbers, K. A. Feenstra, R. van Drunen, and H. J. C. Berendsen. 2004. Gromacs User Manual, version 3.2. http://www.gromacs.org/documentation/paper-manuals.php.Accessed April 2008.
55. Scott, W. R. P., P. H. Hunenberger, I. G. Tironi, A. E. Mark, S. R. Billeter, J. Fennen, A. E. Torda, T. Huber, P. Kruger, and W. F. V. Gunsteren. 1999. The GROMOS biomolecular simulation program package. J. Phys. Chem. A. 103:3596-3607.
56. van Gunsteren, W. F., S. R. Billeter, A. A. Eising, P. H. Hunenberger, P. Kruger, A. E. Mark, W. R. P. Scott, and I. G. Tironi. 1996. Biomolecular Simulation: The GROMOS96 Manual and User Guide. vdf Hochschulverlag AG, Zurich, Switzerland.
57. Sambashivan, S., Y. Liu, M. R. Sawaya, M. Gingery, and D. Eisenberg. 2005. Amyloid-like fibrils of ribonuclease A with three dimensional domain-swapped and native like structure. Nature. 437:266-269.
58. Reference deleted in proof.
59. Melquiond, A., N. Mousseau, and P. Derreumaux. 2006. Structures of soluble amyloid oligomers from computer simulations. Proteins. 65: 180-191.
60. Lashuel, H. A., B. M. Petre, J. Wall, M. Simon, R. J. Nowak, T. Walz, and P. T. J. Lansbury. 2002. α-synuclein, especially the Parkinson's disease-associated mutants, forms pore-like annular and tubular proto-fibrils. J. Mol. Biol. 322:1089-1102.
61. Kwan, A. H., R. D. Winefield, M. Sunde, J. M. Matthews, R. G. Haverkamp, M. D. Templeton, and J. P. Mackay. 2006. Structural basis for rodlet assembly in fungal hydrophobins. Proc. Natl. Acad. Sci. USA. 103:3621-3626.
62. Thundimadathil, J., R. W. Roeske, H. Y. Jiang, and L. L. Guo. 2005. Aggregation and porin-like channel activity of a βsheet peptide. Biochemistry. 44:10259-10270.
63. Zheng, J., B. Y. 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.