Aβ(16-22) peptides can assemble into ordered β-barrels and bilayer β-sheets, while substitution of phenylalanine 19 by tryptophan increases the population of disordered aggregates

Journal of Physical Chemistry B

Volumn 117, Issue 35, 2013, Pages 10149-10160

  Xie, Luogang ^a   Luo, Yin ^a   Wei, Guanghong ^a  

^a FUDAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC SIDE CHAINS; AROMATIC STACKING INTERACTIONS; COMPUTATIONAL STUDIES; EXPLICIT SOLVENTS; LOW MOLECULAR WEIGHT; OCTAMERIC STRUCTURE; PROBABILITY ANALYSIS; REPLICA EXCHANGE MOLECULAR DYNAMICS;

AMINO ACIDS; CONFORMATIONS; OLIGOMERS; PEPTIDES; PH; SELF ASSEMBLY;

AGGREGATES;

AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN (1 16); AMYLOID BETA PROTEIN (16 22); AMYLOID BETA-PROTEIN (1-16); AMYLOID BETA-PROTEIN (16-22); PEPTIDE FRAGMENT; PHENYLALANINE; TRYPTOPHAN;

AMINO ACID SUBSTITUTION; ARTICLE; CHEMICAL PHENOMENA; CHEMISTRY; GENETICS; METABOLISM; MOLECULAR DYNAMICS; PH; PROTEIN SECONDARY STRUCTURE; TEMPERATURE; THERMODYNAMICS;

AMINO ACID SUBSTITUTION; AMYLOID BETA-PEPTIDES; HYDROGEN-ION CONCENTRATION; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MOLECULAR DYNAMICS SIMULATION; PEPTIDE FRAGMENTS; PHENYLALANINE; PROTEIN STRUCTURE, SECONDARY; TEMPERATURE; THERMODYNAMICS; TRYPTOPHAN;

EID: 84883704686     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp405869a     Document Type: Article

References (61)

1. Serpell, L. C.; Sunde, M.; Benson, M. D.; Tennent, G. A.; Pepys, M. B.; Fraser, P. E. The Protofilament Substructure of Amyloid Fibrils J. Mol. Biol. 2000, 300, 1033-1039
2. 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
3. Petkova, A. T.; Yau, W.-M.; Tycko, R. Experimental Constraints on Quaternary Structure in Alzheimer's β-Amyloid Fibrils Biochemistry 2006, 45, 498-512
4. Grant, M. A.; Lazo, N. D.; Lomakin, A.; Condron, M. M.; Arai, H.; Yamin, G.; Rigby, A. C.; Teplow, D. B. Familial Alzheimer's Disease Mutations Alter the Stability of the Amyloid β-Protein Monomer Folding Nucleus Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 16522-16527
5. Walsh, D. M.; Klyubin, I.; Fadeeva, J. V.; Cullen, W. K.; Anwyl, R.; Wolfe, M. S.; Rowan, M. J.; Selkoe, D. J. Naturally Secreted Oligomers of Amyloid-β Protein Potently Inhibit Hippocampal Long-Term Potentiation in Vivo Nature 2002, 416, 535-539
6. Lesné, S.; Koh, M. T.; Kotilinek, L.; Kayed, R.; Glabe, C. G.; Yang, A.; Gallagher, M.; Ashe, K. H. A Specific Amyloid-β Protein Assembly in the Brain Impairs Memory Nature 2006, 440, 352-357
7. Bitan, G.; Vollers, S. S.; Teplow, D. B. Elucidation of Primary Structure Elements Controlling Early Amyloid β-Protein Oligomerization J. Biol. Chem. 2003, 278, 34882-34889
8. Mastrangelo, I. A.; Ahmed, M.; Sato, T.; Liu, W.; Wang, C.; Hough, P.; Smith, S. O. High-Resolution Atomic Force Microscopy of Soluble Aβ42 Oligomers J. Mol. Biol. 2006, 358, 106-119
9. Pitschke, M.; Prior, R.; Haupt, M.; Riesner, D. Detection of Single Amyloid B-Protein Aggregates in the Cerebrospinal Fluid of Alzheimer's Patients by Fluorescence Correlation Spectroscopy Nat. Med. 1998, 4, 832-834
10. Citron, M.; Diehl, T. S.; Gordon, G.; Biere, A. L.; Seubert, P.; Selkoe, D. J. Evidence That the 42-and 40-Amino Acid Forms of Amyloid B Protein Are Generated from the β-Amyloid Precursor Protein by Different Protease Activities Proc. Natl. Acad. Sci. U.S.A. 1996, 93, 13170-13175
11. Nunan, J.; Small, D. H. Regulation of App Cleavage by α-, β- and γ-Secretases FEBS Lett. 2000, 483, 6-10
12. Balbach, J. J.; Ishii, Y.; Antzutkin, O. N.; Leapman, R. D.; Rizzo, N. W.; Dyda, F.; Reed, J.; Tycko, R. Amyloid Fibril Formation by Aβ16-22, a Seven-Residue Fragment of the Alzheimer's β-Amyloid Peptide, and Structural Characterization by Solid State NMR Biochemistry 2000, 39, 13748-13759
13. Burkoth, T. S.; Benzinger, T. L.; Urban, V.; Morgan, D. M.; Gregory, D. M.; Thiyagarajan, P.; Botto, R. E.; Meredith, S. C.; Lynn, D. G. Structure of the Beta-Amyloid (10-35) Fibril J. Am. Chem. Soc. 2000, 122, 7883-7889
14. Kirschner, D. A.; Inouye, H.; Duffy, L. K.; Sinclair, A.; Lind, M.; Selkoe, D. J. Synthetic Peptide Homologous to Beta Protein from Alzheimer Disease Forms Amyloid-Like Fibrils in Vitro Proc. Natl. Acad. Sci. U.S.A. 1987, 84, 6953-6957
15. Hilbich, C.; Kisters-Woike, B.; Reed, J.; Masters, C. L.; Beyreuther, K. Substitutions of Hydrophobic Amino Acids Reduce the Amyloidogenicity of Alzheimer's Disease βA4 Peptides J. Mol. Biol. 1992, 228, 460-473
16. Lu, K.; Jacob, J.; Thiyagarajan, P.; Conticello, V. P.; Lynn, D. G. Exploiting Amyloid Fibril Lamination for Nanotube Self-Assembly J. Am. Chem. Soc. 2003, 125, 6391-6393
17. Mehta, A. K.; Lu, K.; Childers, W. S.; Liang, Y.; Dublin, S. N.; Dong, J.; Snyder, J. P.; Pingali, S. V.; Thiyagarajan, P.; Lynn, D. G. Facial Symmetry in Protein Self-Assembly J. Am. Chem. Soc. 2008, 130, 9829-9835
18. Tao, K.; Wang, J.; Zhou, P.; Wang, C.; Xu, H.; Zhao, X.; Lu, J. R. Self-Assembly of Short Aβ (16-22) Peptides: Effect of Terminal Capping and the Role of Electrostatic Interaction Langmuir 2011, 27, 2723-2730
19. Klimov, D. K.; Thirumalai, D. Dissecting the Assembly of Aβ(16-22) Amyloid Peptides into Antiparallel B Sheets Structure 2003, 11, 295-307
20. Santini, S.; Wei, G.; Mousseau, N.; Derreumaux, P. Pathway Complexity of Alzheimer's β-Amyloid Aβ(16-22) Peptide Assembly Structure 2004, 12, 1245-1255
21. Favrin, G.; Irbäck, A.; Mohanty, S. Oligomerization of Amyloid Aβ(16-22) Peptides Using Hydrogen Bonds and Hydrophobicity Forces Biophys. J. 2004, 87, 3657-3664
22. Gnanakaran, S.; Nussinov, R.; García, A. E. Atomic-Level Description of Amyloid β-Dimer Formation J. Am. Chem. Soc. 2006, 128, 2158-2159
23. Röhrig, U. F.; Laio, A.; Tantalo, N.; Parrinello, M.; Petronzio, R. Stability and Structure of Oligomers of the Alzheimer Peptide Aβ(16-22): From the Dimer to the 32-Mer Biophys. J. 2006, 91, 3217-3229
24. Nguyen, P. H.; Li, M. S.; Stock, G.; Straub, J. E.; Thirumalai, D. Monomer Adds to Preformed Structured Oligomers of Aβ-Peptides by a Two-Stage Dock-Lock Mechanism Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 111-116
25. Irbäck, A.; Mitternacht, S. Spontaneous B-Barrel Formation: An All-Atom Monte Carlo Study of Aβ16-22 Oligomerization Proteins: Struct., Funct., Bioinf. 2008, 71, 207-214
26. Lu, Y.; Derreumaux, P.; Guo, Z.; Mousseau, N.; Wei, G. Thermodynamics and Dynamics of Amyloid Peptide Oligomerization Are Sequence Dependent Proteins: Struct., Funct., Bioinf. 2008, 75, 954-963
27. Li, H.; Luo, Y.; Derreumaux, P.; Wei, G. Carbon Nanotube Inhibits the Formation of β-Sheet-Rich Oligomers of the Alzheimer's Amyloid-β (16-22) Peptide Biophys. J. 2011, 101, 2267-2276
28. Wei, G.; Mousseau, N.; Derreumaux, P. Sampling the Self-Assembly Pathways of KFFE Hexamers Biophys. J. 2004, 87, 3648-3656
29. Liu, C.; Zhao, M.; Jiang, L.; Cheng, P.-N.; Park, J.; Sawaya, M. R.; Pensalfini, A.; Gou, D.; Berk, A. J.; Glabe, C. G. Out-of-Register B-Sheets Suggest a Pathway to Toxic Amyloid Aggregates Proc. Natl. Acad. Sci. U.S.A. 2012, 109, 20913-20918
30. Lee, M. S.; Salsbury, F. R.; Brooks, C. L. Constant-Ph Molecular Dynamics Using Continuous Titration Coordinates Proteins: Struct., Funct., Bioinf. 2004, 56, 738-752
31. Bürgi, R.; Kollman, P. A.; van Gunsteren, W. F. Simulating Proteins at Constant pH: An Approach Combining Molecular Dynamics and Monte Carlo Simulation Proteins: Struct., Funct., Bioinf. 2002, 47, 469-480
32. Krone, M. G.; Hua, L.; Soto, P.; Zhou, R.; Berne, B.; Shea, J.-E. Role of Water in Mediating the Assembly of Alzheimer Amyloid-β Aβ16-22 Protofilaments J. Am. Chem. Soc. 2008, 130, 11066-11072
33. Nguyen, P. H.; Li, M. S.; Derreumaux, P. Effects of All-Atom Force Fields on Amyloid Oligomerization: Replica Exchange Molecular Dynamics Simulations of the Aβ16-22 Dimer and Trimer Phys. Chem. Chem. Phys. 2011, 13, 9778-9788
34. Berhanu, W. M.; Hansmann, U. H. Side-Chain Hydrophobicity and the Stability of Aβ(16-22) Aggregates Protein Sci. 2012, 21, 1837-1848
35. Berendsen, H.; Postma, J.; Van Gunsteren, W.; Hermans, J. Interaction Models for Water in Relation to Protein Hydration Intermol. Forces 1981, 11, 331-342
36. Sugita, Y.; Okamoto, Y. Replica-Exchange Molecular Dynamics Method for Protein Folding Chem. Phys. Lett. 1999, 314, 141-151
37. Okamoto, Y. Generalized-Ensemble Algorithms: Enhanced Sampling Techniques for Monte Carlo and Molecular Dynamics Simulations J. Mol. Graphics Modell. 2004, 22, 425-439
38. Nadler, W.; Hansmann, U. H. Optimized Explicit-Solvent Replica Exchange Molecular Dynamics from Scratch J. Phys. Chem. B 2008, 112, 10386-10387
39. Lindahl, E.; Hess, B.; Van Der Spoel, D. Gromacs 3.0: A Package for Molecular Simulation and Trajectory Analysis J. Mol. Model. 2001, 7, 306-317
40. Gunsteren, W. F. v.; Billeter, S. R.; Eising, A. A.; Hünenberger, P. H.; Krüger, P.; Mark, A. E.; Scott, W. R.; Tironi, I. G. Biomolecular Simulation: The Gromos96 Manual and User Guide; Vdf Hochschulverland, ETH: Zurich, Switzerland, 1996.
41. Soto, P.; Griffin, M. A.; Shea, J.-E. New Insights into the Mechanism of Alzheimer Amyloid-β Fibrillogenesis Inhibition by N-Methylated Peptides Biophys. J. 2007, 93, 3015-3025
42. Seibert, M. M.; Patriksson, A.; Hess, B.; van der Spoel, D. Reproducible Polypeptide Folding and Structure Prediction Using Molecular Dynamics Simulations J. Mol. Biol. 2005, 354, 173-183
43. Miyamoto, S.; Kollman, P. A. Settle: An Analytical Version of the Shake and Rattle Algorithm for Rigid Water Models J. Comput. Chem. 1992, 13, 952-962
44. Hess, B.; Bekker, H.; Berendsen, H. J.; Fraaije, J. G. Lincs: A Linear Constraint Solver for Molecular Simulations J. Comput. Chem. 1997, 18, 1463-1472
45. Berendsen, H. J.; Postma, J. P. M.; van Gunsteren, W. F.; DiNola, A.; Haak, J. Molecular Dynamics with Coupling to an External Bath J. Chem. Phys. 1984, 81, 3684
46. Kabsch, W.; Sander, C. Dictionary of Protein Secondary Structure: Pattern Recognition of Hydrogen-Bonded and Geometrical Features Biopolymers 1983, 22, 2577-2637
47. Daura, X.; Gademann, K.; Jaun, B.; Seebach, D.; van Gunsteren, W. F.; Mark, A. E. Peptide Folding: When Simulation Meets Experiment Angew. Chem., Int. Ed. 1999, 38, 236-240
48. Murzin, A. G.; Lesk, A. M.; Chothia, C. Principles Determining the Structure of β-Sheet Barrels in Proteins I. A Theoretical Analysis J. Mol. Biol. 1994, 236, 1369-1381
49. Liu, W. Shear Numbers of Protein β-barrels: Definition Refinements and Statistics J. Mol. Biol. 1998, 275, 541-545
50. 2-Microglobulin NHVTLSQ Peptide Using a Coarse-Grained Protein Model Reveals a β-Barrel Species J. Phys. Chem. B 2008, 112, 4410-4418
51. Yoda, T.; Sugita, Y.; Okamoto, Y. Comparisons of Force Fields for Proteins by Generalized-Ensemble Simulations Chem. Phys. Lett. 2004, 386, 460-467
52. Wallace, J. A.; Shen, J. K. Probing the Strand Orientation and Registry Alignment in the Propagation of Amyloid Fibrils Biochemistry 2010, 49, 5290-5298
53. Meinke, J. H.; Hansmann, U. H. Aggregation of β-Amyloid Fragments J. Chem. Phys. 2007, 126, 014706
54. 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
55. Chaudhary, N.; Nagaraj, R. Impact on the Replacement of Phe by Trp in a Short Fragment of Aβ Amyloid Peptide on the Formation of Fibrils J. Pept. Sci. 2011, 17, 115-123
56. Senguen, F. T.; Lee, N. R.; Gu, X.; Ryan, D. M.; Doran, T. M.; Anderson, E. A.; Nilsson, B. L. Probing Aromatic, Hydrophobic, and Steric Effects on the Self-Assembly of an Amyloid-B Fragment Peptide Mol. Biosyst. 2011, 7, 486-496
57. Senguen, F. T.; Doran, T. M.; Anderson, E. A.; Nilsson, B. L. Clarifying the Influence of Core Amino Acid Hydrophobicity, Secondary Structure Propensity, and Molecular Volume on Amyloid-β 16-22 Self-Assembly Mol. Biosyst. 2011, 7, 497-510
58. Armstrong, A. H.; Chen, J.; McKoy, A. F.; Hecht, M. H. Mutations That Replace Aromatic Side Chains Promote Aggregation of the Alzheimer's Aβ Peptide Biochemistry 2011, 50, 4058-4067
59. Laganowsky, A.; Liu, C.; Sawaya, M. R.; Whitelegge, J. P.; Park, J.; Zhao, M.; Pensalfini, A.; Soriaga, A. B.; Landau, M.; Teng, P. K. Atomic View of a Toxic Amyloid Small Oligomer Science 2012, 335, 1228-1231
60. Berhanu, W. M.; Hansmann, U. H. The Stability of Cylindrin β-Barrel Amyloid Oligomer Models-A Molecular Dynamics Study. Proteins: Struct., Funct., Bioinf. 2013, in press
61. 2) Proteins: Struct., Funct., Bioinf. 2010, 78, 2306-2321