Molecular mechanism of the inhibition of EGCG on the Alzheimer Aβ1-42 dimer

Journal of Physical Chemistry B

Volumn 117, Issue 15, 2013, Pages 3993-4002

  Zhang, Tong ^a,c   Zhang, Jian ^b   Derreumaux, Philippe ^c,d   Mu, Yuguang ^a  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^b NANJING UNIVERSITY   (China)

^c France   (France)

^d INSTITUT UNIVERSITAIRE DE FRANCE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DEATH; MASS SPECTROMETRY; MOLECULAR DYNAMICS;

ALZHEIMER'S DISEASE; COLLISION CROSS SECTIONS; CONFORMATIONAL CHANGE; EPIGALLOCATECHIN GALLATE; EQUILIBRIUM STRUCTURES; ION MOBILITY-MASS SPECTROMETRY; REPLICA-EXCHANGE MOLECULAR DYNAMICS SIMULATIONS; SECONDARY STRUCTURES;

DIMERS;

EID: 84876488340     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp312573y     Document Type: Article

References (66)

1. Selkoe, D. J. Folding proteins in fatal ways Nature 2003, 426 (6968) 900-904
2. Dobson, C. M. Protein folding and misfolding Nature 2003, 426 (6968) 884-890
3. Taylor, J. P.; Hardy, J.; Fischbeck, K. H. Biomedicine-Toxic proteins in neurodegenerative disease Science 2002, 296 (5575) 1991-1995
4. Sacchettini, J. C.; Kelly, J. W. Therapeutic strategies for human amyloid diseases Nat. Rev. Drug Discov. 2002, 1 (4) 267-275
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 [beta] protein potently inhibit hippocampal long-term potentiation in vivo Nature 2002, 416 (6880) 535-539
6. Thompson, L. K. Unraveling the secrets of Alzheimer's β-amyloid fibrils Proc. Natl. Acad. Sci. U.S.A. 2003, 100 (2) 383-385
7. Kirkitadze, M. D.; Bitan, G.; Teplow, D. B. Paradigm shifts in Alzheimer's disease and other neuro degenerative disorders: The emerging role of oligomeric assemblies J. Neurosci. Res. 2002, 69 (5) 567-577
8. Klein, W. L.; Stine, W. B.; Teplow, D. B. Small assemblies of unmodified amyloid beta-protein are the proximate neurotoxin in Alzheimer's disease Neurobiol. Aging 2004, 25 (5) 569-580
9. Bernstein, S. L.; Dupuis, N. F.; Lazo, N. D.; Wyttenbach, T.; Condron, M. M.; Bitan, G.; Teplow, D. B.; Shea, J.-E.; Ruotolo, B. T.; Robinson, C. V. Amyloid-β protein oligomerization and the importance of tetramers and dodecamers in the aetiology of Alzheimer's disease Nat. Chem. 2009, 1 (4) 326-331
10. Kirkitadze, M. D.; Condron, M. M.; Teplow, D. B. Identification and characterization of key kinetic intermediates in amyloid β-protein fibrillogenesis J. Mol. Biol. 2001, 312 (5) 1103-1119
11. Ono, K.; Condron, M. M.; Teplow, D. B. Structure-neurotoxicity relationships of amyloid β-protein oligomers Proc. Natl. Acad. Sci. U.S.A. 2009, 106 (35) 14745-14750
12. Urbanc, B.; Cruz, L.; Ding, F.; Sammond, D.; Khare, S.; Buldyrev, S. V.; Stanley, H. E.; Dokholyan, N. V. Molecular Dynamics Simulation of Amyloid 2 Dimer Formation Biophys. J. 2004, 87 (4) 2310-2321
13. Coîté, S.; Laghaei, R.; Derreumaux, P.; Mousseau, N. Distinct Dimerization for Various Alloforms of the Amyloid-Beta Protein: Aβ1-40, Aβ1-42, and Aβ1-40(D23N) J. Phys. Chem. B 2012, 116, 4043-4055
14. Mitternacht, S.; Staneva, I.; Härd, T.; Irbäck, A. Monte Carlo Study of the Formation and Conformational Properties of Dimers of Aβ42 Variants J. Mol. Biol. 2011, 410 (2) 357-367
15. Chong, S.-H.; Ham, S. Atomic-level investigations on the amyloid-[small beta] dimerization process and its driving forces in water Phys. Chem. Chem. Phys. 2012, 14 (5) 1573-1575
16. Zhu, X.; Bora, R. P.; Barman, A.; Singh, R.; Prabhakar, R. Dimerization of the Full-Length Alzheimer Amyloid β-Peptide (Aβ42) in Explicit Aqueous Solution: A Molecular Dynamics Study J. Phys. Chem. B 2012, 116, 4405-4416
17. Barz, B.; Urbanc, B. Dimer Formation Enhances Structural Differences between Amyloid β-Protein (1-40) and (1-42): An Explicit-Solvent Molecular Dynamics Study PLoS ONE 2012, 7 (4) e34345
18. Frydman-Marom, A.; Levin, A.; Farfara, D.; Benromano, T.; Scherzer-Attali, R.; Peled, S.; Vassar, R.; Segal, D.; Gazit, E.; Frenkel, D. Orally Administrated Cinnamon Extract Reduces β-Amyloid Oligomerization and Corrects Cognitive Impairment in Alzheimer's Disease Animal Models PLoS ONE 2011, 6 (1) e16564
19. Chen, J.; Armstrong, A. H.; Koehler, A. N.; Hecht, M. H. Small Molecule Microarrays Enable the Discovery of Compounds That Bind the Alzheimer's Aβ Peptide and Reduce its Cytotoxicity J. Am. Chem. Soc. 2010, 132, 17015-17022
20. Scherzer-Attali, R.; Pellarin, R.; Convertino, M.; Frydman-Marom, A.; Egoz-Matia, N.; Peled, S.; Levy-Sakin, M.; Shalev, D. E.; Caflisch, A.; Gazit, E. Complete Phenotypic Recovery of an Alzheimer's Disease Model by a Quinone-Tryptophan Hybrid Aggregation Inhibitor PLoS ONE 2010, 5 (6) e11101
21. Mishra, R.; Sellin, D.; Radovan, D.; Gohlke, A.; Winter, R. Inhibiting Islet Amyloid Polypeptide Fibril Formation by the Red Wine Compound Resveratrol ChemBioChem 2009, 10 (3) 445-449
22. Ehrnhoefer, D. E.; Bieschke, J.; Boeddrich, A.; Herbst, M.; Masino, L.; Lurz, R.; Engemann, S.; Pastore, A.; Wanker, E. E. EGCG redirects amyloidogenic polypeptides into unstructured, off-pathway oligomers Nat. Struct. Mol. Biol. 2008, 15 (6) 558-566
23. Bieschke, J.; Russ, J.; Friedrich, R. P.; Ehrnhoefer, D. E.; Wobst, H.; Neugebauer, K.; Wanker, E. E. EGCG remodels mature alpha-synuclein and amyloid-beta fibrils and reduces cellular toxicity Proc. Natl. Acad. Sci. U.S.A. 2010, 107 (17) 7710-7715
24. Wang, S.-H.; Liu, F.-F.; Dong, X.-Y.; Sun, Y. Thermodynamic Analysis of the Molecular Interactions between Amyloid β-Peptide 42 and (-)-Epigallocatechin-3-gallate J. Phys. Chem. B 2010, 114, 11576-11583
25. Wang, S.-H.; Dong, X.-Y.; Sun, Y. Thermodynamic Analysis of the Molecular Interactions between Amyloid β-Protein Fragments and (-)-Epigallocatechin- 3-gallate J. Phys. Chem. B 2012, 116, 5803-5809
26. Liu, F.-F.; Dong, X.-Y.; He, L.; Middelberg, A. P. J.; Sun, Y. Molecular Insight into Conformational Transition of Amyloid β-Peptide 42 Inhibited by (-)-Epigallocatechin-3-gallate Probed by Molecular Simulations J. Phys. Chem. B 2011, 115, 11879-11887
27. Coîté, S. b.; Derreumaux, P.; Mousseau, N. Distinct Morphologies for Amyloid Beta Protein Monomer: Aβ1-40, Aβ1-42, and Aβ1-40(D23N) J. Chem. Theory Comput. 2011, 7 (8) 2584-2592
28. Melquiond, A.; Dong, X.; Mousseau, N.; Derreumaux, P. Role of the Region 23-28 in A Fibril Formation: Insights from Simulations of the Monomers and Dimers of Alzheimers Peptides A40 and A42 Curr. Alzheimer Res. 2008, 5 (3) 244-250
29. Wu, C.; Scott, J.; Shea, J.-E. Binding of Congo Red to Amyloid Protofibrils of the Alzheimer Aβ9-40 Peptide Probed by Molecular Dynamics Simulations Biophys. J. 2012, 103 (3) 550-557
30. Zhao, L. N.; Chiu, S.-W.; Benoit, J.; Chew, L. Y.; Mu, Y. The Effect of Curcumin on the Stability of Aβ Dimers J. Phys. Chem. B 2012, 116, 7428-7435
31. Sinha, S.; Lopes, D. H. J.; Du, Z.; Pang, E. S.; Shanmugam, A.; Lomakin, A.; Talbiersky, P.; Tennstaedt, A.; McDaniel, K.; Bakshi, R. Lysine-Specific Molecular Tweezers Are Broad-Spectrum Inhibitors of Assembly and Toxicity of Amyloid Proteins J. Am. Chem. Soc. 2011, 133, 16958-16969
32. Takeda, T.; Chang, W. E.; Raman, E. P.; Klimov, D. K. Binding of nonsteroidal anti-inflammatory drugs to Aβ fibril Proteins: Struct., Funct., Bioinf. 2010, 78 (13) 2849-2860
33. Chebaro, Y.; Jiang, P.; Zang, T.; Mu, Y.; Nguyen, P. H.; Mousseau, N.; Derreumaux, P. Structures of Aβ17-42 Trimers in Isolation and with Five Small-Molecule Drugs Using a Hierarchical Computational Procedure J. Phys. Chem. B 2012, 116, 8412-8422
34. Crescenzi, O.; Tomaselli, S.; Guerrini, R.; Salvadori, S.; D'Ursi, A. M.; Temussi, P. A.; Picone, D. Solution structure of the Alzheimer amyloid β-peptide (1-42) in an apolar microenvironment Eur. J. Biochem. 2002, 269 (22) 5642-5648
35. Jorgensen, W. L.; Tirado-Rives, J. The OPLS [optimized potentials for liquid simulations] potential functions for proteins, energy minimizations for crystals of cyclic peptides and crambin J. Am. Chem. Soc. 1988, 110, 1657-1666
36. Sgourakis, N. G.; Yan, Y.; McCallum, S. A.; Wang, C.; Garcia, A. E. The Alzheimer's Peptides Aβ40 and 42 Adopt Distinct Conformations in Water: A Combined MD/NMR Study J. Mol. Biol. 2007, 368 (5) 1448-1457
37. Nguyen, P. H.; Li, M. S.; Derreumaux, P. Effects of all-atom force fields on amyloid oligomerization: replica exchange molecular dynamics simulations of the A[small beta]16-22 dimer and trimer Phys. Chem. Chem. Phys. 2011, 13 (20) 9778-9788
38. Reddy, G.; Straub, J. E.; Thirumalai, D. Influence of Preformed Asp23-Lys28 Salt Bridge on the Conformational Fluctuations of Monomers and Dimers of Aβ Peptides with Implications for Rates of Fibril Formation J. Phys. Chem. B 2009, 113, 1162-1172
39. Shao, Y.; Molnar, L. F.; Jung, Y.; Kussmann, J.; Ochsenfeld, C.; Brown, S. T.; Gilbert, A. T. B.; Slipchenko, L. V.; Levchenko, S. V.; O'Neill, D. P. Advances in methods and algorithms in a modern quantum chemistry program package Phys. Chem. Chem. Phys. 2006, 8 (27) 3172-3191
40. Frisch, M. J.; Trucks, G. W.; Schlegel, H. B.; Scuseria, G. E.; Robb, M. A.; Cheeseman, J. R.; Scalmani, G.; Barone, V.; Mennucci, B.; Petersson, G. A.; Gaussian 09, Revision B.01; Gaussian Inc.: Wallingford, CT, 2009.
41. Dupradeau, F. Y.; Pigache, A.; Zaffran, T.; Savineau, C.; Lelong, R.; Grivel, N.; Lelong, D.; Rosanski, W.; Cieplak, P. The R.ED. tools: advances in RESP and ESP charge derivation and force field library building Phys. Chem. Chem. Phys. 2010, 12 (28) 7821-7839
42. Hermans, J.; Berendsen, H. J. C.; Vangunsteren, W. F.; Postma, J. P. M. A Consistent Empirical Potential for Water-Protein Interactions Biopolymers 1984, 23 (8) 1513-1518
43. Hu, Z.; Jiang, J. Assessment of biomolecular force fields for molecular dynamics simulations in a protein crystal J. Comput. Chem. 2010, 31 (2) 371-380
44. Van der Spoel, D.; Lindahl, E.; Hess, B.; Groenhof, G.; Mark, A. E.; Berendsen, H. J. C. GROMACS: Fast, flexible, and free J. Comput. Chem. 2005, 26 (16) 1701-1718
45. Hess, B.; Bekker, H.; Berendsen, H. J. C.; Fraaije, J. LINCS: A linear constraint solver for molecular simulations J. Comput. Chem. 1997, 18 (12) 1463-1472
46. Essmann, U.; Perera, L.; Berkowitz, M. L.; Darden, T.; Lee, H.; Pedersen, L. G. A Smooth Particle Mesh Ewald Method J. Chem. Phys. 1995, 103 (19) 8577-8593
47. Hansmann, U. H. E. Parallel tempering algorithm for conformational studies of biological molecules Chem. Phys. Lett. 1997, 281 (1-3) 140-150
48. Sugita, Y.; Okamoto, Y. Replica-exchange molecular dynamics method for protein folding Chem. Phys. Lett. 1999, 314 (1-2) 141-151
49. Patriksson, A.; van der Spoel, D. A temperature predictor for parallel tempering simulations Phys. Chem. Chem. Phys. 2008, 10 (15) 2073-2077
50. Bussi, G.; Donadio, D.; Parrinello, M. Canonical sampling through velocity rescaling J. Chem. Phys. 2007, 126 (1) 014101-7
51. Lerbret, A.; Bordat, P.; Affouard, F.; Hédoux, A.; Guinet, Y.; Descamps, M. How Do Trehalose, Maltose, and Sucrose Influence Some Structural and Dynamical Properties of Lysozyme? Insight from Molecular Dynamics Simulations J. Phys. Chem. B 2007, 111, 9410-9420
52. Kabsch, W.; Sander, C. Dictionary of protein secondary structure: Pattern recognition of hydrogen-bonded and geometrical features Biopolymers 1983, 22 (12) 2577-2637
53. Mu, Y.; Nguyen, P. H.; Stock, G. Energy landscape of a small peptide revealed by dihedral angle principal component analysis Proteins: Struct., Funct., Bioinf. 2005, 58 (1) 45-52
54. Shvartsburg, A. A.; Jarrold, M. F. An exact hard-spheres scattering model for the mobilities of polyatomic ions Chem. Phys. Lett. 1996, 261 (1-2) 86-91
55. Mesleh, M. F.; Hunter, J. M.; Shvartsburg, A. A.; Schatz, G. C.; Jarrold, M. F. Structural Information from Ion Mobility Measurements: Effects of the Long-Range Potential J. Phys. Chem. 1996, 100, 16082-16086
56. Dear, G. J.; Munoz-Muriedas, J.; Beaumont, C.; Roberts, A.; Kirk, J.; Williams, J. P.; Campuzano, I. Sites of metabolic substitution: investigating metabolite structures utilising ion mobility and molecular modelling Rapid Commun. Mass Spectrom. 2010, 24 (21) 3157-3162
57. Schlitter, J. Estimation of absolute and relative entropies of macromolecules using the covariance matrix Chem. Phys. Lett. 1993, 215 (6) 617-621
58. Kollman, P. A.; Massova, I.; Reyes, C.; Kuhn, B.; Huo, S.; Chong, L.; Lee, M.; Lee, T.; Duan, Y.; Wang, W. Calculating Structures and Free Energies of Complex Molecules: Combining Molecular Mechanics and Continuum Models Acc. Chem. Res. 2000, 33, 889-897
59. Case, D. A.; Darden, T. A.; Cheatham, T. E.; Simmerling, C. L.; Wang, J.; Duke, R. E.; Luo, R.; Crowley, M.; Walker, R. C.; Zhang, W.; Amber 10; University of California: San Francisco, 2008.
60. Hou, T. J.; Wang, J. M.; Li, Y. Y.; Wang, W. Assessing the Performance of the MM/PBSA and MM/GBSA Methods. 1. The Accuracy of Binding Free Energy Calculations Based on Molecular Dynamics Simulations J. Chem Inf. Model. 2011, 51 (1) 69-82
61. Sitkoff, D.; Sharp, K. A.; Honig, B. Correlating solvation free energies and surface tensions of hydrocarbon solutes Biophys. Chem. 1994, 51 (2-3) 397-409
62. Gorfe, A. A.; Jelesarov, I. Energetics of Sequence-Specific Protein-DNA Association: Computational Analysis of Integrase Tn916 Binding to Its Target DNA Biochemistry 2003, 42 (40) 11568-11576
63. Urbanc, B.; Betnel, M.; Cruz, L.; Bitan, G.; Teplow, D. B. Elucidation of Amyloid β-Protein Oligomerization Mechanisms: Discrete Molecular Dynamics Study J. Am. Chem. Soc. 2010, 132, 4266-4280
64. Bitan, G.; Kirkitadze, M. D.; Lomakin, A.; Vollers, S. S.; Benedek, G. B.; Teplow, D. B. Amyloid β-protein (Aβ) assembly: Aβ40 and Aβ42 oligomerize through distinct pathways Proc. Natl. Acad. Sci. U.S.A. 2003, 100 (1) 330-335
65. Yang, M.; Teplow, D. B. Amyloid β-Protein Monomer Folding: Free-Energy Surfaces Reveal Alloform-Specific Differences J. Mol. Biol. 2008, 384 (2) 450-464
66. Cao, Z. X.; Liu, L.; Zhao, L. L.; Wang, J. H. Effects of Different Force Fields and Temperatures on the Structural Character of Abeta (12-28) Peptide in Aqueous Solution Int. J. Mol. Sci. 2011, 12 (11) 8259-8274