3D NMR structure of a complex between the amyloid beta peptide (1-40) and the polyphenol ε-viniferin glucoside: Implications in Alzheimer's disease

Biochimica et Biophysica Acta - General Subjects

Volumn 1830, Issue 11, 2013, Pages 5068-5074

  Richard, Tristan ^a   Papastamoulis, Yorgos ^a   Pierre, Waffo Teguo ^a   Monti, Jean Pierre ^a  

^a UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

amyloid peptide; Alzheimer's disease; Interaction; NMR; Polyphenol

Indexed keywords

AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42]; EPSILON VINIFERIN GLUCOSIDE; POLYPHENOL DERIVATIVE; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ARTICLE; CELL PROTECTION; CHEMICAL STRUCTURE; COMPLEX FORMATION; MOLECULAR INTERACTION; MOLECULAR MODEL; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN AGGREGATION;

ALZHEIMER'S DISEASE; INTERACTION; NMR; POLYPHENOL; Β-AMYLOID PEPTIDE;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; BENZOFURANS; BINDING SITES; CELL LINE, TUMOR; GLUCOSIDES; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; PC12 CELLS; PEPTIDE FRAGMENTS; POLYPHENOLS; PROTEIN CONFORMATION; RATS; STILBENES;

EID: 84881539841     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2013.06.031     Document Type: Article

References (69)

1. D.S. Gelmacher, and P.J. Whitehouse Evaluation of dementia N. Engl. J. Med. 335 1996 330 336
2. R. Mayeux, and M. Sano Treatment of Alzheimer's disease N. Engl. J. Med. 341 1999 1670 1679
3. D.J. Selkoe Translating cell biology into therapeutic advances in Alzheimer's disease Nature 399 1999 A23 A31
4. B.A. Yankner Mechanisms of neuronal degeneration in Alzheimer's disease Neuron 16 1996 921 922
5. D.J. Selkoe The cell biology of beta-amyloid precursor protein and presenilin in Alzheimer's disease Trends Cell Biol. 8 1998 447 453
6. L. Dumery, F. Bourdel, Y. Soussan, A. Fialkowsky, S. Viale, P. Nicolas, and M. Reboud-Ravaux Beta-amyloid protein aggregation: its implication in the physiopathology of Alzheimer's disease Pathol. Biol. 49 2001 72 85 (Pubitemid 32174334)
7. D.J. Selkoe Cell biology of protein misfolding: the examples of Alzheimer's and Parkinson's diseases Nat. Cell Biol. 6 2004 1054 1061 (Pubitemid 39468006)
8. J. Naslund, A. Schierhorn, U. Hellman, L. Lannfelt, A.D. Roses, L.O. Tjernberg, J. Silberring, S.E. Gandy, B. Winblad, P. Greengard, C. Nordstedt, and L. Terenius Relative abundance of Alzheimer A beta amyloid peptide variants in Alzheimer disease and normal aging Proc. Natl. Acad. Sci. U. S. A. 91 1994 8378 8382 (Pubitemid 24273667)
9. M.E. Larson, and S.E. Lesne Soluble Aβ oligomer production and toxicity J. Neurochem. 120 2012 125 139 (and references herein)
10. D.M. Walsh, and D.B. Teplow Alzheimer's disease and the amyloid β-protein Prog. Mol. Biol. Transl. Sci. 107 2012 101 124 (and references herein)
11. R. Roychaudhuri, M. Yang, M.M. Hoshi, and D.B. Teplow Amyloid beta-protein assembly and Alzheimer disease J. Biol. Chem. 284 2009 4749 4753
12. P.J. Crouch, S.M. Harding, A.R. White, J. Camakaris, A.I. Bush, and C.L. Masters Mechanisms of A beta mediated neurodegeneration in Alzheimer's disease Int. J. Biochem. Cell Biol. 40 2008 181 198 (Pubitemid 350137874)
13. K.A. Dasilva, J.E. Shaw, and J. McLaurin Amyloid-beta fibrillogenesis: structural insight and therapeutic intervention Exp. Neurol. 223 2010 311 321
14. M. Wogulis, S. Wright, D. Cunningham, T. Chilcote, K. Powell, and R.E. Rydel Nucleation-dependent polymerization is an essential component of amyloid-mediated neuronal cell death J. Neurosci. 25 2005 1071 1080 (Pubitemid 41741352)
15. A. Jan, O. Gokce, R. Luthi-Carter, and H.A. Lashuel The ratio of monomeric to aggregated forms of Abeta40 and Abeta42 is an important determinant of amyloid-beta aggregation, fibrillogenesis, and toxicity J. Biol. Chem. 283 2008 28176 28189
16. B.J. Tabner, O.M. El-Agnaf, S. Turnbull, M.J. German, K.E. Paleologou, Y. Hayashi, L.J. Cooper, N.J. Fullwood, and D. Allsop Hydrogen peroxide is generated during the very early stages of aggregation of the amyloid peptides implicated in Alzheimer disease and familial British dementia J. Biol. Chem. 280 2005 35789 35792 (Pubitemid 41633844)
17. S. Renaud, and M. de Lorgeril Wine, alcohol, platelets, and the French paradox for coronary heart disease Lancet 339 1992 1523 1526
18. G.P. Hubbard, S. Wolffram, J.A. Lovegrove, and J.M. Gibbins The role of polyphenolic compounds in the diet as inhibitors of platelet function Proc. Nutr. Soc. 62 2003 469 478 (Pubitemid 36841622)
19. A. Scalbert, C. Manach, C. Morand, C. Remesy, and L. Jimenez Dietary polyphenols and the prevention of diseases Crit. Rev. Food Sci. Nutr. 45 2005 287 306 (Pubitemid 41657352)
20. C. Manach, A. Scalbert, C. Morand, C. Remesy, and L. Jimenez Polyphenols: food sources and bioavailability Am. J. Clin. Nutr. 79 2004 727 747 (and references herein) (Pubitemid 41103873)
21. A. Ebrahimi, and H. Schluesener Natural polyphenols against neurodegenerative disorders: potentials and pitfalls Ageing Res. Rev. 11 2012 329 345 (and references herein)
22. S.L. Albarracin, B. Stab, Z. Casas, J.J. Sutachan, I. Samudio, J. Gonzalez, L. Gonzalo, F. Capani, L. Morales, and G.E. Barreto Effects of natural antioxidants in neurodegenerative disease Nutr. Neurosci. 15 2012 1 9 (and references herein)
23. H.M. Hügel, and N. Jackson Redox chemistry of green tea polyphenols: therapeutic benefits in neurodegenerative diseases Mini Rev. Med. Chem. 12 2012 380 387 (and references herein)
24. D.Y. Choi, Y.J. Lee, J.T. Hong, and H.J. Lee Antioxidant properties of natural polyphenols and their therapeutic potentials for Alzheimer's disease Brain Res. Bull. 87 2012 144 153 (and references herein)
25. T. Richard, S. Verge, B. Berke, J. Vercauteren, and J.P. Monti NMR and simulated annealing investigations of bradykinin in presence of polyphenols J. Biomol. Struct. Dyn. 18 2001 627 637 (Pubitemid 32164737)
26. A.J. Charlton, E. Haslam, and M.P. Williamson Multiple conformations of the proline-rich protein/epigallocatechin gallate complex determined by time-averaged nuclear Overhauser effects J. Am. Chem. Soc. 124 2002 9899 9905
27. S. Verge, T. Richard, S. Moreau, A. Nurich, J.M. Merillon, J. Vercauteren, and J.P. Monti First observation of solution structures of bradykinin-penta-O-galloyl-d-glucopyranose complexes as determined by NMR and simulated annealing Biochim. Biophys. Acta 1571 2002 89 101 (Pubitemid 34607367)
28. T. Richard, X. Vitrac, J.M. Merillon, and J.P. Monti Role of peptide primary sequence in polyphenol-protein recognition: an example with neurotensin Biochim. Biophys. Acta 1726 2005 238 243 (Pubitemid 41668531)
29. N.J. Murray, M.P. Williamson, T.H. Lilley, and E. Haslam Study of the interaction between salivary proline-rich proteins and a polyphenol by 1H-NMR spectroscopy Eur. J. Biochem. 219 1994 923 935 (Pubitemid 24050962)
30. E. Haslam Polyphenol-protein interactions Biochem. J. 139 1974 285 288
31. T. Richard, J.C. Delaunay, J.M. Merillon, and J.P. Monti Is the C-terminal region of bradykinin the binding site of polyphenols? J. Biomol. Struct. Dyn. 21 2003 379 385 (Pubitemid 37549638)
32. S. Kumar, E.J. Okello, and J.R. Harris Experimental inhibition of fibrillogenesis and neurotoxicity by amyloid-beta (Aβ) and other disease-related peptides/proteins by plant extracts and herbal compounds Subcell. Biochem. 65 2012 295 326
33. S. Sinha, Z. Du, P. Maiti, F.G. Klärner, T. Schrader, C. Wang, and G. Bitan Comparison of three amyloid assembly inhibitors: the sugar scyllo-inositol, the polyphenol epigallocatechin gallate, and the molecular tweezer CLR01 ACS Chem. Neurosci. 3 2012 451 458
34. A.R. Ladiwala, M. Mora-Pale, J.C. Lin, S.S. Bale, Z.S. Fishman, J.S. Dordick, and P.M. Tessier Polyphenolic glycosides and aglycones utilize opposing pathways to selectively remodel and inactivate toxic oligomers of amyloid β Chembiochem 12 2011 1749 1758
35. T. Richard, P. Poupard, M. Nassra, Y. Papastamoulis, M.L. Iglesias, S. Krisa, P. Waffo-Teguo, J.M. Merillon, and J.P. Monti Protective effect of ε-viniferin on β-amyloid peptide aggregation investigated by electrospray ionization mass spectrometry Bioorg. Med. Chem. 19 2011 3152 3155
36. T. Richard, A.D. Pawlus, M.L. Iglesias, E. Pedrot, P. Waffo-Teguo, J.M. Merillon, and J.P. Monti Neuroprotective properties of resveratrol and derivatives Ann. N. Y. Acad. Sci. 1215 2011 103 108
37. C. Riviere, Y. Papastamoulis, P.Y. Fortin, N. Delchier, S. Andriamanarivo, P. Waffo-Teguo, G.D. Kapche, H. Amira-Guebalia, J.C. Delaunay, J.M. Merillon, T. Richard, and J.P. Monti New stilbene dimers against amyloid fibril formation Bioorg. Med. Chem. Lett. 20 2010 3441 3443
38. C. Riviere, J.C. Delaunay, F. Immel, C. Cullin, and J.P. Monti The polyphenol piceid destabilizes preformed amyloid fibrils and oligomers in vitro: hypothesis on possible molecular mechanisms Neurochem. Res. 34 2009 1120 1128
39. C. Riviere, T. Richard, X. Vitrac, J.M. Merillon, J. Valls, and J.P. Monti New polyphenols active on beta-amyloid aggregation Bioorg. Med. Chem. Lett. 18 2008 828 831
40. C. Riviere, T. Richard, L. Quentin, S. Krisa, J.M. Merillon, and J.P. Monti Inhibitory activity of stilbenes on Alzheimer's beta-amyloid fibrils in vitro Bioorg. Med. Chem. 15 2007 1160 1167 (Pubitemid 44880692)
41. K. Ono, Y. Yoshiike, A. Taskashima, K. Hasegawa, H. Naiki, and M. Yamada Potent anti-amyloidogenic and fibril-destabilizing effects of polyphenols in vitro: implications for the prevention and therapeutics of Alzheimer's disease J. Neurochem. 87 2003 172 181 (Pubitemid 37210651)
42. K. Ono, K. Hasegawa, H. Naiki, and M. Yamada Curcumin has potent anti-amyloidogenic effects for Alzheimer's beta-amyloid fibrils in vitro J. Neurosci. Res. 75 2004 742 750 (75) (Pubitemid 38296087)
43. F. Yang, G.P. Lim, A.N. Begum, O.J. Ubeda, M.R. Simmons, S.S. Ambegaokar, P. Chen, R. Kayed, C.G. Glabe, S.A. Frautschy, and G.M. Cole Curcumin inhibits formation of amyloid beta oligomers and fibrils, binds plaques, and reduces amyloid in vivo J. Biol. Chem. 280 2005 5892 5901 (Pubitemid 40280072)
44. A. Klegeris, D.G. Walker, and P.L. McGeer Activation of macrophages by Alzheimer beta amyloid peptide Biochem. Biophys. Res. Commun. 199 1994 984 991 (Pubitemid 24181759)
45. S. Mandel, and M.B. Youdim Catechin polyphenols: neurodegeneration and neuroprotection in neurodegenerative diseases Free Radic. Biol. Med. 37 2004 304 317 (Pubitemid 38833997)
46. J.C. Delaunay, C. Castagnino, C. Chèze, and J. Vercauteren Preparative isolation of polyphenolic compounds from Vitis vinifera by centrifugal partition chromatography J. Chromatogr. A 964 2002 123 128 (Pubitemid 34718009)
47. A.M.S. Duarte, C.P.M. van Mierlo, and M.A. Hemminga Molecular dynamics study of the solvation of an α-helical transmembrane peptide by DMSO J. Phys. Chem. B 112 2008 8664 8671
48. W. Braun, C. Bösch, L.R. Brown, N. Go, and K. Wüthrich Combined use of proton-proton Overhauser enhancements and a distance geometry algorithm for determination of polypeptide conformations. Application to micelle-bound glucagon Biochim. Biophys. Acta 667 1981 377 396
49. R.A. Laskowski, J.A. Rullmannn, M.W. MacArthur, R. Kaptein, and J.M. Thornton AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR J. Biomol. NMR 8 1996 477 486 (Pubitemid 126706801)
50. E. Martz Protein Explorer: easy yet powerful macromolecular visualization Trends Biochem. Sci. 27 2002 107 109 (Pubitemid 34164327)
51. K. Wüthrich NMR of Proteins and Nucleic Acids 1986 Wiley and Sons New-York
52. X. Vitrac, A. Bornet, R. Vanderlinde, J. Valls, T. Richard, J.C. Delaunay, J.M. Merillon, and P.L. Teissedre Determination of stilbenes (delta-viniferin, trans-astringin, trans-piceid, cis- and trans-resveratrol, epsilon-viniferin) in Brazilian wines J. Agric. Food Chem. 53 2005 5664 5669 (Pubitemid 41022461)
53. A.J. Charlton, A.L. Davis, D.P. Jones, J.R. Lewis, A.P. Davies, E. Haslam, and M.P. Williamson The self-association of the black tea polyphenol theaflavin and its complexation with caffeine J. Chem. Soc. Perkin Trans. 2 2000 317 322 (Pubitemid 35166009)
54. M. Coles, W. Bicknell, A.A. Watson, D.P. Fairlie, and D.J. Craik Solution structure of amyloid beta-peptide(1-40) in a water-micelle environment. Is the membrane-spanning domain where we think it is? Biochemistry 37 1998 11064 11077 (Pubitemid 28368933)
55. O. Crescenzi, S. Tomaselli, R. Guerrini, S. Salvadori, A.M. D'Ursi, P.A. Temussi, and D. Picone Solution structure of the Alzheimer amyloid beta-peptide (1-42) in an apolar microenvironment. Similarity with a virus fusion domain Eur. J. Biochem. 269 2002 5642 5648 (Pubitemid 35365553)
56. D.E. Ehrnhoefer, J. Bieschke, A. Boeddrich, M. Herbst, L. Masino, R. Lurz, S. Engemann, A. Pastore, and E.E. Wanker EGCG redirects amyloidogenic polypeptides into unstructured off-pathway oligomers Nat. Struct. Mol. Biol. 15 2008 558 566 (Pubitemid 351799141)
57. F.N. Bazoti, J. Bergquist, K. Markides, and A. Tsarbopoulos Localization of the noncovalent binding site between amyloid-beta-peptide and oleuropein using electrospray ionization FT-ICR mass spectrometry J. Am. Soc. Mass Spectrom. 19 2008 1078 1085
58. P.A. Galanakis, F.N. Bazoti, J. Bergquist, K. Markides, G.A. Spyroulias, and A. Tsarbopoulos Study of the interaction between the amyloid beta peptide (1-40) and antioxidant compounds by nuclear magnetic resonance spectroscopy Biopolymers 96 2011 316 327
59. F.F. Liu, X.Y. Dong, L. He, A.P.J. Middelberg, and Y. Sun Molecular insight into conformational transition of amyloid β-peptide 42 inhibited by (-)-epigallocatechin-3-gallate probed by molecular simulations J. Phys. Chem. B 115 2011 11879 11887
60. T. Richard, D. Lefeuvre, A. Descendit, S. Quideau, and J.P. Monti Recognition characters in peptide-polyphenol complex formation Biochim. Biophys. Acta 1760 2006 951 958 (Pubitemid 43833263)
61. A.T. Petkova, Y. Ishii, J.J. Balbach, O.N. Antzutkin, R.D. Leapman, F. Delaglio, and R. Tycko A structural model for Alzheimer's beta-amyloid fibrils based on experimental constraints from solid state NMR Proc. Natl. Acad. Sci. U. S. A. 99 2002 16742 16747 (Pubitemid 36034043)
62. T. Lührs, C. Ritter, M. Adrian, D. Riek-Loher, B. Bohrmann, H. Döbeli, D. Schubert, and R. Riek 3D structure of Alzheimer's amyloid-beta(1-42) fibrils Proc. Natl. Acad. Sci. U. S. A. 102 2005 17342 17347
63. R. Liu, C. McAllister, Y. Lyubchenko, and M.R. Sierks Residues 17-20 and 30-35 of beta-amyloid play critical roles in aggregation J. Neurosci. Res. 75 2004 162 171 (Pubitemid 38049387)
64. A.P. Pawar, K.F. Dubay, J. Zurdo, F. Chiti, M. Vendruscolo, and C.M. Dobson Prediction of "aggregation-prone" and "aggregation- susceptible" regions in proteins associated with neurodegenerative diseases J. Mol. Biol. 350 2005 379 392 (Pubitemid 40805470)
65. D.G. Smith, R. Cappai, and K.J. Barnham The redox chemistry of the Alzheimer's disease amyloid beta peptide Biochim. Biophys. Acta 1768 2007 1976 1990 (Pubitemid 47125850)
66. C. Hureau, and P. Faller Abeta-mediated ROS production by Cu ions: structural insights, mechanisms and relevance to Alzheimer's disease Biochimie 91 2009 1212 1217
67. C. Schöneich Methionine oxidation by reactive oxygen species: reaction mechanisms and relevance to Alzheimer's disease Biochim. Biophys. Acta 1703 2005 111 119 (Pubitemid 40170434)
68. D.A. Butterfield, and D. Boyd-Kimball The critical role of methionine 35 in Alzheimer's amyloid beta-peptide (1-42)-induced oxidative stress and neurotoxicity Biochim. Biophys. Acta 1703 2005 149 156 (Pubitemid 40170438)
69. M. Pappolla, P. Bozner, C. Soto, H. Shao, N.K. Robakis, M. Zagorski, B. Frangione, and J. Ghiso Inhibition of Alzheimer beta-fibrillogenesis by melatonin J. Biol. Chem. 273 1998 7185 7188