Anti-amyloid Aggregation Activity of Natural Compounds: Implications for Alzheimer’s Drug Discovery

Molecular Neurobiology

Volumn 53, Issue 6, 2016, Pages 3565-3575

  Bu, Xian Le ^a   Rao, Praveen P N ^b   Wang, Yan Jiang ^a  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

^b UNIVERSITY OF WATERLOO   (Canada)

Author keywords

Alzheimer s disease; Beta amyloid; Molecular docking; Natural compounds; Pharmacophore modeling

Indexed keywords

AMYLOID; CATECHOL; CURCUMIN; EPIGALLOCATECHIN GALLATE; EXTRA VIRGIN OLIVE OIL; FLAVONOID; ISOLIQUIRITIGENIN; NATURAL PRODUCT; NORDIHYDROGUAIARETIC ACID; RESVERATROL; ROSMARINIC ACID; AMYLOID BETA PROTEIN; BIOLOGICAL PRODUCT;

ALZHEIMER DISEASE; BINDING AFFINITY; BLOOD BRAIN BARRIER; HYDROGEN BOND; METABOLIC STABILITY; MOLECULAR INTERACTION; NEUROTOXICITY; PHYSICAL CHEMISTRY; PROTEIN AGGREGATION; PROTEIN MOTIF; REVIEW; STRUCTURE ANALYSIS; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOLOGY; DRUG DEVELOPMENT; HUMAN; METABOLISM; PATHOLOGY; PROTEINOSIS;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; BIOLOGICAL PRODUCTS; COMPUTATIONAL BIOLOGY; DRUG DISCOVERY; HUMANS; PROTEIN AGGREGATION, PATHOLOGICAL;

EID: 84932139581     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-015-9301-4     Document Type: Review

References (119)

1. Wang YJ, Zhou HD, Zhou XF (2006) Clearance of amyloid-beta in Alzheimer's disease: progress, problems and perspectives. Drug Discov Today 11(19-20):931–8
2. Serrano-Pozo A et al (2011) Neuropathological alterations in Alzheimer disease. Cold Spring Harb Perspect Med 1(1):a006189
3. Hardy J, Selkoe DJ (2002) The amyloid hypothesis of Alzheimer’s disease: progress and problems on the road to therapeutics. Science 297(5580):353–6
4. Liu YH et al (2012) Immunotherapy for Alzheimer disease: the challenge of adverse effects. Nat Rev Neurol 8(8):465–9
5. Ehrnhoefer DE et al (2008) EGCG redirects amyloidogenic polypeptides into unstructured, off-pathway oligomers. Nat Struct Mol Biol 15(6):558–66
6. Liu KN et al (2012) Curcumin’s pre-incubation temperature affects its inhibitory potency toward amyloid fibrillation and fibril-induced cytotoxicity of lysozyme. Biochim Biophys Acta 1820(11):1774–86
7. Ladiwala AR et al (2010) Resveratrol selectively remodels soluble oligomers and fibrils of amyloid Abeta into off-pathway conformers. J Biol Chem 285(31):24228–37
8. Sinha S et al (2012) Comparison of three amyloid assembly inhibitors: the sugar scyllo-inositol, the polyphenol epigallocatechin gallate, and the molecular tweezer CLR01. ACS Chem Neurosci 3(6):451–8
9. Jonsson T et al (2012) A mutation in APP protects against Alzheimer’s disease and age-related cognitive decline. Nature 488(7409):96–9
10. Wong PC et al (2002) Genetically engineered mouse models of neurodegenerative diseases. Nat Neurosci 5(7):633–9
11. Suzuki N et al (1994) An increased percentage of long amyloid beta protein secreted by familial amyloid beta protein precursor (beta APP717) mutants. Science 264(5163):1336–40
12. Kuperstein I et al (2010) Neurotoxicity of Alzheimer’s disease Abeta peptides is induced by small changes in the Abeta42 to Abeta40 ratio. EMBO J 29(19):3408–20
13. Walsh DM, Selkoe DJ (2004) Oligomers on the brain: the emerging role of soluble protein aggregates in neurodegeneration. Protein Pept Lett 11(3):213–28
14. Crouch PJ et al (2005) Copper-dependent inhibition of human cytochrome c oxidase by a dimeric conformer of amyloid-beta1-42. J Neurosci 25(3):672–9
15. Shankar GM et al (2008) Amyloid-beta protein dimers isolated directly from Alzheimer’s brains impair synaptic plasticity and memory. Nat Med 14(8):837–42
16. Pierrot N et al (2004) Intraneuronal amyloid-beta1-42 production triggered by sustained increase of cytosolic calcium concentration induces neuronal death. J Neurochem 88(5):1140–50
17. Golde TE, Janus C (2005) Homing in on intracellular Abeta? Neuron 45(5):639–42
18. Levi O et al (2007) Intraneuronal amyloid-beta plays a role in mediating the synergistic pathological effects of apoE4 and environmental stimulation. J Neurochem 103(3):1031–40
19. Lesne S et al (2006) A specific amyloid-beta protein assembly in the brain impairs memory. Nature 440(7082):352–7
20. Zou K et al (2002) A novel function of monomeric amyloid beta-protein serving as an antioxidant molecule against metal-induced oxidative damage. J Neurosci 22(12):4833–41
21. Gilbert BJ (2013) The role of amyloid beta in the pathogenesis of Alzheimer’s disease. J Clin Pathol 66(5):362–6
22. Walsh DM, Selkoe DJ (2007) A beta oligomers—a decade of discovery. J Neurochem 101(5):1172–84
23. Danielsson J et al (2005) The Alzheimer beta-peptide shows temperature-dependent transitions between left-handed 3-helix, beta-strand and random coil secondary structures. FEBS J 272(15):3938–49
24. Yang DS et al (1999) Manipulating the amyloid-beta aggregation pathway with chemical chaperones. J Biol Chem 274(46):32970–4
25. Serpell LC et al (2000) Fiber diffraction of synthetic alpha-synuclein filaments shows amyloid-like cross-beta conformation. Proc Natl Acad Sci U S A 97(9):4897–902
26. Rochet JC, Lansbury PT Jr (2000) Amyloid fibrillogenesis: themes and variations. Curr Opin Struct Biol 10(1):60–8
27. Wetzel R (2006) Kinetics and thermodynamics of amyloid fibril assembly. Acc Chem Res 39(9):671–9
28. Glabe CG (2008) Structural classification of toxic amyloid oligomers. J Biol Chem 283(44):29639–43
29. Ono K, Condron MM, Teplow DB (2009) Structure-neurotoxicity relationships of amyloid beta-protein oligomers. Proc Natl Acad Sci U S A 106(35):14745–50
30. Necula M et al (2007) Small molecule inhibitors of aggregation indicate that amyloid beta oligomerization and fibrillization pathways are independent and distinct. J Biol Chem 282(14):10311–24
31. Butterfield S et al (2012) Chemical strategies for controlling protein folding and elucidating the molecular mechanisms of amyloid formation and toxicity. J Mol Biol 421(2-3):204–36
32. Wang SS, Chen YT, Chou SW (2005) Inhibition of amyloid fibril formation of beta-amyloid peptides via the amphiphilic surfactants. Biochim Biophys Acta 1741(3):307–13
33. Yang C et al (2010) Exploration of the mechanism for LPFFD inhibiting the formation of beta-sheet conformation of A beta(1-42) in water. J Mol Model 16(4):813–21
34. Lazo ND et al (2005) On the nucleation of amyloid beta-protein monomer folding. Protein Sci 14(6):1581–96
35. Xu Y et al (2005) Conformational transition of amyloid beta-peptide. Proc Natl Acad Sci U S A 102(15):5403–7
36. Gazit E (2002) A possible role for pi-stacking in the self-assembly of amyloid fibrils. FASEB J 16(1):77–83
37. Gazit E (2002) Mechanistic studies of the process of amyloid fibrils formation by the use of peptide fragments and analogues: implications for the design of fibrillization inhibitors. Curr Med Chem 9(19):1725–35
38. Gazit E (2002) Global analysis of tandem aromatic octapeptide repeats: the significance of the aromatic-glycine motif. Bioinformatics 18(6):880–3
39. Sarasa M, Pesini P (2009) Natural non-transgenic animal models for research in Alzheimer’s disease. Curr Alzheimer Res 6(2):171–8
40. Dai X et al (2012) Abeta-40 Y10F increases betafibrils formation but attenuates the neurotoxicity of amyloid-beta peptide. Int J Mol Sci 13(5):5324–37
41. Barnham KJ et al (2004) Tyrosine gated electron transfer is key to the toxic mechanism of Alzheimer’s disease beta-amyloid. FASEB J 18(12):1427–9
42. Yang DS et al (2000) Examining the zinc binding site of the amyloid-beta peptide. Eur J Biochem 267(22):6692–8
43. Schoneich C (2005) Methionine oxidation by reactive oxygen species: reaction mechanisms and relevance to Alzheimer’s disease. Biochim Biophys Acta 1703(2):111–9
44. Pepeu G, Giovannini MG (2009) Cholinesterase inhibitors and beyond. Curr Alzheimer Res 6(2):86–96
45. Bush AI (2008) Drug development based on the metals hypothesis of Alzheimer’s disease. J Alzheimers Dis 15(2):223–40
46. Tougu V et al (2009) Zn(II)- and Cu(II)-induced non-fibrillar aggregates of amyloid-beta (1-42) peptide are transformed to amyloid fibrils, both spontaneously and under the influence of metal chelators. J Neurochem 110(6):1784–95
47. Sharma AK et al (2013) The effect of Cu and Zn on the Abeta peptide aggregation and cellular toxicity. Metallomics 5(11):1529–36
48. Smith DG, Cappai R, Barnham KJ (2007) The redox chemistry of the Alzheimer’s disease amyloid beta peptide. Biochim Biophys Acta 1768(8):1976–90
49. Tickler AK et al (2005) Methylation of the imidazole side chains of the Alzheimer disease amyloid-beta peptide results in abolition of superoxide dismutase-like structures and inhibition of neurotoxicity. J Biol Chem 280(14):13355–63
50. Cheng B et al (2013) Inhibiting toxic aggregation of amyloidogenic proteins: a therapeutic strategy for protein misfolding diseases. Biochim Biophys Acta 1830(10):4860–71
51. Jayasena T et al (2013) The role of polyphenols in the modulation of sirtuins and other pathways involved in Alzheimer’s disease. Ageing Res Rev 12(4):867–883
52. Ono K et al (2003) Potent anti-amyloidogenic and fibril-destabilizing effects of polyphenols in vitro: implications for the prevention and therapeutics of Alzheimer’s disease. J Neurochem 87(1):172–81
53. Rezai-Zadeh K et al (2005) Green tea epigallocatechin-3-gallate (EGCG) modulates amyloid precursor protein cleavage and reduces cerebral amyloidosis in Alzheimer transgenic mice. J Neurosci 25(38):8807–14
54. Lopez del Amo JM et al (2012) Structural properties of EGCG-induced, nontoxic Alzheimer’s disease Abeta oligomers. J Mol Biol 421(4-5):517–24
55. Bieschke J et al (2010) EGCG remodels mature alpha-synuclein and amyloid-beta fibrils and reduces cellular toxicity. Proc Natl Acad Sci U S A 107(17):7710–5
56. Liu FF et al (2011) Molecular insight into conformational transition of amyloid beta-peptide 42 inhibited by (-)-epigallocatechin-3-gallate probed by molecular simulations. J Phys Chem B 115(41):11879–87
57. Palhano FL et al (2013) Toward the molecular mechanism(s) by which EGCG treatment remodels mature amyloid fibrils. J Am Chem Soc 135(20):7503–10
58. Lim GP et al (2001) The curry spice curcumin reduces oxidative damage and amyloid pathology in an Alzheimer transgenic mouse. J Neurosci 21(21):8370–7
59. Yanagisawa D et al (2011) Curcuminoid binds to amyloid-beta1-42 oligomer and fibril. J Alzheimers Dis 24(Suppl 2):33–42
60. Hamaguchi T et al (2009) Phenolic compounds prevent Alzheimer’s pathology through different effects on the amyloid-beta aggregation pathway. Am J Pathol 175(6):2557–65
61. Caesar I et al (2012) Curcumin promotes A-beta fibrillation and reduces neurotoxicity in transgenic Drosophila. PLoS One 7(2):e31424
62. Zhao LN et al (2012) The effect of curcumin on the stability of Abeta dimers. J Phys Chem B 116(25):7428–35
63. Baum L, Ng A (2004) Curcumin interaction with copper and iron suggests one possible mechanism of action in Alzheimer’s disease animal models. J Alzheimers Dis 6(4):367–77, 443-9
64. Sato T et al (2006) Inhibitors of amyloid toxicity based on beta-sheet packing of Abeta40 and Abeta42. Biochemistry 45(17):5503–16
65. Balasubramanian K (2006) Molecular orbital basis for yellow curry spice curcumin’s prevention of Alzheimer’s disease. J Agric Food Chem 54(10):3512–20
66. Masuda Y et al (2011) Solid-state NMR analysis of interaction sites of curcumin and 42-residue amyloid beta-protein fibrils. Bioorg Med Chem 19(20):5967–74
67. Orlando RA et al (2012) A chemical analog of curcumin as an improved inhibitor of amyloid Abeta oligomerization. PLoS One 7(3):e31869
68. Streltsov VA et al (2008) The structure of the amyloid-beta peptide high-affinity copper II binding site in Alzheimer disease. Biophys J 95(7):3447–56
69. Lu Y et al (2010) Copper(I) and copper(II) binding to beta-amyloid 16 (Abeta16) studied by electrospray ionization mass spectrometry. Metallomics 2(7):474–9
70. Zhang X et al (2013) Design and synthesis of curcumin analogues for in vivo fluorescence imaging and inhibiting copper-induced cross-linking of amyloid beta species in Alzheimer’s disease. J Am Chem Soc 135(44):16397–409
71. Baur JA, Sinclair DA (2006) Therapeutic potential of resveratrol: the in vivo evidence. Nat Rev Drug Discov 5(6):493–506
72. Huang TC et al (2011) Resveratrol protects rats from Abeta-induced neurotoxicity by the reduction of iNOS expression and lipid peroxidation. PLoS One 6(12):e29102
73. Jeon SY et al (2007) Beta-secretase (BACE1)-inhibiting stilbenoids from Smilax Rhizoma. Phytomedicine 14(6):403–8
74. Marambaud P, Zhao H, Davies P (2005) Resveratrol promotes clearance of Alzheimer’s disease amyloid-beta peptides. J Biol Chem 280(45):37377–82
75. Vingtdeux V et al (2010) AMP-activated protein kinase signaling activation by resveratrol modulates amyloid-beta peptide metabolism. J Biol Chem 285(12):9100–13
76. Chen J et al (2005) SIRT1 protects against microglia-dependent amyloid-beta toxicity through inhibiting NF-kappaB signaling. J Biol Chem 280(48):40364–74
77. Ge JF et al (2012) The binding of resveratrol to monomer and fibril amyloid beta. Neurochem Int 61(7):1192–201
78. Feng Y et al (2009) Resveratrol inhibits beta-amyloid oligomeric cytotoxicity but does not prevent oligomer formation. Neurotoxicology 30(6):986–95
79. Lu C et al (2013) Design, synthesis, and evaluation of multitarget-directed resveratrol derivatives for the treatment of Alzheimer’s disease. J Med Chem 56(14):5843–5859
80. Ladiwala AR et al (2011) Polyphenolic glycosides and aglycones utilize opposing pathways to selectively remodel and inactivate toxic oligomers of amyloid beta. Chembiochem 12(11):1749–58
81. Ansari MA et al (2009) Protective effect of quercetin in primary neurons against Abeta(1-42): relevance to Alzheimer’s disease. J Nutr Biochem 20(4):269–75
82. Pocernich CB et al (2011) Nutritional approaches to modulate oxidative stress in Alzheimer’s disease. Curr Alzheimer Res 8(5):452–69
83. Lu J et al (2010) Quercetin activates AMP-activated protein kinase by reducing PP2C expression protecting old mouse brain against high cholesterol-induced neurotoxicity. J Pathol 222(2):199–212
84. Shimmyo Y et al (2008) Flavonols and flavones as BACE-1 inhibitors: structure-activity relationship in cell-free, cell-based and in silico studies reveal novel pharmacophore features. Biochim Biophys Acta 1780(5):819–25
85. Kim H et al (2005) Effects of naturally occurring compounds on fibril formation and oxidative stress of beta-amyloid. J Agric Food Chem 53(22):8537–41
86. Shimmyo Y et al (2008) Multifunction of myricetin on A beta: neuroprotection via a conformational change of A beta and reduction of A beta via the interference of secretases. J Neurosci Res 86(2):368–77
87. Akaishi T et al (2008) Structural requirements for the flavonoid fisetin in inhibiting fibril formation of amyloid beta protein. Neurosci Lett 444(3):280–5
88. Bartolini M et al (2011) Kinetic characterization of amyloid-beta 1-42 aggregation with a multimethodological approach. Anal Biochem 414(2):215–25
89. Berhanu WM, Masunov AE (2010) Natural polyphenols as inhibitors of amyloid aggregation. Molecular dynamics study of GNNQQNY heptapeptide decamer. Biophys Chem 149(1-2):12–21
90. Tay WM, da Silva GF, Ming LJ (2013) Metal binding of flavonoids and their distinct inhibition mechanisms toward the oxidation activity of Cu2+-beta-amyloid: not just serving as suicide antioxidants! Inorg Chem 52(2):679–90
91. DeToma AS et al (2011) Myricetin: a naturally occurring regulator of metal-induced amyloid-beta aggregation and neurotoxicity. ChemBioChem 12(8):1198–201
92. Fiori J et al (2012) Disclosure of a fundamental clue for the elucidation of the myricetin mechanism of action as amyloid aggregation inhibitor by mass spectrometry. Electrophoresis 33(22):3380–6
93. Lu JH et al (2011) Baicalein inhibits formation of alpha-synuclein oligomers within living cells and prevents Abeta peptide fibrillation and oligomerisation. ChemBioChem 12(4):615–24
94. Lemkul JA, Bevan DR (2010) Destabilizing Alzheimer’s Abeta(42) protofibrils with morin: mechanistic insights from molecular dynamics simulations. Biochemistry 49(18):3935–46
95. Zhao L et al (2013) Apigenin attenuates copper-mediated beta-amyloid neurotoxicity through antioxidation, mitochondrion protection and MAPK signal inactivation in an AD cell model. Brain Res 1492:33–45
96. Pitozzi V et al (2012) Long-term dietary extra-virgin olive oil rich in polyphenols reverses age-related dysfunctions in motor coordination and contextual memory in mice: role of oxidative stress. Rejuvenation Res 15(6):601–12
97. Farr SA et al (2012) Extra virgin olive oil improves learning and memory in SAMP8 mice. J Alzheimers Dis 28(1):81–92
98. Berr C et al (2009) Olive oil and cognition: results from the three-city study. Dement Geriatr Cogn Disord 28(4):357–64
99. Bazoti FN et al (2006) Noncovalent interaction between amyloid-beta-peptide (1-40) and oleuropein studied by electrospray ionization mass spectrometry. J Am Soc Mass Spectrom 17(4):568–75
100. Bazoti FN et al (2008) 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(8):1078–85
101. Galanakis PA et al (2011) Study of the interaction between the amyloid beta peptide (1-40) and antioxidant compounds by nuclear magnetic resonance spectroscopy. Biopolymers 96(3):316–27
102. Diomede L et al (2013) Oleuropein aglycone protects transgenic C. elegans strains expressing Abeta42 by reducing plaque load and motor deficit. PLoS One 8(3):e58893
103. Grossi C et al (2013) The polyphenol oleuropein aglycone protects TgCRND8 mice against ass plaque pathology. PLoS One 8(8):e71702
104. Chen YP et al (2013) Syntheses and evaluation of novel isoliquiritigenin derivatives as potential dual inhibitors for amyloid-beta aggregation and 5-lipoxygenase. Eur J Med Chem 66:22–31
105. Tarozzi A et al (2010) Neuroprotective effects of cyanidin 3-O-glucopyranoside on amyloid beta (25-35) oligomer-induced toxicity. Neurosci Lett 473(2):72–6
106. Ono K et al (2004) Anti-amyloidogenic activity of tannic acid and its activity to destabilize Alzheimer’s beta-amyloid fibrils in vitro. Biochim Biophys Acta 1690(3):193–202
107. Li G, Pomes R (2013) Binding mechanism of inositol stereoisomers to monomers and aggregates of Abeta(16-22). J Phys Chem B 117(22):6603–13
108. Mohamed T et al (2013) Tau-derived-hexapeptide 306VQIVYK311 aggregation inhibitors: nitrocatechol moiety as a pharmacophore in drug design. ACS Chem Neurosci 4(12):1559–70
109. Landau M et al (2011) Towards a pharmacophore for amyloid. PLoS Biol 9(6):e1001080
110. Jiang L et al (2013) Structure-based discovery of fiber-binding compounds that reduce the cytotoxicity of amyloid beta. Elife 2:e00857
111. Eisenberg DS, et al (2013) Pharmacophores for amyloid fibers involved in Alzheimer’s disease. World Patent WO2013010176A2
112. Miller Y, Ma B, Nussinov R (2010) Polymorphism in Alzheimer Abeta amyloid organization reflects conformational selection in a rugged energy landscape. Chem Rev 110(8):4820–38
113. Sato M et al (2013) Site-specific inhibitory mechanism for amyloid beta42 aggregation by catechol-type flavonoids targeting the Lys residues. J Biol Chem 288(32):23212–24
114. Rao PPN et al (2015) Curcumin binding to beta amyloid: a computational study. Chem Biol Drug Des. doi:10.1111/cbdd.12552
115. Lipinski CA et al (2001) Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Adv Drug Deliv Rev 46(1-3):3–26
116. Cirrito JR et al (2003) In vivo assessment of brain interstitial fluid with microdialysis reveals plaque-associated changes in amyloid-beta metabolism and half-life. J Neurosci 23(26):8844–53
117. Ferri P et al (2015) Enhancement of flavonoid ability to cross the blood-brain barrier of rats by co-administration with alpha-tocopherol. Food Funct 6(2):394–400
118. Shu XH et al (2015) Diffusion efficiency and bioavailability of resveratrol administered to rat brain by different routes: therapeutic implications. Neurotherapeutics 12(2):491–501
119. Sinha S et al (2011) Lysine-specific molecular tweezers are broad-spectrum inhibitors of assembly and toxicity of amyloid proteins. J Am Chem Soc 133(42):16958–69