Natural polyphenols binding to amyloid: A broad class of compounds to treat different human amyloid diseases

Molecular Nutrition and Food Research

Volumn 59, Issue 1, 2015, Pages 8-20

  Ngoungoure, Viviane L Ndam ^a,b   Schluesener, Jan ^b   Moundipa, Paul F ^a   Schluesener, Hermann ^b  

^a UNIVERSITY OF YAOUNDÉ I   (Cameroon)

^b UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

Author keywords

Amyloid diseases; Amyloid fibrils; Amyloidogenesis; Human diet; Natural polyphenols

Indexed keywords

AMYLOID; PLANT MEDICINAL PRODUCT; POLYPHENOL;

ALZHEIMER DISEASE; AMYLOIDOSIS; ANIMAL; CHEMISTRY; DISEASE MODEL; HUMAN; METABOLISM;

ALZHEIMER DISEASE; AMYLOID; AMYLOIDOSIS; ANIMALS; DISEASE MODELS, ANIMAL; HUMANS; PHYTOCHEMICALS; POLYPHENOLS;

EID: 84921282559     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201400290     Document Type: Review

References (118)

1. Tsao, R., Chemistry and biochemistry of dietary polyphenols. Nutrients 2010, 2, 1231-1246.
2. Crozier, A., Jaganath, I. B., Clifford, M. N., Dietary phenolics: chemistry, bioavailability and effects on health. Nat. Prod. Rep. 2009, 26, 1001-1043.
3. Martin, K. R., Appel, C. L., Polyphenols as dietary supplements: a double-edged sword. Nutr. Diet. Suppl. 2010, 2, 1-12.
4. Kennedy, D. O., Wightman, E. L., Herbal extracts and phytochemicals: plant secondary metabolites and the enhancement of human brain function. Adv. Nutr. 2011, 2, 32-50.
5. Kumar, B., Sandhar, H. K., Prasher, S., Tiwari, P. et al., A Review of Phytochemistry and Pharmacology of Flavonoids. Internationale Pharmaceutica Sciencia 2011, 1, 25-41.
6. Pandey, K. B., Rizvi, S. I., Current Understanding of dietary polyphenols and their role in health and disease. Curr. Nutr. Food Sci. 2009, 5, 249-263.
7. Hung, H. C., Joshipura, K. J., Jiang, R., Hu, F. B. et al., Fruit and vegetable intake and risk of major chronic disease. J. Natl. Cancer Inst. 2004, 96, 1577-1584.
8. Massim, D'A., Carmela, F., Roberta, Di B., Raffaella, G. et al., Polyphenols, dietary sources and bioavailability. Ann. Ist. Super. Sanita 2007, 43, 348-361.
9. Manach, C., Scalbert, A., Morand, C., Remesy, C. et al., Polyphenols: food sources and bioavailability. Am. J. Clin. Nutr. 2004, 79, 727-747.
10. Leopoldini, M., Russo, N., Toscano, M., The molecular basis of working mechanism of natural polyphenolic antioxidants. Food Chem. 2011, 125, 288-306.
11. Bahadoran, Z., Mirmiran, P., Azizi, F., Dietary polyphenols as potential nutraceuticals in management of diabetes: a review. J. Diabetes Metab. Disord. 2013, 12, 43.
12. Magrone, T., Marzulli, G., Jirillo, E., Immunopathogenesis of neurodegenerative diseases: current therapeutic models of neuroprotection with special reference to natural products. Curr. Pharm. Des. 2012, 18, 34-42.
13. Stefani, M., Rigacci, S., Protein folding and aggregation into amyloid: the interference by natural phenolic compounds. Int. J. Mol. Sci. 2013, 14, 12411-12457.
14. Herczenik, E., Gebbink, M. F., Molecular and cellular aspects of protein misfolding and disease. FASEB J. 2008, 22, 2115-2133.
15. Makin, O. S., Atkins, E., Sikorski, P., Johansson, J. et al., Molecular basis for amyloid fibril formation and stability. Proc. Natl. Acad. Sci. USA 2005, 102, 315-320.
16. Porat, Y., Abramowitz, A., Gazit, E., Inhibition of amyloid fibril formation by polyphenols: structural similarity and aromatic interactions as a common inhibition mechanism. Chem. Biol. Drug. Des. 2006, 67, 27-37.
17. Dasilva, K. A., Shaw, J. E., McLaurin, J., Amyloid-beta fibrillogenesis: structural insight and therapeutic intervention. Exp. Neurol. 2010, 223, 311-321.
18. Bellotti, V., Nuvolone, M., Giorgetti, S., Obici, L. et al., The workings of the amyloid diseases. Ann. Med. 2007, 39, 200-207.
19. Sipe, J. D., Cohen, A. S., Review: history of the amyloid fibril. J. Struct. Biol. 2000, 130, 88-98.
20. Gazit, E., Mechanisms of amyloid fibril self-assembly and inhibition. Model short peptides as a key research tool. FEBS J. 2005, 272, 5971-5978.
21. Rambaran, R. N., Serpell, L. C., Amyloid fibrils: abnormal protein assembly. Prion 2008, 2, 112-117.
22. Roychaudhuri, R., Yang, M., Hoshi, M. M., Teplow, D. B., Amyloid beta-protein assembly and Alzheimer disease. J. Biol. Chem. 2009, 284, 4749-4753.
23. Ferreira, S. T., Vieira, M. N. N., De Felice, F. G., Soluble protein oligomers as emerging toxins in Alzheimer's and other amyloid diseases. IUBMB Life 2007, 59, 332-345.
24. Glabe, C. G., Structural classification of toxic amyloid oligomers. J. Biol. Chem. 2008, 283, 29639-29643.
25. Malchiodi-Albedi, F., Paradisi, S., Matteucci, A., Frank, C., Diociaiuti, M., Amyloid oligomer neurotoxicity, calcium dysregulation, and lipid rafts. Int. J. Alzheimers Dis. 2011, 2011, 906964.
26. Prasansuklab, A., Tencomnao, T., Amyloidosis in Alzheimer's disease: the toxicity of amyloid beta (Aβ), mechanisms of its accumulation and implications of medicinal plants for therapy beta (Aβ), mechanisms of its accumulation and implications of medicinal plants for therapy. eCAM 2013, 2013, 413808.
27. Benson, M. D., Liepnieks, J. J., Yazaki, M., Yamashita, T. et al., A new human hereditary amyloidosis: the result of a stop-codon mutation in the apolipoprotein AII gene. Genomics 2001, 72, 272-277.
28. Desport, E., Bridoux, F., Sirac, C., Delbes, S. et al., Al amyloidosis. Orphanet J. Rare Dis. 2012, 7, 54.
29. Sanchorawala, V., Light-chain (AL) amyloidosis: diagnosis and treatment. Clin. J. Am. Soc. Nephrol. 2006, 1, 1331-1341.
30. Ebert, E. C., Gastric and esophageal Amyloidosis. Gastroenterol. Hepatol. 2009, 5, 575-576.
31. Solomon, J. P., Page, L. J., Balch, W. E., Kelly, J. W., Gelsolin amyloidosis: genetics, biochemistry, pathology and possible strategies for therapeutic intervention. Crit. Rev. Biochem. Mol. Biol. 2012, 47, 282-296.
32. Ghiso, J., Frangione, B., Cerebral amyloidosis, amyloid angiopathy, and their relationship to stroke and dementia. J. Alzheimer's Dis. 2001, 3, 65-73.
33. Georgiades, C. S., Neyman, E. G., Barish, M. A., Fishman, E. K., Amyloidosis: review and CT manifestations. Radiographics 2004, 24, 405-416.
34. Drueke, T. B., Beta2-microglobulin and amyloidosis. Nephrol. Dial. Transplant. 2000, 15 Suppl 1, 17-24.
35. Murphy, M. P., LeVine, H., 3rd, Alzheimer's disease and the amyloid-beta peptide. J. Alzheimer's Dis. 2010, 19, 311-323.
36. Stefanis, L., alpha-Synuclein in Parkinson's disease. Cold Spring Harb. Perspect. Med. 2012, 2, a009399.
37. Bendor, J. T., Logan, T. P., Edwards, R. H., The function of alpha-synuclein. Neuron 2013, 79, 1044-1066.
38. Knight, R. S. G., Will, R. G., Prion diseases. J. Neurol. Neurosurg. Psychiatr. 2004, 75, i36-i42.
39. Imran, M., Mahmood, S., An overview of human prion diseases. J. Virol. 2011, 8, 559.
40. McKintosh, E., Tabrizi, S. J., Collinge, J., Prion diseases. J. Neurovirol. 2003, 9, 183-193.
41. Mahler, R. J., Adler, M. L., Clinical review 102: Type 2 diabetes mellitus: update on diagnosis, pathophysiology, and treatment. J. Clin. Endocrinol. Metab. 1999, 84, 1165-1171.
42. Jaikaran, E. T., Clark, A., Islet amyloid and type 2 diabetes: from molecular misfolding to islet pathophysiology. Biochim. Biophys. Acta 2001, 1537, 179-203.
43. Gunasekaran, U., Gannon, M., Types 2 Diabetes and the aging pancreatic beta cell. Aging 2011, 3, 565-575.
44. Westermark, P., Andersson, A., Westermark, G. T., Islet amyloid polypeptide, islet amyloid, and diabetes mellitus. Physiol. Rev. 2011, 91, 795-826.
45. Haataja, L., Gurlo, T., Huang, C. J., Butler, P. C., Islet amyloid in type 2 diabetes, and the toxic oligomer hypothesis. Endocr. Rev. 2008, 29, 303-316.
46. Sgarbossa, A., Natural biomolecules and protein aggregation: emerging strategies against amyloidogenesis. Int. J. Mol. Sci. 2012, 13, 17121-17137.
47. Cheng, B., Gong, H., Xiao, H., Petersen, R. B. et al., Inhibiting toxic aggregation of amyloidogenic proteins: a therapeutic strategy for protein misfolding diseases. Biochim. Biophys. Acta. 2013, 1830, 4860-4871.
48. Bastianetto, S., Krantic, S., Quirion, R., Polyphenols as potential inhibitors of amyloid aggregation and toxicity: possible significance to Alzheimer's disease. Min. Rev. Med. Chem. 2008, 8, 429-435.
49. Berhanu, W. M., Masunov, A. E., Natural polyphenols as inhibitors of amyloid aggregation. Molecular dynamics study of GNNQQNY heptapeptide decamer. Biophys. Chem. 2010, 149, 12-21.
50. Ebrahimi, A., Schluesener, H., Natural polyphenols against neurodegenerative disorders: potentials and pitfalls. Ageing Res. Rev. 2012, 11, 329-345.
51. Bhullar, K. S., Rupasinghe, H. P., Polyphenols: multipotent therapeutic agents in neurodegenerative diseases. Oxid. Med. Cell Longev. 2013, 2013, 891748.
52. Wu, C., Lei, H., Wang, Z., Zhang, W. et al., Phenol red interacts with the protofibril-like oligomers of an amyloidogenic hexapeptide nfgail through both hydrophobic and aromatic contacts. Biophys. J. 2006, 91, 3664-3672.
53. Davis, T. J., Soto-Ortega, D. D., Kotarek, J. A., Gonzalez-Velasquez, F. J. et al., Comparative study of inhibition at multiple stages of amyloid-beta self-assembly provides mechanistic insight. Mol. Pharmacol. 2009, 76, 405-413.
54. Caruana, M., Hogen, T., Levin, J., Hillmer, A. et al., Inhibition and disaggregation of alpha-synuclein oligomers by natural polyphenolic compounds. FEBS Lett. 2011, 585, 1113-1120.
55. Porat, Y., Mazor, Y., Efrat, S., Gazit, E., Inhibition of islet amyloid polypeptide fibril formation: a potential role for heteroaromatic interactions. Biochemistry 2004, 43, 14454-14462.
56. Ono, K., Li, L., Takamura, Y., Yoshiike, Y. et al., Phenolic compounds prevent amyloid beta-protein oligomerization and synaptic dysfunction by site-specific binding. J. Biol. Chem. 2012, 287, 14631-14643.
57. Zhang, C., Browne, A., Child, D., Tanzi, R. E., Curcumin decreases amyloid-beta peptide levels by attenuating the maturation of amyloid-beta precursor protein. J. Biol. Chem. 2010, 285, 28472-28480.
58. Pandey, N., Strider, J., Nolan, W. C., Yan, S. X. et al., Curcumin inhibits aggregation of alpha-synuclein. Acta Neuropathol. 2008, 115, 479-489.
59. Daval, M., Bedrood, S., Gurlo, T., Huang, C. J. et al., The effect of curcumin on human islet amyloid polypeptide misfolding and toxicity. Amyloid 2010, 17, 118-128.
60. Ono, K., Hasegawa, K., Naiki, H., Yamada, M., Curcumin has potent anti-amyloidogenic effects for Alzheimer's beta-amyloid fibrils in vitro. J. Neuroscience Res. 2004, 75, 742-750.
61. Wang, S. S., Liu, K. N., Lee, W. H., Effect of curcumin on the amyloid fibrillogenesis of hen egg-white lysozyme. Biophys. Chem. 2009, 144, 78-87.
62. Yang, F., Lim, G. P., Begum, A. N., Ubeda, O. J. et al., Curcumin inhibits formation of amyloid beta oligomers and fibrils, binds plaques, and reduces amyloid in vivo. J. Biol. Chem. 2005, 280, 5892-5901.
63. Singh, P. K., Kotia, V., Ghosh, D., Mohite, G. M. et al., Curcumin modulates alpha-synuclein aggregation and toxicity. ACS Chem. Neurosci. 2013, 4, 393-407.
64. Ahmad, B., Lapidus, L. J., Curcumin prevents aggregation in α-synuclein by increasing the reconfiguration rate. J. Biol. Chem. 2012, 287, 9193-9199.
65. Ferreira, N., Saraiva, M. J., Almeida, M. R., Natural polyphenols inhibit different steps of the process of transthyretin (TTR) amyloid fibril formation. FEBS Lett. 2011, 585, 2424-2430.
66. Sparks, S., Liu, G., Robbins, K. J., Lazo, N. D., Curcumin modulates the self-assembly of the islet amyloid polypeptide by disassembling alpha-helix. Biochem. Biophys. Res. Commun. 2012, 422, 551-555.
67. Feng, Y., Wang, X. P., Yang, S. G., Wang, Y. J. et al., Resveratrol inhibits beta-amyloid oligomeric cytotoxicity but does not prevent oligomer formation. Neurotoxicology 2009, 30, 986-995.
68. Jiang, P., Li, W., Shea, J. E., Mu, Y., Resveratrol inhibits the formation of multiple-layered beta-sheet oligomers of the human islet amyloid polypeptide segment 22-27. Biophys. J. 2011, 100, 1550-1558.
69. Su, D., Cheng, Y., Liu, M., Liu, D. et al., Comparision of piceid and resveratrol in antioxidation and antiproliferation activities in vitro. PLoS One 2013, 8, e54505.
70. Riviere, C., Delaunay, J. C., Immel, F., Cullin, C. et al., The polyphenol piceid destabilizes preformed amyloid fibrils and oligomers in vitro: hypothesis on possible molecular mechanisms. Neurochem. Res. 2009, 34, 1120-1128.
71. Iuvone, T., De Filippis, D., Esposito, G., D'Amico, A. et al., The spice sage and its active ingredient rosmarinic acid protect PC12 cells from amyloid-beta peptide-induced neurotoxicity. J. Pharmacol. Exp. Ther. 2006, 317, 1143-1149.
72. Seyyed Mehdi, M., Effect of two herbal polyphenol compounds on human amylin amyloid formation and destabilization. J. Med. Plants Res. 2012, 6, 3207-3212.
73. Hamaguchi, T., Ono, K., Murase, A., Yamada, M., Phenolic compounds prevent Alzheimer's pathology through different effects on the amyloid-beta aggregation pathway. Am. J. Pathol. 2009, 175, 2557-2565.
74. Ono, K., Hirohata, M., Yamada, M., Ferulic acid destabilizes preformed beta-amyloid fibrils in vitro. Biochem. Biophys. Res. Commun. 2005, 336, 444-449.
75. Aarabi, M. H., Mirhashemi, S. M., The role of two natural flavonoids on human amylin aggregation. Afr. J. Pharm. Pharmacol. 2012, 6, 2374-2379.
76. Zhang, S. Q., Obregon, D., Ehrhart, J., Deng, J. et al., Baicalein reduces beta-amyloid and promotes nonamyloidogenic amyloid precursor protein processing in an Alzheimer's disease transgenic mouse model. J. Neurosci. Res. 2013, 91, 1239-1246.
77. Song, S.-M., Wang, Y.-X., Xiong, L.-M., Qu, L.-B. et al., Interaction between baicalein and amyloid-β fibrils studied by fluorescence spectroscopy. Chem. Res. Chin. Univ. 2013, 29, 20-25.
78. Zhu, M., Rajamani, S., Kaylor, J., Han, S. et al., The flavonoid baicalein inhibits fibrillation of alpha-synuclein and disaggregates existing fibrils. J. Biol. Chem. 2004, 279, 26846-26857.
79. Meng, X., Munishkina, L. A., Fink, A. L., Uversky, V. N., Effects of various flavonoids on the α-synuclein fibrillation process. Parkinson's Dis. 2010, 2010, 650794.
80. Hong, D. P., Fink, A. L., Uversky, V. N., Structural characteristics of alpha-synuclein oligomers stabilized by the flavonoid baicalein. J. Mol. Biol. 2008, 383, 214-223.
81. Ono, K., Hasegawa, K., Naiki, H., Yamada, M., Anti-amyloidogenic activity of tannic acid and its activity to destabilize Alzheimer's beta-amyloid fibrils in vitro. Biochim. Biophys. Acta 2004, 1690, 193-202.
82. Ono, K., Yamada, M., Antioxidant compounds have potent anti-fibrillogenic and fibril-destabilizing effects for α-synuclein fibrils in vitro. J. Neurochem. 2006, 97, 105-115.
83. Rezai-Zadeh, K., Shytle, D., Sun, N., Mori, T. et al., Green tea epigallocatechin-3-gallate (EGCG) modulates amyloid precursor protein cleavage and reduces cerebral amyloidosis in Alzheimer transgenic mice. J. Neurosci. 2005, 25, 8807-8814.
84. Bieschke, J., Russ, J., Friedrich, R. P., Ehrnhoefer, D. E. et al., EGCG remodels mature alpha-synuclein and amyloid-beta fibrils and reduces cellular toxicity. Proc. Natl. Acad. Sci. USA 2010, 107, 7710-7715.
85. Ehrnhoefer, D. E., Duennwald, M., Markovic, P., Wacker, J. L. et al., Green tea (-)-epigallocatechin-gallate modulates early events in huntingtin misfolding and reduces toxicity in Huntington's disease models. Hum. Mol. Genet. 2006, 15, 2743-2751.
86. Meng, F., Abedini, A., Plesner, A., Verchere, C. B. et al., The flavanol (-)-epigallocatechin 3-gallate inhibits amyloid formation by islet amyloid polypeptide, disaggregates amyloid fibrils, and protects cultured cells against IAPP-induced toxicity. Biochemistry 2010, 49, 8127-8133.
87. Ono, K., Yoshiike, Y., Takashima, A., Hasegawa, K. et al., Potent anti-amyloidogenic and fibril-destabilizing effects of polyphenols in vitro: implications for the prevention and therapeutics of Alzheimer's disease. J. Neurochem. 2003, 87, 172-181.
88. Zelus, C., Fox, A., Calciano, A., Faridian, B. S. et al., Myricetin inhibits islet amyloid polypeptide (IAPP) aggregation and rescues living mammalian cells from IAPP toxicity. Open Biochem. J. 2012, 6, 66-70.
89. Noor, H., Cao, P., Raleigh, D. P., Morin hydrate inhibits amyloid formation by islet amyloid polypeptide and disaggregates amyloid fibers. Protein Sci. 2012, 21, 373-382.
90. Pasinetti, G. M., Novel role of red wine-derived polyphenols in the prevention of Alzheimer's disease dementia and brain pathology: experimental approaches and clinical implications. Planta Med. 2012, 78, 1614-1619.
91. Durairajan, S. S. K., Yuan, Q., Xie, L., Chan, W.-S. et al, Salvianolic acid B inhibits Aβ fibril formation and disaggregates preformed fibrils and protects against Aβ-induced cytotoxicty. Neurochem. Int. 2008, 52, 741-750.
92. Cheng, B., Gong, H., Li, X., Sun, Y. et al., Salvianolic acid B inhibits the amyloid formation of human islet amyloid polypeptide and protects pancreatic beta-cells against cytotoxicity. Proteins 2013, 81, 613-621.
93. Rigacci, S., Guidotti, V., Bucciantini, M., Parri, M. et al., Oleuropein aglycon prevents cytotoxic amyloid aggregation of human amylin. J. Nutr. Biochem. 2010, 21, 726-735.
94. Lu, P., Mamiya, T., Lu, L. L., Mouri, A. et al., Silibinin attenuates amyloid beta(25-35) peptide-induced memory impairments: implication of inducible nitric-oxide synthase and tumor necrosis factor-alpha in mice. J. Pharmacol. Exp. Ther. 2009, 331, 319-326.
95. Lu, P., Mamiya, T., Lu, L. L., Mouri, A. et al., Silibinin prevents amyloid beta peptide-induced memory impairment and oxidative stress in mice. Br. J. Pharmacol. 2009, 157, 1270-1277.
96. Yin, F., Liu, J., Ji, X., Wang, Y. et al., Silibinin: a novel inhibitor of Aβ aggregation. Neurochem. Int. 2011, 58, 399-403.
97. Cheng, B., Gong, H., Li, X., Sun, Y. et al., Silibinin inhibits the toxic aggregation of human islet amyloid polypeptide. Biochem. Biophys. Res. Commun. 2012, 419, 495-499.
98. Sarkar, N., Kumar, M., Dubey, V. K., Rottlerin dissolves pre-formed protein amyloid: a study on hen egg white lysozyme. Biochim. Biophys. Acta. 2011, 1810, 809-814.
99. Feng, Y., Yang, S. G., Du, X. T., Zhang, X. et al., Ellagic acid promotes Abeta42 fibrillization and inhibits Abeta42-induced neurotoxicity. Biochem. Biophys. Res. Commun. 2009, 390, 1250-1254.
100. Riviere, C., Papastamoulis, Y., Fortin, P. Y., Delchier, N. et al., New stilbene dimers against amyloid fibril formation. Bioorg. Med. Chem. Lett. 2010, 20, 3441-3443.
101. Riviere, C., Richard, T., Vitrac, X., Merillon, J. M. et al., New polyphenols active on beta-amyloid aggregation. Bioorg. Med. Chem. Lett. 2008, 18, 828-831.
102. Begum, A. N., Jones, M. R., Lim, G. P., Morihara, T. et al., Curcumin structure-function, bioavailability, and efficacy in models of neuroinflammation and Alzheimer's disease. J. Pharmacol. Exp. Ther. 2008, 326, 196-208.
103. Orlando, R. A., Gonzales, A. M., Royer, R. E., Deck, L. M., Vander Jagt, D. L., A chemical analog of curcumin as an improved inhibitor of amyloid Abeta oligomerization. PLoS One 2012, 7, e31869.
104. Alavez, S., Vantipalli, M. C., Zucker, D. J. S., Klang, I. M. et al., Amyloid-binding compounds maintain protein homeostasis during ageing and extend lifespan. Nature 2011, 472, 226-229.
105. Cuanalo-Contreras, K., Mukherjee, A., Soto, C., Role of protein misfolding and proteostasis deficiency in protein misfolding diseases and aging. Int. J. Cell Biol. 2013, 2013, 638083.
106. Ono, M., Saji, H., SPECT imaging agents for detecting cerebral beta-amyloid plaques. Int. J. Mol. Imaging 2011, 2011, 543267.
107. Ni, R., Gillberg, P. G., Bergfors, A., Marutle, A. et al., Amyloid tracers detect multiple binding sites in Alzheimer's disease brain tissue. Brain 2013, 136, 2217-2227.
108. Villemagne, V. L., Klunk, W. E., Mathis, C. A., Rowe, C. C. et al., Abeta Imaging: feasible, pertinent, and vital to progress in Alzheimer's disease. Eur. J. Nucl. Med. Mol. Imaging 2012, 39, 209-219.
109. Maya, Y., Ono, M., Watanabe, H., Haratake, M. et al., Novel Radioiodinated Aurones as Probes for SPECT imaging of β-amyloid plaques in the brain. Bioconjugate Chem. 2009, 20, 95-101.
110. Ono, M., Haratake, M., Mori, H., Nakayama, M., Novel chalcones as probes for in vivo imaging of beta-amyloid plaques in Alzheimer's brains. Bioorg. Med. Chem. 2007, 15, 6802-6809.
111. Ono, M., Maya, Y., Haratake, M., Ito, K. et al., Aurones serve as probes of beta-amyloid plaques in Alzheimer's disease. Biochem. Biophys. Res. Commun. 2007, 361, 116-121.
112. Ono, M., Yoshida, N., Ishibashi, K., Haratake, M. et al., Radioiodinated flavones for in vivo imaging of beta-amyloid plaques in the brain. J. Med. Chem. 2005, 48, 7253-7260.
113. Kung, H. F., Lee, C. W., Zhuang, Z. P., Kung, M. P. et al., Novel stilbenes as probes for amyloid plaques. J. Am. Chem. Soc. 2001, 123, 12740-12741.
114. Lakey-Beitia, J., Berrocal, R., Rao, K. S., Durant, A. A., Polyphenols as Therapeutic Molecules in Alzheimer's Disease Through Modulating Amyloid Pathways. Molecular Neurobiol. 2014.
115. Smid, S. D., Maag, J. L., Musgrave, I. F., Dietary polyphenol-derived protection against neurotoxic beta-amyloid protein: from molecular to clinical. Food Funct. 2012, 3, 1242-1250.
116. Tang, M.-K., Zhang, J., Salvionolic acid B inhibits fibril formation and neurotoxicity of amyloid beta-protein in vitro. Acta Pharmacol. Sin. 2001, 22, 380-384.
117. Mori, T., Koyama, N., Guillot-Sestier, M.-V., Tan, J. et al., Ferulic acid is a nutraceutical β-secretase modulator that improves behavioral impairment and alzheimer-like pathology in transgenic mice. PLoS One 2013, 8, e55774.
118. Zhang, Z. Y., Daniels, R., Schluesener, H. J., Oridonin ameliorates neuropathological changes and behavioural deficits in a mouse model of cerebral amyloidosis. J. Cell. Mol. Med. 2013, 17, 1566-1576.