Protective effects of flavonoids against Alzheimer's disease-related neural dysfunctions

Biomedicine and Pharmacotherapy

Volumn 93, Issue , 2017, Pages 218-229

  Bakhtiari, Mahsa ^a   Panahi, Yunes ^b   Ameli, Javad ^b   Darvishi, Behrad ^c  

^a ISLAMIC AZAD UNIVERSITY   (Iran)

^b BAQIYATALLAH UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^c AVICENNA RESEARCH INSTITUTE   (Iran)

Author keywords

Alzheimer's disease; Amyloid peptides; Dementia; Flavonoids; Signaling pathways; Tau proteins

Indexed keywords

ANTHOCYANIN; APIGENIN; AURANTIIN; BAICALEIN; CHOLINESTERASE INHIBITOR; CYANIDIN 3 O GLUCOPYRANOSIDE; EPIGALLOCATECHIN GALLATE; FLAVONOID; GENISTEIN; HESPERETIN; HESPERIDIN; KAEMPFEROL; LUTEOLIN; QUERCETIN; RUTOSIDE; SILIBININ; SILYMARIN; UNCLASSIFIED DRUG; NEUROPROTECTIVE AGENT;

ALZHEIMER DISEASE; COGNITIVE DEFECT; DEMENTIA; DRUG DELIVERY SYSTEM; DRUG MECHANISM; HUMAN; NANOTECHNOLOGY; NEUROPROTECTION; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; ANIMAL; DRUG EFFECTS; SIGNAL TRANSDUCTION;

ALZHEIMER DISEASE; ANIMALS; FLAVONOIDS; HUMANS; NEUROPROTECTIVE AGENTS; SIGNAL TRANSDUCTION;

EID: 85020928027     PISSN: 07533322     EISSN: 19506007     Source Type: Journal    
DOI: 10.1016/j.biopha.2017.06.010     Document Type: Review

References (154)

1. Prince, M., Bryce, R., Albanese, E., Wimo, A., Ribeiro, W., Ferri, C.P., The global prevalence of dementia: a systematic review and metaanalysis. Alzheimer's Dementia 9:1 (2013), 63–75 (e2).
2. Brookmeyer, R., Kawas, C.H., Abdallah, N., Paganini-Hill, A., Kim, R.C., Corrada, M.M., Impact of interventions to reduce Alzheimer's disease pathology on the prevalence of dementia in the oldest-old. Alzheimer's Dementia 12:3 (2016), 225–232.
3. Polidori, M.C., Pientka, L., Mecocci, P., A review of the major vascular risk factors related to Alzheimer's disease. J. Alzheimer's Dis. 32:3 (2012), 521–530.
4. Huang, Y., Mucke, L., Alzheimer mechanisms and therapeutic strategies. Cell 148:6 (2012), 1204–1222.
5. Desikan, R.S., Cabral, H.J., Hess, C.P., Dillon, W.P., Glastonbury, C.M., Weiner, M.W., Schmansky, N.J., Greve, D.N., Salat, D.H., Buckner, R.L., Automated MRI measures identify individuals with mild cognitive impairment and Alzheimer's disease. Brain, 2009, awp123.
6. Holmes, C., Boche, D., Wilkinson, D., Yadegarfar, G., Hopkins, V., Bayer, A., Jones, R.W., Bullock, R., Love, S., Neal, J.W., Long-term effects of Aβ 42 immunisation in Alzheimer's disease: follow-up of a randomised, placebo-controlled phase I trial. Lancet 372:9634 (2008), 216–223.
7. Sudduth, T.L., Schmitt, F.A., Nelson, P.T., Wilcock, D.M., Neuroinflammatory phenotype in early Alzheimer's disease. Neurobiol. Aging 34:4 (2013), 1051–1059.
8. Hollingworth, P., Harold, D., Jones, L., Owen, M.J., Williams, J., Alzheimer's disease genetics: current knowledge and future challenges. Int. J. Geriatr. Psychiatry 26:8 (2011), 793–802.
9. Gonzalez, Lopez, Irene, et al. “genetic and transcriptomic profiles of inflammation in neurodegenerative diseases: Alzheimer, Parkinson, Creutzfeldt-Jakob and Tauopathies.”. international journal of molecular siences, 17(2), 2016, 206.
10. Singh, S.K., Castellani, R., Perry, G., Oxidative Stress and Alzheimer's Disease, Inflammation, Aging and Oxidative Stress, 2016, 2016, Springer, 189–198.
11. Solfrizzi, V., Panza, F., Frisardi, V., Seripa, D., Logroscino, G., Imbimbo, B.P., Pilotto, A., Diet and Alzheimer's disease risk factors or prevention: the current evidence. Expert Rev. Neurother. 11:5 (2011), 677–708.
12. Choi, D.-Y., Lee, Y.-J., Hong, J.T., Lee, H.-J., Antioxidant properties of natural polyphenols and their therapeutic potentials for Alzheimer's disease. Brain Res. Bull. 87:2 (2012), 144–153.
13. García-Lafuente, A., Guillamón, E., Villares, A., Rostagno, M.A., Martínez, J.A., Flavonoids as anti-inflammatory agents: implications in cancer and cardiovascular disease. Inflamm. Res. 58:9 (2009), 537–552.
14. Masliah, E., Mallory, M., Alford, M., DeTeresa, R., Iwai, A., Saitoh, T., Molecular Mechanisms of Synaptic Disconnection in Alzheimer's Disease, Connections Cognition and Alzheimer's Disease, 1997, 2016, Springer, 121–140.
15. Terry, R.D., Masliah, E., Hansen, L.A., Structural Basis of the Cognitive Alterations in Alzheimer Disease. 1994.
16. DeKosky, S.T., Scheff, S.W., Styren, S.D., Structural correlates of cognition in dementia: quantification and assessment of synapse change. Neurodegeneration 5:4 (1996), 417–421.
17. Iwata, N., Tsubuki, S., Takaki, Y., Shirotani, K., Lu, B., Gerard, N.P., Gerard, C., Hama, E., Lee, H.-J., Saido, T.C., Metabolic regulation of brain Aβ by neprilysin. Science 292:5521 (2001), 1550–1552.
18. Lee, J., Retamal, C., Cuitiño, L., Caruano-Yzermans, A., Shin, J.-E., Van Kerkhof, P., Marzolo, M.-P., Bu, G., Adaptor protein sorting nexin 17 regulates amyloid precursor protein trafficking and processing in the early endosomes. J. Biol. Chem. 283:17 (2008), 11501–11508.
19. Meziane, H., Dodart, J.-C., Mathis, C., Little, S., Clemens, J., Paul, S., Ungerer, A., Memory-enhancing effects of secreted forms of the β-amyloid precursor protein in normal and amnestic mice. Proc. Natl. Acad. Sci. 95:21 (1998), 12683–12688.
20. Faigle, R., Song, H., Signaling mechanisms regulating adult neural stem cells and neurogenesis. Biochim. Biophys. Acta (BBA)-Gen. Subj. 1830:2 (2013), 2435–2448.
21. O'Brien, R.J., Wong, P.C., Amyloid precursor protein processing and Alzheimer's disease. Annu. Rev. Neurosci., 34, 2011, 185.
22. Koo, E.H., Sisodia, S.S., Archer, D.R., Martin, L.J., Weidemann, A., Beyreuther, K., Fischer, P., Masters, C.L., Price, D.L., Precursor of amyloid protein in Alzheimer disease undergoes fast anterograde axonal transport. Proc. Natl. Acad. Sci. 87:4 (1990), 1561–1565.
23. Kamal, A., Stokin, G.B., Yang, Z., Xia, C.-H., Goldstein, L.S., Axonal transport of amyloid precursor protein is mediated by direct binding to the kinesin light chain subunit of kinesin-I. Neuron 28:2 (2000), 449–459.
24. Ehehalt, R., Keller, P., Haass, C., Thiele, C., Simons, K., Amyloidogenic processing of the Alzheimer β-amyloid precursor protein depends on lipid rafts. J. Cell Biol. 160:1 (2003), 113–123.
25. Bendiske, J., Bahr, B.A., Lysosomal activation is a compensatory response against protein accumulation and associated synaptopathogenesis—an approach for slowing Alzheimer disease?. J. Neuropathol. Exp. Neurol. 62:5 (2003), 451–463.
26. Geschwind, D.H., Tau phosphorylation, tangles, and neurodegeneration: the chicken or the egg?. Neuron 40:3 (2003), 457–460.
27. Kim, J., Basak, J.M., Holtzman, D.M., The role of apolipoprotein E in Alzheimer's disease. Neuron 63:3 (2009), 287–303.
28. Cuello, A.C., Intracellular and extracellular Aβ, a tale of two neuropathologies. Brain Pathol. 15:1 (2005), 66–71.
29. Lansbury, P.T., Evolution of amyloid: what normal protein folding may tell us about fibrillogenesis and disease. Proc. Natl. Acad. Sci. 96:7 (1999), 3342–3344.
30. Walsh, D., Klyubin, I., Fadeeva, J., Rowan, M., Selkoe, D., Amyloid-β-oligomers: their production, toxicity and therapeutic inhibition. Biochem. Soc. Trans. 30:4 (2002), 552–557.
31. Nakamura, T., Lipton, S.A., Cell death: protein misfolding and neurodegenerative diseases. Apoptosis 14:4 (2009), 455–468.
32. Nixon, R.A., Cataldo, A.M., Lysosomal system pathways: genes to neurodegeneration in Alzheimer's disease. J. Alzheimer's Dis. 9:3 Supplement (2006), 277–289.
33. Palop, J.J., Chin, J., Roberson, E.D., Wang, J., Thwin, M.T., Bien-Ly, N., Yoo, J., Ho, K.O., Yu, G.-Q., Kreitzer, A., Aberrant excitatory neuronal activity and compensatory remodeling of inhibitory hippocampal circuits in mouse models of Alzheimer's disease. Neuron 55:5 (2007), 697–711.
34. Chin, J., Palop, J.J., Yu, G.-Q., Kojima, N., Masliah, E., Mucke, L., Fyn kinase modulates synaptotoxicity, but not aberrant sprouting, in human amyloid precursor protein transgenic mice. J. Neurosci. 24:19 (2004), 4692–4697.
35. Hooper, C., Markevich, V., Plattner, F., Killick, R., Schofield, E., Engel, T., Hernandez, F., Anderton, B., Rosenblum, K., Bliss, T., Glycogen synthase kinase‐3 inhibition is integral to long‐term potentiation. Eur. J. Neurosci. 25:1 (2007), 81–86.
36. Rockenstein, E., Torrance, M., Adame, A., Mante, M., Bar-on, P., Rose, J.B., Crews, L., Masliah, E., Neuroprotective effects of regulators of the glycogen synthase kinase-3β signaling pathway in a transgenic model of Alzheimer's disease are associated with reduced amyloid precursor protein phosphorylation. J. Neurosci. 27:8 (2007), 1981–1991.
37. Zhu, X., Lee, H.-G., Raina, A.K., Perry, G., Smith, M.A., The role of mitogen-activated protein kinase pathways in Alzheimer's disease. Neurosignals 11:5 (2003), 270–281.
38. Zhu, X., Sun, Z., g. Lee, H., Siedlak, S.L., Perry, G., Smith, M.A., Distribution, levels, and activation of MEK1 in Alzheimer's disease. J. Neurochem. 86:1 (2003), 136–142.
39. Nguyen, T.V.V., Galvan, V., Huang, W., Banwait, S., Tang, H., Zhang, J., Bredesen, D.E., Signal transduction in Alzheimer disease: p21-activated kinase signaling requires C-terminal cleavage of APP at Asp664. J. Neurochem. 104:4 (2008), 1065–1080.
40. Mahomoodally, M.F., Gurib-Fakim, A., Subratty, A.H., Antimicrobial activities and phytochemical profiles of endemic medicinal plants of Mauritius. Pharm. Biol. 43:3 (2005), 237–242.
41. Pandey, A.K., Anti-staphylococcal activity of a pan-tropical aggressive and obnoxious weed Parthenium histerophorus: an in vitro study. Natl. Acad. Sci. Lett. 30:11–12 (2007), 383–386.
42. Heim, K.E., Tagliaferro, A.R., Bobilya, D.J., Flavonoid antioxidants: chemistry, metabolism and structure-activity relationships. J. Nutr. Biochem. 13:10 (2002), 572–584.
43. Narayana, K.R., Reddy, M.S., Chaluvadi, M., Krishna, D., Bioflavonoids classification, pharmacological, biochemical effects and therapeutic potential. Indian J. Pharmacol. 33:1 (2001), 2–16.
44. Kumar, S., Mishra, A., Pandey, A.K., Antioxidant mediated protective effect of Parthenium hysterophorus against oxidative damage using in vitro models. BMC Complement. Altern. Med., 13(1), 2013, 120.
45. Kumar, S., Pandey, A.K., Phenolic content, reducing power and membrane protective activities of Solanum xanthocarpum root extracts. Vegetos-Int. J. Plant Res. 26:1 (2013), 301–307.
46. Kumar, S., Pandey, A.K., Chemistry and biological activities of flavonoids: an overview. Sci. World J., 2013, 2013.
47. Amic, D., Davidovic-Amic, D., Beslo, D., Rastija, V., Lucic, B., Trinajstic, N., SAR and QSAR of the antioxidant activity of flavonoids. Curr. Med. Chem. 14:7 (2007), 827–845.
48. Mix, J.A., Crews, W.D. Jr., An examination of the efficacy of Ginkgo biloba extract EGb 761 on the neuropsychologic functioning of cognitively intact older adults. J. Altern. Complement. Med. 6:3 (2000), 219–229.
49. ® in a sample of cognitively intact older adults: neuropsychological findings. Human Psychopharmacol.: Clin. Exp. 17:6 (2002), 267–277.
50. Duffy, R., Wiseman, H., File, S.E., Improved cognitive function in postmenopausal women after 12 weeks of consumption of a soya extract containing isoflavones. Pharmacol. Biochem. Behav. 75:3 (2003), 721–729.
51. Casini, M.L., Marelli, G., Papaleo, E., Ferrari, A., D'Ambrosio, F., Unfer, V., Psychological assessment of the effects of treatment with phytoestrogens on postmenopausal women: a randomized, double-blind, crossover, placebo-controlled study. Fertil. Steril. 85:4 (2006), 972–978.
52. Henderson, V., John, J.S., Hodis, H., Kono, N., McCleary, C., Franke, A., Mack, W., Long-term soy isoflavone supplementation and cognition in women A randomized, controlled trial. Neurology 78:23 (2012), 1841–1848.
53. Scholey, A.B., French, S.J., Morris, P.J., Kennedy, D.O., Milne, A.L., Haskell, C.F., Consumption of cocoa flavanols results in acute improvements in mood and cognitive performance during sustained mental effort. J. Psychopharmacol. 24:10 (2010), 1505–1514.
54. Field, D.T., Williams, C.M., Butler, L.T., Consumption of cocoa flavanols results in an acute improvement in visual and cognitive functions. Physiol. Behav. 103:3 (2011), 255–260.
55. Birks, J., Grimley Evans, J., Ginkgo Biloba for Cognitive Impairment and Dementia. 2009, The Cochrane Library.
56. Kreijkamp-Kaspers, S., Kok, L., Grobbee, D.E., de Haan, E.H., Aleman, A., Lampe, J.W., van der Schouw, Y.T., Effect of soy protein containing isoflavones on cognitive function, bone mineral density, and plasma lipids in postmenopausal women: a randomized controlled trial. JAMA 292:1 (2004), 65–74.
57. Kang, J.H., Ascherio, A., Grodstein, F., Fruit and vegetable consumption and cognitive decline in aging women. Ann. Neurol. 57:5 (2005), 713–720.
58. Morris, M., Evans, D., Tangney, C., Bienias, J., Wilson, R., Associations of vegetable and fruit consumption with age-related cognitive change. Neurology 67:8 (2006), 1370–1376.
59. Nurk, E., Refsum, H., Drevon, C.A., Tell, G.S., Nygaard, H.A., Engedal, K., Smith, A.D., Intake of flavonoid-rich wine, tea, and chocolate by elderly men and women is associated with better cognitive test performance. J. Nutr. 139:1 (2009), 120–127.
60. Sofi, F., Abbate, R., Gensini, G.F., Casini, A., Accruing evidence on benefits of adherence to the Mediterranean diet on health: an updated systematic review and meta-analysis. Am. J. Clin.Nutr. 92:5 (2010), 1189–1196.
61. Halliwell, B., Oxidative stress and neurodegeneration: where are we now?. J. Neurochem. 97:6 (2006), 1634–1658.
62. Pannala, A., Rice-Evans, C.A., Halliwell, B., Singh, S., Inhibition of peroxynitrite-mediated tyrosine nitration by catechin polyphenols. Biochem. Biophys. Res. Commun. 232:1 (1997), 164–168.
63. Russo, A., Acquaviva, R., Campisi, A., Sorrenti, V., Di Giacomo, C., Virgata, G., Barcellona, M., Vanella, A., Bioflavonoids as antiradicals, antioxidants and DNA cleavage protectors. Cell Biol. Toxicol. 16:2 (2000), 91–98.
64. Visioli, F., Bellomo, G., Galli, C., Free radical-scavenging properties of olive oil polyphenols. Biochem. Biophys. Res. Commun. 247:1 (1998), 60–64.
65. Williams, R.J., Spencer, J.P., Rice-Evans, C., Flavonoids: antioxidants or signalling molecules?. Free Radic. Biol. Med. 36:7 (2004), 838–849.
66. Mandel, S.A., Amit, T., Kalfon, L., Reznichenko, L., Weinreb, O., Youdim, M.B., Cell signaling pathways and iron chelation in the neurorestorative activity of green tea polyphenols: special reference to epigallocatechin gallate (EGCG). J. Alzheimer's Dis. 15:2 (2008), 211–222.
67. Schroeter, H., Bahia, P., Spencer, J.P., Sheppard, O., Rattray, M., Cadenas, E., Rice-Evans, C., Williams, R.J., (-) Epicatechin stimulates ERK-dependent cyclic AMP response element activity and up-regulates GluR2 in cortical neurons. J. Neurochem. 101:6 (2007), 1596–1606.
68. Bliss, T.V., Collingridge, G.L., A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:6407 (1993), 31–39.
69. Malenka, R.C., Bear, M.F., LTP and LTD: an embarrassment of riches. Neuron 44:1 (2004), 5–21.
70. Bramham, C.R., Wells, D.G., Dendritic mRNA: transport, translation and function. Nat. Rev. Neurosci. 8:10 (2007), 776–789.
71. Martin, K.C., Barad, M., Kandel, E.R., Local protein synthesis and its role in synapse-specific plasticity. Curr. Opin. Neurobiol. 10:5 (2000), 587–592.
72. Spencer, J.P., Vauzour, D., Rendeiro, C., Flavonoids and cognition: the molecular mechanisms underlying their behavioural effects. Arch. Biochem. Biophys. 492:1 (2009), 1–9.
73. Spencer, J.P., The impact of flavonoids on memory: physiological and molecular considerations. Chem. Soc. Rev. 38:4 (2009), 1152–1161.
74. Vauzour, D., Vafeiadou, K., Rice-Evans, C., Williams, R.J., Spencer, J.P., Activation of pro-survival Akt and ERK1/2 signalling pathways underlie the anti-apoptotic effects of flavanones in cortical neurons. J. Neurochem. 103:4 (2007), 1355–1367.
75. Llorens, F., Garcia, L., Itarte, E., Gómez, N., Apigenin and LY294002 prolong EGF-stimulated ERK1/2 activation in PC12 cells but are unable to induce full differentiation. FEBS Lett. 510:3 (2002), 149–153.
76. Schroeter, H., Boyd, C., Spencer, J.P., Williams, R.J., Cadenas, E., Rice-Evans, C., MAPK signaling in neurodegeneration: influences of flavonoids and of nitric oxide. Neurobiol. Aging 23:5 (2002), 861–880.
77. Bourtchuladze, R., Frenguelli, B., Blendy, J., Cioffi, D., Schutz, G., Silva, A.J., Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element-binding protein. Cell 79:1 (1994), 59–68.
78. Impey, S., Smith, D.M., Obrietan, K., Donahue, R., Wade, C., Storm, D.R., Stimulation of cAMP response element (CRE)-mediated transcription during contextual learning. Nat. Neurosci. 1:7 (1998), 595–601.
79. Finkbeiner, S., Tavazoie, S.F., Maloratsky, A., Jacobs, K.M., Harris, K.M., Greenberg, M.E., CREB: a major mediator of neuronal neurotrophin responses. Neuron 19:5 (1997), 1031–1047.
80. Ramirez, M.R., Izquierdo, I., Raseira, M.d.C.B., J.Â, Zuanazzi, Barros, D., Henriques, A.T., Effect of lyophilised Vaccinium berries on memory, anxiety and locomotion in adult rats. Pharmacol. Res. 52:6 (2005), 457–462.
81. Maher, P., Akaishi, T., Abe, K., Flavonoid fisetin promotes ERK-dependent long-term potentiation and enhances memory. Proc. Natl. Acad. Sci. 103:44 (2006), 16568–16573.
82. Yin, Y., Edelman, G.M., Vanderklish, P.W., The brain-derived neurotrophic factor enhances synthesis of Arc in synaptoneurosomes. Proc. Natl. Acad. Sci. 99:4 (2002), 2368–2373.
83. Waltereit, R., Dammermann, B., Wulff, P., Scafidi, J., Staubli, U., Kauselmann, G., Bundman, M., Kuhl, D., Arg3. 1/Arc mRNA induction by Ca2+ and cAMP requires protein kinase A and mitogen-activated protein kinase/extracellular regulated kinase activation. J. Neurosci. 21:15 (2001), 5484–5493.
84. Szekely, C.A., Thorne, J.E., Zandi, P.P., Ek, M., Messias, E., Breitner, J.C., Goodman, S.N., Nonsteroidal anti-inflammatory drugs for the prevention of Alzheimer's disease: a systematic review. Neuroepidemiology 23:4 (2004), 159–169.
85. González-Gallego, J., García-Mediavilla, M.V., Sánchez-Campos, S., Tuñón, M.J., Fruit polyphenols, immunity and inflammation. Br. J. Nutr. 104:S3 (2010), S15–S27.
86. Panahi, Y., Darvishi, B., Ghanei, M., Jowzi, N., Beiraghdar, F., Varnamkhasti, B.S., Molecular mechanisms of curcumins suppressing effects on tumorigenesisangiogenesis and metastasis, focusing on NF-κB pathway. Cytokine Growth Factor Rev. 28 (2016), 21–29.
87. Kao, T.-K., Ou, Y.-C., Raung, S.-L., Lai, C.-Y., Liao, S.-L., Chen, C.-J., Inhibition of nitric oxide production by quercetin in endotoxin/cytokine-stimulated microglia. Life Sci. 86:9 (2010), 315–321.
88. Breteler, M.M., Vascular risk factors for Alzheimer's disease: an epidemiologic perspective. Neurobiol. Aging 21:2 (2000), 153–160.
89. Schroeter, H., Heiss, C., Balzer, J., Kleinbongard, P., Keen, C.L., Hollenberg, N.K., Sies, H., Kwik-Uribe, C., Schmitz, H.H., Kelm, M., (–)-Epicatechin mediates beneficial effects of flavanol-rich cocoa on vascular function in humans. Proc. Natl. Acad. Sci. U. S. A. 103:4 (2006), 1024–1029.
90. Gage, F.H., Mammalian neural stem cells. Science 287:5457 (2000), 1433–1438.
91. Van Praag, H., Lucero, M.J., Yeo, G.W., Stecker, K., Heivand, N., Zhao, C., Yip, E., Afanador, M., Schroeter, H., Hammerstone, J., Plant-derived flavanol (−) epicatechin enhances angiogenesis and retention of spatial memory in mice. J. Neurosci. 27:22 (2007), 5869–5878.
92. Xie, Y., Yang, W., Chen, X., Xiao, J., Inhibition of flavonoids on acetylcholine esterase: binding and structure–activity relationship. Food Funct. 5:10 (2014), 2582–2589.
93. Oinonen, P.P., Jokela, J.K., Hatakka, A.I., Vuorela, P.M., Linarin, a selective acetylcholinesterase inhibitor from Mentha arvensis. Fitoterapia 77:6 (2006), 429–434.
94. Fan, P., Hay, A.-E., Marston, A., Hostettmann, K., Acetylcholinesterase-inhibitory activity of linarin from Buddleja davidii, structure-activity relationships of related flavonoids, and chemical investigation of Buddleja nitida. Pharm. Biol. 46:9 (2008), 596–601.
95. Khan, M.T.H., Orhan, I., Şenol, F., Kartal, M., Şener, B., Dvorská, M., Šmejkal, K., Šlapetová, T., Cholinesterase inhibitory activities of some flavonoid derivatives and chosen xanthone and their molecular docking studies. Chem. Biol. Interact. 181:3 (2009), 383–389.
96. Jung, M., Park, M., Acetylcholinesterase inhibition by flavonoids from Agrimonia pilosa. Molecules 12:9 (2007), 2130–2139.
97. Heo, H.J., Kim, M.-J., Lee, J.-M., Choi, S.J., Cho, H.-Y., Hong, B., Kim, H.-K., Kim, E., Shin, D.-H., Naringenin from Citrus junos has an inhibitory effect on acetylcholinesterase and a mitigating effect on amnesia. Dement. Geriatr. Cogn. Disord. 17:3 (2004), 151–157.
98. Kumar, A., Prakash, A., Dogra, S., Naringin alleviates cognitive impairment, mitochondrial dysfunction and oxidative stress induced by D-galactose in mice. Food Chem. Toxicol. 48:2 (2010), 626–632.
99. He, X.-L., Zhou, W.-Q., Bi, M.-G., Du, G.-H., Neuroprotective effects of icariin on memory impairment and neurochemical deficits in senescence-accelerated mouse prone 8 (SAMP8) mice. Brain Res. 1334 (2010), 73–83.
100. Cui, Y.-M., Ao, M.-Z., Li, W., Yu, L.-J., Effect of glabridin from Glycyrrhiza glabra on learning and memory in mice. Planta Med. 74:04 (2008), 377–380.
101. Lee, Y.-B., Lee, H.J., Won, M.H., Hwang, I.K., Kang, T.-C., Lee, J.-Y., Nam, S.-Y., Kim, K.-S., Kim, E., Cheon, S.-H., Soy isoflavones improve spatial delayed matching-to-place performance and reduce cholinergic neuron loss in elderly male rats. J. Nutr. 134:7 (2004), 1827–1831.
102. Guo, A.J., Xie, H.Q., Choi, R.C., Zheng, K.Y., Bi, C.W., Xu, S.L., Dong, T.T., Tsim, K.W., Galangin, a flavonol derived from Rhizoma Alpiniae Officinarum, inhibits acetylcholinesterase activity in vitro. Chem. Biol. Interact. 187:1 (2010), 246–248.
103. Lou, H., Fan, P., Perez, R.G., Lou, H., Neuroprotective effects of linarin through activation of the PI3 K/Akt pathway in amyloid-β-induced neuronal cell death. Bioorg. Med.Chem. 19:13 (2011), 4021–4027.
104. Kennedy, D.O., Wightman, E.L., Herbal extracts and phytochemicals: plant secondary metabolites and the enhancement of human brain function. Adv. Nutr.: Int. Rev. J. 2:1 (2011), 32–50.
105. Hernandez, M.F., Falé, P.L., Araújo, M.E.M., Serralheiro, M.L.M., Acetylcholinesterase inhibition and antioxidant activity of the water extracts of several Hypericum species. Food Chem. 120:4 (2010), 1076–1082.
106. Fu, X., Zhang, J., Guo, L., Xu, Y., Sun, L., Wang, S., Feng, Y., Gou, L., Zhang, L., Liu, Y., Protective role of luteolin against cognitive dysfunction induced by chronic cerebral hypoperfusion in rats. Pharmacol. Biochem. Behav. 126 (2014), 122–130.
107. Liu, Y., Fu, X., Lan, N., Li, S., Zhang, J., Wang, S., Li, C., Shang, Y., Huang, T., Zhang, L., Luteolin protects against high fat diet-induced cognitive deficits in obesity mice. Behav. Brain Res. 267 (2014), 178–188.
108. Rezai-Zadeh, K., Douglas Shytle, R., Bai, Y., Tian, J., Hou, H., Mori, T., Zeng, J., Obregon, D., Town, T., Tan, J., Flavonoid-mediated presenilin-1 phosphorylation reduces Alzheimer's disease β-amyloid production. J. Cell. Mol. Med. 13:3 (2009), 574–588.
109. Zhou, F., Chen, S., Xiong, J., Li, Y., Qu, L., Luteolin reduces zinc-induced tau phosphorylation at Ser262/356 in an ROS-dependent manner in SH-SY5Y cells. Biol. Trace Elem. Res. 149:2 (2012), 273–279.
110. Yu, T.-X., Zhang, P., Guan, Y., Wang, M., Zhen, M.-Q., Protective effects of luteolin against cognitive impairment induced by infusion of Aβ peptide in rats. Int. J. Clin. Exp. Pathol., 8(6), 2015, 6740.
111. Mandel, S., Reznichenko, L., Amit, T., Youdim, M.B., Green tea polyphenol (−)-epigallocatechin-3-gallate protects rat PC12 cells from apoptosis induced by serum withdrawal. Neurotox. Res. 5:6 (2003), 419–424.
112. Choi, Y.-T., Jung, C.-H., Lee, S.-R., Bae, J.-H., Baek, W.-K., Suh, M.-H., Park, J., Park, C.-W., Suh, S.-I., The green tea polyphenol (−)-epigallocatechin gallate attenuates β-amyloid-induced neurotoxicity in cultured hippocampal neurons. Life Sci. 70:5 (2001), 603–614.
113. Levites, Y., Amit, T., Mandel, S., Youdim, M.B., Neuroprotection and neurorescue against Aβ toxicity and PKC-dependent release of nonamyloidogenic soluble precursor protein by green tea polyphenol (−)-epigallocatechin-3-gallate. FASEB J. 17:8 (2003), 952–954.
114. Lin, C.-L., Chen, T.-F., Chiu, M.-J., Way, T.-D., Lin, J.-K., Epigallocatechin gallate (EGCG) suppresses β-amyloid-induced neurotoxicity through inhibiting c-Abl/FE65 nuclear translocation and GSK3β activation. Neurobiol. Aging 30:1 (2009), 81–92.
115. Farooqui, T., Farooqui, A.A., Neuroprotective Effects of Phytochemicals in Neurological Disorders. 2017, John Wiley & Sons.
116. Mandel, S., Youdim, M.B., Catechin polyphenols: neurodegeneration and neuroprotection in neurodegenerative diseases. Free Radic. Biol. Med. 37:3 (2004), 304–317.
117. Marder, M., Viola, H., Wasowski, C., Fernández, S., Medina, J.H., Paladini, A.C., 6-Methylapigenin and hesperidin: new valeriana flavonoids with activity on the CNS. Pharmacol. Biochem. Behav. 75:3 (2003), 537–545.
118. Matsuzaki, K., Yamakuni, T., Hashimoto, M., Haque, A.M., Shido, O., Mimaki, Y., Sashida, Y., Ohizumi, Y., Nobiletin restoring β-amyloid-impaired CREB phosphorylation rescues memory deterioration in Alzheimer's disease model rats. Neurosci. Lett. 400:3 (2006), 230–234.
119. Rainey-Smith, S., Schroetke, L.-W., Bahia, P., Fahmi, A., Skilton, R., Spencer, J.P., Rice-Evans, C., Rattray, M., Williams, R.J., Neuroprotective effects of hesperetin in mouse primary neurones are independent of CREB activation. Neurosci. Lett. 438:1 (2008), 29–33.
120. Darbandi, N., Ramezani, M., Khodagholi, F., Noori, M., Kaempferol promotes memory retention and density of hippocampal CA1 neurons in intra-cerebroventricular STZ-induced experimental AD model in Wistar rats. Biologija, 62(3), 2016.
121. Haddadi, R., Nayebi, A.M., Farajniya, S., Brooshghalan, S.E., Sharifi, H., Silymarin improved 6-OHDA-induced motor impairment in hemi-parkisonian rats: behavioral and molecular study. DARU J. Pharm. Sci., 22(1), 2014, 1.
122. Baluchnejadmojarad, T., Roghani, M., Mafakheri, M., Neuroprotective effect of silymarin in 6-hydroxydopamine hemi-parkinsonian rat: involvement of estrogen receptors and oxidative stress. Neurosci. Lett. 480:3 (2010), 206–210.
123. Lu, P., Mamiya, T., Lu, L., Mouri, A., Zou, L., Nagai, T., Hiramatsu, M., Ikejima, T., Nabeshima, T., Silibinin prevents amyloid β peptide-induced memory impairment and oxidative stress in mice. Br. J. Pharmacol. 157:7 (2009), 1270–1277.
124. Echeverry, C., Arredondo, F., Abin-Carriquiry, J.A., Midiwo, J.O., Ochieng, C., Kerubo, L., Dajas, F., Pretreatment with natural flavones and neuronal cell survival after oxidative stress: a structure- activity relationship study. J. Agric. Food Chem. 58:4 (2010), 2111–2115.
125. Karuppagounder, S., Madathil, S., Pandey, M., Haobam, R., Rajamma, U., Mohanakumar, K., Quercetin up-regulates mitochondrial complex-I activity to protect against programmed cell death in rotenone model of Parkinson's disease in rats. Neuroscience 236 (2013), 136–148.
126. Rodrigues, J., Rinaldo, D., dos Santos, L.C., Vilegas, W., An unusual C6–C6″ linked flavonoid from Miconia cabucu (Melastomataceae). Phytochemistry 68:13 (2007), 1781–1784.
127. Sabogal-Guáqueta, A.M., Muñoz-Manco, J.I., Ramírez-Pineda, J.R., Lamprea-Rodriguez, M., Osorio, E., Cardona-Gómez, G.P., The flavonoid quercetin ameliorates Alzheimer's disease pathology and protects cognitive and emotional function in aged triple transgenic Alzheimer's disease model mice. Neuropharmacology 93 (2015), 134–145.
128. Leem, E., Nam, J.H., Jeon, M.-T., Shin, W.-H., Won, S.-Y., Park, S.-J., Choi, M.-S., Jin, B.K., Jung, U.J., Kim, S.R., Naringin protects the nigrostriatal dopaminergic projection through induction of GDNF in a neurotoxin model of Parkinson's disease. J. Nutr. Biochem. 25:7 (2014), 801–806.
129. Kim, H.-J., Song, J.Y., Park, H.J., Park, H.-K., Yun, D.H., Chung, J.-H., Naringin protects against rotenone-induced apoptosis in human neuroblastoma SH-SY5Y cells. Korean J. Physiol. Pharmacol. 13:4 (2009), 281–285.
130. Ghofrani, S., Joghataei, M.-T., Mohseni, S., Baluchnejadmojarad, T., Bagheri, M., Khamse, S., Roghani, M., Naringenin improves learning and memory in an Alzheimer's disease rat model: insights into the underlying mechanisms. Eur. J. Pharmacol. 764 (2015), 195–201.
131. Badruzzaman Khan, M., MOSHAHID KHAN, M., KHAN, A., EJAZ AHMED, M., ISHRAT, T., TABASSUM, R., VAIBHAV, K., AHMAD, A., ISLAM, F., Naringenin ameliorates Alzheimer's disease (AD)-type neurodegeneration with cognitive impairment (AD-TNDCI) caused by the intracerebroventricular-streptozotocin in rat model. Neurochem. Int. 61:7 (2012), 1081–1093.
132. Lee, E., Park, H.R., Ji, S.T., Lee, Y., Lee, J., Baicalein attenuates astroglial activation in the 1-methyl-4-phenyl-1, 2, 3, 4‐tetrahydropyridine-induced Parkinson's disease model by downregulating the activations of nuclear factor‐κB, ERK, and JNK. J. Neurosci. Res. 92:1 (2014), 130–139.
133. Lee, H.J., Noh, Y.H., Kim, Y.S., Kim, K.Y., Chung, Y.H., Lee, W.B., Kim, S.S., Baicalein attenuates 6-hydroxydopamine-induced neurotoxicity in SH-SY5Y cells. Eur. J. Cell Biol. 84:11 (2005), 897–905.
134. Wei, D., Tang, J., Bai, W., Wang, Y., Zhang, Z., Ameliorative effects of baicalein on an amyloid-β induced alzheimer's disease rat model: a proteomics study. Curr. Alzheimer Res. 11:9 (2014), 869–881.
135. Zhang, S.Q., Obregon, D., Ehrhart, J., Deng, J., Tian, J., Hou, H., Giunta, B., Sawmiller, D., Tan, J., Baicalein reduces β‐amyloid and promotes nonamyloidogenic amyloid precursor protein processing in an Alzheimer's disease transgenic mouse model. J. Neurosci. Res. 91:9 (2013), 1239–1246.
136. Zhao, L., Wang, J.-l., Wang, Y.-r., Fa, X.-z., Apigenin attenuates copper-mediated β-amyloid neurotoxicity through antioxidation, mitochondrion protection and MAPK signal inactivation in an AD cell model. Brain Res. 1492 (2013), 33–45.
137. Souza, C.S., Paulsen, B.S., Devalle, S., Costa, S.L., Borges, H.L., Rehen, S.K., Commitment of human pluripotent stem cells to a neural lineage is induced by the pro-estrogenic flavonoid apigenin. Adv. Regener. Biol., 2, 2015.
138. Nones, J., Costa, A.P., Leal, R.B., Gomes, F.C.A., Trentin, A.G., The flavonoids hesperidin and rutin promote neural crest cell survival. Cell Tissue Res. 350:2 (2012), 305–315.
139. Wang, R., Sun, Y., Huang, H., Wang, L., Chen, J., Shen, W., Rutin, a natural flavonoid protects PC12 cells against sodium nitroprusside-induced neurotoxicity through activating PI3 K/Akt/mTOR and ERK1/2 Pathway. Neurochem. Res. 40:9 (2015), 1945–1953.
140. Yu, X.-L., Li, Y.-N., Zhang, H., Su, Y.-J., Zhou, W.-W., Zhang, Z.-P., Wang, S.-W., Xu, P.-X., Wang, Y.-J., Liu, R.-T., Rutin inhibits amylin-induced neurocytotoxicity and oxidative stress. Food Funct. 6:10 (2015), 3296–3306.
141. Simonyi, A., Chen, Z., Jiang, J., Zong, Y., Chuang, D.Y., Gu, Z., Lu, C.-H., Fritsche, K.L., Greenlief, C.M., Rottinghaus, G.E., Inhibition of microglial activation by elderberry extracts and its phenolic components. Life Sci. 128 (2015), 30–38.
142. Xu, P.-x., Wang, S.-w., Yu, X.-l., Su, Y.-j., Wang, T., Zhou, W.-w., Zhang, H., Wang, Y.-j., Liu, R.-t., Rutin improves spatial memory in Alzheimer's disease transgenic mice by reducing Aβ oligomer level and attenuating oxidative stress and neuroinflammation. Behav. Brain Res. 264 (2014), 173–180.
143. Moghbelinejad, S., Nassiri-Asl, M., Farivar, T.N., Abbasi, E., Sheikhi, M., Taghiloo, M., Farsad, F., Samimi, A., Hajiali, F., Rutin activates the MAPK pathway and BDNF gene expression on beta-amyloid induced neurotoxicity in rats. Toxicol. Lett. 224:1 (2014), 108–113.
144. Bagheri, M., Joghataei, M.-T., Mohseni, S., Roghani, M., Genistein ameliorates learning and memory deficits in amyloid β (1–40) rat model of Alzheimer's disease. Neurobiol. Learn. Mem. 95:3 (2011), 270–276.
145. Tarozzi, A., Morroni, F., Merlicco, A., Bolondi, C., Teti, G., Falconi, M., Cantelli-Forti, G., Hrelia, P., Neuroprotective effects of cyanidin 3-O-glucopyranoside on amyloid beta (25–35) oligomer-induced toxicity. Neurosci. Lett. 473:2 (2010), 72–76.
146. Spuch, C., Navarro, C., Liposomes for targeted delivery of active agents against neurodegenerative diseases (Alzheimer's disease and Parkinson's disease). J. Drug Deliv., 2011, 2011.
147. Pasic, M.D., Diamandis, E.P., McLaurin, J., Holtzman, D.M., Schmitt-Ulms, G., Quirion, R., Alzheimer disease: advances in pathogenesis, diagnosis, and therapy. Clin. Chem. 57:5 (2011), 664–669.
148. Constantinides, P.P., Chaubal, M.V., Shorr, R., Advances in lipid nanodispersions for parenteral drug delivery and targeting. Adv. Drug Deliv. Rev. 60:6 (2008), 757–767.
149. Priprem, A., Watanatorn, J., Sutthiparinyanont, S., Phachonpai, W., Muchimapura, S., Anxiety and cognitive effects of quercetin liposomes in rats. Nanomed.: Nanotechnol. Biol. Med. 4:1 (2008), 70–78.
150. Mishra, S., Palanivelu, K., The effect of curcumin (turmeric) on Alzheimer's disease: an overview. Ann. Indian Acad. Neurol., 11(1), 2008, 13.
151. Doggui, S., Sahni, J.K., Arseneault, M., Dao, L., Ramassamy, C., Neuronal uptake and neuroprotective effect of curcumin-loaded PLGA nanoparticles on the human SK-N-SH cell line. J. Alzheimer's Dis. 30:2 (2012), 377–392.
152. Kakkar, V., Mishra, A.K., Chuttani, K., Kaur, I.P., Proof of concept studies to confirm the delivery of curcumin loaded solid lipid nanoparticles (C-SLNs) to brain. Int. J. Pharm. 448:2 (2013), 354–359.
153. Frozza, R.L., Bernardi, A., Hoppe, J.B., Meneghetti, A.B., Battastini, A.M., Pohlmann, A.R., Guterres, S.S., Salbego, C., Lipid-core nanocapsules improve the effects of resveratrol against Aβ-induced neuroinflammation. J. Biomed. Nanotechnol. 9:12 (2013), 2086–2104.
154. Frozza, R.L., Bernardi, A., Paese, K., Hoppe, J.B., d. Silva, T., Battastini, A.M., Pohlmann, A.R., Guterres, S.S., Salbego, C., Characterization of trans-resveratrol-loaded lipid-core nanocapsules and tissue distribution studies in rats. J. Biomed. Nanotechnol. 6:6 (2010), 694–703.