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Modulation of Neurotrophic Signaling Pathways by Polyphenols

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Modulation of Neurotrophic Signaling Pathways by Polyphenols Journal name: Drug Design, Development and Therapy Article Designation: Review Year: 2016 Volume: 10 Drug Design, Development and Therapy Dovepress Running head verso: Moosavi et al Running head recto: Neurotrophic effects of polyphenols open access to scientific and medical research DOI: http://dx.doi.org/10.2147/DDDT.S96936 Open Access Full Text Article REVIEW Modulation of neurotrophic signaling pathways by polyphenols Fatemeh Moosavi1,2 Abstract: Polyphenols are an important class of phytochemicals, and several lines of evidence Razieh Hosseini1,2 have demonstrated their beneficial effects in the context of a number of pathologies including Luciano Saso3 neurodegenerative disorders such as Alzheimer’s and Parkinson’s disease. In this report, we Omidreza Firuzi1 review the studies on the effects of polyphenols on neuronal survival, growth, proliferation and differentiation, and the signaling pathways involved in these neurotrophic actions. Several 1Medicinal and Natural Products Chemistry Research Center, Shiraz polyphenols including flavonoids such as baicalein, daidzein, luteolin, and nobiletin as well as University of Medical Sciences, Shiraz, nonflavonoid polyphenols such as auraptene, carnosic acid, curcuminoids, and hydroxycinnamic 2 Iran; Department of Pharmacology, acid derivatives including caffeic acid phentyl ester enhance neuronal survival and promote School of Veterinary Medicine, Shiraz University, Shiraz, Iran; 3Department neurite outgrowth in vitro, a hallmark of neuronal differentiation. Assessment of underlying of Physiology and Pharmacology mechanisms, especially in PC12 neuronal-like cells, reveals that direct agonistic effect on tro- “Vittorio Erspamer”, Sapienza pomyosin receptor kinase (Trk) receptors, the main receptors of neurotrophic factors including University of Rome, Rome, Italy nerve growth factor (NGF) and brain-derived neurotrophic factor (BDNF) explains the action of few polyphenols such as 7,8-dihydroxyflavone. However, several other polyphenolic com- pounds activate extracellular signal-regulated kinase (ERK) and phosphoinositide 3-kinase (PI3K)/Akt pathways. Increased expression of neurotrophic factors in vitro and in vivo is the mechanism of neurotrophic action of flavonoids such as scutellarin, daidzein, genistein, and fisetin, while compounds like apigenin and ferulic acid increase cyclic adenosine monophosphate response element-binding protein (CREB) phosphorylation. Finally, the antioxidant activity of polyphenols reflected in the activation of Nrf2 pathway and the consequent upregulation of detoxification enzymes such as heme oxygenase-1 as well as the contribution of these effects to the neurotrophic activity have also been discussed. In conclusion, a better understanding of the neurotrophic effects of polyphenols and the concomitant modulations of signaling pathways is useful for designing more effective agents for management of neurodegenerative diseases. Keywords: flavonoids, hydroxycinnamic acids, neuroprotective, neurodegeneration, Trk Introduction Polyphenolic compounds Polyphenols are an important group of phytochemicals that are abundantly present in food sources.1 Several lines of evidence have demonstrated beneficial effects of these compounds in the context of several pathologies,2–8 and it has been repeatedly shown that consumption of foods rich in phenolic compounds can lower the risk of Correspondence: Omidreza Firuzi 9,10 Medicinal and Natural Products several diseases. Chemistry Research Center, Polyphenols have been reported to be of therapeutic value in neurodegen- Shiraz University of Medical Sciences, erative diseases,11–13 hypertension14 and other cardiovascular diseases,15 cancer,16–18 1 Neshat Street, Shiraz 71348, PO Box 71345-3388, Iran inflammation,19,20 diabetes,21 dyslipidemia,22–24 allergy, and immune system diseases.25,26 Tel +98 713 230 3872 They have also been reported to have a role in the prevention of different types of cancer Fax +98 713 233 2225 Email [email protected] ranging from liver,4 prostate,27 and colorectal28 cancer to lymphoblastic leukemia.29 submit your manuscript | www.dovepress.com Drug Design, Development and Therapy 2016:10 23–42 23 Dovepress © 2016 Moosavi et al. This work is published and licensed by Dove Medical Press Limited. The full terms of this license are available at https://www.dovepress.com/terms.php and incorporate the Creative Commons Attribution – Non Commercial (unported, v3.0) License (http://creativecommons.org/licenses/by-nc/3.0/). By accessing the work you http://dx.doi.org/10.2147/DDDT.S96936 hereby accept the Terms. Non-commercial uses of the work are permitted without any further permission from Dove Medical Press Limited, provided the work is properly attributed. For permission for commercial use of this work, please see paragraphs 4.2 and 5 of our Terms (https://www.dovepress.com/terms.php). Moosavi et al Dovepress Neurodegenerative disorders such as Alzheimer’s, epigallocatechin–gallate (EGCG) significantly improved Parkinson’s, and Huntington’s disease represent rapidly cognitive deficits in individuals with Down syndrome.40 growing causes of disability and death, which have pro- Several studies have demonstrated that different poly- found economic and social implications; nonetheless, only phenolics with neuroprotective activity, such as EGCG,41,42 few effective disease-modifying therapies are available for epicatechin,43 curcumin,44 resveratrol,45 quercetin,46 and these diseases.30–32 Recent research has shown that certain citrus flavonoids (naringenin and hesperetin),47 are able to polyphenols may have considerable neuroprotective effects cross the blood–brain barrier and therefore indicate that in different brain pathologies including neurodegenerative these compounds localize within the brain tissue and may diseases.8,11,33,34 Polyphenols from grape juice administered well exert neuroprotective and neuromodulatory actions in to older adult subjects have been shown to ameliorate the the settings of different brain pathologies. mild cognitive impairment.35 Similarly, Witte et al36 have Polyphenolic compounds can be classified into different shown that administration of resveratrol, a polyphenol pres- groups as described in Figure 1.1 Among them, flavonoids ent in wine, in older adults significantly improves memory constitute a major subgroup, which are highly present performance, indicating potential strategies to maintain in fruits and vegetables and possess several biological brain health during aging. Assessment of cognitive per- activities.1 formance in middle-aged individuals has indicated that Polyphenols have been extensively studied for their consumption of different polyphenols such as catechins, antioxidant action48–52 and some of their beneficial effects, flavonols, and hydroxybenzoic acids is strongly associated including neuroprotective activity, have been attributed to with language and verbal memory.37 Other studies have also this capacity.53–55 The neuroprotective effect of polyphenols shown similar effects of other polyphenols on cognitive against the diseases of nervous system has also been addressed function and memory in older individuals, who are at risk in a number of studies.56–59 The aim of this review, however, for neurodegenerative diseases.38,39 In another human study, is to extensively address the alterations of signaling pathways 3KHQROLF FRPSRXQGV 6WLOEHQHV /LJQDQV +\GUR[\FLQQDPLF +\GUR[\EHQ]RLF +2 )ODYRQRLGV + &2 &+ 2+ DFLGV DFLGV 5 +2 &+2+ 2 2+ +2 2 +2 2 +2 2&+ 2+ 2+ 5 2+ ([DPSOHV ([DPSOHV ([DPSOH ([DPSOH *DOOLFDFLG )HUXOLFDFLG 5HVYHUDWURO 6HFRLVRODULFLUHVLQRO &DIIHLFDFLG 9DQLOOLFDFLG $QWKRF\DQLGLQV )ODYDQROV )ODYDQRQHV )ODYRQROV )ODYRQHV ,VRIODYRQHV 5 5 5 5 5 2+ 5 5 5 5 +2 2 +2 2 +2 2 +2 2 +2 2 +2 2 5 5 5 5 5 2+ 5 2 2+ 2+ 2+ 2+ 2+ 2 2+ 2 2+ 2+ 2 ([DPSOHV ([DPSOHV ([DPSOHV ([DPSOHV ([DPSOHV ([DPSOHV &\DQLGLQ &DWHFKLQV 1DULJHQLQ 4XHUFHWLQ $SLJHQLQ *HQLVWHLQ 3HODUJRQLGLQ (SLFDWHFKLQV +HVSHULWLQ .DHPSIHURO /XWHROLQ 'DLG]HLQ Figure 1 Main classes of polyphenols and their chemical structures. 24 submit your manuscript | www.dovepress.com Drug Design, Development and Therapy 2016:10 Dovepress Dovepress Neurotrophic effects of polyphenols involved in the neurotrophic action of polyphenols that lead the nervous system.63 Several studies have shown that to neuronal survival, growth, proliferation, and differentia- polyphenolic compounds enhance neuronal survival in tion. The other aspects of neuroprotective activity of these serum-deprived conditions. Lin et al64 showed that in neu- compounds, which are mainly ascribed to the antioxidant ronal-like PC12 cells, luteolin (3′,4′,5,7-tetrahydroxyflavone, action and mitigation of oxidative stress, have been reviewed Figure 2) attenuates serum withdrawal-induced cytotoxicity. elsewhere5,7,8,60–62 and are only briefly mentioned here. It Other examples of neuroprotectants that exerted prosurvival should also be mentioned that in in vitro studies, which are action in PC12 cells include curcuminoids, the predominant the main focus of this report, supraphysiological doses of polyphenolic compounds of Curcuma longa Linn.;65 EGCG polyphenols may have been used and, therefore, caution (Figure 2), the major polyphenol of green tea extract;66 caffeic should be exerted in extrapolation of these data to in vivo acid phenethyl ester (CAPE, Figure 3), an active component conditions.56 The structures of some of the most highly studied of propolis;67 5-hydroxy-3,6,7,8,3′,4′-hexamethoxyflavone neurotrophic polyphenols are depicted in
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