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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Polyphenols: Multipotent Therapeutic Agents in Neurodegenerative Diseases</title>
<author><name sortKey="Bhullar, Khushwant S" sort="Bhullar, Khushwant S" uniqKey="Bhullar K" first="Khushwant S." last="Bhullar">Khushwant S. Bhullar</name>
<affiliation><nlm:aff id="I1">Department of Environmental Sciences, Faculty of Agriculture, Dalhousie University, Truro, NS, Canada B2N 5E3</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Rupasinghe, H P Vasantha" sort="Rupasinghe, H P Vasantha" uniqKey="Rupasinghe H" first="H. P. Vasantha" last="Rupasinghe">H. P. Vasantha Rupasinghe</name>
<affiliation><nlm:aff id="I1">Department of Environmental Sciences, Faculty of Agriculture, Dalhousie University, Truro, NS, Canada B2N 5E3</nlm:aff>
</affiliation>
</author>
</titleStmt>
<publicationStmt><idno type="wicri:source">PMC</idno>
<idno type="pmid">23840922</idno>
<idno type="pmc">3690243</idno>
<idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3690243</idno>
<idno type="RBID">PMC:3690243</idno>
<idno type="doi">10.1155/2013/891748</idno>
<date when="2013">2013</date>
<idno type="wicri:Area/Pmc/Corpus">000C63</idno>
<idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000C63</idno>
</publicationStmt>
<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Polyphenols: Multipotent Therapeutic Agents in Neurodegenerative Diseases</title>
<author><name sortKey="Bhullar, Khushwant S" sort="Bhullar, Khushwant S" uniqKey="Bhullar K" first="Khushwant S." last="Bhullar">Khushwant S. Bhullar</name>
<affiliation><nlm:aff id="I1">Department of Environmental Sciences, Faculty of Agriculture, Dalhousie University, Truro, NS, Canada B2N 5E3</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Rupasinghe, H P Vasantha" sort="Rupasinghe, H P Vasantha" uniqKey="Rupasinghe H" first="H. P. Vasantha" last="Rupasinghe">H. P. Vasantha Rupasinghe</name>
<affiliation><nlm:aff id="I1">Department of Environmental Sciences, Faculty of Agriculture, Dalhousie University, Truro, NS, Canada B2N 5E3</nlm:aff>
</affiliation>
</author>
</analytic>
<series><title level="j">Oxidative Medicine and Cellular Longevity</title>
<idno type="ISSN">1942-0900</idno>
<idno type="eISSN">1942-0994</idno>
<imprint><date when="2013">2013</date>
</imprint>
</series>
</biblStruct>
</sourceDesc>
</fileDesc>
<profileDesc><textClass></textClass>
</profileDesc>
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<front><div type="abstract" xml:lang="en"><p>Aging leads to numerous transitions in brain physiology including synaptic dysfunction and disturbances in cognition and memory. With a few clinically relevant drugs, a substantial portion of aging population at risk for age-related neurodegenerative disorders require nutritional intervention. Dietary intake of polyphenols is known to attenuate oxidative stress and reduce the risk for related neurodegenerative diseases such as Alzheimer's disease (AD), stroke, multiple sclerosis (MS), Parkinson's disease (PD), and Huntington's disease (HD). Polyphenols exhibit strong potential to address the etiology of neurological disorders as they attenuate their complex physiology by modulating several therapeutic targets at once. Firstly, we review the advances in the therapeutic role of polyphenols in cell and animal models of AD, PD, MS, and HD and activation of drug targets for controlling pathological manifestations. Secondly, we present principle pathways in which polyphenol intake translates into therapeutic outcomes. In particular, signaling pathways like PPAR, Nrf2, STAT, HIF, and MAPK along with modulation of immune response by polyphenols are discussed. Although current polyphenol researches have limited impact on clinical practice, they have strong evidence and testable hypothesis to contribute clinical advances and drug discovery towards age-related neurological disorders.</p>
</div>
</front>
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<pmc article-type="review-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Oxid Med Cell Longev</journal-id>
<journal-id journal-id-type="iso-abbrev">Oxid Med Cell Longev</journal-id>
<journal-id journal-id-type="publisher-id">OXIMED</journal-id>
<journal-title-group><journal-title>Oxidative Medicine and Cellular Longevity</journal-title>
</journal-title-group>
<issn pub-type="ppub">1942-0900</issn>
<issn pub-type="epub">1942-0994</issn>
<publisher><publisher-name>Hindawi Publishing Corporation</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">23840922</article-id>
<article-id pub-id-type="pmc">3690243</article-id>
<article-id pub-id-type="doi">10.1155/2013/891748</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Review Article</subject>
</subj-group>
</article-categories>
<title-group><article-title>Polyphenols: Multipotent Therapeutic Agents in Neurodegenerative Diseases</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Bhullar</surname>
<given-names>Khushwant S.</given-names>
</name>
<xref ref-type="aff" rid="I1"></xref>
</contrib>
<contrib contrib-type="author"><name><surname>Rupasinghe</surname>
<given-names>H. P. Vasantha</given-names>
</name>
<xref ref-type="aff" rid="I1"></xref>
<xref ref-type="corresp" rid="cor1">*</xref>
</contrib>
</contrib-group>
<aff id="I1">Department of Environmental Sciences, Faculty of Agriculture, Dalhousie University, Truro, NS, Canada B2N 5E3</aff>
<author-notes><corresp id="cor1">*H. P. Vasantha Rupasinghe: <email>vrupasinghe@dal.ca</email>
</corresp>
<fn fn-type="other"><p>Academic Editor: Nilanjana Maulik</p>
</fn>
</author-notes>
<pub-date pub-type="ppub"><year>2013</year>
</pub-date>
<pub-date pub-type="epub"><day>6</day>
<month>6</month>
<year>2013</year>
</pub-date>
<volume>2013</volume>
<elocation-id>891748</elocation-id>
<history><date date-type="received"><day>10</day>
<month>3</month>
<year>2013</year>
</date>
<date date-type="accepted"><day>29</day>
<month>4</month>
<year>2013</year>
</date>
</history>
<permissions><copyright-statement>Copyright © 2013 K. S. Bhullar and H. P. V. Rupasinghe.</copyright-statement>
<copyright-year>2013</copyright-year>
<license license-type="open-access"><license-p>This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.</license-p>
</license>
</permissions>
<abstract><p>Aging leads to numerous transitions in brain physiology including synaptic dysfunction and disturbances in cognition and memory. With a few clinically relevant drugs, a substantial portion of aging population at risk for age-related neurodegenerative disorders require nutritional intervention. Dietary intake of polyphenols is known to attenuate oxidative stress and reduce the risk for related neurodegenerative diseases such as Alzheimer's disease (AD), stroke, multiple sclerosis (MS), Parkinson's disease (PD), and Huntington's disease (HD). Polyphenols exhibit strong potential to address the etiology of neurological disorders as they attenuate their complex physiology by modulating several therapeutic targets at once. Firstly, we review the advances in the therapeutic role of polyphenols in cell and animal models of AD, PD, MS, and HD and activation of drug targets for controlling pathological manifestations. Secondly, we present principle pathways in which polyphenol intake translates into therapeutic outcomes. In particular, signaling pathways like PPAR, Nrf2, STAT, HIF, and MAPK along with modulation of immune response by polyphenols are discussed. Although current polyphenol researches have limited impact on clinical practice, they have strong evidence and testable hypothesis to contribute clinical advances and drug discovery towards age-related neurological disorders.</p>
</abstract>
</article-meta>
</front>
<body><sec id="sec1"><title>1. Introduction</title>
<p>Neurodegenerative disorders such as Alzheimer's disease (AD), stroke, and Parkinson's disease (PD) represent a major clinical problem in the developed countries [<xref ref-type="bibr" rid="B1">1</xref>
, <xref ref-type="bibr" rid="B2">2</xref>
] and are major economic burdens for health care systems [<xref ref-type="bibr" rid="B3">3</xref>
]. Dietary [<xref ref-type="bibr" rid="B4">4</xref>
], genetic, and molecular factors [<xref ref-type="bibr" rid="B5">5</xref>
] are important determinants in progression and intervention of neurodegenerative diseases. AD is a common cause of dementia and mortality in the United States. Total numbers of reported deaths due to AD have increased in past years, and it is among 10 leading causes of deaths in the United States [<xref ref-type="bibr" rid="B6">6</xref>
]. Amyloid-<italic>β</italic>
(A<italic>β</italic>
) peptides derived from amyloid precursor protein (APP) via <italic>γ</italic>
-secretase and <italic>β</italic>
-secretase cleavage are hallmarks of AD [<xref ref-type="bibr" rid="B7">7</xref>
]. Cellular prion protein (PrP(C)) [<xref ref-type="bibr" rid="B8">8</xref>
] and oxidative stress [<xref ref-type="bibr" rid="B9">9</xref>
] mediate A<italic>β</italic>
neurotoxicity, and the latter contributes to neuronal death by lowering intracellular glutathione. Along with A<italic>β</italic>
, tau protein alteration in neuronal microtubules also contributes to the pathology of AD [<xref ref-type="bibr" rid="B10">10</xref>
]. Abnormal phosphorylation and aggregation of tau protein leads to neural dysfunction and leads to pathological events which cause neuronal dysfunction in AD [<xref ref-type="bibr" rid="B11">11</xref>
]. Failed clearance of A<italic>β</italic>
aggregates resulting from impaired autophagy may also contribute to AD [<xref ref-type="bibr" rid="B12">12</xref>
]. AD is also characterized by elevated peripheral blood cytokine concentrations for interleukin- (IL-) 6, tumor necrosis factor alpha (TNF-<italic>α</italic>
), IL-1<italic>β</italic>
, transforming growth factor beta (TGF-<italic>β</italic>
), IL-12, and IL-18 suggestive of a pro-inflammatory response in AD pathology [<xref ref-type="bibr" rid="B13">13</xref>
]. </p>
<p>Multiple sclerosis (MS) is another neurodegenerative disease characterized by chronic inflammation accompanied by demyelination of neurons in brain [<xref ref-type="bibr" rid="B14">14</xref>
]. MS is characterized by symptoms like mood disorder, fatigue, vision changes, muscle weakness, and motor changes [<xref ref-type="bibr" rid="B15">15</xref>
]. Chemokines like IL-17, chemokine (C-C motif) ligand 17 (CCL17), and CCL20 are suggested as major mediators in MS neuroinflammation and pathology [<xref ref-type="bibr" rid="B16">16</xref>
]. </p>
<p>Stroke is the third leading cause of mortality, loss of cognitive functions, and heavy socioeconomic burden in the United States [<xref ref-type="bibr" rid="B17">17</xref>
]. Similar to MS, stroke or cerebral ischemia is a pathological condition accompanied by inflammation and immune system disease [<xref ref-type="bibr" rid="B18">18</xref>
]. One minute of cerebral ischemia is estimated to destroy approximately 2 million neurons and 14 million synapses [<xref ref-type="bibr" rid="B19">19</xref>
]. Like AD and MS, inflammatory cytokines including TNF-<italic>α</italic>
and IL-1 and IL-6 play modulatory role in stroke pathology [<xref ref-type="bibr" rid="B20">20</xref>
]. Transcription factor, nuclear factor kappa B (NF<italic>κ</italic>
B), is an important regulator in pathology of inflammation and neuronal cell survival, as its activation leads to cell death in cerebral ischemia [<xref ref-type="bibr" rid="B21">21</xref>
]. </p>
<p>PD is a progressive neurodegenerative disease; its familial forms are characterized by mutations of six genes including clinically important ATP13A3 resulting in cognitive impairment and depression [<xref ref-type="bibr" rid="B22">22</xref>
]. Some PD cases also involve changes in micro-RNA and <italic>α</italic>
-synuclein level in patients [<xref ref-type="bibr" rid="B23">23</xref>
]. Like other neurodegenerative diseases, PD also involves elevated levels of proinflammatory cytokines monocyte chemoattractant protein-1 (MCP-1), CCL-5, macrophage inflammatory protein-1<italic>α</italic>
(MIP-1<italic>α</italic>
), IL-8, interferon-gamma (IFN<italic>γ</italic>
), IL-1<italic>β</italic>
, and TNF<italic>α</italic>
[<xref ref-type="bibr" rid="B24">24</xref>
]. After examining cytokines in 52 PD patients, researchers [<xref ref-type="bibr" rid="B25">25</xref>
] suggested involvement of TNF-<italic>α</italic>
in production and maintenance of nonmotor symptoms. Mitochondrial dysfunction also plays an important role in pathogenesis of PD [<xref ref-type="bibr" rid="B26">26</xref>
] similar to AD [<xref ref-type="bibr" rid="B27">27</xref>
], MS [<xref ref-type="bibr" rid="B28">28</xref>
], and stroke (CI) [<xref ref-type="bibr" rid="B29">29</xref>
].</p>
<p>Huntington's disease (HD) is another neurological disorder causing cognitive impairment, accompanied by oxidative stress and mitochondrial dysfunction. It results from increased number of CAG triplet nucleotide repeats and expanded polyglutamine region of huntingtin protein [<xref ref-type="bibr" rid="B30">30</xref>
]. HD pathology leads to elevated levels of chemokines like eotaxin-3, MIP-1<italic>β</italic>
, eotaxin, MCP-1, and MCP-4 [<xref ref-type="bibr" rid="B31">31</xref>
]. </p>
<p>The pathophysiology of neurological disorders is also accompanied by alterations in electrical activity of neurons at cellular level. The voltage gated ion channels are required for action potential generation and its propagation in neurons, and their dysfunction contributes to pathology of neurodegenerative diseases. The brain electrical activity is significantly changed in AD and dementia leading to impaired verbal memory and cognitive skills [<xref ref-type="bibr" rid="B32">32</xref>
]. The Kv3 subfamily of K<sup>+</sup>
channel subunits, which possess ability of fast repolarization of action potential [<xref ref-type="bibr" rid="B33">33</xref>
], are compromised and slowed down in AD [<xref ref-type="bibr" rid="B34">34</xref>
]. The upregulation of the K(v)1.3 potassium channel also plays important role in immunopathogenesis of multiple sclerosis and presents therapeutic option by blocking Kv channels [<xref ref-type="bibr" rid="B35">35</xref>
]. As sodium channels (Na<sub>v</sub>
1.8, Na<sub>v</sub>
1.5) play an important role in electrical activity of neurons, their overloading is thus an important mediator in axonal degeneration in MS [<xref ref-type="bibr" rid="B36">36</xref>
, <xref ref-type="bibr" rid="B37">37</xref>
]. Such electric disturbances are also found in PD [<xref ref-type="bibr" rid="B38">38</xref>
] which impose energy burden by Ca<sup>2+</sup>
entry through L type voltage-dependent channels [<xref ref-type="bibr" rid="B39">39</xref>
]. Similarly, sodium and potassium channel abnormalities are proposed to contribute to HD pathogenesis [<xref ref-type="bibr" rid="B40">40</xref>
, <xref ref-type="bibr" rid="B41">41</xref>
].</p>
<p>There are a few clinically relevant medicines and therapies available for AD, HD, MS, PD, and stroke. A few clinically active, yet expensive, options such as acetylcholinesterase inhibitors, interferon <italic>β</italic>
-1a, levodopa, tetrabenazine, and tissue type plasminogen activator (tPA) are available for AD [<xref ref-type="bibr" rid="B42">42</xref>
], MS [<xref ref-type="bibr" rid="B43">43</xref>
], PD [<xref ref-type="bibr" rid="B44">44</xref>
], HD [<xref ref-type="bibr" rid="B45">45</xref>
], and stroke [<xref ref-type="bibr" rid="B46">46</xref>
], respectively. In wake of these pathologies and limited clinical treatments, alternative and preventive therapeutics are required which can control the occurrence and progression of neurodegenerative diseases. All the neurodegenerative diseases discussed above have the common features of pathogenesis which include cytokine changes, genetic alterations, immunomodulation, inflammation, mitochondrial dysfunction, oxidative stress, prions, and protein dysfunction. Recent research has shown that dietary polyphenols target the pathological manifestations of neurological disorders with their ability to cross blood-brain barrier [<xref ref-type="bibr" rid="B47">47</xref>
] as they control neuronal disease pathogenesis at a molecular and symptomatic level by targeting these common features of neurodegeneration pathology. Polyphenols are naturally occurring phytochemicals found in fruits and vegetables, exhibiting strong neuroprotective properties [<xref ref-type="bibr" rid="B48">48</xref>
]. Important dietary sources of polyphenols include apples, berries, cocoa, herbs, red wines, seeds, onions, and tea [<xref ref-type="bibr" rid="B49">49</xref>
]. Dietary polyphenols have also been implicated in prevention of oxidative damage and LDL oxidation [<xref ref-type="bibr" rid="B50">50</xref>
–<xref ref-type="bibr" rid="B52">52</xref>
]. This review briefly outlines the pharmacological role of polyphenols in preventing neurodegenerative diseases based on the most recent scientific literature (<xref ref-type="fig" rid="fig1">Figure 1</xref>
).</p>
</sec>
<sec id="sec2"><title>2. Polyphenols and Pharmacological Properties</title>
<sec id="sec2.1"><title>2.1. Alzheimer's Disease and Dementia</title>
<p>Polyphenols exhibit neuroprotective properties including therapeutic action in AD and dementia. Green and white tea extracts have been shown to inhibit acetylcholinesterase which indicates their potential in treatment of age-related disorders such as AD [<xref ref-type="bibr" rid="B53">53</xref>
]. Green tea polyphenols protect primary rat cortical neurons against A<italic>β</italic>
-induced cytotoxicity [<xref ref-type="bibr" rid="B54">54</xref>
]. In mouse model studies [<xref ref-type="bibr" rid="B55">55</xref>
], polyphenols of grapes improved cognitive functions in mouse model of AD. As well, epicatechin metabolite 3′-<italic>O</italic>
-methyl-epicatechin-5-<italic>O</italic>
-<italic>β</italic>
-glucuronide had improved synaptic transmission through cyclic adenosine monophosphate (cAMP) response element binding protein. In transgenic mice model studies, grape seed polymeric polyphenol extract has been shown to inhibit oligomerization of A<italic>β</italic>
peptides and contributed to reduction in cognitive impairments in transgenic mice [<xref ref-type="bibr" rid="B56">56</xref>
]. A similar study showed that polyphenols of grapes exhibited potential in neutralizing abnormal folding of tau proteins [<xref ref-type="bibr" rid="B57">57</xref>
]. Earlier studies using animal models [<xref ref-type="bibr" rid="B58">58</xref>
, <xref ref-type="bibr" rid="B59">59</xref>
] also confirm anti-A<italic>β</italic>
action of grape seed polyphenols. </p>
<p>Resveratrol, a polyphenol abundant in grapes and red wines, inhibited A<italic>β</italic>
42 fibril formation [<xref ref-type="bibr" rid="B60">60</xref>
] and protected from A<italic>β</italic>
neurotoxicity by inhibiting inducible nitric oxide synthase inhibition [<xref ref-type="bibr" rid="B61">61</xref>
]. Resveratrol, with possibly high bioavailability in lipid core nanocapsules, exhibited therapeutic action in AD [<xref ref-type="bibr" rid="B62">62</xref>
]. Flavonoid fisetin and its analogues also inhibited A<italic>β</italic>
fibril formation and have emerged as new drug candidates for AD treatment [<xref ref-type="bibr" rid="B63">63</xref>
]. Morin (2′,3,4′,5,7-pentahydroxyflavone) has shown to prevent neuronal cell death by protecting neurons against tau hyperphosphorylation induced by A<italic>β</italic>
[<xref ref-type="bibr" rid="B64">64</xref>
]. Similarly, in transgenic mouse model studies [<xref ref-type="bibr" rid="B65">65</xref>
], tannic acid has displayed the attenuation of A<italic>β</italic>
deposition by decreasing cleavage of <italic>β</italic>
-carboxyl terminal amyloid precursor protein (APP) fragment and controlled neural inflammation. A flavonoid, 7,8-dihydroxyflavone, has been shown to improve cognitive abilities in 5XFAD transgenic mouse model of AD by activation of tyrosine receptor kinase B leading to reduction in <italic>β</italic>
-secretase enzyme levels and amyloid beta (A<italic>β</italic>
) synthesis [<xref ref-type="bibr" rid="B66">66</xref>
]. Similarly, liquiritigenin improved memory in Tg2576 mice model of AD, as it attenuated astrocytosis and decreased the Notch-2 expression as the latter can contribute to neuronal decay [<xref ref-type="bibr" rid="B67">67</xref>
]. Unlike resveratrol, quercetin and rutin not only inhibited A<italic>β</italic>
formation but also disaggregated A<italic>β</italic>
fibrils in AD studies [<xref ref-type="bibr" rid="B68">68</xref>
]. Both compounds also prevented scopolamine-induced amnesia in animal model systems [<xref ref-type="bibr" rid="B69">69</xref>
]; however, resveratrol did not reverse scopolamine-induced deficit [<xref ref-type="bibr" rid="B70">70</xref>
]. Rutin has been found to control oxidative stress, malondialdehyde, and glutathione disulfide formation in SH-SY5Y neuroblastoma cells. Rutin has also attenuated the inflammatory cascade by decreasing cytokines like TNF-<italic>α</italic>
and IL-1<italic>β</italic>
[<xref ref-type="bibr" rid="B71">71</xref>
]. Ferulic acid, a phenolic acid, has also exhibited higher neuroprotection against A<italic>β</italic>
toxicity than quercetin [<xref ref-type="bibr" rid="B72">72</xref>
]. Recent research findings have shown that polyphenols have therapeutic relevance in both cell and animal model studies. The ability of polyphenols to improve synaptic transmission by elevating cAMP, target multiple signaling pathways, and reduce A<italic>β</italic>
toxicity suggests their therapeutic utility for age-related disorders like AD and dementia.</p>
</sec>
<sec id="sec2.2"><title>2.2. Multiple Sclerosis</title>
<p>Multiple sclerosis is a neurodegenerative disease characterized by autoimmune-mediated demyelination in the CNS resulting in paralysis and cognitive deficits. MS therapies can reduce inflammation and downregulate immune function [<xref ref-type="bibr" rid="B73">73</xref>
]. Resveratrol, a silent mating type information regulation 2 homolog1 (SIRT1) activator, has exhibited prevention of neural loss without immunosuppression in experimental autoimmune encephalomyelitis (EAE) model of MS [<xref ref-type="bibr" rid="B74">74</xref>
]. Pharmaceutical grade formulation of resveratrol SRT501 was found to attenuate neural damage in EAE through SIRT1 activation [<xref ref-type="bibr" rid="B75">75</xref>
]. Cell culture studies [<xref ref-type="bibr" rid="B76">76</xref>
] have also shown SIRT1-mediated neuroprotection by resveratrol. Quercetin was found to control immune response via modulation of IL-1<italic>β</italic>
and TNF-<italic>α</italic>
and reduced the proliferation of peripheral blood mononuclear cells isolated from multiple sclerosis patients [<xref ref-type="bibr" rid="B77">77</xref>
]. Epigallocatechin-3-gallate (EGCG) exhibited neuroprotective effects by modulating neuroinflammation and attenuating neural damage [<xref ref-type="bibr" rid="B78">78</xref>
]. Quercetin [<xref ref-type="bibr" rid="B79">79</xref>
], apple polyphenols [<xref ref-type="bibr" rid="B80">80</xref>
], myricetin, and piceatannol [<xref ref-type="bibr" rid="B81">81</xref>
] have also activated SIRT1, thus exhibiting potential in MS treatment. Earlier studies have also shown [<xref ref-type="bibr" rid="B82">82</xref>
] that flavonoids limit demyelination in MS suggesting their potential against neuro-inflammation and related disorders. Preclinical data has shown that polyphenols exhibit potential to block neural inflammation and damage by activation of SIRT1 pathway along with modulation of inflammatory cytokines. The potential of polyphenols on limiting demyelination makes them prospective therapeutics in age-related MS and amyotrophic lateral sclerosis (ALS).</p>
</sec>
<sec id="sec2.3"><title>2.3. Ischemic Stroke</title>
<p>Various epidemiological studies suggest that diet rich in polyphenols can extend neuroprotection and lower the risk and severity of stroke, the third leading cause of mortality [<xref ref-type="bibr" rid="B83">83</xref>
]. Experimental evidence using rodent and cellular models also indicates neuroprotective potential of dietary polyphenols in cerebral ischemia. Green tea polyphenol, EGCG, has exhibited neuroprotective action by downregulation of matrix metalloproteinases (MMP) in mice model of cerebral ischemia [<xref ref-type="bibr" rid="B84">84</xref>
]. Green tea polyphenols have also been found to protect neurons against hypoxia-induced ischemic injury by controlling inflammation cascade and attenuating decline in transmembrane potential [<xref ref-type="bibr" rid="B85">85</xref>
]. Quercetin has been found to attenuate ischemic injury by controlling acid-sensing ion channel led calcium dysregulation and lipid peroxidation in neurons [<xref ref-type="bibr" rid="B86">86</xref>
]. Another study with similar experimentation has supported neuroprotective role of quercetin, based on its ability to block sodium channels [<xref ref-type="bibr" rid="B87">87</xref>
]. Quercetin with similar antioxidant therapy to green tea polyphenols has reduced the level of MMP-9 and attenuated blood-brain barrier disruption in cerebral ischemia (CI) studies [<xref ref-type="bibr" rid="B88">88</xref>
]. Researchers have also hypothesized neuroprotective action of quercetin in CI to be based on its inhibitory action against MMP [<xref ref-type="bibr" rid="B89">89</xref>
]. Rutin has been found to control neural damage in CI through downregulation of p53, a protein which leads to necrosis in stroke [<xref ref-type="bibr" rid="B90">90</xref>
]. It has also shown the attenuation of glutathione peroxidase, glutathione reductase, and inflammatory cytokines in rodent model of ischemic stroke [<xref ref-type="bibr" rid="B91">91</xref>
]. In addition, resveratrol has been found to extend protection against ischemic injury by improving brain energy metabolism and controlling oxidative stress during ischemia injury in animal model studies [<xref ref-type="bibr" rid="B92">92</xref>
], along with the modulation of release of multiple therapeutic neurotransmitters and neuromodulators during ischemic injury [<xref ref-type="bibr" rid="B93">93</xref>
]. The flavonoid fisetin has shown neuroprotective action during cerebral ischemia as it stopped infiltration of macrophages and dendritic cells into ischemic hemisphere, thus controlling neural inflammation and damage [<xref ref-type="bibr" rid="B94">94</xref>
]. Another flavonoid baicalin has been shown to reduce ischemic stroke damage by targeting multiple therapeutic targets like MMP-9 [<xref ref-type="bibr" rid="B95">95</xref>
], caspase-3, oxidative stress [<xref ref-type="bibr" rid="B96">96</xref>
], and p38 mitogen-activated protein kinase (MAPK) [<xref ref-type="bibr" rid="B97">97</xref>
] and by downregulating toll-like receptor (TLR2/4) pathway [<xref ref-type="bibr" rid="B98">98</xref>
]. The experimental data reveals that polyphenols may prevent, attenuate, or slow down, via multiple mechanisms, the course of stroke and age-related neural disorders. Since the risk for stroke increases with age, consumption of polyphenol rich diet seems to be an important preventive strategy. </p>
</sec>
<sec id="sec2.4"><title>2.4. Parkinson's Disease (PD)</title>
<p>PD is a neurodegenerative disease accompanied by inflammation and oxidative stress resulting in loss of dopaminergic neurons in the substantia nigra [<xref ref-type="bibr" rid="B99">137</xref>
]. Polyphenols with their ability to attenuate oxidative stress and inflammation present therapeutic option in neurodegenerative disease. Resveratrol has been shown to inhibit the loss of dopaminergic neurons in rat model of PD [<xref ref-type="bibr" rid="B76">76</xref>
]. Resveratrol has also been shown to reduce neural inflammation in PD by lowering mRNA levels of cyclooxygenase-2 (COX-2) and TNF-<italic>α</italic>
mRNA in the substantia nigra [<xref ref-type="bibr" rid="B100">100</xref>
] along with attenuation of oxidative stress, lipid peroxidation, and protein carbonyl (PC) in rat model of PD [<xref ref-type="bibr" rid="B101">138</xref>
]. Oxyresveratrol has demonstrated attenuation of neural damage in SH-SY5Y cells by elevating levels of SIRT1 and downregulating expression of caspase-3, c-Jun N-terminal kinase (JNK), and c-Jun transcription factors [<xref ref-type="bibr" rid="B102">139</xref>
]. Ferulic acid, like oxyresveratrol, has demonstrated neuroprotective effect via downregulation of JNK pathway [<xref ref-type="bibr" rid="B103">140</xref>
]. Quercetin administration to neurons attenuated 1-methyl-4-phenylpyridinium (MMP) evoked microglia activation, which is a precursor for PD pathogenesis [<xref ref-type="bibr" rid="B104">124</xref>
]. Studies have also shown that quercetin promises neuroprotection in PD mice model by stimulating glutathione peroxidase (GPx), superoxide dismutase (SOD), Na(<sup>+</sup>
), and K(<sup>+</sup>
)-ATPase [<xref ref-type="bibr" rid="B105">141</xref>
]. Quercetin suppressed cell death in PD cell model while its metabolite quercetin-3-<italic>O</italic>
-<italic>β</italic>
-glucuronide, due to its low absorption, did not affect cell viability [<xref ref-type="bibr" rid="B106">142</xref>
]. Another study showed that conversion of quercetin metabolites to its aglycone in neural cells is essential for neuroprotective activity [<xref ref-type="bibr" rid="B107">143</xref>
]. These studies had shown consistent results as compared to a contradictory report [<xref ref-type="bibr" rid="B108">144</xref>
] which showed that quercetin had no neuroprotective role in PD cells and rat models. Other polyphenols such as baicalein [<xref ref-type="bibr" rid="B109">145</xref>
], kaempferol [<xref ref-type="bibr" rid="B110">146</xref>
], caffeic acid [<xref ref-type="bibr" rid="B111">147</xref>
], and EGCG [<xref ref-type="bibr" rid="B112">148</xref>
] have been shown to extend neuroprotection in PD studies. Similarly, polyphenolic extracts from various plants have also exhibited pharmacological role in PD studies. For instance, polyphenols-rich mulberry fruit extracts have shown antioxidant and antiapoptotic effect in SH-SY5Y cells by modulating caspase-3, B-cell lymphoma (Bcl-2), and BCL2-associated X protein (Bax) [<xref ref-type="bibr" rid="B113">149</xref>
].</p>
</sec>
<sec id="sec2.5"><title>2.5. Huntington's Disease</title>
<p>CAG triplet nucleotide repeats and expanded polyglutamine region of huntingtin protein form basis of HD [<xref ref-type="bibr" rid="B30">30</xref>
]. Polyphenols hold pharmacological relevance, as they are associated with numerous benefits including antiaging, anti-inflammatory, and anticancer effects. Resveratrol has been found to exhibit positive effects in transgenic mouse model of HD via SIRT1 activation of peroxisome proliferative activated receptor, gamma, and coactivator 1 alpha (PGC-1<italic>α</italic>
) signaling pathway [<xref ref-type="bibr" rid="B76">76</xref>
]. Studies have further demonstrated the Ras-extracellular signal-regulated kinase activation by resveratrol and fisetin as the basis for neuroprotection in models of HD [<xref ref-type="bibr" rid="B114">150</xref>
]. Likewise, hesperidin and naringenin, abundant in citrus fruits, induced neuroprotection in rats possibly via nitric oxide synthase (NOS) inhibition [<xref ref-type="bibr" rid="B115">151</xref>
]. Curcumin has been shown to control Huntington aggregates and improve various transgene-dependent parameters, thereby promising therapeutic action in HD [<xref ref-type="bibr" rid="B116">152</xref>
]. Grape and green tea polyphenols have also exhibited potential for treating/preventing HD disease pathogenesis [<xref ref-type="bibr" rid="B117">153</xref>
, <xref ref-type="bibr" rid="B118">154</xref>
]. The overall preclinical data suggests that polyphenols extend strong neuroprotection through genetic and immunological modulation, thus promising clinical prevention or delay of neurological disorders like PD and HD.</p>
</sec>
</sec>
<sec id="sec3"><title>3. Polyphenols and Oxidative Stress</title>
<p>A large body of literature supports the antioxidant potential of polyphenols against oxidative stress. Resveratrol is a potent antioxidant <italic>in vitro</italic>
[<xref ref-type="bibr" rid="B119">155</xref>
] and <italic>in vivo</italic>
as it attenuates oxidative stress in both animal [<xref ref-type="bibr" rid="B120">156</xref>
] and various cell model studies [<xref ref-type="bibr" rid="B121">157</xref>
]. Resveratrol has been shown to extend antioxidant effect by reducing the production of reactive oxygen species (ROS) and superoxide ions [<xref ref-type="bibr" rid="B122">158</xref>
]. Similarly, quercetin has also shown protection against oxidative stress and related disorders [<xref ref-type="bibr" rid="B123">159</xref>
]. In a variety of cell and disease models, quercetin has been shown to engage in various signaling pathways to attenuate oxidative stress and exhibit pharmacological properties [<xref ref-type="bibr" rid="B51">51</xref>
, <xref ref-type="bibr" rid="B124">114</xref>
]. Polyphenol-rich green tea and its principal constituent EGCG were found to ameliorate oxidative stress in various studies [<xref ref-type="bibr" rid="B125">160</xref>
, <xref ref-type="bibr" rid="B126">161</xref>
]. Other polyphenols such as puerarin [<xref ref-type="bibr" rid="B127">162</xref>
], baicalin [<xref ref-type="bibr" rid="B128">163</xref>
], and phloridzin [<xref ref-type="bibr" rid="B129">136</xref>
] also attenuated oxidative stress in various disease models. Apart from <italic>in vitro</italic>
and<italic> in vivo</italic>
evidence, sufficient clinical evidence also suggests the antioxidant potential of polyphenols. A clinical study [<xref ref-type="bibr" rid="B130">164</xref>
] showed that polyphenol-rich diet reduced LDL oxidation and modulated cluster of differentiation 40-ligand (CD40L) gene expression, thus controlling atherogenesis and inflammation in humans. Polyphenol-rich fruit extracts have been shown to control free radicals and ROS. Polyphenol-rich bilberry juice was found to decrease oxidative stress and inflammatory markers in humans [<xref ref-type="bibr" rid="B131">165</xref>
]. A 13-year long clinical study indicated that higher intake of antioxidant polyphenols including flavonoids and phenolic acids helps in improving memory and has potential for inhibiting brain aging [<xref ref-type="bibr" rid="B132">166</xref>
]. Antioxidant-rich polyphenol supplementation as beverage has also been found to decrease plasma total homocysteine, thus contributing to attenuation of AD pathology [<xref ref-type="bibr" rid="B133">167</xref>
]. It can be concluded that polyphenols are strong antioxidants <italic>in vitro </italic>
and<italic> in vivo </italic>
in both animal models and humans. Clinical translation of polyphenols as antioxidant therapy is a promising approach to attenuate oxidative damage due to aging and age-related disorders. </p>
</sec>
<sec id="sec4"><title>4. Polyphenols and Signal Transduction Pathways</title>
<sec id="sec4.1"><title>4.1. Akt/P13K/mTOR Pathway</title>
<p>Resveratrol has exhibited neuroprotection against brain ischemia through P13K/Akt pathway by downregulating the expression of glycogen synthase kinase 3 (GSK-3<italic>β</italic>
) and cAMP response element binding (CREB) proteins [<xref ref-type="bibr" rid="B134">99</xref>
]. Resveratrol increased cAMP and modulated Akt pathway in cell model studies [<xref ref-type="bibr" rid="B108">144</xref>
]. Baicalein also protects against ischemia through P13K/Akt pathway [<xref ref-type="bibr" rid="B135">126</xref>
]. The scientific evidence suggests therapeutic intervention by polyphenols via P13K/Akt pathway (<xref ref-type="table" rid="tab1">Table 1</xref>
).</p>
</sec>
<sec id="sec4.2"><title>4.2. NF<italic>κ</italic>
B Pathway</title>
<p>NF<italic>κ</italic>
B is an important mediator in inflammatory process and contributes to A<italic>β</italic>
toxicity. Flavonoids and other dietary polyphenols have shown neuroprotective effects in neuronal ischemia through NF<italic>κ</italic>
B pathway. Flavonoids, including kaempferol, quercetin, acacetin, apigenin, and luteolin, inhibit A<italic>β</italic>
1-40 and A<italic>β</italic>
1-42 via NF<italic>κ</italic>
B pathway downregulation [<xref ref-type="bibr" rid="B136">101</xref>
]. Similarly, soybean isoflavone had reversed memory impairment in rats through decrease in NF<italic>κ</italic>
B expression [<xref ref-type="bibr" rid="B137">102</xref>
]. Other flavonoids such as resveratrol and baicalin inhibit A<italic>β</italic>
-induced neural inflammation via a mechanism involving downregulation of NF<italic>κ</italic>
B signaling pathway [<xref ref-type="bibr" rid="B138">103</xref>
, <xref ref-type="bibr" rid="B139">168</xref>
]. Activation of NF<italic>κ</italic>
B is an important event in ischemic injury and contributes to both inflammation and cell death [<xref ref-type="bibr" rid="B21">21</xref>
]. Silymarin, a flavonolignan from milk thistle (<italic>Silybum marianum</italic>
), has protected against cerebral ischemia by inhibiting signal transducer and activating transcription (STAT-1) pathway and NF<italic>κ</italic>
B [<xref ref-type="bibr" rid="B140">105</xref>
]. Tetrahydroxystilbene glucoside from <italic>Polygonum</italic>
multiforum has protected neurons from cerebral ischemia by activating SIRT1 and inhibiting NF<italic>κ</italic>
B signaling pathway in neurons [<xref ref-type="bibr" rid="B58">58</xref>
]. Quercetin administration has also protected rat brain against oxidative stress and hypoxia-induced damage through NF<italic>κ</italic>
B inhibition [<xref ref-type="bibr" rid="B141">106</xref>
]. Similarly, catechin hydrate and fisetin have been shown to protect rat brain against ischemic injury and oxidative damage by inhibiting expression of NF<italic>κ</italic>
B and proinflammatory cytokines such as IL-1<italic>β</italic>
and TNF-<italic>α</italic>
[<xref ref-type="bibr" rid="B83">83</xref>
, <xref ref-type="bibr" rid="B94">94</xref>
]. It is observed that recent research advances confirm an immunomodulatory role of polyphenols as they control inflammatory response by inhibiting NF<italic>κ</italic>
B expression. </p>
</sec>
<sec id="sec4.3"><title>4.3. PPAR Pathway</title>
<p>Peroxisome proliferator activated receptor gamma (PPAR gamma) plays a role of a biomarker in cerebral ischemia as CI results in its upregulation and translocation to nucleus from the cytosol. Baicalein has reversed PPAR gamma expression and also suppresses its translocation to nucleus [<xref ref-type="bibr" rid="B142">104</xref>
]. Resveratrol has attenuated the MMP-9 by modulating the peroxisome proliferator activated receptor (PPAR) alpha expression in hypoxia model of neurons [<xref ref-type="bibr" rid="B143">107</xref>
]. Pterostilbene, a resveratrol derivative, has significant effect on the downregulation and normalization of PPAR-<italic>α</italic>
expression in SAMP8 mouse model studies [<xref ref-type="bibr" rid="B144">108</xref>
]. The scientific evidence shows that benefits associated with polyphenols in age-related and other disorders are associated with downregulation of PPAR pathway.</p>
</sec>
<sec id="sec4.4"><title>4.4. Nrf2/ARE/HO1 and HIF-1 Pathway</title>
<p>Nuclear factor (erythroid-derived 2-) like 2 (Nrf2) pathway is also involved in Sestrin2 (Sesn2), also known as Hi95, a p53 target gene expression which leads to encoding of antioxidant proteins [<xref ref-type="bibr" rid="B145">169</xref>
]. Epicatechin has protected neurons against stroke and oxidative stress by upregulation of Nrf2 cascade and heme oxygenase-1 (HO1) enzyme [<xref ref-type="bibr" rid="B146">109</xref>
]. Similarly, resveratrol has also been shown to protecte brain through increased expression of Nrf2, HO-1 expression, and downregulation of apoptotic enzymes like caspase-3 [<xref ref-type="bibr" rid="B147">110</xref>
]. Xanthohumol, a prenylated chalcone, has demonstrated neuroprotective action by inhibiting HIF-1 pathway and it further stopped signal transduction pathway leading to apoptosis by caspases [<xref ref-type="bibr" rid="B148">111</xref>
]. Resveratrol, apart from Nrf2 and HO-1 expression, has protected against ischemic injury in cells by downregulation of mRNA expression of hypoxia inducible factors-1<italic>α</italic>
(HIF-1<italic>α</italic>
) [<xref ref-type="bibr" rid="B149">112</xref>
]. Upregulation of Nrf2 and HO-1 pathways by polyphenols in response to oxidative insult shows protective role of these compounds in brain health and oxidative damage.</p>
</sec>
</sec>
<sec id="sec5"><title>5. Polyphenols and Immune Response</title>
<p>Proinflammatory cytokines and genes contribute to inflammation and neuronal death in various neurological disorders. Most of the therapeutics target cytokines and other immune responses for therapeutic intervention. Polyphenols are well known for their anti-inflammatory activities and thus control neuroinflammation and neural death. EGCG has been found to inhibit expression of monocyte chemotactic protein (MCP-1/CCL2) and IL-1<italic>β</italic>
, thus protecting blood-brain barrier (BBB) integrity during pathological inflammation [<xref ref-type="bibr" rid="B150">170</xref>
]. In another study, EGCG inhibited cytokine and chemokines including IL-1<italic>β</italic>
, IL-6, and MCP-1 [<xref ref-type="bibr" rid="B151">116</xref>
]. Resveratrol has also controlled hippocampal inflammation by reducing expression of MCP-1 mRNA levels [<xref ref-type="bibr" rid="B152">118</xref>
]. Polyphenols, that is, catechin, caffeic acid, and transresveratrol, reduced production of inflammatory markers MCP-1, MIP-1<italic>α</italic>
, MIP-1<italic>β</italic>
, chemokine receptor-1 (CCR1), and CCR2 in vascular wall [<xref ref-type="bibr" rid="B153">119</xref>
]. Polyphenol-rich olive oil controlled inflammation by inhibiting proinflammatory CD40, a costimulatory protein found on antigen presenting cells, gene expression [<xref ref-type="bibr" rid="B130">164</xref>
]. EGCG reduced expression of inflammatory cytokines and chemokines such as chemokine (C-X-C motif) ligand (CXCL10), CCL22, CCL 17, and TGF-<italic>β</italic>
, promising strong neuroprotection in AD and stroke [<xref ref-type="bibr" rid="B154">117</xref>
]. Quercetin has been shown to inhibit proinflammatory cytokines like IL-1<italic>β</italic>
, IL-6, COX-2, CD40, and TNF<italic>α</italic>
receptor-associated factor-1 (TRAF1) [<xref ref-type="bibr" rid="B155">120</xref>
]. A similar study [<xref ref-type="bibr" rid="B156">121</xref>
] showed that quercetin exhibits neuroprotective effect in PC12 cells and zebrafish possibly by downregulating expression of proinflammatory genes like IL-1<italic>β</italic>
and COX-2. Resveratrol also reduced neuroinflammation and improved memory along with IL-1<italic>β</italic>
inhibition [<xref ref-type="bibr" rid="B157">115</xref>
]. Resveratrol has exhibited restoration of BBB integrity and inhibited rising levels of IL-17A, T-helper 17 lymphocytes, and MMP [<xref ref-type="bibr" rid="B158">171</xref>
]. Apple polyphenols have also reduced expression of a wide range of neuroinflammatory markers including IL-1<italic>β</italic>
, IL-6, IL-17, 1L-22, CXCL9, CXCL10, CXCL11, and IFN-<italic>γ</italic>
, thus providing immune-modulatory effects against inflammation [<xref ref-type="bibr" rid="B159">122</xref>
]. Studies have also shown that blueberry and apple polyphenols can attenuate neuroinflammation and improve cognitive impairment, possibly by lowering the expression of IL-1<italic>β</italic>
and TNF<italic>α</italic>
in rat hippocampus [<xref ref-type="bibr" rid="B160">172</xref>
, <xref ref-type="bibr" rid="B161">173</xref>
]. About 20 structurally related flavonoids have been shown to inhibit hypoxia-induced STAT3 tyrosine phosphorylation promoting cell survival [<xref ref-type="bibr" rid="B162">174</xref>
]. Fisetin and quercetin protected neurons against LPS-induced inflammation by inhibiting TNF<italic>α</italic>
production and JNK/Jun phosphorylation [<xref ref-type="bibr" rid="B155">120</xref>
, <xref ref-type="bibr" rid="B102">139</xref>
]. Resveratrol administration during ischemic stroke inhibits neuronal damage along with reduced expression of IL-1<italic>β</italic>
and TNF<italic>α</italic>
[<xref ref-type="bibr" rid="B163">175</xref>
]. Overall, polyphenols modulate immune response in neurodegenerative diseases as they induce expression of antiapoptotic factors, control neuroinflammation, and modulate cell signaling under stress (<xref ref-type="table" rid="tab2">Table 2</xref>
). These features of polyphenols make them strong neuroprotective candidates and support their translation from laboratory to clinical trials.</p>
</sec>
<sec id="sec6"><title>6. Polyphenols and Metal Ion Chelation</title>
<p>Iron and copper play important roles in the generation of ROS through redox cycling and subsequent neurodegeneration. Metal accumulation in brain contributes to pathology of diseases like AD, MS, PD, and HD [<xref ref-type="bibr" rid="B164">176</xref>
, <xref ref-type="bibr" rid="B165">177</xref>
]. EGCG exhibited iron chelating ability in SH-SY5Y neuroblastoma cells along with the inhibition of apoptotic factors like BCL2-associated agonist of cell death (Bad), Bax, and caspase-3 [<xref ref-type="bibr" rid="B166">178</xref>
]. EGCG has exhibited stronger chelation of iron compared to desferrioxamine and increased transferrin receptor protein along with the elevation in mRNA levels in SH-SY5Y neuroblastoma cells [<xref ref-type="bibr" rid="B167">179</xref>
]. Electron paramagnetic resonance studies [<xref ref-type="bibr" rid="B168">180</xref>
] demonstrated the interaction of EGCG and gallic acid as ligands to copper coordination sphere, thus demonstrating Cu modulatory potential of these polyphenols. Also, iron modulation by curcumin in rat brain homogenate has been observed, thus warranting that curcumin-based therapy in AD and PD disease models [<xref ref-type="bibr" rid="B169">181</xref>
]. Curcumin has extended neuroprotection in a rat model of PD against 6-hydroxydopamine treatment through its iron chelating activity and reduced degeneration of neurons [<xref ref-type="bibr" rid="B170">182</xref>
]. Similarly, curcumin's ability to reverse neurodegeneration in hemi-Parkinson's mice model has been shown [<xref ref-type="bibr" rid="B171">183</xref>
]. Apart from iron chelation, NF<italic>κ</italic>
B modulation by curcumin has also contributed to the reduction in 6-OHDA-induced neurodegeneration [<xref ref-type="bibr" rid="B172">184</xref>
]. Rosmarinic acid, a phenolic acid found in Lamiaceae herbs, protected neurons against 6-OHDA treatment by lowering the expression of Bax/Bcl-2 at gene level and decreasing iron level in both MES23.5 dopaminergic cells and rat model of PD [<xref ref-type="bibr" rid="B173">185</xref>
, <xref ref-type="bibr" rid="B174">186</xref>
]. It is evident that polyphenols are potent metal chelators and extend neuroprotection against iron- and copper-induced oxidative stress and neurotoxicity via metal chelation, modulation of signal transduction, oxidative stress, and inflammation.</p>
</sec>
<sec id="sec7"><title>7. Polyphenols and Prions</title>
<p>Prion proteins are involved in neurodegenerative diseases, and their conformational transition forms basis of prion diseases. The pathology of prion proteins has been inhibited by EGCG and ECG, thus exhibiting neuroprotective potential [<xref ref-type="bibr" rid="B175">187</xref>
]. Studies have also confirmed the antiprion activity of resveratrol through autophagy activation in neuroblastoma cells [<xref ref-type="bibr" rid="B176">188</xref>
]. Resveratrol also protected mouse neurons against PG14-PrP (mutant prion protein) expression [<xref ref-type="bibr" rid="B177">189</xref>
]. Curcumin also downregulated the prion pathology in neuroblastoma cells [<xref ref-type="bibr" rid="B178">190</xref>
]. Therefore, polyphenols seem to protect neurons against prion diseases by controlling prion mutation and pathology.</p>
</sec>
<sec id="sec8"><title>8. Polyphenol and Anti Acetylcholinesterase Activity</title>
<p>Pathology of neurodegenerative diseases including AD includes deficiency of neuromediator acetylcholine, thus making acetylcholinesterase (AChE) inhibitors as important clinically relevant drugs in AD and other dementia [<xref ref-type="bibr" rid="B179">191</xref>
]. Black chokeberry extract, a rich source of polyphenols, in combination with lemon juice inhibited AChE [<xref ref-type="bibr" rid="B180">192</xref>
]. The prenylated flavonols from paper mulberry (<italic>Broussonetia papyrifera</italic>
) were potent inhibitors of AChE, thus exhibiting neuroprotective potential [<xref ref-type="bibr" rid="B181">193</xref>
]. Studies have shown that a polyphenol-rich blueberry extract also inhibited AChE activity <italic>in vitro </italic>
[<xref ref-type="bibr" rid="B182">194</xref>
]. Polyphenols extracted from <italic>Paulownia tomentosa </italic>
fruits exhibited inhibitory action against both AChE and butyrylcholinesterase (BChE) [<xref ref-type="bibr" rid="B183">195</xref>
]. Quercetin was found to improve cognitive ability and exhibit neuroprotection against trimethyltin-induced neurotoxicity by inhibiting AChE [<xref ref-type="bibr" rid="B184">196</xref>
]. A report has also shown that quercetin inhibited AChE activity and improved cognitive abilities in streptozotocin-treated mice [<xref ref-type="bibr" rid="B185">197</xref>
]. Quercetin and macluraxanthone, from <italic>Maclura tinctoria</italic>
and Dyer's mulberry, respectively, inhibited both AChE and BChE <italic>in vitro</italic>
by competitive and noncompetitive inhibition, respectively [<xref ref-type="bibr" rid="B179">191</xref>
]. Molecular docking studies [<xref ref-type="bibr" rid="B179">191</xref>
] have indicated the hydrophobic interactions and strong hydrogen bonding of both flavonoids with enzymes as basis of their inhibitory activity. Polyphenols from <italic>Cistus laurifolius </italic>
L. also exhibited cholinesterase inhibitory effects against AChE and BChE, supporting a neuroprotective role of polyphenols [<xref ref-type="bibr" rid="B186">198</xref>
]. A herbal tea from <italic>Paulownia barbatus</italic>
leaves reduced AChE activity by 40% and its principal constituent, natural polyphenol rosmarinic acid, reduces AChE activity by 25% [<xref ref-type="bibr" rid="B187">199</xref>
]. Galangin, a flavonol isolated from rhizome of<italic> Alpiniae officinarum, </italic>
has also exhibited strong AChE inhibition [<xref ref-type="bibr" rid="B188">200</xref>
]. EGCG enhances huperzine A's (acetylcholinesterase inhibitor) effects against AChE as its supplementation leads to 88–91% inhibition [<xref ref-type="bibr" rid="B189">201</xref>
]. Later reports have supported that EGCG supplementation with huperzine A improves cognitive abilities in AD [<xref ref-type="bibr" rid="B190">202</xref>
]. Linarin, a flavonoid found in <italic>Linaria</italic>
species, inhibited AChE activity in neuronal PC12 cells and extended potential for neuroprotection in AD and related disorders [<xref ref-type="bibr" rid="B191">203</xref>
]. All these pieces of evidences suggest that polyphenols are potent AChE and BChE inhibitors, thus warranting neuroprotection and improved cognitive functions in AD and related dementia.</p>
</sec>
<sec id="sec9"><title>9. Polyphenols and Autophagy-Related Proteins </title>
<p>Flavonoids such as hesperetin and hesperidin inhibited A<italic>β</italic>
-induced glucose metabolism impairment in neurons and downregulated A<italic>β</italic>
stimulated autophagy, resulting in improved cognitive functions [<xref ref-type="bibr" rid="B192">204</xref>
]. Kaempferol also protected SH-SY5Y and primary neurons from rotenone toxicity through induction of autophagy [<xref ref-type="bibr" rid="B118">154</xref>
]. Resveratrol exhibited neuroprotective effect by activating AMPK-SIRT1 autophagy pathway in PD cell model studies [<xref ref-type="bibr" rid="B193">205</xref>
]. Brain-related autophagy studies have a wide research gap, and polyphenols have strong potential for inducing neuroprotection via autophagy and its related pathways.</p>
</sec>
<sec id="sec10"><title>10. Polyphenols as Neuronal Mitochondria Medicine</title>
<p>Polyphenols from wine are known to reduce oxidative stress and increase the expression of antioxidant enzymes like catalase, superoxide dismutase, glutathione reductase, and glutathione peroxidase [<xref ref-type="bibr" rid="B194">131</xref>
]. Resveratrol upregulates antiapoptotic Bcl-2 protein and downregulates Bax protein expression [<xref ref-type="bibr" rid="B195">206</xref>
]. Resveratrol also acted as mitochondrial antioxidant by elevating the levels of antioxidants trioredoxin-2 (TRX2) and X-chromosome-linked inhibitor of apoptosis protein [<xref ref-type="bibr" rid="B196">207</xref>
]. Another study has shown that resveratrol increased expression of Bcl-2, thus preventing neuronal apoptosis [<xref ref-type="bibr" rid="B100">100</xref>
]. Similarly, resveratrol controlled oxidative stress in PC12 cells and inhibited mitochondria-mediated apoptosis by downregulating Bax and upregulating Bcl-2 [<xref ref-type="bibr" rid="B149">112</xref>
]. Similarly, lutein has shown protection of mice against ischemic injury by enhancing the Bcl-2 levels and downregulated Cox-2 and pancreatic ER kinase (PERK) [<xref ref-type="bibr" rid="B197">125</xref>
]. Baicalein also regulated Bcl-2 and antagonized cytochrome c release in cytosol [<xref ref-type="bibr" rid="B135">126</xref>
]. Similarly, ferulic acid, a phenolic acid, attenuates mitochondria apoptosis by inhibiting Bax, tBid expression, and elevating Bcl-2-like proteins [<xref ref-type="bibr" rid="B104">124</xref>
]. Important transcription factors of ERK/Nrf2 pathway like glutamate cysteine ligase catalytic (GCLC) and glutamate-cysteine ligase, modifier subunit (GCLM), are upregulated by flavones like chrysin, apigenin, and luteolin to combat oxidative stress [<xref ref-type="bibr" rid="B198">129</xref>
]. Glutathione peroxidase (GPx) levels were modulated by red wine polyphenols resulting in combat of oxidative stress [<xref ref-type="bibr" rid="B199">132</xref>
]. Similarly, phenolic antioxidant 3,3′,5,5′-tetra-t-butyl-biphenyl-4,4′-diol also controlled expression of GPx and HIF-1<italic>α</italic>
in hypoxia studies [<xref ref-type="bibr" rid="B200">133</xref>
]. Various polyphenols like butein, phloretin, chrysin, apigenin, and luteolin activated HO-1 (HMOX1), GCLC, and GCLM through expression of ERK/Nrf2 pathway [<xref ref-type="bibr" rid="B198">129</xref>
, <xref ref-type="bibr" rid="B201">134</xref>
]. Quercetin has also downregulated inflammatory cascade by lowering the expression of JNK, c-Jun, and interferon-<italic>γ</italic>
inducible protein [<xref ref-type="bibr" rid="B202">135</xref>
]. Similarly, p-JNK and COX-2 were downregulated by polyphenols from <italic>Hibiscus sabdariffa</italic>
L. providing relief from oxidative stress and pathological inflammation [<xref ref-type="bibr" rid="B203">128</xref>
]. EGCG controlled mitochondria lead inflammation by lowering transcription of JNK and activator protein-1 (AP-1) [<xref ref-type="bibr" rid="B151">116</xref>
]. Neuroprotection through the phosphatidylinositol 3-kinase (P13K) and MAPK has also been shown by flavone glycoside [<xref ref-type="bibr" rid="B204">113</xref>
]. Hesperidin carsonic acid, a major rosemary polyphenol, exhibited strong anti-inflammatory action in neurons under hypoxia stress by inhibiting ROS, MAPKs, caspase-3, and COX-2 [<xref ref-type="bibr" rid="B205">127</xref>
]. Lowering of JNK serves as mitochondrial therapy not only in stroke but also in AD as JNK activation in AD brain leads to tau hyperphosphorylation and A<italic>β</italic>
pathogenesis [<xref ref-type="bibr" rid="B206">208</xref>
]. Curcumin and resveratrol exhibited neuroprotection through increased activity of NAD(P)H quinone oxidoreductase (NQO1) via Nrf2 pathway in astrocytes [<xref ref-type="bibr" rid="B207">209</xref>
]. Similarly, structurally modified isomers of resveratrol also elevated the NQO1 activity, thus promising antioxidant effects through NRf2 pathway [<xref ref-type="bibr" rid="B208">210</xref>
]. ECG modulated endophilin-B1, also known as SH3GLB1, which is required for maintaining mitochondrial morphology and plays important role in apoptosis [<xref ref-type="bibr" rid="B209">211</xref>
, <xref ref-type="bibr" rid="B210">212</xref>
]. EGCG has also increased expression of mitochondrial antioxidant enzymes including superoxide dismutase (SOD) and glutathione peroxidase (GPX1) [<xref ref-type="bibr" rid="B211">130</xref>
]. Flavonoid-enriched fraction (AF4) isolated from the peel of “Northern Spy” apples has been shown to suppress the expression of IL-1<italic>β</italic>
, TNF-<italic>α</italic>
, and IL-6 in a mouse model of hypoxic-ischemic (HI) brain damage [<xref ref-type="bibr" rid="B212">123</xref>
]. Phloridzin, also an apple polyphenol, has been shown to increase expression of SOD1 and SOD2 genes, thus protecting mitochondria against oxidative stress [<xref ref-type="bibr" rid="B80">80</xref>
]. Polyphenols are important mitochondrial therapeutics as they play a role in mitochondrial biochemistry by modulating apoptosis, antioxidant action, signal transduction, and inflammation (<xref ref-type="table" rid="tab3">Table 3</xref>
). </p>
</sec>
<sec id="sec11"><title>11. Polyphenols and Ion Channels</title>
<p>The neuroprotective benefits of polyphenols are often attributed to their antioxidant activity and their ability to modulate the cell signaling pathways [<xref ref-type="bibr" rid="B140">105</xref>
, <xref ref-type="bibr" rid="B104">124</xref>
, <xref ref-type="bibr" rid="B119">155</xref>
]. Sodium channels (Na<sub>v</sub>
1.5) involved in pathology of MS were found to be blocked by red grape polyphenols like quercetin, catechin, and resveratrol in rodent and cell model studies [<xref ref-type="bibr" rid="B87">87</xref>
, <xref ref-type="bibr" rid="B213">213</xref>
]. G protein-coupled inwardly rectifying potassium (K<sub>IR</sub>
3) channels, involved in neuron signaling and membrane excitability [<xref ref-type="bibr" rid="B214">214</xref>
], are activated by naringin (flavonoid glycoside), thus exhibiting potential for improving cognition in AD [<xref ref-type="bibr" rid="B215">215</xref>
]. EGCG's neuroprotective effect was proposed to occur through inhibition of high-voltage-activated calcium currents (<italic>I</italic>
<sub>HVA</sub>
) and NMDA-induced inward currents (<italic>I</italic>
<sub>NMDA</sub>
) along with elevation of Ca<sup>2+</sup>
through PLC-IP<sub>3</sub>
pathway [<xref ref-type="bibr" rid="B216">216</xref>
]. Similarly, curcumin exhibited modulation of a wide range of ionic channels including Ca<sup>2+</sup>
-release-activated Ca<sup>2+</sup>
channels (<italic>I</italic>
<sub>CRAC</sub>
), voltage-gated K<sup>+</sup>
channel (<italic>I</italic>
<sub>Kv</sub>
), intermediate-conductance Ca<sup>2+</sup>
-activated K<sup>+</sup>
channel (<italic>I</italic>
<sub>SK4</sub>
), and the cytoplasmic Ca<sup>2+</sup>
concentration Δ[Ca<sup>2+</sup>
]<sub>C</sub>
in Jurkat-T cells [<xref ref-type="bibr" rid="B217">217</xref>
]. However, the current literature has a research gap of specific ion channel study (Kv3 subfamily of K<sup>+</sup>
channel subunits) in disease-specific conditions. Overall, the ability of polyphenols to modulate ion channels and action potential [<xref ref-type="bibr" rid="B218">218</xref>
] complements their ability to protect neurons from disorders and thus supports the growing evidence that polyphenols may act as neuroprotectants in several neuropathological conditions.</p>
</sec>
<sec id="sec12"><title>12. Concluding Remarks</title>
<p>In conclusion, recent scientific evidence suggests that neurodegenerative diseases are accompanied by oxidative stress, inflammation, metal accumulation, and mitochondrial dysfunctions. Various physiological mechanisms are altered by these pathological changes which contribute to etiology of neurodegenerative diseases like stroke, MS, PD, AD, and HD. The prevention and treatment of these disorders with complex mechanisms need novel therapeutic strategies targeted for multiple genes and proteins. Polyphenols are natural plant secondary metabolites which exhibit remarkable multipotent ability to control and modulate ROS, metal toxicity, inflammation, apoptosis, signal transduction, ion channels, and neurotransmitters. Polyphenolic dietary antioxidants, particularly resveratrol, EGCG, quercetin, and other fruit polyphenols, are potent neuroprotectants (<xref ref-type="fig" rid="fig2">Figure 2</xref>
). Their direct usage and dietary supplementation could act as antioxidant and neuroprotective therapy for treatment of these diseases. Most of experimental and epidemiological studies suggest that dietary polyphenols activate antioxidant pathways such as Nrf2/HO1 and downregulate NF<italic>κ</italic>
B, MMPs, PPAR, HIF-1, and STAT pathways. Polyphenols also modulate immune response by inhibiting proinflammatory biomarkers such as CCL17, CCL22, CCR1, CCR2, MIP1<italic>α</italic>
, MIP 1<italic>β</italic>
, CXCL (9, 10, 11), IFN-<italic>γ</italic>
, TNF-<italic>α</italic>
, and IL(1<italic>β</italic>
, 6, 17A, 22). These salient properties of polyphenols help to reduce two hallmarks of neurodegeneration, that is, oxidative damage and inflammation. </p>
<p>Polyphenols also protect mitochondria from pathological events by triggering prosurvival cell signaling. Polyphenols increase antioxidant enzymes, that is, catalase, superoxide dismutase (SOD1, SOD2), and prosurvival Bcl-2 and PERK pathways. Downregulation of Bad/Bax, c-jun, JNK, COX-2, AP-1, and caspase-3 also contributes to the survival of neurons. Polyphenols also help in improving cognitive abilities by inhibiting AChE and BChE. The inhibition of these enzymes plays an important role in clinical medicine of AD. Apart from their anti-AChE activity, polyphenols also induce metal chelation and modulate autophagy and prion proteins. These features along with reduction of A<italic>β</italic>
toxicity, reduction of neural lesions, and activation of cell survival genes are of particular relevance to neurodegenerative diseases. The activation of novel spectrum of these molecular targets forms underlying mechanism of neuroprotection by polyphenols. The lack of toxic effect and availability from natural sources makes polyphenols as clinically relevant therapeutics in neurodegeneration. </p>
<p>The future of polyphenol research needs to aim towards clinical acceptance of health claims from preclinical <italic>in vitro </italic>
and animal model studies. Therefore, future studies focusing on human clinical trials of several potent polyphenols and their combinations should be carried out. Furthermore, polyphenols must be investigated for the risk assessment and safety evaluation to observe any undesirable effects. The success in clinical research of polyphenols will decide their pharmacological relevance for humans.</p>
</sec>
</body>
<back><glossary><title>Abbreviations</title>
<def-list><def-item><term>AAP:</term>
<def><p>Amyloid precursor protein</p>
</def>
</def-item>
<def-item><term>AChE:</term>
<def><p>Acetylcholinesterase</p>
</def>
</def-item>
<def-item><term>AD:</term>
<def><p>Alzheimer's disease</p>
</def>
</def-item>
<def-item><term>AP-1:</term>
<def><p>Activator protein-1</p>
</def>
</def-item>
<def-item><term>A<italic>β</italic>
:</term>
<def><p>Amyloid beta</p>
</def>
</def-item>
<def-item><term>Bad:</term>
<def><p> BCL2-associated agonist of cell death</p>
</def>
</def-item>
<def-item><term>BAX:</term>
<def><p>BCL2-associated X protein</p>
</def>
</def-item>
<def-item><term>BBB:</term>
<def><p>Blood-brain barrier</p>
</def>
</def-item>
<def-item><term>BChE:</term>
<def><p>Butyrylcholinesterase</p>
</def>
</def-item>
<def-item><term>Bcl:</term>
<def><p>B-cell lymphoma</p>
</def>
</def-item>
<def-item><term>Bcl2:</term>
<def><p>B-cell lymphoma 2</p>
</def>
</def-item>
<def-item><term>cAMP:</term>
<def><p> Cyclic adenosine monophosphate </p>
</def>
</def-item>
<def-item><term>CCL:</term>
<def><p>Chemokine (C-C motif) ligand</p>
</def>
</def-item>
<def-item><term>CCR:</term>
<def><p>Chemokine receptor</p>
</def>
</def-item>
<def-item><term>CD:</term>
<def><p>Cluster of differentiation</p>
</def>
</def-item>
<def-item><term>CI:</term>
<def><p>Cerebral ischemia</p>
</def>
</def-item>
<def-item><term>COX:</term>
<def><p>Cyclooxygenase</p>
</def>
</def-item>
<def-item><term>CREB:</term>
<def><p>cAMP response element binding protein</p>
</def>
</def-item>
<def-item><term>CXCL:</term>
<def><p>Chemokine (C-X-C motif) ligand</p>
</def>
</def-item>
<def-item><term>EAE:</term>
<def><p>Experimental autoimmune encephalomyelitis</p>
</def>
</def-item>
<def-item><term>ECG:</term>
<def><p>Epicatechin gallate</p>
</def>
</def-item>
<def-item><term>EGCG:</term>
<def><p>Epigallocatechin gallate</p>
</def>
</def-item>
<def-item><term>GCLC:</term>
<def><p>Glutamate cysteine ligase catalytic</p>
</def>
</def-item>
<def-item><term>GCLM:</term>
<def><p>Glutamate-cysteine ligase, modifier subunit</p>
</def>
</def-item>
<def-item><term>GPx:</term>
<def><p>Glutathione peroxidase</p>
</def>
</def-item>
<def-item><term>GSK:</term>
<def><p>Glycogen synthase kinase</p>
</def>
</def-item>
<def-item><term>HD:</term>
<def><p>Huntington's disease</p>
</def>
</def-item>
<def-item><term>HIF:</term>
<def><p>Hypoxia inducible factor</p>
</def>
</def-item>
<def-item><term>HIF-1:</term>
<def><p> Hypoxia inducible factor-1 </p>
</def>
</def-item>
<def-item><term>HO:</term>
<def><p>Heme oxygenase</p>
</def>
</def-item>
<def-item><term>IFN<italic>γ</italic>
:</term>
<def><p>Interferon-gamma</p>
</def>
</def-item>
<def-item><term>IL:</term>
<def><p>Interleukin</p>
</def>
</def-item>
<def-item><term>JNK:</term>
<def><p>c-Jun N-terminal kinase</p>
</def>
</def-item>
<def-item><term>MAPK:</term>
<def><p>Mitogen activated kinase-like protein</p>
</def>
</def-item>
<def-item><term>MCP-1:</term>
<def><p>Monocyte chemoattractant protein-1</p>
</def>
</def-item>
<def-item><term>MIP:</term>
<def><p>Macrophage inflammatory protein</p>
</def>
</def-item>
<def-item><term>MMP:</term>
<def><p>Metalloproteinases</p>
</def>
</def-item>
<def-item><term>MS:</term>
<def><p>Multiple sclerosis</p>
</def>
</def-item>
<def-item><term>NF<italic>κ</italic>
B:</term>
<def><p>Nuclear factor-kappa B</p>
</def>
</def-item>
<def-item><term>NOS:</term>
<def><p> Nitric oxide synthase</p>
</def>
</def-item>
<def-item><term>NQO1:</term>
<def><p> NAD(P)H quinone oxidoreductase</p>
</def>
</def-item>
<def-item><term>Nrf2:</term>
<def><p> Nuclear factor- (erythroid-derived 2-) like 2</p>
</def>
</def-item>
<def-item><term>PC:</term>
<def><p> Protein carbonyl</p>
</def>
</def-item>
<def-item><term>PD:</term>
<def><p> Parkinson's disease</p>
</def>
</def-item>
<def-item><term>PERK:</term>
<def><p> Pancreatic ER kinase</p>
</def>
</def-item>
<def-item><term>PGC-1<italic>α</italic>
:</term>
<def><p> Peroxisome proliferative activated receptor, coactivator 1 alpha</p>
</def>
</def-item>
<def-item><term>PI3K:</term>
<def><p> Phosphatidylinositol 3-kinase</p>
</def>
</def-item>
<def-item><term>PPAR:</term>
<def><p> Peroxisome proliferator activated receptor</p>
</def>
</def-item>
<def-item><term>PrP(c):</term>
<def><p> Cellular prion protein</p>
</def>
</def-item>
<def-item><term>ROS:</term>
<def><p> Reactive oxygen species</p>
</def>
</def-item>
<def-item><term>SIRT-1:</term>
<def><p> Silent mating type information regulation 2 homolog1</p>
</def>
</def-item>
<def-item><term>SOD:</term>
<def><p> Superoxide dismutase</p>
</def>
</def-item>
<def-item><term>STAT:</term>
<def><p> Signal transducer and activation of transcription</p>
</def>
</def-item>
<def-item><term>TGF<italic>β</italic>
:</term>
<def><p> Transforming growth factors <italic>β</italic>
</p>
</def>
</def-item>
<def-item><term>TLR:</term>
<def><p> Toll-like receptor</p>
</def>
</def-item>
<def-item><term>TNF<italic>α</italic>
:</term>
<def><p> Tumor necrosis factor-alpha</p>
</def>
</def-item>
<def-item><term>TRAF:</term>
<def><p>TNF receptor associated factor</p>
</def>
</def-item>
<def-item><term>TRX:</term>
<def><p> Thioredoxin.</p>
</def>
</def-item>
</def-list>
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<floats-group><fig id="fig1" orientation="portrait" position="float"><label>Figure 1</label>
<caption><p>Neuroprotection by polyphenols against neurological disorders.</p>
</caption>
<graphic xlink:href="OXIMED2013-891748.001"></graphic>
</fig>
<fig id="fig2" orientation="portrait" position="float"><label>Figure 2</label>
<caption><p>Chemical structure of polyphenols with therapeutic use in age-related neurological diseases.</p>
</caption>
<graphic xlink:href="OXIMED2013-891748.002"></graphic>
</fig>
<table-wrap id="tab1" orientation="portrait" position="float"><label>Table 1</label>
<caption><p>Neuroprotective signal transduction by polyphenols. </p>
</caption>
<table frame="hsides" rules="groups"><thead><tr><th align="left" rowspan="1" colspan="1">Pathway</th>
<th align="center" rowspan="1" colspan="1">Polyphenol</th>
<th align="center" rowspan="1" colspan="1">References</th>
</tr>
</thead>
<tbody><tr><td align="left" rowspan="1" colspan="1">P13K/AkT pathway</td>
<td align="center" rowspan="1" colspan="1">Resveratrol</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B134">99</xref>
, <xref ref-type="bibr" rid="B100">100</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"> </td>
<td align="center" rowspan="1" colspan="1">Baicalein</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B97">97</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1">NF<italic>κ</italic>
B pathway</td>
<td align="center" rowspan="1" colspan="1">Kaempferol, acacetin, apigenin, luteolin</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B136">101</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"> </td>
<td align="center" rowspan="1" colspan="1">Soybean isoflavones</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B137">102</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"> </td>
<td align="center" rowspan="1" colspan="1">Fisetin</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B94">94</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"> </td>
<td align="center" rowspan="1" colspan="1">Resveratrol</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B138">103</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"> </td>
<td align="center" rowspan="1" colspan="1">Baicalein</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B142">104</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"> </td>
<td align="center" rowspan="1" colspan="1">Silymarin</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B140">105</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"> </td>
<td align="center" rowspan="1" colspan="1">Tetrahydroxystilbene</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B58">58</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"> </td>
<td align="center" rowspan="1" colspan="1">Quercetin</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B136">101</xref>
, <xref ref-type="bibr" rid="B141">106</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"> </td>
<td align="center" rowspan="1" colspan="1">Catechin hydrate</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B94">94</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1">STAT pathway</td>
<td align="center" rowspan="1" colspan="1">Silymarin</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B140">105</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1">PPAR pathway</td>
<td align="center" rowspan="1" colspan="1">Baicalein</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B142">104</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"> </td>
<td align="center" rowspan="1" colspan="1">Resveratrol</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B143">107</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"> </td>
<td align="center" rowspan="1" colspan="1">Pterostilbene</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B144">108</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1">Nrf2/HO1/ARE pathway</td>
<td align="center" rowspan="1" colspan="1">Epicatechin</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B146">109</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"> </td>
<td align="center" rowspan="1" colspan="1">Resveratrol</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B147">110</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1">HIF-1<italic>α</italic>
</td>
<td align="center" rowspan="1" colspan="1">Xanthohumol</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B148">111</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"> </td>
<td align="center" rowspan="1" colspan="1">Resveratrol</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B149">112</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1">MAPK</td>
<td align="center" rowspan="1" colspan="1">Flavone glycoside</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B204">113</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"> </td>
<td align="center" rowspan="1" colspan="1">Quercetin</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B124">114</xref>
]</td>
</tr>
</tbody>
</table>
</table-wrap>
<table-wrap id="tab2" orientation="portrait" position="float"><label>Table 2</label>
<caption><p>Modulation of cytokines and inflammatory targets by polyphenols. </p>
</caption>
<table frame="hsides" rules="groups"><thead><tr><th align="left" rowspan="1" colspan="1">Polyphenol</th>
<th align="center" rowspan="1" colspan="1">Target</th>
<th align="center" rowspan="1" colspan="1">References</th>
</tr>
</thead>
<tbody><tr><td align="left" rowspan="1" colspan="1">EGCG</td>
<td align="center" rowspan="1" colspan="1">IL-1<italic>β</italic>
</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B157">115</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"> </td>
<td align="center" rowspan="1" colspan="1">IL-6</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B151">116</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"> </td>
<td align="center" rowspan="1" colspan="1">MCP-1</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B157">115</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"> </td>
<td align="center" rowspan="1" colspan="1">CXCL 10, </td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B151">116</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"> </td>
<td align="center" rowspan="1" colspan="1">CCL22, CCL 17</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B154">117</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"> </td>
<td align="center" rowspan="1" colspan="1">TGF <italic>β</italic>
</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B154">117</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1">Resveratrol</td>
<td align="center" rowspan="1" colspan="1">MCP-1</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B152">118</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1">Catechin</td>
<td align="center" rowspan="1" colspan="1">MCP-1 (<italic>α</italic>
and <italic>β</italic>
)</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B153">119</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1">Caffeic acid</td>
<td align="center" rowspan="1" colspan="1">CCR1, CCR2</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B153">119</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1">Quercetin</td>
<td align="center" rowspan="1" colspan="1">IL-1<italic>β</italic>
, IL-6</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B155">120</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"> </td>
<td align="center" rowspan="1" colspan="1">COX-2</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B155">120</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"> </td>
<td align="center" rowspan="1" colspan="1">COX-20, TRAF1</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B156">121</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1">Apple polyphenols</td>
<td align="center" rowspan="1" colspan="1">IL-1<italic>β</italic>
, IL-6, IL-17, IL-22<break></break>
CXCL-9, CXCL-10, CXCL-11, </td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B159">122</xref>
, <xref ref-type="bibr" rid="B212">123</xref>
]</td>
</tr>
</tbody>
</table>
</table-wrap>
<table-wrap id="tab3" orientation="portrait" position="float"><label>Table 3</label>
<caption><p>Modulation of mitochondrial targets by polyphenols. </p>
</caption>
<table frame="hsides" rules="groups"><thead><tr><th align="left" rowspan="1" colspan="1">Target</th>
<th align="center" rowspan="1" colspan="1">Polyphenol</th>
<th align="center" rowspan="1" colspan="1">Effect</th>
<th align="center" rowspan="1" colspan="1">References</th>
</tr>
</thead>
<tbody><tr><td align="left" rowspan="1" colspan="1">AP-1</td>
<td align="center" rowspan="1" colspan="1">EGCG</td>
<td align="center" rowspan="1" colspan="1">Downregulation</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B151">116</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1">Bad/Bax</td>
<td align="center" rowspan="1" colspan="1">Resveratrol</td>
<td align="center" rowspan="1" colspan="1">Downregulation</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B149">112</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"> </td>
<td align="center" rowspan="1" colspan="1">Ferulic acid</td>
<td align="center" rowspan="1" colspan="1">Downregulation</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B104">124</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1">Bcl-2</td>
<td align="center" rowspan="1" colspan="1">Lutein</td>
<td align="center" rowspan="1" colspan="1">Upregulation</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B197">125</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"> </td>
<td align="center" rowspan="1" colspan="1">Baicalein</td>
<td align="center" rowspan="1" colspan="1">Upregulation</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B135">126</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1">Cox-2</td>
<td align="center" rowspan="1" colspan="1">Lutein</td>
<td align="center" rowspan="1" colspan="1">Downregulation</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B197">125</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"> </td>
<td align="center" rowspan="1" colspan="1">Hesperidin</td>
<td align="center" rowspan="1" colspan="1">Downregulation</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B205">127</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"> </td>
<td align="center" rowspan="1" colspan="1"><italic>Hibiscus sabdariffa</italic>
polyphenols</td>
<td align="center" rowspan="1" colspan="1">Downregulation</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B203">128</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1">GCLM</td>
<td align="center" rowspan="1" colspan="1">Chrysin, apigenin, luteolin</td>
<td align="center" rowspan="1" colspan="1">Upregulation</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B198">129</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1">GCLC</td>
<td align="center" rowspan="1" colspan="1">Chrysin, apigenin, luteolin</td>
<td align="center" rowspan="1" colspan="1">Upregulation</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B198">129</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1">GPX</td>
<td align="center" rowspan="1" colspan="1">EGCG</td>
<td align="center" rowspan="1" colspan="1">Upregulation</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B211">130</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"> </td>
<td align="center" rowspan="1" colspan="1">Red wine polyphenols</td>
<td align="center" rowspan="1" colspan="1">Upregulation</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B194">131</xref>
, <xref ref-type="bibr" rid="B199">132</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"> </td>
<td align="center" rowspan="1" colspan="1">3,3′,5,5′-tetra-t-butyl-biphenyl-4,4′-diol</td>
<td align="center" rowspan="1" colspan="1">Upregulation</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B200">133</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1">HO-1</td>
<td align="center" rowspan="1" colspan="1">Butein, apigenin</td>
<td align="center" rowspan="1" colspan="1">Upregulation</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B198">129</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"> </td>
<td align="center" rowspan="1" colspan="1">Luteolin</td>
<td align="center" rowspan="1" colspan="1">Upregulation</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B201">134</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1">IFN-<italic>γ</italic>
</td>
<td align="center" rowspan="1" colspan="1">Quercetin</td>
<td align="center" rowspan="1" colspan="1">Downregulation</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B202">135</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1">JNK</td>
<td align="center" rowspan="1" colspan="1">Quercetin</td>
<td align="center" rowspan="1" colspan="1">Downregulation</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B202">135</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"> </td>
<td align="center" rowspan="1" colspan="1">EGCG</td>
<td align="center" rowspan="1" colspan="1">Downregulation</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B151">116</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"> </td>
<td align="center" rowspan="1" colspan="1"><italic>Hibiscus sabdariffa</italic>
polyphenols</td>
<td align="center" rowspan="1" colspan="1">Downregulation</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B203">128</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1">JUN</td>
<td align="center" rowspan="1" colspan="1">Quercetin</td>
<td align="center" rowspan="1" colspan="1">Downregulation</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B202">135</xref>
]</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1">SOD </td>
<td align="center" rowspan="1" colspan="1">Phloridzin</td>
<td align="center" rowspan="1" colspan="1">Upregulation</td>
<td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B129">136</xref>
]</td>
</tr>
</tbody>
</table>
</table-wrap>
</floats-group>
</pmc>
</record>
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