Anti-inflammatory effects of flavonoids in neurodegenerative disorders

European Journal of Medicinal Chemistry - Tập 153 - Trang 105-115 - 2018
Carmela Spagnuolo1, Stefania Moccia1, Gian Luigi Russo1
1Institute of Food Sciences, National Research Council, 83100 Avellino, Italy

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Hoglund, 2013, Molecular biomarkers of neurodegeneration, Expert Rev. Mol. Diagn, 13, 845, 10.1586/14737159.2013.850033

Solanki, 2015, Flavonoid-based therapies in the early management of neurodegenerative diseases, Adv. Nutr., 6, 64, 10.3945/an.114.007500

Vauzour, 2008, The neuroprotective potential of flavonoids: a multiplicity of effects, Genes Nutr., 3, 115, 10.1007/s12263-008-0091-4

Youdim, 2002, Dietary flavonoids as potential neuroprotectants, Biol. Chem., 383, 503

Macready, 2009, Flavonoids and cognitive function: a review of human randomized controlled trial studies and recommendations for future studies, Genes Nutr., 4, 227, 10.1007/s12263-009-0135-4

Gillette-Guyonnet, 2013, Nutrition and neurodegeneration: epidemiological evidence and challenges for future research, Br. J. Clin. Pharmacol., 75, 738, 10.1111/bcp.12058

Joseph, 1999, Reversals of age-related declines in neuronal signal transduction, cognitive, and motor behavioral deficits with blueberry, spinach, or strawberry dietary supplementation, J. Neurosci., 19, 8114, 10.1523/JNEUROSCI.19-18-08114.1999

Krikorian, 2010, Blueberry supplementation improves memory in older adults, J. Agric. Food Chem., 58, 3996, 10.1021/jf9029332

Spagnuolo, 2016, Neuroprotective role of natural polyphenols, Curr. Top. Med. Chem., 16, 1943, 10.2174/1568026616666160204122449

Spencer, 2012, Neuroinflammation: modulation by flavonoids and mechanisms of action, Mol. Asp. Med., 33, 83, 10.1016/j.mam.2011.10.016

Chen, 2016, Role of neuroinflammation in neurodegenerative diseases (Review), Mol. Med. Rep., 13, 3391, 10.3892/mmr.2016.4948

Schain, 2017, Neuroinflammation in neurodegenerative disorders-a review, Curr. Neurol. Neurosci. Rep., 17, 25, 10.1007/s11910-017-0733-2

McManus, 2017, Role of neuroinflammation in neurodegeneration: new insights, Alzheimers Res. Ther., 9, 14, 10.1186/s13195-017-0241-2

Block, 2005, Microglia and inflammation-mediated neurodegeneration: multiple triggers with a common mechanism, Prog. Neurobiol., 76, 77, 10.1016/j.pneurobio.2005.06.004

Calsolaro, 2016, Neuroinflammation in Alzheimer's disease: current evidence and future directions, Alzheimers Dement., 12, 719, 10.1016/j.jalz.2016.02.010

Dzamko, 2015, Inflammation is genetically implicated in Parkinson's disease, Neuroscience, 302, 89, 10.1016/j.neuroscience.2014.10.028

Ransohoff, 2016, How neuroinflammation contributes to neurodegeneration, Science, 353, 777, 10.1126/science.aag2590

Esiri, 2007, The interplay between inflammation and neurodegeneration in CNS disease, J. Neuroimmunol., 184, 4, 10.1016/j.jneuroim.2006.11.013

Glass, 2010, Mechanisms underlying inflammation in neurodegeneration, Cell, 140, 918, 10.1016/j.cell.2010.02.016

Rahimifard, 2017, Targeting the TLR4 signaling pathway by polyphenols: a novel therapeutic strategy for neuroinflammation, Ageing Res. Rev., 36, 11, 10.1016/j.arr.2017.02.004

Pawate, 2006, C-Jun N-terminal kinase (JNK) regulation of iNOS expression in glial cells: predominant role of JNK1 isoform, Antioxid. Redox Signal, 8, 903, 10.1089/ars.2006.8.903

Zindler, 2010, Neuronal injury in chronic CNS inflammation, Best Pract. Res. Clin. Anaesthesiol., 24, 551, 10.1016/j.bpa.2010.11.001

ElAli, 2016, Microglia in Alzheimer's disease: a multifaceted relationship, Brain Behav. Immun., 55, 138, 10.1016/j.bbi.2015.07.021

Yin, 2016, Energy metabolism and inflammation in brain aging and Alzheimer's disease, Free Radic. Biol. Med., 100, 108, 10.1016/j.freeradbiomed.2016.04.200

Manach, 2004, Polyphenols: food sources and bioavailability, Am. J. Clin. Nutr., 79, 727, 10.1093/ajcn/79.5.727

Aherne, 2002, Dietary flavonols: chemistry, food content, and metabolism, Nutrition, 18, 75, 10.1016/S0899-9007(01)00695-5

Tsao, 2010, Chemistry and biochemistry of dietary polyphenols, Nutrients, 2, 1231, 10.3390/nu2121231

Candiracci, 2012, Anti-inflammatory activity of a honey flavonoid extract on lipopolysaccharide-activated N13 microglial cells, J. Agric. Food Chem., 60, 12304, 10.1021/jf302468h

Cho, 2012, Neuroprotective and anti-inflammatory effects of flavonoids isolated from Rhus verniciflua in neuronal HT22 and microglial BV2 cell lines, Food Chem. Toxicol., 50, 1940, 10.1016/j.fct.2012.03.052

Cho, 2013, Cognitive-enhancing effects of Rhus verniciflua bark extract and its active flavonoids with neuroprotective and anti-inflammatory activities, Food Chem. Toxicol., 58, 355, 10.1016/j.fct.2013.05.007

Guo, 2016, Anti-neuroinflammatory effect of Sophoraflavanone G from Sophora alopecuroides in LPS-activated BV2 microglia by MAPK, JAK/STAT and Nrf2/HO-1 signaling pathways, Phytomedicine, 23, 1629, 10.1016/j.phymed.2016.10.007

Zhang, 2013, Protective effect of flavonoid-rich extract from Rosa laevigata Michx on cerebral ischemia-reperfusion injury through suppression of apoptosis and inflammation, Neurochem. Int., 63, 522, 10.1016/j.neuint.2013.08.008

Mohebali, 2016, Effect of flavonoids rich extract of Capparis spinosa on inflammatory involved genes in amyloid-beta peptide injected rat model of Alzheimer's disease, Nutr. Neurosci., 1

Suganthy, 2016, Bioactive effects of quercetin in the central nervous system: focusing on the mechanisms of actions, Biomed. Pharmacother., 84, 892, 10.1016/j.biopha.2016.10.011

Bournival, 2012, Quercetin and sesamin protect dopaminergic cells from MPP+-induced neuroinflammation in a microglial (N9)-neuronal (PC12) coculture system, Oxid. Med. Cell Longev., 2012, 921941, 10.1155/2012/921941

Testa, 2014, Loading into nanoparticles improves quercetin's efficacy in preventing neuroinflammation induced by oxysterols, PLoS One, 9, e96795, 10.1371/journal.pone.0096795

Mehta, 2017, Quercetin prevents chronic unpredictable stress induced behavioral dysfunction in mice by alleviating hippocampal oxidative and inflammatory stress, Physiol. Behav., 171, 69, 10.1016/j.physbeh.2017.01.006

Kang, 2013, Quercetin inhibits lipopolysaccharide-induced nitric oxide production in BV2 microglial cells by suppressing the NF-kappaB pathway and activating the Nrf2-dependent HO-1 pathway, Int. Immunopharmacol., 17, 808, 10.1016/j.intimp.2013.09.009

Sun, 2015, Quercetin attenuates inflammatory responses in BV-2 microglial cells: role of MAPKs on the Nrf2 pathway and induction of heme Oxygenase-1, PLoS One, 10, e0141509, 10.1371/journal.pone.0141509

Javed, 2012, Rutin prevents cognitive impairments by ameliorating oxidative stress and neuroinflammation in rat model of sporadic dementia of Alzheimer type, Neuroscience, 210, 340, 10.1016/j.neuroscience.2012.02.046

Xu, 2014, Rutin improves spatial memory in Alzheimer's disease transgenic mice by reducing Abeta oligomer level and attenuating oxidative stress and neuroinflammation, Behav. Brain Res., 264, 173, 10.1016/j.bbr.2014.02.002

Wu, 2016, Rutin attenuates neuroinflammation in spinal cord injury rats, J. Surg. Res., 203, 331, 10.1016/j.jss.2016.02.041

Hao, 2016, Rutin inhibits neuroinflammation and provides neuroprotection in an experimental rat model of subarachnoid hemorrhage, possibly through suppressing the RAGE-NF-kappaB inflammatory signaling pathway, Neurochem. Res., 41, 1496, 10.1007/s11064-016-1863-7

Lutz, 2014, A nicotinic receptor-mediated anti-inflammatory effect of the flavonoid rhamnetin in BV2 microglia, Fitoterapia, 98, 11, 10.1016/j.fitote.2014.06.012

Lutz, 2015, The dietary flavonoid rhamnetin inhibits both inflammation and excitotoxicity during ethanol withdrawal in rat organotypic hippocampal slice cultures, Alcohol Clin. Exp. Res., 39, 2345, 10.1111/acer.12896

Yu, 2013, Neuroprotective effect of kaempferol glycosides against brain injury and neuroinflammation by inhibiting the activation of NF-kappaB and STAT3 in transient focal stroke, PLoS One, 8, e55839, 10.1371/journal.pone.0055839

Park, 2011, Kaempferol acts through mitogen-activated protein kinases and protein kinase B/AKT to elicit protection in a model of neuroinflammation in BV2 microglial cells, Br. J. Pharmacol., 164, 1008, 10.1111/j.1476-5381.2011.01389.x

Martens, 2005, Flavones and flavone synthases, Phytochemistry, 66, 2399, 10.1016/j.phytochem.2005.07.013

Shimoi, 1998, Intestinal absorption of luteolin and luteolin 7-O-beta-glucoside in rats and humans, FEBS Lett., 438, 220, 10.1016/S0014-5793(98)01304-0

Comalada, 2006, Inhibition of pro-inflammatory markers in primary bone marrow-derived mouse macrophages by naturally occurring flavonoids: analysis of the structure-activity relationship, Biochem. Pharmacol., 72, 1010, 10.1016/j.bcp.2006.07.016

Zhu, 2011, Luteolin reduces primary hippocampal neurons death induced by neuroinflammation, Neurol. Res., 33, 927, 10.1179/1743132811Y.0000000023

Burton, 2016, Dietary luteolin reduces proinflammatory microglia in the brain of senescent mice, Rejuvenation Res., 19, 286, 10.1089/rej.2015.1708

Dirscherl, 2010, Luteolin triggers global changes in the microglial transcriptome leading to a unique anti-inflammatory and neuroprotective phenotype, J. Neuroinflammation, 7, 3, 10.1186/1742-2094-7-3

Jang, 2008, Luteolin reduces IL-6 production in microglia by inhibiting JNK phosphorylation and activation of AP-1, Proc. Natl. Acad. Sci. U. S. A., 105, 7534, 10.1073/pnas.0802865105

Zhu, 2014, Luteolin inhibits SH-SY5Y cell apoptosis through suppression of the nuclear transcription factor-kappaB, mitogen-activated protein kinase and protein kinase B pathways in lipopolysaccharide-stimulated cocultured BV2 cells, Exp. Ther. Med., 7, 1065, 10.3892/etm.2014.1564

Rezai-Zadeh, 2008, Apigenin and luteolin modulate microglial activation via inhibition of STAT1-induced CD40 expression, J. Neuroinflammation, 5, 41, 10.1186/1742-2094-5-41

Patil, 2014, Neuroprotective and neurotrophic effects of Apigenin and Luteolin in MPTP induced parkinsonism in mice, Neuropharmacology, 86, 192, 10.1016/j.neuropharm.2014.07.012

Ginwala, 2016, Apigenin, a natural flavonoid, attenuates EAE severity through the modulation of dendritic cell and other immune cell functions, J. Neuroimmune Pharmacol., 11, 36, 10.1007/s11481-015-9617-x

Sawmiller, 2016, Diosmin reduces cerebral Abeta levels, tau hyperphosphorylation, neuroinflammation, and cognitive impairment in the 3xTg-AD mice, J. Neuroimmunol., 299, 98, 10.1016/j.jneuroim.2016.08.018

Yuan, 2014, Anti-inflammatory effects of Edaravone and Scutellarin in activated microglia in experimentally induced ischemia injury in rats and in BV-2 microglia, BMC Neurosci., 15, 125, 10.1186/s12868-014-0125-3

Chen, 2013, Scutellarin attenuates hypertension-induced expression of brain Toll-like receptor 4/nuclear factor kappa B, Mediat. Inflamm., 2013, 432623, 10.1155/2013/432623

Wang, 2011, Neuroprotection of Scutellarin is mediated by inhibition of microglial inflammatory activation, Neuroscience, 185, 150, 10.1016/j.neuroscience.2011.04.005

Lee, 2013, Epigallocatechin-3-gallate prevents systemic inflammation-induced memory deficiency and amyloidogenesis via its anti-neuroinflammatory properties, J. Nutr. Biochem., 24, 298, 10.1016/j.jnutbio.2012.06.011

Leea, 2009, (−)-Epigallocatechin-3-gallate prevents lipopolysaccharide-induced elevation of beta-amyloid generation and memory deficiency, Brain Res., 1250, 164, 10.1016/j.brainres.2008.10.012

Wu, 2012, Green tea extract ameliorates learning and memory deficits in ischemic rats via its active component polyphenol epigallocatechin-3-gallate by modulation of oxidative stress and neuroinflammation, Evid. Based Complement. Altern. Med., 2012, 163106, 10.1155/2012/163106

Herges, 2011, Neuroprotective effect of combination therapy of glatiramer acetate and epigallocatechin-3-gallate in neuroinflammation, PLoS One, 6, e25456, 10.1371/journal.pone.0025456

Cheng-Chung Wei, 2016, Epigallocatechin gallate attenuates amyloid beta-induced inflammation and neurotoxicity in EOC 13.31 microglia, Eur. J. Pharmacol., 770, 16, 10.1016/j.ejphar.2015.11.048

Li, 2012, (-)-Epigallocatechin gallate inhibits endotoxin-induced expression of inflammatory cytokines in human cerebral microvascular endothelial cells, J. Neuroinflammation, 9, 161, 10.1186/1742-2094-9-161

Anandhan, 2013, Therapeutic attenuation of neuroinflammation and apoptosis by black tea theaflavin in chronic MPTP/probenecid model of Parkinson's disease, Neurotox. Res., 23, 166, 10.1007/s12640-012-9332-9

Leonardo, 2013, Oral administration of the flavanol (-)-epicatechin bolsters endogenous protection against focal ischemia through the Nrf2 cytoprotective pathway, Eur. J. Neurosci., 38, 3659, 10.1111/ejn.12362

Mohamed, 2011, Epicatechin attenuates doxorubicin-induced brain toxicity: critical role of TNF-alpha, iNOS and NF-kappaB, Brain Res. Bull., 86, 22, 10.1016/j.brainresbull.2011.07.001

Rani, 2016, Pharmacological properties and therapeutic potential of naringenin: a citrus flavonoid of pharmaceutical promise, Curr. Pharm. Des., 22, 4341, 10.2174/1381612822666160530150936

Vafeiadou, 2009, The citrus flavanone naringenin inhibits inflammatory signalling in glial cells and protects against neuroinflammatory injury, Arch. Biochem. Biophys., 484, 100, 10.1016/j.abb.2009.01.016

Raza, 2013, Neuroprotective effect of naringenin is mediated through suppression of NF-kappaB signaling pathway in experimental stroke, Neuroscience, 230, 157, 10.1016/j.neuroscience.2012.10.041

Wu, 2016, Naringenin suppresses neuroinflammatory responses through inducing suppressor of cytokine signaling 3 expression, Mol. Neurobiol., 53, 1080, 10.1007/s12035-014-9042-9

Shi, 2016, Naringenin inhibits spinal cord injury-induced activation of neutrophils through miR-223, Gene, 592, 128, 10.1016/j.gene.2016.07.037

Javed, 2015, Effect of hesperidin on neurobehavioral, neuroinflammation, oxidative stress and lipid alteration in intracerebroventricular streptozotocin induced cognitive impairment in mice, J. Neurol. Sci., 348, 51, 10.1016/j.jns.2014.10.044

Li, 2016, Hesperidin alleviates lipopolysaccharide-induced neuroinflammation in mice by promoting the miRNA-132 pathway, Inflammation, 39, 1681, 10.1007/s10753-016-0402-7

Prior, 2006, Anthocyanins: structural characteristics that result in unique metabolic patterns and biological activities, Free Radic. Res., 40, 1014, 10.1080/10715760600758522

Carvalho, 2017, Anthocyanins control neuroinflammation and consequent memory dysfunction in mice exposed to lipopolysaccharide, Mol. Neurobiol., 54, 3350, 10.1007/s12035-016-9900-8

Khan, 2016, Anthocyanins protect against LPS-induced oxidative stress-mediated neuroinflammation and neurodegeneration in the adult mouse cortex, Neurochem. Int., 100, 1, 10.1016/j.neuint.2016.08.005

Rehman, 2017, Anthocyanins reversed D-galactose-induced oxidative stress and neuroinflammation mediated cognitive impairment in adult rats, Mol. Neurobiol., 54, 255, 10.1007/s12035-015-9604-5

Carvalho, 2015, Anthocyanins suppress the secretion of proinflammatory mediators and oxidative stress, and restore ion pump activities in demyelination, J. Nutr. Biochem., 26, 378, 10.1016/j.jnutbio.2014.11.006

Chhor, 2013, Characterization of phenotype markers and neuronotoxic potential of polarised primary microglia in vitro, Brain Behav. Immun., 32, 70, 10.1016/j.bbi.2013.02.005

Meireles, 2016, Anthocyanin effects on microglia M1/M2 phenotype: consequence on neuronal fractalkine expression, Behav. Brain Res., 305, 223, 10.1016/j.bbr.2016.03.010

Dixon, 2004, Phytoestrogens, Annu. Rev. Plant Biol., 55, 225, 10.1146/annurev.arplant.55.031903.141729

Jantaratnotai, 2013, Phytoestrogens mediated anti-inflammatory effect through suppression of IRF-1 and pSTAT1 expressions in lipopolysaccharide-activated microglia, Int. Immunopharmacol., 17, 483, 10.1016/j.intimp.2013.07.013

Pozzi, 2006, Estrogen action in neuroprotection and brain inflammation, Ann. N. Y. Acad. Sci., 1089, 302, 10.1196/annals.1386.035

Zhou, 2014, Genistein antagonizes inflammatory damage induced by beta-amyloid peptide in microglia through TLR4 and NF-kappaB, Nutrition, 30, 90, 10.1016/j.nut.2013.06.006

Arroyo, 2011, Toll-like receptors are key players in neurodegeneration, Int. Immunopharmacol., 11, 1415, 10.1016/j.intimp.2011.05.006

Ullen, 2012, Phloretin ameliorates 2-chlorohexadecanal-mediated brain microvascular endothelial cell dysfunction in vitro, Free Radic. Biol. Med., 53, 1770, 10.1016/j.freeradbiomed.2012.08.575

Jiwrajka, 2016, The plant-derived chalcone 2,2',5'-trihydroxychalcone provides neuroprotection against toll-like receptor 4 triggered inflammation in microglia, Oxid. Med. Cell Longev., 2016, 6301712, 10.1155/2016/6301712

Luo, 2016, A tetramethoxychalcone from Chloranthus henryi suppresses lipopolysaccharide-induced inflammatory responses in BV2 microglia, Eur. J. Pharmacol., 774, 135, 10.1016/j.ejphar.2016.02.013

Yang, 2016, Safflower Yellow regulates microglial polarization and inhibits inflammatory response in LPS-stimulated Bv2 cells, Int. J. Immunopathol. Pharmacol., 29, 54, 10.1177/0394632015617065

Zhang, 2014, Hydroxy-safflor yellow A inhibits neuroinflammation mediated by Abeta(1)(-)(4)(2) in BV-2 cells, Neurosci. Lett., 562, 39, 10.1016/j.neulet.2014.01.005

Pandareesh, 2015, Bioavailability of dietary polyphenols: factors contributing to their clinical application in CNS diseases, Neurochem. Int., 89, 198, 10.1016/j.neuint.2015.07.003

Alharbi, 2016, Flavonoid-rich orange juice is associated with acute improvements in cognitive function in healthy middle-aged males, Eur. J. Nutr., 55, 2021, 10.1007/s00394-015-1016-9

Lamport, 2016, The effects of flavanone-rich citrus juice on cognitive function and cerebral blood flow: an acute, randomised, placebo-controlled cross-over trial in healthy, young adults, Br. J. Nutr., 116, 2160, 10.1017/S000711451600430X

Lovera, 2015, Polyphenon E, non-futile at neuroprotection in multiple sclerosis but unpredictably hepatotoxic: phase I single group and phase II randomized placebo-controlled studies, J. Neurol. Sci., 358, 46, 10.1016/j.jns.2015.08.006