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The Neuroprotective Effects of Phenolic Acids: Molecular Mechanism of Action

Dominik Szwajgier, Kamila Borowiec, Katarzyna Pustelniak

Nutrients · 2017 · Review · CC BY

doi:10.3390/nu9050477

Abstract

The neuroprotective role of phenolic acids from food has previously been reported by many authors. In this review, the role of phenolic acids in ameliorating depression, ischemia/reperfusion injury, neuroinflammation, apoptosis, glutamate-induced toxicity, epilepsy, imbalance after traumatic brain injury, hyperinsulinemia-induced memory impairment, hearing and vision disturbances, Parkinson’s disease, Huntington’s disease, anti-amyotrophic lateral sclerosis, Chagas disease and other less distributed diseases is discussed. This review covers the in vitro, ex vivo and in vivo studies concerning the prevention and treatment of neurological disorders (on the biochemical and gene expression levels) by phenolic acids.

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    Ning Q.-Q., Liu S., Li Y.-C., Li L., Yu Y., Zhao W.-X., Zhang X.-L. Protective effect of protocatechuic acid on midbrain dopaminergic neurons injured by 1-methyl-4-phenylpyridinium. Chin. Trad. Herb. Drugs. 2016;47:2497-2501.

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    Wang H.Y., Wang H., Wang J.H., Wang Q., Ma Q.F., Chen Y.Y. Protocatechuic acid inhibits inflammatory responses in LPS-stimulated BV2 microglia via NF-κB and MAPKs signaling pathways. Neurochem. Res. 2015;40:1655-1660.

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    Yin X., Su X.Y., Wang X.H., Su J.L., Lian Y., Zhang X.L. Effects of protocatechuic acid on expression of D2DR, iNOS, and TH in striatum and midbrain of Parkinson’s disease model mice. Chin. Trad. Herb. Drugs. 2015;46:866-870.

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    Ju D.T., Kuo W.W., Ho T.J. Protocatechuic acid from Alpinia oxyphylla induces Schwann cell migration via ERK1/2, JNK and p38 activation. Am. J. Chin. Med. 2015;43:653-665.

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    Naghizadeh B., Mansouri M.T. Protective effects of gallic acid against streptozotocin-induced oxidative damage in rat striatum. Drug Res. 2015;65:515-520.

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    Pemminati S. Effect of gallic acid on antioxidative enzymes activities in depression. Indian J. Psychiat. 2015;57:S125.

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    Hajimoradi M., Fazilati M., Gharib-Naseri M.K., Sarkaki A. Gallic acid and exercise training improve motor function, nerve conduction velocity but not pain sense reflex after experimental sciatic nerve crush in male rats. Avicenna J. Phytomed. 2015;5:288-297.

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    Moghadas M., Edalatmanesh M.A., Robati R. Histopathological analysis from gallic acid administration on hippocampal cell density, depression, and anxiety related behaviors in a trimethyltin intoxication model. Cell. J. 2016;17:659-667.

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    Oyagbemi A.A., Omobowale T.O., Saba A.B., Olowu E.R., Dada R.O., Akinrinde A.S. Gallic acid ameliorates cyclophosphamide-induced neurotoxicity in Wistar rats through free radical scavenging activity and improvement in antioxidant defense system. J. Diet. Suppl. 2016;13:402-419.

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    Hsu S.S., Chou C.T., Liao W.C., Shieh P., Kuo D.H., Kuo C.C., Jan C.R., Liang W.Z. The effect of gallic acid on cytotoxicity, Ca2+ homeostasis and ROS production in DBTRG-05MG human glioblastoma cells and CTX TNA2 rat astrocytes. Chem. Biol. Interact. 2016;252:61-73.

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    Tüzmen M.N., Yücel N.C., Kalburcu T., Demiryas N. Effects of curcumin and tannic acid on the aluminum-and lead-induced oxidative neurotoxicity and alterations in NMDA receptors. Toxicol. Mech. Method. 2015;25:120-127.

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    Ashafaq M., Tabassum H., Vishnoi S., Salman M., Raisuddin S., Parvez S. Tannic acid alleviates lead acetate-induced neurochemical perturbations in rat brain. Neurosci. Lett. 2016;617:94-100.

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    Sen H.M., Ozkan A., Güven M., Akman T., Aras A.B., Sehitoglu I., Alacam H., Silan C., Cosar M., Ozisik Karaman H.I. Effects of tannic acid on the ischemic brain tissue of rats. Inflammation. 2015;38:1624-1630.

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    Ashafaq M., Tabassum H., Parvez S. Modulation of behavioral deficits and neurodegeneration by tannic acid in experimental stroke challenged Wistar rats. Mol. Neurobiol. 2016.

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    Ibero-Baraibar I., Perez-Cornago A., Ramirez M.J., Martinez J.A., Zulet M.A. An increase in plasma homovanillic acid with cocoa extract consumption is associated with the alleviation of depressive symptoms in overweight or obese adults on an energy restricted diet in a randomized controlled trial. J. Nutr. 2016;146:897S-904S.

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    Neider D., Lindstrom L.H., Boden R. Risk factors for suicide among patients with schizophrenia: A cohort study focused on cerebrospinal fluid levels of homovanillic acid and 5-hydroxyindoleacetic acid. Neuropsych. Dis. Treat. 2016;12:1711-1714.

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    Van de Kerkhof N.W.A., Fekkes D., van der Heijden F.M.M.A., Egger J.I.M., Verhoeven W.M.A. Relationship between plasma homovanillic acid and outcome in patients with psychosis spectrum disorders. Neuropsychobiology. 2015;71:212-217.

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    Güven M., Aras A.B., Topaloğlu N., Özkan A., Şen H.M., Kalkan Y., Okuyucu A., Akbal A., Gökmen F., Coşar M. The protective effect of syringic acid on ischemia injury in rat brain. Turk. J. Med. Sci. 2015;45:233-240.

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    Tokmak M., Yuksel Y., Sehitoglu M.H., Güven M., Akman T., Aras A.B., Cosar M., Abbed K.M. The neuroprotective effect of syringic acid on spinal cord ischemia/reperfusion injury in rats. Inflammation. 2015;38:1969-1978.

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    Song M., Du Z., Lu G., Li P., Wang L. Syringic acid protects retinal ganglion cells against H2O2-induced apoptosis through the activation of Pl3K/Akt signaling pathway. Cell. Mol. Biol. 2016;62:50-54.

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    Cao Y., Zhang L., Sun S., Yi Z., Jiang X., Jia D. Neuroprotective effects of syringic acid against OGD/R-induced injury in cultured hippocampal neuronal cells. Int. J. Mol. Med. 2016;38:567-573.

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    Alfredsson C.F., Ding M., Liang Q.-L., Sundstrӧm B.E., Nånberg E. Ellagic acid induces a dose-and time-dependent depolarization of mitochondria and activation of caspase-9 and -3 in human neuroblastoma cells. Biomed. Pharmacother. 2014;68:129-135.

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    Alfredsson C.F., Rendel F., Liang Q.L., Sundstrӧm B.E., Nånberg E. Altered sensitivity to ellagic acid in neuroblastoma cells undergoing differentiation with 12-O-tetradecynoylphorbol-13-acetate and all-trans retinoic acid. Biomed. Pharmacother. 2015;76:39-45.

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    Farbood Y., Sarkaki A., Dolatshahi M., Mansouri S.M.T., Khodadadi A. Ellagic acid protects the brain against 6-hydroxydopamine induced neuroinflammation in a rat model of Parkinson’s disease. Basic Clin. Neurosci. 2015;6:15-22.

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    Khatri D., Juvekar A. Abrogation of locomotor impairment in a rotenone-induced Drosophila melanogaster and zebrafish model of Parkinson’s disease by ellagic acid and curcumin. Int. J. Nutr. Pharm. Neurol. Dis. 2016;6:90-96.

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    Mansouri M.T., Farbood Y., Naghizadeh B., Shabani S., Mirshekar M.A., Sarkaki A. Beneficial effects of ellagic acid against animal models of scopolamine- and diazepam-induced cognitive impairments. Pharm. Biol. 2016;54:1947-1953.

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    Liu H.P., Ren T.W., Yan W.J., Liu J., Liu R.B. Ellagic acid alleviates inflammatory pain and paclitaxel-induced neuropathic pain in murine models. Int. J. Clin. Exp. Med. 2016;9:12514-12520.

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    Chen S.Y., Zheng K., Wang Z.Q. Neuroprotective effects of ellagic acid on neonatal hypoxic brain injury via inhibition of inflammatory mediators and down-regulation of JNK/p38 MAPK activation. Trop. J. Pharm. Res. 2016;15:241-251.

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    Liu Q.S., Li S.R., Li K., Li X., Yin X., Pang Z. Ellagic acid improves endogenous neural stem cells proliferation and neurorestoration through Wnt/β-catenin signaling in vivo and in vitro. Mol. Nutr. Food Res. 2017;61.

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    Herrmann K. Occurrence and content of hydroxycinnamic and hydroxybenzoic acid compounds in foods. Crit. Rev. Sci. Food Nutr. 1989;28:315-347.

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    Bourne L.C., Rice-Evans C. Bioavailablility of ferulic acid. Biochem. Biophys. Res. Commun. 1998;253:222-227.

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    Zamora-Ros R., Knaze V., Rothwell J.A., Hémon B., Moskal A., Overvad K., Tjønneland A., Kyrø C., Fagherazzi G., Boutron-Ruault M.C., et al. Dietary polyphenol intake in Europe: The European prospective investigation into cancer and nutrition (EPIC) study. Eur. J. Nutr. 2016;55:1359-1375.

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    Tresserra-Rimbau A., Medina-Remón A., Pérez-Jiménez J., Martínez-González M.A., Covas M.I., Corella D., Salas-Salvadó J., Gómez-Gracia E., Lapetra J., Arós F., et al. Dietary intake and major food sources of polyphenols in a Spanish population at high cardiovascular risk: The PREDIMED study. Nutr. Metab. Cardiovasc. Dis. 2013;23:953-959.

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    Ferruzzi M.G., Lobo J.K., Janle E.M., Cooper B., Simon J.E., Wu Q.L., Welch C., Ho L., Weaver C., Pasinetti G.M. Bioavailability of gallic acid and catechins from grape seed polyphenol extract is improved by repeated dosing in rats: implications for treatment in Alzheimer’s disease. J. Alzheimers Dis. 2009;18:113-124.

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    Zhang Y.J., Wu L., Zhang Q.L., Li J., Yin F.X., Yuan Y. Pharmacokinetics of phenolic compounds of Danshen extract in rat blood and brain by microdialysis sampling. J. Ethnopharmacol. 2011;136:129-136.

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    Margalef M., Pons Z., Bravo F.I., Muguerza B., Arola-Arnal A. Tissue distribution of rat flavanol metabolites at different doses. J. Nutr. Biochem. 2015;26:987-995.

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    Del Bo C., Ciapellano S., Klimis-Zacas D., Martini D., Gardana C., Riso P., Porrini M. Anthocyanin absorption, metabolism, and distribution from a wild blueberry-enriched diet (Vaccinium angustifolium) is affected by diet duration in the Sprague-Dawley rat. J. Agric. Food Chem. 2010;58:2491-2497.

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    Wang D., Ho L., Faith J., Ono K., Janle E.M., Lachcik P.J., Cooper B.R., Jannasch A.H., D’Arcy B.R., Williams B.A., et al. Role of intestinal microbiota in the generation of polyphenol derived phenolic acid mediated attenuation of Alzheimer’s disease β-amyloid oligomerization. Mol. Nutr. Food. Res. 2015;59:1025-1040.

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    Chang M.X., Xu L.Y., Tao J.S., Feng Y. Metabolism and pharmacokinetics of ferulic acid in rats. China J. Chin. Mater. Medica. 1993;18:300-2319.

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    Wu K., Wang Z.Z., Liu D., Qi X.R. Pharmacokinetics, brain distribution, release and blood-brain barrier transport of Shunaoxin pills. J. Ethnopharmacol. 2014;151:1133-1140.

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    Pinheiro Fernandes F.D., Fontenele Menezes A.P., de Sousa Neves J.C., Fonteles A.A., da Silva A.T., de Araújo R.P., Santos do Carmo M.R., de Souza C.M., de Andrade G.M. Caffeic acid protects mice from memory deficits induced by focal cerebral ischemia. Behav. Pharmacol. 2014;25:637-647.

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    Ritschel W.A., Starzacher A., Sabouni A., Hussain A.S., Koch H.P. Percutaneous absorption of rosmarinic acid in the rat. Method. Find. Exp. Clin. Pharmacol. 1989;11:345-352.

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    Yan J.J., Cho J.Y., Kim H.S., Kim K.L., Jung J.S., Huh S.O., Suh H.W., Kim Y.H., Song D.K. Protection against b-amyloid peptide toxicity in vivo with long-term administration of ferulic acid. Br. J. Pharmacol. 2001;133:89-96.

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    Zhao J., Pati S., Redell J.B., Zhang M., Moore A.N., Dash P.K. Caffeic acid phenethyl ester protects blood-brain barrier integrity and reduces contusion volume in rodent models of traumatic brain injury. J. Neurotraum. 2012;29:1209-1218.

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    Vauzour D., Vafeiadou K., Corona G., Pollard S.E., Tzounis X., Spencer J.P. Champagne wine polyphenols protect primary cortical neurons against peroxynitrite-induced injury. J. Agric. Food Chem. 2007;55:2854-2860.

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    Luan H., Kan Z., Xu Y., Lv C., Jiang W. Rosmarinic acid protects against experimental diabetes with cerebral ischemia: relation to inflammation response. J. Neuroinflamm. 2013;10.

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    Scapagnini G., Foresti R., Calabrese V., Giuffrida Stella A.M., Green C.J., Motterlini R. Caffeic acid phenethyl ester and curcumin: A novel class of heme oxygenase-1 inducers. Mol. Pharmacol. 2002;3:554-561.

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    Scapagnini G., Butterfield D.A., Colombrita C., Sultana R., Pascale A., Calabrese V. Ethyl ferulate, a lipophilic polyphenol, induces HO-1 and protects rat neurons against oxidative stress. Antioxid. Redox Signal. 2004;6:811-818.

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