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Current Molecular Pharmacology

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ISSN (Print): 1874-4672
ISSN (Online): 1874-4702

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Research Article

Ferulic Acid Attenuates Kainate-induced Neurodegeneration in a Rat Poststatus Epilepticus Model

Author(s): Ali Jaafari Suha, Seyed Shahabeddin Sadr*, Mehrdad Roghani, Saeed Mohammadian Haftcheshmeh, Safoura Khamse* and Amir Abbas Momtazi-Borojeni

Volume 16, Issue 2, 2023

Published on: 20 May, 2022

Article ID: e250222201434 Pages: 10

DOI: 10.2174/1874467215666220225093737

Price: $65

Abstract

Background and Aims: Increasing research evidence indicates that temporal lobe epilepsy (TLE) induced by kainic acid (KA) has high pathological similarities with human TLE. KA induces excitotoxicity (especially in the acute phase of the disease), which leads to neurodegeneration and epileptogenesis through oxidative stress and inflammation. Ferulic acid (FA) is one of the well-known phytochemical compounds that have shown potential antioxidant and anti-inflammatory properties and promise in treating several diseases. The current study set out to investigate the neuroprotective effects of FA in a rat model of TLE.

Methods: Thirty-six male Wistar rats were divided into four groups. Pretreatment with FA (100 mg/kg/day p.o.) started one week before the intrahippocampal injection of KA (0.8 μg/μl, 5μl). Seizures were recorded and evaluated according to Racine’s scale. Oxidative stress was assessed by measuring its indicators, including malondialdehyde (MDA), nitrite, and catalase. Histopathological evaluations including Nissl staining and immunohistochemical staining of cyclooxygenase-2 (COX-2), and neural nitric oxide synthases (nNOS) were performed for the CA3 region of the hippocampus.

Results: Pretreatment with FA significantly attenuates the severity of the seizure and prevents neuronal loss in the CA3 region of the hippocampus in rats with KA-induced post-status epilepticus. Also, nitrite concentration and nNOS levels were markedly diminished in FA-pretreated animals compared to non-pretreated epileptic rats.

Conclusion: Our findings indicated that neuroprotective properties of FA, therefore, could be considered a valuable therapeutic supplement in treating TLE.

Keywords: Epilepsy, ferulic acid, kainic acid, oxidative stress, seizure, neurodegeneration.

[1]
Shetty, A.K. Progress in cell grafting therapy for temporal lobe epilepsy. Neurotherapeutics, 2011, 8(4), 721-735.
[http://dx.doi.org/10.1007/s13311-011-0064-y] [PMID: 21892793]
[2]
Rattka, M.; Brandt, C. Lِöscher, W. The intrahippocampal kainate model of temporal lobe epilepsy revisited: epileptogenesis, behavioral and cognitive alterations, pharmacological response, and hippoccampal damage in epileptic rats. Epilepsy Res., 2013, 103(2-3), 135-152.
[http://dx.doi.org/10.1016/j.eplepsyres.2012.09.015] [PMID: 23196211]
[3]
Lévesque, M.; Avoli, M. The kainic acid model of temporal lobe epilepsy. Neurosci. Biobehav. Rev., 2013, 37(10 Pt 2), 2887-2899.
[http://dx.doi.org/10.1016/j.neubiorev.2013.10.011] [PMID: 24184743]
[4]
Vezzani, A.; Friedman, A.; Dingledine, R.J. The role of inflammation in epileptogenesis. Neuropharmacology, 2013, 69, 16-24.
[http://dx.doi.org/10.1016/j.neuropharm.2012.04.004] [PMID: 22521336]
[5]
Baluchnejadmojarad, T.; Roghani, M. Coenzyme q10 ameliorates neurodegeneration, mossy fiber sprouting, and oxidative stress in intrahippocampal kainate model of temporal lobe epilepsy in rat. J. Mol. Neurosci., 2013, 49(1), 194-201.
[http://dx.doi.org/10.1007/s12031-012-9886-2] [PMID: 23008120]
[6]
Pitkänen, A.; Lukasiuk, K. Molecular and cellular basis of epileptogenesis in symptomatic epilepsy. Epilepsy Behav., 2009, 14(Suppl. 1), 16-25.
[http://dx.doi.org/10.1016/j.yebeh.2008.09.023]
[7]
Rowley, S.; Patel, M. Mitochondrial involvement and oxidative stress in temporal lobe epilepsy. Free Radic. Biol. Med., 2013, 62, 121-131.
[http://dx.doi.org/10.1016/j.freeradbiomed.2013.02.002] [PMID: 23411150]
[8]
Bruce, A.J.; Baudry, M. Oxygen free radicals in rat limbic structures after kainate-induced seizures. Free Radic. Biol. Med., 1995, 18(6), 993-1002.
[http://dx.doi.org/10.1016/0891-5849(94)00218-9] [PMID: 7628735]
[9]
Gorter, J.A.; Gonçalves Pereira, P.M.; van Vliet, E.A.; Aronica, E.; Lopes da Silva, F.H.; Lucassen, P.J. Neuronal cell death in a rat model for mesial temporal lobe epilepsy is induced by the initial status epilepticus and not by later repeated spontaneous seizures. Epilepsia, 2003, 44(5), 647-658.
[http://dx.doi.org/10.1046/j.1528-1157.2003.53902.x] [PMID: 12752463]
[10]
Fujikawa, D.G. Prolonged seizures and cellular injury: understanding the connection. Epilepsy Behav., 2005, 7(Suppl. 3), S3-S11.
[http://dx.doi.org/10.1016/j.yebeh.2005.08.003]
[11]
Khamse, S.; Sadr, S.S.; Roghani, M.; Hasanzadeh, G.; Mohammadian, M. Rosmarinic acid exerts a neuroprotective effect in the kainate rat model of temporal lobe epilepsy: Underlying mechanisms. Pharm. Biol., 2015, 53(12), 1818-1825.
[http://dx.doi.org/10.3109/13880209.2015.1010738] [PMID: 25874386]
[12]
Khamse, S.; Sadr, S.S.; Roghani, M.; Rashvand, M.; Mohammadian, M.; Marefati, N.; Harati, E.; Ebrahimi, F. The effect of rosmarinic acid on apoptosis and nNOS immunoreactivity following intrahippocampal kainic acid injections in rats. Basic Clin. Neurosci., 2020, 11(1), 41-48.
[http://dx.doi.org/10.32598/bcn.9.10.340] [PMID: 32483474]
[13]
Fatahian, A.; Haftcheshmeh, S.M.; Azhdari, S.; Farshchi, H.K.; Nikfar, B.; Momtazi-Borojeni, A.A. promising anti-atherosclerotic effect of berberine: Evidence from in vitro, in vivo, and clinical studies. Rev. Physiol. Biochem. Pharmacol., 2020, 178, 83-110.
[http://dx.doi.org/10.1007/112_2020_42] [PMID: 32789786]
[14]
Mohammadian Haftcheshmeh, S.; Momtazi-Borojeni, A.A. Immunomodulatory therapeutic effects of curcumin in rheumatoid arthritis. Autoimmun. Rev., 2020, 19(8), 102593.
[http://dx.doi.org/10.1016/j.autrev.2020.102593] [PMID: 32540449]
[15]
Mohammadian Haftcheshmeh, S.; Karimzadeh, M.R.; Azhdari, S.; Vahedi, P.; Abdollahi, E.; Momtazi-Borojeni, A.A. Modulatory effects of curcumin on the atherogenic activities of inflammatory monocytes: Evidence from in vitro and animal models of human atherosclerosis. Biofactors, 2020, 46(3), 341-355.
[http://dx.doi.org/10.1002/biof.1603] [PMID: 31875344]
[16]
Rahimi, K.; Hassanzadeh, K.; Khanbabaei, H.; Haftcheshmeh, S.M.; Ahmadi, A.; Izadpanah, E.; Mohammadi, A.; Sahebkar, A. Curcumin: a dietary phytochemical for targeting the phenotype and function of dendritic cells. Curr. Med. Chem., 2021, 28(8), 1549-1564.
[http://dx.doi.org/10.2174/0929867327666200515101228] [PMID: 32410550]
[17]
Das, U.; Manna, K.; Sinha, M.; Datta, S.; Das, D.K.; Chakraborty, A.; Ghosh, M.; Saha, K.D.; Dey, S. Role of ferulic acid in the amelioration of ionizing radiation induced inflammation: a murine model. PLoS One, 2014, 9(5), e97599.
[http://dx.doi.org/10.1371/journal.pone.0097599] [PMID: 24854039]
[18]
Mancuso, C.; Santangelo, R. Ferulic acid: pharmacological and toxicological aspects. Food Chem. Toxicol., 2014, 65, 185-195.
[http://dx.doi.org/10.1016/j.fct.2013.12.024] [PMID: 24373826]
[19]
Yeh, C.T.; Yen, G.C. Induction of hepatic antioxidant enzymes by phenolic acids in rats is accompanied by increased levels of multidrug resistance-associated protein 3 mRNA expression. J. Nutr., 2006, 136(1), 11-15.
[http://dx.doi.org/10.1093/jn/136.1.11] [PMID: 16365051]
[20]
Paxinos, G.; Watson, C. The rat brain atlas; Academic Press, Inc.: San Diego, Calif, 1986.
[21]
Racine, R.J. Modification of seizure activity by electrical stimulation. I. After-discharge threshold. Electroencephalogr. Clin. Neurophysiol., 1972, 32(3), 269-279.
[http://dx.doi.org/10.1016/0013-4694(72)90176-9] [PMID: 4110396]
[22]
Nassiri-Asl, M.; Naserpour Farivar, T.; Abbasi, E.; Sadeghnia, H.R.; Sheikhi, M.; Lotfizadeh, M.; Bazahang, P. Effects of rutin on oxidative stress in mice with kainic acid-induced seizure. J. Integr. Med., 2013, 11(5), 337-342.
[http://dx.doi.org/10.3736/jintegrmed2013042] [PMID: 24063781]
[23]
Roghani, M.; Baluchnejadmojarad, T. Chronic epigallocatechin-gallate improves aortic reactivity of diabetic rats: underlying mechanisms. Vascul. Pharmacol., 2009, 51(2-3), 84-89.
[http://dx.doi.org/10.1016/j.vph.2009.04.003] [PMID: 19393342]
[24]
Beers, R.F., Jr; Sizer, I.W. A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J. Biol. Chem., 1952, 195(1), 133-140.
[http://dx.doi.org/10.1016/S0021-9258(19)50881-X] [PMID: 14938361]
[25]
Baluchnejadmojarad, T.; Roghani, M. Chronic epigallocatechin-3-gallate ameliorates learning and memory deficits in diabetic rats via modulation of nitric oxide and oxidative stress. Behav. Brain Res., 2011, 224(2), 305-310.
[http://dx.doi.org/10.1016/j.bbr.2011.06.007] [PMID: 21699923]
[26]
Bradford, M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem., 1976, 72(1), 248-254.
[http://dx.doi.org/10.1016/0003-2697(76)90527-3] [PMID: 942051]
[27]
Ciceri, P.; Zhang, Y.; Shaffer, A.F.; Leahy, K.M.; Woerner, M.B.; Smith, W.G.; Seibert, K.; Isakson, P.C. Pharmacology of celecoxib in rat brain after kainate administration. J. Pharmacol. Exp. Ther., 2002, 302(3), 846-852.
[http://dx.doi.org/10.1124/jpet.302.3.846] [PMID: 12183639]
[28]
Yu, L.; Zhang, Y.; Ma, R.; Bao, L.; Fang, J.; Yu, T. Potent protection of ferulic acid against excitotoxic effects of maternal intragastric administration of monosodium glutamate at a late stage of pregnancy on developing mouse fetal brain. Eur. Neuropsychopharmacol., 2006, 16(3), 7-170.
[http://dx.doi.org/10.1016/j.euroneuro.2005.08.006]
[29]
Kim, S.R.; Daily, J.W., III; Lee, Y.E. Ferulic acid: a novel inhibitor of presynaptic glutamate release. J. Med. Food, 2013, 16(2), 95.
[http://dx.doi.org/10.1089/jmf.2013.1602.com] [PMID: 23402635]
[30]
Lin, T.Y.; Lu, C.W.; Huang, S.K.; Wang, S.J. Ferulic acid suppresses glutamate release through inhibition of voltage-dependent calcium entry in rat cerebrocortical nerve terminals. J. Med. Food, 2013, 16(2), 112-119.
[http://dx.doi.org/10.1089/jmf.2012.2387] [PMID: 23342970]
[31]
Cheng, C.Y.; Su, S.Y.; Tang, N.Y.; Ho, T.Y.; Lo, W.Y.; Hsieh, C.L. Ferulic acid inhibits nitric oxide-induced apoptosis by enhancing GABA(B1) receptor expression in transient focal cerebral ischemia in rats. Acta Pharmacol. Sin., 2010, 31(8), 889-899.
[http://dx.doi.org/10.1038/aps.2010.66] [PMID: 20644551]
[32]
Cheng, C-Y.; Ho, T-Y.; Lee, E-J.; Su, S-Y.; Tang, N-Y.; Hsieh, C-L. Ferulic acid reduces cerebral infarct through its antioxidative and anti-inflammatory effects following transient focal cerebral ischemia in rats. Am. J. Chin. Med., 2008, 36(6), 1105-1119.
[http://dx.doi.org/10.1142/S0192415X08006570] [PMID: 19051339]
[33]
Luo, Y.; Zhao, H.P.; Zhang, J.; Wang, J.; Yang, W.L.; Yang, M.; Liao, Z.G. Effect of ferulic acid on learning and memory impairments of vascular dementia rats and its mechanism of action. Yao Xue Xue Bao, 2012, 47(2), 256-260.
[PMID: 22512041]
[34]
Koh, P.O. Ferulic acid modulates nitric oxide synthase expression in focal cerebral ischemia. Lab. Anim. Res., 2012, 28(4), 273-278.
[http://dx.doi.org/10.5625/lar.2012.28.4.273] [PMID: 23326288]
[35]
Zeni, A.L.; Vandresen-Filho, S.; Dal-Cim, T.; Martins, W.C.; Bertoldo, D.B.; Maraschin, M.; Tasca, C.I. Aloysia gratissima prevents cellular damage induced by glutamatergic excitotoxicity. J. Pharm. Pharmacol., 2014, 66(9), 1294-1302.
[http://dx.doi.org/10.1111/jphp.12250] [PMID: 24707860]
[36]
Swamy, M.; Yusof, W.R.; Sirajudeen, K.N.; Mustapha, Z.; Govindasamy, C. Decreased glutamine synthetase, increased citrulline-nitric oxide cycle activities, and oxidative stress in different regions of brain in epilepsy rat model. J. Physiol. Biochem., 2011, 67(1), 105-113.
[http://dx.doi.org/10.1007/s13105-010-0054-2] [PMID: 20960085]
[37]
Kato, N.; Sato, S.; Yokoyama, H.; Kayama, T.; Yoshimura, T. Sequential changes of nitric oxide levels in the temporal lobes of kainic acid-treated mice following application of nitric oxide synthase inhibitors and phenobarbital. Epilepsy Res., 2005, 65(1-2), 81-91.
[http://dx.doi.org/10.1016/j.eplepsyres.2005.05.001] [PMID: 15979286]
[38]
Yasuda, H.; Fujii, M.; Fujisawa, H.; Ito, H.; Suzuki, M. Changes in nitric oxide synthesis and epileptic activity in the contralateral hippocampus of rats following intrahippocampal kainate injection. Epilepsia, 2001, 42(1), 13-20.
[http://dx.doi.org/10.1046/j.1528-1157.2001.083032.x] [PMID: 11207780]
[39]
Kashihara, K.; Sakai, K.; Marui, K.; Shohmori, T. Kainic acid may enhance hippocampal NO generation of awake rats in a seizure stage-related fashion. Neurosci. Res., 1998, 32(3), 189-194.
[http://dx.doi.org/10.1016/S0168-0102(98)00086-8] [PMID: 9875560]
[40]
Chuang, Y.C. Mitochondrial dysfunction and oxidative stress in seizure-induced neuronal cell death. Acta Neurol. Taiwan., 2010, 19(1), 3-15.
[PMID: 20711885]
[41]
Scheckel, K.A.; Degner, S.C.; Romagnolo, D.F. Rosmarinic acid antagonizes activator protein-1-dependent activation of cyclooxygenase-2 expression in human cancer and nonmalignant cell lines. J. Nutr., 2008, 138(11), 2098-2105.
[http://dx.doi.org/10.3945/jn.108.090431] [PMID: 18936204]
[42]
Zhang, H.J.; Sun, R.P.; Lei, G.F.; Yang, L.; Liu, C.X. Cyclooxygenase-2 inhibitor inhibits hippocampal synaptic reorganization in pilocarpine-induced status epilepticus rats. J. Zhejiang Univ. Sci. B, 2008, 9(11), 903-915.
[http://dx.doi.org/10.1631/jzus.B0820018] [PMID: 18988310]
[43]
Lee, J.; Kosaras, B.; Aleyasin, H.; Han, J.A.; Park, D.S.; Ratan, R.R.; Kowall, N.W.; Ferrante, R.J.; Lee, S.W.; Ryu, H.; Lee, J.; Kosaras, B.; Aleyasin, H.; Han, J.A.; Park, D.S.; Ratan, R.R.; Kowall, N.W.; Ferrante, R.J.; Lee, S.W.; Ryu, H. Role of cyclooxygenase-2 induction by transcription factor Sp1 and Sp3 in neuronal oxidative and DNA damage response. FASEB J., 2006, 20(13), 2375-2377.
[http://dx.doi.org/10.1096/fj.06-5957fje] [PMID: 17012241]

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