Phytochemical study of oleuropein and its therapeutic effects in improving seizure, oxidative stress and cognitive disorder in pentylenetetrazole kindling mouse model of epilepsy

Document Type : Research article

Authors

1 Cellular and Molecular Research Center, Basic Health Sciences Institute, Shahrekord University of Medical Sciences, Shahrekord, Iran.

2 Medical Plants Research Center, Basic Health Sciences Institute, Shahrekord University of Medical Sciences, Shahrekord Iran.

3 Department of Seafood Processing, Faculty of Marine Sciences, Tarbiat Modares University, Noor, Iran.

4 Medical Plants Research Center, Basic Health Sciences Institute, Shahrekord University of Medical Sciences, Shahrekord, Iran.

Abstract

Prolonged epileptic seizures are the cause of neuronal death and brain damage. Lesions in different regions of the brain can lead to memory loss and cognitive disorders. It is therefore essential to seek out new neuroprotective drugs. Our aim was to investigate the therapeutic effects of oleuropein to improve seizure, oxidative stress and cognitive disorder in pentylenetetrazole (PTZ) kindling mouse model of epilepsy.
Mice were randomly assigned to four groups; (1) PTZ group that intraperitoneally received PTZ for 10 days, (2) oleuropein group that received oleuropein (20mg/kg) 30 minutes before PTZ administration, (3) diazepam group that received diazepam 30 minutes before PTZ administration and (4) flumazenil group that was administered with flumazenil and then oleuropein 30 minutes before PTZ administration. Epilepsy severity was determined after final administration of PTZ. Then, the hippocampal tissue was removed and stored at -70°C to measure the interleukin-1 (IL-1) and glutamate transporter 1 (GLT-1) gene expression.
Oleuropein treatment caused a significant increase in seizure latency and a significant decrease in total frequencies of head ticks, head and upper limbs seizures, the whole body seizures, frequent spinning and jumping and tonic seizures in PTZ receiving mice. IL-1 expression decreased and GLT-1 levels did not change significantly in oleuropein group. Oleuropein treatment caused significant improvement of passive avoidance memory in PTZ receiving mice in shuttle box test.  Oleuropein can decrease PTZ-induced seizures and memory disorders due to its antioxidant and anti-inflammatory properties and thus can be used to produce antiepileptic drugs.

Graphical Abstract

Phytochemical study of oleuropein and its therapeutic effects in improving seizure, oxidative stress and cognitive disorder in pentylenetetrazole kindling mouse model of epilepsy

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References


 (1) Suleymanova E, Gulyaev M and Chepurnova N.Ginseng extract attenuates early MRI changesafter status epilepticus and decreases subsequentreduction of hippocampal volume in the rat brain.Epilepsy. Res. (2014) 108: 223-31.
(2) André V, Dubé C, François J, Leroy C, RigoulotMA, Roch C, Namer IJ and Nehlig A. Pathogenesisand Pharmacology of Epilepsy in the Lithium‐pilocarpine Model. Epilepsia (2007) 48: 41-7.
 (3)Brandt C, Gastens AM, Zhen Sun M, HausknechtM and Löscher W. Treatment with valproate afterstatus epilepticus: effect on neuronal damage,epileptogenesis, and behavioral alterations in rats.Neuropharmacology (2006) 51: 789-804.
(4) Vezzani A. Epilepsy and inflammation in the brain:overview and pathophysiology. Epilepsy Curr.(2014) 14: 3-7.
(5) Vezzani A, French J, Bartfai T and Baram TZ. Therole of inflammation in epilepsy. Nat. Rev. Neurosci.(2011) 7: 31-40.
(6) Rahimi N, Delfan B, Motamed-Gorji N and DehpourAR. Effects of oleuropein on pentylenetetrazolinduced seizures in mice: involvement of opioidergicand nitrergic systems. J. Nat. Med. (2017) 71: 389-96.
(7) Pourkhodadad S, Alirezaei M, Moghaddasi M,Ahmadvand H, Karami M, Delfan B and KhanipourZ. Neuroprotective effects of oleuropein againstcognitive dysfunction induced by colchicine inhippocampal CA1 area in rats. J. Physiol. SCI.(2016) 66: 397-405.
(8) Dekanski D, Selaković V, Piperski V, Radulović Ž,Korenić A and Radenović L. Protective effect ofolive leaf extract on hippocampal injury induced bytransient global cerebral ischemia and reperfusionin Mongolian gerbils. Phytomedicine (2011) 18:1137-43.109Asgharzade S et al. / IJPR (2020), 19 (1): 98-110
(9) De La Cruz JP, Del Río S, Arrebola MM, LópezVillodres JA, Jebrouni N and González-Correa JA.Effect of virgin olive oil plus acetylsalicylic acid onbrain slices damage after hypoxia-reoxygenation inrats with type 1-like diabetes mellitus. Neurosci. Lett.(2010) 471: 89-93.
(10) Kuem N, Song SJ, Yu R, Yun JW and Park T.Oleuropein attenuates visceral adiposity in high‐fatdiet‐induced obese mice through the modulationof WNT10b‐and galanin‐mediated signalings.Mol. Nutr. Food Res. (2014) 58: 2166-76.
(11) Khalatbary A and GhR Z. Anti-inflammatoryeffect of oleuropein in experimental rat spinal cordtrauma. IRCMJ (2012) 14: 229-34.
(12) Khalatbary AR, Ghaffari E and MohammadnegadB. Protective Role of Oleuropein against AcuteDeltamethrin-Induced Neurotoxicity in Rat Brain.Iran. Biomed. J. (2015) 19: 247.
(13) Khalatbary AR. Olive oil phenols andneuroprotection. Nutr. Neurosci. (2013) 16: 243-9.
(14) Asgharzade S, Rafieian-kopaei M, Mirzaeian A,Reiisi S and Salimzadeh L. Aloe vera toxic effects:expression of inducible nitric oxide synthase(iNOS) in testis of Wistar rat. IJBMS (2015) 18:967.
(15) Zulueta A, Esteve MJ and Frígola A. ORACand TEAC assays comparison to measure theantioxidant capacity of food products. Food Chem.(2009) 114: 310-6.
(16) Wang J, Zhang Q, Zhang Z and Li Z. Antioxidantactivity of sulfated polysaccharide fractionsextracted from Laminaria japonica. Int. J. Biol.Macromol. (2008) 42: 127-32.
(17) Genskowsky E, Puente LA, Pérez‐Álvarez JA,Fernández‐López J, Muñoz LA and Viuda‐Martos M. Determination of polyphenolic profile,antioxidant activity and antibacterial propertiesof maqui [Aristotelia chilensis (Molina) Stuntz]a Chilean blackberry. J. Sci. Food Agric. (2016)96:4235-42.
(18) Nikoo M, Benjakul S, Ehsani A, Li J, Wu F, Yang N,Baocai X, Zhengyu J and Xueming X. Antioxidantand cryoprotective effects of a tetrapeptide isolatedfrom Amur sturgeon skin gelatin.J. Funct. Foods(2014) 7:609-20.
(19) Koutroumanidou E, Kimbaris A, Kortsaris A,Bezirtzoglou E, Polissiou M, Charalabopoulos Kand Pagonopoulou O. Increased seizure latency anddecreased severity of pentylenetetrazol-inducedseizures in mice after essential oil administration.Epilepsy Res. Treat. (2013) 2013: 532657.
(20) Wilkerson A and Levin E. Ventral hippocampaldopamine D 1 and D 2 systems and spatial workingmemory in rats. Neuroscience (1999) 89:743-9.
(21) Benzie IF and Strain JJ. The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal. Biochem. (1996) 239: 70-6.
(22) Rabiei Z, Mokhtari S, Asgharzade S, Gholami M, Rahnama S and Rafieian-kopaei M. Inhibitory effect of Thymus vulgaris extract on memory impairment induced by scopolamine in rat. Asian Pac. J. Trop. Bimed. (2015) 5: 845-51.
(23) Pahuja M, Mehla J, Reeta K, Joshi S and GuptaYK. Hydroalcoholic extract of Zizyphus jujuba ameliorates seizures, oxidative stress, and cognitive
impairment in experimental models of epilepsy in
rats. Epilepsy Behav. (2011) 21: 356-63.
(24) Kaputlu İ and Uzbay T. L-NAME inhibits pentylenetetrazole and strychnine-induced seizures
in mice. Brain Res. (1997) 753: 98-101.
(25) Payandemehr B, Rahimian R, Bahremand A, Ebrahimi A, Saadat S, Moghaddas P, Fadakar
K, Derakhshanian H and Dehpour AR. Role of nitric oxide in additive anticonvulsant effects ofagmatine and morphine. Physiol. Behav. (2013) 118: 52-7.
(26) Campolo M, Di Paola R, Impellizzeri D, Crupi R, Morittu VM, Procopio A, Perri E, Britti D, Peli A, Esposito E and Cuzzocrea S. Effects of a polyphenol present in olive oil, oleuropein aglycone, in a murine model of intestinal ischemia/ reperfusion injury. J. Leukoc. Biol. (2013) 93: 277- 87.
(27) Hassen I, Casabianca H and Hosni K. Biological activities of the natural antioxidant oleuropein: Exceeding the expectation–A mini-review. J. Funct. Foods (2015) 18: 926-40.
(28) Czerwińska M, Kiss AK and Naruszewicz M. A comparison of antioxidant activities of oleuropein and its dialdehydic derivative from olive oil, oleacein. Food Chem. (2012) 131: 940-7.
(29) Turrin NP and Rivest S. Innate immune reactionin response to seizures: implications for theneuropathology associated with epilepsy.Neurobiol. Dis. (2004)16: 321-34.
(30) Viviani B, Bartesaghi S, Gardoni F, VezzaniA, Behrens M, Bartfai T, Binaglia M, CorsiniE, Di Luca M, Galli CL and Marinovich M.Interleukin-1β enhances NMDA receptor mediatedintracellular calcium increase through activation of the Src family of kinases. J. Neurosci. (2003) 23: 8692-700.
(31) Balosso S, Maroso M, Sanchez-Alavez M, Ravizza T, Frasca A, Bartfai T and Vezzani A. A novel nontranscriptional pathway mediates the proconvulsive effects of interleukin-1β. Brain (2008)131:3256- 65.
(32) Impellizzeri D, Esposito E, Mazzon E, PaternitiI, Di Paola R, Bramanti P, Morittu VM, ProcopioA, Perri E, Britti D and Cuzzocrea S. The effectsof a polyphenol present in olive oil, oleuropeinaglycone, in an experimental model of spinal cordinjury in mice. Biochem. Pharmacol. (2012) 83:1413-26.
(33) González-Correa J, Muñoz-Marín J, Arrebola M,Guerrero A, Narbona F, López-Villodres J andDe La Cruz JP. Dietary virgin olive oil reducesoxidative stress and cellular damage in rat brain slices subjected to hypoxia–reoxygenation. Lipids
(2007) 42: 921-9.
(34) Shetty AK and Hattiangady B. Neural Stem Cell Therapy for Easing Status Epilepticus Induced Hippocampus Dysfunction and Chronic Temporal
Lobe Epilepsy. Neural Stem Cells in Health and Disease (2016) 409-38.
(35) Gupta Y, Kumar MV and Srivastava A. Effect of Centella asiatica on pentylenetetrazole-induced kindling, cognition and oxidative stress in rats. Pharmacol. Biochem. Behav. (2003) 74: 579-85.
(36) Agarwal NB, Agarwal NK, Mediratta PK and Sharma KK. Effect of lamotrigine, oxcarbazepine and topiramate on cognitive functions and oxidative stress in PTZ-kindled mice. Seizure (2011) 20: 257-62.
Iranian Journal of Pharmaceutical Research
Volume 19, Issue 1
Winter 2020
Pages 98-110

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