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Effects of Leontice leontopetalum and Bongardia chrysogonum on oxidative stress and neuroprotection in PTZ kindling epilepsy in rats
Corresponding Author(s) : Ozlem Ergul Erkec
Cellular and Molecular Biology,
Vol. 64 No. 15: Issue 15
Abstract
We investigated the effects of Leontice leontopetalum and Bongardia chrysogonum on apoptosis, gamma-aminobutyric acid (GABAA) receptor positive cell number, cyclin-B1 and bcl-2 levels and oxidative stress in pentylenetetrazol (PTZ) kindling in rats. Kindling was produced by subconvulsant doses of PTZ treatments in rats. Wistar albino rats were divided into 4 groups; Control, PTZ treated (PTZ), PTZ+L. leontopetalum extract treated (PTZ+LLE) and PTZ+B. chrysogonum extract treated (PTZ+BCE) groups. Extracts were given a dose (200 mg/kg) 2h before each PTZ injection. PTZ treatment significantly decreased the glutathione peroxidase (GSH-Px), superoxide dismutase (SOD) activities and bcl-2 levels and increased the total oxidant status (TOS), malondialdehyde (MDA), cyclin B1, oxidative stress index (OSI) and number of neurons that expressed GABAA receptors when compared to the control. LLE and BCE possessed antioxidant activity in the brain and ameliorated PTZ induced oxidative stress, decreased cyclin-B1, increased bcl-2 levels, and kept the GABAA receptor number similar to that of the control despite the PTZ application.
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- Taiwe GS, Moto FC, Ayissi ER, Ngoupaye GT, Njapdounke JS, Nkantchoua GC, et al. Effects of a lyophilized aqueous extract of Feretia apodanthera Del. (Rubiaceae) on pentylenetetrazole-induced kindling, oxidative stress, and cognitive impairment in mice. Epilepsy Behav 2015;43:100-8.
- Shin E-J, Jeong JH, Chung YH, Kim W-K, Ko K-H, Bach J-H, et al. Role of oxidative stress in epileptic seizures. Neurochem Int 2011;59(2):122-37.
- Ekonomou A, Smith AL, Angelatou F. Changes in AMPA receptor binding and subunit messenger RNA expression in hippocampus and cortex in the pentylenetetrazole-induced ‘kindling'model of epilepsy. Mol Brain Res 2001;95(1-2):27-35.
- Pavlova T, Stepanichev M, Gulyaeva N. Pentylenetetrazole kindling induces neuronal cyclin B1 expression in rat hippocampus. Neurosci Lett. 2006;392(1-2):154-8.
- Popova M, Aniol V, Lazareva N, Stepanichev MY, Gulyaeva N. Neurodegenerative changes in rat hippocampal fields during the development of pentylenetetrazole kindling. Neurosci Behav Physiol 2013;43(5):592-6.
- Nagy Z, Esiri MM. Neuronal cyclin expression in the hippocampus in temporal lobe epilepsy. Exp Neurol 1998;150(2):240-7.
- Waldbaum S, Patel M. Mitochondria, oxidative stress, and temporal lobe epilepsy. Epilepsy Res 2010;88(1):23-45.
- Martinc B, Grabnar I, Vovk T. The role of reactive species in epileptogenesis and influence of antiepileptic drug therapy on oxidative stress. Curr Neuropharmacol 2012;10(4):328-43.
- Snehunsu A, Ghosal C, Kandwal M, Yadav PK, Nayak BS, Rao KR, et al. 1-Triacontanol cerotate; isolated from Marsilea quadrifolia Linn. ameliorates reactive oxidative damage in the frontal cortex and hippocampus of chronic epileptic rats. J Ethnopharmacol 2015;172:80-4.
- Pahwa P, Goel RK. Ameliorative effect of Asparagus racemosus root extract against pentylenetetrazol-induced kindling and associated depression and memory deficit. Epilepsy Behav 2016;57(Pt A):196-201.
- í–zgökçe F, í–zçelik H. Ethnobotanical aspects of some taxa in East Anatolia, Turkey. Econ Bot
- ;58(4):697.
- Kolak U, Hacibekiroglu I, Boga M, í–zgökçe F, íœnal M, Choudhary M, et al. Phytochemical Investigation of Leontice leontopetalum L. subsp. ewersmannii with Antioxidant and Anticholinesterase Activities. Rec Nat Prod 2011;5(4):309.
- Arslan A, Cakmak E, Ozaslan M, Cengiz B, Bagci C, Tarakcioglu M, et al. The effects of Bongardia chrysogonum (L) spach extract on the serum parameters and liver, kidney, and spleen tissues in rats. Biotechnol Biotechnol Equip 2005;19(3):170-9.
- Abuhamdah SMA, Abuirmeileh AN, Thaer F, Al-Olimat S, Abdel E, Chazot PL. Anti-convulsant Effects of Bongardia chrysogonum L. Tuber in the Pentylenetetrazole-induced Seizure Model. Int J Pharmacol 2018;14(1):127-35.
- Ullah I, Badshah H, Naseer MI, Lee HY, Kim MO. Thymoquinone and vitamin C attenuates pentylenetetrazole-induced seizures via activation of GABAB1 receptor in adult rats cortex and hippocampus. Neuromolecular Med 2015;17(1):35-46.
- Erel O. A novel automated direct measurement method for total antioxidant capacity using a new generation, more stable ABTS radical cation. Clin Biochem 2004;37(4):277-85.
- Erel O. A new automated colorimetric method for measuring total oxidant status. Clin Biochem 2005;38(12):1103-11.
- Altindag O, Erel O, Soran N, Celik H, Selek S. Total oxidative/anti-oxidative status and relation to bone mineral density in osteoporosis. Rheumatol Int 2008;28(4):317-21.
- Yoshioka T, Kawada K, Shimada T, Mori M. Lipid peroxidation in maternal and cord blood and protective mechanism against activated-oxygen toxicity in the blood. Am J Obstet Gynecol 1979;135(3):372-6.
- Spitz DR, Oberley LW. An assay for superoxide dismutase activity in mammalian tissue homogenates. Anal Biochem 1989; 179:8-18.
- Paglia DE, Valentine WN. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 1967; 70: 158-169.
- Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976; 72: 248-254.
- García-López P, Garzón-de la Mora P, Meneses-Medina M, Ramírez Z, Moreno-Sandoval V, Toro-Ureña Id, et al., editors. Lupinus exaltatus obtained lupanine and its measured anticonvulsive activity. Lupin crops: an opportunity for today, a promise for the future Proceedings of the 13th International Lupin Conference, PoznaÅ„, Poland, 6-10 June 2011; 2011: International Lupin Association.
- Pal D, Sannigrahi S, Mazumder UK. Analgesic and anticonvulsant effects of saponin isolated from the leaves of Clerodendrum infortunatum Linn. in mice. Indian J Exp Biol 2009; 47: 743-747.
- Kabuto H, Yokoi I, Mori A. Monoamine metabolites, iron induced seizures, and the anticonvulsant effect of tannins. Neurochem Res 1992; 17: 585-590.
- Eisenman SW, Zaurov DE, Struwe L. Medicinal Plants of Central Asia: Uzbekistan and Kyrgyzstan: Springer Science & Business Media 2012.
- Herrup K, Neve R, Ackerman SL, Copani A. Divide and die: cell cycle events as triggers of nerve cell death. J Neurosci. 2004; 24: 9232-9239.
- Hoh NZ, Wagner AK, Alexander SA, Clark RB, Beers SR, Okonkwo DO, et al. BCL2 genotypes: functional and neurobehavioral outcomes after severe traumatic brain injury. J Neurotrauma 2010; 27: 1413-1427.
- Luo Z, Fang Y, Zhang L. The effects of antiepileptic drug valproic acid on apoptosis of hippocampal neurons in epileptic rats. Pak J Pharm Sci 2015; 28: 319-324.
- Rahmati B, Khalili M, Roghani M, Ahghari P. Anti-epileptogenic and antioxidant effect of Lavandula officinalis aerial part extract against pentylenetetrazol-induced kindling in male mice. J Ethnopharmacol 2013; 148: 152-157.
- Ilhan A, Gurel A, Armutcu F, Kamisli S, Iraz M. Antiepileptogenic and antioxidant effects of Nigella sativa oil against pentylenetetrazol-induced kindling in mice. Neuropharmacology 2005; 49: 456-464.
- Zeng LH, Zhang HD, Xu CJ, Bian YJ, Xu XJ, Xie QM, et al. Neuroprotective effects of flavonoids extracted from licorice on kainate-induced seizure in mice through their antioxidant properties. J Zhejiang Univ Sci B 2013; 14: 1004-12.
- Erdogan H, Ekici F, Katar M, Kesici H, Aslan H. The protective effects of endothelin-A receptor antagonist BQ-123 in pentylenetetrazole-induced seizure in rats. Hum Exp Toxicol 2014; 33: 1008-16.
- Kiasalari Z, Khalili M, Roghani M, Sadeghian A. Antiepileptic and Antioxidant Effect of Brassica nigra on Pentylenetetrazol-Induced Kindling in Mice. Iran J Pharm Res 2012; 11: 1209-1217.
- Tutanc M, Aras M, Dokuyucu R, Altas M, Zeren C, Arica V, et al. Oxidative Status in Epileptic Children Using Carbamazepine. Iran J Pediatr 2015; 25(6).
- Loup F. GABAA Receptors in Human Temporal Lobe Epilepsy. Epileptologie 2006; 23: 187-194.
- Walsh LA, Li M, Zhao TJ, Chiu TH, Rosenberg HC. Acute pentylenetetrazol injection reduces rat GABAA receptor mRNA levels and GABA stimulation of benzodiazepine binding with No effect on benzodiazepine binding site density. J Pharmacol Exp Ther 1999; 289: 1626-1633.
- Meral I, Esrefoglu M, Dar KA, Ustunova S, Aydin MS, Demirtas M, et al. Effects of Nigella sativa on apoptosis and GABAA receptor density in cerebral cortical and hippocampal neurons in pentylenetetrazol induced kindling in rats. Biotech Histochem 2016; 91: 493-500.
References
Taiwe GS, Moto FC, Ayissi ER, Ngoupaye GT, Njapdounke JS, Nkantchoua GC, et al. Effects of a lyophilized aqueous extract of Feretia apodanthera Del. (Rubiaceae) on pentylenetetrazole-induced kindling, oxidative stress, and cognitive impairment in mice. Epilepsy Behav 2015;43:100-8.
Shin E-J, Jeong JH, Chung YH, Kim W-K, Ko K-H, Bach J-H, et al. Role of oxidative stress in epileptic seizures. Neurochem Int 2011;59(2):122-37.
Ekonomou A, Smith AL, Angelatou F. Changes in AMPA receptor binding and subunit messenger RNA expression in hippocampus and cortex in the pentylenetetrazole-induced ‘kindling'model of epilepsy. Mol Brain Res 2001;95(1-2):27-35.
Pavlova T, Stepanichev M, Gulyaeva N. Pentylenetetrazole kindling induces neuronal cyclin B1 expression in rat hippocampus. Neurosci Lett. 2006;392(1-2):154-8.
Popova M, Aniol V, Lazareva N, Stepanichev MY, Gulyaeva N. Neurodegenerative changes in rat hippocampal fields during the development of pentylenetetrazole kindling. Neurosci Behav Physiol 2013;43(5):592-6.
Nagy Z, Esiri MM. Neuronal cyclin expression in the hippocampus in temporal lobe epilepsy. Exp Neurol 1998;150(2):240-7.
Waldbaum S, Patel M. Mitochondria, oxidative stress, and temporal lobe epilepsy. Epilepsy Res 2010;88(1):23-45.
Martinc B, Grabnar I, Vovk T. The role of reactive species in epileptogenesis and influence of antiepileptic drug therapy on oxidative stress. Curr Neuropharmacol 2012;10(4):328-43.
Snehunsu A, Ghosal C, Kandwal M, Yadav PK, Nayak BS, Rao KR, et al. 1-Triacontanol cerotate; isolated from Marsilea quadrifolia Linn. ameliorates reactive oxidative damage in the frontal cortex and hippocampus of chronic epileptic rats. J Ethnopharmacol 2015;172:80-4.
Pahwa P, Goel RK. Ameliorative effect of Asparagus racemosus root extract against pentylenetetrazol-induced kindling and associated depression and memory deficit. Epilepsy Behav 2016;57(Pt A):196-201.
í–zgökçe F, í–zçelik H. Ethnobotanical aspects of some taxa in East Anatolia, Turkey. Econ Bot
;58(4):697.
Kolak U, Hacibekiroglu I, Boga M, í–zgökçe F, íœnal M, Choudhary M, et al. Phytochemical Investigation of Leontice leontopetalum L. subsp. ewersmannii with Antioxidant and Anticholinesterase Activities. Rec Nat Prod 2011;5(4):309.
Arslan A, Cakmak E, Ozaslan M, Cengiz B, Bagci C, Tarakcioglu M, et al. The effects of Bongardia chrysogonum (L) spach extract on the serum parameters and liver, kidney, and spleen tissues in rats. Biotechnol Biotechnol Equip 2005;19(3):170-9.
Abuhamdah SMA, Abuirmeileh AN, Thaer F, Al-Olimat S, Abdel E, Chazot PL. Anti-convulsant Effects of Bongardia chrysogonum L. Tuber in the Pentylenetetrazole-induced Seizure Model. Int J Pharmacol 2018;14(1):127-35.
Ullah I, Badshah H, Naseer MI, Lee HY, Kim MO. Thymoquinone and vitamin C attenuates pentylenetetrazole-induced seizures via activation of GABAB1 receptor in adult rats cortex and hippocampus. Neuromolecular Med 2015;17(1):35-46.
Erel O. A novel automated direct measurement method for total antioxidant capacity using a new generation, more stable ABTS radical cation. Clin Biochem 2004;37(4):277-85.
Erel O. A new automated colorimetric method for measuring total oxidant status. Clin Biochem 2005;38(12):1103-11.
Altindag O, Erel O, Soran N, Celik H, Selek S. Total oxidative/anti-oxidative status and relation to bone mineral density in osteoporosis. Rheumatol Int 2008;28(4):317-21.
Yoshioka T, Kawada K, Shimada T, Mori M. Lipid peroxidation in maternal and cord blood and protective mechanism against activated-oxygen toxicity in the blood. Am J Obstet Gynecol 1979;135(3):372-6.
Spitz DR, Oberley LW. An assay for superoxide dismutase activity in mammalian tissue homogenates. Anal Biochem 1989; 179:8-18.
Paglia DE, Valentine WN. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 1967; 70: 158-169.
Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976; 72: 248-254.
García-López P, Garzón-de la Mora P, Meneses-Medina M, Ramírez Z, Moreno-Sandoval V, Toro-Ureña Id, et al., editors. Lupinus exaltatus obtained lupanine and its measured anticonvulsive activity. Lupin crops: an opportunity for today, a promise for the future Proceedings of the 13th International Lupin Conference, PoznaÅ„, Poland, 6-10 June 2011; 2011: International Lupin Association.
Pal D, Sannigrahi S, Mazumder UK. Analgesic and anticonvulsant effects of saponin isolated from the leaves of Clerodendrum infortunatum Linn. in mice. Indian J Exp Biol 2009; 47: 743-747.
Kabuto H, Yokoi I, Mori A. Monoamine metabolites, iron induced seizures, and the anticonvulsant effect of tannins. Neurochem Res 1992; 17: 585-590.
Eisenman SW, Zaurov DE, Struwe L. Medicinal Plants of Central Asia: Uzbekistan and Kyrgyzstan: Springer Science & Business Media 2012.
Herrup K, Neve R, Ackerman SL, Copani A. Divide and die: cell cycle events as triggers of nerve cell death. J Neurosci. 2004; 24: 9232-9239.
Hoh NZ, Wagner AK, Alexander SA, Clark RB, Beers SR, Okonkwo DO, et al. BCL2 genotypes: functional and neurobehavioral outcomes after severe traumatic brain injury. J Neurotrauma 2010; 27: 1413-1427.
Luo Z, Fang Y, Zhang L. The effects of antiepileptic drug valproic acid on apoptosis of hippocampal neurons in epileptic rats. Pak J Pharm Sci 2015; 28: 319-324.
Rahmati B, Khalili M, Roghani M, Ahghari P. Anti-epileptogenic and antioxidant effect of Lavandula officinalis aerial part extract against pentylenetetrazol-induced kindling in male mice. J Ethnopharmacol 2013; 148: 152-157.
Ilhan A, Gurel A, Armutcu F, Kamisli S, Iraz M. Antiepileptogenic and antioxidant effects of Nigella sativa oil against pentylenetetrazol-induced kindling in mice. Neuropharmacology 2005; 49: 456-464.
Zeng LH, Zhang HD, Xu CJ, Bian YJ, Xu XJ, Xie QM, et al. Neuroprotective effects of flavonoids extracted from licorice on kainate-induced seizure in mice through their antioxidant properties. J Zhejiang Univ Sci B 2013; 14: 1004-12.
Erdogan H, Ekici F, Katar M, Kesici H, Aslan H. The protective effects of endothelin-A receptor antagonist BQ-123 in pentylenetetrazole-induced seizure in rats. Hum Exp Toxicol 2014; 33: 1008-16.
Kiasalari Z, Khalili M, Roghani M, Sadeghian A. Antiepileptic and Antioxidant Effect of Brassica nigra on Pentylenetetrazol-Induced Kindling in Mice. Iran J Pharm Res 2012; 11: 1209-1217.
Tutanc M, Aras M, Dokuyucu R, Altas M, Zeren C, Arica V, et al. Oxidative Status in Epileptic Children Using Carbamazepine. Iran J Pediatr 2015; 25(6).
Loup F. GABAA Receptors in Human Temporal Lobe Epilepsy. Epileptologie 2006; 23: 187-194.
Walsh LA, Li M, Zhao TJ, Chiu TH, Rosenberg HC. Acute pentylenetetrazol injection reduces rat GABAA receptor mRNA levels and GABA stimulation of benzodiazepine binding with No effect on benzodiazepine binding site density. J Pharmacol Exp Ther 1999; 289: 1626-1633.
Meral I, Esrefoglu M, Dar KA, Ustunova S, Aydin MS, Demirtas M, et al. Effects of Nigella sativa on apoptosis and GABAA receptor density in cerebral cortical and hippocampal neurons in pentylenetetrazol induced kindling in rats. Biotech Histochem 2016; 91: 493-500.