The role for nitric oxide on the effects of hydroalcoholic extract of Achillea wilhelmsii on seizure

Document Type : Original Research Article

Authors

1 Neurocognitive Research Center, School of Medicine, Mashhad University of Medical Sciences, I. R. Iran

2 Department of Physiology, School of Medicine, Mashhad University of Medical Sciences Mashhad, I. R. Iran

3 Neurogenic Inflammation Research Center, School of Medicine, Mashhad University of Medical Sciences, I. R. Iran

4 Department of Biochemistry, School of Medicine, Mashhad University of Medical Sciences, I. R. Iran

Abstract

Objective: Nitric oxide (NO) plays an important role both as a consequence and as a cause of epileptic seizures.Regarding the central nervous system depressant effects of Achillea wilhelmsii (A. wilhelmsii), as well the effects of the plant on NO, this study was aimed to elucidatethe possible role for nitric oxide on the effects of hydroalcoholic extract of A. wilhelmsii on pentylenetetrazole (PTZ)-induced seizures.
Materials and Methods: Fifty-six male Wistar rats were divided into 7 groups (n=8 in each group) and treated with (1) normal saline, (2) normal saline before pentylenetetrazole (PTZ, 90 mg/kg), (3-7) A. wilhelmsii extract (100, 200, 400, 800, and 1200 mg/kg) before PTZ. Latency to first minimal colonic seizure (MCS) and the first generalized tonic-clonic seizures (GTCS) as well as the mortality rate were recorded. The brain tissues were then removed for biochemical measurements. Fisher’s exact probability test as well as analysis of variance (ANOVA), followed by Tukey’s test were used for statistical evaluation.
Results: Treatment with 100- 1200 mg/kg of the extract did not affect MCS latencies. 400 mg/kg of the extract prolonged GTCS latency (p<0.001), however, the lower and higher doses were not effective. Nitric oxide metabolites concentrations in the hippocampal tissues of the animals treated with 100, 200, and 400 mg/kg of the extract were increased compared with saline (pConclusion: The present study showed that hydroalcoholic extract of A. wilhelmsii affects NO metabolites in brain tissues as well the severity of seizures in PTZ-induced seizure model.

Keywords

Main Subjects


Afsharypuor S, Asgary S, Lockwood G. 1996. Constituents of the Essential Oil of Achillea wilheimsii from Iran. Planta med, 62: 77-78.
Akula KK, Dhir A, Kulkarni SK. 2008. Nitric oxide signaling pathway in the anti-convulsant effect of adenosine against pentylenetetrazol-induced seizure threshold in mice. Eur J Pharmacol, 587: 129-134.
Ardestani A, Yazdanparast R. 2007. Antioxidant and free radical scavenging potential of Achillea santolina extracts. Food chem, 104: 21-29.
Asgary S, Naderi GH, Sarrafzadegan N, Mohammadifard N, Mostafavi S, Vakili R. 2000. Antihypertensive and antihyperlipidemic effects of Achillea wilhelmsii. Drugs under Experimental and Clinical Research Drugs Exp Clin Res, 26: 89- 93.
Azadbakht M, Semnani M, Khansari N. 2003. The essential oil omposition of Achillea wilhelmsii leaves and flowers. J  Med Plants, 2: 55-59.
Azizi-Malekabadi H, Hosseini M, Soukhtanloo M, Sadeghian R, Fereidoni M, Khodabandehloo F. 2012. Different effects of scopolamine on learning, memory, and nitric oxide metabolite levels in hippocampal tissues of ovariectomized and Sham-operated rats. Arq Neuropsiquiatr, 70: 447-452.
Bashkatova V, Narkevich V, Vitskova G, Vanin A. 2003. The influence of anticonvulsant and antioxidant drugs on nitric oxide level and lipid peroxidation in the rat brain during penthylenetetrazole-induced epileptiform model seizures. Prog Neuropsychopharmacol Biol Psychiatry, 27: 487-492.
Baulac S, Huberfeld G, Gourfinkel-An I, Mitropoulou G, Beranger A, Prud'homme J-F, Baulac M, Brice A, Bruzzone R, LeGuern E. 2001. First genetic evidence of GABAA receptor dysfunction in epilepsy: a mutation in the [gamma]2-subunit gene. Nat Genet, 28: 46-48.
Benedek B, Geisz N, Jager W, Thalhammer T, Kopp B. 2006. Choleretic effects of yarrow (Achillea millefolium s.l.) in the isolated perfused rat liver. Phytomedicine, 24: 702-706.
Benedek B, Rothwangl-Wiltschnigg K, Rozema E, Gjoncaj N, Reznicek G, Jurenitsch J, Kopp B, Glasl S. 2008. Yarrow (Achillea millefolium L. s.l.): pharmaceutical quality of commercial samples. Die Pharmazie, 63: 23-26.
Bosnak M, Ayyildiz M, Yildirim M, Agar E. 2007. The role of nitric oxide in the anticonvulsant effects of pyridoxine on penicillin-induced epileptiform activity in rats. Epilepsy Res, 76: 49-59.
Buisson A, Lakhmeche N, Verrecchia C, Plotkine M, Boulu RG. 1993. Nitric oxide: an endogenous anticonvulsant substance. Neuroreport, 4: 444-446.
Cavalcanti AM, Baggio CH, Freitas CS, Rieck L, de Sousa RS, Da Silva-Santos JE, Mesia-Vela S, Marques MC. 2006. Safety and antiulcer efficacy studies of Achillea millefolium L. after chronic treatment in Wistar rats. J Ethnopharmacol, 107: 277- 284.
Ceccatelli S. 1997. Expression and Plasticity of NO Synthase in the Neuroendocrine System. Brain Res Bull, 44: 533-538.
Coitinho AS, de Mello CF, Lima TTF, de Bastiani J, Fighera MR, Wajner M. 2001. Pharmacological evidence that α-ketoisovaleric acid induces convulsions through GABAergic and glutamatergic mechanisms in rats. Brain Res, 894: 68-73.
Csupor-Loffler B, Hajdu Z, Zupko I, Rethy B, Falkay G, Forgo P, Hohmann J. 2009. Antiproliferative effect of flavonoids and sesquiterpenoids from Achillea millefolium s.l. on cultured human tumour cell lines. Phytother Res, 23: 672-676.
De Luca G, Di Giorgio RM, Macaione S, Calpona PR, Di Paola ED, Costa N, Cuzzocrea S, Citraro R, Russo E, De Sarro G. 2006. Amino acid levels in some brain areas of inducible nitric oxide synthase knock out mouse (iNOS−/−) before and after pentylenetetrazole kindling. Pharmacol Biochem Behav , 85: 804-812.
Dhir A, Naidu PS, Kulkarni SK. 2006. Effect of cyclooxygenase inhibitors on pentylenetetrazol (PTZ)-induced convulsions: Possible mechanism of action. Prog Neuropsychopharmacol Biol Psychiatry., 30: 1478-1485.
Ebrahimzadeh Bideskan AR, Hosseini M, Mohammadpour T, Karami R, Khodamoradi M, Nemati Karimooy H, Alavi H.2011. Effects of soy extract on pentylenetetrazol-induced seizures in ovariectomized rats. Zhong Xi Yi Jie He Xue Bao, 9: 611-618.
Elmann A, Mordechay S, Erlank H, Telerman A, Rindner M, Ofir R.2011. Anti-neuroinflammatory effects of the extract of Achillea fragrantissima. BMC Complement Altern Med, 11: 98.
Emanuelli T, Prauchner CA, Dacanal J, Zeni A, Reis EC, de Mello CF, de Souza DO. 2000. Intrastriatal administration of 5-aminolevulinic acid induces convulsions and body asymmetry through glutamatergic mechanisms. Brain Res, 868: 88-94.
Gupta N, Bhargava VK, Pandhi P. 2000. Tolerance and withdrawal to anticonvulsant action of clonazepam: role of nitric oxide. Methods Find Exp Clin Pharmacol, 22: 229-235.
Hachinski V. 1998. New antiepileptic drugs: the cost of innovation. Arch Neurol, 55: 1142.
Hosseini M, Ghasemzadeh Rahbardar M, Sadeghnia HR, Rakhshandeh H.2011. Effects of different extracts of Rosa damascena on pentylenetetrazol-induced seizures in mice. Zhong Xi Yi Jie He Xue Bao, 9: 1118-1124.
Hosseini M, Taiarani Z, Karami R, Abad AA.2011. The effect of chronic administration of L-arginine and L-NAME on morphine-induced antinociception in ovariectomized rats. Indian J Pharmacol, 43: 541-545.
Hosseini M, Sadeghnia HR, Salehabadi S, Alavi H, Gorji A. 2009. The effect of L-arginine and L-NAME on pentylenetetrazole induced seizures in ovariectomized rats, an in vivo study. Seizure, 18: 695-698.
Hosseini M, Taiarani Z, Hadjzadeh MA, Salehabadi S, Tehranipour M, Alaei HA.2011. Different responses of nitric oxide synthase inhibition on morphine-induced antinociception in male and female rats. Pathophysiology, 18: 143-149.
Hosseini M, Dastghaib SS, Rafatpanah H, Hadjzadeh MA, Nahrevanian H, Farrokhi I. 2010. Nitric oxide contributes to learning and memory deficits observed in hypothyroid rats during neonatal and juvenile growth. Clinics (Sao Paulo), 65: 1175-1181.
Itoh K, Watanabe M. 2009. Paradoxical facilitation of pentylenetetrazole-induced convulsion susceptibility in mice lacking neuronal nitric oxide synthase. Neuroscience, 159: 735-743.
Itoh K, Watanabe M, Yoshikawa K, Kanaho Y, Berliner LJ, Fujii H. 2004. Magnetic resonance and biochemical studies during pentylenetetrazole-kindling development: The relationship between nitric oxide, neuronal nitric oxide synthase and seizures. Neuroscience, 129: 757-766.
Javidnia K, Miri R, Sadeghpour H. 2004. Composition of the volatile oil of Achillea wilhelmsii C. Koch from Iran. DARU, 12: 63- 66.
Jayakumar AR, Sujatha R, Paul V, Puviarasan K, Jayakumar R. 1999. Involvement of nitric oxide and nitric oxide synthase activity in anticonvulsive action. Brain Res Bull, 48: 387-394.
Jiang W, Xiao L, Wang J-C, Huang Y-G, Zhang X. 2004. Effects of nitric oxide on dentate gyrus cell proliferation after seizures induced by pentylenetrazol in the adult rat brain. Neurosci Lett, 367: 344-348.
Kabuto H, Yokoi I, Mori A.1992. Monoamine metabolites, iron induced seizures, and the anticonvulsant effect of tannins. Neurochem Res. 17: 585-590.
Kamoshima W, Kitamura Y, Nomura Y, Taniguchi T. 1997. Possible involvement of ADP-ribosylation of particular enzymes in cell death induced by nitric oxide-donors in human neuroblastoma cells. Neurochem Int, 30: 305-311.
Karami R, Hosseini M, Khodabandehloo F, Khatami L, Taiarani Z.2011. Different effects of L-arginine on morphine tolerance in sham and ovariectomized female mice. J Zhejiang Univ Sci B, 12: 1016-1023.
Khan AM, Rezazadeh SH. 2010.Review on Iranian medicinal plants with antioxidant properties. J Med Plants, 9: 19-32s.
Klioueva IA, van Luijtelaar ELJM, Chepurnova NE, Chepurnov SA. 2001. PTZ-induced seizures in rats: effects of age and strain. Physiol Behav, 72: 421-426.
Lemmens-Gruber R, Marchart E, Rawnduzi P, Engel N, Benedek B, Kopp B. 2006. Investigation of the spasmolytic activity of the flavonoid fraction of Achillea millefolium s.l. on isolated guinea-pig ilea. Arzneimittelforschung, 56: 582- 588.
Lesani A, Javadi-Paydar M, Khodadad TK, Asghari-Roodsari A, Shirkhodaei M, Norouzi A, Dehpour AR. 2010. Involvement of the nitric oxide pathway in the anticonvulsant effect of tramadol on pentylenetetrazole-induced seizures in mice. Epilepsy Behav, 19: 290-295.
Marangoz C, Ayyildiz M, Agar E. 1994. Evidence that sodium nitroprusside possesses anticonvulsant effects mediated through nitric oxide. Neuroreport, 5: 2454-2456.
Moezi L, Shafaroodi H, Hassanipour M, Fakhrzad A, Hassanpour S, Dehpour AR. 2012. Chronic administration of atorvastatin induced anti-convulsant effects in mice: The role of nitric oxide. Epilepsy Behav, 23: 399-404.
Moncada S, Palmer RM, Higgs EA. 1991. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol Rev, 43: 109-142.
Mulsch A, Busse R, Mordvintcev PI, Vanin AF, Nielsen EO, Scheel-Kruger J, Olesen SP. 1994. Nitric oxide promotes seizure activity in kainate-treated rats. Neuroreport, 5: 2325-2328.
Nahrevanian H, Dascombe MJ. 2001. Nitric oxide and reactive nitrogen intermediates during lethal and nonlethal strains of murine malaria. Parasite Immunol, 23: 491-501.
Nahrevanian H, Najafzadeh M, Hajihosseini R, Nazem H, Farahmand M, Zamani Z. 2009. Anti-leishmanial effects of trinitroglycerin in BALB/C mice infected with Leishmania major via nitric oxide pathway. Korean J Parasitol, 47: 109-115.
Nemeth E, Bernath J. 2008. Biological activities of yarrow species (Achillea spp.). Curr Pharm Des, 14: 3151-3167.
Nidhi G, Balakrishnan S, Pandhi P. 1999. Role of nitric oxide in electroshock and pentylenetetrazole seizure threshold in rats. Methods Find Exp Clin Pharmacol, 21: 609-612.
Nowicki JP, Duval D, Poignet H, Scatton B. 1991. Nitric oxide mediates neuronal death after focal cerebral ischemia in the mouse. Eur J Pharmacol, 204: 339-340.
Noyan B, Jensen MS, Danscher G. 2007. The lack of effects of zinc and nitric oxide in initial state of pilocarpine-induced seizures. Seizure, 16: 410-416.
Osonoe K, Mori N, Suzuki K, Osonoe M. 1994. Antiepileptic effects of inhibitors of nitric oxide synthase examined in pentylenetetrazol-induced seizures in rats. Brain Res, 663: 338-340.
Paul V, Subramanian EH. 2002. Evidence for an involvement of nitric oxide and gamma aminobutyric acid in the anticonvulsant action of l-arginine on picrotoxin-induced convulsions in rats. Pharmacol Biochem Behav, 72: 515-519.
Peeters BW, van Rijn CM, Vossen JM, Coenen AM. 1989. Effects of GABA-ergic agents on spontaneous non-convulsive epilepsy, EEG and behaviour, in the WAG/RIJ inbred strain of rats. Life Sci, 45: 1171-1176.
Penix LP, Davis W, Subramaniam S. 1994. Inhibition of NO synthase increases the severity of kainic acid-induced seizures in rodents. Epilepsy Res, 18: 177-184.
Rakhshandah H, Hosseini M. 2006. Potentiation of pentobarbital hypnosis by Rosa damascena in mice. Indian J Exp Biol, 44: 910-912.
Sadeghian R, Fereidoni M, Soukhtanloo M, Azizi-Malekabadi H, Hosseini M.2012. Decreased nitric oxide levels in the hippocampus may play a role in learning and memory deficits in ovariectomized rats treated by a high dose of estradiol. Arq Neuropsiquiatr, 70: 874-879.
Shafaroodi H, Moezi L, Ghorbani H, Zaeri M, Hassanpour S, Hassanipour M, Dehpour AR. 2012. Sub-chronic treatment with pioglitazone exerts anti-convulsant effects in pentylenetetrazole-induced seizures of mice: The role of nitric oxide. Brain Res Bull, 87: 544-550.
Souri E, Amin G, Dehmobed-Sharifabadi A, Nazifi A, Farsam H. 2010.Antioxidative activity of sixty plants from Iran. Iran J Pharm Res, 3: 55-59.
Starr MS, Starr BS. 1993. Paradoxical facilitation of pilocarpine-induced seizures in the mouse by MK-801 and the nitric oxide synthesis inhibitor L-NAME. Pharmacol Biochem Behav, 45: 321-325.
Stojanovic G, Radulovic N, Hashimoto T, Palic R. 2005. In vitro antimicrobial activity of extracts of four Achillea species: the composition of Achillea clavennae L. (Asteraceae) extrac. J Ethnopharmacol, 101: 185-190.
Suzuki E, Nakaki T, Shintani F, Kanba S, Miyaoka H. 2002. Antipsychotic, antidepressant, anxiolytic, and anticonvulsant drugs induce type II nitric oxide synthase mRNA in rat brain. Neurochem Int, 333: 217-219.
Tozyo T, Yoshimura Y, Sakurai K, Uchida N, Takeda Y, Nakai H, Novel IH. 1994. antitumor sesquiterpenoids in Achillea millefolium. Chem Pharm Bull (Tokyo), 42: 1096-1100.
Tuberoso CIG, Kowalczyk A, Coroneo V, Russo MT, Dessى S, Cabras P. 2005. Chemical composition and antioxidant, antimicrobial, and antifungal activities of the essential oil of Achillea ligustica All. J Agric Food Chem, 53: 10148-10153.
Vahid S, Dashti-Khavidaki S, Ahmadi F, Amini M, Salehi Surmaghi MH.2012. Effect of herbal medicine achillea millefolium on plasma nitrite and nitrate levels in patients with chronic kidney disease: a preliminary study. Iran J Kidney Dis, 6: 350-354.
Yaeesh S, Jamal Q, Khan AU, Gilani AH. 2006. Studies on hepatoprotective, antispasmodic and calcium antagonist activities of the aqueous-methanol extract of Achillea millefolium. Phytother Res, 20: 546-551.
Yazdanparast R, Ardestani A, Jamshidi S. 2007. Experimental diabetes treated with Achillea santolina: effect on pancreatic oxidative parameters. J Ethnopharmacol, 112: 13-18.