Altered expression of orexin 1 and endocannabinoid 1 receptors of the hippocampus in three pentylenetetrazol, pilocarpine and kainate seizure models

authors:

avatar Giti Nasudi , avatar Mahmoud Elahdadi Salmani Elahdadi Salmani , * , avatar Narges Hosseinmardi ORCID , avatar Taghi Lashkarbolouki , avatar Iran Goudarzi , avatar Farshad Moradpour

Koomesh: Vol.23, issue 2; 260-266
published online: July 06, 2021
article type: issue_documents_importer
received: March 01, 2020
accepted: October 06, 2020

how to cite: Nasudi G, Elahdadi Salmani M E S, Hosseinmardi N, Lashkarbolouki T, Goudarzi I , et al. Altered expression of orexin 1 and endocannabinoid 1 receptors of the hippocampus in three pentylenetetrazol, pilocarpine and kainate seizure models. koomesh. 2021;23(2):e153264. 

Abstract

Introduction: Seizure is synchronous and abnormal brain neuronal activity that leads to activation of different receptors capable of enhancing or suppressing seizure activity such as orexin receptor 1 (OXR1) and/or endocannabinoid receptor 1(CBR1). The time of activation for the receptors may influence seizure control. Therefore, this study aimed to investigate the latency for and the change of the expression of OXR1 or CBR1 following seizures in three pentylenetetrazol (PTZ), kainic acid (KA), and Pilocarpine seizure models. Materials and Methods: Fifty-six male Wistar rats were allocated in the three PTZ, KA, and Pilocarpine groups. Seizure intensity was calculated upon latencies to seizures (from injection to seizure latency 1 and from seizure to tonic-clonic latency 2) and seizure duration. OXR1 and CBR1 gene expressions were evaluated using RT-PCR and the results were compared with the control group (without seizure induction). Results: Our study showed that latency 1 and 2 significantly increased in the KA and Pilocarpine models compared with PTZ, while the seizure duration reduced. Relatively, the expression of OXR1, four hours, and CBR1, instantly and four hours following the PTZ application was augmented. The expression of OXR1 and CBR1, one week following KA perfusion was enhanced, while the increase in the receptor expressions was demonstrated 28 days after Pilocarpine injection. Conclusion: Results of the study demonstrated that the shorter the latency of seizures in a model and longer the seizure durations, the increase in the OXR1 and CBR1 may be hastened.  

References

  • 1.

    Ropper AH, Adams R, Victor M, Samuels MA. Adams and Victor's principles of neurology. McGraw Hill Medical 2005.

  • 2.

    Merritt HH. A textbook of neurology. Acad Med 1959; 34: 621.

  • 3.

    Binder MD, Hirokawa N, Windhorst U. Encyclopedia of neuroscience. 2009.##https://doi.org/10.1007/978-3-540-29678-2.

  • 4.

    Wallace MJ, Blair RE, Falenski KW, Martin BR, DeLorenzo RJ. The endogenous cannabinoid system regulates seizure frequency and duration in a model of temporal lobe epilepsy. J Pharmacol Exp Ther 2003; 307: 129-137.

  • 5.

    Ben-Ari Y, Crepel V, Represa A. Seizures beget seizures in temporal lobe epilepsies: the boomerang effects of newly formed aberrant kainatergic synapses. Epilepsy Curr 2008; 8: 68-72.

  • 6.

    Choi HS, Lee CH. Time-course changes of hippocalcin expression in the mouse hippocampus following pilocarpine-induced status epilepticus. J Vet Sci 2016; 17: 137-144.

  • 7.

    Smirnova EY, Amakhin DV, Malkin SL, Chizhov AV, Zaitsev AV. Acute changes in electrophysiological properties of cortical regular-spiking cells following seizures in a rat lithium-pilocarpine model. Neuroscience 2018; 379: 202-215.

  • 8.

    Bojnik E, Turun E, Armaan G, Kant L, Benyhe S, Yaln A, Borsodi A. Changes in the cannabinoid (CB1) receptor expression level and G-protein activation in kainic acid induced seizures. Epilepsy Res 2012; 99: 64-68.

  • 9.

    Soltesz I, Alger BE, Kano M, Lee SH, Lovinger DM, Ohno-Shosaku T, Watanabe M. Weeding out bad waves: towards selective cannabinoid circuit control in epilepsy. Nat Rev Neurosci 2015; 16: 264-277.

  • 10.

    Falenski KW, Carter DS, Harrison AJ, Martin BR, Blair RE, DeLorenzo RJ. Temporal characterization of changes in hippocampal cannabinoid CB1 receptor expression following pilocarpine-induced status epilepticus. Brain Res 2009; 1262: 64-72.

  • 11.

    Bhaskaran MD, Smith BN. Cannabinoid-mediated inhibition of recurrent excitatory circuitry in the dentate gyrus in a mouse model of temporal lobe epilepsy. PLoS One 2010; 5: e10683.

  • 12.

    Ludnyi A, Eross L, Czirjk S, Vajda J, Halsz P, Watanabe M, et al. Downregulation of the CB1 cannabinoid receptor and related molecular elements of the endocannabinoid system in epileptic human hippocampus. J Neurosci 2008; 28: 2976-2990.

  • 13.

    Maglczky Z, Tth K, Karlcai R, Nagy S, Eross L, Czirjk S, et al. Dynamic changes of CB1receptor expression in hippocampi of epileptic mice and humans. Epilepsia 2010; 51: 115-120.

  • 14.

    Wilson RI, Nicoll RA. Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature 2001; 410: 588-592.

  • 15.

    Wallace MJ, Wiley JL, Martin BR, DeLorenzo RJ. Assessment of the role of CB1 receptors in cannabinoid anticonvulsant effects. Eur J Pharmacol 2001; 428: 51-57.##https://doi.org/10.1016/S0014-2999(01)01243-2.

  • 16.

    Marsicano G, Goodenough Sh, Monory K, Hermann H, Eder M, Cannich A, et al. CB1 cannabinoid receptors and on-demand defense against excitotoxicity. Science 2003; 302: 84-88.

  • 17.

    Kow RL, Jiang K, Naydenov AV, Le JH, Stella N, Nathanson NM. Modulation of pilocarpine-induced seizures by cannabinoid receptor 1. PLoS One 2014; 9: e95922.

  • 18.

    Zhu F, Wang XQ, Chen YN, Yang N, Lang SY, Zuo PP, et al. Changes and overlapping distribution in the expression of CB1/OX1-GPCRs in rat hippocampus by kainic acid-induced status epilepticus. Brain Res 2015; 1597: 14-27.

  • 19.

    Goudarzi E, Elahdadi Salmani M, Lashkarbolouki T, Goudarzi I. Hippocampal orexin receptors inactivation reduces PTZ induced seizures of male rats. Pharmacol Biochem Behav 2015; 130: 77-83.

  • 20.

    Mokhtarpour M, Elahdadi Salmani M, Lashkarbolouki T, Abrari K, Goudarzi I. Lateral hypothalamus orexinergic system modulates the stress effect on pentylenetetrazol induced seizures through corticotropin releasing hormone receptor type 1. Neuropharmacology 2016; 110: 15-24.

  • 21.

    Rejdak K, Papu E, Grieb P, Stelmasiak Z. Decreased cerebrospinal fluid hypocretin1 (orexin A) in patients after repetitive generalized tonic-clonic seizures. Epilepsia 2009; 50: 1641-1644.

  • 22.

    Bahramzadeh S. Evaluating the role of hippocampal orexin receptors on social learning and memory impairment following stress in male rats, in Animal biology. Damghan Univ 2019; 177. (Persian).

  • 23.

    Dariani S, Baluchnejadmojarad T, Roghani M. Thymoquinone attenuates astrogliosis, neurodegeneration, mossy fiber sprouting, and oxidative stress in a model of temporal lobe epilepsy. J Mol Neurosci 2013; 51: 679-686.

  • 24.

    Sarfi M, Elahdadi Salmani M, Goudarzi I, Lashkar Boluki T, Abrari K. Evaluating the role of astrocytes on -estradiol effect on seizures of Pilocarpine epileptic model. Eur J Pharmacol 2017; 797: 32-38.

  • 25.

    Falenski K, Blair RE, Sim-Selley LJ, Martin BR, DeLorenzo RJ. Status epilepticus causes a long-lasting redistribution of hippocampal cannabinoid type 1 receptor expression and function in the rat pilocarpine model of acquired epilepsy. Neuroscience 2007; 146: 1232-1244.

  • 26.

    Karlcai MR, Tth K, Watanabe M, Ledent C, Juhsz G, Freund TF, Maglczky Z. Redistribution of CB1 cannabinoid receptors in the acute and chronic phases of pilocarpine-induced epilepsy. PloS One 2011; 6: e27196.