The effects of hydrogen sulfide synthesis inhibition in lindane-induced seizures in rats: a behavioral and EEG study

Authors

  • Nikola Šutulović Laboratory of Neurophysiology, Institute of Medical Physiology “Richard Burian”, Faculty of Medicine, Višegradska 26/II, 11000, University of Belgrade, 11000 Belgrade https://orcid.org/0000-0002-9499-3247
  • Aleksandra Rašić-Marković Laboratory of Neurophysiology, Institute of Medical Physiology “Richard Burian”, Faculty of Medicine, Višegradska 26/II, 11000, University of Belgrade, 11000 Belgrade https://orcid.org/0000-0003-1131-2328
  • Željko Grubač Laboratory of Neurophysiology, Institute of Medical Physiology “Richard Burian”, Faculty of Medicine, Višegradska 26/II, 11000, University of Belgrade, 11000 Belgrade
  • Emilija Đurić Laboratory of Neurophysiology, Institute of Medical Physiology “Richard Burian”, Faculty of Medicine, Višegradska 26/II, 11000, University of Belgrade, 11000 Belgrade
  • Dragan Hrnčić Laboratory of Neurophysiology, Institute of Medical Physiology “Richard Burian”, Faculty of Medicine, Višegradska 26/II, 11000, University of Belgrade, 11000 Belgrade https://orcid.org/0000-0003-0806-444X

DOI:

https://doi.org/10.2298/ABS200802039S

Keywords:

aminooxyacetate, cystathionine-β-synthase, EEG, hydrogen sulfide, lindane

Abstract

Paper description:

  • Lindane-induced seizures in rats present a model of refractory generalized epilepsy. Hydrogen sulfide (H2S) is a gasotransmitter with different physiological roles.
  • We examined the influence of aminooxyacetate, an inhibitor of H2S production, when applied before lindane administration. Convulsive behavior was assessed by seizure incidence, latency and severity. The number and duration of ictal periods in EEG were analyzed.
  • Aminooxyacetate significantly decreased the latency and augmented the severity of seizures; EEG analysis revealed an increased number and duration of ictal periods.
  • H2S production inhibition aggravated lindane-induced seizures, revealing a functional relationship between H2S and the effects of lindane.

Abstract: Lindane-induced seizure in rats is a model of refractory generalized epilepsy. Hydrogen sulfide (H2S) is a gasotransmitter with different physiological and pathological roles. Cystathionine-β-synthase (CBS) is a major enzyme responsible for H2S production in the brain. The aim of this study was to investigate the effects of H2S production inhibition using aminooxyacetate (a CBS inhibitor) on behavioral and EEG manifestations of lindane-induced seizures. Male Wistar rats with previously implanted EEG electrodes were intraperitoneally (i.p.) treated with 4 mg/kg lindane and observed for convulsive behavior and EEG manifestations during the next 30 min. Aminooxyacetate (5, 15 and 25 mg/kg, i.p.) or saline, was injected 30 min prior to lindane. Convulsive behavior was assessed by seizure incidence, latency time and severity (grades 0-4). The number and duration of ictal periods in the EEG were also analyzed. Seizure incidence was higher in rats treated with aminooxyacetate (AOA) before lindane, but not significantly when compared with those treated only with lindane. However, AOA significantly decreased the latency time and augmented the severity of lindane-induced seizures in a dose-dependent manner. EEG analysis revealed an increased number and duration of ictal periods in rats receiving AOA prior to lindane. H2S production inhibition aggravated lindane-induced seizures, which showed a functional relationship between H2S and the effects of lindane.

Downloads

Download data is not yet available.

References

Fisher RS, Acevedo C, Arzimanoglou A, Bogacz A, Cross JH, Elger CE, Engel J Jr, Forsgren L, French JA, Glynn M, Hesdorffer DC, Lee BI, Mathern GW, Moshé SL, Perucca E, Scheffer IE, Tomson T, Watanabe M, Wiebe S. ILAE official report: a practical clinical definition of epilepsy. Epilepsia. 2014;55(4):475-82.

Nolan K, Kamrath J, Levitt J. Lindane toxicity: a comprehensive review of the medical literature. Pediatr Dermatol. 2012;29(2):141-6.

Hrnčić D, Rašić-Marković A, Djuric D, Šušić V, Stanojlović O. The Role of nitric oxide in convulsions induced by lindane in rats. Food Chem Toxicol. 2011;49(4):947-54.

Costa LG. The neurotoxicity of organochlorine and pyrethroid pesticides. Handb Clin Neurol. 2015;131:135-48.

Löscher W. Single versus combinatorial therapies in status epilepticus: Novel data from preclinical models. Epilepsy Behav EB. 2015;49:20-5.

Vučević D, Hrncić D, Radosavljević T, Mladenović D, Rasić-Marković A, Loncar-Stevanović H, Djurić D, Macut D, Susić V, Stanojlović O. Correlation between electrocorticographic and motor phenomena in lindane-induced experimental epilepsy in rats. Can J Physiol Pharmacol. 2008;86(4):173-9.

Kaminski RM, Tochman AM, Dekundy A, Turski WA, Czuczwar SJ. Ethosuximide and valproate display high efficacy against lindane-induced seizures in mice. Toxicol Lett. 2004;154(1-2):55-60.

Kumar M, Sandhir R. Hydrogen sulfide in physiological and pathological mechanisms in brain. CNS Neurol Disord Drug Targets. 2018;17(9):654-70.

Kashfi K. The role of hydrogen sulfide in health and disease. Biochem Pharmacol. 2018;149:1-4.

Kimura H. Hydrogen sulfide and polysulfides as biological mediators. Mol Basel Switz. 2014;19(10):16146-57.

Kimura H. Signaling molecules: hydrogen sulfide and polysulfide. Antioxid Redox Signal. 2015;22(5):362-76.

Mendes MI, Colaço HG, Smith DE, Ramos RJ, Pop A, van Dooren SJ, Tavares de Almeida I, Kluijtmans LA, Janssen MC, Rivera I, Salomons GS, Leandro P, Blom HJ. Reduced response of Cystathionine Beta-Synthase (CBS) to S-Adenosylmethionine (SAM): Identification and functional analysis of CBS gene mutations in Homocystinuria patients. J Inherit Metab Dis. 2014;37(2):245-54.

Powell CR, Dillon KM, Matson JB. A review of hydrogen sulfide (H2S) donors: Chemistry and potential therapeutic applications. Biochem Pharmacol. 2018;149:110-23.

Donatti AF, Soriano RN, Sabino JP, Branco LGS. Involvement of endogenous hydrogen sulfide (H2S) in the rostral ventrolateral medulla (RVLM) in hypoxia-induced hypothermia. Brain Res Bull. 2014;108:94-9.

Stanojlović O, Rasić-Marković A, Hrncić D, Susić V, Macut D, Radosavljević T, Djuric D. Two Types of Seizures in Homocysteine Thiolactone-Treated Adult Rats, Behavioral and Electroencephalographic Study. Cell Mol Neurobiol. 2009;29(3):329-39.

Stanojlović O, Nikolić T, Hrnčić D, Radonjić N, Rašić-Marković A, Mladenović D, Petronijević N. Ontogenetic influence on rat susceptibility to lindane seizure after pretreatment with phencyclidine. Environ Toxicol Pharmacol. 2013;35(2):161-70.

Abe K, Kimura H. The possible role of hydrogen sulfide as an endogenous neuromodulator. J Neurosci Off J Soc Neurosci. 1996;16(3):1066-71.

Han Y, Qin J, Chang X, Yang Z, Bu D, Du J. Modulating effect of hydrogen sulfide on gamma-aminobutyric acid B receptor in recurrent febrile seizures in rats. Neurosci Res. 2005;53(2):216-219.

Wiles DA, Russell JL, Olson KR, Walson PD, Kelley M. Massive lindane overdose with toxicokinetics analysis. J Med Toxicol. 2015;11(1):106-109.

Han Y, Qin J, Chang X, Yang Z, Tang X, Du J. Hydrogen sulfide may improve the hippocampal damage induced by recurrent febrile seizures in rats. Biochem Biophys Res Commun. 2005;327(2):431-6.

Gupta YK, Dahiya AK, Reeta KH. Gaso-transmitter hydrogen sulphide: potential new target in pharmacotherapy. Indian J Exp Biol. 2010;48(11):1069-77.

Tochman AM, Kamiński R, Turski WA, Czuczwar SJ. Protection by conventional and new antiepileptic drugs against lindane-induced seizures and lethal effects in mice. Neurotox Res. 2000;2(1):63-70.

Mladenović D, Hrncić D, Vucević D, Radosavljević T, Loncar-Stevanović H, Petrović J, Susic V, Djuric D, Stanojlović O. Ethanol suppressed seizures in lindane-treated rats. Electroencephalographic and behavioral studies. J Physiol Pharmacol. 2007;58(4):641-56.

Hrncić D, Rasić-Marković A, Susić V, Djurić D, Stanojlović O. Influence of NR2B-selective NMDA antagonist on lindane-induced seizures in rats. Pharmacology. 2009;84(4):234-9.

Dawe GS, Han SP, Bian JS, Moore PK. Hydrogen sulphide in the hypothalamus causes an ATP-sensitive K+ channel-dependent decrease in blood pressure in freely moving rats. Neuroscience. 2008;152(1):169-77.

Yamada K, Inagaki N. Neuroprotection by KATP channels. J Mol Cell Cardiol. 2005;38(6):945-9.

Kimura Y, Dargusch R, Schubert D, Kimura H. Hydrogen sulfide protects HT22 neuronal cells from oxidative stress. Antioxid Redox Signal. 2006;8(3-4):661-70.

Kimura Y, Kimura H. Hydrogen sulfide protects neurons from oxidative stress. FASEB J Off Publ Fed Am Soc Exp Biol. 2004;18(10):1165-1167.

Tan BH, Wong PT-H, Bian J-S. Hydrogen sulfide: a novel signaling molecule in the central nervous system. Neurochem Int. 2010;56(1):3-10.

Shefa U, Kim M-S, Jeong NY, Jung J. Antioxidant and Cell-Signaling Functions of Hydrogen Sulfide in the Central Nervous System. Oxid Med Cell Longev. 2018;2018:1873962.

Paul BD, Snyder SH. Gasotransmitter hydrogen sulfide signaling in neuronal health and disease. Biochem Pharmacol. 2018;149:101-9.

Chen WL, Niu YY, Jiang WZ, Tang HL, Zhang C, Xia QM, Tang XQ. Neuroprotective effects of hydrogen sulfide and the underlying signaling pathways. Rev Neurosci. 2015;26(2):129-42.

Luo Y, Wu PF, Zhou J, Xiao W, He JG, Guan XL, Zhang JT, Hu ZL, Wang F, Chen JG. Aggravation of seizure-like events by hydrogen sulfide: involvement of multiple targets that control neuronal excitability. CNS Neurosci Ther. 2014;20(5):411-9.

Chao D, He X, Yang Y, Balboni G, Salvadori S, Kim DH, Xia Y. Hydrogen sulfide induced disruption of Na+ homeostasis in the cortex. Toxicol Sci. 2012;128(1):198-208.

Hou XY, Hu ZL, Zhang DZ, Lu W, Zhou J, Wu PF, Guan XL, Han QQ, Deng SL, Zhang H, Chen JG, Wang F. Rapid Antidepressant Effect of Hydrogen Sulfide: Evidence for Activation of mTORC1-TrkB-AMPA Receptor Pathways. Antioxid Redox Signal. 2017;27(8):472-88.

Rogawski MA. Revisiting AMPA receptors as an antiepileptic drug target. Epilepsy Curr. 2011;11(2):56-63.

Frasca A, Aalbers M, Frigerio F, Fiordaliso F, Salio M, Gobbi M, Cagnotto A, Gardoni F, Battaglia GS, Hoogland G, Di Luca M, Vezzani A. Misplaced NMDA receptors in epileptogenesis contribute to excitotoxicity. Neurobiol Dis. 2011;43(2):507-15.

Yakovlev AV, Kurmasheva ED, Giniatullin R, Khalilov I, Sitdikova GF. Hydrogen sulfide inhibits giant depolarizing potentials and abolishes epileptiform activity of neonatal rat hippocampal slices. Neuroscience. 2017;340:153-65.

Downloads

Published

2020-12-25

How to Cite

1.
Šutulović N, Rašić-Marković A, Grubač Željko, Đurić E, Hrnčić D. The effects of hydrogen sulfide synthesis inhibition in lindane-induced seizures in rats: a behavioral and EEG study. Arch Biol Sci [Internet]. 2020Dec.25 [cited 2024Apr.20];72(4):457-63. Available from: https://www.serbiosoc.org.rs/arch/index.php/abs/article/view/6027

Issue

Vol. 72 No. 4 (2020)

Section

Articles

License

Copyright (c) 2020 Archives of Biological Sciences

Creative Commons License

This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.

Authors grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution 4.0 International License that allows others to share the work with an acknowledgment of the work’s authorship and initial publication in this journal.

Most read articles by the same author(s)