Neuroinflammation in the pathogenesis of the audiogenic epilepsy: altered proinflammatory cytokine levels in Krushinsky-Molodkina seizure-prone rats

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Abstract

Neuroinflammation plays an important role in epileptogenesis, however, most studies are performed on pharmacological models of epilepsy, while data on non-invasive, including genetic, models are practically absent. In Krushinsky-Molodkina (KM) strain rats with high genetically caused predisposition to AE (intensive audiogenic seizure fit in response to the action of sound) and in the control strain “0” (not predisposed to AE), the levels of a number of pro-inflammatory cytokines were investigated using multiplex immunofluorescence magnetic assay (MILLIPLEX map Kit). Cytokine levels were determined in the dorsal striatum tissue and in the brain stem. Background levels of IL-1β, IL-6 and TNF-α in the dorsal striatum of KM rats were significantly lower than in rats “0” (32.31, 27.84 and 38.87% of decrease, respectively, p < 0.05, 0.05 and 0.01), whereas in the brain stem in the “background” state of interstrain differences in levels of these metabolites were not detected. 4 h after sound exposure, the TNF-α level in the dorsal striatum of KM rats was significantly (38.34%, p < 0.01) lower than in “0” rats. In KM rats, after the action of sound and the subsequent seizure fit, the levels of IL-1β and IL-6 in the dorsal striatum were significantly higher compared to the background (35.29 and 50.21%, of increase, p < 0.05, 0.01, respectively). The IL-2 level in KM rats in the background state was not detected, whereas after audiogenic seizures its level was 14.01 pg/ml (significantly higher, p < 0.01). In the brain stem of KM rats, the levels of IL-1β and TNF-α after audiogenic seizures were significantly lower than in the background (13.23 and 23.44% of decrease, respectively, p < 0.05). In rats of the “0” strain, the levels of cytokines in the dorsal striatum after the action of sound (which did not cause AE seizures) did not differ from those in the background, while the levels of IL-1β in their brain stem were lower than in the background (40.28%, p < 0.01). Thus, the differences between the background levels of cytokines and those after the action of sound were different in rats that differed in their predisposition to AE, which suggests the involvement of these metabolites in the pathophysiology of epilepsy.

About the authors

N. M Surina

Biology Department, Lomonosov Moscow State University

Email: opera_ghost@inbox.ru
119234 Moscow, Russia

I. B Fedotova

Biology Department, Lomonosov Moscow State University

Email: opera_ghost@inbox.ru
119234 Moscow, Russia

G. M Nikolaev

Biology Department, Lomonosov Moscow State University

Email: opera_ghost@inbox.ru
119234 Moscow, Russia

V. V Grechenko

Pirogov Russian National Research Medical University

Email: opera_ghost@inbox.ru
117997 Moscow, Russia

L. V Gankovskaya

Pirogov Russian National Research Medical University

Email: opera_ghost@inbox.ru
117997 Moscow, Russia

A. D Ogurtsova

Pirogov Russian National Research Medical University

Email: opera_ghost@inbox.ru
117997 Moscow, Russia

I. I Poletaeva

Biology Department, Lomonosov Moscow State University

Email: ingapoletaeva@mail.ru
119234 Moscow, Russia

References

  1. Li, G., Bauer, S., Nowak, M., Norwood, B., Tackenberg, B., Rosenow, F., Knake, S., Oertel, W. H., and Hamer, H. M. (2011) Cytokines and epilepsy, Seizure, 20, 249-256, doi: 10.1016/j.seizure.2010.12.005.
  2. Lehtimaki, K. A., Keränen, T., Palmio, J., Mäkinen, R., Hurme, M., Honkaniemi, J., et al. (2007) Increased plasma levels of cytokines after seizures in localization-related epilepsy, Acta Neurol. Scand., 116, 226-230, doi: 10.1111/j.1600-0404.2007.00882.x.
  3. Vezzani, A., Balosso, S., and Ravizza, T. (2019) Neuroinflammatory pathways as treatment targets and biomarkers in epilepsy, Nat. Rev. Neurol., 15, 459-472, doi: 10.1038/s41582-019-0217-x.
  4. Zhang, Z., Liu, Q., Liu, M., Wang, H., Dong, Y., Ji, T., Liu, X., Jiang, Y., Cai, L., and Wu, Y. (2018) Upregulation of HMGB1-TLR4 inflammatory pathway in focal cortical dysplasia type II, J. Neuroinflamm., 15, 27, doi: 10.1186/s12974-018-1078-8.
  5. Zhang, X., Wang, M., Feng, B., Zhang, Q., Tong, J., Wang, M., Lu, C., and Peng, S. (2022) Seizures in PPT1 knock-in mice are associated with inflammatory activation of microglia, Int. J. Mol. Sci., 23, 5586, doi: 10.3390/ijms23105586.
  6. Wolinski, P., Ksiazek-Winiarek, D., and Glabinski, A. (2022) Cytokines and neurodegeneration in epileptogenesis, Brain Sci., 12, 380, doi: 10.3390/brainsci12030380.
  7. Plata-Salaman, C. R., Ilyin, S. E., Turrin, N. P., Gayle, D., Flynn, M. C., Romanovitch, A. E., et al. (2000) Kindling modulates the IL-1beta system, TNF-alpha, TGF-beta1 and neuropeptide mRNAs in specific brain regions, Mol. Brain Res., 75, 248-258, doi: 10.1016/s0169-328x(99)00306-x.
  8. Kalueff, A. V., Lehtimaki, K. A., Ylinen, A., Honkaniemi, J., and Peltola, J. (2004) Intranasal administration of human IL-6 increases the severity of chemically induced seizures in rats, Neurosci. Lett., 365, 106-110, doi: 10.1016/j.neulet.2004.04.061.
  9. Hopkins, S. J., and Rothwell, N. J. (1995) Cytokines and the nervous system. I: Expression and recognition, Trends Neurosci., 18, 83-88, doi: 10.1016/0166-2236(95)93890-a.
  10. Walker, A., Russmann, V., Deeg, C. A., von Toerne, C., Kleinwort, K. J. H., Szober, C., Rettenbeck, M. L., von Rüden, E. L., Goc, J., Ongerth, T., Boes, K., Salvamoser, J. D., Vezzani, A., Hauck, S. M., and Potschka, H. (2016) Proteomic profiling of epileptogenesis in a rat model: focus on inflammation, Brain Behav. Immun., 53, 138-158, doi: 10.1016/j.bbi.2015.12.007.
  11. Vezzani, A., Balosso, S., Aronica, E., and Ravizza, T. (2009) Basic mechanisms of status epilepticus due to infection and inflammation, Epilepsia, 50, 56-57, doi: 10.1111/j.1528-1167.2009.02370.x.
  12. De Souza Bernardino, T. C., Teixeira, A. L., Miranda, A. S., Guidine, P. M., Rezende, G., Doretto, M. C., Castro, G. P., Drummond, L., Dutra Moraes, M. F., Lopes Tito, P. A., Pinheiro de Oliveira, A. C., and Reis, H. J. (2015) Wistar Audiogenic Rats (WAR) exhibit altered levels of cytokines and brain derived neurotrophic factor following audiogenic seizures, Neurosci. Lett., 597, 154-158, doi: 10.1016/j.neulet.2015.04.046.
  13. Sayyah, M., Beheshti, S., Shokrgozar, M. A., Eslami-far, A., Deljoo, Z., Khabiri, A. R., et al. (2005) Antiepileptogenic and anticonvulsant activity of interleukin-1 beta in amygdala-kindled rats, Exp. Neurol., 191, 145-153, doi: 10.1016/j.expneurol.2004.08.032.
  14. Minami, M., Kuraishi, Y., Yamaguchi, T., Nakai, S., Hirai, Y., and Satoh, M. (1990) Convulsants induce interleukin-1 beta messenger RNA in rat brain, Biochem. Biophys. Res. Commun., 171, 832-837, doi: 10.1016/0006-291x(90)91221-d.
  15. Eriksson, C., Tehranian, R., Iverfeldt, K., Winblad, B., and Schultzberg, M. (2000) Increased expression of mRNA encoding interleukin-1beta and caspase-1, and the secreted isoform of interleukin-1 receptor antagonist in the rat brain following systemic kainic acid administration, J. Neurosci. Res., 60, 266-279, doi: 10.1002/(SICI)1097-4547(20000415)60:2<266::AID-JNR16>3.0.CO;2-P.
  16. Lehtimaki, K. A., Peltola, J., Koskikallio, E., Keränen, T., and Honkaniemi, J. (2003) Expression of cytokines and cytokine receptors in the rat brain after kainic acid-induced seizures, Mol. Brain. Res., 110, 253-260, doi: 10.1016/s0169-328x(02)00654-x.
  17. Vezzani, A., Conti, M., De Luigi, A., Ravizza, T., Moneta, D., Marchesi, F., et al. (1999) Interleukin-1beta immunoreactivity and microglia are enhanced in the rat hippocampus by focal kainate application: functional evidence for enhancement of electrographic seizures, J. Neurosci., 19, 5054-5065, doi: 10.1523/JNEUROSCI.19-12-05054.1999.
  18. Gahring, L. C., White, H. S., Skradski, S. L., Carlson, N. G., and Rogers, S. W. (1996) Interleukin-1alpha in the brain is induced by audiogenic seizure, Neurobiol. Dis., 3, 263-269, doi: 10.1006/nbdi.1996.0123.
  19. Mika, J. (2008) Modulation of microglia can attenuate neuropathic pain symptoms and enhance morphine effectiveness, Pharmacol. Rep., 60, 297-307.
  20. Wyatt-Johnson, S. K., Herr, S. A., and Brewster, A. L. (2017) Status epilepticus triggers time dependent alterations in microglia abundance and morphological phenotypes in the hippocampus, Front. Neurol., 8, 700, doi: 10.3389/fneur.2017.00700.
  21. Bosco, D. B., Zheng, J., Xu, Z., Peng, J., Eyo, U. B., Tang, K., Yan, C., Huang, J., Feng, L., Wu, G., Richardson, J. R., Wang, H., and Wu, L. J. (2018) RNAseq analysis of hippocampal microglia after kainic acid-induced seizures, Mol. Brain, 11, 34, doi: 10.1186/s13041-018-0376-5.
  22. Poletaeva, I. I., Surina, N. M., Kostina, Z. A., Perepelkina, O. V., and Fedotova, I. B. (2017) The Krushinsky-Molodkina rat strain: the study of audiogenic epilepsy for 65years, Epilepsy Behav., 71, 130-141, doi: 10.1016/j.yebeh.2015.04.072.
  23. Ross, K. C., and Coleman, J. R. (2000) Developmental and genetic audiogenic seizure models: behavior and biological substrates, Neurosci. Biobehav. Rev., 24, 639-653, doi: 10.1016/s0149-7634(00)00029-4.
  24. Dailey, J. W., Reigel, C. E., Mishra, P. K., and Jobe, P. C. (1989) Neurobiology of seizure predisposition in the genetically epilepsy-prone rat, Epilepsy Res., 3, 3-17, doi: 10.1016/0920-1211(89)90063-6.
  25. Ribak, C. E. (2017) An abnormal GABAergic system in the inferior colliculus provides a basis for audiogenic seizures in genetically epilepsy-prone rats, Epilepsy Behav., 71, 160-164, doi: 10.1016/j.yebeh.2015.02.024.
  26. Garcia-Cairasco, N., Doretto, M. C., Prado, R. P., Jorge, B. P., Terra, V. C., and Oliveira, J. A. (1992) New insights into behavioral evaluation of audiogenic seizures. A comparison of two ethological methods, Behav Brain Res., 48, 49-56, doi: 10.1016/s0166-4328(05)80138-x.
  27. Garcia-Cairasco, N., Umeoka, E. H. L., and Cortes de Oliveira, J. A. (2017) The Wistar Audiogenic Rat (WAR) strain and its contributions to epileptology and related comorbidities: history and perspectives, Epilepsy Behav., 71, 250-273, doi: 10.1016/j.yebeh.2017.04.001.
  28. Muñoz, L. J., Carballosa-Gautam, M. M., Yanowsky, K., García-Atarés, N., and López, D. E. (2017) The genetic audiogenic seizure hamster from Salamanca: the GASH:Sal, Epilepsy Behav., 71, 181-192, doi: 10.1016/j.yebeh.2016.03.002.
  29. Maxson, S. C. (2017) A genetic context for the study of audiogenic seizures, Epilepsy Behav., 71, 154-159, doi: 10.1016/j.yebeh.2015.12.031.
  30. Fedotova, I. B., Surina, N. M., Nikolaev, G. M., Revishchin, A. V., and Poletaeva, I. I. (2021) Rodent brain pathology, audiogenic epilepsy, Biomedicines, 9, 1641, doi: 10.3390/biomedicines9111641.
  31. Фирстова Ю. Ю., Абаимов Д. А., Сурина Н. М., Полетаева И. И., Федотова И. Б., Ковалёв Г. И. (2012) Связывание специфических лигандов D2- и NMDA-рецепторами клеток стриатума крыс двух линий, контрастных по предрасположенности к аудиогенной эпилепсии, Бюлл. Эксп. Биол. Мед., 154, 196-198, doi: 10.1007/s10517-012-1910-6.
  32. Сорокин А. Я., Кудрин В. С., Клодт П. М., Туомисто Л., Полетаева И. И., Раевский К. С. (2004) Межлинейные различия в эффектах амфетамина и раклоприда на активность дофаминергической системы в дорзальном стриатуме крыс линии КМ и Вистар (микродиализное исследование), Генетика, 40, 846-849.
  33. Дорофеева Н. A, Глазова M. В., Худик K. A., Никитина Л. С., Kириллова Д., Черниговская E. В. (2015) Сравнительное исследование нигростриарной системы у крыс линии Вистар и крыс, предрасположенных к судорогам, Журн. Эвол. Биохим. Физиол., 51, 204-213.
  34. Федотова И. Б., Костына З. А., Полетаева И. И., Колпаков В. Г., Барыкина Н. Н., Аксенович Т. И. (2005) Генетический анализ предрасположенности крыс линии Крушинского-Молодкиной к аудиогенной эпилепсии, Генетика, 41, 1487-1494.
  35. Kurtz, B. S., Lehman, J., Garlick, P., Amberg, J., Mishra, P. K., Dailey, J. W., Weber, R., and Jobe, P. C. (2001) Penetrance and expressivity of genes involved in the development of epilepsy in the genetically epilepsy-prone rat (GEPR), J. Neurogenet., 15, 233-244, doi: 10.3109/01677060109167379.
  36. Doretto, M. C., Fonseca, C. G., Lobo, R. B., Terra, V. C., Oliveira, J. A., and Garcia-Cairasco, N. (2003) Quantitative study of the response to genetic selection of the Wistar audiogenic rat strain (WAR), Behav. Genet., 33, 33-42, doi: 10.1023/a:1021099432759.
  37. Lee, Y., Rodriguez, O. C., Albanese, C., Santos, V. R., Cortes de Oliveira, J. A., Donatti, A. L. F., Fernandes, A., Garcia-Cairasco, N., N'Gouemo, P., and Forcelli, P. A. (2018) Divergent brain changes in two audiogenic rat strains: a voxel-based morphometry and diffusion tensor imaging comparison of the genetically epilepsy prone rat (GEPR-3) and the Wistar Audiogenic Rat (WAR), Neurobiol. Dis., 111, 80-90, doi: 10.1016/j.nbd.2017.12.014.
  38. Damasceno, S., Gómez-Nieto, R., Garcia-Cairasco, N., Herrero-Turrión, M. J., Marín, F., and Lopéz, D. E. (2020) Top common differentially expressed genes in the epileptogenic nucleus of two strains of rodents susceptible to audiogenic seizures: WAR and GASH/Sal, Front. Neurol., 11, 33, doi: 10.3389/fneur.2020.00033.
  39. Damasceno, S., Menezes, N. B., Rocha, C. S., Matos, A. H. B., Vieira, A. S., Moraes, M. F. D., Martins, A. S., Lopes-Cendes, I., and Godard, A. L. B. (2018) Transcriptome of the Wistar audiogenic rat (WAR) strain following audiogenic seizures, Epilepsy Res., 147, 22-31, doi: 10.1016/j.eplepsyres.2018.08.010.
  40. Chuvakova, L. N., Funikov, S. Y., Rezvykh, A. P., Davletshin, A. I., Evgen'ev, M. B., Litvinova, S. A., Fedotova, I. B., Poletaeva, I. I., and Garbuz, D. G. (2021) Transcriptome of the Krushinsky-Molodkina audiogenic rat strain and Identification of possible audiogenic epilepsy-associated genes, Front. Mol. Neurosci., 14, 738930, doi: 10.3389/fnmol.2021.738930.
  41. Klein, B. D., Fu, Y. H., Ptacek, L. J., and White, H. S. (2004) c-Fos immunohistochemical mapping of the audiogenic seizure network and tonotopic neuronal hyperexcitability in the inferior colliculus of the Frings mouse, Epilepsy Res., 62, 13-25, doi: 10.1016/j.eplepsyres.2004.06.007.
  42. Neumann, P. E., and Collins R. L. (1991) Genetic dissection of susceptibility to audiogenic seizures in inbred mice, Proc. Natl. Acad. Sci. USA, 88, 5408-5412, doi: 10.1073/pnas.88.12.5408.
  43. Damasceno, S., Fonseca, P. A. S., Rosse, I. C., Moraes, M. F. D., de Oliveira, J. A. C., Garcia-Cairasco, N., and Brunialti Godard, A. L. (2021) Putative causal variant on Vlgr1 for the epileptic phenotype in the model Wistar audiogenic rat, Front. Neurol., 9, 12, 647859, doi: 10.3389/fneur.2021.647859.
  44. Shin, D., Lin, S.T., Fu, Y.H., Ptácek, L.J. (2013) Very large G protein-coupled receptor 1 regulates myelin-associated glycoprotein via Gαs/Gαq-mediated protein kinases A/C, Proc. Natl. Acad. Sci. USA, 19, 110, 19101-19106, doi: 10.1073/pnas.1318501110.
  45. Федотова И.Б., Костына З.А., Сурина Н.М., Полетаева И.И. (2012) Селекция лабораторных крыс на признак "отсутствие предрасположенности к аудиогенной эпилепсии", Генетика, 48, 685-691.
  46. Fedotova, I. B., Surina, N. M., Nikolaev, G. M., and Poletaeva, I. I. (2016) Subthreshold corazol doses induced generalized seizures in audigenic seizure-prone rats, Int. J. Neurol Brain Disord., 3, 1-6.
  47. Ravizza, T., Boer, K., Redeker, S., Spliet, W. G., van Rijen, P. C., Troost, D., Vezzani, A., and Aronica, E. (2006) The IL-1beta system in epilepsy-associated malformations of cortical development, Neurobiol. Dis., 24, 128-43, doi: 10.1016/j.nbd.2006.06.003.
  48. Peltola, J., Palmio, J., Korhonen, L., Suhonen, J., Miettinen, A., Hurme, M., et al. (2000) Interleukin-6 and Interleukin-1 receptor antagonist in cerebrospinal fluid from patients with recent tonic-clonic seizures, Epilepsy Res., 41, 205-211, doi: 10.1016/s0920-1211(00)00140-6.
  49. Haspolat, S., Mihci, E., Coskun, M., Gumuslu, S., Ozben, T., and Yegin, O. (2002) Interleukin1beta, tumor necrosis factor-alpha, and nitrite levels in febrile seizures, J. Child Neurol., 17, 749-751, doi: 10.1177/08830738020170101501.
  50. Uludag, I. F., Bilgin, S., Zorlu, Y., Tuna, G., and Kirkali, G. (2013) Interleukin-6, interleukin-1 beta and interleukin-1 receptor antagonist levels in epileptic seizures, Seizure, 22, 457-461, doi: 10.1016/j.seizure.2013.03.004.
  51. Ryo, Y., Yamaguchi, H., Matsushita, T., Fujii, T., Hiwatashi, A., and Kira, J.-I. (2017) Early strong intrathecal inflammation in cerebellar type multiple system atrophy by cerebrospinal fluid cytokine/chemokine profiles: a case control study, J. Neuroinflamm., 14, 89, doi: 10.1186/s12974-017-0863-0.
  52. Tan, T. H., Perucca, P., O'Brien, T. J., Kwan, P., and Monif, M. (2021) Inflammation, ictogenesis, and epileptogenesis: an exploration through human disease, Epilepsia, 62, 303-324, doi: 10.1111/epi.16788.
  53. Matsuo, T., Komori, R., Nakatani, M., Ochi, S., Yokota-Nakatsuma, A., Matsumoto, J., Takata, F., Dohgu, S., Ishihara, Y., and Itoh, K. (2022) Levetiracetam suppresses the infiltration of neutrophils and monocytes and downregulates many Inflammatory cytokines during epileptogenesis in pilocarpine-induced status epilepticus mice, Int. J. Mol. Sci., 23, 7671, doi: 10.3390/ijms23147671.
  54. Balosso, S., Ravizza, T., Perego, C., Peschon, J., Campbell, I. L., De Simoni, M. G., et al. (2005) Tumor necrosis factor-alpha inhibits seizures in mice via p75 receptors, Ann. Neurol., 57, 804-812, doi: 10.1002/ana.20480.
  55. De Sarro, G., Rotiroti, D., Audino, M.G., Gratteri, S., and Nistico, G. (1994) Effects of interleukin-2 on various models of experimental epilepsy in DBA/2 mice. Neuroimmunomodulation, 1, 361-369, doi: 10.1159/000097189.
  56. De Simoni, M. G., Perego, C., Ravizza, T., Moneta, D., Conti, M., Marchesi, F., et al. (2000) Inflammatory cytokines and related genes are induced in the rat hippocampus by limbic status epilepticus, Eur. J. Neurosci., 12, 2623-2633, doi: 10.1046/j.1460-9568.2000.00140.x.
  57. Benczik, M., and Gaffen, S. L. (2004) The interleukin IL-2 family cytokines: survival and proliferation signaling pathways in T lymphocytes, Immunol. Invest., 33, 109-142, doi: 10.1081/imm-120030732.
  58. De Luca, G., Di Giorgio, R. M., Macaione, S., Calpona P. R., Costantino, S., Di Paola, E. D., De Sarro, A., Ciliberto, G., and De Sarro, G. (2004) Susceptibility to audiogenic seizure and neurotransmitter amino acid levels in different brain areas of IL-6-deficient mice, Pharmacol. Biochem. Behav., 78, 75-81, doi: 10.1016/j.pbb.2004.02.004.
  59. Kostic, D., Carlson, R., Henke, D., Rohn, K., and Tipold, A. (2019) Evaluation of IL-1β levels in epilepsy and traumatic brain injury in dogs, BMC Neurosci., 20, 29, doi: 10.1186/s12868-019-0509-5.
  60. Yamada, M., and Hatanaka, H. (1994) Interleukin-6 protects cultured rat hippocampal neurons against glutamate-induced cell death, Brain Res., 643, 173-180, doi: 10.1016/0006-8993(94)90023-x.
  61. Ali, C., Nicole, O., Docagne, F., Lesne, S., MacKenzie, E. T., Nouvelot, A., et al. (2000) Ischemia-induced interleukin-6 as a potential endogenous neuroprotective cytokine against NMDA receptor-mediated excitotoxicity in the brain, J. Cereb. Blood Flow Metab., 20, 956-966, doi: 10.1097/00004647-200006000-00008.
  62. Toulmond, S., Vige, X., Fage, D., and Benavides, J. (1992) Local infusion of interleukin-6 attenuates the neurotoxic effects of NMDA on rat striatal cholinergic neurons, Neurosci. Lett., 144, 49-52, doi: 10.1016/0304-3940(92)90713-h.
  63. Kishimoto, T., Akira, S., Narazaki, M., and Taga, T. (1995) Interleukin-6 family of cytokines and gp130, Blood, 86, 1243-1254, doi: 10.1182/blood.V86.4.1243.bloodjournal8641243.
  64. Ramos, A. B., Cruz, R. A., Villemarette-Pittman, N. R., Olejniczak, P. W., and Mader, Jr. E. C (2019) Dexamethasone as abortive treatment for refractory seizures or status epilepticus in the inpatient setting, J. Invest. Med. High Impact Case Rep., 7, 2324709619848816, doi: 10.1177/2324709619848816.
  65. Vizuete, A. F. K., Hansen, F., Negri, E., Leite, M. C., de Oliveira, D. L., and Gonçalves, C. A. (2018) Effects of dexamethasone on the Li-pilocarpine model of epilepsy: protection against hippocampal inflammation and astrogliosis, J. Neuroinflamm., 15, 68, doi: 10.1186/s12974-018-1109-5.
  66. Guzzo, E. F. M., Lima, K. R., Vargas, C. R., and Coitinho, A. S. (2018) Effect of dexamethasone on seizures and inflammatory profile induced by Kindling Seizure Model, J. Neuroimmunol., 325, 92-98, doi: 10.1016/j.jneuroim.2018.10.005.
  67. Kamali, A. N., Zian, Z., Bautista, J. M., Hamedifar, H., Hossein-Khannazer, N., Hosseinzadeh, R., Yazdani, R., and Azizi, G. (2021) The potential role of pro-inflammatory and anti-inflammatory cytokines in epilepsy pathogenesis, Endocr. Metab. Immune Disord. Drug Targets, 21, 1760-1774, doi: 10.2174/1871530320999201116200940.
  68. Surina, N. M., Fedotova, I. B., and Poletaeva, I. I. (2022) The effects of acute and chronic infusions of dexamethasone on audiogenic seizures and catalepsy in rats of Krushinsky-Molodkina and "0" Strains, J. Evol. Biochem. Physiol., 58, 1110-1118, doi: 10.1134/S0022093022040147.
  69. Leo, A., Nesci, V., Tallarico, M., Amodio, N., Gallo Cantafio, E. M., De Sarro, G., Constanti, A., et al. (2020) IL-6 receptor blockade by tocilizumab Has anti-absence and anti-epileptogenic effects in the WAG/Rij rat model of absence epilepsy, Neurotherapeutics, 17, 2004-2014, doi: 10.1007/s13311-020-00893-8.
  70. Löscher, W., Ferland, R. J., and Ferraro, T. N. (2017) The relevance of inter- and intrastrain differences in mice and rats and their implications for models of seizures and epilepsy, Epilepsy Behav., 73, 214-235, doi: 10.1016/j.yebeh.2017.05.040.

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