The central nervous system is not immunoprivileged: inflammation and epileptogenesis

  • Dragan Hrnčić University of Belgrade, Faculty of Medicine, Institute of Medical Physiology “Richard Burian”, Laboratory of Neurophysiology, Belgrade, Serbia
  • Nikola Šutulović University of Belgrade, Faculty of Medicine, Institute of Medical Physiology “Richard Burian”, Laboratory of Neurophysiology, Belgrade, Serbia
  • Željko Grubač University of Belgrade, Faculty of Medicine, Institute of Medical Physiology “Richard Burian”, Laboratory of Neurophysiology, Belgrade, Serbia
  • Aleksandra Rašić - Marković University of Belgrade, Faculty of Medicine, Institute of Medical Physiology “Richard Burian”, Laboratory of Neurophysiology, Belgrade, Serbia
  • Olivera Stanojlović University of Belgrade, Faculty of Medicine, Institute of Medical Physiology “Richard Burian”, Laboratory of Neurophysiology, Belgrade, Serbia
Keywords: central nervous system;, epilepsy;, inflammation;, oxidative stress.

Author Biographies

Dragan Hrnčić, University of Belgrade, Faculty of Medicine, Institute of Medical Physiology “Richard Burian”, Laboratory of Neurophysiology, Belgrade, Serbia

Assistant Professor, MD, PhD

Olivera Stanojlović, University of Belgrade, Faculty of Medicine, Institute of Medical Physiology “Richard Burian”, Laboratory of Neurophysiology, Belgrade, Serbia

Full Professor, Principal Investigator and Head

References

References

Riazi K, Galic MA, Pittman QJ. Contributions of periph¬eral in-flammation to seizure susceptibility: Cytokines and brain ex-citability. Epilepsy Res 2010; 89(1): 34‒42.

Fisher RS, van Emde BW, Blume W, Elger C, Genton P, Lee P, et al. Epileptic seizures and epilepsy: Definitions pro¬posed by the International League Against Epilepsy (ILAE) and the Inter-national Bureau for Epilepsy (IBE). Epilepsia 2005; 46(4): 470‒2.

McNamara JO, Huang YZ, Leonard AS. Molecular signaling mechanisms underlying epileptogenesis. Sci STKE 2006; 2006(356): re12.

World Health Organization. Epilepsy. Epilepsy: Epidemiol¬ogy, aetiology and prognosis. Fact Sheet No.165.Geneva: World Health Organization; 2001.

World Health Organization. Epilepsy. Epilepsy: Epidemiol¬ogy, aetiology and prognosis. Fact Sheet Update. Geneva: World Health Organization; 2016.

Heise C, Taha E, Murru L, Ponzoni L, Cattaneo A, Guarni¬eri FC, et al. eEF2K/eEF2 Pathway Controls the Excita-tion/Inhibition Balance and Susceptibility to Epileptic Sei-zures. Cereb Cortex 2017; 27(3): 2226‒48.

Shneker BF, Fountain NB. Epilepsy. Dis Mon 2003; 49(7): 426‒78.

Stanojlović O, Živanović D, Šušić V. N-Methyl-D-aspartic acid- and metaphit-induced audiogenic seizures in rat model of sei-zures. Pharmacol. Res 2000; 42(3): 247‒53.

Hrnčić D, Rašić-Marković A, Đurić D, Sušić V, Stanojlović O. The role of nitric oxide in convulsions induced by lin¬dane in rats. Food Chem Toxicol 2011; 49(4): 947‒54.

Mladenović D, Hrnčić D, Vučević D, Radosavljević T, Lon¬čar-Stevanović H, Petrović J, et al. Ethanol suppressed sei¬zures in lin-dane-treated rats. Electroencephalographic and behavioral studies. J Physiol Pharmacol 2007; 58(4): 641‒56.

Šusić V, Marković O. Potentiation of metaphit-induced audio-genic seizures by REM sleep deprivation in rats. Physiol Behav 1993; 54(2): 331‒8.

Hrnčić D, Rašić-Marković A, Bjekić-Macut J, Šušić V, Đuric D, Stanojlović O. Paradoxical sleep deprivation potentiates epilepsy induced by homocysteine thiolactone in adult rats. Exp Biol Med (Maywood) 2013; 238(1): 77‒83.

Hrnčić D, Grubač Ž, Rašić-Marković A, Šutulović N, Šušić V, Bjekić-Macut J, et al. Sleep disruption increases seizure sus-ceptibility: Behavioral and EEG evaluation of an experi-mental model of sleep apnea. Physiol Behav 2016; 155: 188‒94.

Stanojlović O, Rašić-Marković A, Hrnčić D, Šušić V, Macut Đ, Ra-dosavljević T, et al. Two types of seizures in homo¬cysteine thio-lactone-treated adult rats, behavioral and elec-troencephalographic study. Cell Mol Neurobiol 2009; 29(3): 329‒39.

Zifkin BG, Inoue Y. Visual Reflex Seizures Induced by Com-plex Stimuli. Epilepsia 2004; 45(Suppl 1): 27‒9.

Moon HJ, Seo JG, Park SP. Perceived stress and its predic¬tors in people with epilepsy. Epilepsy Behav 2016; 62: 47‒52.

Herzog AG, Fowler KM, Sperling MR, Massaro JM. Progester¬one Trial Study Group. Distribution of seizures across the men-strual cycle in women with epilepsy. Epi¬lepsia 2015; 56(5): e58‒62.

Gordon KE, Dooley JM. Food insecurity and epilepsy in a na-tionally representative sample. Epilepsy Behav 2015; 43: 139‒42.

Hrnčić D, Rašić-Marković A, Stojković T, Velimirović M, Puškaš N, Obrenović R, et al. Hyperhomocysteinemia in¬duced by methio-nine dietary nutritional overload modu¬lates acetylcholinester-ase activity in the rat brain. Mol Cell Biochem 2014; 396(1‒2): 99‒105.

Annegers JF, Rocca WA, Hauser WA. Causes of epilepsy: Con-tributions of the Rochester epidemiology project. Mayo Clin Proc 1996; 71(6): 570‒5.

Stanojlović O, Živanović D. Experimental models of epi¬lepsy. Med Pregl 2004; 57(7‒8): 359‒62.

Živanović D, Stanojlović OS, Šušić V. Effects of manipula¬tion of N-methyl-D-aspartate receptors on imipenem/cilastatin-induced seizures in rats. Indian J Med Res 2004; 119(2): 79‒85.

Živanović D, Stanojlović O, Stojanović J, Šušić V. Induction of au-diogenic seizures in imipenem/cilastatin-treated rats. Epilepsy Behav 2004; 5(2): 151‒8.

Tokiwa T, Inoue T, Fujii M, Ishizuka S, Aou S, Kida H, et al. Penicillin-induced epileptiform activity elevates focal brain temperature in anesthetized rats. Neurosci Res 2013; 76(4): 257‒60.

Ferrero-Miliani L, Nielsen OH, Andersen PS, Girardin SE. Chronic inflammation: Importance of NOD2 and NALP3 in interleukin-1beta generation. Clin Exp Immunol 2007; 147(2): 227‒35.

Gendelman HE. Neural immunity: Friend or foe? J Neuro¬virol 2002; 8(6): 474‒9.

Das Sarma J. Microglia-mediated neuroinflammation is an am-plifier of virus-induced neuropathology. J Neurovirol 2014; 20(2): 122‒36.

di Filippo M, Chiasserini D, Gardoni F, Viviani B, Tozzi A, Giampà C, et al. Effects of central and peripheral inflam-mation on hippocampal synaptic plasticity. Neurobiol Dis 2013; 52: 229‒36.

't Hart BA, den Dunnen WF. Commentary on special issue: CNS diseases and the immune system. J Neuroimmune Phar-macol 2013; 8(4): 757‒9.

Téllez-Zenteno JF, Matijevic S, Wiebe S. Somatic comorbid¬ity of epilepsy in the general population in Canada. Epi¬lepsia 2005; 46(12): 1955‒62.

Majores M, Eils J, Wiestler OD, Becker AJ. Molecular profil¬ing of temporal lobe epilepsy: Comparison of data from human tissue samples and animal models. Epilepsy Res 2004; 60(2‒3): 173‒8.

Ravizza T, Gagliardi B, Noé F, Boer K, Aronica E, Vezzani A. Innate and adaptive immunity during epileptogenesis and spontaneous seizures: Evidence from experimental models and human temporal lobe epilepsy. Neurobiol Dis 2008; 29(1): 142‒60.

Aronica E, Crino PB. Inflammation in epilepsy: Clinical ob-servations. Epilepsia 2011; 52(Suppl 3): 26‒32.

Janigro D, Iffland PH, Marchi N, Granata T. A role for in-flammation in status epilepticus is revealed by a review of cur-rent therapeutic approaches. Epilepsia 2013; 54(Suppl 6): 30‒2.

Godukhin OV, Levin SG, Parnyshkova YE. The effects of in-terleukin-10 on the development of epileptiform activity in the hippocampus induced by transient hypoxia, bicu¬culline, and electrical kindling. Neurosci Behav Physiol 2009; 39(7): 625‒31.

Kawamura Y, Yamazaki Y, Ohashi M, Ihira M, Yoshikawa T. Cy-tokine and chemokine responses in the blood and cerebrospi-nal fluid of patients with human herpesvirus 6B-associated acute encephalopathy with biphasic seizures and late reduced diffusion. J Med Virol 2014; 86(3): 512‒8.

Vezzani A, Granata T. Brain inflammation in epilepsy: Ex-perimental and clinical evidence. Epilepsia 2005; 46(11): 1724‒43.

Xu D, Miller SD, Koh S. Immune mechanisms in epilepto-genesis. Front Cell Neurosci 2013; 7: 195.

Dityatev A. Remodeling of extracellular matrix and epilepto-genesis. Epilepsia 2010; 51(Suppl 3): 61‒5.

Dityatev A, Fellin T. Extracellular matrix in plasticity and epi-leptogenesis. Neuron Glia Biol 2008; 4(3): 235‒47.

Pitkänen A, Ndode-Ekane XE, Łukasiuk K, Wilczynski GM, Dityatev A, Walker MC, et al. Neural ECM and epilepsy. Prog Brain Res 2014; 214: 229‒62.

Sorokin L. The impact of the extracellular matrix on in-flammation. Nat Rev Immunol 2010; 10(10): 712‒23.

Gaudet AD, Popovich PG. Extracellular matrix regulation of in-flammation in the healthy and injured spinal cord. Exp Neurol 2014; 258: 24‒34.

Vezzani A, Baram TZ. New Roles for Interleukin-1 Beta in the Mechanisms of Epilepsy. Epilepsy Curr 2007; 7(2): 45‒50.

Choi J, Nordli DR, Alden TD, Dipatri A, Laux L, Kelley K, et al. Cellular injury and neuroinflammation in children with chron-ic intractable epilepsy. J Neuroinflammation 2009; 6(1): 38.

Viviani B, Gardoni F, Marinovich M. Cytokines and neu¬ronal ion channels in health and disease. Int Rev Neuro¬biol 2009; 82: 247‒63.

Wetherington J, Serrano G, Dingledine R. Astrocytes in the epi-leptic brain. Neuron 2008; 58(2): 168‒78.

Friedman A, Kaufer D, Heinemann U. Blood-brain barrier breakdown-inducing astrocytic transformation: Novel tar¬gets for the prevention of epilepsy. Epilepsy Res 2009; 85(2‒3): 142‒9.

Puttachary S, Sharma S, Stark S, Thippeswamy T. Seizure-in¬duced oxidative stress in temporal lobe epilepsy. Biomed Res Int 2015; 2015: 745613.

Mendez-Armenta M, Nava-Ruiz C, Juarez-Rebollar D, Rodri¬guez-Martinez E, Gomez PY. Oxidative stress associated with neu-ronal apoptosis in experimental models of epi¬lepsy. Oxid Med Cell Longevity 2014; 2014: 293689.

Pecorelli A, Natrella F, Belmonte G, Miracco C, Cervellati F, Ciccoli L, et al. NADPH oxidase activation and 4-hydroxy-2-nonenal/aquaporin-4 adducts as possible new players in oxida-tive neuronal damage presents in drug-resistant epi¬lepsy. Bio-chim Biophys Acta 2015; 1852(3): 507‒19.

Sudha K, Rao AV, Rao A. Oxidative stress and antioxidants in epilepsy. Clin Chim Acta 2001; 303(1‒2): 19‒24.

Warner TA, Kang JQ, Kennard JA, Harrison FE. Low brain ascorbic acid increases susceptibility to seizures in mouse models of decreased brain ascorbic acid transport and Alz-heimer's disease. Epilepsy Res 2015; 110: 20‒5.

Mladenović D, Djuric D, Petronijević N, Radosavljević T, Ra¬donjić N, Matić D, et al. The correlation between lipid peroxidation in different brain regions and the severity of lindane-induced seizures in rats. Mol Cell Biochem 2010; 333(1‒2): 243‒50.

Ambrogini P, Minelli A, Galati C, Betti M, Lattanzi D, Ciffo¬lilli S, et al. Post-seizure α-tocopherol treatment de¬creases neu-roinflammation and neuronal degeneration in¬duced by status epilepticus in rat hippocampus. Mol Neurobiol 2014; 50(1): 246‒56.

Tomé Ada R, Feitosa CM, Freitas RM. Neuronal damage and memory deficits after seizures are reversed by ascorbic acid. Arq Neuropsiquiatr 2010; 68(4): 579‒85.

Hrnčić D, Rašić-Marković A, Leković J, Krstić D, Čolović M, Macut D, et al. Exercise decreases susceptibility to homo¬cysteine sei-zures: The role of oxidative stress. Int J Sports Med 2014; 35(7): 544‒50.

Simard AR, Rivest S. Do pathogen exposure and innate im-munity cause brain diseases? Neurol Res 2005; 27(7): 717‒25.

Vezzani A, Aronica E, Mazarati A, Pittman QJ. Epilepsy and brain inflammation. Exp Neurol 2013; 244: 11‒21.

Sayyah M, Javad-Pour M, Ghazi-Khansari M. The bacterial endo-toxin lipopolysaccharide enhances seizure susceptibil¬ity in mice: Involvement of proinflammatory factors. ni¬tric oxide and prostaglandins. Neurosci 2003; 122(4): 1073‒80.

Balter-Seri J, Yuhas Y, Weizman A, Nofech-Mozes Y, Kamin¬sky E, Ashkenazi S. Role of nitric oxide in the enhancement of pen-tylenetetrazole-induced seizures caused by Shigella dysenteri-ae. Infect. Immun. 1999; 67(12): 6364‒8.

Yuhas Y, Weizman A, Vanichkin A, Ashkenazi S. Involve¬ment of prostaglandins in an animal model of Shigella-re¬lated sei-zures. J Neuroimmunol 2005; 168(1‒2): 34‒9.

Rao RS, Medhi B, Saikia UN, Arora SK, Toor JS, Khanduja KL, et al. Experimentally induced various inflammatory models and seizure: Understanding the role of cytokine in rat. Eur Neuropsychopharmacol 2008; 18(10): 760‒7.

Riazi K, Honar H, Homayoun H, Demehri S, Bahadori M, Dehpour AR. Intestinal inflammation alters the susceptibil¬ity to pen-tylenetetrazole-induced seizure in mice. J. Gas¬troenterol. Hepatol 2004; 19(3): 270‒7.

Hrncić D, Rasić-Marković A, Krstić D, Macut D, Djuric D, Stanojlović O. The role of nitric oxide in homocysteine thio-lactone-induced seizures in adult rats. Cell Mol Neurobiol 2010; 30(2): 219‒31.

Murta V, Farias MI, Pitossi FJ, Ferrari CC. Chronic systemic IL-1beta exacerbates central neuroinflammation independ-ently of the blood-brain barrier integrity. J Neuroimmu¬nol 2015; 278: 30‒43.

D’Mello C, Le T, Swain MG. Cerebral microglia recruit mono-cytes into the brain in response to tumor necrosis factoralpha signaling during peripheral organ inflamma¬tion. J Neurosci 2009; 29(7): 2089‒102.

Silverman HA, Dancho M, Regnier-Golanov A, Nasim M, Ochani M, Olofsson PS, et al. Brain Region-specific Altera¬tions in the Gene Expression of Cytokines, Immune Cell Markers and Cholinergic System Components During Pe¬ripheral Endotox-in-induced Inflammation. Mol Med 2015; 11(20): 601‒11.

Turrin NP, Gayle D, Ilyin SE, Flynn MC, Langhans W, Schwartz GJ, et al. Pro-inflammatory and anti-inflamma¬tory cytokine mRNA induction in the periphery and brain following intra-peritoneal administration of bacterial lipopolysaccharide. Brain Res Bull 2001; 54(4): 443‒53.

Ho YH, Lin YT, Wu CW, Chao YM, Chang AY, Chan JY. Pe-ripheral inflammation increases seizure susceptibility via the induction of neuroinflammation and oxidative stress in the hippocampus. J Biomed Sci 2015; 22: 46.

Wu KL, Chan SH, Chan JY. Neuroinflammation and oxida¬tive stress in rostral ventrolateral medulla contribute to neurogenic hypertension induced by systemic inflam¬mation. J Neuroin-flam 2012; 9: 212.

Rojas A, Jiang J, Ganesh T, Yang M, Lelutiu N, Gueorguieva P, et al. Cyclooxygenase-2 in epilepsy. Epilepsia 2014; 55(1): 17‒25.

Takei S, Hasegawa-Ishii S, Uekawa A, Chiba Y, Umegaki H, Ho-sokawa M, et al. Immunohistochemical demonstration of in-creased prostaglandin F(2)alpha levels in the rat hip¬pocampus following kainic acid-induced seizures. Neurosci 2012; 218: 295‒304.

Eun BL, Abraham J, Mlsna L, Kim MJ, Koh S. Lipopolysac-charide potentiates hyperthermia-induced seizures. Brain Be-hav 2015; 5(8): e00348.

Published
2020/12/08
Section
Review Paper