nach oben

Erschienen in:

30.10.2019 | Original Article

Activation of the phagocyte NADPH oxidase/NOX2 and myeloperoxidase in the mouse brain during pilocarpine-induced temporal lobe epilepsy and inhibition by ketamine

verfasst von: Fatma Tannich, Asma Tlili, Coralie Pintard, Amina Chniguir, Bruno Eto, Pham My-Chan Dang, Ouajdi Souilem, Jamel El-Benna

Erschienen in: Inflammopharmacology | Ausgabe 2/2020

Einloggen, um Zugang zu erhalten

Abstract

Excessive reactive oxygen species (ROS) production can induce tissue injury involved in a variety of neurodegenerative disorders such as neurodegeneration observed in pilocarpine-induced temporal lobe epilepsy. Ketamine, a noncompetitive N-methyl-D-aspartate (NMDA) receptor antagonist has beneficial effects in pilocarpine-induced temporal lobe epilepsy, when administered within minutes of seizure to avoid the harmful neurological lesions induced by pilocarpine. However, the enzymes involved in ROS productions and the effect of ketamine on this process remain less documented. Here we show that during pilocarpine-induced epilepsy in mice, the expression of the phagocyte NADPH oxidase NOX2 subunits (NOX2/gp91^phox, p22^phox, and p47^phox) and the expression of myeloperoxidase (MPO) were dramatically increased in mice brain treated with pilocarpine. Interestingly, treatment of mice with ketamine before or after pilocarpine administration decreased this process, mainly when injected before pilocarpine. Finally, our results showed that pilocarpine induced p47^phox phosphorylation and H₂O₂ production in mice brain and ketamine was able to inhibit these processes. Our results show that pilocarpine induced NOX2 activation to produce ROS in mice brain and that administration of ketamine before or after the induction of temporal lobe epilepsy by pilocarpine inhibited this activation in mice brain. These results suggest a key role of the phagocyte NADPH oxidase NOX2 and MPO in epilepsy and identify a novel effect of ketamine.

Bedard K, Krause KH (2007) The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 87:245–313PubMed

Belambri SA, Rolas L, Raad H, Hurtado-Nedelec M, Dang PM, El-Benna J (2018) NADPH oxidase activation in neutrophils: role of the Phosphorylation of its subunits. Eur J Clin Invest 48:e12951PubMed

Bellissimo MI, Amado D, Abdalla DS, Ferreira EC, Cavalheiro EA, Naffah-Mazzacoratti MG (2001) Superoxide dismutase, glutathione peroxidase activities and the hydroperoxide concentration are modified in the hippocampus of epileptic rats. Epilepsy Res 46:121–128PubMed

Beltramini GC, Cendes F, Yasuda CL (2015) The effects of antiepileptic drugs on cognitive functional magnetic resonance imaging. Quant Imaging Med Surg 5:238–246PubMedPubMedCentral

Boussetta T, Gougerot-Pocidalo MA, Hayem G, Ciappelloni S, Raad H, Arabi Derkawi R, Bournier O, Kroviarski Y, Zhou XZ, Malter JS, Lu PK, Bartegi A, Dang PM, El-Benna J (2010) The prolyl isomerase Pin1 acts as a novel molecular switch for TNF-alpha-induced priming of the NADPH oxidase in human neutrophils. Blood 116:5795–5802PubMedPubMedCentral

Brennan-Minnella AM, Shen Y, El-Benna J, Swanson RA (2013) Phosphoinositide 3-kinase couples NMDA receptors to superoxide release in excitotoxic neuronal death. Cell Death Dis 4:e580PubMedPubMedCentral

Can A, Zanos P, Moaddel R, Kang HJ, Dossou KS, Wainer IW, Cheer JF, Frost DO, Huang XP, Gould TD (2016) Effects of ketamine and ketamine metabolites on evoked striatal dopamine release, dopamine receptors, and monoamine transporters. J Pharmacol Exp 359:159–170

Cavalheiro EA, Leite JP, Bortolotto ZA, Turski WA, Ikonomidou C, Turski L (1991) Long-term effects of pilocarpine in rats: structural damage of brain triggers kindling and spontaneous recurrent seizures. Epilepsia 32:778–782PubMed

Colucci DG, Puig NR (2013) Influence of anaesthetic drugs on immune response: from inflammation to immunosuppression. OA Anaesth 1:1–7

Curia G, Longo D, Biagini G, Jones RSG, Avoli M (2008) The pilocarpine model of temporal lobe epilepsy. J Neurosci Methods 172:143–157PubMedPubMedCentral

Curia G, Lucchi C, Vinet J, Gualtieri F, Marinelli C, Torsello A, Costantino L, Biagini G (2014) Pathophysiogenesis of mesial temporal lobe epilepsy: is prevention of damage antiepileptogenic? Curr Med Chem 21:663–688PubMedPubMedCentral

Cusin C, Ionescu DF, Pavone KJ, Akeju O, Cassano P, Taylor N, Eikermann M, Durham K, Swee MB, Chang T, Dording C, Soskin D, Kelley J, Mischoulon D, Brown EN, Fava M (2017) Ketamine augmentation for outpatients with treatment-resistant depression: preliminary evidence for two-step intravenous dose escalation. Aust N Z J Psychiatry 51:55–64PubMed

De Oliveira DL, Fischer A, Jorge RS, da Silva MC, Leite M, Gonçalves CA, Quillfeldt JA, Souza DO, e Souza TM, Wofchuk S (2008) Effects of early-life LiCl-pilocarpine-induced status epilepticus on memory and anxiety in adult rats are associated with mossy fiber sprouting and elevated CSF S100B protein. Epilepsia 49:842–852PubMed

Degos V, Charpentier TL, Chhor V, Brissaud O, Lebon S, Schwendimann L, Bednareck N, Passemard S, Mantz J, Gressens P (2013) Neuroprotective effects of dexmedetomidine against glutamate agonist-induced neuronal cell death are related to increased astrocyte brain-derived neurotrophic factor expression. Anesthesiology 118:1123–1132PubMed

Dhote F, Carpentier P, Barbier L, Peinnequin A, Baille V, Pernot F, Testylier G, Beaup C, Foquin A, Dorandeu F (2012) Combinations of ketamine and atropine are neuroprotective and reduce neuroinflammation after a toxic status epilepticus in mice. Toxicol Appl Pharmacol 259:195–209PubMed

El-benna J, Dang PM, Marie J, Braut-boucher F (2009) p47phox, the phagocyte NADPH oxidase/NOX2 organizer: structure, phosphorylation and implication in diseases. Exp Mol Med 41:217–225PubMedPubMedCentral

El-Benna J, Hurtado-Nedelec M, Marzaioli V, Marie JC, Gougerot-Pocidalo MA, Dang PM (2016) Priming of the neutrophil respiratory burst: role in host defense and inflammation. Immunol Rev 273:180–193PubMed

Fujikawa DG (1995) Neuroprotective effect of ketamine administered after status epilepticus onset. Epilepsia 36:186–195PubMed

Garber JC, National Research Council (2011) Guide for the care and use of laboratory animals, 8th edn. National Academies Press, Washington, DC, pp 246–247

Giordano C, Vinet J, Curia G, Biagini G (2015) Repeated 6-Hz corneal stimulation progressively increases FosB/ΔFosB levels in the lateral amygdala and induces seizure generalization to the hippocampus. PLoS One 10:e0141221PubMedPubMedCentral

Goldblum SE, Wu KM, Jay M (1985) Lung myeloperoxidase as a measure of pulmonary leukostasis in rabbits. J Appl Physiol 59:1978–1985PubMed

Görlach A, Bertram K, Hudecova S, Krizanova O (2015) Calcium and ROS: a mutual interplay. Redox Biol 6:260–271PubMedPubMedCentral

Gröticke I, Hoffmann K, Löscher W (2007) Behavioral alterations in the pilocarpine model of temporal lobe epilepsy in mice. Exp Neurol 207:329–349PubMed

Hayashi Y, Kawaji K, Sun I, Zhang X, Koyano K, Yokoyama T, Kohsaka S, Inoue K, Nakanishi H (2011) Microglia Ca (2+)-activated K (+) channels are possible molecular targets for the analgesic effects of S-ketamine on neuropathic pain. J Neurosci 31:17370–17382PubMedPubMedCentral

Hernandes MS, Britto LRG (2012) NADPH oxidase and neurodegeneration. Curr Neuropharmacol 10:321–327PubMedPubMedCentral

Hervera A, De Virgiliis F, Palmisano I, Zhou L, Tantardini E, Kong G, Hutson T, Danzi MC, Perry RB, Santos CXC, Kapustin AN, Fleck RA, Del Río JA, Carroll T, Lemmon V, Bixby JL, Shah AM, Fainzilber M, Di Giovanni S (2018) Regeneration through the release of exosomal NADPH oxidase 2 complexes into injured axons. Nat Cell Biol 20:307–319PubMed

Hiragi T, Ikegaya Y, Koyama R (2018) Microglia after seizures and in epilepsy. Cells 7:26PubMedCentral

Honeycutt JA, Chrobak JJ (2018) Parvalbumin loss following chronic sub-anesthetic NMDA antagonist treatment is age-dependent in the hippocampus: implications for modeling NMDA hypofunction. Neuroscience 21:73–82

Infanger DW, Sharma RV, Davisson RL (2006) NADPH oxidases of the brain distribution, regulation and function. Int J Biol Stress 8:152–162

Khan AA, Alsahli MA, Rahmani AH (2018) Myeloperoxidase as an active disease biomarker: its recent biochemical and pathological perspectives. Med Sci (Basel) 6:33

Kim JH, Jang BG, Choi BY, Kim HS, Sohn M, Chung TN, Choi HC, Song HK, Suh SW (2013) Post-treatment of an NADPH oxidase inhibitor prevents seizure-induced neuronal death. Brain Res 1499:163–172PubMed

Kobayashi M, Wen X, Buckmaster PS (2003) Reduced inhibition and increased output of layer II neurons in the medial entorhinal cortex in a model of temporal lobe epilepsy. J Neurosci 23:8471–8479PubMedPubMedCentral

Kumar SS, Buckmaster PS (2006) Hyperexcitability, interneurons, and loss of GABAergic synapses in entorhinal cortex in a model of temporal lobe epilepsy. Neurobiol Dis 26:4613–4623

Kwak SE, Kim JE, Kim DS, Won MH, Lee HJ, Choi SY (2006) Differential paired-pulse responses between the CA1 region and the dentate gyrus are related to altered CLC-2 immunoreactivity in the pilocarpine-induced rat epilepsy model. Brain Res 1115:162–168PubMed

Lenz M, Ben Shimon M, Deller T, Vlachos A, Maggio N (2017) Pilocarpine-induced status epilepticus is associated with changes in the actin-modulating protein synaptopodin and alterations in long-term potentiation in the mouse hippocampus. Neural Plast 2017:2652560PubMedPubMedCentral

Liang J, Wu S, Xie W, He H (2018) Ketamine ameliorates oxidative stress-induced apoptosis in experimental traumatic brain injury via the Nrf2 pathway. Drug Des Dev Ther 12:845–853

Loix S, De Kock M, Henin P (2011) The anti-inflammatory effects of ketamine: state of the art. Acta Anaesthesiol Belg 62:47–58PubMed

Loo CK, Gálvez V, O’Keefe E, Mitchell PB, Hadzi-Pavlovic D, Leyden J, Harper S, Somogyi AA, Lai R, Weickert CS, Glue P (2016) Placebo-controlled pilot trial testing dose titration and intravenous, intramuscular and subcutaneous routes for ketamine in depression. Acta Psychiatr Scand 134:48–56PubMed

Loss CM, Córdova SD, De Oliveira DL (2012) Ketamine reduces neuronal degeneration and anxiety levels when administered during early life-induced status epilepticus in rats. Brain Res 1474:110–117PubMed

Ma MW, Wang J, Zhang Q, Wang R, Dhandapani KM, Vadlamudi RK, Brann DW (2017) NADPH oxidase in brain injury and neurodegenerative disorders. Mol Neurodegener 12:1–28

Manocha A, Sharma KK, Mediratta PK (2001) Possible mechanism of anticonvulsant effect of ketamine in mice. Indian J Exp Biol 39:1002–1008PubMed

Marchi N, Oby E, Batra A, Uva L, De Curtis M, Hernandez N, Van Boxel-Dezaire A, Najm I, Janigro D (2007) Invivo and invitro effects of pilocarpine: relevance to ictogenesis. Epilepsia 48:1934–1946PubMedPubMedCentral

Mazzuferi M, Kumar G, Rospo C, Kaminski RM (2012) Rapid epileptogenesis in the mouse pilocarpine model: video-EEG, pharmacokinetic and histopathological characterization. Exp Neurol 238:156–167PubMed

Mcgirr A, Ledue JA, Chan W, Xie Y (2017) Murphy TH Cortical functional hyperconnectivity in a mouse model of depression and selective network effects of ketamine. Brain 140:2210–2225PubMed

Müller CJ, Gröticke I, Hoffmann K, Schughart K, Löscher W (2009) Differences in sensitivity to the convulsant pilocarpine in substrains and sublines of C57BL/6 mice. Genes Brain Behav 8:481–492PubMed

Nishina K, Akamatsu H, Mikawa K, Shiga M, Maekawa N, Obara H, Niwa Y (1998) The inhibitory effects of thiopental, midazolam, and ketamine on human neutrophil functions. Anesth Analg 86:159–165PubMed

Patel M, Li Q, Chang L, Crapo J, Liang L (2005) Activation of NADPH oxidase and extracellular superoxide production in seizure-induced hippocampal damage. J Neurochem 92:123–131PubMed

Pestana RRF, Kinjo ER, Hernandes MS, Britto LRG (2010) Neuroscience letters reactive oxygen species generated by NADPH oxidase are involved in neurodegeneration in the pilocarpine model of temporal lobe epilepsy. Neurosci Lett 484:187–191PubMed

Pitsch J, Schoch S, Gueler N, Flor PJ, van der Putten H, Becker AJ (2007) Functional role of mGluR1 and mGluR4 in pilocarpine-induced temporal lobe epilepsy. Neurobiol Dis 26:623–633PubMed

Qin B, Wang Q, Lu Y, Li C, Hu H, Zhang J, Wang Y, Zhu J, Zhu Y, Xun Y, Wang S (2018) Losartan ameliorates calcium oxalate-induced elevation of stone-related proteins in renal tubular cells by inhibiting NADPH oxidase and oxidative stress. Oxidative Med Cell Longev 2018:1271864

Rana A, Musto AE (2018) The role of inflammation in the development of epilepsy. J Neuroinflamm 15:1–12

Rasmussen KG, Lineberry TW, Galardy CW, Kung S, Lapid MI, Palmer BA, Ritter MJ, Schak KM, Sola CL, Hanson AJ, Frye MA (2013) Serial infusions of low-dose ketamine for major depression. J Psychopharmacol 27:444–450PubMed

Ravizza T, Gagliardi B, Noé F, Boer K, Aronica E, Vezzani A (2008) Innate and adaptive immunity during epileptogenesis and spontaneous seizures: evidence from experimental models and human temporal lobe epilepsy. Neurobiol Dis 29:142–160PubMed

Réus GZ, Stringari RB, Ribeiro KF, Ferraro AK, Vitto MF, Cesconetto P, Souza CT, Quevedo J (2011) Ketamine plus imipramine treatment induces antidepressant-like behavior and increases CREB and BDNF protein levels and PKA and PKC phosphorylation in rat brain. Behav Brain Res 221:166–171PubMed

Santi SA, Cook LL, Persinger MA, O’Connor RP (2001) Normal spatial memory following postseizure treatment with ketamine: selective damage attenuates memory deficits in brain-damaged rodents. Int J Neurosci 107:63–75PubMed

Sills GJ, Solomon T (2009) Breaching the barrier and inflaming epilepsy research. Epilepsy Curr 9:148–150PubMedPubMedCentral

Silverberg J, Ginsburg D, Orman R, Amassian V, Durkin HG, Stewart M (2010) Lymphocyte infiltration of neocortex and hippocampus after a single brief seizure in mice. Brain Behav Immun 24:263–272PubMed

Singh JB, Fedgchin M, Daly E, Xi L, Melman C, De Bruecker G, Tadic A, Sienaert P, Wiegand F, Manji H, Drevets WC, Van Nueten L (2016) Intravenous esketamine in adult treatment resistant depression: a double-blind, double-randomization, placebo-controlled study. Biol Psychiatry 80:424–431PubMed

Stewart LS, Persinger MA (2001) Ketamine prevents learning impairment when administered immediately after status epilepticus onset. Epilepsy Behav 2:585–591PubMed

Takahashi T, Kinoshita M, Shono S, Habu Y, Ogura T, Seki S, Kazama T (2010) The effect of ketamine anesthesia on the immune function of mice with postoperative septicemia. Anesth Analg 111:1051–1058PubMed

Turski WA, Cavalheiro EA, Bortolotto ZA, Mello LM, Schwarz M, Turski L (1984) Seizures produced by pilocarpine in mice: a behavioral, electroencephalographic and morphological analysis. Brain Res 321:237–253PubMed

Üllen A, Singewald E, Konya V, Fauler G, Reicher H, Nusshold C, Hammer A, Kratky D, Heinemann A, Holzer P, Malle E, Sattler W (2013) Myeloperoxidase-derived oxidants induce blood–brain barrier dysfunction in vitro and in vivo. PLoS One 8:1–15

Vinet J, Vainchtein ID, Spano C, Giordano C, Bordini D, Curia G, Dominici M, Boddeke HW, Eggen BJ, Biagini G (2016) Microglia are less pro-inflammatory than myeloid infiltrates in the hippocampus of mice exposed to status epilepticus. Glia 64:1350–1362PubMed

Waldbaum S, Patel M (2010) Mitochondrial dysfunction and oxidative stress: a contributing link to acquired epilepsy? J Bioenerg Biomembr 42:449–455PubMedPubMedCentral

Wang NAN, Yu HY, Shen XF, Gao ZQ, Yang C, Yang JJ, Zhang GF (2015) The rapid antidepressant effect of ketamine in rats is associated with down-regulation of pro-inflammatory cytokines in the hippocampus. Upsala J Med Sci 120:241–248PubMedPubMedCentral

Webster KM, Sun M, Crack P, O’Brien TJ, Shultz SR, Semple BD (2017) Inflammation in epileptogenesis after traumatic brain injury. J Neuroinflamm 14:10

Weigand MA, Schmidt H, Zhao Q, Plaschke K, Martin E, Bardenheuer HJ (2000) Ketamine modulates the stimulated adhesion molecule expression on human neutrophils in vitro. Anesth Analg 90:206–212PubMed

Wymann MP, von Tscharner V, Deranleau DA, Baggiolini M (1987) Chemiluminescence detection of H₂O₂ produced by human neutrophils during the respiratory burst. Anal Biochem 165:371–378PubMed

Yang L, Jin M, Du P, Chen G, Zhang C, Wang J, Jin F, Shao H, She Y, Wang S, Zheng L, Wang J (2015) Study on enhancement principle and stabilization for the luminol-H₂O₂-HRP chemiluminescence system. PLoS One 10:1–14

Yuryev M, Pellegrino C, Jokinen V, Andriichuk L, Khirug S, Khiroug L, Rivera C (2016) In vivo calcium imaging of evoked calcium waves in the embryonic cortex. Front Cell Neurosci 9:1–9

Zanos P (2018) Ketamine and ketamine metabolite pharmacology: insights into therapeutic mechanisms. Pharmacol Rev 70:621–660PubMedPubMedCentral

Zappacosta B, Persichilli S, Mormile F, Minucci A, Russo A, Giardina B, De Sole P (2001) A fast chemiluminescent method for H₂O₂ measurement in exhaled breath condensate. Clin Chim Acta 310:187–191PubMed

Zhang Y, Seeburg DP, Pulli B, Wojtkiewicz GR, Bure L, Atkinson W, Schob S, Iwamoto Y, Ali M, Zhang W, Rodriguez E, Milewski A, Keliher EJ, Wang C, Pan Y, Swirski FK, Chen JW (2016) Myeloperoxidase nuclear imaging for epileptogenesis. Radiology 278:1–9

Titel: Activation of the phagocyte NADPH oxidase/NOX2 and myeloperoxidase in the mouse brain during pilocarpine-induced temporal lobe epilepsy and inhibition by ketamine
verfasst von: Fatma Tannich
Asma Tlili
Coralie Pintard
Amina Chniguir
Bruno Eto
Pham My-Chan Dang
Ouajdi Souilem
Jamel El-Benna
Publikationsdatum: 30.10.2019
Verlag: Springer International Publishing
Erschienen in: Inflammopharmacology / Ausgabe 2/2020
Print ISSN: 0925-4692
Elektronische ISSN: 1568-5608
DOI: https://doi.org/10.1007/s10787-019-00655-9

Live-Webinar "Chronische Unterbauch- und Viszeralschmerzen in der Praxis managen"

Springer Medizin

Activation of the phagocyte NADPH oxidase/NOX2 and myeloperoxidase in the mouse brain during pilocarpine-induced temporal lobe epilepsy and inhibition by ketamine

Abstract

Live-Webinar "Chronische Unterbauch- und Viszeralschmerzen in der Praxis managen"

Springer Medizin

Abstract

Bitte loggen Sie sich ein, um Zugang zu diesem Inhalt zu erhalten

Weitere Artikel der Ausgabe 2/2020

The inflammatory effect of epigenetic factors and modifications in type 2 diabetes

Combinatorial therapeutic effect of resveratrol and piperine on murine model of systemic lupus erythematosus

Pitfalls in meta-analysis

Brachychiton populneus as a novel source of bioactive ingredients with therapeutic effects: antioxidant, enzyme inhibitory, anti-inflammatory properties and LC–ESI-MS profile

Chromium picolinate attenuates cognitive deficit in ICV-STZ rat paradigm of sporadic Alzheimer’s-like dementia via targeting neuroinflammatory and IRS-1/PI3K/AKT/GSK-3β pathway

Analysis of lncRNA expression profiles by sequencing reveals that lnc-AL928768.3 and lnc-AC091493.1 are novel biomarkers for disease risk and activity of rheumatoid arthritis