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

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A Correction to this article was published on 04 January 2021

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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/gp91phox, p22phox, and p47phox) 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 p47phox 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.

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  • 04 January 2021

    Actually, the same mice brain extracts were used in both figures, and we thought it was more accurate to check whether in the same mice brain extracts used.

References

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

    CAS  PubMed  Google Scholar 

  • 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:e12951

    PubMed  Google Scholar 

  • 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 46:121–128

    CAS  PubMed  Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

  • 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 116:5795–5802

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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:e580

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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 32:778–782

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 21:663–688

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 51:55–64

    PubMed  Google Scholar 

  • 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 49:842–852

    PubMed  Google Scholar 

  • 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 118:1123–1132

    CAS  PubMed  Google Scholar 

  • 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 259:195–209

    CAS  PubMed  Google Scholar 

  • 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 41:217–225

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 273:180–193

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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:e0141221

    PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

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

    PubMed  Google Scholar 

  • 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 31:17370–17382

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 20:307–319

    CAS  PubMed  Google Scholar 

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

    PubMed Central  Google Scholar 

  • 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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • 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 1499:163–172

    CAS  PubMed  Google Scholar 

  • 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 23:8471–8479

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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 1115:162–168

    CAS  PubMed  Google Scholar 

  • 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 2017:2652560

    PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • 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 134:48–56

    CAS  PubMed  Google Scholar 

  • 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 1474:110–117

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • 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 48:1934–1946

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • 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 140:2210–2225

    PubMed  Google Scholar 

  • 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 8:481–492

    PubMed  Google Scholar 

  • 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 86:159–165

    CAS  PubMed  Google Scholar 

  • 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 92:123–131

    CAS  PubMed  Google Scholar 

  • 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 484:187–191

    CAS  PubMed  Google Scholar 

  • 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 26:623–633

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

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

    Google Scholar 

  • 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 27:444–450

    CAS  PubMed  Google Scholar 

  • 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 29:142–160

    CAS  PubMed  Google Scholar 

  • 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 221:166–171

    PubMed  Google Scholar 

  • 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 107:63–75

    CAS  PubMed  Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

  • 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 24:263–272

    CAS  PubMed  Google Scholar 

  • 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 80:424–431

    CAS  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • 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 111:1051–1058

    CAS  PubMed  Google Scholar 

  • 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 321:237–253

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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 64:1350–1362

    PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 120:241–248

    PubMed  PubMed Central  Google Scholar 

  • 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

    Google Scholar 

  • 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 90:206–212

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 310:187–191

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

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Acknowledgements

This work was supported by INSERM, CNRS, and Université Paris-Diderot.

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  1. Ouajdi Souilem and Jamel El-Benna have contributed equally to this work.

Authors and Affiliations

  1. Laboratory of Physiology and Pharmacology, National School of Veterinary Medicine, University of Manouba, Sidi Thabet, Tunisia

    Fatma Tannich & Ouajdi Souilem

  2. Neurophysiology Laboratory and Functional Pathology, Department of Biological Sciences, Faculty of Sciences of Tunis, University Campus of Al-Manar, Tunis, Tunisia

    Fatma Tannich

  3. INSERM U1149, ERL 8252 CNRS, Centre de Recherche sur l’Inflammation, Université Paris Diderot, Sorbonne Paris Cité, Laboratoire d’Excellence Inflamex, Faculté de Médecine, Site Xavier Bichat, 16 rue Henri Huchard, 75018, Paris, France

    Fatma Tannich, Asma Tlili, Coralie Pintard, Amina Chniguir, Pham My-Chan Dang & Jamel El-Benna

  4. Laboratoires TBC, Faculty of Pharmaceutical and Biological Sciences, 59006, Lille, France

    Bruno Eto

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Tannich, F., Tlili, A., Pintard, C. et al. Activation of the phagocyte NADPH oxidase/NOX2 and myeloperoxidase in the mouse brain during pilocarpine-induced temporal lobe epilepsy and inhibition by ketamine. Inflammopharmacol 28, 487–497 (2020). https://doi.org/10.1007/s10787-019-00655-9

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