Skip to main content
Top
Published in: Journal of Neuroinflammation 1/2018

Open Access 01-12-2018 | Research

Inflammatory and cytotoxic effects of bifenthrin in primary microglia and organotypic hippocampal slice cultures

Authors: Brahim Gargouri, Nizar M. Yousif, Michèle Bouchard, Hamadi Fetoui, Bernd L. Fiebich

Published in: Journal of Neuroinflammation | Issue 1/2018

Login to get access

Abstract

Background

Pyrethroids, such as bifenthrin (BF), are among the most widely used class of insecticides that pose serious risks to human and wildlife health. Pyrethroids are proposed to affect astrocytic functions and to cause neuron injury in the central nervous system (CNS). Microglia are key cells involved in innate immune responses in the CNS, and microglia activation has been linked to inflammation and neurotoxicity. However, little information is known about the effects of BF-induced toxicity in primary microglial cells as well as in organotypic hippocampal slice cultures (OHSCs).

Methods

Oxidative stress and inflammatory responses induced by BF were evaluated in primary microglial cells and OHSCs incubated with different concentrations of BF (1–20 μM) for 4 and 24 h. mRNA and protein synthesis of cyclooxygenase-2 (COX-2), tumor necrosis factor-alpha (TNF-alpha), interleukin-6 (IL-6), nuclear erythroid-2 like factor-2 (Nrf-2), and microsomal prostaglandin synthase-1 (mPGES-1) was also studied by qPCR and Western blot. Cell viability was analyzed by MTT-tetrazolio (MTT) and lactate dehydrogenase (LDH) assays. Neurotoxicity in OHSCs was analyzed by propidium iodide (PI) staining and confocal microscopy.

Results

Exposure of microglial cells to BF for 24 h resulted in a dose-dependent reduction in the number of viable cells. At sub-cytotoxic concentrations, BF increased reactive oxygen species (ROS), TNF-alpha synthesis, and prostaglandin E2 (PGE2) production, at both 4- and 24-h time points, respectively. Furthermore, BF incubation decreased superoxide dismutase (SOD), catalase (CAT), and glutathione peroxidase (GPx) activities and increased lipid peroxidation, protein oxidation, and H2O2 formation. In addition, BF significantly induced protein synthesis and mRNA expression of oxidative and inflammatory mediators after 4 and 24 h, including Nrf-2, COX-2, mPGES-1, and nuclear factor kappaB (NF-kappaB). A 24-h exposure of OHSCs to BF also increased neuronal death compared to untreated controls. Furthermore, depletion of microglia from OHSCs potently enhanced neuronal death induced by BF.

Conclusions

Overall, BF exhibited cytotoxic effects in primary microglial cells, accompanied by the induction of various inflammatory and oxidative stress markers including the Nrf-2/COX-2/mPGES-1/NF-kappaB pathways. Moreover, the study provided evidence that BF induced neuronal death in OHSCs and suggests that microglia exert a protective function against BF toxicity.
Appendix
Available only for authorised users
Literature
1.
go back to reference Thompson LA, Darwish WS, Ikenaka Y, Nakayama SMM, Mizukawa H, Ishizuka M. Organochlorine pesticide contamination of foods in Africa: incidence and public health significance. J Vet Med Sci. 2017;79:751–64.PubMedPubMedCentralCrossRef Thompson LA, Darwish WS, Ikenaka Y, Nakayama SMM, Mizukawa H, Ishizuka M. Organochlorine pesticide contamination of foods in Africa: incidence and public health significance. J Vet Med Sci. 2017;79:751–64.PubMedPubMedCentralCrossRef
2.
go back to reference Kale M, Rathore N, John S, Bhatnagar D. Lipid peroxidative damage on pyrethroid exposure and alterations in antioxidant status in rat erythrocytes: a possible involvement of reactive oxygen species. Toxicol Lett. 1999;105:197–205.PubMedCrossRef Kale M, Rathore N, John S, Bhatnagar D. Lipid peroxidative damage on pyrethroid exposure and alterations in antioxidant status in rat erythrocytes: a possible involvement of reactive oxygen species. Toxicol Lett. 1999;105:197–205.PubMedCrossRef
3.
go back to reference Fetoui H, Garoui EM, Makni-ayadi F, Zeghal N. Oxidative stress induced by lambda-cyhalothrin (LTC) in rat erythrocytes and brain: attenuation by vitamin C. Environ Toxicol Pharmacol. 2008;26:225–31.PubMedCrossRef Fetoui H, Garoui EM, Makni-ayadi F, Zeghal N. Oxidative stress induced by lambda-cyhalothrin (LTC) in rat erythrocytes and brain: attenuation by vitamin C. Environ Toxicol Pharmacol. 2008;26:225–31.PubMedCrossRef
4.
go back to reference Deziel NC, Friesen MC, Hoppin JA, Hines CJ, Thomas K, Freeman LEB. A review of nonoccupational pathways for pesticide exposure in women living in agricultural areas. Environ Health Perspect. 2015;123:515–24.PubMedPubMedCentralCrossRef Deziel NC, Friesen MC, Hoppin JA, Hines CJ, Thomas K, Freeman LEB. A review of nonoccupational pathways for pesticide exposure in women living in agricultural areas. Environ Health Perspect. 2015;123:515–24.PubMedPubMedCentralCrossRef
5.
go back to reference Narayan S, Sinsheimer JS, Paul KC, Liew Z, Cockburn M, Bronstein JM, et al. Genetic variability in ABCB1, occupational pesticide exposure, and Parkinson’s disease. Environ Res. 2015;143:98–106.PubMedPubMedCentralCrossRef Narayan S, Sinsheimer JS, Paul KC, Liew Z, Cockburn M, Bronstein JM, et al. Genetic variability in ABCB1, occupational pesticide exposure, and Parkinson’s disease. Environ Res. 2015;143:98–106.PubMedPubMedCentralCrossRef
6.
go back to reference Aldridge WN, Dinsdale D, Nemery B, Verschoyle RD. Some aspects of the toxicology of trimethyl and triethyl phosphorothioates. Fundam Appl Toxicol Off J Soc Toxicology 1985;5:S47–S60. Aldridge WN, Dinsdale D, Nemery B, Verschoyle RD. Some aspects of the toxicology of trimethyl and triethyl phosphorothioates. Fundam Appl Toxicol Off J Soc Toxicology 1985;5:S47–S60.
7.
go back to reference Lawrence LJ, Casida JE. Pyrethroid toxicology: mouse intracerebral structure-toxicity relationships. Pestic Biochem Physiol. 1982;18:9–14.CrossRef Lawrence LJ, Casida JE. Pyrethroid toxicology: mouse intracerebral structure-toxicity relationships. Pestic Biochem Physiol. 1982;18:9–14.CrossRef
8.
go back to reference Soderlund DM, Clark JM, Sheets LP, Mullin LS, Piccirillo VJ, Sargent D, et al. Mechanisms of pyrethroid neurotoxicity: implications for cumulative risk assessment. Toxicology. 2002;171:3–59.PubMedCrossRef Soderlund DM, Clark JM, Sheets LP, Mullin LS, Piccirillo VJ, Sargent D, et al. Mechanisms of pyrethroid neurotoxicity: implications for cumulative risk assessment. Toxicology. 2002;171:3–59.PubMedCrossRef
9.
go back to reference Scollon EJ, Starr JM, Crofton KM, Wolansky MJ, DeVito MJ, Hughes MF. Correlation of tissue concentrations of the pyrethroid bifenthrin with neurotoxicity in the rat. Toxicology. 2011;290:1–6.PubMedPubMedCentralCrossRef Scollon EJ, Starr JM, Crofton KM, Wolansky MJ, DeVito MJ, Hughes MF. Correlation of tissue concentrations of the pyrethroid bifenthrin with neurotoxicity in the rat. Toxicology. 2011;290:1–6.PubMedPubMedCentralCrossRef
10.
go back to reference Shafer TJ, Meyer DA, Crofton KM. Developmental neurotoxicity of pyrethroid insecticides: critical review and future research needs. Environ Health Perspect. 2005;113:123–36.PubMedCrossRef Shafer TJ, Meyer DA, Crofton KM. Developmental neurotoxicity of pyrethroid insecticides: critical review and future research needs. Environ Health Perspect. 2005;113:123–36.PubMedCrossRef
11.
go back to reference Wolansky MJ, Harrill JA. Neurobehavioral toxicology of pyrethroid insecticides in adult animals: a critical review. Neurotoxicol Teratol. 2008;30:55–78.PubMedCrossRef Wolansky MJ, Harrill JA. Neurobehavioral toxicology of pyrethroid insecticides in adult animals: a critical review. Neurotoxicol Teratol. 2008;30:55–78.PubMedCrossRef
12.
go back to reference Fetoui H, Feki A, Salah GB, Kamoun H, Fakhfakh F, Gdoura R. Exposure to lambda-cyhalothrin, a synthetic pyrethroid, increases reactive oxygen species production and induces genotoxicity in rat peripheral blood. Toxicol Ind Health. 2015;31:433–41.PubMedCrossRef Fetoui H, Feki A, Salah GB, Kamoun H, Fakhfakh F, Gdoura R. Exposure to lambda-cyhalothrin, a synthetic pyrethroid, increases reactive oxygen species production and induces genotoxicity in rat peripheral blood. Toxicol Ind Health. 2015;31:433–41.PubMedCrossRef
13.
go back to reference Aouey B, Derbali M, Chtourou Y, Bouchard M, Khabir A, Fetoui H. Pyrethroid insecticide lambda-cyhalothrin and its metabolites induce liver injury through the activation of oxidative stress and proinflammatory gene expression in rats following acute and subchronic exposure. Environ Sci Pollut Res Int. 2017;24:5841–56.PubMedCrossRef Aouey B, Derbali M, Chtourou Y, Bouchard M, Khabir A, Fetoui H. Pyrethroid insecticide lambda-cyhalothrin and its metabolites induce liver injury through the activation of oxidative stress and proinflammatory gene expression in rats following acute and subchronic exposure. Environ Sci Pollut Res Int. 2017;24:5841–56.PubMedCrossRef
14.
go back to reference Singh AK, Tiwari MN, Prakash O, Singh MP. A current review of Cypermethrin-induced neurotoxicity and nigrostriatal dopaminergic neurodegeneration. Curr Neuropharmacol. 2012;10:64–71.PubMedPubMedCentralCrossRef Singh AK, Tiwari MN, Prakash O, Singh MP. A current review of Cypermethrin-induced neurotoxicity and nigrostriatal dopaminergic neurodegeneration. Curr Neuropharmacol. 2012;10:64–71.PubMedPubMedCentralCrossRef
15.
go back to reference Narahashi T, Ginsburg KS, Nagata K, Song JH, Tatebayashi H. Ion channels as targets for insecticides. Neurotoxicology. 1998;19:581–90.PubMed Narahashi T, Ginsburg KS, Nagata K, Song JH, Tatebayashi H. Ion channels as targets for insecticides. Neurotoxicology. 1998;19:581–90.PubMed
16.
go back to reference Bradberry SM, Thanacoody HKR, Watt BE, Thomas SHL, Vale JA. Management of the cardiovascular complications of tricyclic antidepressant poisoning: role of sodium bicarbonate. Toxicol Rev. 2005;24:195–204.PubMedCrossRef Bradberry SM, Thanacoody HKR, Watt BE, Thomas SHL, Vale JA. Management of the cardiovascular complications of tricyclic antidepressant poisoning: role of sodium bicarbonate. Toxicol Rev. 2005;24:195–204.PubMedCrossRef
17.
go back to reference Breckenridge CB, Holden L, Sturgess N, Weiner M, Sheets L, Sargent D, et al. Evidence for a separate mechanism of toxicity for the type I and the type II pyrethroid insecticides. Neurotoxicology. 2009;30(1):S17–31.PubMedCrossRef Breckenridge CB, Holden L, Sturgess N, Weiner M, Sheets L, Sargent D, et al. Evidence for a separate mechanism of toxicity for the type I and the type II pyrethroid insecticides. Neurotoxicology. 2009;30(1):S17–31.PubMedCrossRef
19.
go back to reference Zhao M, Lewis Wang FS, Hu X, Chen F, Chan HM. Acrylamide-induced neurotoxicity in primary astrocytes and microglia: roles of the Nrf2-ARE and NF-κB pathways. Food Chem Toxicol Int J Publ Br Ind Biol Res Assoc. 2017;106:25–35.CrossRef Zhao M, Lewis Wang FS, Hu X, Chen F, Chan HM. Acrylamide-induced neurotoxicity in primary astrocytes and microglia: roles of the Nrf2-ARE and NF-κB pathways. Food Chem Toxicol Int J Publ Br Ind Biol Res Assoc. 2017;106:25–35.CrossRef
20.
go back to reference Li H, Wu S, Ma Q, Shi N. The pesticide deltamethrin increases free radical production and promotes nuclear translocation of the stress response transcription factor Nrf2 in rat brain. Toxicol Ind Health. 2011;27:579–90.PubMedPubMedCentralCrossRef Li H, Wu S, Ma Q, Shi N. The pesticide deltamethrin increases free radical production and promotes nuclear translocation of the stress response transcription factor Nrf2 in rat brain. Toxicol Ind Health. 2011;27:579–90.PubMedPubMedCentralCrossRef
21.
go back to reference Baltazar MT, Dinis-Oliveira RJ, de Lourdes Bastos M, Tsatsakis AM, Duarte JA, Carvalho F. Pesticides exposure as etiological factors of Parkinson’s disease and other neurodegenerative diseases—a mechanistic approach. Toxicol Lett. 2014;230:85–103.PubMedCrossRef Baltazar MT, Dinis-Oliveira RJ, de Lourdes Bastos M, Tsatsakis AM, Duarte JA, Carvalho F. Pesticides exposure as etiological factors of Parkinson’s disease and other neurodegenerative diseases—a mechanistic approach. Toxicol Lett. 2014;230:85–103.PubMedCrossRef
22.
go back to reference Singh AK, Tiwari MN, Upadhyay G, Patel DK, Singh D, Prakash O, et al. Long term exposure to cypermethrin induces nigrostriatal dopaminergic neurodegeneration in adult rats: postnatal exposure enhances the susceptibility during adulthood. Neurobiol Aging. 2012;33:404–15.PubMedCrossRef Singh AK, Tiwari MN, Upadhyay G, Patel DK, Singh D, Prakash O, et al. Long term exposure to cypermethrin induces nigrostriatal dopaminergic neurodegeneration in adult rats: postnatal exposure enhances the susceptibility during adulthood. Neurobiol Aging. 2012;33:404–15.PubMedCrossRef
23.
go back to reference Hossain MM, Richardson JR. Mechanism of pyrethroid pesticide–induced apoptosis: role of Calpain and the ER stress pathway. Toxicol Sci. 2011;122:512–25.PubMedPubMedCentralCrossRef Hossain MM, Richardson JR. Mechanism of pyrethroid pesticide–induced apoptosis: role of Calpain and the ER stress pathway. Toxicol Sci. 2011;122:512–25.PubMedPubMedCentralCrossRef
24.
go back to reference Ponomarev ED, Veremeyko T, Weiner HL. MicroRNAs are universal regulators of differentiation, activation and polarization of microglia and macrophages in normal and diseased CNS. Glia. 2013;61:91–103.PubMedCrossRef Ponomarev ED, Veremeyko T, Weiner HL. MicroRNAs are universal regulators of differentiation, activation and polarization of microglia and macrophages in normal and diseased CNS. Glia. 2013;61:91–103.PubMedCrossRef
25.
go back to reference Koziorowski D, Tomasiuk R, Szlufik S, Friedman A. Inflammatory cytokines and NT-proCNP in Parkinson’s disease patients. Cytokine. 2012;60:762–6.PubMedCrossRef Koziorowski D, Tomasiuk R, Szlufik S, Friedman A. Inflammatory cytokines and NT-proCNP in Parkinson’s disease patients. Cytokine. 2012;60:762–6.PubMedCrossRef
26.
go back to reference Morales R, Estrada LD, Diaz-Espinoza R, Morales-Scheihing D, Jara MC, Castilla J, et al. Molecular cross talk between misfolded proteins in animal models of Alzheimer’s and prion diseases. J Neurosci. 2010;30:4528–35.PubMedPubMedCentralCrossRef Morales R, Estrada LD, Diaz-Espinoza R, Morales-Scheihing D, Jara MC, Castilla J, et al. Molecular cross talk between misfolded proteins in animal models of Alzheimer’s and prion diseases. J Neurosci. 2010;30:4528–35.PubMedPubMedCentralCrossRef
27.
go back to reference Rubio-Perez JM, Morillas-Ruiz JM. A review: inflammatory process in Alzheimer’s disease, role of cytokines. ScientificWorldJournal. 2012;2012:756357.PubMedPubMedCentralCrossRef Rubio-Perez JM, Morillas-Ruiz JM. A review: inflammatory process in Alzheimer’s disease, role of cytokines. ScientificWorldJournal. 2012;2012:756357.PubMedPubMedCentralCrossRef
28.
go back to reference Venegas C, Kumar S, Franklin BS, Dierkes T, Brinkschulte R, Tejera D, et al. Microglia-derived ASC specks cross-seed amyloid-β in Alzheimer’s disease. Nature. 2017;552:355–61.PubMedCrossRef Venegas C, Kumar S, Franklin BS, Dierkes T, Brinkschulte R, Tejera D, et al. Microglia-derived ASC specks cross-seed amyloid-β in Alzheimer’s disease. Nature. 2017;552:355–61.PubMedCrossRef
29.
go back to reference Spangenberg EE, Green KN. Inflammation in Alzheimer’s disease: lessons learned from microglia-depletion models. Brain Behav Immun. 2017;61:1–11.PubMedCrossRef Spangenberg EE, Green KN. Inflammation in Alzheimer’s disease: lessons learned from microglia-depletion models. Brain Behav Immun. 2017;61:1–11.PubMedCrossRef
30.
go back to reference di Penta A, Moreno B, Reix S, Fernandez-Diez B, Villanueva M, Errea O, et al. Oxidative stress and proinflammatory cytokines contribute to demyelination and axonal damage in a cerebellar culture model of neuroinflammation. PLoS One. 2013;8:e54722.PubMedPubMedCentralCrossRef di Penta A, Moreno B, Reix S, Fernandez-Diez B, Villanueva M, Errea O, et al. Oxidative stress and proinflammatory cytokines contribute to demyelination and axonal damage in a cerebellar culture model of neuroinflammation. PLoS One. 2013;8:e54722.PubMedPubMedCentralCrossRef
31.
go back to reference Vinet J, Weering HRJ, van Heinrich A, Kälin RE, Wegner A, Brouwer N, et al. Neuroprotective function for ramified microglia in hippocampal excitotoxicity. J Neuroinflammation. 2012;9:27.PubMedPubMedCentralCrossRef Vinet J, Weering HRJ, van Heinrich A, Kälin RE, Wegner A, Brouwer N, et al. Neuroprotective function for ramified microglia in hippocampal excitotoxicity. J Neuroinflammation. 2012;9:27.PubMedPubMedCentralCrossRef
33.
go back to reference Mou YH, Yang JY, Cui N, Wang JM, Hou Y, Song S, et al. Effects of cobalt chloride on nitric oxide and cytokines/chemokines production in microglia. Int Immunopharmacol. 2012;13:120–5.PubMedCrossRef Mou YH, Yang JY, Cui N, Wang JM, Hou Y, Song S, et al. Effects of cobalt chloride on nitric oxide and cytokines/chemokines production in microglia. Int Immunopharmacol. 2012;13:120–5.PubMedCrossRef
34.
go back to reference Lehnardt S. Innate immunity and neuroinflammation in the CNS: the role of microglia in Toll-like receptor-mediated neuronal injury. Glia. 2010;58:253–63.PubMed Lehnardt S. Innate immunity and neuroinflammation in the CNS: the role of microglia in Toll-like receptor-mediated neuronal injury. Glia. 2010;58:253–63.PubMed
35.
go back to reference Rosenberger K, Derkow K, Dembny P, Krüger C, Schott E, Lehnardt S. The impact of single and pairwise Toll-like receptor activation on neuroinflammation and neurodegeneration. J Neuroinflammation. 2014;11:166.PubMedPubMedCentralCrossRef Rosenberger K, Derkow K, Dembny P, Krüger C, Schott E, Lehnardt S. The impact of single and pairwise Toll-like receptor activation on neuroinflammation and neurodegeneration. J Neuroinflammation. 2014;11:166.PubMedPubMedCentralCrossRef
36.
go back to reference Jazwa A, Cuadrado A. Targeting heme oxygenase-1 for neuroprotection and neuroinflammation in neurodegenerative diseases. Curr Drug Targets. 2010;11:1517–31.PubMedCrossRef Jazwa A, Cuadrado A. Targeting heme oxygenase-1 for neuroprotection and neuroinflammation in neurodegenerative diseases. Curr Drug Targets. 2010;11:1517–31.PubMedCrossRef
37.
go back to reference Innamorato NG, Jazwa A, Rojo AI, García C, Fernández-Ruiz J, Grochot-Przeczek A, et al. Different susceptibility to the Parkinson’s toxin MPTP in mice lacking the redox master regulator Nrf2 or its target gene heme oxygenase-1. PLoS One. 2010;5:e11838.PubMedPubMedCentralCrossRef Innamorato NG, Jazwa A, Rojo AI, García C, Fernández-Ruiz J, Grochot-Przeczek A, et al. Different susceptibility to the Parkinson’s toxin MPTP in mice lacking the redox master regulator Nrf2 or its target gene heme oxygenase-1. PLoS One. 2010;5:e11838.PubMedPubMedCentralCrossRef
38.
go back to reference Yoh K, Hirayama A, Ishizaki K, Yamada A, Takeuchi M, Yamagishi S, et al. Hyperglycemia induces oxidative and nitrosative stress and increases renal functional impairment in Nrf2-deficient mice. Genes Cells Devoted Mol Cell Mech. 2008;13:1159–70. Yoh K, Hirayama A, Ishizaki K, Yamada A, Takeuchi M, Yamagishi S, et al. Hyperglycemia induces oxidative and nitrosative stress and increases renal functional impairment in Nrf2-deficient mice. Genes Cells Devoted Mol Cell Mech. 2008;13:1159–70.
39.
go back to reference Thimmulappa RK, Scollick C, Traore K, Yates M, Trush MA, Liby KT, et al. Nrf2-dependent protection from LPS induced inflammatory response and mortality by CDDO-Imidazolide. Biochem Biophys Res Commun. 2006;351:883–9.PubMedPubMedCentralCrossRef Thimmulappa RK, Scollick C, Traore K, Yates M, Trush MA, Liby KT, et al. Nrf2-dependent protection from LPS induced inflammatory response and mortality by CDDO-Imidazolide. Biochem Biophys Res Commun. 2006;351:883–9.PubMedPubMedCentralCrossRef
40.
go back to reference Ross G, Hübschle T, Pehl U, Braun H-A, Voigt K, Gerstberger R, et al. Fever induction by localized subcutaneous inflammation in guinea pigs: the role of cytokines and prostaglandins. J Appl Physiol Bethesda Md 1985. 2003;94:1395–402. Ross G, Hübschle T, Pehl U, Braun H-A, Voigt K, Gerstberger R, et al. Fever induction by localized subcutaneous inflammation in guinea pigs: the role of cytokines and prostaglandins. J Appl Physiol Bethesda Md 1985. 2003;94:1395–402.
41.
go back to reference Mancino A, Lawrence T. Nuclear factor-kappaB and tumor-associated macrophages. Clin Cancer Res Off J Am Assoc Cancer Res 2010;16:784–789. Mancino A, Lawrence T. Nuclear factor-kappaB and tumor-associated macrophages. Clin Cancer Res Off J Am Assoc Cancer Res 2010;16:784–789.
42.
go back to reference Romero A, Ares I, Ramos E, Castellano V, Martínez M, Martínez-Larrañaga MR, et al. Evidence for dose-additive effects of a type II pyrethroid mixture. In vitro assessment. Environ Res. 2015;138:58–66.PubMedCrossRef Romero A, Ares I, Ramos E, Castellano V, Martínez M, Martínez-Larrañaga MR, et al. Evidence for dose-additive effects of a type II pyrethroid mixture. In vitro assessment. Environ Res. 2015;138:58–66.PubMedCrossRef
44.
go back to reference Yousif NM, de Oliveira ACP, Brioschi S, Huell M, Biber K, Fiebich BL. Activation of EP 2 receptor suppresses poly(I: C) and LPS-mediated inflammation in primary microglia and organotypic hippocampal slice cultures: contributing role for MAPKs. Glia [Internet]. 2017 [cited 2018 Jan 14]; Available from: http://doi.wiley.com/10.1002/glia.23276 Yousif NM, de Oliveira ACP, Brioschi S, Huell M, Biber K, Fiebich BL. Activation of EP 2 receptor suppresses poly(I: C) and LPS-mediated inflammation in primary microglia and organotypic hippocampal slice cultures: contributing role for MAPKs. Glia [Internet]. 2017 [cited 2018 Jan 14]; Available from: http://​doi.​wiley.​com/​10.​1002/​glia.​23276
45.
go back to reference Denizot F, Lang R. Rapid colorimetric assay for cell growth and survival. Modifications to the tetrazolium dye procedure giving improved sensitivity and reliability. J Immunol Methods. 1986;89:271–7.PubMedCrossRef Denizot F, Lang R. Rapid colorimetric assay for cell growth and survival. Modifications to the tetrazolium dye procedure giving improved sensitivity and reliability. J Immunol Methods. 1986;89:271–7.PubMedCrossRef
46.
go back to reference Green LC, Wagner DA, Glogowski J, Skipper PL, Wishnok JS, Tannenbaum SR. Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids. Anal Biochem. 1982;126:131–8.PubMedCrossRef Green LC, Wagner DA, Glogowski J, Skipper PL, Wishnok JS, Tannenbaum SR. Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids. Anal Biochem. 1982;126:131–8.PubMedCrossRef
47.
go back to reference Ou P, Wolff SP. A discontinuous method for catalase determination at “near physiological” concentrations of H2O2 and its application to the study of H2O2 fluxes within cells. J Biochem Biophys Methods. 1996;31:59–67.PubMedCrossRef Ou P, Wolff SP. A discontinuous method for catalase determination at “near physiological” concentrations of H2O2 and its application to the study of H2O2 fluxes within cells. J Biochem Biophys Methods. 1996;31:59–67.PubMedCrossRef
48.
go back to reference Draper HH, Hadley M. Malondialdehyde determination as index of lipid peroxidation. Methods Enzymol. 1990;186:421–31.PubMedCrossRef Draper HH, Hadley M. Malondialdehyde determination as index of lipid peroxidation. Methods Enzymol. 1990;186:421–31.PubMedCrossRef
50.
go back to reference Marklund S, Marklund G. Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem. 1974;47:469–74.PubMedCrossRef Marklund S, Marklund G. Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem. 1974;47:469–74.PubMedCrossRef
51.
52.
go back to reference Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods San Diego Calif. 2001;25:402–8.CrossRef Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods San Diego Calif. 2001;25:402–8.CrossRef
53.
go back to reference Stoppini L, Buchs PA, Muller D. A simple method for organotypic cultures of nervous tissue. J Neurosci Methods. 1991;37:173–82.PubMedCrossRef Stoppini L, Buchs PA, Muller D. A simple method for organotypic cultures of nervous tissue. J Neurosci Methods. 1991;37:173–82.PubMedCrossRef
54.
go back to reference Masuch A, Shieh C-H, van Rooijen N, van Calker D, Biber K. Mechanism of microglia neuroprotection: involvement of P2X7, TNFα, and valproic acid. Glia. 2016;64:76–89.PubMedCrossRef Masuch A, Shieh C-H, van Rooijen N, van Calker D, Biber K. Mechanism of microglia neuroprotection: involvement of P2X7, TNFα, and valproic acid. Glia. 2016;64:76–89.PubMedCrossRef
55.
go back to reference Shieh C-H, Heinrich A, Serchov T, van Calker D, Biber K. P2X7-dependent, but differentially regulated release of IL-6, CCL2, and TNF-α in cultured mouse microglia. Glia. 2014;62:592–607.PubMedCrossRef Shieh C-H, Heinrich A, Serchov T, van Calker D, Biber K. P2X7-dependent, but differentially regulated release of IL-6, CCL2, and TNF-α in cultured mouse microglia. Glia. 2014;62:592–607.PubMedCrossRef
56.
57.
go back to reference Eaton DL, Daroff RB, Autrup H, Bridges J, Buffler P, Costa LG, et al. Review of the toxicology of chlorpyrifos with an emphasis on human exposure and neurodevelopment. Crit Rev Toxicol. 2008;38(2):1–125.PubMedCrossRef Eaton DL, Daroff RB, Autrup H, Bridges J, Buffler P, Costa LG, et al. Review of the toxicology of chlorpyrifos with an emphasis on human exposure and neurodevelopment. Crit Rev Toxicol. 2008;38(2):1–125.PubMedCrossRef
59.
go back to reference Lahouel A, Kebieche M, Lakroun Z, Rouabhi R, Fetoui H, Chtourou Y, et al. Neurobehavioral deficits and brain oxidative stress induced by chronic low dose exposure of persistent organic pollutants mixture in adult female rat. Environ Sci Pollut Res Int. 2016;23:19030–40.PubMedCrossRef Lahouel A, Kebieche M, Lakroun Z, Rouabhi R, Fetoui H, Chtourou Y, et al. Neurobehavioral deficits and brain oxidative stress induced by chronic low dose exposure of persistent organic pollutants mixture in adult female rat. Environ Sci Pollut Res Int. 2016;23:19030–40.PubMedCrossRef
60.
go back to reference Paul KC, Sinsheimer JS, Rhodes SL, Cockburn M, Bronstein J, Ritz B. Organophosphate pesticide exposures, nitric oxide synthase gene variants, and gene–pesticide interactions in a case–control study of Parkinson’s disease, California. Environ Health Perspect [Internet]. 2015 [cited 2018 14];124. Available from: http://ehp.niehs.nih.gov/1408976 Paul KC, Sinsheimer JS, Rhodes SL, Cockburn M, Bronstein J, Ritz B. Organophosphate pesticide exposures, nitric oxide synthase gene variants, and gene–pesticide interactions in a case–control study of Parkinson’s disease, California. Environ Health Perspect [Internet]. 2015 [cited 2018 14];124. Available from: http://​ehp.​niehs.​nih.​gov/​1408976
61.
go back to reference Hossain MM, Liu J, Richardson JR. Pyrethroid insecticides directly activate microglia through interaction with voltage-gated sodium channels. Toxicol Sci. 2017;155:112–23.PubMedCrossRef Hossain MM, Liu J, Richardson JR. Pyrethroid insecticides directly activate microglia through interaction with voltage-gated sodium channels. Toxicol Sci. 2017;155:112–23.PubMedCrossRef
62.
go back to reference Romero A, Ramos E, Castellano V, Martínez MA, Ares I, Martínez M, et al. Cytotoxicity induced by deltamethrin and its metabolites in SH-SY5Y cells can be differentially prevented by selected antioxidants. Toxicol Vitro Int J Publ Assoc BIBRA. 2012;26:823–30.CrossRef Romero A, Ramos E, Castellano V, Martínez MA, Ares I, Martínez M, et al. Cytotoxicity induced by deltamethrin and its metabolites in SH-SY5Y cells can be differentially prevented by selected antioxidants. Toxicol Vitro Int J Publ Assoc BIBRA. 2012;26:823–30.CrossRef
63.
go back to reference Heneka MT, Kummer MP, Latz E. Innate immune activation in neurodegenerative disease. Nat Rev Immunol. 2014;14:463–77.PubMedCrossRef Heneka MT, Kummer MP, Latz E. Innate immune activation in neurodegenerative disease. Nat Rev Immunol. 2014;14:463–77.PubMedCrossRef
64.
go back to reference Blank T, Prinz M. Type I interferon pathway in CNS homeostasis and neurological disorders. Glia. 2017;65:1397–406.PubMedCrossRef Blank T, Prinz M. Type I interferon pathway in CNS homeostasis and neurological disorders. Glia. 2017;65:1397–406.PubMedCrossRef
65.
go back to reference Rice RA, Pham J, Lee RJ, Najafi AR, West BL, Green KN. Microglial repopulation resolves inflammation and promotes brain recovery after injury. Glia. 2017;65:931–44.PubMedCrossRefPubMedCentral Rice RA, Pham J, Lee RJ, Najafi AR, West BL, Green KN. Microglial repopulation resolves inflammation and promotes brain recovery after injury. Glia. 2017;65:931–44.PubMedCrossRefPubMedCentral
66.
go back to reference Mumaw CL, Surace M, Levesque S, Kodavanti UP, Kodavanti PRS, Royland JE, et al. Atypical microglial response to biodiesel exhaust in healthy and hypertensive rats. Neurotoxicology. 2017;59:155–63.PubMedCrossRef Mumaw CL, Surace M, Levesque S, Kodavanti UP, Kodavanti PRS, Royland JE, et al. Atypical microglial response to biodiesel exhaust in healthy and hypertensive rats. Neurotoxicology. 2017;59:155–63.PubMedCrossRef
67.
go back to reference Zhang W, Yan Z, Gao J, Sun L, Huang X, Liu Z, et al. Role and mechanism of microglial activation in iron-induced selective and progressive dopaminergic neurodegeneration. Mol Neurobiol. 2014;49:1153–65.PubMedCrossRef Zhang W, Yan Z, Gao J, Sun L, Huang X, Liu Z, et al. Role and mechanism of microglial activation in iron-induced selective and progressive dopaminergic neurodegeneration. Mol Neurobiol. 2014;49:1153–65.PubMedCrossRef
68.
go back to reference Taupin P. A dual activity of ROS and oxidative stress on adult neurogenesis and Alzheimer’s disease. Cent Nerv Syst Agents Med Chem. 2010;10:16–21.PubMedCrossRef Taupin P. A dual activity of ROS and oxidative stress on adult neurogenesis and Alzheimer’s disease. Cent Nerv Syst Agents Med Chem. 2010;10:16–21.PubMedCrossRef
70.
go back to reference Liu H, Xu L, Zhao M, Liu W, Zhang C, Zhou S. Enantiomer-specific, bifenthrin-induced apoptosis mediated by MAPK signalling pathway in Hep G2 cells. Toxicology. 2009;261:119–25.PubMedCrossRef Liu H, Xu L, Zhao M, Liu W, Zhang C, Zhou S. Enantiomer-specific, bifenthrin-induced apoptosis mediated by MAPK signalling pathway in Hep G2 cells. Toxicology. 2009;261:119–25.PubMedCrossRef
71.
go back to reference Nita M, Grzybowski A. The role of the reactive oxygen species and oxidative stress in the pathomechanism of the age-related ocular diseases and other pathologies of the anterior and posterior eye segments in adults. Oxidative Med Cell Longev. 2016;2016:3164734.CrossRef Nita M, Grzybowski A. The role of the reactive oxygen species and oxidative stress in the pathomechanism of the age-related ocular diseases and other pathologies of the anterior and posterior eye segments in adults. Oxidative Med Cell Longev. 2016;2016:3164734.CrossRef
72.
go back to reference Narra MR, Rajender K, Reddy RR, Murty US, Begum G. Insecticides induced stress response and recuperation in fish: biomarkers in blood and tissues related to oxidative damage. Chemosphere. 2017;168:350–7.PubMedCrossRef Narra MR, Rajender K, Reddy RR, Murty US, Begum G. Insecticides induced stress response and recuperation in fish: biomarkers in blood and tissues related to oxidative damage. Chemosphere. 2017;168:350–7.PubMedCrossRef
73.
go back to reference El-Demerdash FM. Lipid peroxidation, oxidative stress and acetylcholinesterase in rat brain exposed to organophosphate and pyrethroid insecticides. Food Chem Toxicol. 2011;49:1346–52.PubMedCrossRef El-Demerdash FM. Lipid peroxidation, oxidative stress and acetylcholinesterase in rat brain exposed to organophosphate and pyrethroid insecticides. Food Chem Toxicol. 2011;49:1346–52.PubMedCrossRef
74.
go back to reference Zhou H, Yuan Y, Qi Z, Tong Q, Zhang K. Study on changes of plasma levels of oxidative stress biomarkers and its relation with cognition function in patients with parkinson’s disease. Zhonghua Yi Xue Za Zhi. 2015;95:3357–60.PubMed Zhou H, Yuan Y, Qi Z, Tong Q, Zhang K. Study on changes of plasma levels of oxidative stress biomarkers and its relation with cognition function in patients with parkinson’s disease. Zhonghua Yi Xue Za Zhi. 2015;95:3357–60.PubMed
75.
go back to reference Hu F, Li L, Wang C, Zhang Q, Zhang X, Zhao M. Enantioselective induction of oxidative stress by permethrin in rat adrenal pheochromocytoma (PC12) cells. Environ Toxicol Chem. 2010;29:683–90.PubMedCrossRef Hu F, Li L, Wang C, Zhang Q, Zhang X, Zhao M. Enantioselective induction of oxidative stress by permethrin in rat adrenal pheochromocytoma (PC12) cells. Environ Toxicol Chem. 2010;29:683–90.PubMedCrossRef
76.
go back to reference Choi SH, Lee DY, Kim SU, Jin BK. Thrombin-induced oxidative stress contributes to the death of hippocampal neurons in vivo: role of microglial NADPH oxidase. J Neurosci. 2005;25:4082–90.PubMedCrossRef Choi SH, Lee DY, Kim SU, Jin BK. Thrombin-induced oxidative stress contributes to the death of hippocampal neurons in vivo: role of microglial NADPH oxidase. J Neurosci. 2005;25:4082–90.PubMedCrossRef
77.
go back to reference Kraft AD, Harry GJ. Features of microglia and neuroinflammation relevant to environmental exposure and neurotoxicity. Int J Environ Res Public Health. 2011;8:2980–3018.PubMedPubMedCentralCrossRef Kraft AD, Harry GJ. Features of microglia and neuroinflammation relevant to environmental exposure and neurotoxicity. Int J Environ Res Public Health. 2011;8:2980–3018.PubMedPubMedCentralCrossRef
78.
go back to reference Spielman LJ, Gibson DL, Klegeris A. Incretin hormones regulate microglia oxidative stress, survival and expression of trophic factors. Eur J Cell Biol. 2017;96:240–53.PubMedCrossRef Spielman LJ, Gibson DL, Klegeris A. Incretin hormones regulate microglia oxidative stress, survival and expression of trophic factors. Eur J Cell Biol. 2017;96:240–53.PubMedCrossRef
79.
go back to reference Buendia I, Michalska P, Navarro E, Gameiro I, Egea J, León R. Nrf2-ARE pathway: an emerging target against oxidative stress and neuroinflammation in neurodegenerative diseases. Pharmacol Ther. 2016;157:84–104.PubMedCrossRef Buendia I, Michalska P, Navarro E, Gameiro I, Egea J, León R. Nrf2-ARE pathway: an emerging target against oxidative stress and neuroinflammation in neurodegenerative diseases. Pharmacol Ther. 2016;157:84–104.PubMedCrossRef
80.
go back to reference Ahmed SMU, Luo L, Namani A, Wang XJ, Tang X. Nrf2 signaling pathway: pivotal roles in inflammation. Biochim Biophys Acta (BBA) - Mol Basis Dis. 1863;2017:585–97. Ahmed SMU, Luo L, Namani A, Wang XJ, Tang X. Nrf2 signaling pathway: pivotal roles in inflammation. Biochim Biophys Acta (BBA) - Mol Basis Dis. 1863;2017:585–97.
81.
go back to reference Li H, Wang P, Huang F, Jin J, Wu H, Zhang B, et al. Astragaloside IV protects blood-brain barrier integrity from LPS-induced disruption via activating Nrf2 antioxidant signaling pathway in mice. Toxicol Appl Pharmacol. 2018;340:58–66.PubMedCrossRef Li H, Wang P, Huang F, Jin J, Wu H, Zhang B, et al. Astragaloside IV protects blood-brain barrier integrity from LPS-induced disruption via activating Nrf2 antioxidant signaling pathway in mice. Toxicol Appl Pharmacol. 2018;340:58–66.PubMedCrossRef
82.
go back to reference Tebay LE, Robertson H, Durant ST, Vitale SR, Penning TM, Dinkova-Kostova AT, et al. Mechanisms of activation of the transcription factor Nrf2 by redox stressors, nutrient cues, and energy status and the pathways through which it attenuates degenerative disease. Free Radic Biol Med. 2015;88:108–46.PubMedPubMedCentralCrossRef Tebay LE, Robertson H, Durant ST, Vitale SR, Penning TM, Dinkova-Kostova AT, et al. Mechanisms of activation of the transcription factor Nrf2 by redox stressors, nutrient cues, and energy status and the pathways through which it attenuates degenerative disease. Free Radic Biol Med. 2015;88:108–46.PubMedPubMedCentralCrossRef
83.
go back to reference Shang Y, Zhou Q, Wang T, Jiang Y, Zhong Y, Qian G, et al. Airborne nitro-PAHs induce Nrf2/ARE defense system against oxidative stress and promote inflammatory process by activating PI3K/Akt pathway in A549 cells. Toxicol Vitro Int J Publ Assoc BIBRA. 2017;44:66–73.CrossRef Shang Y, Zhou Q, Wang T, Jiang Y, Zhong Y, Qian G, et al. Airborne nitro-PAHs induce Nrf2/ARE defense system against oxidative stress and promote inflammatory process by activating PI3K/Akt pathway in A549 cells. Toxicol Vitro Int J Publ Assoc BIBRA. 2017;44:66–73.CrossRef
84.
go back to reference Li HY, Wu S-Y, Shi N. Transcription factor Nrf2 activation by deltamethrin in PC12 cells: involvement of ROS. Toxicol Lett. 2007;171:87–98.PubMedCrossRef Li HY, Wu S-Y, Shi N. Transcription factor Nrf2 activation by deltamethrin in PC12 cells: involvement of ROS. Toxicol Lett. 2007;171:87–98.PubMedCrossRef
86.
go back to reference Attoff K, Kertika D, Lundqvist J, Oredsson S, Forsby A. Acrylamide affects proliferation and differentiation of the neural progenitor cell line C17.2 and the neuroblastoma cell line SH-SY5Y. Toxicol Vitro Int J Publ Assoc BIBRA. 2016;35:100–11.CrossRef Attoff K, Kertika D, Lundqvist J, Oredsson S, Forsby A. Acrylamide affects proliferation and differentiation of the neural progenitor cell line C17.2 and the neuroblastoma cell line SH-SY5Y. Toxicol Vitro Int J Publ Assoc BIBRA. 2016;35:100–11.CrossRef
87.
go back to reference Dansokho C, Heneka MT. Neuroinflammatory responses in Alzheimer’s disease. J Neural Transm Vienna Austria 1996. 2018;125:771–9. Dansokho C, Heneka MT. Neuroinflammatory responses in Alzheimer’s disease. J Neural Transm Vienna Austria 1996. 2018;125:771–9.
88.
go back to reference Juckel G, Manitz MP, Brüne M, Friebe A, Heneka MT, Wolf RJ. Microglial activation in a neuroinflammational animal model of schizophrenia—a pilot study. Schizophr Res. 2011;131:96–100.PubMedCrossRef Juckel G, Manitz MP, Brüne M, Friebe A, Heneka MT, Wolf RJ. Microglial activation in a neuroinflammational animal model of schizophrenia—a pilot study. Schizophr Res. 2011;131:96–100.PubMedCrossRef
89.
go back to reference Smith JA, Das A, Ray SK, Banik NL. Role of pro-inflammatory cytokines released from microglia in neurodegenerative diseases. Brain Res Bull. 2012;87:10–20.PubMedCrossRef Smith JA, Das A, Ray SK, Banik NL. Role of pro-inflammatory cytokines released from microglia in neurodegenerative diseases. Brain Res Bull. 2012;87:10–20.PubMedCrossRef
90.
go back to reference Perez Nievas BG, Hammerschmidt T, Kummer MP, Terwel D, Leza JC, Heneka MT. Restraint stress increases neuroinflammation independently of amyloid β levels in amyloid precursor protein/PS1 transgenic mice. J Neurochem. 2011;116:43–52.PubMedCrossRef Perez Nievas BG, Hammerschmidt T, Kummer MP, Terwel D, Leza JC, Heneka MT. Restraint stress increases neuroinflammation independently of amyloid β levels in amyloid precursor protein/PS1 transgenic mice. J Neurochem. 2011;116:43–52.PubMedCrossRef
91.
go back to reference Sadasivan S, Pond BB, Pani AK, Qu C, Jiao Y, Smeyne RJ. Methylphenidate exposure induces dopamine neuron loss and activation of microglia in the basal ganglia of mice. PLoS One. 2012;7:e33693.PubMedPubMedCentralCrossRef Sadasivan S, Pond BB, Pani AK, Qu C, Jiao Y, Smeyne RJ. Methylphenidate exposure induces dopamine neuron loss and activation of microglia in the basal ganglia of mice. PLoS One. 2012;7:e33693.PubMedPubMedCentralCrossRef
94.
go back to reference Fiebich BL, Akter S, Akundi RS. The two-hit hypothesis for neuroinflammation: role of exogenous ATP in modulating inflammation in the brain. Front Cell Neurosci. 2014;8:260.PubMedPubMedCentralCrossRef Fiebich BL, Akter S, Akundi RS. The two-hit hypothesis for neuroinflammation: role of exogenous ATP in modulating inflammation in the brain. Front Cell Neurosci. 2014;8:260.PubMedPubMedCentralCrossRef
95.
go back to reference Spangenberg EE, Lee RJ, Najafi AR, Rice RA, Elmore MRP, Blurton-Jones M, et al. Eliminating microglia in Alzheimer’s mice prevents neuronal loss without modulating amyloid-β pathology. Brain J Neurol. 2016;139:1265–81.CrossRef Spangenberg EE, Lee RJ, Najafi AR, Rice RA, Elmore MRP, Blurton-Jones M, et al. Eliminating microglia in Alzheimer’s mice prevents neuronal loss without modulating amyloid-β pathology. Brain J Neurol. 2016;139:1265–81.CrossRef
96.
go back to reference Rice RA, Spangenberg EE, Yamate-Morgan H, Lee RJ, Arora RPS, Hernandez MX, et al. Elimination of microglia improves functional outcomes following extensive neuronal loss in the hippocampus. J Neurosci. 2015;35:9977–89.PubMedPubMedCentralCrossRef Rice RA, Spangenberg EE, Yamate-Morgan H, Lee RJ, Arora RPS, Hernandez MX, et al. Elimination of microglia improves functional outcomes following extensive neuronal loss in the hippocampus. J Neurosci. 2015;35:9977–89.PubMedPubMedCentralCrossRef
97.
go back to reference Shemer A, Erny D, Jung S, Prinz M. Microglia plasticity during health and disease: an immunological perspective. Trends Immunol. 2015;36:614–24.PubMedCrossRef Shemer A, Erny D, Jung S, Prinz M. Microglia plasticity during health and disease: an immunological perspective. Trends Immunol. 2015;36:614–24.PubMedCrossRef
99.
go back to reference Raasch J, Zeller N, van Loo G, Merkler D, Mildner A, Erny D, et al. IkappaB kinase 2 determines oligodendrocyte loss by non-cell-autonomous activation of NF-kappaB in the central nervous system. Brain J Neurol. 2011;134:1184–98.CrossRef Raasch J, Zeller N, van Loo G, Merkler D, Mildner A, Erny D, et al. IkappaB kinase 2 determines oligodendrocyte loss by non-cell-autonomous activation of NF-kappaB in the central nervous system. Brain J Neurol. 2011;134:1184–98.CrossRef
100.
go back to reference de Oliveira ACP, Yousif NM, Bhatia HS, Hermanek J, Huell M, Fiebich BL. Poly(I:C) increases the expression of mPGES-1 and COX-2 in rat primary microglia. J Neuroinflammation. 2016;13:11.PubMedPubMedCentralCrossRef de Oliveira ACP, Yousif NM, Bhatia HS, Hermanek J, Huell M, Fiebich BL. Poly(I:C) increases the expression of mPGES-1 and COX-2 in rat primary microglia. J Neuroinflammation. 2016;13:11.PubMedPubMedCentralCrossRef
101.
go back to reference Bhatia HS, Baron J, Hagl S, Eckert GP, Fiebich BL. Rice bran derivatives alleviate microglia activation: possible involvement of MAPK pathway. J Neuroinflammation. 2016;13:148.PubMedPubMedCentralCrossRef Bhatia HS, Baron J, Hagl S, Eckert GP, Fiebich BL. Rice bran derivatives alleviate microglia activation: possible involvement of MAPK pathway. J Neuroinflammation. 2016;13:148.PubMedPubMedCentralCrossRef
102.
go back to reference Kim SF, Huri DA, Snyder SH. Inducible nitric oxide synthase binds, S-nitrosylates, and activates cyclooxygenase-2. Science. 2005;310:1966–70.PubMedCrossRef Kim SF, Huri DA, Snyder SH. Inducible nitric oxide synthase binds, S-nitrosylates, and activates cyclooxygenase-2. Science. 2005;310:1966–70.PubMedCrossRef
103.
go back to reference Cuadrado A, Martín-Moldes Z, Ye J, Lastres-Becker I. Transcription factors NRF2 and NF-κB are coordinated effectors of the Rho family, GTP-binding protein RAC1 during inflammation. J Biol Chem. 2014;289:15244–58. Cuadrado A, Martín-Moldes Z, Ye J, Lastres-Becker I. Transcription factors NRF2 and NF-κB are coordinated effectors of the Rho family, GTP-binding protein RAC1 during inflammation. J Biol Chem. 2014;289:15244–58.
104.
go back to reference Taetzsch T, Levesque S, McGraw C, Brookins S, Luqa R, Bonini MG, et al. Redox regulation of NF-κB p50 and M1 polarization in microglia. Glia. 2015;63:423–40.PubMedCrossRef Taetzsch T, Levesque S, McGraw C, Brookins S, Luqa R, Bonini MG, et al. Redox regulation of NF-κB p50 and M1 polarization in microglia. Glia. 2015;63:423–40.PubMedCrossRef
105.
go back to reference Lee PC, Raaschou-Nielsen O, Lill CM, Bertram L, Sinsheimer JS, Hansen J, et al. Gene-environment interactions linking air pollution and inflammation in Parkinson’s disease. Environ Res. 2016;151:713–20.PubMedCrossRef Lee PC, Raaschou-Nielsen O, Lill CM, Bertram L, Sinsheimer JS, Hansen J, et al. Gene-environment interactions linking air pollution and inflammation in Parkinson’s disease. Environ Res. 2016;151:713–20.PubMedCrossRef
106.
go back to reference Brigelius-Flohé R, Flohé L. Basic principles and emerging concepts in the redox control of transcription factors. Antioxid Redox Signal. 2011;15:2335–81.PubMedPubMedCentralCrossRef Brigelius-Flohé R, Flohé L. Basic principles and emerging concepts in the redox control of transcription factors. Antioxid Redox Signal. 2011;15:2335–81.PubMedPubMedCentralCrossRef
107.
108.
go back to reference Minelli A, Conte C, Grottelli S, Bellezza I, Cacciatore I, Bolaños JP. Cyclo (His-pro) promotes cytoprotection by activating Nrf2-mediated up-regulation of antioxidant defence. J Cell Mol Med. 2009;13:1149–61.PubMedCrossRef Minelli A, Conte C, Grottelli S, Bellezza I, Cacciatore I, Bolaños JP. Cyclo (His-pro) promotes cytoprotection by activating Nrf2-mediated up-regulation of antioxidant defence. J Cell Mol Med. 2009;13:1149–61.PubMedCrossRef
109.
go back to reference Lutz JA, Carter M, Fields L, Barron S, Littleton JM. Altered relation between lipopolysaccharide-induced inflammatory response and excitotoxicity in rat organotypic hippocampal slice cultures during ethanol withdrawal. Alcohol Clin Exp Res. 2015;39:827–35.PubMedPubMedCentralCrossRef Lutz JA, Carter M, Fields L, Barron S, Littleton JM. Altered relation between lipopolysaccharide-induced inflammatory response and excitotoxicity in rat organotypic hippocampal slice cultures during ethanol withdrawal. Alcohol Clin Exp Res. 2015;39:827–35.PubMedPubMedCentralCrossRef
110.
go back to reference Järvelä JT, Ruohonen S, Kukko-Lukjanov T-K, Plysjuk A, Lopez Picon FR, Holopainen IE. Kainic acid-induced neurodegeneration and activation of inflammatory processes in organotypic hippocampal slice cultures: treatment with cyclooxygenase-2 inhibitor does not prevent neuronal death. Neuropharmacology. 2011;60:1116–25.PubMedCrossRef Järvelä JT, Ruohonen S, Kukko-Lukjanov T-K, Plysjuk A, Lopez Picon FR, Holopainen IE. Kainic acid-induced neurodegeneration and activation of inflammatory processes in organotypic hippocampal slice cultures: treatment with cyclooxygenase-2 inhibitor does not prevent neuronal death. Neuropharmacology. 2011;60:1116–25.PubMedCrossRef
Metadata
Title
Inflammatory and cytotoxic effects of bifenthrin in primary microglia and organotypic hippocampal slice cultures
Authors
Brahim Gargouri
Nizar M. Yousif
Michèle Bouchard
Hamadi Fetoui
Bernd L. Fiebich
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Journal of Neuroinflammation / Issue 1/2018
Electronic ISSN: 1742-2094
DOI
https://doi.org/10.1186/s12974-018-1198-1

Other articles of this Issue 1/2018

Journal of Neuroinflammation 1/2018 Go to the issue