Pinocembrin Suppresses H2O2-Induced Mitochondrial Dysfunction by a Mechanism Dependent on the Nrf2/HO-1 Axis in SH-SY5Y Cells
Tóm tắt
Mitochondria are susceptible to redox impairment, which has been associated with neurodegeneration. These organelles are both a source and target of reactive species. In that context, there is increasing interest in finding natural compounds that modulate mitochondrial function and mitochondria-related signaling in order to prevent or to treat diseases involving mitochondrial impairment. Herein, we investigated whether and how pinocembrin (PB) would prevent mitochondrial dysfunction elicited by the exposure of human neuroblastoma SH-SY5Y cells to hydrogen peroxide (H2O2). PB (25 μM) was administrated for 4 h before H2O2 treatment (300 μM for 24 h). PB prevented H2O2-induced loss of cell viability mitochondrial depolarization in SH-SY5Y cells. PB also attenuated redox impairment in mitochondrial membranes. The production of superoxide anion radical (O2
−•) and nitric oxide (NO•) was alleviated by PB in cells exposed to H2O2. PB suppressed the H2O2-induced inhibition of the tricarboxylic acid (TCA) cycle enzymes aconitase, α-ketoglutarate dehydrogenase, and succinate dehydrogenase. Furthermore, PB induced anti-inflammatory effects by abolishing the H2O2-dependent activation of the nuclear factor-κB (NF-κB) and upregulation of interleukin-1β (IL-1β) and tumor necrosis factor-α (TNF-α). The PB-induced antioxidant and anti-inflammatory effects are dependent on the heme oxygenate-1 (HO-1) enzyme and on the activation of the transcription factor nuclear factor erythroid 2-related factor 2 (Nrf2), since HO-1 inhibition (with 0.5 μM ZnPP IX) or Nrf2 silencing (with small interfering RNA (siRNA)) abolished the effects of PB. Overall, PB afforded cytoprotection by the Nrf2/HO-1 axis in H2O2-treated SH-SY5Y cells.
Tài liệu tham khảo
Brown GC (1992) Control of respiration and ATP synthesis in mammalian mitochondria and cells. Biochem J 284:1–13
Hill BG, Benavides GA, Lancaster JR Jr, Ballinger S, Dell’Italia L, Jianhua Z, Darley-Usmar VM (2012) Integration of cellular bioenergetics with mitochondrial quality control and autophagy. Biol Chem 393:1485–1512
Van Bergen NJ, Blake RE, Crowston JG, Trounce IA (2014) Oxidative phosphorylation measurement in cell lines and tissues. Mitochondrion 15:24–33. doi:10.1016/j.mito.2014.03.003
Yoshikawa S, Muramoto K, Shinzawa-Itoh K (2011) Proton-pumping mechanism of cytochrome C oxidase. Annu Rev Biophys 40:205–223. doi:10.1146/annurev-biophys-042910-155341
Lenaz G, Cavazzoni M, Genova ML, D’Aurelio M, Merlo Pich M, Pallotti F, Formiggini G, Marchetti M et al (1998) Oxidative stress, antioxidant defences and aging. Biofactors 8:195–204
Cadenas E, Davies KJ (2000) Mitochondrial free radical generation, oxidative stress, and aging. Free Radic Biol Med 29:222–230
Naoi M, Maruyama W, Shamoto-Nagai M, Yi H, Akao Y, Tanaka M (2005) Oxidative stress in mitochondria: decision to survival and death of neurons in neurodegenerative disorders. Mol Neurobiol 31:81–93
Liu SS (2010) Mitochondrial Q cycle-derived superoxide and chemiosmotic bioenergetics. Ann N Y Acad Sci 1201:84–95. doi:10.1111/j.1749-6632.2010.05632.x
Aluri HS, Simpson DC, Allegood JC, Hu Y, Szczepanek K, Gronert S, Chen Q, Lesnefsky EJ (2014) Electron flow into cytochrome c coupled with reactive oxygen species from the electron transport chain converts cytochrome c to a cardiolipin peroxidase: role during ischemia-reperfusion. Biochim Biophys Acta 1840:3199–3207. doi:10.1016/j.bbagen.2014.07.017
Tajeddine N (2016) How do reactive oxygen species and calcium trigger mitochondrial membrane permeabilisation? Biochim Biophys Acta 1860:1079–1088. doi:10.1016/j.bbagen.2016.02.013
de Oliveira MR, Soares Oliveira MW, Müller Hoff ML, Behr GA, da Rocha RF, Fonseca Moreira JC (2009) Evaluation of redox and bioenergetics states in the liver of vitamin A-treated rats. Eur J Pharmacol 610:99–105. doi:10.1016/j.ejphar.2009.03.046
Gobe G, Crane D (2010) Mitochondria, reactive oxygen species and cadmium toxicity in the kidney. Toxicol Lett 198:49–55. doi:10.1016/j.toxlet.2010.04.013
Abarikwu SO, Pant AB, Farombi EO (2012) 4-Hydroxynonenal induces mitochondrial-mediated apoptosis and oxidative stress in SH-SY5Y human neuronal cells. Basic Clin Pharmacol Toxicol 110:441–448. doi:10.1111/j.1742-7843.2011.00834.x
de Oliveira MR, da Rocha RF, Pasquali MA, Moreira JC (2012) The effects of vitamin A supplementation for 3 months on adult rat nigrostriatal axis: increased monoamine oxidase enzyme activity, mitochondrial redox dysfunction, increased β-amyloid(1-40) peptide and TNF-α contents, and susceptibility of mitochondria to an in vitro H2O2 challenge. Brain Res Bull 87:432–444. doi:10.1016/j.brainresbull.2012.01.005
de Oliveira MR (2015) Vitamin A and retinoids as mitochondrial toxicants. Oxidative Med Cell Longev 2015:140267. doi:10.1155/2015/140267
de Oliveira MR (2016) Fluoxetine and the mitochondria: a review of the toxicological aspects. Toxicol Lett 258:185–191. doi:10.1016/j.toxlet.2016.07.001
de Oliveira MR, Jardim FR (2016) Cocaine and mitochondria-related signaling in the brain: a mechanistic view and future directions. Neurochem Int 92:58–66. doi:10.1016/j.neuint.2015.12.006
Rezin GT, Amboni G, Zugno AI, Quevedo J, Streck EL (2009) Mitochondrial dysfunction and psychiatric disorders. Neurochem Res 34:1021–1029. doi:10.1007/s11064-008-9865-8
Paradies G, Petrosillo G, Paradies V, Ruggiero FM (2011) Mitochondrial dysfunction in brain aging: role of oxidative stress and cardiolipin. Neurochem Int 58:447–457. doi:10.1016/j.neuint.2010.12.016
Kasote DM, Hegde MV, Katyare SS (2013) Mitochondrial dysfunction in psychiatric and neurological diseases: cause(s), consequence(s), and implications of antioxidant therapy. Biofactors 39:392–406
Bird MJ, Thorburn DR, Frazier AE (2014) Modelling biochemical features of mitochondrial neuropathology. Biochim Biophys Acta 1840:1380–1392. doi:10.1016/j.bbagen.2013.10.017
Kotiadis VN, Duchen MR, Osellame LD (2014) Mitochondrial quality control and communications with the nucleus are important in maintaining mitochondrial function and cell health. Biochim Biophys Acta 1840:1254–1265. doi:10.1016/j.bbagen.2013.10.041
Procaccini C, Santopaolo M, Faicchia D, Colamatteo A, Formisano L, de Candia P, Galgani M, De Rosa V et al (2016) Role of metabolism in neurodegenerative disorders. Metabolism 65:1376–1390. doi:10.1016/j.metabol.2016.05.018
Niedzielska E, Smaga I, Gawlik M, Moniczewski A, Stankowicz P, Pera J, Filip M (2016) Oxidative stress in neurodegenerative diseases. Mol Neurobiol 53:4094–4125. doi:10.1007/s12035-015-9337-5
Picard M, Wallace DC, Burelle Y (2016) The rise of mitochondria in medicine. Mitochondrion 30:105–116. doi:10.1016/j.mito.2016.07.003
Ryu SY, Peixoto PM, Teijido O, Dejean LM, Kinnally KW (2010) Role of mitochondrial ion channels in cell death. Biofactors 36:255–263
Shoshan-Barmatz V, Ben-Hail D (2012) VDAC, a multi-functional mitochondrial protein as a pharmacological target. Mitochondrion 12:24–34. doi:10.1016/j.mito.2011.04.001
Green DR, Galluzzi L, Kroemer G (2014) Metabolic control of cell death. Science 345:1250256. doi:10.1126/science.1250256
Atamna H, Mackey J, Dhahbi JM (2012) Mitochondrial pharmacology: electron transport chain bypass as strategies to treat mitochondrial dysfunction. Biofactors 38:158–166
Gruber J, Fong S, Chen CB, Yoong S, Pastorin G, Schaffer S, Cheah I, Halliwell B (2013) Mitochondria-targeted antioxidants and metabolic modulators as pharmacological interventions to slow ageing. Biotechnol Adv 31:563–592. doi:10.1016/j.biotechadv.2012.09.005
de Oliveira MR, Nabavi SF, Habtemariam S, Erdogan Orhan I, Daglia M, Nabavi SM (2015) The effects of baicalein and baicalin on mitochondrial function and dynamics: a review. Pharmacol Res 100:296–308. doi:10.1016/j.phrs.2015.08.021
de Oliveira MR, Jardim FR, Setzer WN, Nabavi SM, Nabavi SF (2016) Curcumin, mitochondrial biogenesis, and mitophagy: exploring recent data and indicating future needs. Biotechnol Adv 34:813–826. doi:10.1016/j.biotechadv.2016.04.004
de Oliveira MR, Nabavi SM, Braidy N, Setzer WN, Ahmed T, Nabavi SF (2016) Quercetin and the mitochondria: a mechanistic view. Biotechnol Adv 34:532–549. doi:10.1016/j.biotechadv.2015.12.014
de Oliveira MR, Nabavi SF, Manayi A, Daglia M, Hajheydari Z, Nabavi SM (2016) Resveratrol and the mitochondria: from triggering the intrinsic apoptotic pathway to inducing mitochondrial biogenesis, a mechanistic view. Biochim Biophys Acta 1860:727–745. doi:10.1016/j.bbagen.2016.01.017
Nguyen T, Nioi P, Pickett CB (2009) The Nrf2-antioxidant response element signaling pathway and its activation by oxidative stress. J Biol Chem 284:13291–13295. doi:10.1074/jbc.R900010200
Uruno A, Motohashi H (2011) The Keap1-Nrf2 system as an in vivo sensor for electrophiles. Nitric Oxide 25:153–160. doi:10.1016/j.niox.2011.02.007
Tufekci KU, Civi Bayin E, Genc S, Genc K (2011) The Nrf2/ARE pathway: a promising target to counteract mitochondrial dysfunction in Parkinson’s disease. Parkinsons Dis 2011:314082. doi:10.4061/2011/314082
Piantadosi CA, Suliman HB (2012) Transcriptional control of mitochondrial biogenesis and its interface with inflammatory processes. Biochim Biophys Acta 1820:532–541. doi:10.1016/j.bbagen.2012.01.003
Denzer I, Münch G, Friedland K (2016) Modulation of mitochondrial dysfunction in neurodegenerative diseases via activation of nuclear factor erythroid-2-related factor 2 by food-derived compounds. Pharmacol Res 103:80–94. doi:10.1016/j.phrs.2015.11.019
Choi AM, Alam J (1996) Heme oxygenase-1: function, regulation, and implication of a novel stress-inducible protein in oxidant-induced lung injury. Am J Respir Cell Mol Biol 15:9–19
Gozzelino R, Jeney V, Soares MP (2010) Mechanisms of cell protection by heme oxygenase-1. Annu Rev Pharmacol Toxicol 50:323–354. doi:10.1146/annurev.pharmtox.010909.105600
Kumar S, Bandyopadhyay U (2005) Free heme toxicity and its detoxification systems in human. Toxicol Lett 157:175–188
Jansen T, Daiber A (2012) Direct antioxidant properties of bilirubin and biliverdin. Is there a role for biliverdin reductase? Front Pharmacol 3:30. doi:10.3389/fphar.2012.00030
Megías J, Busserolles J, Alcaraz MJ (2007) The carbon monoxide-releasing molecule CORM-2 inhibits the inflammatory response induced by cytokines in Caco-2 cells. Br J Pharmacol 150:977–986
Rasul A, Millimouno FM, Ali Eltayb W, Ali M, Li J, Li X (2013) Pinocembrin: a novel natural compound with versatile pharmacological and biological activities. Biomed Res Int 2013:379850. doi:10.1155/2013/379850
Reddy KK, Grossman L, Rogers GS (2013) Common complementary and alternative therapies with potential use in dermatologic surgery: risks and benefits. J Am Acad Dermatol 68:e127–1e35. doi:10.1016/j.jaad.2011.06.030
Lan X, Wang W, Li Q, Wang J (2016) The natural flavonoid pinocembrin: molecular targets and potential therapeutic applications. Mol Neurobiol 53:1794–1801. doi:10.1007/s12035-015-9125-2
Liu R, Wu CX, Zhou D, Yang F, Tian S, Zhang L, Zhang TT, Du GH (2012) Pinocembrin protects against β-amyloid-induced toxicity in neurons through inhibiting receptor for advanced glycation end products (RAGE)-independent signaling pathways and regulating mitochondrion-mediated apoptosis. BMC Med 10:105. doi:10.1186/1741-7015-10-105
Liu R, Li JZ, Song JK, Sun JL, Li YJ, Zhou SB, Zhang TT, Du GH (2014) Pinocembrin protects human brain microvascular endothelial cells against fibrillar amyloid-β(1-40) injury by suppressing the MAPK/NF-κB inflammatory pathways. Biomed Res Int 2014:470393. doi:10.1155/2014/470393
Liu R, Li JZ, Song JK, Zhou D, Huang C, Bai XY, Xie T, Zhang X et al (2014) Pinocembrin improves cognition and protects the neurovascular unit in Alzheimer related deficits. Neurobiol Aging 35:1275–1285. doi:10.1016/j.neurobiolaging.2013.12.031
Wang Y, Miao Y, Mir AZ, Cheng L, Wang L, Zhao L, Cui Q, Zhao W et al (2016) Inhibition of beta-amyloid-induced neurotoxicity by pinocembrin through Nrf2/HO-1 pathway in SH-SY5Y cells. J Neurol Sci 368:223–230. doi:10.1016/j.jns.2016.07.010
Wang H, Wang Y, Zhao L, Cui Q, Wang Y, Du G (2016) Pinocembrin attenuates MPP(+)-induced neurotoxicity by the induction of heme oxygenase-1 through ERK1/2 pathway. Neurosci Lett 612:104–109. doi:10.1016/j.neulet.2015.11.048
Jin X, Liu Q, Jia L, Li M, Wang X (2015) Pinocembrin attenuates 6-OHDA-induced neuronal cell death through Nrf2/ARE pathway in SH-SY5Y cells. Cell Mol Neurobiol 35:323–333. doi:10.1007/s10571-014-0128-8
Gao M, Zhang WC, Liu QS, Hu JJ, Liu GT, Du GH (2008) Pinocembrin prevents glutamate-induced apoptosis in SH-SY5Y neuronal cells via decrease of bax/bcl-2 ratio. Eur J Pharmacol 591:73–79. doi:10.1016/j.ejphar.2008.06.071
Meng F, Liu R, Gao M, Wang Y, Yu X, Xuan Z, Sun J, Yang F et al (2011) Pinocembrin attenuates blood-brain barrier injury induced by global cerebral ischemia-reperfusion in rats. Brain Res 1391:93–101. doi:10.1016/j.brainres.2011.03.010
Saad MA, Abdel Salam RM, Kenawy SA, Attia AS (2015) Pinocembrin attenuates hippocampal inflammation, oxidative perturbations and apoptosis in a rat model of global cerebral ischemia reperfusion. Pharmacol Rep 67:115–122. doi:10.1016/j.pharep.2014.08.014
Shi LL, Chen BN, Gao M, Zhang HA, Li YJ, Wang L, Du GH (2011) The characteristics of therapeutic effect of pinocembrin in transient global brain ischemia/reperfusion rats. Life Sci 88:521–528. doi:10.1016/j.lfs.2011.01.011
Wu CX, Liu R, Gao M, Zhao G, Wu S, Wu CF, Du GH (2013) Pinocembrin protects brain against ischemia/reperfusion injury by attenuating endoplasmic reticulum stress induced apoptosis. Neurosci Lett 546:57–62. doi:10.1016/j.neulet.2013.04.060
de Oliveira MR, Peres A, Gama CS, Bosco SM (2016) Pinocembrin provides mitochondrial protection by the activation of the Erk1/2-Nrf2 signaling pathway in SH-SY5Y neuroblastoma cells exposed to paraquat. Mol Neurobiol DOI. doi:10.1007/s12035-016-0135-5
Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55–63
de Oliveira MR, Ferreira GC, Schuck PF, Dal Bosco SM (2015) Role for the PI3K/Akt/Nrf2 signaling pathway in the protective effects of carnosic acid against methylglyoxal-induced neurotoxicity in SH-SY5Y neuroblastoma cells. Chem Biol Interact 242:396–406. doi:10.1016/j.cbi.2015.11.003
de Oliveira MR, Ferreira GC, Schuck PF (2016) Protective effect of carnosic acid against paraquat-induced redox impairment and mitochondrial dysfunction in SH-SY5Y cells: role for PI3K/Akt/Nrf2 pathway. Toxicol in Vitro 32:41–54. doi:10.1016/j.tiv.2015.12.005
LeBel CP, Ischiropoulos H, Bondy SC (1992) Evaluation of the probe 2′,7′-dichlorofluorescin as an indicator of reactive oxygen species formation and oxidative stress. Chem Res Toxicol 5:227–231
De Oliveira MR, Oliveira MW, Da Rocha RF, Moreira JC (2009) Vitamin A supplementation at pharmacological doses induces nitrosative stress on the hypothalamus of adult Wistar rats. Chem Biol Interact 180:407–413. doi:10.1016/j.cbi.2009.02.006
de Oliveira MR, Lorenzi R, Schnorr CE, Morrone M, Moreira JC (2011) Increased 3-nitrotyrosine levels in mitochondrial membranes and impaired respiratory chain activity in brain regions of adult female rats submitted to daily vitamin A supplementation for 2 months. Brain Res Bull 86:246–253. doi:10.1016/j.brainresbull.2011.08.006
de Oliveira MR, da Rocha RF, Moreira JC (2012) Increased susceptibility of mitochondria isolated from frontal cortex and hippocampus of vitamin A-treated rats to non-aggregated amyloid-β peptides 1-40 and 1-42. Acta Neuropsychiatr 24:101–108. doi:10.1111/j.1601-5215.2011.00588.x
de Oliveira MR, da Rocha RF, Schnorr CE, Moreira JC (2012) L-NAME cotreatment did prevent neither mitochondrial impairment nor behavioral abnormalities in adult Wistar rats treated with vitamin A supplementation. Fundam Clin Pharmacol 26:513–529. doi:10.1111/j.1472-8206.2011.00943.x
Wang K, Zhu L, Zhu X, Zhang K, Huang B, Zhang J, Zhang Y, Zhu L et al (2014) Protective effect of paeoniflorin on Aβ25-35-induced SH-SY5Y cell injury by preventing mitochondrial dysfunction. Cell Mol Neurobiol 34:227–234. doi:10.1007/s10571-013-0006-9
Poderoso JJ, Carreras MC, Lisdero C, Riobó N, Schöpfer F, Boveris A (1996) Nitric oxide inhibits electron transfer and increases superoxide radical production in rat heart mitochondria and submitochondrial particles. Arch Biochem Biophys 328:85–92
De Oliveira MR, Moreira JC (2008) Impaired redox state and respiratory chain enzyme activities in the cerebellum of vitamin A-treated rats. Toxicology 253:125–130. doi:10.1016/j.tox.2008.09.003
de Oliveira MR, Moreira JC (2007) Acute and chronic vitamin A supplementation at therapeutic doses induces oxidative stress in submitochondrial particles isolated from cerebral cortex and cerebellum of adult rats. Toxicol Lett 173:145–150
de Oliveira MR, Peres A, Ferreira GC, Schuck PF, Bosco SM (2016) Carnosic acid affords mitochondrial protection in chlorpyrifos-treated Sh-Sy5y cells. Neurotox Res 30:367–379. doi:10.1007/s12640-016-9620-x
Lenaz G (2001) The mitochondrial production of reactive oxygen species: mechanisms and implications in human pathology. IUBMB Life 52:159–164
St-Pierre J, Buckingham JA, Roebuck SJ, Brand MD (2002) Topology of superoxide production from different sites in the mitochondrial electron transport chain. J Biol Chem 277:44784–44790
González-Aragón D, Burón MI, López-Lluch G, Hermán MD, Gómez-Díaz C, Navas P, Villalba JM (2005) Coenzyme Q and the regulation of intracellular steady-state levels of superoxide in HL-60 cells. Biofactors 25:31–41
Quinlan CL, Perevoshchikova IV, Hey-Mogensen M, Orr AL, Brand MD (2013) Sites of reactive oxygen species generation by mitochondria oxidizing different substrates. Redox Biol 1:304–312. doi:10.1016/j.redox.2013.04.005
Dröse S, Brandt U (2008) The mechanism of mitochondrial superoxide production by the cytochrome bc1 complex. J Biol Chem 283:21649–21654. doi:10.1074/jbc.M803236200
Dröse S, Brandt U (2012) Molecular mechanisms of superoxide production by the mitochondrial respiratory chain. Adv Exp Med Biol 748:145–169. doi:10.1007/978-1-4614-3573-0_6
Candas D, Li JJ (2014) MnSOD in oxidative stress response-potential regulation via mitochondrial protein influx. Antioxid Redox Signal 20:1599–1617. doi:10.1089/ars.2013.5305
He C, Hart PC, Germain D, Bonini MG (2016) SOD2 and the mitochondrial UPR: partners regulating cellular phenotypic transitions. Trends Biochem Sci 41:568–577. doi:10.1016/j.tibs.2016.04.004
Radi R, Cassina A, Hodara R (2002) Nitric oxide and peroxynitrite interactions with mitochondria. Biol Chem 383:401–409
Fernandez-Espejo E (2004) Pathogenesis of Parkinson’s disease: prospects of neuroprotective and restorative therapies. Mol Neurobiol 29:15–30
Pavlin M, Repič M, Vianello R, Mavri J (2016) The chemistry of neurodegeneration: kinetic data and their implications. Mol Neurobiol 53:3400–3415. doi:10.1007/s12035-015-9284-1
Kamsler A, Segal M (2004) Hydrogen peroxide as a diffusible signal molecule in synaptic plasticity. Mol Neurobiol 29:167–178
Canevari L, Abramov AY, Duchen MR (2004) Toxicity of amyloid beta peptide: tales of calcium, mitochondria, and oxidative stress. Neurochem Res 29:637–650
Tretter L, Sipos I, Adam-Vizi V (2004) Initiation of neuronal damage by complex I deficiency and oxidative stress in Parkinson’s disease. Neurochem Res 29:569–577
Zhao B (2005) Natural antioxidants for neurodegenerative diseases. Mol Neurobiol 31:283–293
Bacman SR, Bradley WG, Moraes CT (2006) Mitochondrial involvement in amyotrophic lateral sclerosis: trigger or target? Mol Neurobiol 33:113–131
Gubert C, Stertz L, Pfaffenseller B, Panizzutti BS, Rezin GT, Massuda R, Streck EL, Gama CS et al (2013) Mitochondrial activity and oxidative stress markers in peripheral blood mononuclear cells of patients with bipolar disorder, schizophrenia, and healthy subjects. J Psychiatr Res 47:1396–1402. doi:10.1016/j.jpsychires.2013.06.018
Hjelm BE, Rollins B, Mamdani F, Lauterborn JC, Kirov G, Lynch G, Gall CM, Sequeira A et al (2015) Evidence of mitochondrial dysfunction within the complex genetic etiology of schizophrenia. Mol Neuropsychiatry 1:201–219. doi:10.1159/000441252
Oliveira MR, Nabavi SF, Daglia M, Rastrelli L, Nabavi SM (2016) Epigallocatechin gallate and mitochondria-a story of life and death. Pharmacol Res 104:70–85. doi:10.1016/j.phrs.2015.12.027
Morris G, Berk M, Klein H, Walder K, Galecki P, Maes M (2016) Nitrosative stress, hypernitrosylation, and autoimmune responses to nitrosylated proteins: new pathways in neuroprogressive disorders including depression and chronic fatigue syndrome. Mol Neurobiol DOI. doi:10.1007/s12035-016-9975-2
Lu SC (2013) Glutathione synthesis. Biochim Biophys Acta 1830:3143–3153. doi:10.1016/j.bbagen.2012.09.008
Morris G, Anderson G, Dean O, Berk M, Galecki P, Martin-Subero M, Maes M (2014) The glutathione system: a new drug target in neuroimmune disorders. Mol Neurobiol 50:1059–1084. doi:10.1007/s12035-014-8705-x
Pae HO, Oh GS, Lee BS, Rim JS, Kim YM, Chung HT (2006) 3-Hydroxyanthranilic acid, one of L-tryptophan metabolites, inhibits monocyte chemoattractant protein-1 secretion and vascular cell adhesion molecule-1 expression via heme oxygenase-1 induction in human umbilical vein endothelial cells. Atherosclerosis 187:274–284
Choi BM, Lee JA, Gao SS, Eun SY, Kim YS, Ryu SY, Choi YH, Park R et al (2007) Brazilin and the extract from Caesalpinia sappan L. protect oxidative injury through the expression of heme oxygenase-1. Biofactors 30:149–157
Gullotta F, di Masi A, Coletta M, Ascenzi P (2012) CO metabolism, sensing, and signaling. Biofactors 38:1–13
Zhou LT, Wang KJ, Li L, Li H, Geng M (2015) Pinocembrin inhibits lipopolysaccharide-induced inflammatory mediators production in BV2 microglial cells through suppression of PI3K/Akt/NF-κB pathway. Eur J Pharmacol 761:211–216. doi:10.1016/j.ejphar.2015.06.003
Yang D, Elner SG, Bian ZM, Till GO, Petty HR, Elner VM (2007) Pro-inflammatory cytokines increase reactive oxygen species through mitochondria and NADPH oxidase in cultured RPE cells. Exp Eye Res 85:462–472
Pelletier M, Lepow TS, Billingham LK, Murphy MP, Siegel RM (2012) New tricks from an old dog: mitochondrial redox signaling in cellular inflammation. Semin Immunol 24:384–392. doi:10.1016/j.smim.2013.01.002