Regulated Necrosis Orchestrates Microglial Cell Death in Manganese-Induced Toxicity

Neuroscience - Tập 393 - Trang 206-225 - 2018
Soledad Porte Alcon1, Roxana Mayra Gorojod1, Mónica Lidia Kotler1
1CONICET-Universidad de Buenos Aires, Instituto de Química Biológica Ciencias Exactas y Naturales (IQUIBICEN), Facultad de Ciencias Exactas y Naturales, Departamento de Química Biológica, Laboratorio de Disfunción Celular en Enfermedades Neurodegenerativas y Nanomedicina, Buenos Aires, Argentina

Tài liệu tham khảo

Aits, 2013, Lysosomal cell death at a glance, J Cell Sci, 126, 1905, 10.1242/jcs.091181 Alaimo, 2014, Deregulation of mitochondria-shaping proteins Opa-1 and Drp-1 in manganese-induced apoptosis, PLoS One, 9, 10.1371/journal.pone.0091848 Alaimo, 2011, The extrinsic and intrinsic apoptotic pathways are involved in manganese toxicity in rat astrocytoma C6 cells, Neurochem Int, 59, 297, 10.1016/j.neuint.2011.06.001 Andrabi, 2008, Mitochondrial and nuclear cross talk in cell death: parthanatos, Ann N Y Acad Sci, 1147, 233, 10.1196/annals.1427.014 Andrabi, 2006, Poly(ADP-ribose) (PAR) polymer is a death signal, Proc Natl Acad Sci U S A, 103, 18308, 10.1073/pnas.0606526103 Aschner, 2006, Manganese: pharmacokinetics and molecular mechanisms of brain uptake, Toxicol Rev, 25, 147, 10.2165/00139709-200625030-00002 Aschner, 2007, Manganese: recent advances in understanding its transport and neurotoxicity, Toxicol Appl Pharmacol, 221, 131, 10.1016/j.taap.2007.03.001 Bae, 2006, Manganese induces inducible nitric oxide synthase (iNOS) expression via activation of both MAP kinase and PI3K/Akt pathways in BV2 microglial cells, Neurosci Lett, 398, 151, 10.1016/j.neulet.2005.12.067 Blasi, 1990, Immortalization of murine microglial cells by a v-raf/v-myc carrying retrovirus, J Neuroimmunol, 27, 229, 10.1016/0165-5728(90)90073-V Bocchini, 1992, An immortalized cell line expresses properties of activated microglial cells, J Neurosci Res, 31, 616, 10.1002/jnr.490310405 Bornhorst, 2013, Molecular mechanisms of Mn induced neurotoxicity: RONS generation, genotoxicity, and DNA-damage response, Mol Nutr Food Res, 57, 1255, 10.1002/mnfr.201200758 Bornhorst, 2015, Chapter 24: DNA damage induced by manganese, 604 Boujrad, 2007, AIF-mediated programmed necrosis: a highly regulated way to die, Cell Cycle, 6, 2612, 10.4161/cc.6.21.4842 Bradford, 1976, A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding, Anal Biochem, 72, 248, 10.1016/0003-2697(76)90527-3 Burguillos, 2011, Caspase signalling controls microglia activation and neurotoxicity, Nature, 472, 319, 10.1038/nature09788 Bussi, 2017, Autophagy down regulates pro-inflammatory mediators in BV2 microglial cells and rescues both LPS and alpha-synuclein induced neuronal cell death, Sci Rep, 7, 43153, 10.1038/srep43153 Butterworth, 1986, Changes in nine enzyme markers for neurons, glia, and endothelial cells in agonal state and Huntington’s disease caudate nucleus, J Neurochem, 47, 583, 10.1111/j.1471-4159.1986.tb04539.x Candé, 2004, Apoptosis-inducing factor (AIF): caspase-independent after all, Cell Death Differ, 11, 591, 10.1038/sj.cdd.4401400 Cersosimo, 2006, The diagnosis of manganese-induced parkinsonism, Neurotoxicology, 27, 340, 10.1016/j.neuro.2005.10.006 Chaitanya, 2008, Multiple apoptogenic proteins are involved in the nuclear translocation of Apoptosis Inducing Factor during transient focal cerebral ischemia in rat, Brain Res, 1246, 178, 10.1016/j.brainres.2008.09.075 Chaitanya, 2010, PARP-1 cleavage fragments: signatures of cell-death proteases in neurodegeneration, Cell Commun Signal, 8, 31, 10.1186/1478-811X-8-31 Chang, 2013, Exosomes of BV-2 cells induced by alpha-synuclein: important mediator of neurodegeneration in PD, Neurosci Lett, 548, 190, 10.1016/j.neulet.2013.06.009 Chang, 1999, Manganese potentiates nitric oxide production by microglia, Brain Res Mol Brain Res, 68, 22, 10.1016/S0169-328X(99)00082-0 Cheung, 2005, Apoptosis-inducing factor is a key factor in neuronal cell death propagated by BAX-dependent and BAX-independent mechanisms. – Semantic Scholar, J Neurosci, 25, 1324, 10.1523/JNEUROSCI.4261-04.2005 Circu, 2010, Reactive oxygen species, cellular redox systems, and apoptosis, Free Radical Biol Med, 48, 749, 10.1016/j.freeradbiomed.2009.12.022 Connolly, 2014, New roles for old enzymes: killer caspases as the engine of cell behavior changes, Front Physiol, 5, 149, 10.3389/fphys.2014.00149 Couper, 1837, On the effects of black oxide of manganese when inhaled into the lungs, Br Ann Med Pharmacol, 1, 41 Cummings, 2012, Measurement of cell death in mammalian cells, Curr Protoc Pharmacol, 12, 8 Dheen, 2007, Microglial activation and its implications in the brain diseases, Curr Med Chem, 14, 1189, 10.2174/092986707780597961 Dodd, 2011, Manganese potentiates LPS-induced heme-oxygenase 1 in microglia but not dopaminergic cells: role in controlling microglial hydrogen peroxide and inflammatory cytokine output, Neurotoxicology, 32, 683, 10.1016/j.neuro.2011.09.002 Dorstyn, 2012, Caspase-2 deficiency promotes aberrant DNA-damage response and genetic instability, Cell Death Differ, 19, 1288, 10.1038/cdd.2012.36 Erikson, 2003, Manganese neurotoxicity and glutamate-GABA interaction, Neurochem Int, 43, 475, 10.1016/S0197-0186(03)00037-8 Erikson, 2005, Interactions between excessive manganese exposures and dietary iron-deficiency in neurodegeneration, Environ Toxicol Pharmacol, 19, 415, 10.1016/j.etap.2004.12.053 Fan, 2010, Critical role of lysosome and its associated protein cathepsin D in manganese-induced toxicity in cultured midbrain astrocyte, Neurochem Int, 56, 291, 10.1016/j.neuint.2009.11.001 Fatokun, 2014, Parthanatos: mitochondrial-linked mechanisms and therapeutic opportunities, Br J Pharmacol, 171, 2000, 10.1111/bph.12416 Fenech, 2011, Molecular mechanisms of micronucleus, nucleoplasmic bridge and nuclear bud formation in mammalian and human cells, Mutagenesis, 26, 125, 10.1093/mutage/geq052 Ferrara, 2013, Phosphatidylserine metabolism modification precedes manganese-induced apoptosis and phosphatidylserine exposure in PC12 cells, Neurotoxicology, 39, 25, 10.1016/j.neuro.2013.07.006 Filipov, 2005, Manganese potentiates in vitro production of proinflammatory cytokines and nitric oxide by microglia through a nuclear factor kappa B-dependent mechanism, Toxicol Sci, 84, 139, 10.1093/toxsci/kfi055 Forsberg, 2017, Caspase-2: an orphan enzyme out of the shadows, Oncogene, 36, 5441, 10.1038/onc.2017.169 Galli, 2009, A new paradigm for MAPK: structural interactions of hERK1 with mitochondria in HeLa cells, PLoS One, 4, 10.1371/journal.pone.0007541 Galluzzi, 2015, Essential versus accessory aspects of cell death: recommendations of the NCCD 2015, Cell Death Differ, 22, 58, 10.1038/cdd.2014.137 Gandhi, 2018, Manganese-induced neurotoxicity and alterations in gene expression in human neuroblastoma SH-SY5Y cells, Biol Trace Elem Res, 183, 245, 10.1007/s12011-017-1153-5 Gavin, 1999, Manganese and calcium transport in mitochondria: implications for manganese toxicity, Neurotoxicology, 20, 445 Gobeil, 2001, Characterization of the necrotic cleavage of poly(ADP-ribose) polymerase (PARP-1): implication of lysosomal proteases, Cell Death Differ, 8, 588, 10.1038/sj.cdd.4400851 Gonzalez, 2008, Manganese activates the mitochondrial apoptotic pathway in rat astrocytes by modulating the expression of proteins of the Bcl-2 family, Neurochem Int, 53, 408, 10.1016/j.neuint.2008.09.008 Gordon, 2016, Protein kinase Cδ upregulation in microglia drives neuroinflammatory responses and dopaminergic neurodegeneration in experimental models of Parkinson’s disease, Neurobiol Dis, 93, 96, 10.1016/j.nbd.2016.04.008 Gorojod, 2015, The autophagic-lysosomal pathway determines the fate of glial cells under manganese-induced oxidative stress conditions, Free Radical Biol Med, 87, 237, 10.1016/j.freeradbiomed.2015.06.034 Gorojod, 2017, Interplay between lysosomal, mitochondrial and death receptor pathways during manganese-induced apoptosis in glial cells, Arch Toxicol, 91, 3065, 10.1007/s00204-017-1936-7 Henn, 2009, The suitability of BV2 cells as alternative model system for primary microglia cultures or for animal experiments examining brain inflammation, ALTEX, 26, 83, 10.14573/altex.2009.2.83 Higashi, 2004, Parkin attenuates manganese-induced dopaminergic cell death, J Neurochem, 89, 1490, 10.1111/j.1471-4159.2004.02445.x Hirata, 2002, Manganese-induced apoptosis in PC12 cells, Neurotoxicol Teratol, 24, 639, 10.1016/S0892-0362(02)00215-5 Hirata, 1998, Activation of JNK pathway and induction of apoptosis by manganese in PC12 cells, J Neurochem, 71, 1607, 10.1046/j.1471-4159.1998.71041607.x Hirata, 2004, Anti-apoptotic and pro-apoptotic effect of NEPP11 on manganese-induced apoptosis and JNK pathway activation in PC12 cells, Brain Res, 1021, 241, 10.1016/j.brainres.2004.06.064 Hivert, 1998, Hydrogen peroxide-induced motoneuron apoptosis is prevented by poly ADP ribosyl synthetase inhibitors, NeuroReport, 9, 1835, 10.1097/00001756-199806010-00031 Hurley, 1987, Manganese Jana, 2014, Interleukin-12 (IL-12), but not IL-23, induces the expression of IL-7 in microglia and macrophages: implications for multiple sclerosis, Immunology, 141, 549, 10.1111/imm.12214 Jiang, 2014, Upregulation of mitochondrial protease HtrA2/Omi contributes to manganese-induced neuronal apoptosis in rat brain striatum, Neuroscience, 268, 169, 10.1016/j.neuroscience.2014.03.003 Kirkley, 2017, Microglia amplify inflammatory activation of astrocytes in manganese neurotoxicity, J Neuroinflammation, 14, 99, 10.1186/s12974-017-0871-0 Kreutzberg, 1996, Microglia: a sensor for pathological events in the CNS, Trends Neurosci, 19, 312, 10.1016/0166-2236(96)10049-7 Kroemer, 2007, Mitochondrial membrane permeabilization in cell death, Physiol Rev, 87, 99, 10.1152/physrev.00013.2006 Krysko, 2008, Apoptosis and necrosis: detection, discrimination and phagocytosis, Methods, 44, 205, 10.1016/j.ymeth.2007.12.001 Laakko, 2002, Versatility of merocyanine 540 for the flow cytometric detection of apoptosis in human and murine cells, J Immunol Methods, 261, 129, 10.1016/S0022-1759(01)00562-2 Li, 2010, Alpha-Synuclein overexpression during manganese-induced apoptosis in SH-SY5Y neuroblastoma cells, Brain Res Bull, 81, 428, 10.1016/j.brainresbull.2009.11.007 Lin, 2011, S-Adenosylhomocysteine enhances DNA damage through increased β-amyloid formation and inhibition of the DNA-repair enzyme OGG1b in microglial BV-2 cells, Toxicology, 290, 342, 10.1016/j.tox.2011.10.016 Lin, 2007, Synergistic effects of S-adenosylhomocysteine and homocysteine on DNA damage in a murine microglial cell line, Clin Chim Acta, 379, 139, 10.1016/j.cca.2007.01.007 Liu, 2006, Modulation of microglial pro-inflammatory and neurotoxic activity for the treatment of Parkinson’s disease, AAPS J, 8, E606, 10.1208/aapsj080369 Liu, 2009, Effects of S-adenosylhomocysteine and homocysteine on DNA damage and cell cytotoxicity in murine hepatic and microglia cell lines, J Biochem Mol Toxicol, 23, 349, 10.1002/jbt.20298 Liu, 2013, Complex II of the mitochondrial respiratory chain is the key mediator of divalent manganese-induced hydrogen peroxide production in microglia, Toxicol Sci, 132, 298, 10.1093/toxsci/kfs344 Lopez de Lapuente, 2016, Novel insights into the multiple sclerosis risk gene ANKRD55, J Immunol, 196, 4553, 10.4049/jimmunol.1501205 Love, 1999, Increased poly(ADP-ribosyl)ation of nuclear proteins in Alzheimer’s disease, Brain, 122, 247, 10.1093/brain/122.2.247 Lull, 2010, Microglial activation and chronic neurodegeneration, Neurotherapeutics, 7, 354, 10.1016/j.nurt.2010.05.014 Lund, 2006, The dynamics of the LPS triggered inflammatory response of murine microglia under different culture and in vivo conditions, J Neuroimmunol, 180, 71, 10.1016/j.jneuroim.2006.07.007 Ma, 2017, The role S-nitrosylation in manganese-induced autophagy dysregulation in SH-SY5Y cells, Environ Toxicol, 32, 2428, 10.1002/tox.22457 Maddirala, 2015, N-acetylcysteineamide protects against manganese-induced toxicity in SHSY5Y cell line, Brain Res, 1608, 157, 10.1016/j.brainres.2015.02.006 Mah, 2010, gammaH2AX: a sensitive molecular marker of DNA damage and repair, Leukemia, 24, 679, 10.1038/leu.2010.6 Malecki, 2001, Manganese toxicity is associated with mitochondrial dysfunction and DNA fragmentation in rat primary striatal neurons, Brain Res Bull Metals Brain, 55, 225, 10.1016/S0361-9230(01)00456-7 Mandir, 1999, Poly(ADP-ribose) polymerase activation mediates 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-induced parkinsonism, Proc Natl Acad Sci U S A, 96, 5774, 10.1073/pnas.96.10.5774 Martinez-Finley, 2013, Manganese neurotoxicity and the role of reactive oxygen species, Free Radical Biol Med, 62, 65, 10.1016/j.freeradbiomed.2013.01.032 Mauriz, 2013, A review of the molecular aspects of melatonin’s anti-inflammatory actions: recent insights and new perspectives, J Pineal Res, 54, 1, 10.1111/j.1600-079X.2012.01014.x Miramar, 2001, NADH oxidase activity of mitochondrial apoptosis-inducing factor, J Biol Chem, 276, 16391, 10.1074/jbc.M010498200 Mosmann, 1983, Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays, J Immunol Methods, 65, 55, 10.1016/0022-1759(83)90303-4 Moubarak, 2007, Sequential activation of poly(ADP-ribose) polymerase 1, calpains, and Bax is essential in apoptosis-inducing factor-mediated programmed necrosis, Mol Cell Biol, 27, 4844, 10.1128/MCB.02141-06 Nayak, 2014, Microglia development and function, Annu Rev Immunol, 32, 367, 10.1146/annurev-immunol-032713-120240 Nguyen, 2002, Innate immunity: the missing link in neuroprotection and neurodegeneration?, Nat Rev Neurosci, 3, 216, 10.1038/nrn752 Oh, 2017, 4-hydroxybenzaldehyde-chitooligomers suppresses H2O2-induced oxidative damage in microglia BV-2 cells, Carbohydr Res, 440–441, 32, 10.1016/j.carres.2017.01.007 O’Neal, 2015, Manganese toxicity upon overexposure: a decade in review, Curr Environ Health Rpt, 2, 315, 10.1007/s40572-015-0056-x Oikawa, 2006, Mechanism for manganese enhancement of dopamine-induced oxidative DNA damage and neuronal cell death, Free Radical Biol Med, 41, 748, 10.1016/j.freeradbiomed.2006.05.018 Outeiro, 2007, Pharmacological inhibition of PARP-1 reduces alpha-synuclein- and MPP+-induced cytotoxicity in Parkinson’s disease in vitro models, Biochem Biophys Res Commun, 357, 596, 10.1016/j.bbrc.2007.03.163 Page, 1993, A new fluorometric assay for cytotoxicity measurements in-vitro, Int J Oncol, 3, 473 Pangestuti, 2013, Fucoxanthin ameliorates inflammation and oxidative responses in microglia, J Agric Food Chem, 61, 3876, 10.1021/jf400015k Park, 2017, Protective effects of curcumin on manganese-induced BV-2 microglial cell death, Biol Pharm Bull, 40, 1275, 10.1248/bpb.b17-00160 Park, 2017, Melatonin attenuates manganese and lipopolysaccharide-induced inflammatory activation of BV2 microglia, Neurochem Res, 42, 656, 10.1007/s11064-016-2122-7 Park, 2010, Induction of oxidative stress and inflammatory cytokines by manganese chloride in cultured T98G cells, human brain glioblastoma cell line, Toxicol In Vitro, 24, 472, 10.1016/j.tiv.2009.09.022 Peres, 2016, Manganese-induced neurotoxicity: a review of its behavioral consequences and neuroprotective strategies, BMC Pharmacol Toxicol, 17, 57, 10.1186/s40360-016-0099-0 Porte Alcon, 2015, Vías de muerte celular inducida por Mn en células microgliales BV2, Medicina, 75, 108 Porte Alcon, 2014, El manganeso induce muerte celular y activación de las células microgliales murinas BV2, Medicina, 74, 175 Prabhakaran, 2009, BNIP3 up-regulation and mitochondrial dysfunction in manganese-induced neurotoxicity, Neurotoxicology, 30, 414, 10.1016/j.neuro.2009.02.012 Puli, 2006, Signaling pathways mediating manganese-induced toxicity in human glioblastoma cells (u87), Neurochem Res, 31, 1211, 10.1007/s11064-006-9178-8 Qin, 2015, Macrophage-microglia networks drive M1 microglia polarization after mycobacterium infection, Inflammation, 38, 1609, 10.1007/s10753-015-0136-y Reiter, 2016, Melatonin as an antioxidant: under promises but over delivers, J Pineal Res, 61, 253, 10.1111/jpi.12360 Rojo, 2014, Redox control of microglial function: molecular mechanisms and functional significance, Antioxid Redox Signal, 21, 1766, 10.1089/ars.2013.5745 Roth, 2009, Are there common biochemical and molecular mechanisms controlling manganism and parkisonism, Neuromol Med, 11, 281, 10.1007/s12017-009-8088-8 Sava, 2004, Effects of melanin and manganese on DNA damage and repair in PC12-derived neurons, Free Radical Biol Med, 36, 1144, 10.1016/j.freeradbiomed.2004.01.019 Seo, 2013, Iron depletion increases manganese uptake and potentiates apoptosis through ER stress, Neurotoxicology, 38, 67, 10.1016/j.neuro.2013.06.002 Serrano-Puebla, 2016, Lysosomal membrane permeabilization in cell death: new evidence and implications for health and disease, Ann N Y Acad Sci, 1371, 30, 10.1111/nyas.12966 Shen, 2016, Frataxin deficiency promotes excess microglial DNA damage and inflammation that is rescued by PJ34, PLoS One, 11 Smith, 2017, Redox dynamics of manganese as a mitochondrial life-death switch, Biochem Biophys Res Commun, 482, 388, 10.1016/j.bbrc.2016.10.126 Stansley, 2012, A comparative review of cell culture systems for the study of microglial biology in Alzheimer’s disease, J Neuroinflammation, 9, 115, 10.1186/1742-2094-9-115 Stephenson, 2013, Manganese-induced oxidative DNA damage in neuronal SH-SY5Y cells: attenuation of thymine base lesions by glutathione and N-acetylcysteine, Toxicol Lett, 218, 299, 10.1016/j.toxlet.2012.12.024 Susin, 1999, Molecular characterization of mitochondrial apoptosis-inducing factor, Nature, 397, 441, 10.1038/17135 Tait, 2010, Mitochondria and cell death: outer membrane permeabilization and beyond, Nat Rev Mol Cell Biol, 11, 621, 10.1038/nrm2952 Tait, 2014, Die another way–non-apoptotic mechanisms of cell death, J Cell Sci, 127, 2135, 10.1242/jcs.093575 Tamm, 2008, Mitochondrial-mediated apoptosis in neural stem cells exposed to manganese, Toxicol Sci, 101, 310, 10.1093/toxsci/kfm267 Tansey, 2008, Neuroinflammation in Parkinson’s disease: is there sufficient evidence for mechanism-based interventional therapy?, Front Biosci, 13, 709, 10.2741/2713 Tjalkens, 2017, Inflammatory activation of microglia and astrocytes in manganese neurotoxicity, Adv Neurobiol, 18, 159, 10.1007/978-3-319-60189-2_8 Tu, 2015, Amyloid-β activates microglia and regulates protein expression in a manner similar to prions, J Mol Neurosci, 56, 509, 10.1007/s12031-015-0553-2 Vanden Berghe, 2014, Regulated necrosis: the expanding network of non-apoptotic cell death pathways, Nat Rev Mol Cell Biol, 15, 135, 10.1038/nrm3737 Verina, 2011, Manganese exposure induces microglia activation and dystrophy in the substantia nigra of non-human primates, Neurotoxicology, 32, 215, 10.1016/j.neuro.2010.11.003 Vis, 2005, Expression pattern of apoptosis-related markers in Huntington’s disease, Acta Neuropathol, 109, 321, 10.1007/s00401-004-0957-5 Yin, 2008, Mitochondrial-dependent manganese neurotoxicity in rat primary astrocyte cultures, Brain Res, 1203, 1, 10.1016/j.brainres.2008.01.079 Yu, 2006, Apoptosis-inducing factor mediates poly(ADP-ribose) (PAR) polymer-induced cell death, Proc Natl Acad Sci U S A, 103, 18314, 10.1073/pnas.0606528103 Yu, 2002, Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor, Science, 297, 259, 10.1126/science.1072221 Yuste, 2005, Cysteine protease inhibition prevents mitochondrial apoptosis-inducing factor (AIF) release, Cell Death Differ, 12, 1445, 10.1038/sj.cdd.4401687 Zhang, 2016, PINK1/Parkin-mediated mitophagy play a protective role in manganese induced apoptosis in SH-SY5Y cells, Toxicol In Vitro, 34, 212, 10.1016/j.tiv.2016.04.006 Zhang, 1994, Nitric oxide activation of poly(ADP-ribose) synthetase in neurotoxicity, Science, 263, 687, 10.1126/science.8080500 Zhang, 2007, Manganese chloride stimulates rat microglia to release hydrogen peroxide, Toxicol Lett, 173, 88, 10.1016/j.toxlet.2007.06.013 Zhang, 2010, Synergistic dopaminergic neurotoxicity of manganese and lipopolysaccharide: differential involvement of microglia and astroglia, J Neurochem, 112, 434, 10.1111/j.1471-4159.2009.06477.x Zhang, 2009, Microglia enhance manganese chloride-induced dopaminergic neurodegeneration: role of free radical generation, Exp Neurol, 217, 219, 10.1016/j.expneurol.2009.02.013 Zhao, 2009, Manganese induces dopaminergic neurodegeneration via microglial activation in a rat model of manganism, Toxicol Sci, 107, 156, 10.1093/toxsci/kfn213 Zheng, 2013, Evaluation of the pathogenesis of meningitis caused by Streptococcus suis sequence type 7 using the infection of BV2 microglial cells, J Med Microbiol, 62, 360, 10.1099/jmm.0.046698-0