Manganese nanoparticle activates mitochondrial dependent apoptotic signaling and autophagy in dopaminergic neuronal cells

Afeseh Ngwa, 2009, Vanadium induces dopaminergic neurotoxicity via protein kinase Cdelta dependent oxidative signaling mechanisms: relevance to etiopathogenesis of Parkinson's disease, Toxicol. Appl. Pharmacol., 240, 273, 10.1016/j.taap.2009.07.025 Anantharam, 2002, Caspase-3-dependent proteolytic cleavage of protein kinase Cdelta is essential for oxidative stress-mediated dopaminergic cell death after exposure to methylcyclopentadienyl manganese tricarbonyl, J. Neurosci., 22, 1738, 10.1523/JNEUROSCI.22-05-01738.2002 Anglade, 1997, Apoptosis and autophagy in nigral neurons of patients with Parkinson's disease, Histol. Histopathol., 12, 25 Aschner, 1991, Manganese neurotoxicity: cellular effects and blood–brain barrier transport, Neurosci. Biobehav. Rev., 15, 333, 10.1016/S0149-7634(05)80026-0 Aschner, 2005, Manganese dosimetry: species differences and implications for neurotoxicity, Crit. Rev. Toxicol., 35, 1, 10.1080/10408440590905920 Aschner, 2006, The Manganese Health Research Program (MHRP): status report and future research needs and directions, Neurotoxicology, 27, 733, 10.1016/j.neuro.2005.10.005 Auffan, 2009, Towards a definition of inorganic nanoparticles from an environmental, health and safety perspective, Nat. Nanotechnol., 4, 634, 10.1038/nnano.2009.242 Balshaw, 2005, Research strategies for safety evaluation of nanomaterials, part III: nanoscale technologies for assessing risk and improving public health, Toxicol. Sci., 88, 298, 10.1093/toxsci/kfi312 Borm, 2006, Research strategies for safety evaluation of nanomaterials, part V: role of dissolution in biological fate and effects of nanoscale particles, Toxicol. Sci., 90, 23, 10.1093/toxsci/kfj084 Braydich-Stolle, 2005, In vitro cytotoxicity of nanoparticles in mammalian germline stem cells, Toxicol. Sci., 88, 412, 10.1093/toxsci/kfi256 Cassarino, 1999, An evaluation of the role of mitochondria in neurodegenerative diseases: mitochondrial mutations and oxidative pathology, protective nuclear responses, and cell death in neurodegeneration, Brain Res. Brain Res. Rev., 29, 1, 10.1016/S0165-0173(98)00046-0 Chen, 2008, Oxidative stress induces autophagic cell death independent of apoptosis in transformed and cancer cells, Cell Death Differ., 15, 171, 10.1038/sj.cdd.4402233 Cheung, 2009, The emerging role of autophagy in Parkinson's disease, Mol. Brain, 2, 29, 10.1186/1756-6606-2-29 Clarkson, 1999, Immortalized dopamine neurons: a model to study neurotoxicity and neuroprotection, Proc. Soc. Exp. Biol. Med., 222, 157, 10.1046/j.1525-1373.1999.d01-126.x Cui, 2003, Advance and prospect of bionanomaterials, Biotechnol. Prog., 19, 683, 10.1021/bp025791i Dodel, 1999, Caspase-3-like proteases and 6-hydroxydopamine induced neuronal cell death, Brain Res. Mol. Brain Res., 64, 141, 10.1016/S0169-328X(98)00318-0 Erikson, 2004, Globus pallidus: a target brain region for divalent metal accumulation associated with dietary iron deficiency, J. Nutr. Biochem., 15, 335, 10.1016/j.jnutbio.2003.12.006 Gao, 2003, Novel anti-inflammatory therapy for Parkinson's disease, Trends Pharmacol. Sci., 24, 395, 10.1016/S0165-6147(03)00176-7 Guilarte, 2010, Manganese and Parkinson's disease: a critical review and new findings, Environ. Health Perspect., 118, 10.1289/ehp.0901748 Gunasekar, 2001, Mechanisms of the apoptotic and necrotic actions of trimethyltin in cerebellar granule cells, Toxicol. Sci., 64, 83, 10.1093/toxsci/64.1.83 HaMai, 2004, Oxidative basis of manganese neurotoxicity, Ann. N. Y. Acad. Sci., 1012, 129, 10.1196/annals.1306.010 Han, 2005, Electronic structure and magnetic properties of small manganese oxide clusters, J. Chem. Phys., 123, 34306, 10.1063/1.1953387 Hartmann, 2000, Caspase-3: a vulnerability factor and final effector in apoptotic death of dopaminergic neurons in Parkinson's disease, Proc. Natl. Acad. Sci. U. S. A., 97, 2875, 10.1073/pnas.040556597 Holsapple, 2005, Research strategies for safety evaluation of nanomaterials, part II: toxicological and safety evaluation of nanomaterials, current challenges and data needs, Toxicol. Sci., 88, 12, 10.1093/toxsci/kfi293 Hussain, 2005, In vitro toxicity of nanoparticles in BRL 3A rat liver cells, Toxicol. Vitr., 19, 975, 10.1016/j.tiv.2005.06.034 Hussain, 2006, The interaction of manganese nanoparticles with PC-12 cells induces dopamine depletion, Toxicol. Sci., 92, 456, 10.1093/toxsci/kfl020 Jayakumar, 2004, Combined effects of ammonia and manganese on astrocytes in culture, Neurochem. Res., 29, 2051, 10.1007/s11064-004-6878-9 Junn, 2001, Apoptotic signaling in dopamine-induced cell death: the role of oxidative stress, p38 mitogen-activated protein kinase, cytochrome c and caspases, J. Neurochem., 78, 374, 10.1046/j.1471-4159.2001.00425.x Kabeya, 2000, LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing, EMBO J., 19, 5720, 10.1093/emboj/19.21.5720 Kanthasamy, 2002, A novel oxidative stress-dependent apoptotic pathway in pesticide-induced dopaminergic degeneration: relevance to environmental factors and Parkinson's disease, J. Neurochem., 81, 76 Kanthasamy, 2003, Role of proteolytic activation of protein kinase C delta in oxidative stress-induced apoptosis, Antioxid. Redox Signal., 5, 609, 10.1089/152308603770310275 Kanthasamy, 2003, Proteolytic activation of proapoptotic kinase PKCdelta is regulated by overexpression of Bcl-2: implications for oxidative stress and environmental factors in Parkinson's disease, Ann. N. Y. Acad. Sci., 1010, 683, 10.1196/annals.1299.125 Kanthasamy, 2005, Dieldrin-induced neurotoxicity: relevance to Parkinson's disease pathogenesis, Neurotoxicology, 26, 701, 10.1016/j.neuro.2004.07.010 Kanthasamy, 2006, Methamphetamine induces autophagy and apoptosis in a mesencephalic dopaminergic neuronal culture model: role of cathepsin-D in methamphetamine-induced apoptotic cell death, Ann. N. Y. Acad. Sci., 1074, 234, 10.1196/annals.1369.022 Kanthasamy, 2010, Novel cell death signaling pathways in neurotoxicity models of dopaminergic degeneration: relevance to oxidative stress and neuroinflammation in Parkinson's disease, Neurotoxicology, 31, 555, 10.1016/j.neuro.2009.12.003 Kaul, 2003, Low dose oxidative insult promotes apoptosis in dopaminergic cells via caspase-3 dependent proteolytic activation of PKC delta: relevance to environmental factors and Parkinson's disease, Toxicol. Sci., 72, 79-79 Kaul, 2003, Caspase-3 dependent proteolytic activation of protein kinase C delta mediates and regulates 1-methyl-4-phenylpyridinium (MPP+)-induced apoptotic cell death in dopaminergic cells: relevance to oxidative stress in dopaminergic degeneration, Eur. J. Neurosci., 18, 1387, 10.1046/j.1460-9568.2003.02864.x Kaul, 2005, Tyrosine phosphorylation regulates the proteolytic activation of protein kinase Cdelta in dopaminergic neuronal cells, J. Biol. Chem., 280, 28721, 10.1074/jbc.M501092200 Kitazawa, 2001, Activation of oxidative stress-dependent cell signaling pathways in methylcyclopentadienyl manganese tricarbonyl (MMT)-induced apoptosis: downstream events and regulatory mechanisms Kitazawa, 2001, Dieldrin-induced oxidative stress and neurochemical changes contribute to apoptopic cell death in dopaminergic cells, Free Radic. Biol. Med., 31, 1473, 10.1016/S0891-5849(01)00726-2 Kitazawa, 2002, Oxidative stress and mitochondrial-mediated apoptosis in dopaminergic cells exposed to methylcyclopentadienyl manganese tricarbonyl, J. Pharmacol. Exp. Ther., 302, 26, 10.1124/jpet.302.1.26 Kitazawa, 2003, Translocation of protein kinase CS to mitochondria promotes proteolytic inactivation of Bcl-2 during MMT-induced apoptosis in dopaminergic cells, Neurotoxicology, 24, 305 Kitazawa, 2004, Dieldrin promotes proteolytic cleavage of poly(ADP-ribose) polymerase and apoptosis in dopaminergic cells: protective effect of mitochondrial anti-apoptotic protein Bcl-2, Neurotoxicology, 25, 589, 10.1016/j.neuro.2003.09.014 Kitazawa, 2005, Activation of protein kinase C delta by proteolytic cleavage contributes to manganese-induced apoptosis in dopaminergic cells: protective role of Bcl-2, Biochem. Pharmacol., 69, 133, 10.1016/j.bcp.2004.08.035 Klionsky, 2008, Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes, Autophagy, 4, 151, 10.4161/auto.5338 Kokoszka, 2001, Increased mitochondrial oxidative stress in the Sod2 (+/−) mouse results in the age-related decline of mitochondrial function culminating in increased apoptosis, Proc. Natl. Acad. Sci. U. S. A., 98, 2278, 10.1073/pnas.051627098 Konishi, 1997, Activation of protein kinase C by tyrosine phosphorylation in response to H2O2, Proc. Natl. Acad. Sci. U. S. A., 94, 11233, 10.1073/pnas.94.21.11233 Lam, 2004, Pulmonary toxicity of single-wall carbon nanotubes in mice 7 and 90days after intratracheal instillation, Toxicol. Sci., 77, 126, 10.1093/toxsci/kfg243 Latchoumycandane, 2005, Protein kinase Cdelta is a key downstream mediator of manganese-induced apoptosis in dopaminergic neuronal cells, J. Pharmacol. Exp. Ther., 313, 46, 10.1124/jpet.104.078469 Li, 2010, Autophagy and oxidative stress associated with gold nanoparticles, Biomaterials, 31, 5996, 10.1016/j.biomaterials.2010.04.014 Lloyd, 1995, Mechanism of the manganese-catalyzed autoxidation of dopamine, Chem. Res. Toxicol., 8, 111, 10.1021/tx00043a015 Maiuri, 2007, Functional and physical interaction between Bcl-X(L) and a BH3-like domain in Beclin-1, EMBO J., 26, 2527, 10.1038/sj.emboj.7601689 Maiuri, 2007, Self-eating and self-killing: crosstalk between autophagy and apoptosis, Nat. Rev. Mol. Cell Biol., 8, 741, 10.1038/nrm2239 Mao, 2007, Induction of microglial reactive oxygen species production by the organochlorinated pesticide dieldrin, Brain Res., 1186, 267, 10.1016/j.brainres.2007.10.020 Marquis, 2009, Analytical methods to assess nanoparticle toxicity, Analyst, 134, 425, 10.1039/b818082b Miranda, 2004, Multiple molecular determinants in the carboxyl terminus regulate dopamine transporter export from endoplasmic reticulum, J. Biol. Chem., 279, 30760, 10.1074/jbc.M312774200 Mizushima, 2007, How to interpret LC3 immunoblotting, Autophagy, 3, 542, 10.4161/auto.4600 Mizushima, 2010, Methods in mammalian autophagy research, Cell, 140, 313, 10.1016/j.cell.2010.01.028 Monteiro-Riviere, 2005, Multi-walled carbon nanotube interactions with human epidermal keratinocytes, Toxicol. Lett., 155, 377, 10.1016/j.toxlet.2004.11.004 Mukhopadhyay, 2007, Simple quantitative detection of mitochondrial superoxide production in live cells, Biochem. Biophys. Res. Commun., 358, 203, 10.1016/j.bbrc.2007.04.106 Nel, 2006, Toxic potential of materials at the nanolevel, Science, 311, 622, 10.1126/science.1114397 Oberdorster, 2004, Manufactured nanomaterials (fullerenes, C60) induce oxidative stress in the brain of juvenile largemouth bass, Environ. Health Perspect., 112, 1058, 10.1289/ehp.7021 Oberdorster, 1995, Association of particulate air pollution and acute mortality: involvement of ultrafine particles?, Inhal. Toxicol., 7, 111, 10.3109/08958379509014275 Oberdorster, 2005, Nanotoxicology: an emerging discipline evolving from studies of ultrafine particles, Environ. Health Perspect., 113, 823, 10.1289/ehp.7339 Olanow, 2004, Manganese-induced parkinsonism and Parkinson's disease, Ann. N. Y. Acad. Sci., 1012, 209, 10.1196/annals.1306.018 Oztap, 2003, A cell protective mechanism in a murine model of Parkinson's disease, Turk. J. Med. Sci., 33, 295 Park, 2006, Issues in neurological risk assessment for occupational exposures: the Bay Bridge welders, Neurotoxicology, 27, 373, 10.1016/j.neuro.2005.10.010 Pattingre, 2005, Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy, Cell, 122, 927, 10.1016/j.cell.2005.07.002 Peng, 2005, Alpha-synuclein activation of protein phosphatase 2A reduces tyrosine hydroxylase phosphorylation in dopaminergic cells, J. Cell Sci., 118, 3523, 10.1242/jcs.02481 Segura-Aguilar, 1989, On the mechanism of the Mn3(+)-induced neurotoxicity of dopamine: prevention of quinone-derived oxygen toxicity by DT diaphorase and superoxide dismutase, Chem. Biol. Interact., 72, 309, 10.1016/0009-2797(89)90006-9 Song, 2010, Environmental neurotoxic pesticide increases histone acetylation to promote apoptosis in dopaminergic neuronal cells: relevance to epigenetic mechanisms of neurodegeneration, Mol. Pharmacol., 77, 621, 10.1124/mol.109.062174 Sun, 2006, Proteasome inhibitor MG-132 induces dopaminergic degeneration in cell culture and animal models, Neurotoxicology, 27, 807, 10.1016/j.neuro.2006.06.006 Sun, 2008, Endocytosis of a single mesoporous silica nanoparticle into a human lung cancer cell observed by differential interference contrast microscopy, Anal. Bioanal. Chem., 391, 2119, 10.1007/s00216-008-2162-1 Tanida, 2008, LC3 and autophagy, Methods Mol. Biol., 445, 77, 10.1007/978-1-59745-157-4_4 Technology, T. P. s. C. o. A. o. S. a., 2010, Report to the President and Congress on the Third Assessment of the National Nanotechnology Initiative, 1 Teeguarden, 2007, Particokinetics in vitro: dosimetry considerations for in vitro nanoparticle toxicity assessments, Toxicol. Sci., 95, 300, 10.1093/toxsci/kfl165 Thomas, 2005, Research strategies for safety evaluation of nanomaterials, part I: evaluating the human health implications of exposure to nanoscale materials, Toxicol. Sci., 87, 316, 10.1093/toxsci/kfi270 Thomas, 2006, Research strategies for safety evaluation of nanomaterials, part VII: evaluating consumer exposure to nanoscale materials, Toxicol. Sci., 91, 14, 10.1093/toxsci/kfj129 Toh, 2008, Antioxidants: promising neuroprotection against cardiotoxin-4b-induced cell death which triggers oxidative stress with early calpain activation, Toxicon, 51, 964, 10.1016/j.toxicon.2007.11.019 Tsuji, 2006, Research strategies for safety evaluation of nanomaterials, part IV: risk assessment of nanoparticles, Toxicol. Sci., 89, 42, 10.1093/toxsci/kfi339 Warheit, 2007, Testing strategies to establish the safety of nanomaterials: conclusions of an ECETOC workshop, Inhal. Toxicol., 19, 631, 10.1080/08958370701353080 Wirawan, 2010, Caspase-mediated cleavage of Beclin-1 inactivates Beclin-1-induced autophagy and enhances apoptosis by promoting the release of proapoptotic factors from mitochondria, Cell Death Dis., 1, e18, 10.1038/cddis.2009.16 Wu, 2004, Labeling cellular targets with semiconductor quantum dot conjugates, Methods Cell Biol., 75, 171, 10.1016/S0091-679X(04)75007-4 Yang, 2004, Suppression of caspase-3-dependent proteolytic activation of protein kinase C delta by small interfering RNA prevents MPP+-induced dopaminergic degeneration, Mol. Cell. Neurosci., 25, 406, 10.1016/j.mcn.2003.11.011 Zhang, 2011, Effects of manganese on tyrosine hydroxylase (TH) activity and TH-phosphorylation in a dopaminergic neural cell line, Toxicol. Appl. Pharmacol., 254, 65, 10.1016/j.taap.2010.03.023