Intracellular zinc is a critical intermediate in the excitotoxic cascade

Neurobiology of Disease - Tập 81 - Trang 25-37 - 2015
Alberto Granzotto1,2, Stefano L. Sensi1,2,3,4
1Molecular Neurology Unit, Center of Excellence on Aging (Ce.S.I.), Chieti, Italy
2Department of Neuroscience and Imaging, University “G. D'Annunzio”, Chieti, Italy
3Departments of Neurology and Pharmacology, University of California-Irvine, Irvine, CA, USA
4Institute for Memory Impairment and Neurological Disorders, University of California-Irvine, Irvine, CA, USA

Tài liệu tham khảo

Aarts, 2002, Treatment of ischemic brain damage by perturbing NMDA receptor-PSD-95 protein interactions, Science, 298, 846, 10.1126/science.1072873 Aizenman, 2000, Induction of neuronal apoptosis by thiol oxidation: putative role of intracellular zinc release, J. Neurochem., 75, 1878, 10.1046/j.1471-4159.2000.0751878.x Ankarcrona, 1995, Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function, Neuron, 15, 961, 10.1016/0896-6273(95)90186-8 Bano, 2005, Cleavage of the plasma membrane Na+/Ca2+ exchanger in excitotoxicity, Cell, 120, 275, 10.1016/j.cell.2004.11.049 Beal, 1993, Neurochemical and histologic characterization of striatal excitotoxic lesions produced by the mitochondrial toxin 3-nitropropionic acid, J. Neurosci., 13, 4181, 10.1523/JNEUROSCI.13-10-04181.1993 Bidmon, 2001, Nitric oxide synthase-I containing cortical interneurons co-express antioxidative enzymes and anti-apoptotic Bcl-2 following focal ischemia: evidence for direct and indirect mechanisms towards their resistance to neuropathology, J. Chem. Neuroanat., 22, 167, 10.1016/S0891-0618(01)00126-0 Boillee, 2006, ALS: a disease of motor neurons and their nonneuronal neighbors, Neuron, 52, 39, 10.1016/j.neuron.2006.09.018 Bonanni, 2006, Zinc-dependent multi-conductance channel activity in mitochondria isolated from ischemic brain, J. Neurosci., 26, 6851, 10.1523/JNEUROSCI.5444-05.2006 Bossy-Wetzel, 2004, Crosstalk between nitric oxide and zinc pathways to neuronal cell death involving mitochondrial dysfunction and p38-activated K+ channels, Neuron, 41, 351, 10.1016/S0896-6273(04)00015-7 Brennan, 2009, NADPH oxidase is the primary source of superoxide induced by NMDA receptor activation, Nat. Neurosci., 12, 857, 10.1038/nn.2334 Canzoniero, 2013, nNOS(+) striatal neurons, a subpopulation spared in Huntington's Disease, possess functional NMDA receptors but fail to generate mitochondrial ROS in response to an excitotoxic challenge, Front. Physiol., 4, 112, 10.3389/fphys.2013.00112 Castilho, 1999, Oxidative stress, mitochondrial function, and acute glutamate excitotoxicity in cultured cerebellar granule cells, J. Neurochem., 72, 1394, 10.1046/j.1471-4159.1999.721394.x Choi, 1988, Glutamate neurotoxicity and diseases of the nervous system, Neuron, 1, 623, 10.1016/0896-6273(88)90162-6 Choi, 1992, Excitotoxic cell death, J. Neurobiol., 23, 1261, 10.1002/neu.480230915 Choi, 1996, Ischemia-induced neuronal apoptosis, Curr. Opin. Neurobiol., 6, 667, 10.1016/S0959-4388(96)80101-2 Clapham, 1995, Calcium signaling, Cell, 80, 259, 10.1016/0092-8674(95)90408-5 Clausen, 2013, Mechanisms of rapid reactive oxygen species generation in response to cytosolic Ca2+ or Zn2+ loads in cortical neurons, PLoS One, 8, e83347, 10.1371/journal.pone.0083347 Corona, 2011, New therapeutic targets in Alzheimer's disease: brain deregulation of calcium and zinc, Cell Death Dis., 2, e176, 10.1038/cddis.2011.57 Cowan, 2006, Selective neuronal degeneration in Huntington's disease, Curr. Top. Dev. Biol., 75, 25, 10.1016/S0070-2153(06)75002-5 Dawson, 1991, Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues, Proc. Natl. Acad. Sci. U. S. A., 88, 7797, 10.1073/pnas.88.17.7797 de la Fuente, 2012, Mitochondrial free [Ca(2+)] dynamics measured with a novel low-Ca(2+) affinity aequorin probe, Biochem. J., 445, 371, 10.1042/BJ20120423 Duchen, 2012, Mitochondria, calcium-dependent neuronal death and neurodegenerative disease, Pflugers Arch., 464, 111, 10.1007/s00424-012-1112-0 Dugan, 1995, Mitochondrial production of reactive oxygen species in cortical neurons following exposure to N-methyl-d-aspartate, J. Neurosci., 15, 6377, 10.1523/JNEUROSCI.15-10-06377.1995 Ferrante, 1985, Selective sparing of a class of striatal neurons in Huntington's disease, Science, 230, 561, 10.1126/science.2931802 Galluzzi, 2009, Mitochondrial membrane permeabilization in neuronal injury, Nat. Rev. Neurosci., 10, 481, 10.1038/nrn2665 Gee, 2002, Detection and imaging of zinc secretion from pancreatic beta-cells using a new fluorescent zinc indicator, J. Am. Chem. Soc., 124, 776, 10.1021/ja011774y Giacomello, 2007, Mitochondrial Ca2+ as a key regulator of cell life and death, Cell Death Differ., 14, 1267, 10.1038/sj.cdd.4402147 Gleichmann, 2011, Neuronal calcium homeostasis and dysregulation, Antioxid. Redox Signal., 14, 1261, 10.1089/ars.2010.3386 Gonzalez-Zulueta, 1998, Manganese superoxide dismutase protects nNOS neurons from NMDA and nitric oxide-mediated neurotoxicity, J. Neurosci., 18, 2040, 10.1523/JNEUROSCI.18-06-02040.1998 Group, H. s. D. C. R., 1993, A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes, Cell, 72, 971, 10.1016/0092-8674(93)90585-E He, 2002, Regulated and unregulated mitochondrial permeability transition pores: a new paradigm of pore structure and function?, FEBS Lett., 512, 1, 10.1016/S0014-5793(01)03314-2 Hope, 1991, Neuronal NADPH diaphorase is a nitric oxide synthase, Proc. Natl. Acad. Sci. U. S. A., 88, 2811, 10.1073/pnas.88.7.2811 Huntington Study Group Reach, H. D. I., 2015, Safety, tolerability, and efficacy of PBT2 in Huntington's disease: a phase 2, randomised, double-blind, placebo-controlled trial, Lancet Neurol., 14, 39, 10.1016/S1474-4422(14)70262-5 Hyrc, 2000, Ionic selectivity of low-affinity ratiometric calcium indicators: mag-Fura-2, Fura-2FF and BTC, Cell Calcium, 27, 75, 10.1054/ceca.1999.0092 Ichas, 1998, From calcium signaling to cell death: two conformations for the mitochondrial permeability transition pore. Switching from low- to high-conductance state, Biochim. Biophys. Acta, 1366, 33, 10.1016/S0005-2728(98)00119-4 Jiang, 2001, Zn(2+) induces permeability transition pore opening and release of pro-apoptotic peptides from neuronal mitochondria, J. Biol. Chem., 276, 47524, 10.1074/jbc.M108834200 Koh, 1987, Quantitative determination of glutamate mediated cortical neuronal injury in cell culture by lactate dehydrogenase efflux assay, J. Neurosci. Methods, 20, 83, 10.1016/0165-0270(87)90041-0 Koh, 1988, Vulnerability of cultured cortical neurons to damage by excitotoxins: differential susceptibility of neurons containing NADPH-diaphorase, J. Neurosci., 8, 2153, 10.1523/JNEUROSCI.08-06-02153.1988 Koh, 1986, Neurons containing NADPH-diaphorase are selectively resistant to quinolinate toxicity, Science, 234, 73, 10.1126/science.2875522 Koh, 1996, The role of zinc in selective neuronal death after transient global cerebral ischemia, Science, 272, 1013, 10.1126/science.272.5264.1013 Kowaltowski, 1996, Opening of the mitochondrial permeability transition pore by uncoupling or inorganic phosphate in the presence of Ca2+ is dependent on mitochondrial-generated reactive oxygen species, FEBS Lett., 378, 150, 10.1016/0014-5793(95)01449-7 Kowaltowski, 2001, Mitochondrial permeability transition and oxidative stress, FEBS Lett., 495, 12, 10.1016/S0014-5793(01)02316-X Krzywinski, 2014, Visualizing samples with box plots, Nat. Methods, 11, 119, 10.1038/nmeth.2813 Landwehrmeyer, 1995, NMDA receptor subunit mRNA expression by projection neurons and interneurons in rat striatum, J. Neurosci., 15, 5297, 10.1523/JNEUROSCI.15-07-05297.1995 Lau, 2010, Glutamate receptors, neurotoxicity and neurodegeneration, Pflugers Arch., 460, 525, 10.1007/s00424-010-0809-1 Maret, 1994, Oxidative metal release from metallothionein via zinc–thiol/disulfide interchange, Proc. Natl. Acad. Sci. U. S. A., 91, 237, 10.1073/pnas.91.1.237 Mattson, 1992, Beta-amyloid peptides destabilize calcium homeostasis and render human cortical neurons vulnerable to excitotoxicity, J. Neurosci., 12, 376, 10.1523/JNEUROSCI.12-02-00376.1992 McCord, 2013, Convergent Ca2+ and Zn2+ signaling regulates apoptotic Kv2.1K+ currents, Proc. Natl. Acad. Sci. U. S. A., 110, 13988, 10.1073/pnas.1306238110 McCord, 2014, The role of intracellular zinc release in aging, oxidative stress, and Alzheimer's disease, Front. Aging Neurosci., 6, 77, 10.3389/fnagi.2014.00077 McCormack, 1990, Role of calcium ions in regulation of mammalian intramitochondrial metabolism, Physiol. Rev., 70, 391, 10.1152/physrev.1990.70.2.391 Medvedeva, 2014, Intramitochondrial Zn2+ accumulation via the Ca2+ uniporter contributes to acute ischemic neurodegeneration, Neurobiol. Dis., 68, 137, 10.1016/j.nbd.2014.04.011 Medvedeva, 2009, Intracellular Zn2+ accumulation contributes to synaptic failure, mitochondrial depolarization, and cell death in an acute slice oxygen–glucose deprivation model of ischemia, J. Neurosci., 29, 1105, 10.1523/JNEUROSCI.4604-08.2009 Miller, 1998, Mitochondria — the Kraken wakes!, Trends Neurosci., 21, 95, 10.1016/S0166-2236(97)01206-X Nicholls, 2009, Mitochondrial calcium function and dysfunction in the central nervous system, Biochim. Biophys. Acta, 1787, 1416, 10.1016/j.bbabio.2009.03.010 Nicholls, 2004, The integration of mitochondrial calcium transport and storage, J. Bioenerg. Biomembr., 36, 277, 10.1023/B:JOBB.0000041753.52832.f3 Nydegger, 2010, Zinc is externalized rather than released during synaptic transmission, ACS Chem. Neurosci., 1, 728, 10.1021/cn100065s Olney, 1969, Brain lesions, obesity, and other disturbances in mice treated with monosodium glutamate, Science, 164, 719, 10.1126/science.164.3880.719 Palty, 2010, NCLX is an essential component of mitochondrial Na+/Ca2+ exchange, Proc. Natl. Acad. Sci. U. S. A., 107, 436, 10.1073/pnas.0908099107 Panov, 2002, Early mitochondrial calcium defects in Huntington's disease are a direct effect of polyglutamines, Nat. Neurosci., 5, 731, 10.1038/nn884 Paoletti, 2013, NMDA receptor subunit diversity: impact on receptor properties, synaptic plasticity and disease, Nat. Rev. Neurosci., 14, 383, 10.1038/nrn3504 Parsons, 2014, Extrasynaptic NMDA receptor involvement in central nervous system disorders, Neuron, 82, 279, 10.1016/j.neuron.2014.03.030 Pivovarova, 2014, The interactive roles of zinc and calcium in mitochondrial dysfunction and neurodegeneration, J. Neurochem., 128, 592, 10.1111/jnc.12489 Price, 1993, Nitric oxide synthase neurons in rat brain express more NMDA receptor mRNA than non-NOS neurons, Neuroreport, 4, 807, 10.1097/00001756-199306000-00053 Radford, 2013, Chelators for investigating zinc metalloneurochemistry, Curr. Opin. Chem. Biol., 17, 129, 10.1016/j.cbpa.2013.01.009 Rizzuto, 2003, Calcium and apoptosis: facts and hypotheses, Oncogene, 22, 8619, 10.1038/sj.onc.1207105 Rizzuto, 2012, Mitochondria as sensors and regulators of calcium signalling, Nat. Rev. Mol. Cell Biol., 13, 566, 10.1038/nrm3412 Robinson, 2006, Selective fluorescent imaging of superoxide in vivo using ethidium-based probes, Proc. Natl. Acad. Sci. U. S. A., 103, 15038, 10.1073/pnas.0601945103 Ross, 2011, Huntington's disease: from molecular pathogenesis to clinical treatment, Lancet Neurol., 10, 83, 10.1016/S1474-4422(10)70245-3 Rothman, 1986, Glutamate and the pathophysiology of hypoxic–ischemic brain damage, Ann. Neurol., 19, 105, 10.1002/ana.410190202 Rothstein, 1995, Selective loss of glial glutamate transporter GLT-1 in amyotrophic lateral sclerosis, Ann. Neurol., 38, 73, 10.1002/ana.410380114 Rudolf, 2003, Looking forward to seeing calcium, Nat. Rev. Mol. Cell Biol., 4, 579, 10.1038/nrm1153 Sattler, 1997, Determination of the time course and extent of neurotoxicity at defined temperatures in cultured neurons using a modified multiwell plate fluorescence scanner, J. Cereb. Blood Flow Metab., 17, 455, 10.1097/00004647-199704000-00011 Sattler, 1999, Specific coupling of NMDA receptor activation to nitric oxide neurotoxicity by PSD-95 protein, Science, 284, 1845, 10.1126/science.284.5421.1845 Schindelin, 2012, Fiji: an open-source platform for biological-image analysis, Nat. Methods, 9, 676, 10.1038/nmeth.2019 Schinder, 1996, Mitochondrial dysfunction is a primary event in glutamate neurotoxicity, J. Neurosci., 16, 6125, 10.1523/JNEUROSCI.16-19-06125.1996 Sensi, 1997, Measurement of intracellular free zinc in living cortical neurons: routes of entry, J. Neurosci., 17, 9554, 10.1523/JNEUROSCI.17-24-09554.1997 Sensi, 2000, AMPA/kainate receptor-triggered Zn2+ entry into cortical neurons induces mitochondrial Zn2+ uptake and persistent mitochondrial dysfunction, Eur. J. Neurosci., 12, 3813, 10.1046/j.1460-9568.2000.00277.x Sensi, 2003, Modulation of mitochondrial function by endogenous Zn2+ pools, Proc. Natl. Acad. Sci. U. S. A., 100, 6157, 10.1073/pnas.1031598100 Sensi, 2009, Zinc in the physiology and pathology of the CNS, Nat. Rev. Neurosci., 10, 780, 10.1038/nrn2734 Shuttleworth, 2011, Zinc: new clues to diverse roles in brain ischemia, Trends Pharmacol. Sci., 32, 480, 10.1016/j.tips.2011.04.001 Stout, 1998, Glutamate-induced neuron death requires mitochondrial calcium uptake, Nat. Neurosci., 1, 366, 10.1038/1577 Szabadkai, 2008, Mitochondria: the hub of cellular Ca2+ signaling, Physiology (Bethesda), 23, 84, 10.1152/physiol.00046.2007 Uemura, 1990, Selective sparing of NADPH-diaphorase–somatostatin–neuropeptide Y neurons in ischemic gerbil striatum, Ann. Neurol., 27, 620, 10.1002/ana.410270606 Vander Jagt, 2009, Intracellular Zn2+ increases contribute to the progression of excitotoxic Ca2+ increases in apical dendrites of CA1 pyramidal neurons, Neuroscience, 159, 104, 10.1016/j.neuroscience.2008.11.052 Vercesi, 1997, The role of reactive oxygen species in mitochondrial permeability transition, Biosci. Rep., 17, 43, 10.1023/A:1027335217774 Vergnano, 2014, Zinc dynamics and action at excitatory synapses, Neuron, 82, 1101, 10.1016/j.neuron.2014.04.034 Wang, 2002, NMDA-induced calcium loads recycle across the mitochondrial inner membrane of hippocampal neurons in culture, J. Neurophysiol., 87, 740, 10.1152/jn.00345.2001 Yu, 2001, Ion homeostasis and apoptosis, Curr. Opin. Cell Biol., 13, 405, 10.1016/S0955-0674(00)00228-3 Zhao, 2008, The zinc indicator FluoZin-3 is not perturbed significantly by physiological levels of calcium or magnesium, Cell Calcium, 44, 422, 10.1016/j.ceca.2008.01.006 Zorov, 2000, Reactive oxygen species (ROS)-induced ROS release: a new phenomenon accompanying induction of the mitochondrial permeability transition in cardiac myocytes, J. Exp. Med., 192, 1001, 10.1084/jem.192.7.1001