Mitochondrial Ca2+ Overload Underlies Aβ Oligomers Neurotoxicity Providing an Unexpected Mechanism of Neuroprotection by NSAIDs

PLoS ONE - Tập 3 Số 7 - Trang e2718
Sara Sanz‐Blasco1, Ruth A. Valero1, Ignacio Rodrı́guez-Crespo2, Carlos Villalobos1, Lucı́a Núñez1
1Instituto de Biología y Genética Molecular (IBGM), Universidad de Valladolid and Consejo Superior de Investigaciones Científicas (CSIC), Valladolid, Spain
2Departamento de Bioquímica y Biología Molecular, Facultad de Ciencias Químicas, Universidad Complutense de Madrid, Madrid, Spain

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J Wegiel, 1999, Cerebellar atrophy in Alzheimer's disease-clinicopathological correlations., Brain Res, 818, 41, 10.1016/S0006-8993(98)01279-7

JW Allen, 1999, Beta-amyloid-induced apoptosis of cerebellar granule cells and cortical neurons: exacerbation by selective inhibition of group I metabotropic glutamate receptors., Neuropharmacology, 38, 1243, 10.1016/S0028-3908(99)00044-1

N Canu, 2003, In vitro cultured neurons for molecular studies correlating apoptosis with events related to Alzheimer disease., Cerebellum, 2, 270, 10.1080/14734220310004289

LD Plant, 2006, Amyloid beta peptide as a physiological modulator of neuronal ‘A’-type K<sup>+</sup> current., Neurobiol Aging, 11, 1673, 10.1016/j.neurobiolaging.2005.09.038

PL McGeer, 2006, Inflammation, anti-inflammatory agents and Alzheimer disease: the last 12 years., J Alzheimers Dis, 9, 271, 10.3233/JAD-2006-9S330

L Canevari, 2004, Toxicity of amyloid beta peptide: tales of calcium mitochondria and oxidative stress., Neurochem Res, 29, 637, 10.1023/B:NERE.0000014834.06405.af

C Caspersen, 2005, Mitochondrial Abeta: a potential focal point for neuronal metabolic dysfunction in Alzheimer&apos;s disease., FASEB J, 19, 2040, 10.1096/fj.05-3735fje

M Manczak, 2006, Mitochondria are a direct site of A beta accumulation in Alzheimer&apos;s disease neurons: implications for free radical generation and oxidative damage in disease progression., Hum Mol Genet, 15, 1437, 10.1093/hmg/ddl066

PH Reddy, 2008, Amyloid beta, mitochondrial dysfunction and synaptic damage: implications for cognitive decline in aging and Alzheimer&apos;s disease., Trends Mol Med, 14, 45, 10.1016/j.molmed.2007.12.002

FM LaFerla, 2002, Calcium dyshomeostasis and intracellular signalling in Alzheimer&apos;s Disease., Nat Rev Neurosci, 3, 862, 10.1038/nrn960

AY Abramov, 2003, Changes in intracellular calcium and glutathione in astrocytes as the primary mechanism of amyloid neurotoxicity., J Neurosci, 23, 5088, 10.1523/JNEUROSCI.23-12-05088.2003

J Marx, 2007, Alzheimer&apos;s disease: Fresh evidence points to an old suspect: calcium., Science, 318, 384, 10.1126/science.318.5849.384

WL Klein, 2004, Small assemblies of unmodified amyloid beta-protein are the proximate neurotoxin in Alzheimer&apos;s disease., Neurobiol Aging, 25, 569, 10.1016/j.neurobiolaging.2004.02.010

C Haass, 2007, Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer&apos;s amyloid beta-peptide., Nat Rev Mol Cell Biol, 8, 101, 10.1038/nrm2101

Q Guo, 1998, Calbindin D28k blocks the proapoptotic actions of mutant presenilin 1: reduced oxidative stress and preserved mitochondrial function., Proc Natl Acad Sci USA, 95, 3227, 10.1073/pnas.95.6.3227

L Núñez, 2007, Bioluminescence imaging of mitochondrial Ca<sup>2+</sup> dynamics in soma and neurites of individual adult mouse sympathetic neurons., J Physiol, 580, 385, 10.1113/jphysiol.2006.126524

WL Klein, 2002, Abeta toxicity in Alzheimer&apos;s disease: globular oligomers (ADDLs) as new vaccine and drug targets., Neurochem Int, 41, 345, 10.1016/S0197-0186(02)00050-5

D Burdick, 1992, Assembly and aggregation properties of synthetic Alzheimer&apos;s A4/beta amyloid peptide analogs., J Biol Chem, 267, 546, 10.1016/S0021-9258(18)48529-8

M Kawahara, 2001, Intracellular calcium changes in neuronal cells induced by Alzheimer&apos;s beta-amyloid protein are blocked by estradiol and cholesterol., Cell Mol Neurobiol, 21, 1, 10.1023/A:1007168910582

KN Dahlgren, 2002, Oligomeric and fibrillar species of amyloid-beta peptides differentially affect neuronal viability., J Biol Chem, 277, 32046, 10.1074/jbc.M201750200

A Deshpande, 2006, Different conformations of amyloid beta induce neurotoxicity by distinct mechanisms in human cortical neurons., J Neurosci, 26, 6011, 10.1523/JNEUROSCI.1189-06.2006

C Villalobos, 2001, Mitochondrial [Ca<sup>2+</sup>] oscillations driven by local high [Ca<sup>2+</sup>] domains generated by spontaneous electric activity., J Biol Chem, 276, 40293, 10.1074/jbc.C100465200

C Villalobos, 2002, Redistribution of Ca<sup>2+</sup> among cytosol and organella during stimulation of bovine chromaffin cells., FASEB J, 16, 343, 10.1096/fj.01-0630com

M Montero, 2000, Chromaffin-cell stimulation triggers fast millimolar mitochondrial Ca<sup>2+</sup> transients that modulate secretion., Nat Cell Biol, 2, 57, 10.1038/35000001

KL Rogers, 2005, Visualization of local Ca<sup>2+</sup> dynamics with genetically encoded bioluminescent reporters., Eur J Neurosci, 21, 597, 10.1111/j.1460-9568.2005.03871.x

II Kruman, 1999, Pivotal role of mitochondrial calcium uptake in neural cell apoptosis and necrosis., J Neurochem, 72, 529, 10.1046/j.1471-4159.1999.0720529.x

MD Norenberg, 2007, The mitochondrial permeability transition in neurologic disease., Neurochem Int, 50, 983, 10.1016/j.neuint.2007.02.008

V Petronilli, 1998, Imaging the mitochondrial permeability transition pore in intact cells., Biofactors, 8, 263, 10.1002/biof.5520080314

L Núñez, 2006, Cell proliferation depends on mitochondrial Ca<sup>2+</sup> uptake: inhibition by salicylate., J Physiol, 571, 57, 10.1113/jphysiol.2005.100586

RA Valero, 2008, The role of mitochondrial potential in control of calcium signals involved in cell proliferation., Cell Calcium. In press

SG Voronina, 2004, Effects of secretagogues and bile acids on mitochondrial membrane potential of pancreatic acinar cells: comparison of different modes of evaluating DeltaPsim., J Biol Chem, 279, 27327, 10.1074/jbc.M311698200

Y Duan, 2007, Ca<sup>2+</sup>-dependent generation of mitochondrial reactive oxygen species serves as a signal for poly(ADP-ribose) polymerase-1 activation during glutamate excitotoxicity., J Physiol, 585, 741, 10.1113/jphysiol.2007.145409

JB Brocard, 2001, Quantitative evaluation of mitochondrial calcium content in rat cortical neurones following a glutamate stimulus., J Physiol, 531, 793, 10.1111/j.1469-7793.2001.0793h.x

A Demuro, 2005, Calcium dysregulation and membrane disruption as a ubiquitous neurotoxic mechanism of soluble amyloid oligomers., J Biol Chem, 280, 17294, 10.1074/jbc.M500997200

O Simakova, 2006, Early and late cytotoxic effects of external application of the Alzheimer&apos;s Abeta result from the initial formation and function of Abeta ion channels., Biochemistry, 45, 5907, 10.1021/bi060148g

N Arispe, 2007, Abeta ion channels: Prospects for treating Alzheimer&apos;s disease with Abeta channel blockers., Biochim Biophys Acta, 1768, 1952, 10.1016/j.bbamem.2007.03.014

FG De Felice, 2007, Abeta oligomers induce neuronal oxidative stress through an N-methyl-D-aspartate receptor-dependent mechanism that is blocked by the Alzheimer drug memantine., J Biol Chem, 282, 11590, 10.1074/jbc.M607483200

AE Palmer, 2006, Ca<sup>2+</sup> indicators based on computationally redesigned calmodulin-peptide pairs., Chem Biol, 13, 521, 10.1016/j.chembiol.2006.03.007

JM Dubinsky, 1998, Calcium-induced activation of the mitochondrial permeability transition in hippocampal neurons., J Neurosci Res, 53, 728, 10.1002/(SICI)1097-4547(19980915)53:6<728::AID-JNR10>3.0.CO;2-U

AK Stout, 1998, Glutamate-induced neuron death requires mitochondrial calcium uptake., Nat Neurosci, 1, 366, 10.1038/1577

NB Pivovarova, 2004, Excitotoxic calcium overload in a subpopulation of mitochondria triggers delayed death in hippocampal neurons., J Neurosci, 24, 5611, 10.1523/JNEUROSCI.0531-04.2004

BA In t' Veld, 2001, Nonsteroidal anti-inflammatory drugs and the risk of Alzheimer&apos;s disease., N Engl J Med, 345, 1515, 10.1056/NEJMoa010178

KP Townsend, 2005, Novel therapeutic opportunities for Alzheimer&apos;s disease: focus on nonsteroidal anti-inflammatory drugs., FASEB J, 19, 1592, 10.1096/fj.04-3620rev

S Weggen, 2001, A subset of NSAIDs lower amyloidogenic Abeta42 independently of cyclooxygenase activity., Nature, 414, 212, 10.1038/35102591

JL Eriksen, 2003, NSAIDs and enantiomers of flurbiprofen target gamma-secretase and lower Aβ<sub>42</sub> in vivo., J Clin Invest, 112, 440, 10.1172/JCI18162

T Mahmud, 1996, Nonsteroidal antiinflammatory drugs and uncoupling of mitochondrial oxidative phosphorylation., Arthritis Rheum, 39, 1998, 10.1002/art.1780391208

Y Kirichok, 2004, The mitochondrial calcium uniporter is a highly selective ion channel., Nature, 427, 360, 10.1038/nature02246

H Tu, 2006, Presenilins form ER Ca<sup>2+</sup> leak channels, a function disrupted by familial Alzheimer&apos;s disease-linked mutations., Cell, 126, 981, 10.1016/j.cell.2006.06.059

O Nelson, 2007, Familial Alzheimer disease-linked mutations specifically disrupt Ca<sup>2+</sup> leak function of presenilin 1., J Clin Invest, 117, 1230, 10.1172/JCI30447

GE Stutzmann, 2007, Enhanced ryanodine-mediated calcium release in mutant PS1-expressing Alzheimer&apos;s mouse models., Ann N Y Acad Sci, 1097, 265, 10.1196/annals.1379.025

G Zatti, 2006, Presenilin mutations linked to familial Alzheimer&apos;s disease reduce endoplasmic reticulum and Golgi apparatus calcium levels., Cell Calcium, 39, 539, 10.1016/j.ceca.2006.03.002

R Rizzuto, 1998, Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca<sup>2+</sup> responses., Science, 280, 1763, 10.1126/science.280.5370.1763

C Geula, 2003, Loss of calbindin-D28k from aging human cholinergic basal forebrain: relation to neuronal loss., J Comp Neurol, 455, 249, 10.1002/cne.10475

JJ Palop, 2003, Neuronal depletion of calcium-dependent proteins in the dentate gyrus is tightly linked to Alzheimer&apos;s disease-related cognitive deficits., Proc Natl Acad Sci USA, 100, 9572, 10.1073/pnas.1133381100

L Núñez, 1996, Mechanisms for synchronous calcium oscillations in cultured rat cerebellar neurons., Eur J Neurosci, 8, 192, 10.1111/j.1460-9568.1996.tb01180.x

TH Murphy, 1992, Spontaneous synchronous synaptic calcium transients in cultured cortical neurons., J Neurosci, 12, 4834, 10.1523/JNEUROSCI.12-12-04834.1992

GJ Brewer, 1993, Optimized survival of hippocampal neurons in B27-supplemented Neurobasal, a new serum-free medium combination., J Neurosci Res, 35, 567, 10.1002/jnr.490350513

I Pérez-Otaño, 2006, Endocytosis and synaptic removal of NR3A-containing NMDA receptors by PACSIN1/syndapin1., Nat Neurosci, 9, 611, 10.1038/nn1680

JE Bottestein, 1979, Growth of a rat neuroblastoma cell line in serum-free supplemented medium., Proc Natl Acad Sci USA, 76, 514, 10.1073/pnas.76.1.514

L Xie, 2005, Inhibition of NGF deprivation-induced death by low oxygen involves suppression of BIMEL and activation of HIF-1., J Cell Biol, 168, 911, 10.1083/jcb.200407079