Regulation of extracellular Zn²⁺ homeostasis in the hippocampus as a therapeutic target for Alzheimer’s disease

Bibliography

• Zola-Morgan SM, Squire LR. The primate hippocampal formation: evidence for a time-limited role in memory storage. Science 1990;250:288-90
   PubMed Web of Science ®Google Scholar
• Neves G, Cooke SF, Bliss TVP. Synaptic plasticity, memory and the hippocampus: a neural network approach to causality. Nat Rev Neurosci 2008;9:65-7
   PubMed Web of Science ®Google Scholar
• Frederickson CJ. Neurobiology of zinc and zinc-containing neurons. Int Rev Neurobiol 1989;31:145-238
   PubMed Web of Science ®Google Scholar
• Takeda A. Zinc signaling in the hippocampus and its relation to pathogenesis of depression. Mol Neurobiol 2011;44:167-74
   Google Scholar
• Takeda A, Tamano H. Insight into zinc signaling from dietary zinc deficiency. Brain Res Rev 2009;62:33-4
   PubMed Web of Science ®Google Scholar
• Takeda A, Tamano H. Cognitive decline due to excess synaptic Zn2+ signaling in the hippocampus. Front Aging Neurosci 2014;6:26
   PubMed Web of Science ®Google Scholar
• Takeda A, Tamano H, Ogawa T, et al. Intracellular Zn2+ signaling in the dentate gyrus is required for object recognition memory. Hippocampus 2014;24:1404-12
   Google Scholar
• Martinez-Guijarro FJ, Soriano E, Del Rio JA, et al. Zinc-positive boutons in the cerebral cortex of lizards show glutamate immunoreactivity. J Neurocytol 1991;20:834-43
   Google Scholar
• Nacher J, Palop JJ, Ramirez C, et al. Early histological maturation in the hippocampus of the guinea pig. Brain Behav Evol 2000;56:38-44
   Google Scholar
• Palmiter RD, Cole TB, Quaife CJ, et al. ZnT-3, a putative transporter of zinc into synaptic vesicles. Proc Natl Acad Sci USA 1996;93:14934-9
   PubMed Web of Science ®Google Scholar
• Frederickson CJ, Koh JY, Bush AI. The neurobiology of zinc in health and disease. Nat Rev Neurosci 2005;6:449-62
   PubMed Web of Science ®Google Scholar
• Takeda A. Insight into glutamate excitotoxicity from synaptic zinc homeostasis. Int J Alzheimers Dis 2011;2011:491597
   Google Scholar
• Jack CRJr, Petersen RC, Xu YC, et al. Prediction of AD with MRI-based hippocampal volume in mild cognitive impairment. Neurology 1999;52:1397-403
   PubMed Web of Science ®Google Scholar
• Wang PN, Lirng JF, Lin KN, et al. Prediction of Alzheimer’s disease in mild cognitive impairment: a prospective study in Taiwan. Neurobiol Aging 2006;27:1797-806
   PubMed Web of Science ®Google Scholar
• Hampel H, Burger K, Teipel SJ, et al. Core candidate neurochemical and imaging biomarkers of Alzheimer’s disease. Alzheimers Dement 2008;4:38-48
   PubMed Web of Science ®Google Scholar
• Selkoe DJ. Alzheimer’s disease: genes, proteins, and therapy. Physiol Rev 2001;81:741-66
   PubMed Web of Science ®Google Scholar
• Costa RO, Lacor PN, Ferreira IL, et al. Endoplasmic reticulum stress occurs downstream of GluN2B subunit of N-methyl-D-aspartate receptor in mature hippocampal cultures treated with amyloid-beta oligomers. Aging cell 2012;11:823-33
   Google Scholar
• Parameshwaran K, Dhanasekaran M, Suppiramaniam V. Amyloid beta peptides and glutamatergic synaptic dysregulation. Exp Neurol 2008;210:7-13
   PubMed Web of Science ®Google Scholar
• Kelly BL, Ferreira A. Beta-amyloid-induced dynamin 1 degradation is mediated by N-methyl-D-aspartate receptors in hippocampal neurons. J Biol Chem 2006;281:28079-89
   Google Scholar
• Hershey CO, Hershey LA, Varnes A, et al. Cerebrospinal fluid trace element content in dementia: clinical, radiologic, and pathologic correlations. Neurology 1983;33:1350-3
   PubMed Web of Science ®Google Scholar
• Weiss JH, Sensi SL, Koh JY, et al. Zn(2+): a novel ionic mediator of neural injury in brain disease. Trends Pharmacol Sci 2000;21:395-401
   PubMed Web of Science ®Google Scholar
• Frederickson CJ, Giblin LJ, Krezel A, et al. Concentrations of extracellular free zinc (pZn)e in the central nervous system during simple anesthetization, ischemia and reperfusion. Exp Neurol 2006;198:285-93
   PubMed Web of Science ®Google Scholar
• Minami A, Sakurada N, Fuke S, et al. Inhibition of presynaptic activity by zinc released from mossy fiber terminals during tetanic stimulation. J Neurosci Res 2006;83:167-76
   Google Scholar
• Sensi SL, Canzoniero LMT, Yu SP, et al. Measurement of intracellular free zinc in living cortical neurons: routes of entry. J Neurosci 1997;15:9554-64
   Google Scholar
• Colvin RA, Bush AI, Volitakis I, et al. Insights into Zn2+ homeostasis in neurons from experimental and modeling studies. Am J Physiol Cell Physiol 2008;294:C726-42
   Web of Science ®Google Scholar
• Takeda A, Itoh H, Tamano H, et al. Responsiveness to kainate in young rats after 2-week zinc deprivation. Biometals 2006;19:565-72
   Google Scholar
• Emmetsberger J, Mirrione MM, Zhou C, et al. Tissue plasminogen activator alters intracellular sequestration of zinc through interaction with the transporter ZIP4. J Neurosci 2010;30:6538-47
   PubMed Web of Science ®Google Scholar
• Sensi SL, Ton-That D, Sullivan PG, et al. Modulation of mitochondrial function by endogenous Zn2+ pools. Proc Natl Acad Sci USA 2003;100:6157-62
   PubMed Web of Science ®Google Scholar
• Colvin RA, Laskowski M, Fontaine CP. Zinquin identifies subcellular compartmentalization of zinc in cortical neurons. Relation to the trafficking of zinc and the mitochondrial compartment. Brain Res 2006;1085:1-10
   Google Scholar
• Lee JY, Kim JS, Byun HR, et al. Dependence of the histofluorescently reactive zinc pool on zinc transporter-3 in the normal brain. Brain Res 2011;1418:12-22
   Google Scholar
• Sekler I, Moran A, Hershfinkel M, et al. Distribution of the zinc transporter ZnT-1 in comparison with chelatable zinc in the mouse brain. J Comp Neurol 2002;447:201-9
   PubMed Web of Science ®Google Scholar
• Nolte C, Gore A, Sekler I, et al. ZnT-1 expression in astroglial cells protects against zinc toxicity and slows the accumulation of intracellular zinc. Glia 2004;48:145-55
   PubMedGoogle Scholar
• Fukada T, Kambe T. Molecular and genetic features of zinc transporters in physiology and pathogenesis. Metallomics 2011;3:662-74
   PubMed Web of Science ®Google Scholar
• Ueno S, Tsukamoto M, Hirano T, et al. Mossy fiber Zn2+ spillover modulates heterosynaptic N-methyl-D-aspartate receptor activity in hippocampal CA3 circuits. J Cell Biol 2002;158:215-20
   PubMed Web of Science ®Google Scholar
• Takeda A, Nakamura M, Fujii H, et al. Synaptic Zn2+ homeostasis and its significance. Metallomics 2013;5:417-23
   Google Scholar
• Hardy JA, Higgins GA. Alzheimer’s disease: the amyloid cascade hypothesis. Science 1992;256:184-5
   PubMed Web of Science ®Google Scholar
• Cirrito JR, May PC, O’Dell MA, et al. In vivo assessment of brain interstitial fluid with microdialysis reveals plaque-associated changes in amyloid-beta metabolism and half-life. J Neurosci 2003;23:8844-53
   PubMed Web of Science ®Google Scholar
• Morley J, Farr S, Banks M, et al. A physiological role for amyloid beta protein: enhancement of learning and memory. J Alzheimer Dis 2010;19:441-9
   PubMed Web of Science ®Google Scholar
• Cárdenas-Aguayo MC, Silva-Lucero MC, Cortes-Ortiz M, et al. Physiological role of amyloid beta in neural cells: the cellular trophic activity. INTECH; 2014. p. 1-24. Available from: http://www.intechopen.com/books/neurochemistry/physiological-role-of-amyloid-beta-in-neural-cells-the-cellular-trophic-activity
   Google Scholar
• Kayed R, Lasagna-Reeves CA. Molecular mechanisms of amyloid oligomers toxicity. J. Alzheimers Dis 2013;33:S67-78
   PubMed Web of Science ®Google Scholar
• Lambert MP, Barlow AK, Chromy BA, et al. Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc Natl Acad Sci USA 1998;95:6448-53
   PubMed Web of Science ®Google Scholar
• Walsh DM, Klyubin I, Fadeeva JV, et al. Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 2002;416:535-9
   PubMed Web of Science ®Google Scholar
• Zhao D, Watson JB, Xie CW. Amyloid beta prevents activation of calcium/calmodulin-dependent protein kinase II and AMPA receptor phosphorylation during hippocampal long-term potentiation. J Neurophysiol 2004;92:2853-8
   Google Scholar
• Cleary JP, Walsh DM, Hofmeister JJ, et al. Natural oligomers of the amyloid-beta protein specifically disrupt cognitive function. Nat Neurosci 2005;8:79-84
   PubMed Web of Science ®Google Scholar
• Holscher C, Gengler S, Gault VA, et al. Soluble beta-amyloid [25–35] reversibly impairs hippocampal synaptic plasticity and spatial learning. Eur J Pharmacol 2007;561:85-90
   PubMed Web of Science ®Google Scholar
• Watt NT, Whitehouse IJ, Hooper NM. The role of zinc in Alzheimer’s disease. Int J Alzheimers Dis 2011;2011:1-10
   Google Scholar
• Lovell MA, Robertson JD, Teesdale WJ, et al. Copper, iron and zinc in Alzheimer’s disease senile plaques. J Neurol Sci 1998;158:47-52
   PubMed Web of Science ®Google Scholar
• Lee JY, Cole TB, Palmiter RD, et al. Contribution by synaptic zinc to the gender-disparate plaque formation in human Swedish mutant APP transgenic mice. Proc Natl Acad Sci USA 2002;99:7705-10
   PubMed Web of Science ®Google Scholar
• Bush AI, Pettingell WH, Multhaup G, et al. Rapid induction of Alzheimer A beta amyloid formation by zinc. Science 1994;265:1464-7
   PubMed Web of Science ®Google Scholar
• Hane F, Leonenko Z. Effect of metals on kinetic pathways of amyloid-beta aggregation. Biomolecules 2014;4:101-16
   PubMedGoogle Scholar
• Mantyh PW, Ghilardi JR, Rogers S, et al. Aluminum, iron, and zinc ions promote aggregation of physiological concentrations of beta-Amyloid peptide. J Neurochem 1993;61:1171-4
   PubMed Web of Science ®Google Scholar
• Noy D, Solomonov I, Sinkevich O, et al. Zinc-amyloid beta interactions on a millisecond time-scale stabilize non-fibrillar Alzheimer-related species. J Am Chem Soc 2008;130:1376-83
   PubMedGoogle Scholar
• Pan L, Patterson JC. Molecular dynamics study of Zn(Abeta) and Zn(Abeata)2. PLoS One 2013;8:e70681
   PubMedGoogle Scholar
• Sensi SL, Paoletti P, Bush AI, et al. Zinc in the physiology and pathology of the CNS. Nat Rev Neurosci 2009;10:780-91
   PubMed Web of Science ®Google Scholar
• Bush AI, Tanzi RE. The galvanization of beta-amyloid in Alzheimer’s disease. Proc Natl Acad Sci USA 2002;99:7317-19
   PubMed Web of Science ®Google Scholar
• Li S, Hong S, Shepardson NE, et al. Soluble oligomers of amyloid beta protein facilities hippocampal long-term depression by disrupting neuronal glutamate uptake. Neuron 2009;62:788-801
   PubMed Web of Science ®Google Scholar
• Kabogo D, Rauw G, Amritraj A, et al. Beta-amyloid-related peptides potentiate K+-evoked glutamate release from adult rat hippocampal slices. Neurobiol Aging 2010;31:1164-72
   Google Scholar
• Brito-Moreira J, Paula-Lima AC, Bomfim TR, et al. Abeta oligomers induce glutamate release from hippocampal neurons. Curr Alzheimer Res 2011;8:552-62
   PubMed Web of Science ®Google Scholar
• Li S, Jin M, Koeglsperger T, et al. Soluble Abeta oligomers inhibit long-term potentiation through a mechanism involving excessive activation of extrasynaptic NR2B-containing NMDA receptors. J Neurosci 2011;31:6627-38
   PubMed Web of Science ®Google Scholar
• Deshpande A, Kawai H, Metherate R, et al. A role for synaptic zinc in activity-dependent Abeta oligomer formation and accumulation at excitatory synapses. J Neurosci 2009;29:4004-15
   PubMed Web of Science ®Google Scholar
• Barili P, Fringuelli C, Ricci A, et al. Age-related changes of sulphide-silver staining in the rat hippocampus. Mech Aging Dev 1997;99:83-94
   Google Scholar
• Adlard PA, Parncutt JM, Finkelstein DI, et al. Cognitive loss in zinc transporter-3 knock-out mice: a phenocopy for the synaptic and memory deficits of Alzheimer’s disease? J Neurosci 2009;29:4004-15
   Google Scholar
• Sensi SL, Paoletti P, Koh JY, et al. The neurophysiology and pathology of brain zinc. J Neurosci 2011;31:16076-85
   PubMed Web of Science ®Google Scholar
• Ritchie CW, Bush AI, Mackinnon A, et al. Metal-protein attenuation with iodochlorhydroxyquin (clioquinol) targeting Abeta amyloid deposition and toxicity in Alzheimer disease: a pilot phase 2 clinical trial. Arch Neurol 2003;60:1685-91
   PubMed Web of Science ®Google Scholar
• Faux NG, Ritchie CW, Gunn A, et al. PBT2 rapidly improves cognition in Alzheimer’s Disease: additional phase II analyses. J Alzheimers Dis 2010;20:509-16
   PubMed Web of Science ®Google Scholar
• Gomez-Isla T, Price JL, McKeel DWJr, et al. Profound loss of layer II entorhinal cortex neurons occurs in very mild Alzheimer’s disease. J Neurosci 1996;16:4491-500
   PubMed Web of Science ®Google Scholar
• Scheff SW, Price DA, Schmitt FA, et al. Hippocampal synaptic loss in early Alzheimer’s disease and mild cognitive impairment. Neurobiol Aging 2006;27:1372-84
   PubMed Web of Science ®Google Scholar
• Crews L, Masliah E. Molecular mechanisms of neurodegeneration in Alzheimer’s disease. Hum Mol Genet 2010;19:R12-20
   PubMed Web of Science ®Google Scholar
• Brouillette J, Caillierez R, Zommer N, et al. Neurotoxicity and memory deficits induced by soluble low-molecular-weight amyloid-beta1-42 oligomers are revealed in vivo by using a novel animal model. J Neurosci 2012;32:7852-61
   PubMed Web of Science ®Google Scholar
• Hyman BT, Van Hoesen GW, Damasio AR, et al. Alzheimer’s disease: cell-specific pathology isolates the hippocampal formation. Science 1984;225:1168-70
   PubMed Web of Science ®Google Scholar
• Nestor PJ, Scheltens P, Hodges JR. Advances in the early detection of Alzheimer’s disease. Nat Med 2004;10:S34-41
   PubMed Web of Science ®Google Scholar
• Takeda A, Nakamura M, Fujii H, et al. Amyloid beta-mediated Zn2+ influx into dentate granule cells transiently induces a short-term cognitive deficit. PLoS One 2014;9:e115923
   Google Scholar
• Morrison JH, Hof PR. Life and death of neurons in the aging brain. Science 1997;278:412-19
   PubMed Web of Science ®Google Scholar
• Takamura Y, Ono K, Matsumoto J, et al. Effects of the neurotrophic agent T-817MA on oligomeric amyloid-beta-induced deficits in long-term potentiation in the hippocampal CA1 subfield. Neurobiol Aging 2014;35:532-6
   PubMed Web of Science ®Google Scholar
• Li S, Hong S, Shepardson NE, et al. Soluble oligomers of amyloid beta protein facilitate hippocampal long-term depression by disrupting neuronal glutamate uptake. Neuron 2009;62:788-801
   PubMed Web of Science ®Google Scholar
• Lesné S, Koh MT, Kotilinek L, et al. A specific amyloid-beta protein assembly in the brain impairs memory. Nature 2006;440:352-7
   PubMed Web of Science ®Google Scholar
• Shankar GM, Li S, Mehta TH, et al. Amyloid-beta protein dimers isolated directly from Alzheimer’s brains impair synaptic plasticity and memory. Nat Med 2008;14:837-42
   PubMed Web of Science ®Google Scholar
• Selkoe DJ. Alzheimer’s disease is a synaptic failure. Science 2002;298:789-91
   PubMed Web of Science ®Google Scholar
• Takeda A, Takada S, Nakamura M, et al. Transient increase in Zn2+ in hippocampal CA1 pyramidal neurons causes reversible memory deficit. PLoS One 2011;6:e28615
   Google Scholar
• Wang T, Wang CY, Shan ZY, et al. Clioquinol reduces zinc accumulation in neuritic plaques and inhibits the amyloidogenic pathway in AbetaPP/PS1 transgenic mouse brain. J Alzheimers Dis 2012;29:549-59
   PubMedGoogle Scholar
• Matlack KE, Tardiff DF, Narayan P, et al. Clioquinol promotes the degradation of metal-dependent amyloid-beta (Abeta) oligomers to restore endocytosis and ameliorate Abeta toxicity. Proc Natl Acad Sci USA 2014;111:4013-18
   Google Scholar
• Zhang YH, Raymick J, Sarkar S, et al. Efficacy and toxicity of clioquinol treatment and A-beta42 inoculation in the APP/PSI mouse model of Alzheimer’s disease. Curr Alzheimer Res 2013;10:494-506
   PubMedGoogle Scholar
• Wang Z, Wang Y, Li W, et al. Design, synthesis, and evaluation of multitarget-directed selenium-containing clioquinol derivatives for the treatment of Alzheimer’s disease. ACS Chem Neurosci 2014;5:952-62
   PubMed Web of Science ®Google Scholar
• Lannfelt L, Blennow K, Zetterberg H, et al. Safety, efficacy, and biomarker findings of PBT2 in targeting Abeta as a modifying therapy for Alzheimer’s disease: a phase IIa, double-blind, randomised, placebo-controlled trial. Lancet Neurol 2008;7:779-86
   PubMed Web of Science ®Google Scholar
• Ayton S, Lei P, Bush AI. Biometals and their therapeutic implications in Alzheimer’s disease. Neurotherapeutics 2015;12:109-20
   PubMed Web of Science ®Google Scholar