Maintained LTP and Memory Are Lost by Zn2+ Influx into Dentate Granule Cells, but Not Ca2+ Influx

Molecular Neurobiology - Tập 55 Số 2 - Trang 1498-1508 - 2018
Atsüshi Takeda1, Haruna Tamano1, Hisatsune Marie1, Taku Murakami1, Hiroyuki Nakada1, Hiroaki Fujii1
1Department of Neurophysiology, School of Pharmaceutical Sciences, University of Shizuoka, Shizuoka, Japan

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Tài liệu tham khảo

Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31–39

Malenka RC, Nicoll RA (1999) Long-term potentiation—a decade of progress? Science 285:1870–1874

Nicoll RA, Malenka RC (1995) Contrasting properties of two forms of long-term potentiation in the hippocampus. Nature 377:115–118

Takeda A, Tamano H, Ogawa T, Takada S, Nakamura M, Fujii H, Ando M (2014) Intracellular Zn2+ signaling in the dentate gyrus is required for object recognition memory. Hippocampus 24:1404–1412

Takeda A, Suzuki M, Tempaku M, Ohashi K, Tamano H (2015) Influx of extracellular Zn2+ into the hippocampal CA1 neurons is required for cognitive performance via long-term potentiation. Neuroscience 304:209–216

Danbolt NC (2001) Glutamate uptake. Prog Neurobiol 65:1–105

Dong XX, Wang Y, Qin ZH (2009) Molecular mechanisms of excitotoxicity and their relevance to pathogenesis of neurodegenerative diseases. Acta Pharmacol Sin 30:379–387

Lai TW, Zhang S, Wang YT (2014) Excitotoxicity and stroke: identifying novel targets for neuroprotection. Prog Neurobiol 115:157–188

Lewerenz J, Maher P (2015) Chronic glutamate toxicity in neurodegenerative diseases—what is the evidence? Front Neurosci 9:469

Lo EH, Dalkara T, Moskowitz MA (2003) Mechanisms, challenges and opportunities in stroke. Nat Rev Neurosci 4:399–415

Malairaman U, Dandapani K, Katyal A (2014) Effect of Ca2EDTA on zinc mediated inflammation and neuronal apoptosis in hippocampus of an in vivo mouse model of hypobaric hypoxia. PLoS One 9:e110253

Medvedeva YV, Weiss JH (2014) Intramitochondrial Zn2+ accumulation via the Ca2+ uniporter contributes to acute ischemic neurodegeneration. Neurobiol Dis 68:137–144

Colbourne F, Grooms SY, Zukin RS, Buchan AM, Bennett MV (2003) Hypothermia rescues hippocampal CA1 neurons and attenuates down-regulation of the AMPA receptor GluR2 subunit after forebrain ischemia. Proc Natl Acad Sci U S A 100:2906–2910

Frederickson CJ, Koh JY, Bush AI (2005) The neurobiology of zinc in health and disease. Nat Rev Neurosci 6:449–462

Noh KM, Yokota H, Mashiko T, Castillo PE, Zukin RS, Bennett MV (2005) Blockade of calcium-permeable AMPA receptors protects hippocampal neurons against global ischemia-induced death. Proc Nat Acad Sci USA 102:12230–12235

Stork CJ, Li YV (2009) Rising zinc: a significant cause of ischemic neuronal death in the CA1 region of rat hippocampus. J Cereb Blood Flow Metab 29:1399–1408

Suzuki M, Fujise Y, Tsuchiya Y, Tamano H, Takeda A (2015) Excess influx of Zn2+ into dentate granule cells affects object recognition memory via attenuated LTP. Neurochem Int 87:60–65

Takeda A, Takada S, Nakamura M, Suzuki M, Tamano H, Ando M, Oku N (2011) Transient increase in Zn2+ in hippocampal CA1 pyramidal neurons causes reversible memory deficit. PLoS One 6:e28615

Sindreu CB, Varoqui H, Erickson JD, Pérez-Clausell J (2003) Boutons containing vesicular zinc define a subpopulation of synapses with low AMPAR content in rat hippocampus. Cereb Cortex 13:823–829

Tamano H, Minamino T, Fujii H, Takada S, Nakamura M, Ando M, Takeda A (2015) Blockade of intracellular Zn2+ signaling in the dentate gyrus erases recognition memory via impairment of maintained LTP. Hippocampus 25:952–962

Hirano T, Kikuchi K, Urano Y, Nagano T (2002) Improvement and biological applications of fluorescent probes for zinc, ZnAFs. J Am Chem Soc 124:6555–6562

Ueno S, Tsukamoto M, Hirano T, Kikuchi K, Yamada MK, Nishiyama N, Nagano T, Matsuki N et al (2002) Mossy fiber Zn2+ spillover modulates heterosynaptic N-methyl-D-aspartate receptor activity in hippocampal CA3 circuits. J Cell Biol 158:215–220

Pastalkova E, Serrano P, Pinkhasova D, Wallace E, Fenton AA, Sacktor TC (2006) Storage of spatial information by the maintenance mechanism of LTP. Science 313:1141–1144

Choi DW, Koh JY (1998) Zinc and brain injury. Annu Rev Neurosci 21:347–375

Sensi SL, Canzoniero LM, Yu SP, Ying HS, Koh JY, Kerchner GA, Choi DW (1997) Measurement of intracellular free zinc in living cortical neurons: routes of entry. J Neurosci 17:9554–9564

Karst H, Berger S, Turiault M, Tronche F, Schütz G, Joëls M (2005) Mineralocorticoid receptors are indispensable for nongenomic modulation of hippocampal glutamate transmission by corticosterone. Proc Natl Acad Sci U S A 102:19204–19207

Takeda A, Suzuki M, Tamano H, Takada S, Ide K, Oku N (2012) Involvement of glucocorticoid-mediated Zn2+ signaling in attenuation of hippocampal CA1 LTP by acute stress. Neurochem Int 60:394–399

Hansen AZ, Zeuthen T (1981) Extracellular ion concentrations during spreading depression and ischemia in the rat brain cortex. Acta Physiol Scand 113:437–445

Liu D, Slevin JR, Lu C, Chan SL, Hansson M, Elmér E, Mattson MP (2003) Involvement of mitochondrial K+ release and cellular efflux in ischemic and apoptotic neuronal death. J Neurochem 86:966–979

Pagliusi SR, Gerrard P, Abdallah M, Talabot D, Catsicas S (1994) Age-related changes in expression of AMPA-selective glutamate receptor subunits: is calcium-permeability altered in hippocampal neurons? Neuroscience 61:429–433

Coelho BP, Giraldi-Guimarães A (2014) Effect of age and gender on recovery after stroke in rats treated with bone marrow mononuclear cells. Neurosci Res 88:67–73

Brickman AM, Khan UA, Provenzano FA, Yeung LK, Suzuki W, Schroeter H, Wall M, Sloan RP et al (2014) Enhancing dentate gyrus function with dietary flavanols improves cognition in older adults. Nat Neurosci 17:1798–1803

Small SA, Schobel SA, Buxton RB, Witter MP, Barnes CA (2011) A pathophysiological framework of hippocampal dysfunction in ageing and disease. Nat Rev Neurosci 12:585–601

Jinno S (2015) Aging affects new cell production in the adult hippocampus: a quantitative anatomic review. J Chem Neuroanat S0891-0618(15):00094–00090

Fukazawa Y, Saitoh Y, Ozawa F, Ohta Y, Mizuno K, Inokuchi K (2003) Hippocampal LTP is accompanied by enhanced F-actin content within the dendritic spine that is essential for late LTP maintenance in vivo. Neuron 38:447–460

McNaughton BL, Barnes CA (1997) Physiological identification and analysis of dentate granule cell responses to stimulation of the medial and lateral perforant pathways in the rat. J Comp Neurol 175:439–454

Colvin RA, Bush AI, Volitakis I, Fontaine CP, Thomas D, Kikuchi K, Holmes WR (2008) Insights into Zn2+ homeostasis in neurons from experimental and modeling studies. Am J Physiol Cell Physiol 294:C726–C742

Frederickson CJ, Giblin LJ, Krezel A, McAdoo DJ, Muelle RN, Zeng Y, Balaji RV, Masalha R et al (2006) Concentrations of extracellular free zinc (pZn)e in the central nervous system during simple anesthetization, ischemia and reperfusion. Exp Neurol 198:285–293

Hyrc K, Handran SD, Rothman SM, Goldberg MP (1997) Ionized intracellular calcium concentration predicts excitotoxic neuronal death: observations with low-affinity fluorescent calcium indicators. J Neurosci 17:6669–6677

Sensi SL, Paoletti P, Bush AI, Sekler I (2009) Zinc in the physiology and pathology of the CNS. Nat Rev Neurosci 10:780–791

Bouron A, Oberwinkler J (2014) Contribution of calcium-conducting channels to the transport of zinc ions. Pflugers Arch 466:381–387

Liu S, Lau L, Wei J, Zhu D, Zou S, Sun HS, Fu Y, Liu F et al (2004) Expression of Ca(2+)-permeable AMPA receptor channels primes cell death in transient forebrain ischemia. Neuron 43:43–55

Weiss JH (2011) Ca permeable AMPA channels in diseases of the nervous system. Front Mol Neurosci 4:42