Endogenous zinc depresses GABAergic transmission via T-type Ca(2+) channels and broadens the time window for integration of glutamatergic inputs in dentate granule cells
Engel, Dominique ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Pharmacologie
Ruiz, AJ
Language :
English
Title :
Endogenous zinc depresses GABAergic transmission via T-type Ca(2+) channels and broadens the time window for integration of glutamatergic inputs in dentate granule cells
Publication date :
01 January 2014
Journal title :
Journal of Physiology
ISSN :
0022-3751
eISSN :
1469-7793
Publisher :
Blackwell Publishing, New York, United States - New York
Acsady L, Kamondi A, Sik A, Freund T & Buzsaki G (1998). GABAergic cells are the major postsynaptic targets of mossy fibers in the rat hippocampus. J Neurosci 18, 3386-3403.
Aizenman E, Stout AK, Hartnett KA, Dineley KE, McLaughlin B & Reynolds IJ (2000). Induction of neuronal apoptosis by thiol oxidation: putative role of intracellular zinc release. J Neurochem 75, 1878-1888.
Alle H, Jonas P & Geiger JR (2001). PTP and LTP at a hippocampal mossy fibre-interneuron synapse. Proc Natl Acad Sci U S A 98, 14708-14713.
Barberis A, Cherubini E & Mozrzymas JW (2000). Zinc inhibits miniature GABAergic currents by allosteric modulation of GABAA receptor gating. J Neurosci 20, 8618-8627.
Barrett JN & Crill WE (1974). Influence of dendritic location and membrane properties on the effectiveness of synapses on cat motoneurones. J Physiol 239, 325-345.
Bartos M, Alle H & Vida I (2011). Role of microcircuit structure and input integration in hippocampal interneuron recruitment and plasticity. Neuropharmacology 60, 730-739.
Bartos M, Vida I & Jonas P (2007). Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat Rev Neurosci 8, 45-56.
Bean BP (2007). The action potential in mammalian central neurons. Nat Rev Neurosci 8, 451-465.
Berger T, Schwarz C, Kraushaar U & Monyer H (1998). Dentate gyrus basket cell GABAA receptors are blocked by Zn2+ via changes of their desensitization kinetics: an in situ patch-clamp and single-cell PCR study. J Neurosci 18, 2437-2448.
Blasco-Ibanez JM, Martinez-Guijarro FJ & Freund TF (2000). Recurrent mossy fibers preferentially innervate parvalbumin-immunoreactive interneurons in the granule cell layer of the rat dentate gyrus. Neuroreport 11, 3219-3225.
Brandt A, Khimich D & Moser T (2005). Few Cav1.3 channels regulate the exocytosis of a synaptic vesicle at the hair cell ribbon synapse. J Neurosci 25, 11577-11585.
Buhl EH, Otis TS & Mody I (1996). Zinc-induced collapse of augmented inhibition by GABA in a temporal lobe epilepsy model. Science 271, 369-373.
Busselberg D, Platt B, Michael D, Carpenter DO & Haas HL (1994). Mammalian voltage-activated Ca2+ channel currents are blocked by Pb2+, Zn2+, and Al3+. J Neurophysiol 71, 1491-1497.
Buzsaki G (1984). Feed-forward inhibition in the hippocampal formation. Prog Neurobiol 22, 131-153.
Calixto E, Galvan EJ, Card JP & Barrionuevo G (2008). Coincidence detection of convergent perforant path and mossy fibre inputs by CA3 interneurons. J Physiol 586, 2695-2712.
Chiang PH, Wu PY, Kuo TW, Liu YC, Chan CF, Chien TC, Cheng JK, Huang YY, Chiu CD & Lien CC (2012). GABA is depolarizing in hippocampal dentate granule cells of the adolescent and adult rats. J Neurosci 32, 62-67.
Cueni L, Canepari M, Adelman JP & Luthi A (2009). Ca2+ signalling by T-type Ca2+ channels in neurons. Pflugers Arch 457, 1161-1172.
Doherty JJ, Alagarsamy S, Bough KJ, Conn PJ, Dingledine R & Mott DD (2004). Metabotropic glutamate receptors modulate feedback inhibition in a developmentally regulated manner in rat dentate gyrus. J Physiol 561, 395-401.
Duce JA, Tsatsanis A, Cater MA, James SA, Robb E, Wikhe K, Leong SL, Perez K, Johanssen T, Greenough MA, Cho HH, Galatis D, Moir RD, Masters CL, McLean C, Tanzi RE, Cappai R, Barnham KJ, Ciccotosto GD, Rogers JT & Bush AI (2010). Iron-export ferroxidase activity of beta-amyloid precursor protein is inhibited by zinc in Alzheimer's disease. Cell 142, 857-867.
Ewell LA & Jones MV (2010). Frequency-tuned distribution of inhibition in the dentate gyrus. J Neurosci 30, 12597-12607.
Freund TF & Buzsaki G (1996). Interneurons of the hippocampus. Hippocampus 6, 347-470.
Geiger JR, Lubke J, Roth A, Frotscher M & Jonas P (1997). Submillisecond AMPA receptor-mediated signalling at a principal neuron-interneuron synapse. Neuron 18, 1009-1023.
Gielen M, Siegler Retchless B, Mony L, Johnson JW & Paoletti P (2009). Mechanism of differential control of NMDA receptor activity by NR2 subunits. Nature 459, 703-707.
Goldberg JH, Lacefield CO & Yuste R (2004). Global dendritic Ca2+ spikes in mouse layer 5 low threshold spiking interneurones: implications for control of pyramidal cell bursting. J Physiol 558, 465-478.
Gu Y, Barry J & Gu C (2013). Kv3 channel assembly, trafficking and activity are regulated by zinc through different binding sites. J Physiol 591, 2491-2507.
Hershfinkel M, Kandler K, Knoch ME, Dagan-Rabin M, Aras MA, Abramovitch-Dahan C, Sekler I & Aizenman E (2009). Intracellular zinc inhibits KCC2 transporter activity. Nat Neurosci 12, 725-727.
Huang L, Keyser BM, Tagmose TM, Hansen JB, Taylor JT, Zhuang H, Zhang M, Ragsdale DS & Li M (2004). NNC 55-0396 [(1S, 2S)-2-(2-(N-[(3-benzimidazol-2-yl)propyl]-N-methylamino)ethyl)-6-fluoro-1, 2, 3, 4-tetrahydro-1-isopropyl-2-naphtyl cyclopropanecarboxylate dihydrochloride]: a new selective inhibitor of T-type Ca2+ channels. J Pharm Exp Ther 309, 193-199.
Huang YZ, Pan E, Xiong ZQ & McNamara JO (2008). Zinc-mediated transactivation of TrkB potentiates the hippocampal mossy fibre-CA3 pyramid synapse. Neuron 57, 546-558.
Huang Z, Lujan R, Kadurin I, Uebele VN, Renger JJ, Dolphin AC & Shah MM (2011). Presynaptic HCN1 channels regulate Cav3.2 activity and neurotransmission at select cortical synapses. Nat Neurosci 14, 478-486.
Imbrici P, D'Adamo MC, Cusimano A & Pessia M (2007). Episodic ataxia type 1 mutation F184C alters Zn2+-induced modulation of the human K+ channel KV1.4-KV1.1/KVbeta1.1. Am J Physiol Cell Physiol 292, C778-C787.
Kapur J, Haas KF & Macdonald RL (1999). Physiological properties of GABAA receptors from acutely dissociated rat dentate granule cells. J Neurophysiol 81, 2464-2471.
Kerr AM & Capogna M (2007). Unitary IPSPs enhance hilar mossy cell gain in the rat hippocampus. J Physiol 578, 451-470.
Kodirov SA, Takizawa S, Joseph J, Kandel ER, Shumyatsky GP & Bolshakov VY (2006). Synaptically released zinc gates long-term potentiation in fear conditioning pathways. Proc Natl Acad Sci U S A 103, 15218-15223.
Koh DS, Geiger JR, Jonas P & Sakmann B (1995). Ca2+-permeable AMPA and NMDA receptor channels in basket cells of rat hippocampal dentate gyrus. J Physiol 485, 383-402.
Kraushaar U & Jonas P (2000). Efficacy and stability of quantal GABA release at a hippocampal interneuron-principal neuron synapse. J Neurosci 20, 5594-5607.
Magee JC & Johnston D (1995). Synaptic activation of voltage-gated channels in the dendrites of hippocampal pyramidal neurons. Science 268, 301-304.
Mayer ML & Vyklicky L Jr (1989). The action of zinc on synaptic transmission and neuronal excitability in cultures of mouse hippocampus. J Physiol 415, 351-365.
McDonough SI & Bean BP (1998). Mibefradil inhibition of T-type Ca2+ channels in cerebellar Purkinje neurons. Mol Pharmacol 54, 1080-1087.
McKay BE, McRory JE, Molineux ML, Hamid J, Snutch TP, Zamponi GW & Turner RW (2006). Cav3 T-type Ca2+ channel isoforms differentially distribute to somatic and dendritic compartments in rat central neurons. Eur J Neurosci 24, 2581-2594.
Misgeld U, Deisz RA, Dodt HU & Lux HD (1986). The role of chloride transport in postsynaptic inhibition of hippocampal neurons. Science 232, 1413-1415.
Mitchell SJ & Silver RA (2003). Shunting inhibition modulates neuronal gain during synaptic excitation. Neuron 38, 433-445.
Molnar P & Nadler JV (2001a). Synaptically-released zinc inhibits N-methyl-d-aspartate receptor activation at recurrent mossy fibre synapses. Brain Res 910, 205-207.
Molnar P & Nadler JV (2001b). Lack of effect of mossy fibre-released zinc on granule cell GABAA receptors in the pilocarpine model of epilepsy. J Neurophysiol 85, 1932-1940.
Mott DD, Benveniste M & Dingledine RJ (2008). pH-dependent inhibition of kainate receptors by zinc. J Neurosci 28, 1659-1671.
Myatt DR, Hadlington T, Ascoli GA & Nasuto SJ (2012). Neuromantic - from semimanual to semi-automatic reconstruction of neuron morphology. Front Neuroinform 6, 4.
Nozaki C, Vergnano AM, Filliol D, Ouagazzal AM, Le Goff A, Carvalho S, Reiss D, Gaveriaux-Ruff C, Neyton J, Paoletti P & Kieffer BL (2011). Zinc alleviates pain through high-affinity binding to the NMDA receptor NR2A subunit. Nat Neurosci 14, 1017-1022.
Paoletti P, Perin-Dureau F, Fayyazuddin A, Le Goff A, Callebaut I & Neyton J (2000). Molecular organization of a zinc binding n-terminal modulatory domain in a NMDA receptor subunit. Neuron 28, 911-925.
Paoletti P, Vergnano AM, Barbour B & Casado M (2009). Zinc at glutamatergic synapses. Neuroscience 158, 126-136.
Pavlov I, Scimemi A, Savtchenko L, Kullmann DM & Walker MC (2011). I(h)-mediated depolarization enhances the temporal precision of neuronal integration. Nat Commun 2, 199.
Penttonen M, Kamondi A, Sik A, Acsady L & Buzsaki G (1997). Feed-forward and feed-back activation of the dentate gyrus in vivo during dentate spikes and sharp wave bursts. Hippocampus 7, 437-450.
Perez-Reyes E (2003). Molecular physiology of low-voltage-activated T-type Ca2+ channels. Physiol Rev 83, 117-161.
Pouille F & Scanziani M (2004). Routing of spike series by dynamic circuits in the hippocampus. Nature 429, 717-723.
Rall W (1964). Theoretical significance of dendritic trees for neuronal input-output relations. In Neural Theory and Modeling, ed. Reiss RF. pp. 73-97. Stanford University Press, Stanford, CA.
Ribak CE, Nitsch R & Seress L (1990). Proportion of parvalbumin-positive basket cells in the GABAergic innervation of pyramidal and granule cells of the rat hippocampal formation. J Comp Neurol 300, 449-461.
Ribak CE & Peterson GM (1991). Intragranular mossy fibers in rats and gerbils form synapses with the somata and proximal dendrites of basket cells in the dentate gyrus. Hippocampus 1, 355-364.
Ruiz A, Walker MC, Fabian-Fine R & Kullmann DM (2004). Endogenous zinc inhibits GABAA receptors in a hippocampal pathway. J Neurophysiol 91, 1091-1096.
Sambandan S, Sauer JF, Vida I & Bartos M (2010). Associative plasticity at excitatory synapses facilitates recruitment of fast-spiking interneurons in the dentate gyrus. J Neurosci 30, 11826-11837.
Sauer JF, Struber M & Bartos M (2012). Interneurons provide circuit-specific depolarization and hyperpolarization. J Neurosci 32, 4224-4229.
Seress L & Gallyas F (2000). The use of a sodium tungstate developer markedly improves the electron microscopic localization of zinc by the Timm method. J Neurosci Methods 100, 33-39.
Sik A, Ylinen A, Penttonen M & Buzsaki G (1994). Inhibitory CA1-CA3-hilar region feedback in the hippocampus. Science 265, 1722-1724.
Smart TG, Hosie AM & Miller PS (2004). Zn2+ ions: modulators of excitatory and inhibitory synaptic activity. Neuroscientist 10, 432-442.
Smart TG, Moss SJ, Xie X & Huganir RL (1991). GABAA receptors are differentially sensitive to zinc: dependence on subunit composition. Br J Pharmacol 103, 1837-1839.
Soltesz I & Mody I (1994). Patch-clamp recordings reveal powerful GABAergic inhibition in dentate hilar neurons. J Neurosci 14, 2365-2376.
Spiridon M, Kamm D, Billups B, Mobbs P & Attwell D (1998). Modulation by zinc of the glutamate transporters in glial cells and cones isolated from the tiger salamander retina. J Physiol 506 (Pt 2), 363-376.
Sun HS, Hui K, Lee DW & Feng ZP (2007). Zn2+ sensitivity of high- and low-voltage activated Ca2+ channels. Biophys J 93, 1175-1183.
Szabadics J & Soltesz I (2009). Functional specificity of mossy fibre innervation of GABAergic cells in the hippocampus. J Neurosci 29, 4239-4251.
Talley EM, Cribbs LL, Lee JH, Daud A, Perez-Reyes E & Bayliss DA (1999). Differential distribution of three members of a gene family encoding low voltage-activated (T-type) Ca2+ channels. J Neurosci 19, 1895-1911.
Tang AH, Karson MA, Nagode DA, McIntosh JM, Uebele VN, Renger JJ, Klugmann M, Milner TA & Alger BE (2011). Nerve terminal nicotinic acetylcholine receptors initiate quantal GABA release from perisomatic interneurons by activating axonal T-type (Cav3) Ca2+ channels and Ca2+ release from stores. J Neurosci 31, 13546-13561.
Toth K (2011). Zinc in neurotransmission. Annu Rev Nutr 31, 139-153.
Traboulsie A, Chemin J, Chevalier M, Quignard JF, Nargeot J & Lory P (2007). Subunit-specific modulation of T-type Ca2+ channels by zinc. J Physiol 578, 159-171.
Tsuda M, Imaizumi K, Katayama T, Kitagawa K, Wanaka A, Tohyama M & Takagi T (1997). Expression of zinc transporter gene, ZnT-1, is induced after transient forebrain ischemia in the gerbil. J Neurosci 17, 6678-6684.
Veran J, Kumar J, Pinheiro PS, Athane A, Mayer ML, Perrais D & Mulle C (2012). Zinc potentiates GluK3 glutamate receptor function by stabilizing the ligand binding domain dimer interface. Neuron 76, 565-578.
Vinet J & Sik A (2006). Expression pattern of voltage-dependent Ca2+ channel subunits in hippocampal inhibitory neurons in mice. Neuroscience 143, 189-212.
Vogt K, Mellor J, Tong G & Nicoll R (2000). The actions of synaptically released zinc at hippocampal mossy fibre synapses. Neuron 26, 187-196.
Weisskopf MG, Zalutsky RA & Nicoll RA (1993). The opioid peptide dynorphin mediates heterosynaptic depression of hippocampal mossy fibre synapses and modulates long-term potentiation. Nature 365, 188.
Wu SM, Qiao X, Noebels JL & Yang XL (1993). Localization and modulatory actions of zinc in vertebrate retina. Vision research 33, 2611-2616.
