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Erschienen in: Anatomical Science International 1/2016

01.01.2016 | Review Article

Molecular and anatomical evidence for the input pathway- and target cell type-dependent regulation of glutamatergic synapses

verfasst von: Miwako Yamasaki

Erschienen in: Anatomical Science International | Ausgabe 1/2016

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Abstract

Glutamate mediates most fast excitatory transmission in the central nervous system by activating primarily two types of ionotropic glutamate receptors: α-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid (AMPA) and N-methyl-d-aspartate (NMDA) receptors. Differential subunit combinations generate great functional diversity in both categories of receptors, making them highly suitable for meeting complex functional requirements. Converging evidence has indicated that distinct AMPA and NMDA receptor subtypes are selectively targeted to functionally different synapses according to different factors, including presynaptic inputs, postsynaptic cell types, and synaptic configurations. This article provides an overview of recent progress in understanding the basic principles governing the synaptic allocation of AMPA and NMDA receptors, and discusses the underlying mechanisms and functional implications.
Literatur
Zurück zum Zitat Aiba A, Kano M, Chen C, Stanton ME, Fox GD, Herrup K, Zwingman TA, Tonegawa S (1994) Deficient cerebellar long-term depression and impaired motor learning in mGluR1 mutant mice. Cell 79:377–388CrossRefPubMed Aiba A, Kano M, Chen C, Stanton ME, Fox GD, Herrup K, Zwingman TA, Tonegawa S (1994) Deficient cerebellar long-term depression and impaired motor learning in mGluR1 mutant mice. Cell 79:377–388CrossRefPubMed
Zurück zum Zitat Barria A, Malinow R (2002) Subunit-specific NMDA receptor trafficking to synapses. Neuron 35:345–353CrossRefPubMed Barria A, Malinow R (2002) Subunit-specific NMDA receptor trafficking to synapses. Neuron 35:345–353CrossRefPubMed
Zurück zum Zitat Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31–39CrossRefPubMed Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31–39CrossRefPubMed
Zurück zum Zitat Bolam JP, Clarke DJ, Smith AD, Somogyi P (1983) A type of aspiny neuron in the rat neostriatum accumulates [3H] γ-aminobutyric acid: combination of Golgi-staining, autoradiography, and electron microscopy. J Comp Neurol 213:121–134CrossRefPubMed Bolam JP, Clarke DJ, Smith AD, Somogyi P (1983) A type of aspiny neuron in the rat neostriatum accumulates [3H] γ-aminobutyric acid: combination of Golgi-staining, autoradiography, and electron microscopy. J Comp Neurol 213:121–134CrossRefPubMed
Zurück zum Zitat Borges K, Dingledine R (1998) AMPA receptors: molecular and functional diversity. Prog Brain Res 116:153–170CrossRefPubMed Borges K, Dingledine R (1998) AMPA receptors: molecular and functional diversity. Prog Brain Res 116:153–170CrossRefPubMed
Zurück zum Zitat Bowie D, Mayer ML (1995) Inward rectification of both AMPA and kainate subtype glutamate receptors generated by polyamine-mediated ion channel block. Neuron 15:453–462CrossRefPubMed Bowie D, Mayer ML (1995) Inward rectification of both AMPA and kainate subtype glutamate receptors generated by polyamine-mediated ion channel block. Neuron 15:453–462CrossRefPubMed
Zurück zum Zitat Bredt DS, Nicoll RA (2003) AMPA receptor trafficking at excitatory synapses. Neuron 40:361–379CrossRefPubMed Bredt DS, Nicoll RA (2003) AMPA receptor trafficking at excitatory synapses. Neuron 40:361–379CrossRefPubMed
Zurück zum Zitat Brunel N, Hakim V, Isope P, Nadal JP, Barbour B (2004) Optimal information storage and the distribution of synaptic weights: perceptron versus Purkinje cell. Neuron 43:745–757PubMed Brunel N, Hakim V, Isope P, Nadal JP, Barbour B (2004) Optimal information storage and the distribution of synaptic weights: perceptron versus Purkinje cell. Neuron 43:745–757PubMed
Zurück zum Zitat Collingridge GL, Isaac JT, Wang YT (2004) Receptor trafficking and synaptic plasticity. Nat Rev Neurosci 5:952–962CrossRefPubMed Collingridge GL, Isaac JT, Wang YT (2004) Receptor trafficking and synaptic plasticity. Nat Rev Neurosci 5:952–962CrossRefPubMed
Zurück zum Zitat Craig AM, Blackstone CD, Huganir RL, Banker G (1993) The distribution of glutamate receptors in cultured rat hippocampal neurons: postsynaptic clustering of AMPA-selective subunits. Neuron 10:1055–1068CrossRefPubMed Craig AM, Blackstone CD, Huganir RL, Banker G (1993) The distribution of glutamate receptors in cultured rat hippocampal neurons: postsynaptic clustering of AMPA-selective subunits. Neuron 10:1055–1068CrossRefPubMed
Zurück zum Zitat Cull-Candy S, Brickley S, Farrant M (2001) NMDA receptor subunits: diversity, development and disease. Curr Opin Neurobiol 11:327–335CrossRefPubMed Cull-Candy S, Brickley S, Farrant M (2001) NMDA receptor subunits: diversity, development and disease. Curr Opin Neurobiol 11:327–335CrossRefPubMed
Zurück zum Zitat Ehrlich I, Malinow R (2004) Postsynaptic density 95 controls AMPA receptor incorporation during long-term potentiation and experience-driven synaptic plasticity. J Neurosci 24:916–927CrossRefPubMed Ehrlich I, Malinow R (2004) Postsynaptic density 95 controls AMPA receptor incorporation during long-term potentiation and experience-driven synaptic plasticity. J Neurosci 24:916–927CrossRefPubMed
Zurück zum Zitat Fritschy JM, Weinmann O, Wenzel A, Benke D (1998) Synapse-specific localization of NMDA and GABA(A) receptor subunits revealed by antigen-retrieval immunohistochemistry. J Comp Neurol 390:194–210CrossRefPubMed Fritschy JM, Weinmann O, Wenzel A, Benke D (1998) Synapse-specific localization of NMDA and GABA(A) receptor subunits revealed by antigen-retrieval immunohistochemistry. J Comp Neurol 390:194–210CrossRefPubMed
Zurück zum Zitat Fukaya M, Watanabe M (2000) Improved immunohistochemical detection of postsynaptically located PSD-95/SAP90 protein family by protease section pretreatment: a study in the adult mouse brain. J Comp Neurol 426:572–586CrossRefPubMed Fukaya M, Watanabe M (2000) Improved immunohistochemical detection of postsynaptically located PSD-95/SAP90 protein family by protease section pretreatment: a study in the adult mouse brain. J Comp Neurol 426:572–586CrossRefPubMed
Zurück zum Zitat Fukaya M, Tsujita M, Yamazaki M, Kushiya E, Abe M, Akashi K, Natsume R, Kano M, Kamiya H, Watanabe M, Sakimura K (2006) Abundant distribution of TARP gamma-8 in synaptic and extrasynaptic surface of hippocampal neurons and its major role in AMPA receptor expression on spines and dendrites. Eur J Neurosci 24:2177–2190CrossRefPubMed Fukaya M, Tsujita M, Yamazaki M, Kushiya E, Abe M, Akashi K, Natsume R, Kano M, Kamiya H, Watanabe M, Sakimura K (2006) Abundant distribution of TARP gamma-8 in synaptic and extrasynaptic surface of hippocampal neurons and its major role in AMPA receptor expression on spines and dendrites. Eur J Neurosci 24:2177–2190CrossRefPubMed
Zurück zum Zitat Fukazawa Y, Shigemoto R (2012) Intra-synapse-type and inter-synapse-type relationships between synaptic size and AMPAR expression. Curr Opin Neurobiol 22:446–452CrossRefPubMed Fukazawa Y, Shigemoto R (2012) Intra-synapse-type and inter-synapse-type relationships between synaptic size and AMPAR expression. Curr Opin Neurobiol 22:446–452CrossRefPubMed
Zurück zum Zitat Gardner SM, Takamiya K, Xia J, Suh JG, Johnson R, Yu S, Huganir RL (2005) Calcium-permeable AMPA receptor plasticity is mediated by subunit-specific interactions with PICK1 and NSF. Neuron 45:903–915CrossRefPubMed Gardner SM, Takamiya K, Xia J, Suh JG, Johnson R, Yu S, Huganir RL (2005) Calcium-permeable AMPA receptor plasticity is mediated by subunit-specific interactions with PICK1 and NSF. Neuron 45:903–915CrossRefPubMed
Zurück zum Zitat Geiger JR, Melcher T, Koh DS, Sakmann B, Seeburg PH, Jonas P, Monyer H (1995) Relative abundance of subunit mRNAs determines gating and Ca2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS. Neuron 15:193–204CrossRefPubMed Geiger JR, Melcher T, Koh DS, Sakmann B, Seeburg PH, Jonas P, Monyer H (1995) Relative abundance of subunit mRNAs determines gating and Ca2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS. Neuron 15:193–204CrossRefPubMed
Zurück zum Zitat Greger IH, Khatri L, Ziff EB (2002) RNA editing at arg607 controls AMPA receptor exit from the endoplasmic reticulum. Neuron 34:759–772CrossRefPubMed Greger IH, Khatri L, Ziff EB (2002) RNA editing at arg607 controls AMPA receptor exit from the endoplasmic reticulum. Neuron 34:759–772CrossRefPubMed
Zurück zum Zitat Hirai H, Launey T, Mikawa S, Torashima T, Yanagihara D, Kasaura T, Miyamoto A, Yuzaki M (2003) New role of δ2-glutamate receptors in AMPA receptor trafficking and cerebellar function. Nat Neurosci 6:869–876CrossRefPubMed Hirai H, Launey T, Mikawa S, Torashima T, Yanagihara D, Kasaura T, Miyamoto A, Yuzaki M (2003) New role of δ2-glutamate receptors in AMPA receptor trafficking and cerebellar function. Nat Neurosci 6:869–876CrossRefPubMed
Zurück zum Zitat Isaac JT, Ashby MC, McBain CJ (2007) The role of the GluR2 subunit in AMPA receptor function and synaptic plasticity. Neuron 54:859–871CrossRefPubMed Isaac JT, Ashby MC, McBain CJ (2007) The role of the GluR2 subunit in AMPA receptor function and synaptic plasticity. Neuron 54:859–871CrossRefPubMed
Zurück zum Zitat Jackson AC, Nicoll RA (2011) The expanding social network of ionotropic glutamate receptors: TARPs and other transmembrane auxiliary subunits. Neuron 70:178–199PubMedCentralCrossRefPubMed Jackson AC, Nicoll RA (2011) The expanding social network of ionotropic glutamate receptors: TARPs and other transmembrane auxiliary subunits. Neuron 70:178–199PubMedCentralCrossRefPubMed
Zurück zum Zitat John HA, Birnstiel ML, Jones KW (1969) RNA–DNA hybrids at the cytological level. Nature 223:582–587CrossRefPubMed John HA, Birnstiel ML, Jones KW (1969) RNA–DNA hybrids at the cytological level. Nature 223:582–587CrossRefPubMed
Zurück zum Zitat Kashiwabuchi N, Ikeda K, Araki K, Hirano T, Shibuki K, Takayama C, Inoue Y, Kutsuwada T, Yagi T, Kang Y et al (1995) Impairment of motor coordination, Purkinje cell synapse formation, and cerebellar long-term depression in GluR delta 2 mutant mice. Cell 81:245–252CrossRefPubMed Kashiwabuchi N, Ikeda K, Araki K, Hirano T, Shibuki K, Takayama C, Inoue Y, Kutsuwada T, Yagi T, Kang Y et al (1995) Impairment of motor coordination, Purkinje cell synapse formation, and cerebellar long-term depression in GluR delta 2 mutant mice. Cell 81:245–252CrossRefPubMed
Zurück zum Zitat Kawakami R, Shinohara Y, Kato Y, Sugiyama H, Shigemoto R, Ito I (2003) Asymmetrical allocation of NMDA receptor epsilon2 subunits in hippocampal circuitry. Science 300:990–994CrossRefPubMed Kawakami R, Shinohara Y, Kato Y, Sugiyama H, Shigemoto R, Ito I (2003) Asymmetrical allocation of NMDA receptor epsilon2 subunits in hippocampal circuitry. Science 300:990–994CrossRefPubMed
Zurück zum Zitat Keinanen K, Wisden W, Sommer B, Werner P, Herb A, Verdoorn TA, Sakmann B, Seeburg PH (1990) A family of AMPA-selective glutamate receptors. Science 249:556–560CrossRefPubMed Keinanen K, Wisden W, Sommer B, Werner P, Herb A, Verdoorn TA, Sakmann B, Seeburg PH (1990) A family of AMPA-selective glutamate receptors. Science 249:556–560CrossRefPubMed
Zurück zum Zitat Kelly L, Farrant M, Cull-Candy SG (2009) Synaptic mGluR activation drives plasticity of calcium-permeable AMPA receptors. Nat Neurosci 12:593–601CrossRefPubMed Kelly L, Farrant M, Cull-Candy SG (2009) Synaptic mGluR activation drives plasticity of calcium-permeable AMPA receptors. Nat Neurosci 12:593–601CrossRefPubMed
Zurück zum Zitat Koh DS, Burnashev N, Jonas P (1995a) Block of native Ca(2+)-permeable AMPA receptors in rat brain by intracellular polyamines generates double rectification. J Physiol 486(Pt 2):305–312PubMedCentralCrossRefPubMed Koh DS, Burnashev N, Jonas P (1995a) Block of native Ca(2+)-permeable AMPA receptors in rat brain by intracellular polyamines generates double rectification. J Physiol 486(Pt 2):305–312PubMedCentralCrossRefPubMed
Zurück zum Zitat Koh DS, Geiger JR, Jonas P, Sakmann B (1995b) Ca(2+)-permeable AMPA and NMDA receptor channels in basket cells of rat hippocampal dentate gyrus. J Physiol 485(Pt 2):383–402PubMedCentralCrossRefPubMed Koh DS, Geiger JR, Jonas P, Sakmann B (1995b) Ca(2+)-permeable AMPA and NMDA receptor channels in basket cells of rat hippocampal dentate gyrus. J Physiol 485(Pt 2):383–402PubMedCentralCrossRefPubMed
Zurück zum Zitat Kullmann DM, Lamsa KP (2007) Long-term synaptic plasticity in hippocampal interneurons. Nat Rev Neurosci 8:687–699CrossRefPubMed Kullmann DM, Lamsa KP (2007) Long-term synaptic plasticity in hippocampal interneurons. Nat Rev Neurosci 8:687–699CrossRefPubMed
Zurück zum Zitat Kurihara H, Hashimoto K, Kano M, Takayama C, Sakimura K, Mishina M, Inoue Y, Watanabe M (1997) Impaired parallel fiber → Purkinje cell synapse stabilization during cerebellar development of mutant mice lacking the glutamate receptor δ2 subunit. J Neurosci 17:9613–9623PubMed Kurihara H, Hashimoto K, Kano M, Takayama C, Sakimura K, Mishina M, Inoue Y, Watanabe M (1997) Impaired parallel fiber → Purkinje cell synapse stabilization during cerebellar development of mutant mice lacking the glutamate receptor δ2 subunit. J Neurosci 17:9613–9623PubMed
Zurück zum Zitat Kutsuwada T, Sakimura K, Manabe T, Takayama C, Katakura N, Kushiya E, Natsume R, Watanabe M, Inoue Y, Yagi T, Aizawa S, Arakawa M, Takahashi T, Nakamura Y, Mori H, Mishina M (1996) Impairment of suckling response, trigeminal neuronal pattern formation, and hippocampal LTD in NMDA receptor ε2 subunit mutant mice. Neuron 16:333–344CrossRefPubMed Kutsuwada T, Sakimura K, Manabe T, Takayama C, Katakura N, Kushiya E, Natsume R, Watanabe M, Inoue Y, Yagi T, Aizawa S, Arakawa M, Takahashi T, Nakamura Y, Mori H, Mishina M (1996) Impairment of suckling response, trigeminal neuronal pattern formation, and hippocampal LTD in NMDA receptor ε2 subunit mutant mice. Neuron 16:333–344CrossRefPubMed
Zurück zum Zitat Lalouette A, Lohof A, Sotelo C, Guenet J, Mariani J (2001) Neurobiological effects of a null mutation depend on genetic context: comparison between two hotfoot alleles of the delta-2 ionotropic glutamate receptor. Neuroscience 105:443–455CrossRefPubMed Lalouette A, Lohof A, Sotelo C, Guenet J, Mariani J (2001) Neurobiological effects of a null mutation depend on genetic context: comparison between two hotfoot alleles of the delta-2 ionotropic glutamate receptor. Neuroscience 105:443–455CrossRefPubMed
Zurück zum Zitat Lambolez B, Audinat E, Bochet P, Crepel F, Rossier J (1992) AMPA receptor subunits expressed by single Purkinje cells. Neuron 9:247–258CrossRefPubMed Lambolez B, Audinat E, Bochet P, Crepel F, Rossier J (1992) AMPA receptor subunits expressed by single Purkinje cells. Neuron 9:247–258CrossRefPubMed
Zurück zum Zitat Landsend AS, Amiry-Moghaddam M, Matsubara A, Bergersen L, Usami S, Wenthold RJ, Ottersen OP (1997) Differential localization of δ glutamate receptors in the rat cerebellum: coexpression with AMPA receptors in parallel fiber–spine synapses and absence from climbing fiber–spine synapses. J Neurosci 17:834–842PubMed Landsend AS, Amiry-Moghaddam M, Matsubara A, Bergersen L, Usami S, Wenthold RJ, Ottersen OP (1997) Differential localization of δ glutamate receptors in the rat cerebellum: coexpression with AMPA receptors in parallel fiber–spine synapses and absence from climbing fiber–spine synapses. J Neurosci 17:834–842PubMed
Zurück zum Zitat Liu SQ, Cull-Candy SG (2000) Synaptic activity at calcium-permeable AMPA receptors induces a switch in receptor subtype. Nature 405:454–458CrossRefPubMed Liu SQ, Cull-Candy SG (2000) Synaptic activity at calcium-permeable AMPA receptors induces a switch in receptor subtype. Nature 405:454–458CrossRefPubMed
Zurück zum Zitat Lu W, Shi Y, Jackson AC, Bjorgan K, During MJ, Sprengel R, Seeburg PH, Nicoll RA (2009) Subunit composition of synaptic AMPA receptors revealed by a single-cell genetic approach. Neuron 62:254–268PubMedCentralCrossRefPubMed Lu W, Shi Y, Jackson AC, Bjorgan K, During MJ, Sprengel R, Seeburg PH, Nicoll RA (2009) Subunit composition of synaptic AMPA receptors revealed by a single-cell genetic approach. Neuron 62:254–268PubMedCentralCrossRefPubMed
Zurück zum Zitat Malinow R, Malenka RC (2002) AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25:103–126CrossRefPubMed Malinow R, Malenka RC (2002) AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25:103–126CrossRefPubMed
Zurück zum Zitat Masugi-Tokita M, Tarusawa E, Watanabe M, Molnar E, Fujimoto K, Shigemoto R (2007) Number and density of AMPA receptors in individual synapses in the rat cerebellum as revealed by SDS-digested freeze-fracture replica labeling. J Neurosci 27:2135–2144CrossRefPubMed Masugi-Tokita M, Tarusawa E, Watanabe M, Molnar E, Fujimoto K, Shigemoto R (2007) Number and density of AMPA receptors in individual synapses in the rat cerebellum as revealed by SDS-digested freeze-fracture replica labeling. J Neurosci 27:2135–2144CrossRefPubMed
Zurück zum Zitat Matsuda I, Mishina M (2000) Identification of a juxtamembrane segment of the glutamate receptor δ2 subunit required for the plasma membrane localization. Biochem Biophys Res Commun 275:565–571CrossRefPubMed Matsuda I, Mishina M (2000) Identification of a juxtamembrane segment of the glutamate receptor δ2 subunit required for the plasma membrane localization. Biochem Biophys Res Commun 275:565–571CrossRefPubMed
Zurück zum Zitat Matsuda S, Launey T, Mikawa S, Hirai H (2000) Disruption of AMPA receptor GluR2 clusters following long-term depression induction in cerebellar Purkinje neurons. EMBO J 19:2765–2774PubMedCentralCrossRefPubMed Matsuda S, Launey T, Mikawa S, Hirai H (2000) Disruption of AMPA receptor GluR2 clusters following long-term depression induction in cerebellar Purkinje neurons. EMBO J 19:2765–2774PubMedCentralCrossRefPubMed
Zurück zum Zitat Matsuda K, Miura E, Miyazaki T, Kakegawa W, Emi K, Narumi S, Fukazawa Y, Ito-Ishida A, Kondo T, Shigemoto R, Watanabe M, Yuzaki M (2010) Cbln1 is a ligand for an orphan glutamate receptor δ2, a bidirectional synapse organizer. Science 328:363–368CrossRefPubMed Matsuda K, Miura E, Miyazaki T, Kakegawa W, Emi K, Narumi S, Fukazawa Y, Ito-Ishida A, Kondo T, Shigemoto R, Watanabe M, Yuzaki M (2010) Cbln1 is a ligand for an orphan glutamate receptor δ2, a bidirectional synapse organizer. Science 328:363–368CrossRefPubMed
Zurück zum Zitat McBain CJ, Dingledine R (1993) Heterogeneity of synaptic glutamate receptors on CA3 stratum radiatum interneurones of rat hippocampus. J Physiol 462:373–392PubMedCentralCrossRefPubMed McBain CJ, Dingledine R (1993) Heterogeneity of synaptic glutamate receptors on CA3 stratum radiatum interneurones of rat hippocampus. J Physiol 462:373–392PubMedCentralCrossRefPubMed
Zurück zum Zitat Misra C, Brickley SG, Farrant M, Cull-Candy SG (2000a) Identification of subunits contributing to synaptic and extrasynaptic NMDA receptors in Golgi cells of the rat cerebellum. J Physiol 524(Pt 1):147–162PubMedCentralCrossRefPubMed Misra C, Brickley SG, Farrant M, Cull-Candy SG (2000a) Identification of subunits contributing to synaptic and extrasynaptic NMDA receptors in Golgi cells of the rat cerebellum. J Physiol 524(Pt 1):147–162PubMedCentralCrossRefPubMed
Zurück zum Zitat Misra C, Brickley SG, Wyllie DJ, Cull-Candy SG (2000b) Slow deactivation kinetics of NMDA receptors containing NR1 and NR2D subunits in rat cerebellar Purkinje cells. J Physiol 525(Pt 2):299–305PubMedCentralCrossRefPubMed Misra C, Brickley SG, Wyllie DJ, Cull-Candy SG (2000b) Slow deactivation kinetics of NMDA receptors containing NR1 and NR2D subunits in rat cerebellar Purkinje cells. J Physiol 525(Pt 2):299–305PubMedCentralCrossRefPubMed
Zurück zum Zitat Miyazaki T, Fukaya M, Shimizu H, Watanabe M (2003) Subtype switching of vesicular glutamate transporters at parallel fibre-Purkinje cell synapses in developing mouse cerebellum. Eur J Neurosci 17:2563–2572CrossRefPubMed Miyazaki T, Fukaya M, Shimizu H, Watanabe M (2003) Subtype switching of vesicular glutamate transporters at parallel fibre-Purkinje cell synapses in developing mouse cerebellum. Eur J Neurosci 17:2563–2572CrossRefPubMed
Zurück zum Zitat Momiyama A, Silver RA, Hausser M, Notomi T, Wu Y, Shigemoto R, Cull-Candy SG (2003) The density of AMPA receptors activated by a transmitter quantum at the climbing fibre-Purkinje cell synapse in immature rats. J Physiol 549:75–92PubMedCentralCrossRefPubMed Momiyama A, Silver RA, Hausser M, Notomi T, Wu Y, Shigemoto R, Cull-Candy SG (2003) The density of AMPA receptors activated by a transmitter quantum at the climbing fibre-Purkinje cell synapse in immature rats. J Physiol 549:75–92PubMedCentralCrossRefPubMed
Zurück zum Zitat Monyer H, Seeburg PH, Wisden W (1991) Glutamate-operated channels: developmentally early and mature forms arise by alternative splicing. Neuron 6:799–810CrossRefPubMed Monyer H, Seeburg PH, Wisden W (1991) Glutamate-operated channels: developmentally early and mature forms arise by alternative splicing. Neuron 6:799–810CrossRefPubMed
Zurück zum Zitat Monyer H, Burnashev N, Laurie DJ, Sakmann B, Seeburg PH (1994) Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12:529–540CrossRefPubMed Monyer H, Burnashev N, Laurie DJ, Sakmann B, Seeburg PH (1994) Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12:529–540CrossRefPubMed
Zurück zum Zitat Mori H, Mishina M (1995) Structure and function of the NMDA receptor channel. Neuropharmacology 34:1219–1237CrossRefPubMed Mori H, Mishina M (1995) Structure and function of the NMDA receptor channel. Neuropharmacology 34:1219–1237CrossRefPubMed
Zurück zum Zitat Nakanishi S, Masu M (1994) Molecular diversity and functions of glutamate receptors. Annu Rev Biophys Biomol Struct 23:319–348CrossRefPubMed Nakanishi S, Masu M (1994) Molecular diversity and functions of glutamate receptors. Annu Rev Biophys Biomol Struct 23:319–348CrossRefPubMed
Zurück zum Zitat Nicholson DA, Trana R, Katz Y, Kath WL, Spruston N, Geinisman Y (2006) Distance-dependent differences in synapse number and AMPA receptor expression in hippocampal CA1 pyramidal neurons. Neuron 50:431–442CrossRefPubMed Nicholson DA, Trana R, Katz Y, Kath WL, Spruston N, Geinisman Y (2006) Distance-dependent differences in synapse number and AMPA receptor expression in hippocampal CA1 pyramidal neurons. Neuron 50:431–442CrossRefPubMed
Zurück zum Zitat Nimchinsky EA, Yasuda R, Oertner TG, Svoboda K (2004) The number of glutamate receptors opened by synaptic stimulation in single hippocampal spines. J Neurosci 24:2054–2064CrossRefPubMed Nimchinsky EA, Yasuda R, Oertner TG, Svoboda K (2004) The number of glutamate receptors opened by synaptic stimulation in single hippocampal spines. J Neurosci 24:2054–2064CrossRefPubMed
Zurück zum Zitat Noguchi J, Matsuzaki M, Ellis-Davies GC, Kasai H (2005) Spine–neck geometry determines NMDA receptor-dependent Ca2+ signaling in dendrites. Neuron 46:609–622PubMedCentralCrossRefPubMed Noguchi J, Matsuzaki M, Ellis-Davies GC, Kasai H (2005) Spine–neck geometry determines NMDA receptor-dependent Ca2+ signaling in dendrites. Neuron 46:609–622PubMedCentralCrossRefPubMed
Zurück zum Zitat Nusser Z, Cull-Candy S, Farrant M (1997) Differences in synaptic GABA(A) receptor number underlie variation in GABA mini amplitude. Neuron 19:697–709CrossRefPubMed Nusser Z, Cull-Candy S, Farrant M (1997) Differences in synaptic GABA(A) receptor number underlie variation in GABA mini amplitude. Neuron 19:697–709CrossRefPubMed
Zurück zum Zitat Nusser Z, Lujan R, Laube G, Roberts JD, Molnar E, Somogyi P (1998) Cell type and pathway dependence of synaptic AMPA receptor number and variability in the hippocampus. Neuron 21:545–559CrossRefPubMed Nusser Z, Lujan R, Laube G, Roberts JD, Molnar E, Somogyi P (1998) Cell type and pathway dependence of synaptic AMPA receptor number and variability in the hippocampus. Neuron 21:545–559CrossRefPubMed
Zurück zum Zitat Nyiri G, Stephenson FA, Freund TF, Somogyi P (2003) Large variability in synaptic N-methyl-d-aspartate receptor density on interneurons and a comparison with pyramidal-cell spines in the rat hippocampus. Neuroscience 119:347–363CrossRefPubMed Nyiri G, Stephenson FA, Freund TF, Somogyi P (2003) Large variability in synaptic N-methyl-d-aspartate receptor density on interneurons and a comparison with pyramidal-cell spines in the rat hippocampus. Neuroscience 119:347–363CrossRefPubMed
Zurück zum Zitat Ottersen OP, Landsend AS (1997) Organization of glutamate receptors at the synapse. Eur J Neurosci 9:2219–2224CrossRefPubMed Ottersen OP, Landsend AS (1997) Organization of glutamate receptors at the synapse. Eur J Neurosci 9:2219–2224CrossRefPubMed
Zurück zum Zitat Palay S, Chan-Palay V (1974) Cerebellar cortex: cytology and organization. Springer, New YorkCrossRef Palay S, Chan-Palay V (1974) Cerebellar cortex: cytology and organization. Springer, New YorkCrossRef
Zurück zum Zitat Pellegrini-Giampietro DE, Bennett MV, Zukin RS (1991) Differential expression of three glutamate receptor genes in developing rat brain: an in situ hybridization study. Proc Natl Acad Sci USA 88:4157–4161PubMedCentralCrossRefPubMed Pellegrini-Giampietro DE, Bennett MV, Zukin RS (1991) Differential expression of three glutamate receptor genes in developing rat brain: an in situ hybridization study. Proc Natl Acad Sci USA 88:4157–4161PubMedCentralCrossRefPubMed
Zurück zum Zitat Petralia RS, Wenthold RJ (1999) Immunocytochemistry of NMDA receptors. In: Li M (ed) Methods in molecular biology: NMDA receptor protocols. Humana, Totowa, NJ, pp 73–92 Petralia RS, Wenthold RJ (1999) Immunocytochemistry of NMDA receptors. In: Li M (ed) Methods in molecular biology: NMDA receptor protocols. Humana, Totowa, NJ, pp 73–92
Zurück zum Zitat Petralia RS, Wang YX, Mayat E, Wenthold RJ (1997) Glutamate receptor subunit 2-selective antibody shows a differential distribution of calcium-impermeable AMPA receptors among populations of neurons. J Comp Neurol 385:456–476CrossRefPubMed Petralia RS, Wang YX, Mayat E, Wenthold RJ (1997) Glutamate receptor subunit 2-selective antibody shows a differential distribution of calcium-impermeable AMPA receptors among populations of neurons. J Comp Neurol 385:456–476CrossRefPubMed
Zurück zum Zitat Racca C, Stephenson FA, Streit P, Roberts JD, Somogyi P (2000) NMDA receptor content of synapses in stratum radiatum of the hippocampal CA1 area. J Neurosci 20:2512–2522PubMed Racca C, Stephenson FA, Streit P, Roberts JD, Somogyi P (2000) NMDA receptor content of synapses in stratum radiatum of the hippocampal CA1 area. J Neurosci 20:2512–2522PubMed
Zurück zum Zitat Rubio ME, Wenthold RJ (1997) Glutamate receptors are selectively targeted to postsynaptic sites in neurons. Neuron 18:939–950CrossRefPubMed Rubio ME, Wenthold RJ (1997) Glutamate receptors are selectively targeted to postsynaptic sites in neurons. Neuron 18:939–950CrossRefPubMed
Zurück zum Zitat Sans N, Vissel B, Petralia RS, Wang YX, Chang K, Royle GA, Wang CY, O’Gorman S, Heinemann SF, Wenthold RJ (2003) Aberrant formation of glutamate receptor complexes in hippocampal neurons of mice lacking the GluR2 AMPA receptor subunit. J Neurosci 23:9367–9373PubMed Sans N, Vissel B, Petralia RS, Wang YX, Chang K, Royle GA, Wang CY, O’Gorman S, Heinemann SF, Wenthold RJ (2003) Aberrant formation of glutamate receptor complexes in hippocampal neurons of mice lacking the GluR2 AMPA receptor subunit. J Neurosci 23:9367–9373PubMed
Zurück zum Zitat Sato K, Kiyama H, Tohyama M (1993) The differential expression patterns of messenger RNAs encoding non-N-methyl-d-aspartate glutamate receptor subunits (GluR1–4) in the rat brain. Neuroscience 52:515–539CrossRefPubMed Sato K, Kiyama H, Tohyama M (1993) The differential expression patterns of messenger RNAs encoding non-N-methyl-d-aspartate glutamate receptor subunits (GluR1–4) in the rat brain. Neuroscience 52:515–539CrossRefPubMed
Zurück zum Zitat Schnell E, Sizemore M, Karimzadegan S, Chen L, Bredt DS, Nicoll RA (2002) Direct interactions between PSD-95 and stargazin control synaptic AMPA receptor number. Proc Natl Acad Sci USA 99:13902–13907PubMedCentralCrossRefPubMed Schnell E, Sizemore M, Karimzadegan S, Chen L, Bredt DS, Nicoll RA (2002) Direct interactions between PSD-95 and stargazin control synaptic AMPA receptor number. Proc Natl Acad Sci USA 99:13902–13907PubMedCentralCrossRefPubMed
Zurück zum Zitat Seeburg PH (1993) The TINS/TiPS Lecture. The molecular biology of mammalian glutamate receptor channels. Trends Neurosci 16:359–365CrossRefPubMed Seeburg PH (1993) The TINS/TiPS Lecture. The molecular biology of mammalian glutamate receptor channels. Trends Neurosci 16:359–365CrossRefPubMed
Zurück zum Zitat Sobczyk A, Scheuss V, Svoboda K (2005) NMDA receptor subunit-dependent [Ca2 +] signaling in individual hippocampal dendritic spines. J Neurosci 25:6037–6046CrossRefPubMed Sobczyk A, Scheuss V, Svoboda K (2005) NMDA receptor subunit-dependent [Ca2 +] signaling in individual hippocampal dendritic spines. J Neurosci 25:6037–6046CrossRefPubMed
Zurück zum Zitat Stein V, House DR, Bredt DS, Nicoll RA (2003) Postsynaptic density-95 mimics and occludes hippocampal long-term potentiation and enhances long-term depression. J Neurosci 23:5503–5506PubMed Stein V, House DR, Bredt DS, Nicoll RA (2003) Postsynaptic density-95 mimics and occludes hippocampal long-term potentiation and enhances long-term depression. J Neurosci 23:5503–5506PubMed
Zurück zum Zitat Takayama C, Nakagawa S, Watanabe M, Mishina M, Inoue Y (1996) Developmental changes in expression and distribution of the glutamate receptor channel δ2 subunit according to the Purkinje cell maturation. Brain Res Dev Brain Res 92:147–155CrossRefPubMed Takayama C, Nakagawa S, Watanabe M, Mishina M, Inoue Y (1996) Developmental changes in expression and distribution of the glutamate receptor channel δ2 subunit according to the Purkinje cell maturation. Brain Res Dev Brain Res 92:147–155CrossRefPubMed
Zurück zum Zitat Takeuchi T, Miyazaki T, Watanabe M, Mori H, Sakimura K, Mishina M (2005) Control of synaptic connection by glutamate receptor delta2 in the adult cerebellum. J Neurosci 25:2146–2156CrossRefPubMed Takeuchi T, Miyazaki T, Watanabe M, Mori H, Sakimura K, Mishina M (2005) Control of synaptic connection by glutamate receptor delta2 in the adult cerebellum. J Neurosci 25:2146–2156CrossRefPubMed
Zurück zum Zitat Takumi Y, Ramirez-Leon V, Laake P, Rinvik E, Ottersen OP (1999) Different modes of expression of AMPA and NMDA receptors in hippocampal synapses. Nat Neurosci 2:618–624CrossRefPubMed Takumi Y, Ramirez-Leon V, Laake P, Rinvik E, Ottersen OP (1999) Different modes of expression of AMPA and NMDA receptors in hippocampal synapses. Nat Neurosci 2:618–624CrossRefPubMed
Zurück zum Zitat Tempia F, Kano M, Schneggenburger R, Schirra C, Garaschuk O, Plant T, Konnerth A (1996) Fractional calcium current through neuronal AMPA-receptor channels with a low calcium permeability. J Neurosci 16:456–466PubMed Tempia F, Kano M, Schneggenburger R, Schirra C, Garaschuk O, Plant T, Konnerth A (1996) Fractional calcium current through neuronal AMPA-receptor channels with a low calcium permeability. J Neurosci 16:456–466PubMed
Zurück zum Zitat Toth K, McBain CJ (1998) Afferent-specific innervation of two distinct AMPA receptor subtypes on single hippocampal interneurons. Nat Neurosci 1:572–578CrossRefPubMed Toth K, McBain CJ (1998) Afferent-specific innervation of two distinct AMPA receptor subtypes on single hippocampal interneurons. Nat Neurosci 1:572–578CrossRefPubMed
Zurück zum Zitat Tsuzuki K, Lambolez B, Rossier J, Ozawa S (2001) Absolute quantification of AMPA receptor subunit mRNAs in single hippocampal neurons. J Neurochem 77:1650–1659CrossRefPubMed Tsuzuki K, Lambolez B, Rossier J, Ozawa S (2001) Absolute quantification of AMPA receptor subunit mRNAs in single hippocampal neurons. J Neurochem 77:1650–1659CrossRefPubMed
Zurück zum Zitat Uemura T, Kakizawa S, Yamasaki M, Sakimura K, Watanabe M, Iino M, Mishina M (2007) Regulation of long-term depression and climbing fiber territory by glutamate receptor δ2 at parallel fiber synapses through its C-terminal domain in cerebellar Purkinje cells. J Neurosci 27:12096–12108CrossRefPubMed Uemura T, Kakizawa S, Yamasaki M, Sakimura K, Watanabe M, Iino M, Mishina M (2007) Regulation of long-term depression and climbing fiber territory by glutamate receptor δ2 at parallel fiber synapses through its C-terminal domain in cerebellar Purkinje cells. J Neurosci 27:12096–12108CrossRefPubMed
Zurück zum Zitat Wang YT, Linden DJ (2000) Expression of cerebellar long-term depression requires postsynaptic clathrin-mediated endocytosis. Neuron 25:635–647CrossRefPubMed Wang YT, Linden DJ (2000) Expression of cerebellar long-term depression requires postsynaptic clathrin-mediated endocytosis. Neuron 25:635–647CrossRefPubMed
Zurück zum Zitat Watanabe M, Inoue Y, Sakimura K, Mishina M (1992) Developmental changes in distribution of NMDA receptor channel subunit mRNAs. NeuroReport 3:1138–1140CrossRefPubMed Watanabe M, Inoue Y, Sakimura K, Mishina M (1992) Developmental changes in distribution of NMDA receptor channel subunit mRNAs. NeuroReport 3:1138–1140CrossRefPubMed
Zurück zum Zitat Watanabe M, Fukaya M, Sakimura K, Manabe T, Mishina M, Inoue Y (1998) Selective scarcity of NMDA receptor channel subunits in the stratum lucidum (mossy fibre-recipient layer) of the mouse hippocampal CA3 subfield. Eur J Neurosci 10:478–487CrossRefPubMed Watanabe M, Fukaya M, Sakimura K, Manabe T, Mishina M, Inoue Y (1998) Selective scarcity of NMDA receptor channel subunits in the stratum lucidum (mossy fibre-recipient layer) of the mouse hippocampal CA3 subfield. Eur J Neurosci 10:478–487CrossRefPubMed
Zurück zum Zitat Wenthold RJ, Petralia RS, Blahos J II, Niedzielski AS (1996) Evidence for multiple AMPA receptor complexes in hippocampal CA1/CA2 neurons. J Neurosci 16:1982–1989PubMed Wenthold RJ, Petralia RS, Blahos J II, Niedzielski AS (1996) Evidence for multiple AMPA receptor complexes in hippocampal CA1/CA2 neurons. J Neurosci 16:1982–1989PubMed
Zurück zum Zitat Yamasaki M, Miyazaki T, Azechi H, Abe M, Natsume R, Hagiwara T, Aiba A, Mishina M, Sakimura K, Watanabe M (2011) Glutamate receptor δ2 is essential for input pathway-dependent regulation of synaptic AMPAR contents in cerebellar Purkinje cells. J Neurosci 31:3362–3374CrossRefPubMed Yamasaki M, Miyazaki T, Azechi H, Abe M, Natsume R, Hagiwara T, Aiba A, Mishina M, Sakimura K, Watanabe M (2011) Glutamate receptor δ2 is essential for input pathway-dependent regulation of synaptic AMPAR contents in cerebellar Purkinje cells. J Neurosci 31:3362–3374CrossRefPubMed
Zurück zum Zitat Yamasaki M, Okada R, Takasaki C, Toki S, Fukaya M, Natsume R, Sakimura K, Mishina M, Shirakawa T, Watanabe M (2014) Opposing role of NMDA receptor GluN2B and GluN2D in somatosensory development and maturation. J Neurosci 34:11534–11548CrossRefPubMed Yamasaki M, Okada R, Takasaki C, Toki S, Fukaya M, Natsume R, Sakimura K, Mishina M, Shirakawa T, Watanabe M (2014) Opposing role of NMDA receptor GluN2B and GluN2D in somatosensory development and maturation. J Neurosci 34:11534–11548CrossRefPubMed
Zurück zum Zitat Yuzaki M (2009) New (but old) molecules regulating synapse integrity and plasticity: Cbln1 and the δ2 glutamate receptor. Neuroscience 162:633–643CrossRefPubMed Yuzaki M (2009) New (but old) molecules regulating synapse integrity and plasticity: Cbln1 and the δ2 glutamate receptor. Neuroscience 162:633–643CrossRefPubMed
Metadaten
Titel
Molecular and anatomical evidence for the input pathway- and target cell type-dependent regulation of glutamatergic synapses
verfasst von
Miwako Yamasaki
Publikationsdatum
01.01.2016
Verlag
Springer Japan
Erschienen in
Anatomical Science International / Ausgabe 1/2016
Print ISSN: 1447-6959
Elektronische ISSN: 1447-073X
DOI
https://doi.org/10.1007/s12565-015-0303-0

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