Development of Cortical Pyramidal Cell and Interneuronal Dendrites: a Role for Kainate Receptor Subunits and NETO1.
Animals
Animals, Newborn
Dendrites
/ drug effects
Interneurons
/ drug effects
Kainic Acid
/ pharmacology
Organ Culture Techniques
Organogenesis
/ drug effects
Protein Subunits
/ agonists
Pyramidal Cells
/ drug effects
Rats
Rats, Long-Evans
Receptors, Kainic Acid
/ agonists
Receptors, N-Methyl-D-Aspartate
/ physiology
Visual Cortex
/ drug effects
GluK2 Kainate Receptor
Dendritogenesis
GluK2
Glutamate receptors
NETO
Postnatal development
Rat neocortex
Journal
Molecular neurobiology
ISSN: 1559-1182
Titre abrégé: Mol Neurobiol
Pays: United States
ID NLM: 8900963
Informations de publication
Date de publication:
Jul 2019
Jul 2019
Historique:
received:
25
06
2018
accepted:
25
10
2018
pubmed:
14
11
2018
medline:
15
1
2020
entrez:
14
11
2018
Statut:
ppublish
Résumé
During neuronal development, AMPA receptors (AMPARs) and NMDA receptors (NMDARs) are important for neuronal differentiation. Kainate receptors (KARs) are closely related to AMPARs and involved in the regulation of cortical network activity. However, their role for neurite growth and differentiation of cortical neurons is unclear. Here, we used KAR agonists and overexpression of selected KAR subunits and their auxiliary neuropilin and tolloid-like proteins, NETOs, to investigate their influence on dendritic growth and network activity in organotypic cultures of rat visual cortex. Kainate at 500 nM enhanced network activity and promoted development of dendrites in layer II/III pyramidal cells, but not interneurons. GluK2 overexpression promoted dendritic growth in pyramidal cells and interneurons. GluK2 transfectants were highly active and acted as drivers for network activity. GluK1 and NETO1 specifically promoted dendritic growth of interneurons. Our study provides new insights for the roles of KARs and NETOs in the morphological and physiological development of the visual cortex.
Identifiants
pubmed: 30421168
doi: 10.1007/s12035-018-1414-0
pii: 10.1007/s12035-018-1414-0
doi:
Substances chimiques
Gluk1 kainate receptor
0
Neto1 protein, mouse
0
Protein Subunits
0
Receptors, Kainic Acid
0
Receptors, N-Methyl-D-Aspartate
0
Kainic Acid
SIV03811UC
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
4960-4979Subventions
Organisme : Deutsche Forschungsgemeinschaft
ID : WA 541/9-1 and 541/9-2
Références
Hollmann M, Heinemann S (1994) Cloned glutamate receptors. Annu Rev Neurosci 17:31–108. https://doi.org/10.1146/annurev.ne.17.030194.000335
doi: 10.1146/annurev.ne.17.030194.000335
pubmed: 8210177
Lodge D (2009) The history of the pharmacology and cloning of ionotropic glutamate receptors and the development of idiosyncratic nomenclature. Neuropharmacology 56:6–21. https://doi.org/10.1016/j.neuropharm.2008.08.006
doi: 10.1016/j.neuropharm.2008.08.006
pubmed: 18765242
Wu GY, Cline HT (1998) Stabilization of dendritic arbor structure in vivo by CaMKII. Science 279:222–226. https://doi.org/10.1126/science.279.5348.222
doi: 10.1126/science.279.5348.222
pubmed: 9422694
Rajan I, Cline HT (1998) Glutamate receptor activity is required for normal development of tectal cell dendrites in vivo. J Neurosci 18:7836–7846. https://doi.org/10.1523/JNEUROSCI.18-19-07836.1998
doi: 10.1523/JNEUROSCI.18-19-07836.1998
pubmed: 9742152
pmcid: 6793000
Sin WC, Haas K, Ruthazer ES, Cline HT (2002) Dendrite growth increased by visual activity requires NMDA receptor and Rho GTPases. Nature 419:475–480. https://doi.org/10.1038/nature00987
doi: 10.1038/nature00987
pubmed: 12368855
Iwasato T, Datwani A, Wolf AM, Nishiyama H, Taguchi Y, Tonegawa S, Knöpfel T, Erzurumlu RS et al (2000) Cortex-restricted disruption of NMDAR1 impairs neuronal patterns in the barrel cortex. Nature 406:726–731. https://doi.org/10.1038/35021059
doi: 10.1038/35021059
pubmed: 10963597
pmcid: 3558691
Lee L-J, Lo F-S, Erzurumlu RS (2005) NMDA receptor-dependent regulation of axonal and dendritic branching. J Neurosci 25:2304–2311. https://doi.org/10.1523/JNEUROSCI.4902-04.2005
doi: 10.1523/JNEUROSCI.4902-04.2005
pubmed: 15745956
pmcid: 3556734
Haas K, Li J, Cline HT (2006) AMPA receptors regulate experience-dependent dendritic arbor growth in vivo. Proc Natl Acad Sci U S A 103:12127–12131. https://doi.org/10.1073/pnas.0602670103
doi: 10.1073/pnas.0602670103
pubmed: 16882725
pmcid: 1525049
Hamad MIK, Ma-Högemeier Z-L, Riedel C, Conrads C, Veitinger T, Habijan T, Schulz J-N, Krause M et al (2011) Cell class-specific regulation of neocortical dendrite and spine growth by AMPA receptor splice and editing variants. Development 138:4301–4313. https://doi.org/10.1242/dev.071076
doi: 10.1242/dev.071076
pubmed: 21865324
Hamad MIK, Jack A, Klatt O, Lorkowski M, Strasdeit T, Kott S, Sager C, Hollmann M et al (2014) Type I TARPs promote dendritic growth of early postnatal neocortical pyramidal cells in organotypic cultures. Development 141:1737–1748. https://doi.org/10.1242/dev.099697
doi: 10.1242/dev.099697
pubmed: 24667327
Traynelis SF, Wollmuth LP, McBain CJ, Menniti FS, Vance KM, Ogden KK, Hansen KB, Yuan H et al (2010) Glutamate receptor ion channels. Pharmacol Rev 62:405–496. https://doi.org/10.1124/pr.109.002451
doi: 10.1124/pr.109.002451
pubmed: 20716669
pmcid: 2964903
Herb A, Burnashev N, Werner P, Sakmann B, Wisden W, Seeburg PH (1992) The KA-2 subunit of excitatory amino acid receptors shows widespread expression in brain and forms ion channels with distantly related subunits. Neuron 8:775–785. https://doi.org/10.1016/0896-6273(92)90098-X
doi: 10.1016/0896-6273(92)90098-X
pubmed: 1373632
Contractor A, Mulle C, Swanson GT (2011) Kainate receptors coming of age. Trends Neurosci 34:154–163. https://doi.org/10.1016/j.tins.2010.12.002
doi: 10.1016/j.tins.2010.12.002
pubmed: 21256604
pmcid: 3051042
Hadzic M, Jack A, Wahle P (2017) Ionotropic glutamate receptors. J Comp Neurol 525:976–1033. https://doi.org/10.1002/cne.24103
doi: 10.1002/cne.24103
pubmed: 27560295
Wisden W, Seeburg PH (1993) A complex mosaic of high-affinity kainate receptors in rat brain. J Neurosci 13:3582–3598. https://doi.org/10.1523/JNEUROSCI.13-08-03582.1993
doi: 10.1523/JNEUROSCI.13-08-03582.1993
pubmed: 8393486
pmcid: 6576517
Bernard A, Ferhat L, Dessi F, Charton G, Represa A, Ben-Ari Y, Khrestchatisky M (1999) Q/R editing of the rat GluR5 and GluR6 kainate receptors in vivo and in vitro. Eur J Neurosci 11:604–616. https://doi.org/10.1046/j.1460-9568.1999.00479.x
doi: 10.1046/j.1460-9568.1999.00479.x
pubmed: 10051761
Bahn S, Volk B, Wisden W (1994) Kainate receptor gene expression in the developing rat brain. J Neurosci 14:5525–5547. https://doi.org/10.1523/JNEUROSCI.14-09-05525.1994
doi: 10.1523/JNEUROSCI.14-09-05525.1994
pubmed: 8083752
pmcid: 6577101
Paschen W, Dux E, Djuricic B (1994) Developmental changes in the extent of RNA editing of glutamate receptor subunit GluR5 in rat brain. Neurosci Lett 174:109–112. https://doi.org/10.1016/0304-3940(94)90131-7
doi: 10.1016/0304-3940(94)90131-7
pubmed: 7970143
Paschen W, Schmitt J, Gissel C, Dux E (1997) Developmental changes of RNA editing of glutamate receptor subunits GluR5 and GluR6. Brain research. Dev Brain Res 98:271–280. https://doi.org/10.1016/S0165-3806(96)00193-9
doi: 10.1016/S0165-3806(96)00193-9
Valbuena S, Lerma J (2016) Non-canonical signaling, the hidden life of ligand-gated ion channels. Neuron 92:316–329. https://doi.org/10.1016/j.neuron.2016.10.016
doi: 10.1016/j.neuron.2016.10.016
pubmed: 27764665
Sihra TS, Rodriguez-Moreno A (2013) Presynaptic kainate receptor mediated bidirectional modulatory actions: mechanisms. Neurochem Int 62:982–987. https://doi.org/10.1016/j.neuint.2013.03.012
doi: 10.1016/j.neuint.2013.03.012
pubmed: 23538266
Negrete-Díaz JV, Sihra TS, Flores G, Rodríguez-Moreno A (2018) Non-canonical mechanisms of presynaptic kainate receptors controlling glutamate release. Front Mol Neurosci 11:128. https://doi.org/10.3389/fnmol.2018.00128
doi: 10.3389/fnmol.2018.00128
pubmed: 29731708
pmcid: 5920280
Monnerie H, Le Roux PD (2006) Glutamate receptor agonist kainate enhances primary dendrite number and length from immature mouse cortical neurons in vitro. J Neurosci Res 83:944–956. https://doi.org/10.1002/jnr.20805
doi: 10.1002/jnr.20805
pubmed: 16498632
Marques JM, Rodrigues RJ, Valbuena S, Rozas JL, Selak S, Marin P, Aller MI, Lerma J (2013) CRMP2 tethers kainate receptor activity to cytoskeleton dynamics during neuronal maturation. J Neurosci 33:18298–18310. https://doi.org/10.1523/JNEUROSCI.3136-13.2013
doi: 10.1523/JNEUROSCI.3136-13.2013
pubmed: 24227739
pmcid: 6619754
Joseph DJ, Williams DJ, MacDermott AB (2011) Modulation of neurite outgrowth by activation of calcium-permeable kainate receptors expressed by rat nociceptive-like dorsal root ganglion neurons. Dev Neurobiol 71:818–835. https://doi.org/10.1002/dneu.20906
doi: 10.1002/dneu.20906
pubmed: 21557511
pmcid: 3973019
Campbell SL, Mathew SS, Hablitz JJ (2007) Pre- and postsynaptic effects of kainate on layer II/III pyramidal cells in rat neocortex. Neuropharmacology 53:37–47. https://doi.org/10.1016/j.neuropharm.2007.04.008
doi: 10.1016/j.neuropharm.2007.04.008
pubmed: 17543353
pmcid: 2033380
Nasu-Nishimura Y, Jaffe H, Isaac JTR, Roche KW (2010) Differential regulation of kainate receptor trafficking by phosphorylation of distinct sites on GluR6. J Biol Chem 285:2847–2856. https://doi.org/10.1074/jbc.M109.081141
doi: 10.1074/jbc.M109.081141
pubmed: 19920140
Park Y, Jo J, Isaac JTR, Cho K (2006) Long-term depression of kainate receptor-mediated synaptic transmission. Neuron 49:95–106. https://doi.org/10.1016/j.neuron.2005.11.035
doi: 10.1016/j.neuron.2005.11.035
pubmed: 16387642
Petrovic MM, Viana da Silva S, Clement JP, Vyklicky L, Mulle C, González-González IM, Henley JM (2017) Metabotropic action of postsynaptic kainate receptors triggers hippocampal long-term potentiation. Nat Neurosci 20:529–539. https://doi.org/10.1038/nn.4505
doi: 10.1038/nn.4505
pubmed: 28192396
Juuri J, Clarke VRJ, Lauri SE, Taira T (2010) Kainate receptor-induced ectopic spiking of CA3 pyramidal neurons initiates network bursts in neonatal hippocampus. J Neurophysiol 104:1696–1706. https://doi.org/10.1152/jn.00840.2009
doi: 10.1152/jn.00840.2009
pubmed: 20660426
Orav, E., Atanasova, T., Shintyapina, A., Kesaf, S., Kokko, M., Partanen, J., Taira, T., Lauri, S.E. (2017). NETO1 guides development of glutamatergic connectivity in the hippocampus by regulating axonal kainate receptors. eNeuro 4. https://doi.org/10.1523/ENEURO.0048-17.2017
doi: 10.1523/ENEURO.0048-17.2017
Vernon CG, Swanson GT (2017) Neto2 assembles with kainate receptors in DRG neurons during development and modulates neurite outgrowth in adult sensory neurons. J Neurosci 37:3352–3363. https://doi.org/10.1523/JNEUROSCI.2978-16.2017
doi: 10.1523/JNEUROSCI.2978-16.2017
pubmed: 28235897
pmcid: 5373122
Wirth MJ, Wahle P (2003) Biolistic transfection of organotypic cultures of rat visual cortex using a handheld device. J Neurosci Methods 125:45–54. https://doi.org/10.1016/S0165-0270(03)00024-4
doi: 10.1016/S0165-0270(03)00024-4
pubmed: 12763229
Bouskila M, Esoof N, Gay L, Fang EH, Deak M, Begley MJ, Cantley LC, Prescott A et al (2011) TTBK2 kinase substrate specificity and the impact of spinocerebellar-ataxia-causing mutations on expression, activity, localization and development. Biochem J 437:157–167. https://doi.org/10.1042/BJ20110276
doi: 10.1042/BJ20110276
pubmed: 21548880
pmcid: 3739326
Chen TW, Wardill TJ, Sun Y, Pulver SR, Renninger SL, Baohan A, Schreiter ER, Kerr RA et al (2013) Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499(7458):295–300. https://doi.org/10.1038/nature12354
doi: 10.1038/nature12354
pubmed: 23868258
pmcid: 3777791
Yang B, Treweek JB, Kulkarni RP, Deverman BE, Chen CK, Lubeck E, Shah S, Cai L et al (2014) 808 Single-cell phenotyping within transparent intact tissue through whole-body clearing. Cell 158(4):945–958. https://doi.org/10.1016/j.cell.2014.07.017
doi: 10.1016/j.cell.2014.07.017
pubmed: 25088144
pmcid: 4153367
Hamad MIK, Krause M, Wahle P (2015) Improving AM ester calcium dye loading efficiency. J Neurosci Methods 240:48–60. https://doi.org/10.1016/j.jneumeth.2014.11.010
doi: 10.1016/j.jneumeth.2014.11.010
pubmed: 25448382
Pologruto TA, Sabatini BL, Svoboda K (2003) ScanImage. Biomed Eng Online 2:13. https://doi.org/10.1186/1475-925X-2-13
doi: 10.1186/1475-925X-2-13
pubmed: 12801419
pmcid: 161784
Rasband WS (1997–2012) ImageJ. National Institutes of Health, Bethesda, MD, USA. Available online at: https://imagej.nih.gov/ij/
Hoerder-Suabedissen A, Paulsen O, Molnar Z (2008) Thalamocortical maturation in mice is influenced by body weight. J Comp Neurol 511:415–420. https://doi.org/10.1002/cne.21853
doi: 10.1002/cne.21853
pubmed: 18803242
Oh E, Maejima T, Liu C, Deneris E, Herlitze S (2010) Substitution of 5-HT1A receptor signaling by a light-activated G protein-coupled receptor. J Biol Chem 285:30825–30836. https://doi.org/10.1074/jbc.M110.147298
doi: 10.1074/jbc.M110.147298
pubmed: 20643652
pmcid: 2945576
Lauri SE, Taira T (2011) Role of kainate receptors in network activity during development. Adv Exp Med Biol 717:81–91. https://doi.org/10.1007/978-1-4419-9557-5_8
doi: 10.1007/978-1-4419-9557-5_8
pubmed: 21713669
Beed PS, Salmen B, Schmitz D (2009) GluK2-mediated excitability within the superficial layers of the entorhinal cortex. PLoS One 4:e5576. https://doi.org/10.1371/journal.pone.0005576
doi: 10.1371/journal.pone.0005576
pubmed: 19440371
pmcid: 2679203
Clarke VR, Ballyk BA, Hoo KH, Mandelzys A, Pellizzari A, Bath CP, Thomas J, Sharpe EF et al (1997) A hippocampal GluR5 kainate receptor regulating inhibitory synaptic transmission. Nature 389:599–603. https://doi.org/10.1038/39315
doi: 10.1038/39315
pubmed: 9335499
Cossart R, Esclapez M, Hirsch JC, Bernard C, Ben-Ari Y (1998) GluR5 kainate receptor activation in interneurons increases tonic inhibition of pyramidal cells. Nat Neurosci 1:470–478. https://doi.org/10.1038/2185
doi: 10.1038/2185
pubmed: 10196544
Frerking M, Malenka RC, Nicoll RA (1998) Synaptic activation of kainate receptors on hippocampal interneurons. Nat Neurosci 1:479–486. https://doi.org/10.1038/2194
doi: 10.1038/2194
pubmed: 10196545
Khalilov I, Hirsch J, Cossart R, Ben-Ari Y (2002) Paradoxical anti-epileptic effects of a GluR5 agonist of kainate receptors. J Neurophysiol 88:523–527. https://doi.org/10.1152/jn.2002.88.1.523
doi: 10.1152/jn.2002.88.1.523
pubmed: 12091575
Rodríguez-Moreno A, López-García JC, Lerma J (2000) Two populations of kainate receptors with separate signaling mechanisms in hippocampal interneurons. Proc Natl Acad Sci U S A 97:1293–1298. https://doi.org/10.1073/pnas
doi: 10.1073/pnas
pubmed: 10655524
pmcid: 15601
Cunningham MO, Davies CH, Buhl EH, Kopell N, Whittington MA (2003) Gamma oscillations induced by kainate receptor activation in the entorhinal cortex in vitro. J Neurosci 23:9761–9769. https://doi.org/10.1523/JNEUROSCI.23-30-09761.2003
doi: 10.1523/JNEUROSCI.23-30-09761.2003
pubmed: 14586003
pmcid: 6740890
Fisahn A, Contractor A, Traub RD, Buhl EH, Heinemann SF, McBain CJ (2004) Distinct roles for the kainate receptor subunits GluR5 and GluR6 in kainate-induced hippocampal gamma oscillations. J Neurosci 24:9658–9668. https://doi.org/10.1523/JNEUROSCI.2973-04.2004
doi: 10.1523/JNEUROSCI.2973-04.2004
pubmed: 15509753
pmcid: 6730151
Melyan Z, Wheal HV, Lancaster B (2002) Metabotropic-mediated kainate receptor regulation of IsAHP and excitability in pyramidal cells. Neuron 34:107–114. https://doi.org/10.1016/S0896-6273(02)00624-4
doi: 10.1016/S0896-6273(02)00624-4
pubmed: 11931745
Melyan Z, Lancaster B, Wheal HV (2004) Metabotropic regulation of intrinsic excitability by synaptic activation of kainate receptors. J Neurosci 24:4530–4534. https://doi.org/10.1523/JNEUROSCI.5356-03.2004
doi: 10.1523/JNEUROSCI.5356-03.2004
pubmed: 15140923
pmcid: 1351223
Mulle C, Sailer A, Pérez-Otaño I, Dickinson-Anson H, Castillo PE, Bureau I, Maron C, Gage FH et al (1998) Altered synaptic physiology and reduced susceptibility to kainate-induced seizures in GluR6-deficient mice. Nature 392:601–605. https://doi.org/10.1038/33408
doi: 10.1038/33408
pubmed: 9580260
Nieding K, Matschke V, Meuth SG, Lang F, Seebohm G, Strutz-Seebohm N (2016) Tau tubulin kinase TTBK2 sensitivity of glutamate receptor GluK2. Cell Physiol Biochem 39:1444–1452. https://doi.org/10.1159/000447847
doi: 10.1159/000447847
pubmed: 27607061
Fièvre S, Carta M, Chamma I, Labrousse V, Thoumine O, Mulle C (2016) Molecular determinants for the strictly compartmentalized expression of kainate receptors in CA3 pyramidal cells. Nat Commun 7:12738. https://doi.org/10.1038/ncomms12738
doi: 10.1038/ncomms12738
pubmed: 27669960
pmcid: 5052629
Bureau I, Bischoff S, Heinemann SF, Mulle C (1999) Kainate receptor-mediated responses in the CA1 field of wild-type and GluR6-deficient mice. J Neurosci 19:653–663. https://doi.org/10.1523/JNEUROSCI.19-02-00653.1999
doi: 10.1523/JNEUROSCI.19-02-00653.1999
pubmed: 9880586
pmcid: 6782223
Petralia RS, Wang YX, Wenthold RJ (1994) Histological and ultrastructural localization of the kainate receptor subunits, KA2 and GluR6/7, in the rat nervous system using selective antipeptide antibodies. J Comp Neurol 349:85–110. https://doi.org/10.1002/cne.903490107
doi: 10.1002/cne.903490107
pubmed: 7852627
Copits BA, Swanson GT (2012) Dancing partners at the synapse. Nat Rev Neurosci 13:675–686. https://doi.org/10.1038/nrn3335
doi: 10.1038/nrn3335
pubmed: 22948074
pmcid: 3520510
Zhang W, St-Gelais F, Grabner CP, Trinidad JC, Sumioka A, Morimoto-Tomita M, Kim KS, Straub C et al (2009) A transmembrane accessory subunit that modulates kainate-type glutamate receptors. Neuron 61:385–396. https://doi.org/10.1111/ejn.12519
doi: 10.1111/ejn.12519
pubmed: 19217376
pmcid: 2803770
Palacios-Filardo J, Aller MI, Lerma J (2016) Synaptic targeting of kainate receptors. Cereb Cortex 26:1464–1472. https://doi.org/10.1093/cercor/bhu244
doi: 10.1093/cercor/bhu244
pubmed: 25316333
Wyeth MS, Pelkey KA, Yuan X, Vargish G, Johnston AD, Hunt S, Fang C, Abebe D et al (2017) Neto auxiliary subunits regulate interneuron somatodendritic and presynaptic kainate receptors to control network inhibition. Cell Rep 20:2156–2168. https://doi.org/10.1016/j.celrep.2017.08.017
doi: 10.1016/j.celrep.2017.08.017
pubmed: 28854365
pmcid: 5600503
Fisher JL, Mott DD (2011) Distinct functional roles of subunits within the heteromeric kainate receptor. J Neurosci 31:17113–17122. https://doi.org/10.1523/JNEUROSCI.3685-11.2011
doi: 10.1523/JNEUROSCI.3685-11.2011
pubmed: 22114280
pmcid: 3237056
Paternain AV, Rodríguez-Moreno A, Villarroel A, Lerma J (1998) Activation and desensitization properties of native and recombinant kainate receptors. Neuropharmacology 37:1249–1259. https://doi.org/10.1016/S0028-3908(98)00098-7
doi: 10.1016/S0028-3908(98)00098-7
pubmed: 9849662
Fernandes HB, Catches JS, Petralia RS, Copits BA, Xu J, Russell TA, Swanson GT, Contractor A (2009) High-affinity kainate receptor subunits are necessary for ionotropic but not metabotropic signaling. Neuron 63:818–829. https://doi.org/10.1016/j.neuron.2009.08.010
doi: 10.1016/j.neuron.2009.08.010
pubmed: 19778510
pmcid: 2756730
Barberis A, Sachidhanandam S, Mulle C (2008) GluR6/KA2 kainate receptors mediate slow-deactivating currents. J Neurosci 28:6402–6406. https://doi.org/10.1523/JNEUROSCI.1204-08.2008
doi: 10.1523/JNEUROSCI.1204-08.2008
pubmed: 18562611
pmcid: 6670893
Ibarretxe G, Perrais D, Jaskolski F, Vimeney A, Mulle C (2007) Fast regulation of axonal growth cone motility by electrical activity. J Neurosci 27:7684–7695. https://doi.org/10.1523/JNEUROSCI.1070-07.2007
doi: 10.1523/JNEUROSCI.1070-07.2007
pubmed: 17634363
pmcid: 6672867
Tashiro A, Dunaevsky A, Blazeski R, Mason CA, Yuste R (2003) Bidirectional regulation of hippocampal mossy fiber filopodial motility by kainate receptors. Neuron 38:773–784. https://doi.org/10.1016/S0896-6273(03)00299-X
doi: 10.1016/S0896-6273(03)00299-X
pubmed: 12797961
Dai W-M, Christensen KV, Egebjerg J, Ebert B, Lambert JDC (2002) Correlation of the expression of kainate receptor subtypes to responses evoked in cultured cortical and spinal cord neurones. Brain Res 926:94–107. https://doi.org/10.1016/S0006-8993(01)03308-X
doi: 10.1016/S0006-8993(01)03308-X
pubmed: 11814411
Paternain AV, Herrera MT, Nieto MA, Lerma J (2000) GluR5 and GluR6 kainate receptor subunits coexist in hippocampal neurons and coassemble to form functional receptors. J Neurosci 20:196–205. https://doi.org/10.1523/JNEUROSCI.20-01-00196.2000
doi: 10.1523/JNEUROSCI.20-01-00196.2000
pubmed: 10627597
pmcid: 6774114
Eder M, Becker K, Rammes G, Schierloh A, Azad SC, Zieglgänsberger W, Dodt H-U (2003) Distribution and properties of functional postsynaptic kainate receptors on neocortical layer V pyramidal neurons. J Neurosci 23:6660–6670. https://doi.org/10.1523/JNEUROSCI.23-16-06660.2003
doi: 10.1523/JNEUROSCI.23-16-06660.2003
pubmed: 12878707
pmcid: 6740632
Sommer B, Keinänen K, Verdoorn TA, Wisden W, Burnashev N, Herb A, Köhler M, Takagi T et al (1990) Flip and flop: a cell-specific functional switch in glutamate-operated channels of the CNS. Science 249:1580–1585. https://doi.org/10.1126/science.1699275
doi: 10.1126/science.1699275
pubmed: 1699275
Ali AB (2003) Involvement of post-synaptic kainate receptors during synaptic transmission between unitary connections in rat neocortex. Eur J Neurosci 17:2344–2350. https://doi.org/10.1046/j.1460-9568.2003.02677.x
doi: 10.1046/j.1460-9568.2003.02677.x
pubmed: 12814386
Swanson GT, Feldmeyer D, Kaneda M, Cull-Candy SG (1996) Effect of RNA editing and subunit co-assembly single-channel properties of recombinant kainate receptors. J Physiol 492:129–142. https://doi.org/10.1113/jphysiol.1996.sp021295
doi: 10.1113/jphysiol.1996.sp021295
pubmed: 8730589
pmcid: 1158867
Chow DK, Groszer M, Pribadi M, Machniki M, Carmichael ST, Liu X, Trachtenberg JT (2009) Laminar and compartmental regulation of dendritic growth in mature cortex. Nat Neurosci 12:116–118. https://doi.org/10.1038/nn.2255
doi: 10.1038/nn.2255
pubmed: 19151711
pmcid: 2842592
Romand S, Wang Y, Toledo-Rodriguez M, Markram H (2011) Morphological development of thick-tufted layer v pyramidal cells in the rat somatosensory cortex. Front Neuroanat 5:5. https://doi.org/10.3389/fnana.2011.00005
doi: 10.3389/fnana.2011.00005
pubmed: 21369363
pmcid: 3043270
Han Y, Wang C, Park JS, Niu L (2012) Channel-opening kinetic mechanism of wild-type GluK1 kainate receptors and a C-terminal mutant. Biochemistry 51:761–768. https://doi.org/10.1021/bi201446z
doi: 10.1021/bi201446z
pubmed: 22191429
pmcid: 3272274
Salmen B, Beed PS, Ozdogan T, Maier N, Johenning FW, Winterer J, Breustedt J, Schmitz D (2012) GluK1 inhibits calcium dependent and independent transmitter release at associational/commissural synapses in area CA3 of the hippocampus. Hippocampus 22:57–68. https://doi.org/10.1002/hipo.20846
doi: 10.1002/hipo.20846
pubmed: 20848601
Vignes M, Clarke VR, Parry MJ, Bleakman D, Lodge D, Ornstein PL, Collingridge GL (1998) The GluR5 subtype of kainate receptor regulates excitatory synaptic transmission in areas CA1 and CA3 of the rat hippocampus. Neuropharmacology 37:1269–1277. https://doi.org/10.1016/S0028-3908(98)00148-8
doi: 10.1016/S0028-3908(98)00148-8
pubmed: 9849664
Wu L-J, Xu H, Ren M, Zhuo M (2007) Genetic and pharmacological studies of GluR5 modulation of inhibitory synaptic transmission in the anterior cingulate cortex of adult mice. Dev Neurobiol 67:146–157. https://doi.org/10.1002/dneu.20331
doi: 10.1002/dneu.20331
pubmed: 17443779
Wu L-J, Zhao M-G, Toyoda H, Ko SW, Zhuo M (2005) Kainate receptor-mediated synaptic transmission in the adult anterior cingulate cortex. J Neurophysiol 94:1805–1813. https://doi.org/10.1152/jn.00091.2005
doi: 10.1152/jn.00091.2005
pubmed: 15928066
Andrade-Talavera Y, Duque-Feria P, Negrete-Díaz JV, Sihra TS, Flores G, Rodríguez-Moreno A (2012) Presynaptic kainate receptor-mediated facilitation of glutamate release involves Ca
doi: 10.1111/j.1471-4159.2012.07844.x
pubmed: 22731109
Rodríguez-Moreno A, Sihra TS (2013) Presynaptic kainate receptor-mediated facilitation of glutamate release involves Ca
doi: 10.1016/j.febslet.2013.01.071
pubmed: 23416300