Skip to main content

Advertisement

Log in

Development of Cortical Pyramidal Cell and Interneuronal Dendrites: a Role for Kainate Receptor Subunits and NETO1

  • Published:
Molecular Neurobiology Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. Hollmann M, Heinemann S (1994) Cloned glutamate receptors. Annu Rev Neurosci 17:31–108. https://doi.org/10.1146/annurev.ne.17.030194.000335

    Article  CAS  PubMed  Google Scholar 

  2. 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

    Article  CAS  PubMed  Google Scholar 

  3. 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

    Article  CAS  PubMed  Google Scholar 

  4. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. 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

    Article  CAS  PubMed  Google Scholar 

  6. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. 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

    Article  CAS  PubMed  Google Scholar 

  10. 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

    Article  CAS  PubMed  Google Scholar 

  11. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. 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

    Article  CAS  PubMed  Google Scholar 

  13. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Hadzic M, Jack A, Wahle P (2017) Ionotropic glutamate receptors. J Comp Neurol 525:976–1033. https://doi.org/10.1002/cne.24103

    Article  CAS  PubMed  Google Scholar 

  15. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. 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

    Article  CAS  PubMed  Google Scholar 

  17. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. 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

    Article  CAS  PubMed  Google Scholar 

  19. 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

    Article  CAS  Google Scholar 

  20. 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

    Article  CAS  PubMed  Google Scholar 

  21. 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

    Article  CAS  PubMed  Google Scholar 

  22. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. 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

    Article  CAS  PubMed  Google Scholar 

  24. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. 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

    Article  CAS  PubMed  Google Scholar 

  28. 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

    Article  CAS  PubMed  Google Scholar 

  29. 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

    Article  CAS  PubMed  Google Scholar 

  30. 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

    Article  CAS  PubMed  Google Scholar 

  31. 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

    Article  Google Scholar 

  32. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. 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

    Article  CAS  PubMed  Google Scholar 

  34. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. 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

    Article  CAS  PubMed  Google Scholar 

  38. Pologruto TA, Sabatini BL, Svoboda K (2003) ScanImage. Biomed Eng Online 2:13. https://doi.org/10.1186/1475-925X-2-13

    Article  PubMed  PubMed Central  Google Scholar 

  39. Rasband WS (1997–2012) ImageJ. National Institutes of Health, Bethesda, MD, USA. Available online at: https://imagej.nih.gov/ij/

  40. 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

    Article  PubMed  Google Scholar 

  41. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. 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

    Article  CAS  PubMed  Google Scholar 

  43. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. 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

    Article  CAS  PubMed  Google Scholar 

  45. 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

    Article  CAS  PubMed  Google Scholar 

  46. 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

    Article  CAS  PubMed  Google Scholar 

  47. 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

    Article  CAS  PubMed  Google Scholar 

  48. 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

    Article  PubMed  PubMed Central  Google Scholar 

  49. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. 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

    Article  CAS  PubMed  Google Scholar 

  52. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. 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

    Article  CAS  PubMed  Google Scholar 

  54. 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

    Article  CAS  PubMed  Google Scholar 

  55. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. 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

    Article  CAS  PubMed  Google Scholar 

  58. Copits BA, Swanson GT (2012) Dancing partners at the synapse. Nat Rev Neurosci 13:675–686. https://doi.org/10.1038/nrn3335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. 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

    Article  PubMed  Google Scholar 

  61. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. 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

    Article  CAS  PubMed  Google Scholar 

  64. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. 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

    Article  CAS  PubMed  Google Scholar 

  68. 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

    Article  CAS  PubMed  Google Scholar 

  69. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. 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

    Article  CAS  PubMed  Google Scholar 

  72. 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

    Article  PubMed  Google Scholar 

  73. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. 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

    Article  PubMed  PubMed Central  Google Scholar 

  76. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. 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

    Article  CAS  PubMed  Google Scholar 

  78. 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

    Article  CAS  PubMed  Google Scholar 

  79. 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

    Article  CAS  PubMed  Google Scholar 

  80. 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

    Article  CAS  PubMed  Google Scholar 

  81. 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 Ca2+-calmodulin at mossy fiber-CA3 synapses. J Neurochem 122:891–899. https://doi.org/10.1111/j.1471-4159.2012.07844.x

    Article  CAS  PubMed  Google Scholar 

  82. Rodríguez-Moreno A, Sihra TS (2013) Presynaptic kainate receptor-mediated facilitation of glutamate release involves Ca2+-calmodulin and PKA in cerebrocortical synaptosomes. FEBS Lett 587:788–792. https://doi.org/10.1016/j.febslet.2013.01.071

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Andrea Räk, Sabine Schönfelder, and Christian Riedel for technical support. We thank Prof. Nathalie Strutz-Seebohm, University Münster, for providing the TTBK2-KD plasmid. We thank Prof. Andreas Reiner, Ruhr University Bochum, for discussion. We thank Bente Janssen-Weets and Felix Burgmann for help with reconstructions during their BSc thesis work.

Funding

Supported by Deutsche Forschungsgemeinschaft grants WA 541/9-1 and 541/9-2.

Author information

Authors and Affiliations

Authors

Contributions

AJ, MIKH, and PW designed experiments. AJ, MIKH, SG, SG, SP, and PW performed experiments. AJ and PW did the data management and interpretation. AJ and PW wrote the manuscript. MH commented on the manuscript. All authors approved the final version.

Corresponding author

Correspondence to Petra Wahle.

Ethics declarations

Conflict of Interest

The authors declare that they do not have any conflict of interest.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jack, A., Hamad, M.I.K., Gonda, S. et al. Development of Cortical Pyramidal Cell and Interneuronal Dendrites: a Role for Kainate Receptor Subunits and NETO1. Mol Neurobiol 56, 4960–4979 (2019). https://doi.org/10.1007/s12035-018-1414-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12035-018-1414-0

Keywords

Navigation