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In the Developing Hippocampus Kainate Receptors Control the Release of GABA from Mossy Fiber Terminals via a Metabotropic Type of Action

  • Chapter
Kainate Receptors

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 717))

Abstract

Kainate receptors (KARs) are glutamate-gated ion channels assembled from various combinations of GluK1-GluK5 subunits with different physiological and pharmacological properties. In the hippocampus, KARs expressed at postsynaptic sites mediate a small component of excitatory postsynaptic currents while at presynaptic sites they exert a powerful control on transmitter release at both excitatory and inhibitory connections. KARs are developmentally regulated and play a key role in several developmental processes including neuronal migration, differentiation and synapse formation. Interestingly, they can signal through a canonical ionotropic pathway but also through a noncanonical modality involving pertussis toxin-sensitive G proteins and downstream signaling molecules.

In this Chapter some of our recent data concerning the functional role of presynaptic KARs in regulation of transmitter release from immature mossy fiber terminals and in synaptic plasticity processes will be reviewed. Early in postnatal development, MFs release into their targeted neurons mainly GABA which is depolarizing and excitatory. Endogenous activation of GluK1 KARs localized on MF terminals by glutamate present in the extracellular space down regulates GABA release, leading sometimes to synapse silencing. The depressant effect of GluK1 on MF responses is mediated by a metabotropic process, sensitive to pertussis toxin and phospholipase C (PLC) along the transduction pathway downstream to G protein activation. Blocking PLC with the selective antagonist U73122, unmasks the potentiating effect of GluK1 on MF-evoked GABAergic currents, which probably depend on the ionotropic type of action of these receptors.

In addition, GluK1 KARs dynamically regulate the direction of spike-time dependent plasticity, a particular form of Hebbian type of learning which consists in bidirectional modifications in synaptic strength according to the temporal order of pre and postsynaptic spiking. At immature MF-CA3 synapses pairing MF stimulation with postsynaptic spiking and vice versa induces long term depression of MF-evoked GABAergic currents. In the case of positive pairing synaptic depression can be switched into spike-time dependent potentiation by blocking GluK1 KARs with UBP 302. The depressant action exerted by GluK1 KARs on MF responses would prevent the excessive activation of the CA3 associative network by the excitatory action of GABA early in postnatal development.

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  1. Neurobiology Sector and IIT Unit, Internationa School of Advanced Studies (SISSA), Ed. Q1 Area Science Park, S.S. 14 Km 163.5, 34012, Basovizza, Trieste, Italy

    Enrico Cherubini

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  1. Enrico Cherubini
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  2. Maddalena D. Caiati
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  3. Sudhir Sivakumaran
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Correspondence to Enrico Cherubini .

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  1. Departamento de Fisiología, Anatomía y Biología Celular, Universidad Pablo de Olavide, Sevilla, Spain

    Antonio Rodríguez-Moreno PhD

  2. Department of Neuroscience, Physiology and Pharmacology, University College London, London, UK

    Talvinder S. Sihra PhD

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Cherubini, E., Caiati, M.D., Sivakumaran, S. (2011). In the Developing Hippocampus Kainate Receptors Control the Release of GABA from Mossy Fiber Terminals via a Metabotropic Type of Action. In: Rodríguez-Moreno, A., Sihra, T.S. (eds) Kainate Receptors. Advances in Experimental Medicine and Biology, vol 717. Springer, Boston, MA. https://doi.org/10.1007/978-1-4419-9557-5_2

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