Target-Cell Specificity of Kainate Autoreceptor and Ca<sup>2+</sup>-Store-Dependent Short-Term Plasticity at Hippocampal Mossy Fiber Synapses

Scott, Ricardo; Lalic, Tatjana; Kullmann, Dimitri M.; Capogna, Marco; Rusakov, Dmitri A.

doi:10.1523/jneurosci.2932-08.2008

Cited by 72 publications

(116 citation statements)

References 48 publications

(78 reference statements)

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“…A similar mechanism thus appears to be triggered in VP neurons when postsynaptic Ca 2ϩ -permeable Gluk1-containing KARs are activated, leading to the Ca 2ϩ -dependent release of a retrograde signal. Our data, however, do not allow us to assess whether the entry of Ca 2ϩ through GluK1-containing KARs is sufficient by itself to induce the release of dynorphin or whether other mechanisms, such as Ca 2ϩ release from intracellular stores, also contribute to this process (Lauri et al, 2003;Mathew and Hablitz, 2008;Scott et al, 2008).…”

Section: Indirect Inhibitory Action Of Kars On Glutamatergic Inputs Tmentioning

confidence: 76%

Kainate Receptor-Induced Retrograde Inhibition of Glutamatergic Transmission in Vasopressin Neurons

Bonfardin

Theodosis²,

Konnerth³

et al. 2012

J. Neurosci.

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Presynaptic kainate receptors (KARs) exert a modulatory action on transmitter release. We here report that applications of agonists of GluK1-containing KARs in the rat supraoptic nucleus has an opposite action on glutamatergic transmission according to the phenotype of the postsynaptic neuron. Whereas glutamate release was facilitated in oxytocin (OT) neurons, it was inhibited in vasopressin (VP) cells. Interestingly, an antagonist of GluK1-containing KARs caused an inhibition of glutamate release in both OT and VP neurons, revealing the existence of tonically activated presynaptic KARs that are positively coupled to transmitter release. We thus postulated that the inhibition of glutamate release observed with exogenous applications of GluK1 agonists on VP neurons could be indirect. In agreement with this hypothesis, we first showed that functional GluK1-containing KARs were present postsynaptically on VP neurons but not on OT cells. We next showed that the inhibitory effect induced by exogenous GluK1 receptor agonist was compromised when BAPTA was added in the recording pipette to buffer intracellular Ca 2ϩ and block the release of a putative retrograde messenger. Under these conditions, GluK1-containing KAR agonist facilitates glutamatergic transmission in VP neurons in a manner similar to that observed for OT neurons and that resulted from the activation of presynaptic GluK1 receptors. GluK1-mediated inhibition of glutamate release in VP neurons was also blocked by a -opioid receptor antagonist. These findings suggest that activation of postsynaptic GluK1-containing KARs on VP neurons leads to the release of dynorphin, which in turn acts on presynaptic -opioid receptors to inhibit glutamate release.

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Section: Indirect Inhibitory Action Of Kars On Glutamatergic Inputs Tmentioning

confidence: 76%

Kainate Receptor-Induced Retrograde Inhibition of Glutamatergic Transmission in Vasopressin Neurons

Bonfardin

Theodosis²,

Konnerth³

et al. 2012

J. Neurosci.

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“…Alternatively, activation of presynaptic kainate receptors at the release site could initiate an intracellular cascade that would propagate to other release sites. Likely candidates include calcium stores that are present at mossy fibers (Scott et al, 2008) and modulate short-term plasticity (Lauri et al, 2003;Scott et al, 2008).…”

Section: Implications For Gluk3 Receptor Function In Synaptic Transmimentioning

confidence: 99%

Atypical Functional Properties of GluK3-Containing Kainate Receptors

Perrais¹,

Coussen²,

Mulle³

2009

J. Neurosci.

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The properties of synaptic receptors determine their mode of action at presynaptic and postsynaptic loci. Here, we investigated the atypical biophysical properties of GluK3-containing kainate receptors, which contribute to presynaptic facilitation at hippocampal mossy fiber synapses. We show, using fast glutamate applications on outside-out patches and kinetic modeling, that the low sensitivity of GluK3 receptors for glutamate is attributable to fast desensitization of partially bound receptors. Consequently, these receptors can only be activated by fast transients of high glutamate concentration. In addition, GluK3 receptors are very sensitive to voltage-dependent block by intracellular spermine that precludes activation of substantial currents at potentials positive to Ϫ50 mV. Two specific residues within the channel pore define this high-affinity site. Finally, GluK3 are calcium permeable in the same way as unedited GluK2 receptors. These receptors present unique properties among AMPA/kainate receptors that could reflect a specialized presynaptic function.

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“…How can an increased MF excitability be reconciled with a depression of GABA release? Although, according to Kamiya and Ozawa (2000), a downregulation of transmitter release may occur via inactivation of Na ϩ / Ca 2ϩ channels or electrical shunting, this seems unlikely in view of the recent finding of KA-induced facilitation of action potential evoked calcium entry in MF boutons via a calcium storedependent mechanism (Scott et al, 2008). In addition, it is worth noting that, unlike adults, immature MFs terminate in very small spherical expansions (Amaral and Dent, 1981) and do not exhibit use-dependent synaptic facilitation yet (Marchal and Mulle, 2004).…”

Section: Discussionmentioning

confidence: 98%

“…7C,D). Since GluK1 receptors are known to be highly permeable to calcium (Lauri et al, 2003;Scott et al, 2008), in another set of experiments we applied PhTx (3 M), which blocks calciumpermeable AMPA/kainate receptor (Fletcher and Lodge, 1996). As UBP 302, PhTx significantly reduced the number of successes from 0.59 Ϯ 0.04 to 0.15 Ϯ 0.05 (n ϭ 7; p ϭ 0.001) (Fig.…”

Section: Activation Of Presynaptic Kainate Receptors Enhances Mf Excimentioning

confidence: 94%

“…In particular, activation of KARs localized on glutamatergic mossy fibers (MFs), the axons of dentate gyrus granule cells, enhances glutamate release particularly during frequency-dependent facilitation, a form of short-term plasticity characteristic of MF-CA3 synapses (Contractor et al, 2001;Lauri et al, 2001a;Schmitz et al, 2001) (but see Kwon and Castillo, 2008). This effect has been attributed to kainate-induced depolarization of presynaptic boutons or axon terminals (Lauri et al, 2001b;Kamiya et al, 2002;Nicoll and Schmitz, 2005) and the release of calcium from local stores (Scott et al, 2008). Interestingly, KARs are present also on presynaptic GABAergic terminals, where they exert either a facilitatory (Mulle et al, 2000;Cossart et al, 2001) or a depressant (Clarke et al, 1997;Rodríguez-Moreno et al, 1997;Rodríguez-Moreno and Lerma, 1998;Maingret et al, 2005) effect on GABA release.…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

In the Developing Rat Hippocampus, Endogenous Activation of Presynaptic Kainate Receptors Reduces GABA Release from Mossy Fiber Terminals

Caiati¹,

Sivakumaran²,

Cherubini³

2010

J. Neurosci.

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Target-Cell Specificity of Kainate Autoreceptor and Ca²⁺-Store-Dependent Short-Term Plasticity at Hippocampal Mossy Fiber Synapses

Cited by 72 publications

References 48 publications

Kainate Receptor-Induced Retrograde Inhibition of Glutamatergic Transmission in Vasopressin Neurons

Kainate Receptor-Induced Retrograde Inhibition of Glutamatergic Transmission in Vasopressin Neurons

Atypical Functional Properties of GluK3-Containing Kainate Receptors

In the Developing Rat Hippocampus, Endogenous Activation of Presynaptic Kainate Receptors Reduces GABA Release from Mossy Fiber Terminals

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Target-Cell Specificity of Kainate Autoreceptor and Ca2+-Store-Dependent Short-Term Plasticity at Hippocampal Mossy Fiber Synapses

Cited by 72 publications

References 48 publications

Kainate Receptor-Induced Retrograde Inhibition of Glutamatergic Transmission in Vasopressin Neurons

Kainate Receptor-Induced Retrograde Inhibition of Glutamatergic Transmission in Vasopressin Neurons

Atypical Functional Properties of GluK3-Containing Kainate Receptors

In the Developing Rat Hippocampus, Endogenous Activation of Presynaptic Kainate Receptors Reduces GABA Release from Mossy Fiber Terminals

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Target-Cell Specificity of Kainate Autoreceptor and Ca²⁺-Store-Dependent Short-Term Plasticity at Hippocampal Mossy Fiber Synapses