Kainate Receptor-Induced Retrograde Inhibition of Glutamatergic Transmission in Vasopressin Neurons
Journal of Neuroscience. 2012-01-25; 32(4): 1301-1310
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1. J Neurosci. 2012 Jan 25;32(4):1301-10. doi: 10.1523/JNEUROSCI.3017-11.2012.
Kainate receptor-induced retrograde inhibition of glutamatergic transmission in
Bonfardin VD(1), Theodosis DT, Konnerth A, Oliet SH.
(1)Inserm, Unité 862, Neurocentre Magendie, 33077 Bordeaux, France.
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
Ca2+ 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 κ-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 κ-opioid receptors to inhibit glutamate release.
PMID: 22279215 [Indexed for MEDLINE]