Muscarinic Enhancement of R-Type Calcium Currents in Hippocampal CA1 Pyramidal Neurons

Tai, Cheng‐Chi; Kuzmiski, J. Brent; MacVicar, Brian A.

doi:10.1523/jneurosci.1009-06.2006

Cited by 59 publications

(71 citation statements)

References 65 publications

(96 reference statements)

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“…This finding agrees with a recent demonstration by Tai et al (2006) that the voltage dependence of activation of native R-type currents is shifted to negative potentials during modulation by muscarinic acetylcholine receptors. It is worth noting that the negative shift in voltage dependence reported here and by Tai et al (2006) is opposite that typically observed for G protein-inhibited channels of the Ca V 2 family. Additional experiments are needed to elucidate the underlying mechanism.…”

Section: Discussionsupporting

confidence: 93%

“…Several previous studies demonstrated that Ca V 2.3 and native R-type currents are modulated by signaling mechanisms linked to G protein-coupled receptors (Wu et al, 1998;Yu and Shinnick-Gallagher, 1998;Meza et al, 1999;Melliti et al, 2000;Sabatini and Svoboda, 2000;Bannister et al, 2004;Kohlmeier and Leonard, 2006;Tai et al, 2006). In our previous experiments, we showed that Ca V 2.3 is both inhibited and stimulated through G␣ q/11 -coupled muscarinic acetylcholine receptors (Meza et al, 1999;Melliti et al, 2000;Bannister et al, 2004).…”

mentioning

confidence: 57%

“…For example, Yu and Shinnick-Gallagher (1998) showed that native R-type currents are stimulated through corticotropin-releasing factor receptors in central amygdala neurons. In addition, Tai et al (2006) showed that native R-type currents are stimulated through muscarinic acetylcholine and metabotropic glutamate receptors in hippocampal CA1 neurons. Our present experiments indicate that PKC mediated stimulation of Ca V 2.3 through NK1 receptors (Fig.…”

Section: Discussionmentioning

confidence: 99%

“…Recent studies have begun to elucidate the physiological roles of both R-type currents and Ca V 2.3. For example, R-type currents have been shown to participate in neurosecretion and in the formation of afterdepolarizations, plateau potentials, and bursting activity in hippocampal CA1 pyramidal neurons (Wu et al, 1998;Gasparini et al, 2001;Kuzmiski et al, 2005;Metz et al, 2005;Tai et al, 2006). Studies also indicate that native R-type channels mediate Ca 2ϩ entry into dendritic spines (Sabatini and Svoboda, 2000) and that R-type channels play important roles in synaptic plasticity (Yasuda et al, 2003;Humeau et al, 2005).…”

mentioning

confidence: 99%

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Neurokinin 1 Receptors Trigger Overlapping Stimulation and Inhibition of Ca_V2.3 (R-Type) Calcium Channels

Meza

Thapliyal²,

Bannister³

et al. 2006

Mol Pharmacol

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Neurokinin (NK) 1 receptors and Ca V 2.3 calcium channels are both expressed in nociceptive neurons, and mice lacking either protein display altered responses to noxious stimuli. Here, we examined modulation of Ca V 2.3 through NK1 receptors expressed in human embryonic kidney 293 cells. We find that NK1 receptors generate complex modulation of Ca V 2.3. In particular, weak activation of these receptors evokes mainly stimulation of Ca V 2.3, whereas strong receptor activation elicits profound inhibition that overlaps with channel stimulation. Unlike R-type channels encoded by Ca V 2.3, L-type (Ca V 1.3), Ntype (Ca V 2.2), and P/Q-type (Ca V 2.1) channels are inhibited, but not stimulated, through NK1 receptors. Pharmacological experiments show that protein kinase C (PKC) mediates stimulation of Ca V 2.3 through NK1 receptors. The signaling mechanisms underlying inhibition were explored by expressing proteins that buffer either G␣ q/11 (regulator of G protein signaling protein 3T and carboxyl-terminal region of phospholipase C-␤1) or G␤␥ subunits (transducin and the carboxyl-terminal region of bovine G-protein-coupled receptor kinase). A fast component of inhibition was attenuated by buffering G␤␥, whereas a slow component of inhibition was reduced by buffering G␣ q/11 . When both G␤␥ and G␣ q/11 were simultaneously buffered in the same cells, inhibition was virtually eliminated, but receptor activation still triggered substantial stimulation of Ca V 2.3. We also report that NK1 receptors accelerate the inactivation kinetics of Ca V 2.3 currents. Altogether, our results indicate that NK1 receptors modulate Ca V 2.3 using three different signaling mechanisms: a fast inhibition mediated by G␤␥, a slow inhibition mediated by G␣ q/11 , and a slow stimulation mediated by PKC. This new information concerning R-type calcium channels and NK1 receptors may help in understanding nociception, synaptic plasticity, and other physiological processes.

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Section: Discussionsupporting

confidence: 93%

mentioning

confidence: 57%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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Neurokinin 1 Receptors Trigger Overlapping Stimulation and Inhibition of Ca_V2.3 (R-Type) Calcium Channels

Meza

Thapliyal²,

Bannister³

et al. 2006

Mol Pharmacol

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“…Muscarinic (especially M 1 ) receptor activation, elevating local calcium concentrations, may also trigger the nNOS-NO-NOsGC-cGMP pathway, as it was shown in several paradigms (Castoldi et al, 1993;Hu and elFakahany, 1993;Ando et al, 1994;Mathes and Thompson, 1996;Liu et al, 1997;Borda et al, 2005;Cuadra and ElFakahany, 2005). In addition, muscarinic enhancement of R-type calcium currents has also been observed in hippocampal pyramidal neurons (Tai et al, 2006), whereas M 1 receptors are widely expressed in pyramidal cells (Levey et al, 1995(Levey et al, , 1996. In vivo, M 1 receptors can be activated by the septohippocampal cholinergic pathway that plays a crucial role in synaptic plasticity (Freund and Buzsaki, 1996).…”

Section: Synapse-specific No Production In Gabaergic Synapsesmentioning

confidence: 99%

Hippocampal GABAergic Synapses Possess the Molecular Machinery for Retrograde Nitric Oxide Signaling

Szabadits¹,

Cserép²,

Ludányi³

et al. 2007

J. Neurosci.

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Nitric oxide (NO) plays an important role in synaptic plasticity as a retrograde messenger at glutamatergic synapses. Here we describe that, in hippocampal pyramidal cells, neuronal nitric oxide synthase (nNOS) is also associated with the postsynaptic active zones of GABAergic symmetrical synapses terminating on their somata, dendrites, and axon initial segments in both mice and rats. The NO receptor nitric oxide-sensitive guanylyl cyclase (NOsGC) is present in the brain in two functional subunit compositions: ␣ 1 ␤ 1 and ␣ 2 ␤ 1 . The ␤ 1 subunit is expressed in both pyramidal cells and interneurons in the hippocampus. Using immunohistochemistry and in situ hybridization methods, we describe that the ␣ 1 subunit is detectable only in interneurons, which are always positive for ␤ 1 subunit as well; however, pyramidal cells are labeled only for ␤ 1 and ␣ 2 subunits. With double-immunofluorescent staining, we also found that most cholecystokinin-and parvalbumin-positive and smaller proportion of the somatostatin-and nNOS-positive interneurons are ␣ 1 subunit positive. We also found that the ␣ 1 subunit is present in parvalbumin-and cholecystokinin-positive interneuron terminals that establish synapses on somata, dendrites, or axon initial segments. Our results demonstrate that NOsGC, composed of ␣ 1 ␤ 1 subunits, is selectively expressed in different types of interneurons and is present in their presynaptic GABAergic terminals, in which it may serve as a receptor for NO produced postsynaptically by nNOS in the very same synapse.

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Plasma membrane insertion of TRPC5 channels contributes to the cholinergic plateau potential in hippocampal CA1 pyramidal neurons

et al. 2011

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In cultured hippocampal neurons, transient receptor potential 5 (TRPC5) channels are translocated and inserted into plasma membranes of hippocampal neurons to generate nonselective cation (NSC) currents. We investigated whether TRPC5 channel translocation also contributes to the generation of NSC currents underlying the afterdepolarizations and plateau potentials (PPs) in hippocampal pyramidal cells that are induced by muscarinic receptor activation. Using a biotinylation assay to quantify the change in surface membrane proteins in acute hippocampal slices, we found that muscarinic stimulation significantly enhanced the levels of TRPC5 protein on the membrane surface but not those of TRPC1 or TRPC4 channels. We then investigated the pharmacological sensitivity of the cation current observed during muscarinic stimulation to determine if a component could be due to TRPC5 channels. The TRPC channel antagonists 2-APB and SKF96365 strongly depressed the generation of PPs, the underlying tail currents (I(tail)) and the associated dendritic Ca(2+) influx induced by muscarinic receptor activation in pyramidal neurons. High intracellular concentrations of ATP, which specifically inhibit TRPC5 channels, depressed I(tail). In addition, pretreatment with the calmodulin (CaM) inhibitor W-7, which depresses recombinant TRPC5 currents, inhibited both the cation current (I(tail)) and the surface insertion of TRPC5 channels. Finally, the phosphatidylinositide 3-kinase (PI(3)K) inhibitor wortmannin, which blocks translocation of TRPC5 channels in cell culture, also inhibited both the I(tail) and the surface insertion of TRPC5 channels. Therefore, we conclude that insertion of TRPC5 channels contributes to the generation of the prolonged afterdepolarizations following muscarinic stimulation. This altered plasma membrane expression of TRPC5 channels in pyramidal neurons may play an important role in the generation of prolonged neuronal depolarization and bursting during the epileptiform seizure discharges of epilepsy.

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Muscarinic Enhancement of R-Type Calcium Currents in Hippocampal CA1 Pyramidal Neurons

Cited by 59 publications

References 65 publications

Neurokinin 1 Receptors Trigger Overlapping Stimulation and Inhibition of Ca_V2.3 (R-Type) Calcium Channels

Neurokinin 1 Receptors Trigger Overlapping Stimulation and Inhibition of Ca_V2.3 (R-Type) Calcium Channels

Hippocampal GABAergic Synapses Possess the Molecular Machinery for Retrograde Nitric Oxide Signaling

Plasma membrane insertion of TRPC5 channels contributes to the cholinergic plateau potential in hippocampal CA1 pyramidal neurons

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Muscarinic Enhancement of R-Type Calcium Currents in Hippocampal CA1 Pyramidal Neurons

Cited by 59 publications

References 65 publications

Neurokinin 1 Receptors Trigger Overlapping Stimulation and Inhibition of CaV2.3 (R-Type) Calcium Channels

Neurokinin 1 Receptors Trigger Overlapping Stimulation and Inhibition of CaV2.3 (R-Type) Calcium Channels

Hippocampal GABAergic Synapses Possess the Molecular Machinery for Retrograde Nitric Oxide Signaling

Plasma membrane insertion of TRPC5 channels contributes to the cholinergic plateau potential in hippocampal CA1 pyramidal neurons

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Neurokinin 1 Receptors Trigger Overlapping Stimulation and Inhibition of Ca_V2.3 (R-Type) Calcium Channels

Neurokinin 1 Receptors Trigger Overlapping Stimulation and Inhibition of Ca_V2.3 (R-Type) Calcium Channels