Ionotropic and metabotropic GABA and glutamate receptors in primate basal ganglia

Smith, Yoland; Charara, Ali; Paquet, Maryse; Kieval, Jeremy Z.; Paré, Jean‐François; Hanson, Jesse E.; Hubert, George W.; Kuwajima, Masaaki; Levey, Aĺlan I.

doi:10.1016/s0891-0618(01)00098-9

Cited by 70 publications

(49 citation statements)

References 205 publications

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“…In conclusion, data obtained over the past few years have clearly shown that the three groups of mGluRs are widely distributed throughout the basal ganglia in which they play various functions at presynaptic and postsynaptic levels to regulate GABAergic and glutamatergic transmission Rouse et al, 2000;Smith and Kieval, 2000;Smith et al, , 2001Valenti et al, 2002). Our findings suggest that these receptors may be important in regulating neurotransmission in the basal ganglia and pave the way for the development of novel therapeutic strategies in Parkinson's disease.…”

Section: Discussionsupporting

confidence: 53%

Distinct Functional Roles of the Metabotropic Glutamate Receptors 1 and 5 in the Rat Globus Pallidus

Poisik¹,

Mannaioni²,

Traynelis³

et al. 2003

J. Neurosci.

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Group I metabotropic glutamate receptors (mGluRs) 1 and 5 frequently colocalize in the same neurons throughout the CNS. Because both receptors can couple to the same effector systems, the purpose of their cellular coexpression remains unclear. Here, we report that group I mGluR1 and mGluR5 have distinct functional roles in type II neurons of the rat globus pallidus (GP). Type II GP neurons form a large population of GABAergic projection neurons that are characterized by the presence of inwardly rectifying current I h , low-threshold voltage-activated calcium current I t , and activity at rest. Although immunocytochemical analysis reveals a high degree of neuronal colocalization of the two group I mGluRs in the GP, activation of mGluR1 only directly depolarizes type II GP neurons. Interestingly, blockade of mGluR5 by a highly selective antagonist, methylphenylethynylpyridine, leads to the potentiation of the mGluR1-mediated depolarization in this neuronal subpopulation. Metabotropic GluR1 desensitizes during repeated activation with the agonist in type II GP neurons, and blocking mGluR5 prevents the desensitization of the mGluR1-mediated depolarization. Elimination of the activity of protein kinase C (PKC) by an application of 1 M bisendolylmaleimide or 1 M chelerythrine, both protein kinase C inhibitors, potentiates the mGluR1-mediated response and prevents the desensitization of mGluR1 in type II GP neurons, suggesting that the effect of mGluR5 on mGluR1 signaling may involve PKC. Together, these data illustrate a novel mechanism by which mGluR1 and mGluR5, members of the same family of G-protein-coupled receptors, can interact to modulate neuronal activity in the rat GP.

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Section: Discussionsupporting

confidence: 53%

Distinct Functional Roles of the Metabotropic Glutamate Receptors 1 and 5 in the Rat Globus Pallidus

Poisik¹,

Mannaioni²,

Traynelis³

et al. 2003

J. Neurosci.

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“…Our data demonstrate that Ͼ70% of both presynaptic and postsynaptic KAR subunit immunoreactivity is expressed intracellularly and that almost two-thirds of the plasma membrane-bound KARS are extrasynaptic. This pattern of distribution resembles that of G-protein-coupled metabotropic receptors which, for the most part, are expressed intracellularly or at nonsynapic sites along plasma membrane (Pasquini et al, 1992;Wang et al, 1997;Bernard et al, 1999;Hanson and Smith, 1999;Smith et al, 2000Smith et al, , 2001. Interestingly, both the presynaptic and postsynaptic effects of kainate receptors are consistent with those of metabotropic glutamate receptor functions (for review, see Conn and Pin, 1997;Anwyl, 1999;Cartmell and Schoepp, 2000).…”

Section: Subcellular Localization Of Kainate Receptor Subunitsmentioning

confidence: 68%

Subcellular and Subsynaptic Localization of Presynaptic and Postsynaptic Kainate Receptor Subunits in the Monkey Striatum

et al. 2001

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The localization and functions of kainate receptors (KARs) in the CNS are still poorly known. In the striatum, GluR6/7 and KA2 immunoreactivity is expressed presynaptically in a subpopulation of glutamatergic terminals and postsynaptically in dendrites and spines. The goal of this study was to further characterize the subcellular and subsynaptic localization of kainate receptor subunits in the monkey striatum. Immunoperoxidase data reveal that the relative abundance of GluR6/7-and KA2-immunoreactive terminals is homogeneous throughout the striatum irrespective of the differential degree of striatal degeneration in Huntington's disease. Pre-embedding and post-embedding immunogold data indicate that Ͼ70% of the presynaptic or postsynaptic GluR6/7 and KA2 labeling is expressed intracellularly. In material stained with the post-embedding immunogold method, approximately one-third of plasma membrane-bound gold particles labeling in axon terminals and spines is associated with asymmetric synapses, thereby representing synaptic kainate receptor subunits. On the other hand, Ͼ60% of the plasmamembrane bound labeling is extrasynaptic. Both GluR6/7 and KA2 labeling in glutamatergic terminals often occurs in clusters of gold particles along the membrane of large vesicular organelles located at various distances from the presynaptic grid. Anterograde labeling from the primary motor cortex or the centromedian thalamic nucleus indicate that both corticostriatal and thalamostriatal terminals express presynaptic GluR6/7 and KA2 immunoreactivity in the postcommissural putamen. In conclusion, these data demonstrate that kainate receptors in the striatum display a pattern of subcellular distribution different from other ionotropic glutamate receptor subtypes, but consistent with their metabotropic-like functions recently shown in the hippocampus.

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“…This action might be exterted at different levels. Both mGlu1 and mGlu5 receptors are expressed by nigral dopaminergic neurons of the pars compacta of substantia nigra, where they are commonly found at the edges of asymmetric postsynaptic densities Smith et al, 2001). In addition, mGlu5 receptors are found in striatal dopaminergic terminals, where they negatively modulate DAT activity (Page et al, 2001).…”

Section: Discussionmentioning

confidence: 99%

Endogenous Activation of mGlu5 Metabotropic Glutamate Receptors Contributes to the Development of Nigro-Striatal Damage Induced by 1-Methyl-4-Phenyl-1,2,3,6-Tetrahydropyridine in Mice

Battaglia¹,

Busceti²,

Molinaro³

et al. 2004

J. Neurosci.

116

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Ionotropic and metabotropic GABA and glutamate receptors in primate basal ganglia

Cited by 70 publications

References 205 publications

Distinct Functional Roles of the Metabotropic Glutamate Receptors 1 and 5 in the Rat Globus Pallidus

Distinct Functional Roles of the Metabotropic Glutamate Receptors 1 and 5 in the Rat Globus Pallidus

Subcellular and Subsynaptic Localization of Presynaptic and Postsynaptic Kainate Receptor Subunits in the Monkey Striatum

Endogenous Activation of mGlu5 Metabotropic Glutamate Receptors Contributes to the Development of Nigro-Striatal Damage Induced by 1-Methyl-4-Phenyl-1,2,3,6-Tetrahydropyridine in Mice

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