Evidence for the preferential localization of Glutamate Receptor-1 subunits of AMPA receptors to the dendritic spines of medium spiny neurons in rat striatum

Chen, Q; Veenman, Leo; Knopp, Kelly L.; Yan, Zhen; Medina, Loreta; Song, Wen Jie; Surmeíer, D. James; Reiner, Anton

doi:10.1016/s0306-4522(97)00452-1

Cited by 79 publications

(100 citation statements)

References 41 publications

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“…Moreover, we found that striato-GPe and striatonigral neuron perikarya appear to contain less amounts of GluR2 than do striato-GPi neuron perikarya. The present study further shows that projection neuron perikarya are less rich in GluR1 than GluR2 protein, as also implied by prior ISHH, RT-PCR and immunolabeling studies, and that only 50-70% of striatal projection neuron perikarya contain GluR1 (Bernard et al, 1996(Bernard et al, ,1997Chen et al, 1996Chen et al, ,1998Stefani et al, 1998;Vorobjev et al, 2000). In contrast to the situation for GluR2, we found that striato-GPe perikarya are richer than striato-GPi perikarya in GluR1.…”

Section: Implications For Ampa Receptor Subunit Composition and Functsupporting

confidence: 84%

“…11E, F; Table 7). As described previously (Bernard et al, 1997;Chen et al, 1998), the heads of many GluR-immunolabeled as well as many nonimmunolabeled spines received asymmetric synaptic contact from unlabeled axon terminals containing round vesicles clustered near the synaptic specialization. This was true of GluR-immunolabeled and nonimmunolabeled dendrites as well.…”

Section: Ultrastructural Localization Of Glur1 Glur2 and Glur2/3 In mentioning

confidence: 69%

“…While prior immunohistochemical, in situ hybridization histochemical (ISHH), and single cell reverse transcription-polymerase chain reaction (RT-PCR) studies have examined the localization of AMPA subunits in striatal neurons, the relative frequency and abundance of GluR1 and GluR2 in the various striatal projection neuron and interneuron types has not been fully clarified (Tallaksen-Greene and Albin, 1994;Chen et al, 1996Chen et al, ,1998Bernard et al, 1997;Kwok et al, 1997). We thus used LM and EM immunolabeling to: 1) detail the percent of each major striatal projection neuron type and interneuron that contains GluR1 and GluR2; and 2) characterize relative GluR1 and GluR2 abundance in each.…”

Section: Introductionmentioning

confidence: 99%

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Differential localization of the GluR1 and GluR2 subunits of the AMPA-type glutamate receptor among striatal neuron types in rats

Deng

Xie

Wang

et al. 2007

Journal of Chemical Neuroanatomy

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Differences among the various striatal projection neuron and interneuron types in cortical input, function, and vulnerability to degenerative insults may be related to differences among them in AMPA-type glutamate receptor abundance and subunit configuration. We therefore used immunolabeling to assess the frequency and abundance of GluR1 and GluR2, the most common AMPA subunits in striatum, in the main striatal neuron types. All neurons projecting to the external pallidum (GPe), internal pallidum (GPi) or substantia nigra, as identified by retrograde labeling, possessed perikaryal GluR2, while GluR1 was more common in striato-GPe than striato-GPi perikarya. The frequency and intensity of immunostaining indicated the rank order of their perikaryal GluR1:GluR2 ratio to be striato-GPe > striatonigral > striato-GPi. Ultrastructural studies suggested a differential localization of GluR1 and GluR2 to striatal projection neuron dendritic spines as well, with GluR1 seemingly more common in striato-GPe spines and GluR2 more common in striato-GPi and/or striatonigral spines. Comparisons among projection neurons and interneurons revealed GluR1 to be most common and abundant in parvalbuminergic interneurons, and GluR2 most common and abundant in projection neurons, with the rank order for the GluR1:GluR2 ratio being parvalbuminergic interneurons > calretinergic interneurons > cholinergic interneurons > projection neurons > somatostatinergic interneurons. Striosomal projection neurons had a higher GluR1:GluR2 ratio than did matrix projection neurons. The abundance of both GluR1 and GluR2 in striatal parvalbuminergic interneurons and projection neurons is consistent with their prominent cortical input and susceptibility to excitotoxic insult, while differences in GluR1: GluR2 ratio among projection neurons are likely to yield differences in Ca2+ permeability, desensitization, and single channel current, which may contribute to differences among them in plasticity, synaptic integration, and excitotoxic vulnerability. The apparent association of the GluR1 subunit with synaptic plasticity, in particular, suggests striato-GPe neuron spines as a particular site of corticostriatal synaptic plasticity, presumably associated with motor learning.

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Section: Implications For Ampa Receptor Subunit Composition and Functsupporting

confidence: 84%

Section: Ultrastructural Localization Of Glur1 Glur2 and Glur2/3 In mentioning

confidence: 69%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Differential localization of the GluR1 and GluR2 subunits of the AMPA-type glutamate receptor among striatal neuron types in rats

Deng

Xie

Wang

et al. 2007

Journal of Chemical Neuroanatomy

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“…Precedent for this possibility comes from studies showing that conformational changes associated with altered subcellular localization of the glucose transporter 4 can dramatically and differentially influence Western blot and immunocytochemical analyses of this protein (Joost et al 1988;Smith et al 1991Smith et al , 1993. However, the anti-GluR1 antibody detects GluR1 in a number of cellular compartments (e.g., Martin et al 1993;Chen et al 1998;Paquet et al 1997). Most importantly, the type of change in GluR1 disposition most likely to explain enhanced electrophysiological responsiveness, that is, an increase in cell surface expression, should be detectable with immunohistochemical methods.…”

Section: Electrophysiological Supersensitivity Is Unlikely To Reflectmentioning

confidence: 99%

Repeated Administration of Amphetamine or Cocaine Does Not Alter AMPA Receptor Subunit Expression in the Rat Midbrain,

Monteggia

Wolf

2002

Neuropsychopharmacology

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We previously reported that ventral tegmental area (VTA) dopamine neurons are supersensitive to AMPA when recorded three days after discontinuing repeated amphetamine or cocaine administration. By increasing dopamine cell activity, this may contribute to the induction of behavioral sensitization. The goal of this study was to determine if increased sensitivity to AMPA reflects increased AMPA receptor expression in the midbrain.Immunolabeling for GluR1, GluR2, GluR2/3, and Behavioral sensitization refers to the persistent augmentation of behavioral responses to psychomotor stimulants that occurs as a result of their repeated administration. It provides an animal model for neuroadaptations that may contribute to drug addiction (Robinson and Berridge 1993). Sensitization is initiated by drug actions within the ventral tegmental area (VTA), the origin of mesocorticolimbic dopamine (DA) projections (Kalivas and Stewart 1991). It is now well accepted that the induction of sensitization requires glutamate transmission within the VTA (Wolf 1998;Vanderschuren and Kalivas 2000). Glutamate's involvement in sensitization implies mechanistic similarities between sensitization and other forms of neuronal plasticity. This in turn has important implications for the development of therapeutic strategies for drug dependency (Li et al. 2000).Sensitization can be induced by treatments that have in common the ability to produce brief but intense activation of VTA DA cells (Schenk and Snow 1994;Ben-Shahar and Ettenberg 1994). Moreover, many lines of evidence suggest that DA cell activity is increased shortly after discontinuation of repeated stimulant administration (White 26 , NO . 1 1996; Wolf 1998). These findings suggest that the physiological mechanisms responsible for induction involve a transient increase in excitatory drive to VTA DA cells. Electrophysiological results suggest that this might be due, in part, to a transient increase in the responsiveness of VTA DA neurons to ␣ -amino-3-hydroxy-5-methylisoxazole-4-priopionate (AMPA) receptor stimulation. Thus, VTA DA neurons recorded three but not 14 days after discontinuation of repeated cocaine or amphetamine administration show increased responsiveness to the excitatory effects of iontophoretically applied glutamate and AMPA (White et al. 1995;Zhang et al. 1997).Increased AMPA receptor expression is one possible explanation for this increase in responsiveness to AMPA. Indeed, GluR1 levels in the VTA, quantified using Western blots, are increased shortly after discontinuation of repeated cocaine, morphine, ethanol, or stress paradigms (Ortiz et al. 1995;Fitzgerald et al. 1996;Churchill et al. 1999). While increased GluR1 levels might explain enhanced responses to AMPA after repeated cocaine or amphetamine administration, an important concern is that increased GluR1 has been demonstrated after 16-24 hrs of withdrawal from psychostimulants (Fitzgerald et al. 1996;Churchill et al. 1999) whereas the increase in electrophysiological responsiveness to AMPA has been demonstr...

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“…Studies indicate that the majority of glutamate receptors are found on medium spiny neurons. These neurons contain the NMDA NR1 and NR2A/2b subunits in the striatum as well as AMPA GluR1, GluR2/3, and GluR4 subunits Chen et al, 1998;Hu et al, 2004;Wang et al, 2004). Cholinergic interneurons and half of the GABAergic parvalbumin-containing interneurons express NMDA NR2A/2B R while SST interneurons do not (Landwehrmeyer et al, 1995;.…”

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confidence: 99%

Methamphetamine-induced cell death: Selective vulnerability in neuronal subpopulations of the striatum in mice

2006

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Methamphetamine (METH) is an illicit and potent psychostimulant, which acts as an indirect dopamine agonist. In the striatum, METH has been shown to cause long lasting neurotoxic damage to dopaminergic nerve terminals and recently, the degeneration and death of striatal cells. The present study was undertaken to identify the type of striatal neurons that undergo apoptosis after METH. Male mice received a single high dose of METH (30 mg/kg, i.p.) and were killed 24 h later. To demonstrate that METH induces apoptosis in neurons, we combined terminal deoxynucleotidyl transferase-mediated dUTP nick end labeling (TUNEL) staining with immunohistofluorescence for the neuronal marker neuron-specific nuclear protein (NeuN). Staining for TUNEL and NeuN was colocalized throughout the striatum. METH induces apoptosis in approximately 25% of striatal neurons. Cell counts of TUNEL-positive neurons in the dorsomedial, ventromedial, dorsolateral and ventrolateral quadrants of the striatum did not reveal anatomical preference. The type of striatal neuron undergoing cell death was determined by combining TUNEL with immunohistofluorescence for selective markers of striatal neurons: dopamine-and cAMP-regulated phosphoprotein, of apparent M r 32,000, parvalbumin, choline acetyltransferase and somatostatin (SST). METH induces apoptosis in approximately 21% of dopamine-and cAMP-regulated phosphoprotein, of apparent M r 32,000-positive neurons (projection neurons), 45% of GABA-parvalbumin-positive neurons in the dorsal striatum, and 29% of cholinergic neurons in the dorsal-medial striatum. In contrast, the SST-positive interneurons were refractory to METH-induced apoptosis. Finally, the amount of cell loss determined with Nissl staining correlated with the amount of TUNEL staining in the striatum of METH-treated animals. In conclusion, some of the striatal projection neurons and the GABAparvalbumin and cholinergic interneurons were removed by apoptosis in the aftermath of METH. This imbalance in the populations of striatal neurons may lead to functional abnormalities in the output and processing of neural information in this part of the brain. Keywords methamphetamine; apoptosis; striatum; projection neurons; interneurons Methamphetamine (METH) is a potent and addictive psychostimulant. The neurotoxic effects of this substituted amphetamine are associated with its ability to induce an overflow of dopamine in the synapse by displacing vesicular dopamine stores (Raiteri et al., 1979; Liang and Rutledge, 1982a,b;Schmidt et al., 1985;Sulzer et al., 1995). Displaced dopamine molecules and its metabolites can be readily oxidized to reactive quinones and semiquinones (Cadet and Brannock, 1998) and nitrogen radicals (Lipton and Rosenberg, 1994;Imam et al., 1999) that affect a wide range of modifications of proteins, sugars, and lipids. Augmented levels of dopamine in the synapse induced by METH have been shown in humans (Wilson et al., 1996;McCann et al., 1998), non-human primates (Seiden et al., 1976;Villemagne et al., 1998;Harvey e...

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Evidence for the preferential localization of Glutamate Receptor-1 subunits of AMPA receptors to the dendritic spines of medium spiny neurons in rat striatum

Cited by 79 publications

References 41 publications

Differential localization of the GluR1 and GluR2 subunits of the AMPA-type glutamate receptor among striatal neuron types in rats

Differential localization of the GluR1 and GluR2 subunits of the AMPA-type glutamate receptor among striatal neuron types in rats

Repeated Administration of Amphetamine or Cocaine Does Not Alter AMPA Receptor Subunit Expression in the Rat Midbrain,

Methamphetamine-induced cell death: Selective vulnerability in neuronal subpopulations of the striatum in mice

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