EVIDENCE FOR ASPARTATE-IMMUNOREACTIVE NEURONS IN THE NEOSTRIATUM OF THE RAT: MODULATION BY THE MESENCEPHALIC DOPAMINE PATHWAY VIA D1-SUBTYPE OF RECEPTOR

doi:10.1016/0306-4522(96)00124-8

Neuroscience

Volume 74, Issue 1, September 1996, Pages 51-66

https://doi.org/10.1016/0306-4522(96)00124-8 Get rights and content

Abstract

Aspartate-like immunoreactivity was visualized in the neostriatum of rats using indirect immunofluorescence techniques and antibodies raised against aspartate conjugated to keyhole limpet hemocyanine. In normal rats only a few aspartate-positive cell bodies with limited processes were observed. A moderate increase was seen after treatment with (+)methamphetamine and haloperidol. A dramatic increase in the number and fluorescence intensity was observed in the unilaterally 6-hydroxy-dopamine lesioned rats after multiple injections of the D₁-dopamine receptor agonist SKF 38393. In these rats strongly fluorescent processes as well as extensive terminal varicose fibre networks were observed. This increase could partly be blocked by the D₁-dopamine receptor antagonist SCH 23390. Using a modified technique the aspartate-positive cell bodies and processes were observed even when the antiserum was diluted 1:80.000. Positive cell bodies and fibres were also seen on the ipsilateral side outside the neostriatum, for example in the islet of Calleja and in the piriform cortex. The aspartate-positive cells were negative for dopamine- and cyclic AMP-regulated phosphoprotein-32, a marker for neurons bearing dopamine D₁-receptor subtype. A proportion of the aspartate-positive neurons (20%) contained neuropeptide tyrosine-like immunoreactivity. On adjacent sections there was a marked up-regulation of preprodynorphin-like immunoreactivity. The up-regulation of dynorphin and aspartate was only observed when there was an almost complete denervation of the neostriatum as visualized with antiserum to tyrosine hydroxylase, a marker for dopamine fibres.

Section snippets

EXPERIMENTAL PROCEDURES

Male Sprague-Dawley rats (B & K, Stockholm, Sweden) with access to food and water ad libitum were used in the experiments. The rats were maintained in a temperature-controlled environment on a 12 h light/dark cycle, and all experiments were performed under the light period. The experimental protocols performed in the present study were approved by the Swedish Committee for Ethical Experiments on Laboratory Animals.

RESULTS

All 6-OHDA-lesioned rats showed a strong contralateral rotational behaviour (> 10 turns/min) following SKF 38393 (20 mg/kg, s.c.) or quinpirole (5 mg/kg, s.c.), whether given in a single or four repeated doses. The rotational behaviour induced by SKF 38393 was totally abolished following SCH 23390 (0.5 mg/kg, s.c.). No rotational behaviour was observed following saline.

DISCUSSION

The present results demonstrate that there is a small number of neurons in the neostriatum of the rat which binds antibodies raised against aspartate conjugated with keyhole-limpet hemocyanine. The levels of this aspartate-LI are influenced by DA stimulation, probably via D₁ subtype of receptors. Indeed, the strongest staining pattern was seen in the 6-OHDA-deafferented neostriatum following multiple doses of the D₁ receptor agonist SKF 38393. [64]The effect was unilateral, suggesting that it

CONCLUSION

An interesting question is whether or not the increase in aspartate levels seen in the rat in the present study can occur also in the human brain. For example, can L-DOPA treatment increase aspartate-levels in the DA denervated Parkinsonian brain, and if so, what are the behavioural and long-term biochemical consequences of an increased aspartate release? Can this increased aspartate release produce overstimulation of glutamate receptors, leading to excitotoxic and to further neurodegenerative

Acknowledgements

This study was supported by grants from the Swedish Medical Research Council (2887, 8669), Marianne och Marcus Wallenbergs Stiftelse, Karolinska Institutes fonder andÅke Wibergs Stiftelse. Z-B. Y. is recipient of a scholarship from Karolinska Institute; E.P. is a recipient of a Parke-Davis Neuroscience Research Centre (Cambridge, U.K.) scholarship. R. R-P. is a recipient of a “Basque Government Postdoctoral Research Fellowship”.

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Citation Excerpt :
A potential candidate is GABA as the vast majority of neostriatal neurons and intrinsic intrastriatal synapses are GABAergic, the latter arising from GABAergic interneurons and from axon collaterals of spiny projection neurons (Tepper et al., 2004); GABA has also been shown to be increased by CCK-8 (Barnes et al., 1991; Rakovska, 1995b). It could be that the effect is mediated through an increase in aspartate (Asp) as intrinsic Asp neurons (seemingly not colocalized with glutamate) (Pettersson et al., 1996) have also been observed in neostriatum and aspartate is significantly increased by CCK-8 as monitored by in vivo microdialysis (You et al., 1994, 1996). Several lines of evidence indicate a complex interplay between dopamine and CCK-8 in striatum: a coexistence of CCK-8 and dopamine in mesencephalic neurons innervating striatum (Hokfelt et al., 1980), an apparently complex modulatory role of CCK-8 for DA release, as CCK-8 has been reported to either increase (Vickeroy and Bianchi, 1987; Marshall et al., 1990) or decrease DA release (Altar et al., 1988; Lane et al., 1986; Cosi et al., 1989; Rakovska, 1995a), and a reciprocal complex modulatory role of DA for CCK-8 as it has been elucidated that at low doses DA enhances CCK release (due to interaction with the more sensitive D2-receptors) whereas high DA doses reduce neostriatal CCK release (due to DA interaction with D1-receptors (Meyer and Krauss, 1983, Meyer et al., 1984; Conzelmann et al., 1984); mRNA CCK levels in the rat striatum have been shown to be elevated following treatment with DA agonists (Ding and Mocchetti, 1992).
Cholecystokinin, a neuroactive peptide functioning as a neurotransmitter and neuromodulator in the central nervous system, mediates a number of processes and is implicated in neurological and psychiatric disorders such as Parkinson's disease, anxiety and schizophrenia. Striatum is one of the brain structures with the highest concentrations of CCK in the brain, rich in CCK receptors as well. The physiological effect of CCK on cholinergic interneurons, which are the major interneurons in striatum and the modulatory interactions which exist between dopamine, acetylcholine and cholecystokinin in this brain structure are still unclear. We studied the effect of cholecystokinin octapeptide (CCK-8) on the release of acetylcholine (ACh) from striatal slices of the rat brain. CCK-8 (0.01–0.1 μM) showed no statistically significant effect on the basal but enhanced dose-dependently the electrically (2 Hz)-evoked release of [³H]ACh. When slices were preperfused with 100 μM sulpiride, a selective dopamine D₂ receptor antagonist, the CCK-8 (0.01 μM) effect on electrically stimulated ACh release was increased nearly 2-fold. A similar increase was observed after depletion of endogenous dopamine (DA) from nigro-striatal dopaminergic neurons with 6-hydroxydopamine (6-OHDA) (2× 250 μg/animal, i.c.v.). Furthermore in the presence of dopamine (100 μM) or apomorphine (10 μM), the prototypical DA receptor agonist, CCK-8 (0.01 μM) failed to enhance the stimulation-evoked release of [³H]ACh. The D₂ receptor agonist quinpirol (1 μM) abolished the CCK-8 effect on electrically stimulated ACh release as well. The increase in electrically induced [³H]ACh release produced by 0.01 μM CCK-8 was antagonized by d,l loxiglumide (CR 1505), 10 μM, a non-peptide CCK-A receptor antagonist and by Suc-Tyr-(OSO3)-Met-Gly-Trp-Met-Asp-β-phenethyl-amide (GE-410), 1 μM, a peptide CCK-A receptor antagonist. The antagonistic effect of GE-410 on the CCK-8-potentiated, electrically induced release of [³H]ACh was studied in striatum for the first time. CAM 1028 (10 μM), a CCK-B receptor antagonist, also prevented the potentiating effect of CCK-8 (0.01 μM) on electrically stimulated release of [³H]ACh.
The presented results indicate that (i) CCK-8 is capable of increasing ACh elicited by field electrical stimulation in striatum; (ii) CCK-8 is more effective in its ACh-stimulating effect when dopaminergic activity in striatum is blocked i.e. CCK-8-facilitated release of electrically induced ACh from cholinergic interneurons in the striatum is under the inhibitory control of the tonic activity of dopamine from the nigrostriatal pathway; (iii) the enhancing effect of CCK-8 on electrically evoked ACh release is mediated through both CCK-A and CCK-B cholecystokinin receptors located most likely on the cell bodies of cholinergic interneurons in striatum.
Chronic exposure to manganese decreases striatal dopamine turnover in human alpha-synuclein transgenic mice
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Our additional finding showing that changes in the striatal HVA/DA ratios were paralleled by corresponding changes in striatal aspartate levels, adds strength to the above interpretation. Thus, striatal aspartate immunoreactive neurons have been reported to be subjected to modulation by the mesencephalic dopamine pathway, with both upregulation after D-1 receptor stimulation (Pettersson et al., 1996), and selective D1 agonist induced increase of aspartate but not glutamate release, as determined by microdialysis (Herrera-Marschitz et al., 1998). This is in accord with our observations of elevated striatal HVA/DA ratios (as an Index of increased DA release) being accompanied, in the human α-syn group of mice, by elevated striatal aspartate levels, that is, increased release; exposure to Mn decreased striatal DA release (cf. lower HVA/DA ratios) and simultaneously cancelled the aspartate changes.
Interaction of genetic and environmental factors is likely involved in Parkinson's disease (PD). Mutations and multiplications of alpha-synuclein (α-syn) cause familial PD, and chronic manganese (Mn) exposure can produce an encephalopathy with signs of parkinsonism. We exposed male transgenic C57BL/6J mice expressing human α-syn or the A53T/A30P doubly mutated human α-syn under the tyrosine hydroxylase promoter and non-transgenic littermates to MnCl₂-enriched (1%) or control food, starting at the age of 4 months. Locomotor activity was increased by Mn without significant effect of the transgenes. Mice were sacrificed at the age of 7 or 20 months. Striatal Mn was significantly increased about three-fold in those exposed to MnCl₂. The number of tyrosine hydroxylase positive substantia nigra compacta neurons was significantly reduced in 20 months old mice (−10%), but Mn or transgenes were ineffective (three-way ANOVA with the factors gene, Mn and age). In 7 months old mice, striatal homovanillic acid (HVA)/dopamine (DA) ratios and aspartate levels were significantly increased in control mice with human α-syn as compared to non-transgenic controls (+17 and +11%, respectively); after Mn exposure both parameters were significantly reduced (−16 and −13%, respectively) in human α-syn mice, but unchanged in non-transgenic animals and mice with mutated α-syn (two-way ANOVA with factors gene and Mn). None of the parameters were changed in the 20 months old mice. Single HVA/DA ratios and single aspartate levels significantly correlated across all treatment groups suggesting a causal relationship between the rate of striatal DA metabolism and aspartate release. In conclusion, under our experimental conditions, Mn and human α-syn, wild-type and doubly mutated, did not interact to induce PD-like neurodegenerative changes. However, Mn significantly and selectively interacted with human wild-type α-syn on indices of striatal DA neurotransmission, the neurotransmitter most relevant to PD.
Aspartate immunoreactivity in the telencephalon of the adult sea lamprey: Comparison with GABA immunoreactivity
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The excitatory amino acid l-aspartate (Asp) plays a number of roles in neuronal function. We studied the distribution of Asp-immunoreactive (ir) cells in the telencephalon of young and upstream migrating adult sea lamprey, Petromyzon marinus, and compared it with the distribution of γ-aminobutyric acid (GABA) immunoreactivity, by using double immunofluorescence methods. Our results reveal for the first time the existence of Asp-ir neuronal populations in the lamprey forebrain. In the olfactory bulbs, Asp-ir neurons were observed in the mitral cell layer and in the inner cellular layer. Many granule-like cells were both Asp-ir and GABA-ir. In the pallium, Asp-ir cells were abundant in the lateral pallium and most of them were also GABA-ir. In the septum/terminal lamina nucleus, some cerebrospinal fluid-contacting type (CSF-c) cells were either Asp-ir or GABA-ir, and a few were double-labeled. Some non-CSF-c septal cells were both Asp-ir and GABA-ir. In the striatum, Asp-ir and/or GABA-ir cells were either subependymal or located in the characteristic arched cell row. In the lateral preoptic region, a few small Asp-ir/GABA-ir neurons were observed. In the caudal preoptic recess nucleus, numerous CSF-c cells were Asp-ir and/or GABA-ir. This study also reveals that colocalization of GABA and Asp immunoreactivities in telencephalic neurons is partial. Further investigation is required to establish whether Asp is a neurotransmitter and/or an intermediate in GABA synthesis in lamprey telencephalon.
Immunohistological characterization of striatal and amygdalar structures in the telencephalon of the fire-bellied toad Bombina orientalis
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In Bombina, the dorsal pallidum differs from the rostrally situated striatum proper by the presence of neuron clusters containing high concentrations of NADPH-diaphorase at its very caudal aspect. Further similarities with the mammalian pattern are the presence of neurons ir for aspartate (Pettersson et al., 1996), calretinin (Cooper and Stanford, 2002; Lévesque et al., 2003) and GABA, although the latter seem to be much less abundant. As in mammals, the striato-pallidum of frogs reveals a high concentration of catecholaminergic fibers (i.e. dopamine) and a homogenous distribution of serotonergic fibers (Pasik et al., 1984; Soghomonian et al., 1987).
The subpallium of the fire-bellied toad Bombina orientalis was studied by means of enzyme-histological detection of NADPH-diaphorase and immunohistological demonstration of aspartate, GABA, calretinin, choline-acetyl transferase, Leu-and Met-enkephalin, neuropeptide Y, 5-hydroxy-tryptamine (serotonin), somatostatin, substance P and tyrosine-hydroxylase. As in other vertebrates, the striato-pallidum is characterized by GABA-, substance P- and enkephalin-immunoreactivity. Neurons and fibers differing in immunoreactivity are arranged in layers. Choline-acetyl transferase-immunoreactive neurons were found in a position corresponding to the mammalian cholinergic cell-group (Ch4-group), which therefore may be homologous to the nucleus basalis of Meynert. Within the amygdaloid complex, the cortical and lateral (vomeronasal) nuclei are similar in calretinin-, GABA-, NADPH-diaphorase-, enkephalin, substance P- and neuropeptide Y-(immuno)histology. The medial and central amygdaloid nuclei reveal a dense peptidergic innervation, and the medial amygdala additionally exhibits serotonergic fibers and cell bodies staining for neuropeptides and tyrosine-hydroxylase. Differences between Bombina and other anuran species exist, such as the absence of cholinergic neurons in the striatum. Our findings corroborate the view based on recent studies on the hodology and cytoarchitecture of the anuran telencephalon that the anuran ventral telencephalon contains most of the structures found in the mammalian brain. This concerns a septal region, a dorsal and ventral striato-pallidum including a nucleus accumbens and an amygdaloid complex consisting of a central, cortical and vomeronasal amygdala. The only major difference appears to concern the lack of a basolateral amygdala.
A dual probe characterization of dialysate amino acid levels in the medial prefrontal cortex and ventral tegmental area of the awake freely moving rat
2002, Journal of Neuroscience Methods
Dual probe microdialysis was employed to characterize the origins of dialysate glutamate, aspartate and gamma-aminobutyric acid (GABA) in the medial prefrontal cortex (mPfc) and to investigate functional interactions between the mPfc and ventral tegmental area (VTA) in awake, freely moving rats. Perfusion with elevated potassium (K⁺; KCl, 100 mM, 20 min), low Ca²⁺ (0.1 mM, 60 min) or tetrodotoxin (TTX, 10 μM, 100 min) was performed in the mPfc and dialysate levels of glutamate, aspartate and GABA were measured locally and in the VTA. Elevated K⁺ in the mPfc rapidly increased dialysate glutamate and aspartate locally (+90±10 and +41±9% from basal, respectively) and in the VTA (+71±14 and +42±14%, respectively). MPfc GABA was also rapidly increased (+241±62%) while VTA GABA was not affected. Perfusion with low Ca²⁺ in the mPfc decreased local glutamate, aspartate and GABA (−26±8; −35±7 and −45±8%, respectively) and decreased only GABA (−40±5%) in the VTA. Intra-mPfc TTX increased glutamate and aspartate locally (+82±23 and +54±27%, respectively) and in the VTA (+84±18 and +38±17%, respectively). In contrast, intra-mPfc TTX decreased local GABA (−33+6%) while VTA GABA levels were not affected. Taken together, these data confirm the influence of the mPfc upon the ipsilateral VTA and provide evidence for two neuronal pools which contribute to basal extracellular mPfc and VTA glutamate, aspartate and GABA levels, the first pool derived from Na⁺- and Ca²⁺-dependent release and the second derived from voltage-dependent reuptake.
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The present multidisciplinary study examined nigrostriatal dopamine and striatal amino acid transmission in the R6/1 line of transgenic Huntington's disease (HD) mice expressing exon 1 of the HD gene with 115 CAG repeats. Although the number of tyrosine hydroxylase-positive neurons was not reduced and nigrostriatal connectivity remained intact in 16-week-old R6/1 mice, the size of tyrosine hydroxylase-positive neurons in the substantia nigra was reduced by 15%, and approximately 30% of these cells exhibited aggregated huntingtin. In addition, using in vivo microdialysis, we found that basal extracellular striatal dopamine levels were reduced by 70% in R6/1 mice compared to their wild-type littermates. Intrastriatal perfusion with malonate in R6/1 mice resulted in a short-lasting, attenuated increase in local dopamine release compared to wild-type mice. Furthermore, the size of the malonate-induced striatal lesion was 80% smaller in these animals. Taken together, these findings suggest that a functional deficit in nigrostriatal dopamine transmission may contribute to the behavioral phenotype and the resistance to malonate-induced neurotoxicity characteristic of R6/1 HD mice.

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EVIDENCE FOR ASPARTATE-IMMUNOREACTIVE NEURONS IN THE NEOSTRIATUM OF THE RAT: MODULATION BY THE MESENCEPHALIC DOPAMINE PATHWAY VIA D1-SUBTYPE OF RECEPTOR

Abstract

Section snippets

EXPERIMENTAL PROCEDURES

RESULTS

DISCUSSION

CONCLUSION

Acknowledgements

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Effect of cholecystokinin octapeptide on endogenous amino acid release from the rat ventromedial nucleus of the hypothalamus and striatum

J. Neurochem.

Glutamate decarboxylase-immunoreactive structures in the rat neostriatum: a correlated light and electron microscopic study including a combination of Golgi impregnation with immunocytochemistry

J. comp. Neurol.

Excitatory amino acid receptors in the vertebrate central nervous system

Pharmac. Rev.

The pharmacology of amino acids related to γ-aminobutyric acid

Pharmac. Rev.

Glutamate: a neurotransmitter in mammalian brain

J. Neurochem.

Dopamine differentially regulates dynorphin, substance P, and enkephalin expression in striatal neurons: in situ hybridization histochemical analysis

J. Neurosci.

In vivo release of endogeneous amino acids from rat striatum: further evidence for a role of glutamate and aspartate in corticostriatal neurotransmission

J. Neurochem.

Production and characterization of four anti-neuropeptide Y monoclonal antibodies

Hybridoma

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Eur. J. Neurosci.

EVIDENCE FOR ASPARTATE-IMMUNOREACTIVE NEURONS IN THE NEOSTRIATUM OF THE RAT: MODULATION BY THE MESENCEPHALIC DOPAMINE PATHWAY VIA D₁-SUBTYPE OF RECEPTOR