Presynaptic Dopamine D2 Receptors Modulate [ 3 H]GABA Release at StriatoPallidal Terminals via Activation of PLC → IP3 → Calcineurin and Inhibition of AC → cAMP → PKA Signaling Cascades

Jijón-Lorenzo, Rafael; Caballero-Florán, Isaac H.; Recillas‐Morales, Sergio; Cortés, Hernán; Ávalos-Fuentes, José Arturo; Paz‐Bermúdez, Francisco; Erlij, David; Florán, Benjamí­n

doi:10.1016/j.neuroscience.2017.12.041

Cited by 19 publications

(18 citation statements)

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“…In contrast, the blockade of D 4 R with its selective antagonist (Patel et al., 1997) L 745,870 (100 nM) prevented partially the Quinpirole effect diminishing it in around 28% (GABA release; median Quinpirole 39%, ranks 24–50 versus median Quinpirole + L 745,870 69%, ranks 60–75, mean rank difference −10, p = 0.05, n = 10). These data indicate the control of GABA release by D 2 R and D 4 R. To establish the sole contribution of D 2 R, we performed experiments with slices perfused with the selective D 4 R antagonist throughout the experiment (Jijon‐Lorenzo et al., 2018). In this condition, D2‐like agonist Quinpirole only decreased GABA release in circa of 40% (Figure 3f, GABA release; median control 100% versus median Quinpirole 64%, ranks 53–71, mean rank difference 10, p = 0.0136, n = 6).…”

Section: Resultsmentioning

confidence: 99%

“…[ 3 H]‐GABA release was determined with previous methods described in detail by Jijon‐Lorenzo et al. (2018). In each experiment, Pallidal slices from eight rats were pooled in a single incubation assay tube and left equilibrating for 30 min in ACSF maintained at 37°C and gassed with O 2 /CO 2 (95:5 v/v); then, they were incubated for 30 min in ACSF containing 80 nM [ 3 H]‐GABA (95 Ci/mmol).…”

Section: Methodsmentioning

confidence: 99%

“…On the other hand, different subtypes of the dopamine D2‐like receptors family are expressed predominantly in each population of neurons: D2 receptor subtype (D 2 R) is preferentially expressed in enkephalin‐positive MSNs (Surmeier et al., 1996), while pallidal neurons express the D4 receptor subtype (D 4 R) (Ariano et al., 1997; Mauger et al., 1998; Mrzljak et al., 1996). In this regard, D 2 Rs modulate the firing rate of MSNs (Hernandez‐Lopez et al., 2000) and the GABA release at striato‐pallidal terminals (Caballero‐Floran et al., 2016; Cooper & Stanford, 2001; Floran et al., 1997; Jijon‐Lorenzo et al., 2018) and striato‐striatal collaterals (Guzman et al., 2003). Likewise, D 4 Rs modulate the activity of pallidal neurons (Hernandez et al., 2006; Shin et al., 2003) and the GABA release at pallidal projections toward SNr (Aceves et al., 2011; Acosta‐Garcia et al., 2009; Cruz‐Trujillo et al., 2013), Sth (Floran et al., 2004b), and RTN (Barrientos et al., 2019; Crandall et al., 2010; Floran et al., 2004a; Gasca‐Martinez et al., 2010; Govindaiah et al., 2010).…”

Section: Introductionmentioning

confidence: 99%

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Dopamine D4 receptor modulates inhibitory transmission in pallido‐pallidal terminals and regulates motor behavior

Rojas

Acosta-García

Caballero‐Florán

et al. 2020

Eur J of Neuroscience

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Two major groups of terminals release GABA within the Globus pallidus; one group is constituted by projections from striatal neurons, while endings of the intranuclear collaterals form the other one. Each neurons' population expresses different subtypes of dopamine D2-like receptors: D 2 R subtype is expressed by encephalin-positive MSNs, while pallidal neurons express the D 4 R subtype. The D 2 R modulates the firing rate of striatal neurons and GABA release at their projection areas, while the D 4 R regulates Globus pallidus neurons excitability and GABA release at their projection areas. However, it is unknown if these receptors control GABA release at pallidopallidal collaterals and regulate motor behavior. Here, we present neurochemical evidence of protein content and binding of D 4 R in pallidal synaptosomes, control of [ 3 H] GABA release in pallidal slices of rat, electrophysiological evidence of the presence of D 4 R on pallidal recurrent collaterals in mouse slices, and turning behavior induced by D 4 R antagonist microinjected in amphetamine challenged rats. As in projection areas of pallidal neurons, GABAergic transmission in pallido-pallidal recurrent synapses is under modulation of D 4 R, while the D 2 R subtype, as known, modulates striato-pallidal projections. Also, as in projection areas, D 4 R contributes to 4564 | CONDE ROJAS Et Al. 2 | EXPERIMENTAL PROCEDURES 2.1 | Animals All procedures were carried out following the National Institutes of Health Guide for Care and Use of Laboratory Animals and approved by the Institutional Animal Care Committee of the CINVESTAV-IPN. Due to conveniences for technics and the amount of tissue required for experiments, Western blot, [ 3 H] YM-09151-2 D 4 R binding, [ 3 H] GABA release, and behavioral observations were done using

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Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Dopamine D4 receptor modulates inhibitory transmission in pallido‐pallidal terminals and regulates motor behavior

Rojas

Acosta-García

Caballero‐Florán

et al. 2020

Eur J of Neuroscience

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“…In this study, we found that chemogenetic activation of D2R-containing neurons in the dSTR did not significantly affect the behavioral stereotypies of vehicle-treated mice. This may be due to the activation of various types of D2R-containing neurons in the dSTR, including GABAergic projection neurons that can inhibit movement in indirect pathways, as well as inhibitory GABAergic or acetylcholinergic interneurons, which can inhibit GABAergic projection neurons ( Figure 9D ; Alcantara et al, 2003 ; Maurice et al, 2004 ; Zhang et al, 2009 ; Jijon-Lorenzo et al, 2018 ; Brandenburg et al, 2020 ; Lewis et al, 2020 ). Since D2R-containing projection and interneurons played the opposite role in movement, chemogenetic activation of D2R-containing neurons in the dSTR had no significant effect on behavioral stereotypies in mice.…”

Section: Discussionmentioning

confidence: 99%

“…D1Rs and D2Rs are distributed on DA neurons in the SNpc, as well as inhibitory interneurons ( Yung et al, 1995 ; Beaulieu and Gainetdinov, 2011 ; Yang et al, 2019 ). In addition, D2Rs are distributed on GABAergic projecting neurons of the indirect pathway and inhibitory interneurons in the dSTR ( Alcantara et al, 2003 ; Maurice et al, 2004 ; Zhang et al, 2009 ; Jijon-Lorenzo et al, 2018 ; Brandenburg et al, 2020 ; Lewis et al, 2020 ). However, D1R is only expressed on GABAergic projecting neurons of the direct pathway in the dSTR ( Avila-Luna et al, 2019 ; Assali et al, 2021 ), which is closely related to the regulation of dyskinesia in patients with Parkinson’s disease ( Calabrese et al, 2020 ).…”

Section: Introductionmentioning

confidence: 99%

Effects of Chemogenetic Inhibition of D1 or D2 Receptor-Containing Neurons of the Substantia Nigra and Striatum in Mice With Tourette Syndrome

Lin

Lan

Zhang

et al. 2021

Front. Mol. Neurosci.

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As tourette syndrome (TS) is a common neurobehavioral disorder, the primary symptoms of which include behavioral stereotypies. Dysfunction of the substantia nigra–striatum network could be the main pathogenesis of TS, which is closely associated with dopamine (DA) and its receptors. TS is often resistant to conventional treatments. Therefore, it is necessary to investigate the neurobiological mechanisms underlying its pathogenesis. In this study, we investigated whether chemogenetic activation or inhibition of dopaminergic D1 receptor (D1R)- or D2 receptor (D2R)-containing neurons in the substantia nigra pars compacta (SNpc) or dorsal striatum (dSTR) affected the stereotyped behavior and motor functions of TS mice. Intraperitoneal injection of 3,3′-iminodipropionitrile (IDPN) was used to induce TS in mice. Stereotyped behavior test and open-field, rotarod, and grip strength tests were performed to evaluate stereotyped behavior and motor functions, respectively. Immunofluorescence labeling was used to detect the co-labeling of virus fluorescence and D1R or D2R. We found that chemogenetic inhibition of D1R- or D2R-containing neurons in the SNpc and dSTR alleviated behavioral stereotypies and motor functions in TS mice. Chemogenetic activation of D1R-containing neurons in the dSTR aggravated behavioral stereotypies and motor functions in vehicle-treated mice, but neither was aggravated in TS mice. In conclusion, chemogenetic inhibition of D1R- or D2R-containing neurons in the SNpc and dSTR alleviated behavioral stereotypies of TS, providing a new treatment target for TS. Moreover, the activation of D1R-containing neurons in the dSTR may contribute to the pathogenesis of TS, which can be chosen as a more precise target for treatment.

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Activation of dopamine 2 receptors modulates glutamate decarboxylases 65 and 67 during stroke recovery in mice

Talhada,

Nilsson,

Walser

et al. 2023

Neuroprotection

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BackgroundsTreatment with levodopa enhances recovery of lost neurological functions in preclinical stroke models and patients. Here, we studied whether dopamine signaling modulates GABAergic neurotransmission in parvalbumin‐positive interneurons after experimental stroke.MethodsFollowing block randomization, mice were subjected to experimental stroke induced by photothrombosis (PT). Two days after the insult, mice were treated either with the D1 receptor antagonist by R(+)‐SCH‐23390 (0.1 mg/kg), the selective D1 receptor agonist (R)‐(+)‐SKF‐38393 hydrochloride (1 mg/kg), the D2 receptor agonist R(−)‐2,10,11‐trihydroxy‐N‐propyl‐noraporphine hydrobromide hydrate (TNPA) (1 mg/kg), the D2 receptor antagonist S‐(−)‐eticlopride hydrochloride (0.3 mg/kg), or vehicle (saline) by daily intraperitoneal injection for five consecutive days, respectively. Recovery of function was assessed by paw placement and foot fault test before and on Days 2 and 7 after surgery.ResultsMice treated with TNPA showed a statistically significant improvement of recovery compared to all other treatment conditions. Synthesis of gamma‐aminobutyric acid (GABA) was quantified by levels of full‐length and cleaved glutamate acid decarboxylase 67 and 65 (GAD65 and GAD67) in the peri‐infarct area and homotypic regions of the contralateral cortex. Compared to the other treatments, TNPA significantly reduced the level of the GAD67 isoform both in the ischemic and contralateral hemispheres. Levels of GAD65 were found significantly higher in the contralateral hemisphere in TNPA‐treated mice after PT accompanied by an increase in the 58 kDa‐truncated form.ConclusionOur results point toward reduced GABA synthesis in a D2 receptor‐mediated mechanism possibly contributing to counteract functional inhibition after stroke.

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Presynaptic Dopamine D2 Receptors Modulate [ 3 H]GABA Release at StriatoPallidal Terminals via Activation of PLC → IP3 → Calcineurin and Inhibition of AC → cAMP → PKA Signaling Cascades

Cited by 19 publications

References 60 publications

Dopamine D4 receptor modulates inhibitory transmission in pallido‐pallidal terminals and regulates motor behavior

Dopamine D4 receptor modulates inhibitory transmission in pallido‐pallidal terminals and regulates motor behavior

Effects of Chemogenetic Inhibition of D1 or D2 Receptor-Containing Neurons of the Substantia Nigra and Striatum in Mice With Tourette Syndrome

Activation of dopamine 2 receptors modulates glutamate decarboxylases 65 and 67 during stroke recovery in mice

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Presynaptic Dopamine D2 Receptors Modulate [ 3 H]GABA Release at StriatoPallidal Terminals via Activation of PLC → IP3 → Calcineurin and Inhibition of AC → cAMP → PKA Signaling Cascades

Cited by 19 publications

References 60 publications

Dopamine D4 receptor modulates inhibitory transmission in pallido‐pallidal terminals and regulates motor behavior

Dopamine D4 receptor modulates inhibitory transmission in pallido‐pallidal terminals and regulates motor behavior

Effects of Chemogenetic Inhibition of D1 or D2 Receptor-Containing Neurons of the Substantia Nigra and Striatum in Mice With Tourette Syndrome

Activation of dopamine 2 receptors modulates glutamate decarboxylases 65 and 67 during stroke recovery in mice

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Presynaptic Dopamine D2 Receptors Modulate [ 3 H]GABA Release at StriatoPallidal Terminals via Activation of PLC → IP3 → Calcineurin and Inhibition of AC → cAMP → PKA Signaling Cascades