Locomotor activity depends on β-arrestin recruitment by the dopamine D1 receptor in the striatal D1-D3 receptor heteromer

Several dopaminergic compounds, including the clinically used pramipexole, are labelled as preferential dopamine D3 receptor (D3R) agonists based on their moderately higher affinity for the D3R versus other D2-like receptor subtypes. In rodents, these compounds typically produce locomotor depression...

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Main Authors: Alexandra H. Evans, Marc Ciruela-Jardí, William Rea, Bradley M. Keegan, Marjorie R. Levinstein, Alessandro Bonifazi, Jianjing Cao, Shelley N. Jackson, Lei Shi, Nil Casajuana-Martin, Ning-Sheng Cai, Vicent Casadó, Christopher J. Earley, Amy H. Newman, Michael Michaelides, Leonardo Pardo, Estefanía Moreno, Sergi Ferré
Format: Article
Language:English
Published: Elsevier 2025-08-01
Series:Pharmacological Research
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Online Access:http://www.sciencedirect.com/science/article/pii/S1043661825002518
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author Alexandra H. Evans
Marc Ciruela-Jardí
William Rea
Bradley M. Keegan
Marjorie R. Levinstein
Alessandro Bonifazi
Jianjing Cao
Shelley N. Jackson
Lei Shi
Nil Casajuana-Martin
Ning-Sheng Cai
Vicent Casadó
Christopher J. Earley
Amy H. Newman
Michael Michaelides
Leonardo Pardo
Estefanía Moreno
Sergi Ferré
author_facet Alexandra H. Evans
Marc Ciruela-Jardí
William Rea
Bradley M. Keegan
Marjorie R. Levinstein
Alessandro Bonifazi
Jianjing Cao
Shelley N. Jackson
Lei Shi
Nil Casajuana-Martin
Ning-Sheng Cai
Vicent Casadó
Christopher J. Earley
Amy H. Newman
Michael Michaelides
Leonardo Pardo
Estefanía Moreno
Sergi Ferré
author_sort Alexandra H. Evans
collection DOAJ
description Several dopaminergic compounds, including the clinically used pramipexole, are labelled as preferential dopamine D3 receptor (D3R) agonists based on their moderately higher affinity for the D3R versus other D2-like receptor subtypes. In rodents, these compounds typically produce locomotor depression with low doses and locomotor activation with higher doses, which has been assumed to be mediated by presynaptic D3Rs and postsynaptic striatal D2Rs, respectively. However, studies with selective pharmacological and genetic blockade of each dopamine receptor subtype suggest opposite roles. We address this apparent conundrum by performing a comprehensive in vitro, in vivo and ex vivo pharmacological comparison of several preferential D3R agonists. Their differential properties reveal that their locomotor activating effects in mice are dependent on the striatal postsynaptic D3Rs forming heteromers with D1Rs, via their ability to potentiate β-arrestin recruitment by the D1R in the D1R-D3R heteromer. The results also indicate that the locomotor depressant effects are largely dependent on their ability to activate presynaptic D2Rs. More broadly, it is demonstrated that locomotor activity in mice depends on β-arrestin recruitment by the D1R in the striatal D1R-D3R heteromer. These results can have implications for the treatment of L-dopa-induced dyskinesia and Restless Legs Syndrome.
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spelling doaj-art-7c442476baee47efb3cac2234a75ff8b2025-08-20T02:45:42ZengElsevierPharmacological Research1096-11862025-08-0121810782610.1016/j.phrs.2025.107826Locomotor activity depends on β-arrestin recruitment by the dopamine D1 receptor in the striatal D1-D3 receptor heteromerAlexandra H. Evans0Marc Ciruela-Jardí1William Rea2Bradley M. Keegan3Marjorie R. Levinstein4Alessandro Bonifazi5Jianjing Cao6Shelley N. Jackson7Lei Shi8Nil Casajuana-Martin9Ning-Sheng Cai10Vicent Casadó11Christopher J. Earley12Amy H. Newman13Michael Michaelides14Leonardo Pardo15Estefanía Moreno16Sergi Ferré17Integrative Neurobiology Section, National Institute on Drug Abuse, Intramural Research Program, National Institutes of Health, Baltimore, MD, USALaboratory of Molecular Neuropharmacology, Department of Biochemistry and Molecular Biomedicine, Faculty of Biology and Institute of Biomedicine, University of Barcelona, Barcelona, Spain; Laboratory of Computational Medicine, Biostatistics Unit, Faculty of Medicine, Autonomous University of Barcelona, Bellaterra, SpainIntegrative Neurobiology Section, National Institute on Drug Abuse, Intramural Research Program, National Institutes of Health, Baltimore, MD, USAComputational Chemistry and Molecular Biophysics Section, National Institute on Drug Abuse, Intramural Research Program, National Institutes of Health, Baltimore, MD, USA; Medicinal Chemistry Section, National Institute on Drug Abuse, Intramural Research Program, National Institutes of Health, Baltimore, MD, USABiobehavioral Imaging and Molecular Neuropsychopharmacology Section, National Institute on Drug Abuse, Intramural Research Program, National Institutes of Health, Baltimore, MD, USAMedicinal Chemistry Section, National Institute on Drug Abuse, Intramural Research Program, National Institutes of Health, Baltimore, MD, USAMedicinal Chemistry Section, National Institute on Drug Abuse, Intramural Research Program, National Institutes of Health, Baltimore, MD, USATranslational Analytical Core, National Institute on Drug Abuse, Intramural Research Program, National Institutes of Health, Baltimore, MD, USAComputational Chemistry and Molecular Biophysics Section, National Institute on Drug Abuse, Intramural Research Program, National Institutes of Health, Baltimore, MD, USALaboratory of Computational Medicine, Biostatistics Unit, Faculty of Medicine, Autonomous University of Barcelona, Bellaterra, SpainIntegrative Neurobiology Section, National Institute on Drug Abuse, Intramural Research Program, National Institutes of Health, Baltimore, MD, USALaboratory of Molecular Neuropharmacology, Department of Biochemistry and Molecular Biomedicine, Faculty of Biology and Institute of Biomedicine, University of Barcelona, Barcelona, SpainDepartment of Neurology and Sleep Medicine, Johns Hopkins University School of Medicine, Baltimore, MD, USAMedicinal Chemistry Section, National Institute on Drug Abuse, Intramural Research Program, National Institutes of Health, Baltimore, MD, USABiobehavioral Imaging and Molecular Neuropsychopharmacology Section, National Institute on Drug Abuse, Intramural Research Program, National Institutes of Health, Baltimore, MD, USALaboratory of Computational Medicine, Biostatistics Unit, Faculty of Medicine, Autonomous University of Barcelona, Bellaterra, SpainLaboratory of Molecular Neuropharmacology, Department of Biochemistry and Molecular Biomedicine, Faculty of Biology and Institute of Biomedicine, University of Barcelona, Barcelona, Spain; Corresponding authors.Integrative Neurobiology Section, National Institute on Drug Abuse, Intramural Research Program, National Institutes of Health, Baltimore, MD, USA; Corresponding authors.Several dopaminergic compounds, including the clinically used pramipexole, are labelled as preferential dopamine D3 receptor (D3R) agonists based on their moderately higher affinity for the D3R versus other D2-like receptor subtypes. In rodents, these compounds typically produce locomotor depression with low doses and locomotor activation with higher doses, which has been assumed to be mediated by presynaptic D3Rs and postsynaptic striatal D2Rs, respectively. However, studies with selective pharmacological and genetic blockade of each dopamine receptor subtype suggest opposite roles. We address this apparent conundrum by performing a comprehensive in vitro, in vivo and ex vivo pharmacological comparison of several preferential D3R agonists. Their differential properties reveal that their locomotor activating effects in mice are dependent on the striatal postsynaptic D3Rs forming heteromers with D1Rs, via their ability to potentiate β-arrestin recruitment by the D1R in the D1R-D3R heteromer. The results also indicate that the locomotor depressant effects are largely dependent on their ability to activate presynaptic D2Rs. More broadly, it is demonstrated that locomotor activity in mice depends on β-arrestin recruitment by the D1R in the striatal D1R-D3R heteromer. These results can have implications for the treatment of L-dopa-induced dyskinesia and Restless Legs Syndrome.http://www.sciencedirect.com/science/article/pii/S1043661825002518Dopamine D1 receptorDopamine D3 receptorHeteromersStriatumβ-arrestinLocomotor activity
spellingShingle Alexandra H. Evans
Marc Ciruela-Jardí
William Rea
Bradley M. Keegan
Marjorie R. Levinstein
Alessandro Bonifazi
Jianjing Cao
Shelley N. Jackson
Lei Shi
Nil Casajuana-Martin
Ning-Sheng Cai
Vicent Casadó
Christopher J. Earley
Amy H. Newman
Michael Michaelides
Leonardo Pardo
Estefanía Moreno
Sergi Ferré
Locomotor activity depends on β-arrestin recruitment by the dopamine D1 receptor in the striatal D1-D3 receptor heteromer
Pharmacological Research
Dopamine D1 receptor
Dopamine D3 receptor
Heteromers
Striatum
β-arrestin
Locomotor activity
title Locomotor activity depends on β-arrestin recruitment by the dopamine D1 receptor in the striatal D1-D3 receptor heteromer
title_full Locomotor activity depends on β-arrestin recruitment by the dopamine D1 receptor in the striatal D1-D3 receptor heteromer
title_fullStr Locomotor activity depends on β-arrestin recruitment by the dopamine D1 receptor in the striatal D1-D3 receptor heteromer
title_full_unstemmed Locomotor activity depends on β-arrestin recruitment by the dopamine D1 receptor in the striatal D1-D3 receptor heteromer
title_short Locomotor activity depends on β-arrestin recruitment by the dopamine D1 receptor in the striatal D1-D3 receptor heteromer
title_sort locomotor activity depends on β arrestin recruitment by the dopamine d1 receptor in the striatal d1 d3 receptor heteromer
topic Dopamine D1 receptor
Dopamine D3 receptor
Heteromers
Striatum
β-arrestin
Locomotor activity
url http://www.sciencedirect.com/science/article/pii/S1043661825002518
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