D1 dopamine receptor stimulation increases GluR1 surface expression in nucleus accumbens neurons

Steven Z. Chao, Marjorie A. Ariano, Daniel A. Peterson, Marina Wolf

Research output: Contribution to journalArticle

95 Citations (Scopus)

Abstract

The goal of this study was to understand how dopamine receptors, which are activated during psychostimulant administration, might influence glutamate-dependent forms of synaptic plasticity that are increasingly recognized as important to drug addiction. Regulation of the surface expression of the α-amino-3-hydroxy-5-methylisoxazole-4-propionate (AMPA) receptor subunit GluR1 plays a critical role in long-term potentiation, a well-characterized form of synaptic plasticity. Primary cultures of rat nucleus accumbens neurons were used to examine whether dopamine receptor stimulation influences cell surface expression of GluR1, detected using antibody to the extracellular portion of GluR1 and fluorescence microscopy. Surface GluR1 labeling on processes of medium spiny neurons and interneurons was increased by brief (5-15 min) incubation with a D1 agonist (1 μM SKF 81297). This effect was attenuated by the D1 receptor antagonist SCH 23390 (10 μM) and reproduced by the adenylyl cyclase activator forskolin (10 μM). Labeling was decreased by glutamate (10-50 μM, 15 min). These results are the first to demonstrate modulation of AMPA receptor surface expression by a non-glutamatergic G protein-coupled receptor. Normally, this may enable ongoing regulation of AMPA receptor transmission in response to changes in the activity of dopamine projections to the nucleus accumbens. When dopamine receptors are over-stimulated during chronic drug administration, this regulation may be disrupted, leading to inappropriate plasticity in neuronal circuits governing motivation and reward.

Original languageEnglish (US)
Pages (from-to)704-712
Number of pages9
JournalJournal of Neurochemistry
Volume83
Issue number3
DOIs
StatePublished - Nov 1 2002
Externally publishedYes

Fingerprint

Dopamine D1 Receptors
Neuronal Plasticity
Propionates
Dopamine Receptors
Nucleus Accumbens
Neurons
Plasticity
Glutamic Acid
Labeling
Long-Term Potentiation
Drug and Narcotic Control
Interneurons
Colforsin
G-Protein-Coupled Receptors
Reward
Fluorescence Microscopy
Adenylyl Cyclases
Substance-Related Disorders
Motivation
Fluorescence microscopy

Keywords

  • AMPA receptors
  • GluR1
  • Primary cultures
  • Protein kinase A
  • Receptor trafficking

ASJC Scopus subject areas

  • Biochemistry
  • Cellular and Molecular Neuroscience

Cite this

D1 dopamine receptor stimulation increases GluR1 surface expression in nucleus accumbens neurons. / Chao, Steven Z.; Ariano, Marjorie A.; Peterson, Daniel A.; Wolf, Marina.

In: Journal of Neurochemistry, Vol. 83, No. 3, 01.11.2002, p. 704-712.

Research output: Contribution to journalArticle

Chao, Steven Z. ; Ariano, Marjorie A. ; Peterson, Daniel A. ; Wolf, Marina. / D1 dopamine receptor stimulation increases GluR1 surface expression in nucleus accumbens neurons. In: Journal of Neurochemistry. 2002 ; Vol. 83, No. 3. pp. 704-712.
@article{78916e0f96794d4fb546c1ee74fedfcd,
title = "D1 dopamine receptor stimulation increases GluR1 surface expression in nucleus accumbens neurons",
abstract = "The goal of this study was to understand how dopamine receptors, which are activated during psychostimulant administration, might influence glutamate-dependent forms of synaptic plasticity that are increasingly recognized as important to drug addiction. Regulation of the surface expression of the α-amino-3-hydroxy-5-methylisoxazole-4-propionate (AMPA) receptor subunit GluR1 plays a critical role in long-term potentiation, a well-characterized form of synaptic plasticity. Primary cultures of rat nucleus accumbens neurons were used to examine whether dopamine receptor stimulation influences cell surface expression of GluR1, detected using antibody to the extracellular portion of GluR1 and fluorescence microscopy. Surface GluR1 labeling on processes of medium spiny neurons and interneurons was increased by brief (5-15 min) incubation with a D1 agonist (1 μM SKF 81297). This effect was attenuated by the D1 receptor antagonist SCH 23390 (10 μM) and reproduced by the adenylyl cyclase activator forskolin (10 μM). Labeling was decreased by glutamate (10-50 μM, 15 min). These results are the first to demonstrate modulation of AMPA receptor surface expression by a non-glutamatergic G protein-coupled receptor. Normally, this may enable ongoing regulation of AMPA receptor transmission in response to changes in the activity of dopamine projections to the nucleus accumbens. When dopamine receptors are over-stimulated during chronic drug administration, this regulation may be disrupted, leading to inappropriate plasticity in neuronal circuits governing motivation and reward.",
keywords = "AMPA receptors, GluR1, Primary cultures, Protein kinase A, Receptor trafficking",
author = "Chao, {Steven Z.} and Ariano, {Marjorie A.} and Peterson, {Daniel A.} and Marina Wolf",
year = "2002",
month = "11",
day = "1",
doi = "10.1046/j.1471-4159.2002.01164.x",
language = "English (US)",
volume = "83",
pages = "704--712",
journal = "Journal of Neurochemistry",
issn = "0022-3042",
publisher = "Wiley-Blackwell",
number = "3",

}

TY - JOUR

T1 - D1 dopamine receptor stimulation increases GluR1 surface expression in nucleus accumbens neurons

AU - Chao, Steven Z.

AU - Ariano, Marjorie A.

AU - Peterson, Daniel A.

AU - Wolf, Marina

PY - 2002/11/1

Y1 - 2002/11/1

N2 - The goal of this study was to understand how dopamine receptors, which are activated during psychostimulant administration, might influence glutamate-dependent forms of synaptic plasticity that are increasingly recognized as important to drug addiction. Regulation of the surface expression of the α-amino-3-hydroxy-5-methylisoxazole-4-propionate (AMPA) receptor subunit GluR1 plays a critical role in long-term potentiation, a well-characterized form of synaptic plasticity. Primary cultures of rat nucleus accumbens neurons were used to examine whether dopamine receptor stimulation influences cell surface expression of GluR1, detected using antibody to the extracellular portion of GluR1 and fluorescence microscopy. Surface GluR1 labeling on processes of medium spiny neurons and interneurons was increased by brief (5-15 min) incubation with a D1 agonist (1 μM SKF 81297). This effect was attenuated by the D1 receptor antagonist SCH 23390 (10 μM) and reproduced by the adenylyl cyclase activator forskolin (10 μM). Labeling was decreased by glutamate (10-50 μM, 15 min). These results are the first to demonstrate modulation of AMPA receptor surface expression by a non-glutamatergic G protein-coupled receptor. Normally, this may enable ongoing regulation of AMPA receptor transmission in response to changes in the activity of dopamine projections to the nucleus accumbens. When dopamine receptors are over-stimulated during chronic drug administration, this regulation may be disrupted, leading to inappropriate plasticity in neuronal circuits governing motivation and reward.

AB - The goal of this study was to understand how dopamine receptors, which are activated during psychostimulant administration, might influence glutamate-dependent forms of synaptic plasticity that are increasingly recognized as important to drug addiction. Regulation of the surface expression of the α-amino-3-hydroxy-5-methylisoxazole-4-propionate (AMPA) receptor subunit GluR1 plays a critical role in long-term potentiation, a well-characterized form of synaptic plasticity. Primary cultures of rat nucleus accumbens neurons were used to examine whether dopamine receptor stimulation influences cell surface expression of GluR1, detected using antibody to the extracellular portion of GluR1 and fluorescence microscopy. Surface GluR1 labeling on processes of medium spiny neurons and interneurons was increased by brief (5-15 min) incubation with a D1 agonist (1 μM SKF 81297). This effect was attenuated by the D1 receptor antagonist SCH 23390 (10 μM) and reproduced by the adenylyl cyclase activator forskolin (10 μM). Labeling was decreased by glutamate (10-50 μM, 15 min). These results are the first to demonstrate modulation of AMPA receptor surface expression by a non-glutamatergic G protein-coupled receptor. Normally, this may enable ongoing regulation of AMPA receptor transmission in response to changes in the activity of dopamine projections to the nucleus accumbens. When dopamine receptors are over-stimulated during chronic drug administration, this regulation may be disrupted, leading to inappropriate plasticity in neuronal circuits governing motivation and reward.

KW - AMPA receptors

KW - GluR1

KW - Primary cultures

KW - Protein kinase A

KW - Receptor trafficking

UR - http://www.scopus.com/inward/record.url?scp=0036829202&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0036829202&partnerID=8YFLogxK

U2 - 10.1046/j.1471-4159.2002.01164.x

DO - 10.1046/j.1471-4159.2002.01164.x

M3 - Article

VL - 83

SP - 704

EP - 712

JO - Journal of Neurochemistry

JF - Journal of Neurochemistry

SN - 0022-3042

IS - 3

ER -