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Articles, Cellular/Molecular

Opposing Role for Egr3 in Nucleus Accumbens Cell Subtypes in Cocaine Action

Ramesh Chandra, T. Chase Francis, Prasad Konkalmatt, Ariunzaya Amgalan, Amy M. Gancarz, David M. Dietz and Mary Kay Lobo
Journal of Neuroscience 20 May 2015, 35 (20) 7927-7937; DOI: https://doi.org/10.1523/JNEUROSCI.0548-15.2015
Ramesh Chandra
1Department of Anatomy and Neurobiology and
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T. Chase Francis
1Department of Anatomy and Neurobiology and
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Prasad Konkalmatt
2Department of Medicine, Division of Nephrology, University of Maryland School of Medicine Baltimore, Maryland 21201, and
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Ariunzaya Amgalan
1Department of Anatomy and Neurobiology and
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Amy M. Gancarz
3Department of Pharmacology and Toxicology, The Research Institution Addictions, State University of New York at Buffalo, Buffalo, New York 14214
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David M. Dietz
3Department of Pharmacology and Toxicology, The Research Institution Addictions, State University of New York at Buffalo, Buffalo, New York 14214
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Mary Kay Lobo
1Department of Anatomy and Neurobiology and
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Abstract

An imbalance in molecular signaling cascades and transcriptional regulation in nucleus accumbens (NAc) medium spiny neuron (MSN) subtypes, those enriched in dopamine D1 versus D2 receptors, is implicated in the behavioral responses to psychostimulants. To provide further insight into the molecular mechanisms occurring in MSN subtypes by cocaine, we examined the transcription factor early growth response 3 (Egr3). We evaluated Egr3 because it is a target of critical cocaine-mediated signaling pathways and because Egr3-binding sites are found on promoters of key cocaine-associated molecules. We first used a RiboTag approach to obtain ribosome-associated transcriptomes from each MSN subtype and found that repeated cocaine administration induced Egr3 ribosome-associated mRNA in NAc D1-MSNs while reducing Egr3 in D2-MSNs. Using Cre-inducible adeno-associated viruses combined with D1-Cre and D2-Cre mouse lines, we observed that Egr3 overexpression in D1-MSNs enhances rewarding and locomotor responses to cocaine, whereas overexpression in D2-MSNs blunts these behaviors. miRNA knock-down of Egr3 in MSN subtypes produced opposite behavioral responses from those observed with overexpression. Finally, we found that repeated cocaine administration altered Egr3 binding to promoters of genes that are important for cocaine-mediated cellular and behavioral plasticity. Genes with increased Egr3 binding to promoters, Camk2α, CREB, FosB, Nr4a2, and Sirt1, displayed increased mRNA in D1-MSNs and, in some cases, a reduction in D2-MSNs. Histone and the DNA methylation enzymes G9a and Dnmt3a displayed reduced Egr3 binding to their promoters and reduced mRNA in D1-MSNs. Our study provides novel insight into an opposing role of Egr3 in select NAc MSN subtypes in cocaine action.

  • cocaine
  • Egr3
  • medium spiny neurons
  • nucleus accumbens
  • RiboTag
  • transcription
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The Journal of Neuroscience: 35 (20)
Journal of Neuroscience
Vol. 35, Issue 20
20 May 2015
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Opposing Role for Egr3 in Nucleus Accumbens Cell Subtypes in Cocaine Action
Ramesh Chandra, T. Chase Francis, Prasad Konkalmatt, Ariunzaya Amgalan, Amy M. Gancarz, David M. Dietz, Mary Kay Lobo
Journal of Neuroscience 20 May 2015, 35 (20) 7927-7937; DOI: 10.1523/JNEUROSCI.0548-15.2015

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Opposing Role for Egr3 in Nucleus Accumbens Cell Subtypes in Cocaine Action
Ramesh Chandra, T. Chase Francis, Prasad Konkalmatt, Ariunzaya Amgalan, Amy M. Gancarz, David M. Dietz, Mary Kay Lobo
Journal of Neuroscience 20 May 2015, 35 (20) 7927-7937; DOI: 10.1523/JNEUROSCI.0548-15.2015
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Keywords

  • cocaine
  • Egr3
  • medium spiny neurons
  • nucleus accumbens
  • RiboTag
  • transcription

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