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Glucagon-like peptide 1 receptor activation regulates cocaine actions and dopamine homeostasis in the lateral septum by decreasing arachidonic acid levels

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Reddy, I A, Pino, J A, Weikop, P, Osses, N, Sørensen, G, Bering, T, Valle, C, Bluett, R J +10 more·2016·Translational Psychiatry
DOI 10.1038/tp.2016.86PMC PMC5070047
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Abstract

Agonism of the glucagon-like peptide 1 (GLP-1) receptor (GLP-1R) has been effective at treating aspects of addictive behavior for a number of abused substances, including cocaine. However, the molecular mechanisms and brain circuits underlying the therapeutic effects of GLP-1R signaling on cocaine actions remain elusive. Recent evidence has revealed that endogenous signaling at the GLP-1R within the forebrain lateral septum (LS) acts to reduce cocaine-induced locomotion and cocaine conditioned place preference, both considered dopamine (DA)-associated behaviors. DA terminals project from the ventral tegmental area to the LS and express the DA transporter (DAT). Cocaine acts by altering DA bioavailability by targeting the DAT. Therefore, GLP-1R signaling might exert effects on DAT to account for its regulation of cocaine-induced behaviors. We show that the GLP-1R is highly expressed within the LS. GLP-1, in LS slices, significantly enhances DAT surface expression and DAT function. Exenatide (Ex-4), a long-lasting synthetic analog of GLP-1 abolished cocaine-induced elevation of DA. Interestingly, acute administration of Ex-4 reduces septal expression of the retrograde messenger 2-arachidonylglycerol (2-AG), as well as a product of its presynaptic degradation, arachidonic acid (AA). Notably, AA reduces septal DAT function pointing to AA as a novel regulator of central DA homeostasis. We further show that AA oxidation product γ-ketoaldehyde (γ-KA) forms adducts with the DAT and reduces DAT plasma membrane expression and function. These results support a mechanism in which postsynaptic septal GLP-1R activation regulates 2-AG levels to alter presynaptic DA homeostasis and cocaine actions through AA.

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  • Increased extracellular LS-DA release has been observed in response to systemic application of cocaine in rats and morphine in mice.

    “Increased extracellular LS-DA release has been observed in response to systemic application of drugs of abuse such as cocaine in rats and morphine in mice [32,33]”

    From Involvement of dopamine, but not norepinephrine, in the sex-specific regulation of juvenile socially rewarding behavior by vasopressin (2018) · cites this paper as [32]

    The Results section (page unavailable) reports that cocaine increased extracellular lateral-septum dopamine in mice and that the results were paralleled in rats. But cocaine was perfused locally through a microdialysis probe, not administered systemically; the systemic injection was the GLP-1R agonist Ex-4. The morphine-in-mice finding is separately cited in the citing sentence and is not attributed to this paper. (LLM, conf=0.86)

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Authors
Reddy, I. A., Pino, J. A., Weikop, P., Osses, N., Sørensen, G., Bering, T., Valle, C., Bluett, R. J., Erreger, K., Wortwein, G., Reyes, J. G., Graham, D., Stanwood, G. D., Hackett, T. A., Patel, S., Fink-Jensen, A., Torres, G. E., & Galli, A.
Affiliations
  • Vanderbilt University (US)
  • Pontificia Universidad Católica de Valparaíso (CL)
  • University of Copenhagen (DK)
  • Viña del Mar University (CL)
  • Vanderbilt University Medical Center (US)
  • Florida State University (US)
  • University of Florida (US)
Corresponding author
  • Reddy, I A
  • Pino, J A
  • Galli, A
ORCID
Venue
Translational Psychiatry
Publisher
Springer Science and Business Media LLC
Published
2016-05-17
Volume
6
Issue
5
Pages
e809-e809
ISSN
2158-3188 (ISSN-L)
DOI
10.1038/tp.2016.86
PMC
PMC5070047
OpenAlex
W2398164808
Cited by
96
References
11
Citations by year
2026: 13 · 2025: 15 · 2024: 9 · 2023: 4 · 2022: 13 · 2021: 10 · 2020: 6 · 2019: 8 · 2018: 7 · 2017: 11
FWCI
4.86
Type
journal article
Language
en
Open access
Licence
Locations
  • Translational Psychiatry (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Research at the University of Copenhagen (University of Copenhagen) (publishedVersion, cc-by)
  • DigiNole (Florida State University) (submittedVersion)
Funders
  • Vanderbilt University
  • Vanderbilt University Medical Center (T32GM007347)
  • Pontificia Universidad Católica de Valparaíso
  • National Institutes of Health (1s10od017997-01a1, 5r01da035263-11)
  • Comisión Nacional de Investigación Científica y Tecnológica
  • National Institute of Mental Health (R01MH100096, F31MH106192)
  • National Institute on Drug Abuse (R21DA035588, R01-DA035263, R01DA038598, F30DA036940, R01DA021213, R01DA038058)
  • National Cancer Institute (P01CA077839)
  • National Institute on Deafness and Other Communication Disorders (K18DC012527, R01DC015388)
  • National Institute of General Medical Sciences (T32GM007347)
  • Eunice Kennedy Shriver National Institute of Child Health and Human Development (U54HD083211)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Health Sciences › Medicine › Pharmacology › Cannabis and Cannabinoid Research
Keywords
GLP-1 receptor, cocaine, dopamine homeostasis, lateral septum, arachidonic acid, 2-arachidonoylglycerol, dopamine transporter, exenatide, cocaine-induced locomotion, cocaine conditioned place preference, ventral tegmental area, presynaptic modulation, endocannabinoid signaling
MeSH terms
Glucagon-Like Peptide-1 Receptor, Exenatide, Glucagon-Like Peptide-1 Receptor Agonists, Animals, Arachidonic Acids, Cocaine, Dopamine, Glycerides, Homeostasis, Peptides, Septal Nuclei, Venoms, Arachidonic Acid, Proto-Oncogene Proteins c-fos, Microdialysis, Dopamine Uptake Inhibitors, Dopamine Plasma Membrane Transport Proteins, Mice, Incretins, Endocannabinoids

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