Neurotensin receptor 1-biased ligand attenuates neurotensin-mediated excitation of ventral tegmental area dopamine neurons and dopamine release in the nucleus accumbens.


Journal

Neuropharmacology
ISSN: 1873-7064
Titre abrégé: Neuropharmacology
Pays: England
ID NLM: 0236217

Informations de publication

Date de publication:
15 08 2023
Historique:
received: 02 12 2022
revised: 29 03 2023
accepted: 10 04 2023
pmc-release: 15 08 2024
medline: 17 5 2023
pubmed: 14 4 2023
entrez: 13 4 2023
Statut: ppublish

Résumé

Strong expression of the G protein-coupled receptor (GPCR) neurotensin receptor 1 (NTR1) in ventral tegmental area (VTA) dopamine (DA) neurons and terminals makes it an attractive target to modulate DA neuron activity and normalize DA-related pathologies. Recent studies have identified a novel class of NTR1 ligand that shows promising effects in preclinical models of addiction. A lead molecule, SBI-0654553 (SBI-553), can act as a positive allosteric modulator of NTR1 β-arrestin recruitment while simultaneously antagonizing NTR1 Gq protein signaling. Using cell-attached recordings from mouse VTA DA neurons we discovered that, unlike neurotensin (NT), SBI-553 did not independently increase spontaneous firing. Instead, SBI-553 blocked the NT-mediated increase in firing. SBI-553 also antagonized the effects of NT on dopamine D2 auto-receptor signaling, potentially through its inhibitory effects on G-protein signaling. We also measured DA release directly, using fast-scan cyclic voltammetry in the nucleus accumbens and observed antagonist effects of SBI-553 on an NT-induced increase in DA release. Further, in vivo administration of SBI-553 did not notably change basal or cocaine-evoked DA release measured in NAc using fiber photometry. Overall, these results indicate that SBI-553 blunts NT's effects on spontaneous DA neuron firing, D2 auto-receptor function, and DA release, without independently affecting these measures. In the presence of NT, SBI-553 has an inhibitory effect on mesolimbic DA activity, which could contribute to its efficacy in animal models of psychostimulant use.

Identifiants

pubmed: 37055008
pii: S0028-3908(23)00134-X
doi: 10.1016/j.neuropharm.2023.109544
pmc: PMC10192038
mid: NIHMS1893083
pii:
doi:

Substances chimiques

Dopamine VTD58H1Z2X
neurotensin type 1 receptor 0
Receptors, Neurotensin 0
Neurotensin 39379-15-2
Ligands 0
Dopamine D2 Receptor Antagonists 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

109544

Subventions

Organisme : BLRD VA
ID : I01 BX005782
Pays : United States
Organisme : NIDA NIH HHS
ID : R00 DA048970
Pays : United States
Organisme : NIDA NIH HHS
ID : R01 DA036612
Pays : United States
Organisme : BLRD VA
ID : I01 BX003759
Pays : United States
Organisme : NIDA NIH HHS
ID : R33 DA038019
Pays : United States

Informations de copyright

Published by Elsevier Ltd.

Déclaration de conflit d'intérêts

Declaration of competing interest US patents 9 868 707 and 10 118 902 relating to the chemistry of SBI-553 and its derivatives have been issued to the Sanford Burnham Prebys Medical Research Institute (A.B·P.) and Duke University (M.G.C., L.S·B.).

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Auteurs

Sarthak M Singhal (SM)

Department of Neurosciences, University of California San Diego, La Jolla, CA, USA.

Vivien Zell (V)

Department of Neurosciences, University of California San Diego, La Jolla, CA, USA.

Lauren Faget (L)

Department of Neurosciences, University of California San Diego, La Jolla, CA, USA.

Lauren M Slosky (LM)

Department of Pharmacology, University of Minnesota, Minneapolis, MN, USA.

Lawrence S Barak (LS)

Department of Cell Biology, Duke University, Durham, NC, USA.

Marc G Caron (MG)

Departments of Cell Biology, Neurobiology and Medicine, Duke University, Durham, NC, USA.

Anthony B Pinkerton (AB)

Conrad Prebys Center for Chemical Genomics, Sanford Burnham Prebys Medical Discovery Institute, La Jolla, CA, USA.

Thomas S Hnasko (TS)

Department of Neurosciences, University of California San Diego, La Jolla, CA, USA; Research Service, VA San Diego Healthcare System, San Diego, CA, USA. Electronic address: thnasko@health.ucsd.edu.

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Classifications MeSH