Synaptic Zn2+ potentiates the effects of cocaine on striatal dopamine neurotransmission and behavior

Gomez, Juan L.; Bonaventura, Jordi; Keighron, Jacqueline; Wright, Kelsey M.; Marable, Dondre L.; Rodriguez, Lionel A.; Lam, Sherry; Carlton, Meghan L.; Ellis, Randall J.; Jordan, Chloe J.; Bi, Guo-hua; Solis, Oscar; Pignatelli, Marco; Bannon, Michael J.; Xi, Zheng-Xiong; Tanda, Gianluigi; Michaelides, Michael

doi:10.1038/s41398-021-01693-0

Title: Synaptic Zn2+ potentiates the effects of cocaine on striatal dopamine neurotransmission and behavior

Journal Article · Mon Nov 08 00:00:00 EST 2021 · Translational Psychiatry

DOI:https://doi.org/10.1038/s41398-021-01693-0· OSTI ID:1829344

Gomez, Juan L.;

; Keighron, Jacqueline;

; Marable, Dondre L.; Rodriguez, Lionel A.; Lam, Sherry; Carlton, Meghan L.; Ellis, Randall J.;

; Bi, Guo-hua; Solis, Oscar; Pignatelli, Marco;

; Xi, Zheng-Xiong;

;

Abstract Cocaine binds to the dopamine (DA) transporter (DAT) to regulate cocaine reward and seeking behavior. Zinc (Zn ²⁺ ) also binds to the DAT, but the in vivo relevance of this interaction is unknown. We found that Zn ²⁺ concentrations in postmortem brain (caudate) tissue from humans who died of cocaine overdose were significantly lower than in control subjects. Moreover, the level of striatal Zn ²⁺ content in these subjects negatively correlated with plasma levels of benzoylecgonine, a cocaine metabolite indicative of recent use. In mice, repeated cocaine exposure increased synaptic Zn ²⁺ concentrations in the caudate putamen (CPu) and nucleus accumbens (NAc). Cocaine-induced increases in Zn ²⁺ were dependent on the Zn ²⁺ transporter 3 (ZnT3), a neuronal Zn ²⁺ transporter localized to synaptic vesicle membranes, as ZnT3 knockout (KO) mice were insensitive to cocaine-induced increases in striatal Zn ²⁺ . ZnT3 KO mice showed significantly lower electrically evoked DA release and greater DA clearance when exposed to cocaine compared to controls. ZnT3 KO mice also displayed significant reductions in cocaine locomotor sensitization, conditioned place preference (CPP), self-administration, and reinstatement compared to control mice and were insensitive to cocaine-induced increases in striatal DAT binding. Finally, dietary Zn ²⁺ deficiency in mice resulted in decreased striatal Zn ²⁺ content, cocaine locomotor sensitization, CPP, and striatal DAT binding. These results indicate that cocaine increases synaptic Zn ²⁺ release and turnover/metabolism in the striatum, and that synaptically released Zn ²⁺ potentiates the effects of cocaine on striatal DA neurotransmission and behavior and is required for cocaine-primed reinstatement. In sum, these findings reveal new insights into cocaine’s pharmacological mechanism of action and suggest that Zn ²⁺ may serve as an environmentally derived regulator of DA neurotransmission, cocaine pharmacodynamics, and vulnerability to cocaine use disorders.

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Research Organization:: Brookhaven National Lab. (BNL), Upton, NY (United States)

Sponsoring Organization:: USDOE; USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division

Grant/Contract Number:: FG02-92ER14244; SC0012704

OSTI ID:: 1829344

Alternate ID(s):: OSTI ID: 1875644

Report Number(s):: BNL-223142-2022-JACI; 570; PII: 1693

Journal Information:: Translational Psychiatry, Journal Name: Translational Psychiatry Vol. 11 Journal Issue: 1; ISSN 2158-3188

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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