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Impaired Acquisition of Nicotine-Induced Conditioned Place Preference in Fatty Acid-Binding Protein 3 Null Mice

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Abstract

Nicotine causes psychological dependence through its interactions with nicotinic acetylcholine receptors in the brain. We previously demonstrated that fatty acid-binding protein 3 (FABP3) colocalizes with dopamine D2 receptors (D2Rs) in the dorsal striatum, and FABP3 deficiency leads to impaired D2R function. Moreover, D2R null mice do not exhibit increased nicotine-induced conditioned place preference (CPP) following chronic nicotine administration. To investigate the role of FABP3 in nicotine-induced CPP, FABP3 knockout (FABP3−/−) mice were evaluated using a CPP apparatus following consecutive nicotine administration (0.5 mg/kg) for 14 days. Importantly, nicotine-induced CPP was suppressed in the conditioning, withdrawal, and relapse phases in FABP3−/− mice. To resolve the mechanisms underlying impaired nicotine-induced CPP in these mice, we assessed c-Fos expression and Ca2+/calmodulin-dependent protein kinase II (CaMKII) and extracellular signal-regulated kinase (ERK) signaling in both dopamine D1 receptor (D1R)- and D2R-positive neurons in the nucleus accumbens (NAc). Notably, 64% of dopamine receptor-positive neurons in the mouse NAc expressed both D1R and D2R. Impaired nicotine-induced CPP was correlated with lack of responsiveness of both CaMKII and ERK phosphorylation. The number of D2R-positive neurons was increased in FABP3−/− mice, while the number of D1R-positive neurons and the responsiveness of c-Fos expression to nicotine were decreased. The aberrant c-Fos expression was closely correlated with CaMKII but not ERK phosphorylation levels in the NAc of FABP3−/− mice. Taken together, these results indicate that impaired D2R signaling due to lack of FABP3 may affect D1R and c-Fos signaling and underlie nicotine-induced CPP behaviors.

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Funding

This research was funded by the Strategic Research Program for Brain Sciences of the Japan Agency for Medical Research and Development (AMED) (grant numbers JP18dm0107071, JP19dm0107071, and 20dm0107071) to K.F. W.J. is a recipient of funding from the Otsuka Toshimi Scholarship Foundation.

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Authors and Affiliations

  1. Department of Pharmacology, Graduate School of Pharmaceutical Sciences, Tohoku University, 6-3 Aramaki-Aoba, Aoba-ku, Sendai, 980-0845, Japan

    Wenbin Jia, Gofarana Wilar, Ichiro Kawahata, An Cheng & Kohji Fukunaga

  2. Department of Pharmacology and Clinical Pharmacy, Faculty of Pharmacy, Universitas Padjadjaran, JL. Raya Bandung-Sumedang KM 20.5 Jatinangor, Sumedang, Jawa Barat, 45363, Indonesia

    Gofarana Wilar

  3. Sendai, Japan

    Kohji Fukunaga

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  1. Wenbin Jia
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  2. Gofarana Wilar
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  3. Ichiro Kawahata
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  4. An Cheng
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  5. Kohji Fukunaga
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Contributions

W.J. conducted the experiments and wrote the manuscript. G.W. provided technical assistance. A.C. performed methodology and validation. I.K. performed the validation and revised the manuscript. K.F. conceived, supervised, and coordinated the study; wrote, reviewed, and edited the manuscript; and secured funding.

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Correspondence to Kohji Fukunaga.

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All experimental procedures using mice were approved by the Committee on Animal Experiments at the Tohoku University.

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Jia, W., Wilar, G., Kawahata, I. et al. Impaired Acquisition of Nicotine-Induced Conditioned Place Preference in Fatty Acid-Binding Protein 3 Null Mice. Mol Neurobiol 58, 2030–2045 (2021). https://doi.org/10.1007/s12035-020-02228-2

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