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Crucial Role of Dopamine D2 Receptor Signaling in Nicotine-Induced Conditioned Place Preference

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Abstract

Nicotine in tobacco causes psychological dependence through its rewarding effect in the central nervous system (CNS). Although nicotine dependence is explained by dopamine receptor (DR) signaling together with nicotinic acetylcholine receptors (nAChRs), the synaptic molecular mechanism underlying the interaction between dopamine receptor and nAChRs remains unclear. Since reward signaling is mediated by dopamine receptors, we hypothesized that the dopamine D2 receptor (D2R), in part, mediates the synaptic modulation of nicotine-induced conditioned place preference (CPP) in addition to dopamine D1 receptor. To investigate the involvement of D2R, wild-type (WT) and dopamine D2 receptor knockout (D2RKO) mice were assessed using the CPP task after induction of nicotine-induced CPP. As expected, D2RKO mice failed to induce CPP behaviors after repeated nicotine administration (0.5 mg/kg). When kinase signaling was assessed in the nucleus accumbens and hippocampal CA1 region after repeated nicotine administration, both Ca2+/calmodulin-dependent protein kinase (CaMKII) and extracellular signal-regulated kinase (ERK) were upregulated in WT mice but not in D2RKO mice. Likewise, nicotine-induced CPP was associated with elevation of pro- brain-derived neurotropic factor (BDNF) and BDNF protein levels in WT mice, but not in D2RKO mice. Taken together, in addition to dopamine D1 receptor signaling, dopamine D2 receptor signaling is critical for induction of nicotine-induced CPP in mice.

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Abbreviations

AcS:

Nucleus accumbens shell

ACC:

Anterior cingulate cortex

α4β2nAChR:

Alpha 4 beta 2 nicotinic acetylcholine receptors

α7nAChRs:

Alpha 7 nicotinic acetylcholine receptors

BDNF:

Brain-derived neurotropic factor

CaMKII:

Calcium/calmodulin-dependent protein kinase II

CHRNA4:

Nicotinic acetylcholine receptor (Nachr) Α4 subunit

CPP:

Conditioned placed preference

CREB:

cAMP response element binding

D2RKO:

Dopamine D2 receptor knockout

DLS:

Dorsolateral striatum

D1R:

Dopamine D1 receptors

D2R:

Dopamine D2 receptors

ERK:

Extracellular signal-regulated kinase

LTP:

Long-term potentiation

MSN:

Medium spiny neurons

NAc:

Nucleus accumbens

NTRK2:

Neurotrophic tyrosine kinase receptor 2

pCREB:

Phosphorylation cAMP response element binding

PK:

Phosphokinase C

PVDF:

Polyvinylidene difluoride

PtC:

Parietal association cortex

VTA:

Ventral tegmental area

WT:

Wild type

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Conflict of Interest

The authors declare that they have no conflict of interest.

Funding

This research was funded by the Grant Indonesia Endowment Fund for Education (LPDP) to G.W. and Indonesia Endowment fund for Education (LPDP) and Smoking Research Foundation and the Project of Translational and Clinical Research Core Centers, AMED, Japan (JP17dm0107071 and JP18dm0107071 to K.F.).

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Authors and Affiliations

  1. Department of Pharmacology, Graduate School of Pharmaceutical Sciences, Tohoku University, Miyagi-ken, Sendai-shi, Aoba-Ku, Aramaki, Aoba 6-3, Sendai, 980-8578, Japan

    Gofarana Wilar, Yasuharu Shinoda & 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. Department of Comparative and Experimental Medicine, Brain Research Institute, Niigata University, Niigata, 951-8585, Japan

    Toshikuni Sasaoka

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  1. Gofarana Wilar
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  2. Yasuharu Shinoda
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  4. Kohji Fukunaga
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Contributions

K.F. and G.W. conceived and coordinated the study and wrote the paper. G.W. performed and analyzed the experiment shown in figures. Y.S. provided technical assistance. K.F. and G.W. reviewed the results. All authors approved the final version of the manuscript.

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Correspondence to Kohji Fukunaga.

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All experimental animal procedures were approved by the Committee on Animal Experiments at Tohoku University, and studies were conducted in accordance with committee guidelines.

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Wilar, G., Shinoda, Y., Sasaoka, T. et al. Crucial Role of Dopamine D2 Receptor Signaling in Nicotine-Induced Conditioned Place Preference. Mol Neurobiol 56, 7911–7928 (2019). https://doi.org/10.1007/s12035-019-1635-x

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