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Dopamine D1 receptor subtype mediates acute stress-induced dendritic growth in excitatory neurons of the medial prefrontal cortex and contributes to suppression of stress susceptibility in mice

Molecular Psychiatry volume 23, pages 1717–1730 (2018)Cite this article

Abstract

Dopamine in prefrontal cortices is implicated in cognitive and emotional functions, and the dysfunction of prefrontal dopamine has been associated with cognitive and emotional deficits in mental illnesses. These findings have led to clinical trials of dopamine-targeting drugs and brain imaging of dopamine receptors in patients with mental illnesses. Rodent studies have suggested that dopaminergic pathway projecting to the medial prefrontal cortex (mPFC) suppresses stress susceptibility. Although various types of mPFC neurons express several dopamine receptor subtypes, previous studies neither isolated a role of dopamine receptor subtype nor identified the site of its action in mPFC. Using social defeat stress (SDS) in mice, here we identified a role of dopamine D1 receptor subtype in mPFC excitatory neurons in suppressing stress susceptibility. Repeated social defeat stress (R-SDS) reduces the expression of D1 receptor subtype in mPFC of mice susceptible to R-SDS. Knockdown of D1 receptor subtype in whole neuronal populations or excitatory neurons in mPFC facilitates the induction of social avoidance by SDS. Single social defeat stress (S-SDS) induces D1 receptor-mediated extracellular signal-regulated kinase phosphorylation and c-Fos expression in mPFC neurons. Whereas R-SDS reduces dendritic lengths of mPFC layer II/III pyramidal neurons, S-SDS increases arborization and spines of apical dendrites of these neurons in a D1 receptor-dependent manner. Collectively, our findings show that D1 receptor subtype and related signaling in mPFC excitatory neurons mediate acute stress-induced dendritic growth of these neurons and contribute to suppression of stress susceptibility. Therefore, we propose that D1 receptor-mediated dendritic growth in mPFC excitatory neurons suppresses stress susceptibility.

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Acknowledgments

We thank Dr Dai Watanabe for his helpful comments and discussions; Tae Arai, Akiko Washimi, Yuki Nakanishi and Misako Takizawa for secretarial helps; and Nodoka Asamoto for animal breeding and care. The present study was supported by a grant from AMED-CREST of JST (to SN), Grants-in-Aids for Scientific Research from the Japan Society for the Promotion of Science (24689015 and 16H05132 to TF; 13J04246 and 16K18365 to RS), Grants-in-Aids for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology in Japan (25116517, 25116715, 15H01289, 17H05572 and 17H06057 to TF), a grant from AMED (to TF), grants from the Uehara Memorial Foundation (to TF), the Sumitomo Foundation (to TF), the Astellas Foundation for Research on Metabolic Disorders (to TF) and the Takeda Science Foundation (to TF), United States Public Health Service Grants MH-084018, MH-094268, MH-069853, MH-085226, MH-088753 and MH-092443 (to AS) and grants from Stanley (to AS), RUSK (to AS), S-R foundations (to AS), NARSAD (to AS) and Maryland Stem Cell Research Fund (to AS).

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  1. These authors contributed equally to this work.

  2. Current address: Douglas Mental Health University Institute, McGill University, Montreal, Quebec, Canada.

Authors and Affiliations

  1. Division of Pharmacology, Kobe University Graduate School of Medicine, Kobe, Japan

    R Shinohara, M Taniguchi, S Kitaoka & T Furuyashiki

  2. Medical Innovation Center, Kyoto University Graduate School of Medicine, Kyoto, Japan

    R Shinohara, A T Ehrlich, K Yokogawa, Y Deguchi, A Ogawa, S Kitaoka, S Narumiya & T Furuyashiki

  3. Department of Biological Sciences, Kyoto University Graduate School of Medicine, Kyoto, Japan

    M Taniguchi

  4. International Institute for Integrative Sleep Medicine, University of Tsukuba, Tsukuba, Japan

    Y Cherasse, M Lazarus & Y Urade

  5. Department of Psychiatry, Johns Hopkins University School of Medicine, Baltimore, MD, USA

    A Sawa

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Shinohara, R., Taniguchi, M., Ehrlich, A.T. et al. Dopamine D1 receptor subtype mediates acute stress-induced dendritic growth in excitatory neurons of the medial prefrontal cortex and contributes to suppression of stress susceptibility in mice. Mol Psychiatry 23, 1717–1730 (2018). https://doi.org/10.1038/mp.2017.177

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