Article

Dendritic cell nuclear protein-1 regulates melatonin biosynthesis by binding to BMAL1 and inhibiting the transcription of N-acetyltransferase in C6 cells

Dong CHEN1, Yi-pei LI1, Yan-xia YU2, Tian ZHOU3, Chao LIU4, Er-kang FEI5, Feng GAO1, Chen-chen MU1, Hai-gang REN1, Guang-hui WANG1
1 Laboratory of Molecular Neuropathology, Jiangsu Key Laboratory of Translational Research and Therapy for Neuro-Psycho-Diseases and College of Pharmaceutical Sciences, Soochow University, Suzhou 215123, China
2 Department of Pharmacy, Suzhou Hospital Affiliated with Nanjing Medical University, Suzhou 215002, China
3 Medical School of Nanchang University, Nanchang 330031, China
4 Department of Histology and Embryology, School of Basic Medical Science, Anhui Medical University, Hefei 230032, China
5 Laboratory of Synapse Development and Plasticity, Institute of Life Science, Nanchang University, Nanchang 330031, China
Correspondence to: Dong CHEN: 2018@aps.com, Hai-gang REN: rhg@suda.edu.cn, Guang-hui WANG: wanggh@suda.edu.cn,
DOI: 10.1038/aps.2017.163
Received: 7 December 2017
Accepted: 1 July 2017
Advance online: 12 September 2017

Abstract

Abstract
Dendritic cell nuclear protein-1 (DCNP1) is a protein associated with major depression. In the brains of depression patients, DCNP1 is up-regulated. However, how DCNP1 participates in the pathogenesis of major depression remains unknown. In this study, we first transfected HEK293 cells with EGFP-DCNP1 and demonstrated that the full-length DCNP1 protein was localized in the nucleus, and RRK (the residues 117-119) composed its nuclear localization signal (NLS). An RRK-deletion form of DCNP1 (DCNP1ΔRRK) and truncated form (DCNP11-116), each lacking the RRK residues, did not show the specific nuclear localization like full-length DCNP1 in the cells. A rat glioma cell line C6 can synthesize melatonin, a hormone that plays important roles in both sleep and depression. We then revealed that transfection of C6 cells with full-length DCNP1 but not DCNP1ΔRRK or DCNP11-116 significantly decreased the levels of melatonin. Furthermore, overexpression of full-length DCNP1, but not DCNP1ΔRRK or DCNP11-116, in C6 cells significantly decreased both the mRNA and protein levels of N-acetyltransferase (NAT), a key enzyme in melatonin synthesis. Full-length DCNP1 but not DCNP1ΔRRK or DCNP11-116 was detected to interact with the Nat promoter and inhibited its activity through its E-box motif. Furthermore, full-length DCNP1 but not the mutants interacted with and repressed the transcriptional activity of BMAL1, a transcription factor that transactivates Nat through the E-box motif. In conclusion, we have shown that RRK (the residues 117-119) are the NLS responsible for DCNP1 nuclear localization. Nuclear DCNP1 represses NAT expression and melatonin biosynthesis by interacting with BMAL1 and repressing its transcriptional activity. Our study reveals a connection between the major depression candidate protein DCNP1, circadian system and melatonin biosynthesis, which may contribute to the pathogenesis of depression.
Keywords: major depression; DCNP1; N-acetyltransferase; melatonin; circadian system; BMAL1; rat glioma cell line C6

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