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E3 ubiquitin ligase UBR5 modulates circadian rhythm by facilitating the ubiquitination and degradation of the key clock transcription factor BMAL1

Chun-yan Duan1,2, Yue Li1, Hao-yu Zhi1, Yao Tian3, Zheng-yun Huang4, Su-ping Chen1, Yang Zhang1, Qing Liu1, Liang Zhou1, Xiao-gang Jiang1, Kifayat Ullah1, Qing Guo5, Zhao-hui Liu5, Ying Xu4, Jun-hai Han3, Jiajie Hou6, Darran P O’Connor2, Guoqiang Xu1,7,8
1 Jiangsu Key Laboratory of Neuropsychiatric Diseases and College of Pharmaceutical Sciences, Jiangsu Province Engineering Research Center of Precision Diagnostics and Therapeutics Development, Jiangsu Key Laboratory of Preventive and Translational Medicine for Geriatric Diseases, Suzhou Key Laboratory of Drug Research for Prevention and Treatment of Hyperlipidemic Diseases, Soochow University, Suzhou 215123, China
2 School of Pharmacy and Biomolecular Sciences, RCSI University of Medicine and Health Sciences, 123 St Stephen’s Green, Dublin 2, D02 YN77 Dublin, Ireland
3 School of Life Science and Technology, The Key Laboratory of Developmental Genes and Human Disease, Southeast University, 2 Sipailou Road, Nanjing 210096, China
4 Jiangsu Key Laboratory of Neuropsychiatric Diseases and Cambridge-Suda Genomic Resource Center, Soochow University, Suzhou 215123, China
5 Department of Human Anatomy and Cytoneurobiology, Medical School of Soochow University, Suzhou 215123, China
6 Cancer Centre, Faculty of Health Sciences, University of Macau, Macau SAR, China
7 Suzhou International Joint Laboratory for Diagnosis and Treatment of Brain Diseases, College of Pharmaceutical Sciences, Soochow University, Suzhou 215123, China
8 MOE Key Laboratory of Geriatric Diseases and Immunology, Suzhou Medical College of Soochow University, Suzhou 215123, China
Correspondence to: Guoqiang Xu: gux2002@suda.edu.cn,
DOI: 10.1038/s41401-024-01290-z
Received: 1 January 2024
Accepted: 10 April 2024
Advance online: 13 May 2024

Abstract

The circadian clock is the inner rhythm of life activities and is controlled by a self-sustained and endogenous molecular clock, which maintains a ~ 24 h internal oscillation. As the core element of the circadian clock, BMAL1 is susceptible to degradation through the ubiquitin-proteasome system (UPS). Nevertheless, scant information is available regarding the UPS enzymes that intricately modulate both the stability and transcriptional activity of BMAL1, affecting the cellular circadian rhythm. In this work, we identify and validate UBR5 as a new E3 ubiquitin ligase that interacts with BMAL1 by using affinity purification, mass spectrometry, and biochemical experiments. UBR5 overexpression induced BMAL1 ubiquitination, leading to diminished stability and reduced protein level of BMAL1, thereby attenuating its transcriptional activity. Consistent with this, UBR5 knockdown increases the BMAL1 protein. Domain mapping discloses that the C-terminus of BMAL1 interacts with the N-terminal domains of UBR5. Similarly, cell-line-based experiments discover that HYD, the UBR5 homolog in Drosophila, could interact with and downregulate CYCLE, the BMAL1 homolog in Drosophila. PER2-luciferase bioluminescence real-time reporting assay in a mammalian cell line and behavioral experiments in Drosophila reveal that UBR5 or hyd knockdown significantly reduces the period of the circadian clock. Therefore, our work discovers a new ubiquitin ligase UBR5 that regulates BMAL1 stability and circadian rhythm and elucidates the underlying molecular mechanism. This work provides an additional layer of complexity to the regulatory network of the circadian clock at the post-translational modification level, offering potential insights into the modulation of the dysregulated circadian rhythm.

Keywords: BMAL1; circadian rhythm; proteomics; transcriptional activity; ubiquitination; UBR5

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