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.
School of Pharmacy and Biomolecular Sciences, RCSI University of Medicine and Health Sciences, 123 St Stephen's Green, Dublin 2, D02 YN77, Dublin, Ireland.
Acta Pharmacol Sin. 2024 Sep;45(9):1793-1808. doi: 10.1038/s41401-024-01290-z. Epub 2024 May 13.
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.
生物钟是生命活动的内在节律,由一个自我维持和内源性的分子钟控制,维持着大约 24 小时的内部振荡。作为生物钟的核心元件,BMAL1 容易通过泛素蛋白酶体系统(UPS)降解。然而,关于UPS 酶如何精细调节 BMAL1 的稳定性和转录活性,从而影响细胞生物钟节律的信息却很少。在这项工作中,我们通过亲和纯化、质谱和生化实验鉴定并验证了 UBR5 是一种新的 E3 泛素连接酶,它与 BMAL1 相互作用。UBR5 的过表达诱导了 BMAL1 的泛素化,导致 BMAL1 的稳定性降低和蛋白水平降低,从而减弱其转录活性。与此一致的是,UBR5 的敲低增加了 BMAL1 蛋白。结构域映射显示 BMAL1 的 C 端与 UBR5 的 N 端结构域相互作用。同样,基于细胞系的实验发现,果蝇中 UBR5 的同源物 HYD 可以与 BMAL1 的同源物 CYCLE 相互作用并下调其表达。在哺乳动物细胞系中的 PER2-荧光素酶生物发光实时报告测定和果蝇中的行为实验表明,UBR5 或 hyd 的敲低显著缩短了生物钟的周期。因此,我们的工作发现了一种新的泛素连接酶 UBR5,它可以调节 BMAL1 的稳定性和生物钟节律,并阐明了潜在的分子机制。这项工作在翻译后修饰水平上为生物钟的调控网络提供了额外的复杂性,为失调生物钟的调控提供了潜在的见解。