Li Yuanyuan, Gao Wenqing, Qiu Yuxin, Pan Jiasong, Guo Qingqing, Liu Xuehe, Geng Lu, Shen Yajie, Deng Yifan, Hu Zhidong, Li Suhua, Liu Shanshan, Idris Adi, Huang Jinqing, Yang Hua, Ge Baoxue, Fan Xiaoyong, Chen Xiangjun, Li Jixi
State Key Laboratory of Genetics and Development of Complex Phenotypes, Department of Neurology, Huashan Hospital and School of Life Sciences, Fudan University, Shanghai, China.
Centre for Immunology and Infection Control, School of Biomedical Sciences, Queensland University of Technology, Brisbane, QLD, Australia.
Cell Death Differ. 2025 May 14. doi: 10.1038/s41418-025-01527-2.
RING1 is an E3 ligase component of the polycomb repressive complex 1 (PRC1) with known roles in chromatin regulation and cellular processes such as apoptosis and autophagy. However, its involvement in inflammation and pyroptosis remains elusive. Here, we demonstrate that human RING1, not RING2, promotes K48-linked ubiquitination of Gasdermin D (GSDMD) and acts as a negative regulator of pyroptosis and bacterial infection. Indeed, we showed that loss of Ring1 increased S. typhimurium infectious load and mortality in vivo. Though RING1 deletion initially reduced M. tuberculosis (Mtb) infectious load in vivo, increased lung inflammation and impaired immune defense responses were later observed. Moreover, Ring1 knockout exacerbated acute sepsis induced by lipopolysaccharide (LPS) in vivo. Mechanistically, RING1 directly interacts with GSDMD and ubiquitinates the K51 and K168 sites of GSDMD for K48-linked proteasomal degradation, thereby inhibiting pyroptosis. Inhibition of RING1 E3 ligase activity by direct mutation or with the use of small molecule inhibitors increased GSDMD level and cell death during pyroptosis. Our findings reveal that RING1 dictates GSDMD-mediated inflammatory response and host susceptibility to pathogen infection, highlighting RING1 as a potential therapeutic target for combating infectious diseases.
RING1是多梳抑制复合物1(PRC1)的一种E3连接酶成分,在染色质调控以及细胞凋亡和自噬等细胞过程中发挥着已知作用。然而,其在炎症和细胞焦亡中的作用仍不清楚。在此,我们证明人RING1而非RING2促进Gasdermin D(GSDMD)的K48连接的泛素化,并作为细胞焦亡和细菌感染的负调节因子。事实上,我们表明Ring1缺失会增加鼠伤寒沙门氏菌在体内的感染负荷和死亡率。虽然RING1缺失最初会降低结核分枝杆菌(Mtb)在体内的感染负荷,但随后会观察到肺部炎症增加和免疫防御反应受损。此外,Ring1基因敲除会加剧体内脂多糖(LPS)诱导的急性脓毒症。从机制上讲,RING1直接与GSDMD相互作用,并使GSDMD的K51和K168位点发生泛素化,以进行K48连接的蛋白酶体降解,从而抑制细胞焦亡。通过直接突变或使用小分子抑制剂抑制RING1 E3连接酶活性,会增加细胞焦亡期间的GSDMD水平和细胞死亡。我们的研究结果表明,RING1决定了GSDMD介导的炎症反应和宿主对病原体感染的易感性,突出了RING1作为对抗传染病的潜在治疗靶点。