a Department of Medical Oncology, the First Affiliated Hospital of Xi'an Jiaotong University, Xi'an, 710061, China;
b School of Pharmacy, Health Science Center, Xi'an Jiaotong University, Xi'an, 710061, China;
c State Key Laboratory of Shaanxi for Natural Medicines Research and Engineering Xi'an, 710061, China
Funds:
This work was supported by the National Natural Science Foundation of China (Grant No.: 82374095), the Shaanxi Province Science Fund for Distinguished Young Scholars, China (Grant No.: 2023-JC-JQ-59), the Shaanxi Province Science and Technology Development Plan Project, China (Project No.: 2022ZDLSF05-05), and the Shaanxi Province Key Research Development Plan Project, China (Project No.: 2023-YBSF-523).
The nucleotide-binding oligomerization domain (NOD)-like receptor protein 3 (NLRP3) inflammasome is downregulated in hepatocellular carcinoma (HCC), and its stability is regulated by ubiquitination. However, the regulatory mechanisms underlying NLRP3 deubiquitination and its role in HCC metastasis remains unclear. We demonstrated that ubiquitin-specific protease 50 (USP50) directly interacts with NLRP3, exhibiting deubiquitinase (DUB) activity through specific cleavage of K48-linked polyubiquitination chains to stabilize NLRP3 by preventing proteasomal degradation. Clinically, we observed that low NLRP3 and high β-catenin levels were negatively correlated in HCC specimens. Subsequent mechanistic exploration confirmed that NLRP3 exerts negative regulation on β-catenin by binding with glycogen synthase kinase 3 beta (GSK3β), reversing the downstream epithelial-mesenchymal transition (EMT) process, and inhibiting HCC metastasis. Notably, USP50 was found to activate NLRP3 inflammasome by promoting nuclear factor-kappa B (NF-κB) signaling, consequently enhancing proinflammatory cytokines. Furthermore, USP50 overexpression negatively regulated β-catenin, reversed EMT process and inhibited HCC metastasis in vivo. In conclusion, USP50 has emerged as a key player in regulating the NLRP3 inflammasome and inhibiting HCC metastasis by reversing the EMT process. As a result, it presents itself as a promising therapeutic target for HCC in the clinical setting. The intricacies of this regulatory mechanism, as revealed by our study, provide valuable insights into the understanding and potential interventions for HCC.