Wang Yichen, Nan Yanyang, Ma Chunguang, Lu Xiaolin, Wang Qian, Huang Xiting, Xue Wenjing, Fan Jiajun, Ju Dianwen, Ye Dingwei, Zhang Xuyao
Department of Urology, Fudan University Shanghai Cancer Center, Department of Oncology, Shanghai Medical College, Fudan University, Shanghai, 200032, China.
Department of Biological Medicines & Shanghai Engineering Research Center of Immunotherapeutic, Fudan University School of Pharmacy, Shanghai, 201203, China.
Cell Death Dis. 2024 Apr 25;15(4):293. doi: 10.1038/s41419-024-06665-y.
Research and development on Nectin-4 antibody-drug conjugates (ADC) have been greatly accelerated since the approval of enfortumab vedotin to treat uroepithelial cancer. During the course of this study, we identified that autophagy serves as a cytoprotective mechanism during Nectin-4-MMAE treatment and proposed a strategy to enhance the antitumor effects of Nectin-4-MMAE in bladder cancer. Nectin-4-MMAE rapidly internalized into bladder cancer cells in 30 minutes and released MMAE, inducing the onset of caspase-mediated apoptosis and leading to the inhibition of tumor cell growth. Transcriptomics showed significant alterations in autophagy-associated genes in bladder cancer cells treated with Nectin-4-MMAE, which suggested autophagy was activated by Nectin-4-MMAE. Furthermore, autophagy activation was characterized by ultrastructural analysis of autophagosome accumulation, immunofluorescence of autophagic flux, and immunoblotting autophagy marker proteins SQSTM1 and LC3 I/II. Importantly, inhibiting autophagy by LY294002 and chloroquine significantly enhances the cytotoxicity effects of Nectin-4-MMAE in bladder cancer cells. Additionally, we detected the participation of the AKT/mTOR signaling cascade in the induction of autophagy by Nectin-4-MMAE. The combination of Nectin-4-MMAE and an autophagy inhibitor demonstrated enhanced antitumor effects in the HT1376 xenograft tumor model. After receiving a single dose of Nectin-4-MMAE, the group that received the combination treatment showed a significant decrease in tumor size compared to the group that received only one type of treatment. Notably, one mouse in the combination treatment group achieved complete remission of the tumor. The combination group exhibited a notable rise in apoptosis and necrosis, as indicated by H&E staining and immunohistochemistry (cleaved caspase-3, ki67). These findings demonstrated the cytoprotective role of autophagy during Nectin-4-MMAE treatment and highlighted the potential of combining Nectin-4-MMAE with autophagy inhibitors for bladder cancer treatment.
自恩沃利单抗获批用于治疗尿路上皮癌以来,Nectin-4抗体药物偶联物(ADC)的研发进程大大加快。在本研究过程中,我们发现自噬在Nectin-4-MMAE治疗期间起到细胞保护作用,并提出了一种增强Nectin-4-MMAE对膀胱癌抗肿瘤作用的策略。Nectin-4-MMAE在30分钟内迅速内化进入膀胱癌细胞并释放MMAE,诱导半胱天冬酶介导的凋亡发生并导致肿瘤细胞生长受到抑制。转录组学显示,用Nectin-4-MMAE处理的膀胱癌细胞中自噬相关基因有显著改变,这表明Nectin-4-MMAE激活了自噬。此外,通过自噬体积累的超微结构分析、自噬流的免疫荧光以及自噬标记蛋白SQSTM1和LC3 I/II的免疫印迹对自噬激活进行了表征。重要的是,用LY294002和氯喹抑制自噬可显著增强Nectin-4-MMAE对膀胱癌细胞的细胞毒性作用。此外,我们检测到AKT/mTOR信号级联参与了Nectin-4-MMAE诱导的自噬过程。Nectin-4-MMAE与自噬抑制剂联合使用在HT1376异种移植肿瘤模型中显示出增强的抗肿瘤作用。在接受单剂量Nectin-4-MMAE后,联合治疗组的肿瘤大小与仅接受一种治疗的组相比显著减小。值得注意的是,联合治疗组中有一只小鼠实现了肿瘤完全缓解。苏木精-伊红染色和免疫组织化学(裂解的半胱天冬酶-3、ki67)显示,联合组的凋亡和坏死显著增加。这些发现证明了自噬在Nectin-4-MMAE治疗期间的细胞保护作用,并突出了将Nectin-4-MMAE与自噬抑制剂联合用于膀胱癌治疗的潜力。