Gillespie Matthew S, Chiang Kelly, Regan-Mochrie Gemma L, Choi Soo-Youn, Ward Ciara M, Sahay Debashish, Garcia Paloma, Arnold Roland, Davies Clare C
Department of Cancer and Genomic Sciences, University of Birmingham, Birmingham, B15 2TT, UK.
School of Cancer Sciences, University of Southampton, Southampton, SO16 6YD, UK.
Oncogene. 2025 Apr;44(13):862-876. doi: 10.1038/s41388-024-03264-1. Epub 2024 Dec 18.
Breast cancer stem cells (BCSCs) are a rare cell population that is responsible for tumour initiation, metastasis and chemoresistance. Despite this, the mechanism by which BCSCs withstand genotoxic stress is largely unknown. Here, we uncover a pivotal role for the arginine methyltransferase PRMT5 in mediating BCSC chemoresistance by modulating DNA repair efficiency. Mechanistically, we identify PRMT5 as a major regulator of DNA damage response (DDR) gene splicing in BCSCs, particularly those integral to the Fanconi Anaemia and homologous recombination pathways, with PRMT5 inhibition synergising with chemotherapy to promote BCSC apoptosis. A comparison of BCSCs and their bulk cell progeny identified some shared (ATM, DDX11, EXO1, FAN1, SLX4) but many unique (ATR, RAD17, RAD51D, RUVBL1) PRMT5-dependent alternative DDR splicing events. Surprisingly, these skipped exons and retained intron events rarely lead to substantial gene expression repression, suggesting that PRMT5 inhibition predominantly results in nuclear detention of intron-containing transcripts and the production of non-canonical isoforms with compromised protein function. Since many genes within the same DDR pathway undergo deregulated splicing, this study thus reveals additional points of vulnerability and alternative combination drug strategies that could improve the therapeutic efficacy of PRMT5 inhibitors to promote BCSC eradication.
乳腺癌干细胞(BCSCs)是一种罕见的细胞群体,负责肿瘤的起始、转移和化疗耐药。尽管如此,BCSCs耐受基因毒性应激的机制在很大程度上仍不清楚。在此,我们揭示了精氨酸甲基转移酶PRMT5在通过调节DNA修复效率介导BCSC化疗耐药中的关键作用。从机制上讲,我们确定PRMT5是BCSCs中DNA损伤反应(DDR)基因剪接的主要调节因子,特别是那些对范可尼贫血和同源重组途径至关重要的因子,PRMT5抑制与化疗协同作用以促进BCSC凋亡。对BCSCs及其大量细胞后代的比较确定了一些共同的(ATM、DDX11、EXO1、FAN1、SLX4)但许多独特的(ATR、RAD17、RAD51D、RUVBL1)PRMT5依赖性替代DDR剪接事件。令人惊讶的是,这些跳过的外显子和保留的内含子事件很少导致大量基因表达抑制,这表明PRMT5抑制主要导致含内含子转录本的核滞留以及产生蛋白质功能受损的非经典异构体。由于同一DDR途径中的许多基因经历失调剪接,因此本研究揭示了额外的脆弱点和替代联合药物策略,这些策略可以提高PRMT5抑制剂的治疗效果以促进BCSC根除。