Department of Thoracic Surgery, Zhongshan Hospital, Fudan University, Shanghai, China.
Commun Biol. 2024 Jun 20;7(1):751. doi: 10.1038/s42003-024-06452-7.
Ferroptosis is a recently discovered form of cell death that plays an important role in tumor growth and holds promise as a target for antitumor therapy. However, evidence in the regulation of ferroptosis in lung adenocarcinoma (LUAD) remains elusive. Here, we show that retinoic acid receptor alpha (RARA) is upregulated with the treatment of ferroptosis inducers (FINs). Pharmacological activation of RARA increases the resistance of LUAD to ferroptosis according to cell viability and lipid peroxidation assays, while RARA inhibitor or knockdown (KD) does the opposite. Through transcriptome sequencing in RARA-KD cells and chromatin immunoprecipitation (CHIP)-Seq data, we identify thioredoxin (TXN) and protein phosphatase 1 F (PPM1F) as downstream targets of RARA, both of which inhibit ferroptosis. We confirm that RARA binds to the promotor region of TXN and PPM1F and promotes their transcription by CHIP-qPCR and dual-luciferase assays. Overexpression of TXN and PPM1F reverses the effects of RARA knockdown on ferroptosis in vitro and vivo. Clinically, RARA knockdown or inhibitor increases cells' sensitivity to pemetrexed and cisplatin (CDDP). Immunohistochemistry (IHC) of LUAD from our cohort shows the same expression tendency of RARA and the downstream targets. Our study uncovers that RARA inhibits ferroptosis in LUAD by promoting TXN and PPM1F, and inhibiting RARA-TXN/PPM1F axis represents a promising strategy for improving the efficacy of FINs or chemotherapy in the treatment of LUAD patients.
铁死亡是一种新发现的细胞死亡形式,在肿瘤生长中起着重要作用,并有望成为抗肿瘤治疗的靶点。然而,在肺腺癌(LUAD)中,铁死亡的调节证据仍不清楚。在这里,我们表明视黄酸受体α(RARA)在铁死亡诱导剂(FINs)的治疗下上调。根据细胞活力和脂质过氧化测定,RARA 的药理学激活增加了 LUAD 对铁死亡的耐药性,而 RARA 抑制剂或敲低(KD)则相反。通过 RARA-KD 细胞的转录组测序和染色质免疫沉淀(CHIP)-Seq 数据,我们确定硫氧还蛋白(TXN)和蛋白磷酸酶 1F(PPM1F)为 RARA 的下游靶点,两者均抑制铁死亡。我们证实 RARA 结合到 TXN 和 PPM1F 的启动子区域,并通过 CHIP-qPCR 和双荧光素酶测定促进它们的转录。TXN 和 PPM1F 的过表达逆转了 RARA 敲低对体外和体内铁死亡的影响。临床上,RARA 敲低或抑制剂增加了细胞对培美曲塞和顺铂(CDDP)的敏感性。我们队列中 LUAD 的免疫组织化学(IHC)显示出 RARA 和下游靶点相同的表达趋势。我们的研究揭示了 RARA 通过促进 TXN 和 PPM1F 来抑制 LUAD 中的铁死亡,抑制 RARA-TXN/PPM1F 轴代表了提高 FINs 或化疗治疗 LUAD 患者疗效的有前途的策略。