Liu Liang, Wang Rui, Cheng Ke, Bai Chunmei, Ji Yuke, Zhang Yifei, Yang Haoran, Gong Miaomiao, Xie Fang, Zhao Yongshun, Pan Jinjin, Yuan Yuhui
The Second Affiliated Hospital, Institute of Cancer Stem Cell, Dalian Medical University, Dalian, China.
College of Pharmacy, Dalian Medical University, Dalian, China.
Oncogene. 2025 Jul 15. doi: 10.1038/s41388-025-03494-x.
Glioblastoma (GBM) is an incurable disease with a poor prognosis. However, the potential impact of steroid receptor coactivator-1 (SRC-1) on N6-methyladenosine (m6A) RNA modification and its role in promoting malignant progression in GBM remain unclear. The relationship between SRC-1 and the m6A "writer" protein, methyltransferase 3 (METTL3), was analyzed using data from the CGGA database. Dot blot and MeRIP‒qPCR were performed to evaluate the effects of SRC-1 knockdown or overexpression on the level of m6A modification in GBM. The biological functions of SRC-1 in regulating METTL3 in GBM were evaluated by assessing its effects on proliferation, migration, cell cycle, colony formation, and apoptosis in vitro and the tumor volume/weight of nude mice xenografted with GBM cells in vivo. Co-IP, immunofluorescence, dual-luciferase, and ChIP‒qPCR assays were subsequently conducted. By analyzing the CGGA database, we determined that SRC-1 has a close positive relationship with METTL3 in GBM. SRC-1 significantly increased the m6A RNA modification level in GBM, SRC-1 knockdown markedly inhibited c-Myc m6A methylation and mRNA stability by suppressing METTL3, and SRC-1 overexpression led to hypermethylation by increasing METTL3. SRC-1 knockdown inhibited the proliferation, migration, apoptosis resistance, and S and G2/M phases of GBM cells in vitro. Mechanically, SRC-1 interacted with the heterodimer of NF-κB p50/p65, whereby p65 activated METTL3 by directly binding to a specific region of its promoter (+18 to +27 bp), thereby increasing the m6A modification of c-Myc and ultimately promoting GBM progression. Importantly, both SRC-1 knockdown and treatment with bufalin, an SRC inhibitor, reduced GBM progression. In conclusion, this study provides the first comprehensive evidence that SRC-1 facilitates GBM progression by binding to NF-κB and regulating METTL3-mediated m6A modification of c-Myc, offering new insights into potential therapeutic strategies for GBM. Schematic diagram of the mechanism revealed in this research. SRC-1 regulates METTL3-mediated m6A RNA modification of c-Myc to promote GBM progression by binding to the NF-κB transcription factor. Created in BioRender. https://BioRender.com .
胶质母细胞瘤(GBM)是一种无法治愈且预后较差的疾病。然而,类固醇受体共激活因子-1(SRC-1)对N6-甲基腺苷(m6A)RNA修饰的潜在影响及其在GBM恶性进展中的作用仍不清楚。利用中国胶质瘤基因组图谱(CGGA)数据库的数据分析了SRC-1与m6A“书写器”蛋白甲基转移酶3(METTL3)之间的关系。进行斑点杂交和甲基化RNA免疫沉淀定量PCR(MeRIP-qPCR)以评估SRC-1敲低或过表达对GBM中m6A修饰水平的影响。通过评估其对体外增殖、迁移、细胞周期、集落形成和凋亡的影响以及对体内接种GBM细胞的裸鼠肿瘤体积/重量的影响,来评价SRC-1在GBM中调节METTL3的生物学功能。随后进行了免疫共沉淀(Co-IP)、免疫荧光、双荧光素酶和染色质免疫沉淀定量PCR(ChIP-qPCR)分析。通过分析CGGA数据库,我们确定SRC-1在GBM中与METTL3存在密切的正相关关系。SRC-1显著提高了GBM中的m6A RNA修饰水平,SRC-1敲低通过抑制METTL3显著抑制c-Myc的m6A甲基化和mRNA稳定性,而SRC-1过表达通过增加METTL3导致高甲基化。SRC-1敲低在体外抑制了GBM细胞的增殖、迁移、抗凋亡能力以及S期和G2/M期。机制上,SRC-1与NF-κB p50/p65异二聚体相互作用,由此p65通过直接结合其启动子的特定区域(+18至+27bp)激活METTL3,从而增加c-Myc的m6A修饰并最终促进GBM进展。重要的是,SRC-1敲低和SRC抑制剂蟾毒灵处理均降低了GBM进展。总之,本研究首次提供了全面的证据,表明SRC-1通过与NF-κB结合并调节METTL3介导的c-Myc的m6A修饰促进GBM进展,为GBM的潜在治疗策略提供了新的见解。本研究揭示的机制示意图。SRC-1通过与NF-κB转录因子结合来调节METTL3介导的c-Myc的m6A RNA修饰,从而促进GBM进展。由BioRender创建。https://BioRender.com 。