Regulatory RNAs and Cancer Section, Genetics Branch, Center for Cancer Research (CCR), National Cancer Institute (NCI), National Institutes of Health (NIH), Bethesda, Maryland, USA.
DNA Replication Group, Developmental Therapeutics Branch, CCR, NCI, NIH, Bethesda, Maryland, USA.
Mol Cell Biol. 2024;44(2):43-56. doi: 10.1080/10985549.2024.2307574. Epub 2024 Feb 12.
Transcription factors play key roles in development and disease by controlling gene expression. Forkhead box A1 (FOXA1), is a pioneer transcription factor essential for mouse development and functions as an oncogene in prostate and breast cancer. In colorectal cancer (CRC), FOXA1 is significantly downregulated and high FOXA1 expression is associated with better prognosis, suggesting potential tumor suppressive functions. We therefore investigated the regulation of FOXA1 expression in CRC, focusing on well-differentiated CRC cells, where FOXA1 is robustly expressed. Genome-wide RNA stability assays identified FOXA1 as an unstable mRNA in CRC cells. We validated FOXA1 mRNA instability in multiple CRC cell lines and in patient-derived CRC organoids, and found that the FOXA1 3'UTR confers instability to the FOXA1 transcript. RNA pulldowns and mass spectrometry identified Staufen1 (STAU1) as a potential regulator of FOXA1 mRNA. Indeed, STAU1 knockdown resulted in increased FOXA1 mRNA and protein expression due to increased FOXA1 mRNA stability. Consistent with these data, RNA-seq following STAU1 knockdown in CRC cells revealed that FOXA1 targets were upregulated upon STAU1 knockdown. Collectively, this study uncovers a molecular mechanism by which FOXA1 is regulated in CRC cells and provides insights into our understanding of the complex mechanisms of gene regulation in cancer.
转录因子通过控制基因表达在发育和疾病中发挥关键作用。叉头框蛋白 A1(FOXA1)是一种在小鼠发育中必不可少的先驱转录因子,也是前列腺癌和乳腺癌的癌基因。在结直肠癌(CRC)中,FOXA1的表达显著下调,高 FOXA1 表达与更好的预后相关,提示其具有潜在的肿瘤抑制功能。因此,我们研究了 CRC 中 FOXA1 表达的调控,重点关注分化良好的 CRC 细胞,这些细胞中 FOXA1 表达丰富。全基因组 RNA 稳定性测定确定 FOXA1 是 CRC 细胞中不稳定的 mRNA。我们在多个 CRC 细胞系和患者来源的 CRC 类器官中验证了 FOXA1 mRNA 的不稳定性,并发现 FOXA1 3'UTR 赋予 FOXA1 转录本不稳定性。RNA 下拉和质谱分析鉴定出 Staufen1(STAU1)是 FOXA1 mRNA 的潜在调节因子。事实上,由于 FOXA1 mRNA 稳定性增加,STAU1 敲低导致 FOXA1 mRNA 和蛋白表达增加。与这些数据一致,在 CRC 细胞中 STAU1 敲低后进行 RNA-seq 显示,FOXA1 靶点在 STAU1 敲低后上调。总之,这项研究揭示了 CRC 细胞中 FOXA1 调控的分子机制,并为我们理解癌症中基因调控的复杂机制提供了新的见解。