Harrell Stewart Desmond R, Schmidt M Lee, Donninger Howard, Clark Geoffrey J
Department of Pharmacology & Toxicology, University of Louisville School of Medicine, Louisville, KY 40202, USA.
Department of Medicine, University of Louisville School of Medicine, Louisville, KY 40202, USA.
Cancers (Basel). 2020 Dec 17;12(12):3807. doi: 10.3390/cancers12123807.
Lung cancer is the leading cause of cancer-related death worldwide. Lung cancer is commonly driven by mutations in the RAS oncogenes, the most frequently activated oncogene family in human disease. RAS-induced tumorigenesis is inhibited by the tumor suppressor RASSF1A, which induces apoptosis in response to hyperactivation of RAS. RASSF1A expression is suppressed in cancer at high rates, primarily owing to promoter hypermethylation. Recent reports have shown that loss of RASSF1A expression uncouples RAS from apoptotic signaling in vivo, thereby enhancing tumor aggressiveness. Moreover, a concomitant upregulation of RAS mitogenic signaling upon RASSF1A loss has been observed, suggesting RASSF1A may directly regulate RAS activation. Here, we present the first mechanistic evidence for control of RAS activation by RASSF1A. We present a novel interaction between RASSF1A and the Ras GTPase Activating Protein (RasGAP) DAB2IP, an important negative regulator of RAS. Using shRNA-mediated knockdown and stable overexpression approaches, we demonstrate that RASSF1A upregulates DAB2IP protein levels in NSCLC cells. Suppression of RASSF1A and subsequent downregulation of DAB2IP enhances GTP loading onto RAS, thus increasing RAS mitogenic signaling in both mutant- and wildtype-RAS cells. Moreover, co-suppression of RASSF1A and DAB2IP significantly enhances in vitro and in vivo growth of wildtype-RAS cells. Tumors expressing wildtype RAS, therefore, may still suffer from hyperactive RAS signaling when RASSF1A is downregulated. This may render them susceptible to the targeted RAS inhibitors currently in development.
肺癌是全球癌症相关死亡的主要原因。肺癌通常由RAS癌基因的突变驱动,RAS癌基因是人类疾病中最常被激活的癌基因家族。肿瘤抑制因子RASSF1A可抑制RAS诱导的肿瘤发生,RASSF1A可响应RAS的过度激活而诱导细胞凋亡。RASSF1A的表达在癌症中被高频率抑制,主要是由于启动子高甲基化。最近的报告表明,RASSF1A表达缺失使RAS在体内与凋亡信号解偶联,从而增强肿瘤侵袭性。此外,还观察到RASSF1A缺失时RAS促有丝分裂信号的伴随上调,提示RASSF1A可能直接调节RAS激活。在此,我们提供了RASSF1A控制RAS激活的首个机制证据。我们展示了RASSF1A与Ras GTP酶激活蛋白(RasGAP)DAB2IP之间的一种新相互作用,DAB2IP是RAS的一个重要负调节因子。使用shRNA介导的敲低和稳定过表达方法,我们证明RASSF1A上调非小细胞肺癌细胞中DAB2IP的蛋白水平。抑制RASSF1A并随后下调DAB2IP可增强RAS上的GTP负载,从而增加突变型和野生型RAS细胞中的RAS促有丝分裂信号。此外,共同抑制RASSF1A和DAB2IP可显著增强野生型RAS细胞的体外和体内生长。因此,当RASSF1A下调时,表达野生型RAS的肿瘤仍可能遭受RAS信号过度激活。这可能使它们易受目前正在研发的靶向RAS抑制剂的影响。