Li Ziyao, Xin Shiyong, Huang Liqun, Tian Ye, Chen Weihua, Liu Xiang, Ye Bowen, Bai Rong, Yang Guosheng, Wang Wenwen, Ye Lin
Department of Urology, Shanghai East Hospital, School of Medicine, Tongji University, Shanghai, China.
School of Electrical Engineering of Zhengzhou University, Zhengzhou, China.
Oncogene. 2025 Mar;44(10):665-678. doi: 10.1038/s41388-024-03235-6. Epub 2024 Dec 5.
Clear cell renal cell carcinoma (ccRCC) is one of the most common malignancies. Recently, the role of brain-expressed X-linked 4 (BEX4) in cancer progression has received increasing attention. This study aimed to investigate the function of BEX4 in ccRCC and to reveal the underlying mechanisms. We first confirmed that BEX4 was significantly downregulated in ccRCC by bioinformatics analysis and that patients with low BEX4 expression tended to have prolonged overall survival time. Subsequently, we confirmed that BEX4 inhibited ccRCC cell proliferation in vitro and tumorigenesis in vivo through a series of cell function assays and the establishment of a nude mouse xenograft model, respectively. Mechanistically, we found that BEX4 positively regulates the expression of Src homology 2 domain-containing 4A (SH2D4A), an inhibitor of the NOTCH pathway, which further promoted the tumor-suppressive effects of BEX4. In addition, our study confirmed that the promoting effect of BEX4 on SH2D4A was achieved by inhibiting the deacetylase sirtuin 2 (SIRT2) activity. On this basis, we found that there was a competition between acetylation and ubiquitination modifications at the K69 site of SH2DA4 and that BEX4-induced upregulation of acetylation at the k69 site stabilizes SH2D4A protein expression by inhibiting ubiquitination at the same site. In addition, dual-luciferase assays showed that the transcriptional activity of BEX4 was positively regulated by activation transcription factor 3 (ATF3). Our study suggests that BEX4 plays a role in inhibiting tumor progression in ccRCC and maybe a new diagnostic and therapeutic target for ccRCC patients.
透明细胞肾细胞癌(ccRCC)是最常见的恶性肿瘤之一。近年来,脑表达X连锁4(BEX4)在癌症进展中的作用受到越来越多的关注。本研究旨在探讨BEX4在ccRCC中的功能,并揭示其潜在机制。我们首先通过生物信息学分析证实BEX4在ccRCC中显著下调,且BEX4表达低的患者总生存时间往往延长。随后,我们分别通过一系列细胞功能试验和建立裸鼠异种移植模型,证实BEX4在体外抑制ccRCC细胞增殖,在体内抑制肿瘤发生。机制上,我们发现BEX4正向调节含Src同源2结构域蛋白4A(SH2D4A)的表达,SH2D4A是NOTCH通路的抑制剂,这进一步促进了BEX4的肿瘤抑制作用。此外,我们的研究证实BEX4对SH2D4A的促进作用是通过抑制去乙酰化酶沉默调节蛋白2(SIRT2)的活性实现的。在此基础上,我们发现SH2DA4的K69位点存在乙酰化和泛素化修饰之间的竞争,BEX4诱导的K69位点乙酰化上调通过抑制同一位点的泛素化来稳定SH2D4A蛋白表达。此外,双荧光素酶报告基因检测表明BEX4的转录活性受到激活转录因子3(ATF3)的正向调节。我们的研究表明,BEX4在抑制ccRCC肿瘤进展中发挥作用,可能是ccRCC患者新的诊断和治疗靶点。