Zhang Zhifeng, Zheng Fufu, Yu Zhenlong, Hao Jiajiao, Chen Miao, Yu Wendan, Guo Wei, Chen Yiming, Huang Wenlin, Duan Zhijun, Deng Wuguo
The First Affiliated Hospital & Institute of Cancer Stem Cell, Dalian Medical University, Dalian, China.
The First Affiliated Hospital, Sun Yat-sen University, Guangzhou, China.
PLoS One. 2017 Oct 19;12(10):e0186900. doi: 10.1371/journal.pone.0186900. eCollection 2017.
Cyclooxygenase (COX) is the rate-limiting enzyme in prostaglandins (PGs) biosynthesis. Previous studies indicate that COX-2, one of the isoforms of COX, is highly expressed in colon cancers and plays a key role in colon cancer carcinogenesis. Thus, searching for novel transcription factors regulating COX-2 expression will facilitate drug development for colon cancer. In this study, we identified XRCC5 as a binding protein of the COX-2 gene promoter in colon cancer cells with streptavidin-agarose pulldown assay and mass spectrometry analysis, and found that XRCC5 promoted colon cancer growth through modulation of COX-2 signaling. Knockdown of XRCC5 by siRNAs inhibited the growth of colon cancer cells in vitro and of tumor xenografts in a mouse model in vivo by suppressing COX-2 promoter activity and COX-2 protein expression. Conversely, overexpression of XRCC5 promoted the growth of colon cancer cells by activating COX-2 promoter and increasing COX-2 protein expression. Moreover, the role of p300 (a transcription co-activator) in acetylating XRCC5 to co-regulate COX-2 expression was also evaluated. Immunofluorescence assay and confocal microscopy showed that XRCC5 and p300 proteins were co-located in the nucleus of colon cancer cells. Co-immunoprecipitation assay also proved the interaction between XRCC5 and p300 in nuclear proteins of colon cancer cells. Cell viability assay indicated that the overexpression of wild-type p300, but not its histone acetyltransferase (HAT) domain deletion mutant, increased XRCC5 acetylation, thereby up-regulated COX-2 expression and promoted the growth of colon cancer cells. In contrast, suppression of p300 by a p300 HAT-specific inhibitor (C646) inhibited colon cancer cell growth by suppressing COX-2 expression. Taken together, our results demonstrated that XRCC5 promoted colon cancer growth by cooperating with p300 to regulate COX-2 expression, and suggested that the XRCC5/p300/COX-2 signaling pathway was a potential target in the treatment of colon cancers.
环氧化酶(COX)是前列腺素(PGs)生物合成中的限速酶。先前的研究表明,COX的亚型之一COX-2在结肠癌中高表达,并在结肠癌致癌过程中起关键作用。因此,寻找调节COX-2表达的新型转录因子将有助于结肠癌药物的开发。在本研究中,我们通过链霉亲和素-琼脂糖下拉实验和质谱分析,确定XRCC5为结肠癌细胞中COX-2基因启动子的结合蛋白,并发现XRCC5通过调节COX-2信号促进结肠癌生长。用小干扰RNA(siRNAs)敲低XRCC5可抑制体外结肠癌细胞的生长以及体内小鼠模型中肿瘤异种移植瘤的生长,其机制是通过抑制COX-2启动子活性和COX-2蛋白表达。相反,XRCC5的过表达通过激活COX-2启动子并增加COX-2蛋白表达来促进结肠癌细胞的生长。此外,还评估了p300(一种转录共激活因子)在乙酰化XRCC5以共同调节COX-2表达中的作用。免疫荧光分析和共聚焦显微镜显示,XRCC5和p300蛋白共定位于结肠癌细胞的细胞核中。免疫共沉淀实验也证明了XRCC5与p300在结肠癌细胞核蛋白中的相互作用。细胞活力实验表明,野生型p300的过表达而非其组蛋白乙酰转移酶(HAT)结构域缺失突变体的过表达,增加了XRCC5的乙酰化,从而上调了COX-2表达并促进了结肠癌细胞的生长。相反,用p300 HAT特异性抑制剂(C646)抑制p300可通过抑制COX-2表达来抑制结肠癌细胞的生长。综上所述,我们的结果表明XRCC5通过与p300协同调节COX-2表达来促进结肠癌生长,并提示XRCC5/p300/COX-2信号通路是结肠癌治疗的潜在靶点。