Zhang Qian-Qian, Miao Ying-Shuang, Hu Jun-Yi, Liu Rui-Xuan, Hu Yue-Xiao, Wang Feng
State Key Laboratory of Bioactive Molecules and Druggability Assessment, Institute of Genomic Medicine, International Cooperative Laboratory of Traditional Chinese Medicine Modernization and Innovative Drug Development of Chinese Ministry of Education (MOE), College of Pharmacy, Jinan University, Guangzhou, 510632, China.
International School, Jinan University, Guangzhou, 510632, China.
Mol Cell Biochem. 2025 Apr;480(4):2247-2263. doi: 10.1007/s11010-024-05012-1. Epub 2024 May 15.
Axis inhibitor protein 1 (AXIN1) is a protein recognized for inhibiting tumor growth and is commonly involved in cancer development. In this study, we explored the potential molecular mechanisms that connect alternative splicing of AXIN1 to the metastasis of hepatocellular carcinoma (HCC). Transcriptome sequencing, RT‒PCR, qPCR and Western blotting were utilized to determine the expression levels of AXIN1 in human HCC tissues and HCC cells. The effects of the AXIN1 exon 9 alternative splice isoform and SRSF9 on the migration and invasion of HCC cells were assessed through wound healing and Transwell assays, respectively. The interaction between SRSF9 and AXIN1 was investigated using UV crosslink RNA immunoprecipitation, RNA pulldown, and RNA immunoprecipitation assays. Furthermore, the involvement of the AXIN1 isoform and SRSF9 in HCC metastasis was validated in a nude mouse model. AXIN1-L (exon 9 including) expression was downregulated, while AXIN1-S (exon 9 skipping) was upregulated in HCC. SRSF9 promotes the production of AXIN1-S by interacting with the sequence of exons 8 and 10 of AXIN1. AXIN1-S significantly promoted HCC cells migration and invasion by activating the Wnt pathway, while the opposite effects were observed for AXIN1-L. In vivo experiments demonstrated that AXIN1-L inhibited HCC metastasis, whereas SRSF9 promoted HCC metastasis in part by regulating the level of AXIN1-S. AXIN1, a tumor suppressor protein that targets the AXIN1/Wnt/β-catenin signaling axis, may be a promising prognostic factor and a valuable therapeutic target for HCC.
轴抑制蛋白1(AXIN1)是一种因抑制肿瘤生长而被认可的蛋白质,通常参与癌症发展。在本研究中,我们探索了将AXIN1的可变剪接与肝细胞癌(HCC)转移联系起来的潜在分子机制。利用转录组测序、逆转录-聚合酶链反应(RT-PCR)、定量聚合酶链反应(qPCR)和蛋白质免疫印迹法来确定AXIN1在人HCC组织和HCC细胞中的表达水平。分别通过伤口愈合实验和Transwell实验评估AXIN1外显子9可变剪接异构体和丝氨酸/精氨酸丰富剪接因子9(SRSF9)对HCC细胞迁移和侵袭的影响。使用紫外线交联RNA免疫沉淀、RNA下拉和RNA免疫沉淀实验研究SRSF9与AXIN1之间的相互作用。此外,在裸鼠模型中验证了AXIN1异构体和SRSF9在HCC转移中的作用。在HCC中,AXIN1-L(包括外显子9)的表达下调,而AXIN1-S(外显子9缺失)的表达上调。SRSF9通过与AXIN1的外显子8和10序列相互作用促进AXIN1-S的产生。AXIN1-S通过激活Wnt通路显著促进HCC细胞的迁移和侵袭,而AXIN1-L则产生相反的作用。体内实验表明,AXIN1-L抑制HCC转移,而SRSF9部分通过调节AXIN1-S的水平促进HCC转移。AXIN1是一种靶向AXIN1/ Wnt/β-连环蛋白信号轴的肿瘤抑制蛋白,可能是HCC一个有前景的预后因素和有价值的治疗靶点。