Guo Xirui, Huang Haishan, Jin Honglei, Xu Jiheng, Risal Sanjiv, Li Jingxia, Li Xin, Yan Huiying, Zeng Xingruo, Xue Lei, Chen Changyan, Huang Chuanshu
Nelson Institute of Environmental Medicine, New York University School of Medicine, Tuxedo, NY 10987, USA; School of Laboratory Medicine and Life Science, Wenzhou Medical University, Wenzhou, Zhejiang 325035, China.
School of Laboratory Medicine and Life Science, Wenzhou Medical University, Wenzhou, Zhejiang 325035, China.
Mol Ther Nucleic Acids. 2018 Sep 7;12:337-349. doi: 10.1016/j.omtn.2018.05.017. Epub 2018 Jul 4.
Our most recent studies demonstrate that miR-137 is downregulated in human bladder cancer (BC) tissues, while treatment of human BC cells with isorhapontigenin (ISO) elevates miR-137 abundance. Since ISO showed a strong inhibition of invasive BC formation in the N-butyl-N-(4-hydroxybutyl) nitrosamine (BBN)-induced invasive BC mouse model, the elucidation of a potential biological effect of miR-137 on antagonizing BC invasion and molecular mechanisms underlying ISO upregulation of miR-137 are very important. Here we discovered that ectopic expression of miR-137 led to specific inhibition of BC invasion in human high-grade BC T24T and UMUC3 cells, while miR-137 deletion promoted the invasion of both cells, indicating the inhibitory effect of miR-137 on human BC invasion. Mechanistic studies revealed that ISO treatment induced miR-137 transcription by promoting c-Jun phosphorylation and, in turn, abolishing matrix metalloproteinase-2 (MMP-2) abundance and invasion in BC cells. Moreover, miR-137 was able to directly bind to the 3' UTR of Glycogen synthase kinase-3β (GSK3β) mRNA and inhibit GSK3β protein translation, consequently leading to a reduction of heat shock protein-70 (HSP70) translation via targeting the mTOR/S6 axis. Collectively, our studies discover an unknown function of miR-137, directly targeting the 3' UTR of GSK3β mRNA and, thereby, inhibiting GSK3β protein translation, mTOR/S6 activation, and HSP70 protein translation and, consequently, attenuating HSP70-mediated MMP-2 expression and invasion in human BC cells. These novel discoveries provide a deep insight into understanding the biomedical significance of miR-137 downregulation in invasive human BCs and the anti-cancer effect of ISO treatment on mouse invasive BC formation.
我们最近的研究表明,miR-137在人膀胱癌(BC)组织中表达下调,而异丹叶大黄素(ISO)处理人BC细胞可提高miR-137丰度。由于ISO在N-丁基-N-(4-羟丁基)亚硝胺(BBN)诱导的侵袭性BC小鼠模型中对侵袭性BC形成具有强烈抑制作用,因此阐明miR-137对拮抗BC侵袭的潜在生物学效应以及ISO上调miR-137的分子机制非常重要。在此,我们发现miR-137的异位表达导致人高级别BC T24T和UMUC3细胞中BC侵袭受到特异性抑制,而miR-137缺失则促进了两种细胞的侵袭,表明miR-137对人BC侵袭具有抑制作用。机制研究表明,ISO处理通过促进c-Jun磷酸化诱导miR-137转录,进而消除BC细胞中基质金属蛋白酶-2(MMP-2)的丰度和侵袭。此外,miR-137能够直接结合糖原合酶激酶-3β(GSK3β)mRNA的3'UTR并抑制GSK3β蛋白翻译,从而通过靶向mTOR/S6轴导致热休克蛋白-70(HSP70)翻译减少。总体而言,我们的研究发现了miR-137的一个未知功能,即直接靶向GSK3β mRNA的3'UTR,从而抑制GSK3β蛋白翻译、mTOR/S6激活和HSP70蛋白翻译,进而减弱HSP70介导的人BC细胞中MMP-2表达和侵袭。这些新发现为深入理解侵袭性人BC中miR-137下调的生物医学意义以及ISO治疗对小鼠侵袭性BC形成的抗癌作用提供了深刻见解。