Shu Yi-Jun, Bao Run-Fa, Jiang Lin, Wang Zheng, Wang Xu-An, Zhang Fei, Liang Han-Bin, Li Huai-Feng, Ye Yuan-Yuan, Xiang Shan-Shan, Weng Hao, Wu Xiang-Song, Li Mao-Lan, Hu Yun-Ping, Lu Wei, Zhang Yi-Jian, Zhu Jian, Dong Ping, Liu Ying-Bin
Department of General Surgery and Laboratory of General Surgery, Xinhua Hospital, Affiliated with Shanghai Jiao Tong University School of Medicine, No. 1665 Kongjiang Road, Shanghai 200092, China.
Institute of Biliary Tract Disease, Shanghai Jiao Tong University School of Medicine, No. 1665 Kongjiang Road, Shanghai 200092, China.
Cell Death Differ. 2017 Mar;24(3):445-457. doi: 10.1038/cdd.2016.146. Epub 2017 Jan 6.
Gallbladder cancer (GBC) is a leading cause of cancer-related deaths worldwide, and its prognosis remains poor, with a 5-year survival rate of ~5%. Given the crucial role of microRNAs (miRNAs) in cancer metastasis, we aimed to analyze the expression and function of the metastasis-associated miRNA miR-29c-5p in GBC.We validated that expression of miR-29c-5p was significantly downregulated in GBC and was closely associated with lymph node metastasis, overall survival and disease-free survival in 40 GBC patients who were followed clinically. Ectopic overexpression of miR-29c-5p dramatically repressed proliferation, metastasis, and colony formation and induced apoptosis in vitro, and it suppressed tumorigenicity in vivo through the MAPK pathway. Cytoplasmic polyadenylation element binding protein 4 (CPEB4) was identified as a critical effector target of miR-29c-5p. Enforced expression of miR-29c-5p significantly inhibited the expression of CPEB4, and restoration of CPEB4 expression reversed the inhibitory effects of miR-29c-5p on GBC cell proliferation and metastasis. Transforming growth factor-β (TGF-β) upregulated CPEB4 by downregulating miR-29c-5p, leading to MAPK pathway activation. In conclusion, the TGF-β/miR-29c-5p/CPEB4 axis has a pivotal role in the pathogenesis and poor prognosis of GBC, suggesting that miR-29c-5p is a tumor-suppressive miRNA that may serve as potential prognostic biomarker or therapeutic target for GBC.
胆囊癌(GBC)是全球癌症相关死亡的主要原因之一,其预后仍然很差,5年生存率约为5%。鉴于微小RNA(miRNA)在癌症转移中起关键作用,我们旨在分析与转移相关的miRNA miR-29c-5p在胆囊癌中的表达和功能。我们验证了miR-29c-5p在胆囊癌中的表达显著下调,并且与40例接受临床随访的胆囊癌患者的淋巴结转移、总生存期和无病生存期密切相关。miR-29c-5p的异位过表达在体外显著抑制增殖、转移和集落形成,并诱导细胞凋亡,在体内通过丝裂原活化蛋白激酶(MAPK)途径抑制肿瘤发生。细胞质聚腺苷酸化元件结合蛋白4(CPEB4)被确定为miR-29c-5p的关键效应靶点。miR-29c-5p的强制表达显著抑制CPEB4的表达,CPEB4表达的恢复逆转了miR-29c-5p对胆囊癌细胞增殖和转移的抑制作用。转化生长因子-β(TGF-β)通过下调miR-29c-5p上调CPEB4,导致MAPK途径激活。总之,TGF-β/miR-29c-5p/CPEB4轴在胆囊癌的发病机制和不良预后中起关键作用,表明miR-29c-5p是一种肿瘤抑制性miRNA,可能作为胆囊癌潜在的预后生物标志物或治疗靶点。