Department of Clinical Research, University of Bern, and Department of Medical Oncology, Inselspital, Bern University Hospital, Bern, Switzerland.
Oncogene. 2012 Sep 20;31(38):4221-32. doi: 10.1038/onc.2011.578. Epub 2012 Jan 16.
The c-Src kinase regulates cancer cell invasion through inhibitor of DNA binding/differentiation 1 (ID1). Src and ID1 are frequently overexpressed in human lung adenocarcinoma. The current study aimed at identifying microRNAs (miRNAs) involved in the Src-ID1 signaling in lung cancer. Incubation of lung cancer cells with the Src inhibitor saracatinib led to the upregulation of several miRNAs including miR-29b, which was the most highly upregulated miRNA with predicted binding to the ID1 3'-untranslated region (UTR). Luciferase reporter assays confirmed direct binding of miR-29b to the ID1 3'-UTR. Expression of miR-29b suppressed ID1 levels and significantly reduced migration and invasion. Expression of antisense-miR-29b (anti-miR-29b), on the other hand, enhanced ID1 mRNA and protein levels, and significantly increased lung cancer cell migration and invasion, a hallmark of the Src-ID1 pathway. The ectopic expression of ID1 in miR-29b-overexpressing cells was able to rescue the migratory potential of these cells. Both, anti-miR-29b and ID1 overexpression diminished the effects of the Src inhibitors saracatinib and dasatinib on migration and invasion. Saracatinib and dasatinib decreased c-Myc transcriptional repression on miR-29b and led to increased ID1 protein levels, whereas forced expression of c-Myc repressed miR-29b and induced ID1. In agreement, we showed direct recruitment of c-Myc to the miR-29b promoter. miR-29b was significantly downregulated in primary lung adenocarcinoma samples compared with matched alveolar lung tissue, and miR-29b expression was a significant prognostic factor for patient outcome. These results suggest that miR-29b is involved in the Src-ID1 signaling pathway, is dysregulated in lung adenocarcinoma and is a potential predictive marker for Src kinase inhibitors.
c-Src 激酶通过 DNA 结合/分化抑制因子 1(ID1)调节癌细胞侵袭。Src 和 ID1 在人肺腺癌中经常过表达。本研究旨在鉴定参与肺癌中 Src-ID1 信号的 microRNAs(miRNAs)。用 Src 抑制剂 saracatinib 孵育肺癌细胞导致包括 miR-29b 在内的几种 miRNAs 的上调,miR-29b 是上调最显著的 miRNA,预测与 ID1 的 3'-非翻译区(UTR)结合。荧光素酶报告基因测定证实 miR-29b 直接与 ID1 的 3'-UTR 结合。miR-29b 的表达抑制 ID1 水平,并显著降低迁移和侵袭。另一方面,表达反义-miR-29b(anti-miR-29b)可增强 ID1 mRNA 和蛋白水平,并显著增加肺癌细胞的迁移和侵袭,这是 Src-ID1 通路的标志。在 miR-29b 过表达细胞中外源表达 ID1 能够挽救这些细胞的迁移潜能。anti-miR-29b 和 ID1 的过表达均减弱了 Src 抑制剂 saracatinib 和 dasatinib 对迁移和侵袭的影响。Saracatinib 和 dasatinib 降低了 c-Myc 对 miR-29b 的转录抑制作用,导致 ID1 蛋白水平增加,而强制表达 c-Myc 抑制 miR-29b 并诱导 ID1。我们还表明 c-Myc 直接募集到 miR-29b 启动子。与匹配的肺泡肺组织相比,miR-29b 在原发性肺腺癌样本中明显下调,miR-29b 的表达是患者预后的一个重要预测因子。这些结果表明,miR-29b 参与 Src-ID1 信号通路,在肺腺癌中失调,是 Src 激酶抑制剂的潜在预测标志物。