Chang Shun-Fu, Chang Cheng Allen, Lee Ding-Yu, Lee Pei-Ling, Yeh Yu-Ming, Yeh Chiuan-Ren, Cheng Cheng-Kung, Chien Shu, Chiu Jeng-Jiann
Department of Biological Science and Technology, National Chiao Tung University, Hsinchu 300, Taiwan.
Proc Natl Acad Sci U S A. 2008 Mar 11;105(10):3927-32. doi: 10.1073/pnas.0712353105. Epub 2008 Feb 29.
Interstitial flow in and around tumor tissue affects the mechanical microenvironment to modulate tumor cell growth and metastasis. We investigated the roles of flow-induced shear stress in modulating cell cycle distribution in four tumor cell lines and the underlying mechanisms. In all four cell lines, incubation under static conditions for 24 or 48 h led to G(0)/G(1) arrest; in contrast, shear stress (12 dynes/cm(2)) induced G(2)/M arrest. The molecular basis of the shear effect was analyzed, and the presentation on molecular mechanism is focused on human MG63 osteosarcoma cells. Shear stress induced increased expressions of cyclin B1 and p21(CIP1) and decreased expressions of cyclins A, D1, and E, cyclin-dependent protein kinases (Cdk)-1, -2, -4, and -6, and p27(KIP1) as well as a decrease in Cdk1 activity. Using specific antibodies and small interfering RNA, we found that the shear-induced G(2)/M arrest and corresponding changes in G(2)/M regulatory protein expression and activity were mediated by alpha(v)beta(3) and beta(1) integrins through bone morphogenetic protein receptor type IA-specific Smad1 and Smad5. Shear stress also down-regulated runt-related transcription factor 2 (Runx2) binding activity and osteocalcin and alkaline phosphatase expressions in MG63 cells; these responses were mediated by alpha(v)beta(3) and beta(1) integrins through Smad5. Our findings provide insights into the mechanism by which shear stress induces G(2)/M arrest in tumor cells and inhibits cell differentiation and demonstrate the importance of mechanical microenvironment in modulating molecular signaling, gene expression, cell cycle, and functions in tumor cells.
肿瘤组织内部及其周围的间质流会影响机械微环境,从而调节肿瘤细胞的生长和转移。我们研究了流动诱导的剪切应力在调节四种肿瘤细胞系细胞周期分布中的作用及其潜在机制。在所有这四种细胞系中,静态条件下培养24或48小时会导致G(0)/G(1)期阻滞;相反,剪切应力(12达因/平方厘米)会诱导G(2)/M期阻滞。分析了剪切效应的分子基础,并以人MG63骨肉瘤细胞为重点阐述分子机制。剪切应力诱导细胞周期蛋白B1和p21(CIP1)表达增加,而细胞周期蛋白A、D1和E、细胞周期蛋白依赖性蛋白激酶(Cdk)-1、-2、-4和-6以及p27(KIP1)表达减少,同时Cdk1活性降低。使用特异性抗体和小干扰RNA,我们发现剪切诱导的G(2)/M期阻滞以及G(2)/M调节蛋白表达和活性的相应变化是由α(v)β(3)和β(1)整合素通过骨形态发生蛋白受体IA型特异性Smadl和Smad5介导的。剪切应力还下调了MG63细胞中与矮小相关转录因子2(Runx2)的结合活性以及骨钙素和碱性磷酸酶的表达;这些反应是由α(v)β(3)和β(1)整合素通过Smad5介导的。我们的研究结果为剪切应力诱导肿瘤细胞G(2)/M期阻滞并抑制细胞分化的机制提供了见解,并证明了机械微环境在调节肿瘤细胞分子信号传导、基因表达、细胞周期和功能方面的重要性。