Shih Shou-Ping, Lee Man-Gang, El-Shazly Mohamed, Juan Yung-Shun, Wen Zhi-Hong, Du Ying-Chi, Su Jui-Hsin, Sung Ping-Jyun, Chen Yu-Cheng, Yang Juan-Cheng, Wu Yang-Chang, Lu Mei-Chin
Graduate Institute of Marine Biotechnology, National Dong Hwa University, Pingtung 944, Taiwan.
Department of Marine Biotechnology and Resources, National Sun Yat-sen University, Kaohsiung 804, Taiwan.
Mar Drugs. 2015 May 20;13(5):3132-53. doi: 10.3390/md13053132.
A marine polycyclic quinone-type metabolite, halenaquinone (HQ), was found to inhibit the proliferation of Molt 4, K562, MDA-MB-231 and DLD-1 cancer cell lines, with IC50 of 0.48, 0.18, 8.0 and 6.76 μg/mL, respectively. It exhibited the most potent activity against leukemia Molt 4 cells. Accumulating evidence showed that HQ may act as a potent protein kinase inhibitor in cancer therapy. To fully understand the mechanism of HQ, we further explored the precise molecular targets in leukemia Molt 4 cells. We found that the use of HQ increased apoptosis by 26.23%-70.27% and caused disruption of mitochondrial membrane potential (MMP) by 17.15%-53.25% in a dose-dependent manner, as demonstrated by Annexin-V/PI and JC-1 staining assays, respectively. Moreover, our findings indicated that the pretreatment of Molt 4 cells with N-acetyl-l-cysteine (NAC), a reactive oxygen species (ROS) scavenger, diminished MMP disruption and apoptosis induced by HQ, suggesting that ROS overproduction plays a crucial rule in the cytotoxic activity of HQ. The results of a cell-free system assay indicated that HQ could act as an HDAC and topoisomerase catalytic inhibitor through the inhibition of pan-HDAC and topoisomerase IIα expression, respectively. On the protein level, the expression of the anti-apoptotic proteins p-Akt, NFκB, HDAC and Bcl-2, as well as hexokinase II was inhibited by the use of HQ. On the other hand, the expression of the pro-apoptotic protein Bax, PARP cleavage, caspase activation and cytochrome c release were increased after HQ treatment. Taken together, our results suggested that the antileukemic effect of HQ is ROS-mediated mitochondrial apoptosis combined with the inhibitory effect on HDAC and topoisomerase activities.
一种海洋多环醌类代谢产物——卤化醌(HQ),被发现可抑制Molt 4、K562、MDA-MB-231和DLD-1癌细胞系的增殖,其IC50分别为0.48、0.18、8.0和6.76μg/mL。它对白血病Molt 4细胞表现出最强的活性。越来越多的证据表明,HQ在癌症治疗中可能作为一种有效的蛋白激酶抑制剂。为了全面了解HQ的作用机制,我们进一步探究了白血病Molt 4细胞中的精确分子靶点。我们发现,使用HQ可使凋亡增加26.23% - 70.27%,并以剂量依赖的方式使线粒体膜电位(MMP)破坏17.15% - 53.25%,分别通过Annexin-V/PI和JC-1染色试验证实。此外,我们的研究结果表明,用活性氧(ROS)清除剂N-乙酰-L-半胱氨酸(NAC)预处理Molt 4细胞,可减少HQ诱导的MMP破坏和凋亡,这表明ROS的过度产生在HQ的细胞毒性活性中起关键作用。无细胞系统试验结果表明,HQ可分别通过抑制泛HDAC和拓扑异构酶IIα的表达,作为HDAC和拓扑异构酶催化抑制剂。在蛋白水平上,使用HQ可抑制抗凋亡蛋白p-Akt、NFκB、HDAC和Bcl-2以及己糖激酶II的表达。另一方面,HQ处理后促凋亡蛋白Bax的表达、PARP裂解、半胱天冬酶激活和细胞色素c释放增加。综上所述,我们的结果表明,HQ的抗白血病作用是由ROS介导的线粒体凋亡以及对HDAC和拓扑异构酶活性的抑制作用共同导致的。