Department of Toxicology and Cancer Biology, University of Kentucky, Lexington, KY.
Toxicol Sci. 2019 May 1;169(1):224-234. doi: 10.1093/toxsci/kfz032.
Chronic exposure of human bronchial epithelial BEAS-2B cells to hexavalent chromium [Cr(VI)] causes malignant cell transformation. Sirtuin-3 (SIRT3) regulates mitochondrial adaptive response to stress, such as metabolic reprogramming and antioxidant defense mechanisms. In Cr(VI)-transformed cells, SIRT3 was upregulated and mitochondrial adenosine triphosphate (ATP) production and proton leak were reduced. Knockdown of SIRT3 by its shRNA further decreased mitochondrial ATP production, proton leak, mitochondrial mass, and mitochondrial membrane potential, indicating that SIRT3 positively regulates mitochondrial oxidative phosphorylation and maintenance of mitochondrial integrity. Mitophagy is critical to maintain proper cellular functions. In Cr(VI)-transformed cells expressions of Pink 1 and Parkin, two mitophagy proteins, were elevated, and mitophagy remained similar as that in passage-matched normal BEAS-2B cells, indicating that in -Cr(VI)-transformed cells mitophagy is suppressed. Knockdown of SIRT3 induced mitophagy, suggesting that SIRT3 plays an important role in mitophagy suppression of Cr(VI)-transformed cells. In Cr(VI)-transformed cells, nuclear factor (erythroid-derived 2)-like 2 (Nrf2) was constitutively activated, and protein levels of p62 and p-p62Ser349 were elevated. Knockdown of SIRT3 or treatment with carbonyl cyanide m-chlorophenyl hydrazone (CCCP) decreased the binding of p-p62Ser349 to Keap1, resulting in increased binding of Keap1 to Nrf2 and consequently reduced Nrf2 activation. The results from CHIP assay showed that in Cr(VI)-transformed cells binding of Nrf2 to antioxidant response element (ARE) of SIRT3 gene promoter was dramatically increased. Knockdown of SIRT3 suppressed cell proliferation and tumorigenesis of Cr(VI)-transformed cells. Overexpression of SIRT3 in normal BEAS-2B cells exhibited mitophagy suppression phenotype and increased cell proliferation and tumorigenesis. The present study demonstrated that upregulation of SIRT3 causes mitophagy suppression and plays an important role in cell survival and tumorigenesis of Cr(VI)-transformed cells.
六价铬[Cr(VI)]慢性暴露于人体支气管上皮 BEAS-2B 细胞可导致恶性细胞转化。沉默信息调节因子 3(SIRT3)调节线粒体对压力的适应性反应,如代谢重编程和抗氧化防御机制。在 Cr(VI)转化的细胞中,SIRT3 上调,三磷酸腺苷(ATP)的产生和质子泄漏减少。SIRT3 的 shRNA 敲低进一步降低了线粒体 ATP 的产生、质子泄漏、线粒体质量和线粒体膜电位,表明 SIRT3 正向调节线粒体氧化磷酸化和维持线粒体完整性。自噬对于维持适当的细胞功能至关重要。在 Cr(VI)转化的细胞中,两种自噬蛋白 Pink1 和 Parkin 的表达升高,与传代匹配的正常 BEAS-2B 细胞中的自噬相似,表明在 Cr(VI)转化的细胞中自噬受到抑制。SIRT3 的敲低诱导了自噬,表明 SIRT3 在 Cr(VI)转化的细胞中自噬抑制中起重要作用。在 Cr(VI)转化的细胞中,核因子(红系衍生 2)样 2(Nrf2)持续激活,p62 和 p-p62Ser349 的蛋白水平升高。SIRT3 的敲低或羰基氰化物 m-氯苯腙(CCCP)处理降低了 p-p62Ser349 与 Keap1 的结合,导致 Keap1 与 Nrf2 的结合增加,从而减少了 Nrf2 的激活。CHIP 检测结果表明,在 Cr(VI)转化的细胞中,Nrf2 与 SIRT3 基因启动子的抗氧化反应元件(ARE)的结合显著增加。SIRT3 的敲低抑制了 Cr(VI)转化的细胞的增殖和肿瘤发生。在正常 BEAS-2B 细胞中过表达 SIRT3 表现出自噬抑制表型,并增加了细胞增殖和肿瘤发生。本研究表明,SIRT3 的上调导致自噬抑制,并在 Cr(VI)转化的细胞的细胞存活和肿瘤发生中起重要作用。