Division of Molecular Medicine, Ruđer Bošković Institute, Bijenička cesta 54, 10000, Zagreb, Croatia.
ELKH Research Centre for Natural Sciences, Magyar Tudósok krt. 2, 1117, Budapest, Hungary.
Histochem Cell Biol. 2022 Sep;158(3):261-277. doi: 10.1007/s00418-022-02106-z. Epub 2022 Jun 1.
Overexpression of ABC transporters, such as ABCB1 and ABCG2, plays an important role in mediating multidrug resistance (MDR) in cancer. This feature is also attributed to a subpopulation of cancer stem cells (CSCs), having enhanced tumourigenic potential. ABCG2 is specifically associated with the CSC phenotype, making it a valuable target for eliminating aggressive and resistant cells. Several natural and synthetic ionophores have been discovered as CSC-selective drugs that may also have MDR-reversing ability, whereas their interaction with ABCG2 has not yet been explored. We previously reported the biological activities, including ABCB1 inhibition, of a group of adamantane-substituted diaza-18-crown-6 (DAC) compounds that possess ionophore capabilities. In this study, we investigated the mechanism of ABCG2-inhibitory activity of DAC compounds and the natural ionophores salinomycin, monensin and nigericin. We used a series of functional assays, including real-time microscopic analysis of ABCG2-mediated fluorescent substrate transport in cells, and docking studies to provide comparative aspects for the transporter-compound interactions and their role in restoring chemosensitivity. We found that natural ionophores did not inhibit ABCG2, suggesting that their CSC selectivity is likely mediated by other mechanisms. In contrast, DACs with amide linkage in the side arms demonstrated noteworthy ABCG2-inhibitory activity, with DAC-3Amide proving to be the most potent. This compound induced conformational changes of the transporter and likely binds to both Cavity 1 and the NBD-TMD interface. DAC-3Amide reversed ABCG2-mediated MDR in model cells, without affecting ABCG2 expression or localization. These results pave the way for the development of new crown ether compounds with improved ABCG2-inhibitory properties.
ABCB1 和 ABCG2 等 ABC 转运蛋白的过表达在介导癌症的多药耐药(MDR)中起着重要作用。这一特征也归因于具有增强肿瘤形成潜力的癌症干细胞(CSC)的亚群。ABCG2 与 CSC 表型特别相关,使其成为消除侵袭性和耐药细胞的有价值的靶标。已经发现几种天然和合成的离子载体作为 CSC 选择性药物,它们可能具有逆转 MDR 的能力,而它们与 ABCG2 的相互作用尚未得到探索。我们之前报道了一组具有离子载体能力的金刚烷取代的二氮杂-18-冠-6(DAC)化合物的生物学活性,包括对 ABCB1 的抑制作用。在这项研究中,我们研究了 DAC 化合物和天然离子载体萨利霉素、莫能菌素和 Nigericin 抑制 ABCG2 活性的机制。我们使用了一系列功能测定,包括实时显微镜分析细胞中 ABCG2 介导的荧光底物转运,以及对接研究,为转运蛋白-化合物相互作用及其在恢复化疗敏感性中的作用提供了比较方面。我们发现天然离子载体不抑制 ABCG2,这表明它们的 CSC 选择性可能由其他机制介导。相比之下,具有酰胺键的侧臂的 DAC 表现出显著的 ABCG2 抑制活性,其中 DAC-3Amide 被证明是最有效的。该化合物诱导转运蛋白构象变化,可能与 Cavity 1 和 NBD-TMD 界面都结合。DAC-3Amide 在模型细胞中逆转了 ABCG2 介导的 MDR,而不影响 ABCG2 的表达或定位。这些结果为开发具有改善的 ABCG2 抑制特性的新型冠醚化合物铺平了道路。