Department of Biology and Environment, School of Life Sciences and Environment, University of Trás-os-Montes e Alto Douro (UTAD), Quinta de Prados, 5001-801 Vila Real, Portugal.
Center for Research and Technology of Agro-Environmental and Biological Sciences (CITAB-UTAD), Quinta de Prados, 5001-801 Vila Real, Portugal.
Int J Mol Sci. 2022 Jul 23;23(15):8107. doi: 10.3390/ijms23158107.
In this work, three pesticides of different physicochemical properties: glyphosate (GLY, herbicide), imidacloprid (IMD, insecticide), and imazalil (IMZ, fungicide), were selected to assess their cytotoxicity against Caco-2 and HepG2 cells. Cell viability was assessed by the Alamar Blue assay, after 24 and 48 h exposure to different concentrations, and IC50 values were calculated. The mechanisms underlying toxicity, namely cellular reactive oxygen species (ROS), glutathione (GSH) content, lipid peroxidation, loss of mitochondrial membrane potential (MMP), and apoptosis/necrosis induction were assessed by flow cytometry. Cytotoxic profiles were further correlated with the molecular physicochemical parameters of pesticides, namely: water solubility, partition coefficient in an n-octanol/water (Log Pow) system, topological polar surface area (TPSA), the number of hydrogen-bonds (donor/acceptor), and rotatable bonds. In vitro outputs resulted in the following toxicity level: IMZ (Caco-2: IC50 = 253.5 ± 3.37 μM, and HepG2: IC50 = 94 ± 12 μM) > IMD (Caco-2: IC50 > 1 mM and HepG2: IC50 = 624 ± 24 μM) > GLY (IC50 >>1 mM, both cell lines), after 24 h treatment, being toxicity time-dependent (lower IC50 values at 48 h). Toxicity is explained by oxidative stress, as IMZ induced a higher intracellular ROS increase and lipid peroxidation, followed by IMD, while GLY did not change these markers. However, the three pesticides induced loss of MMP in HepG2 cells while in Caco-2 cells only IMZ produced significant MMP loss. Increased ROS and loss of MMP promoted apoptosis in Caco-2 cells subjected to IMZ, and in HepG2 cells exposed to IMD and IMZ, as assessed by Annexin-V/PI. The toxicity profile of pesticides is directly correlated with their Log Pow, as affinity for the lipophilic environment favours interaction with cell membranes governs, and is inversely correlated with their TPSA; however, membrane permeation is favoured by lower TPSA. IMZ presents the best molecular properties for membrane interaction and cell permeation, i.e., higher Log Pow, lower TPSA and lower hydrogen-bond (H-bond) donor/acceptor correlating with its higher toxicity. In conclusion, molecular physicochemical factors such as Log Pow, TPSA, and H-bond are likely to be directly correlated with pesticide-induced toxicity, thus they are key factors to potentially predict the toxicity of other compounds.
在这项工作中,选择了三种具有不同物理化学性质的农药:草甘膦(GLY,除草剂)、吡虫啉(IMD,杀虫剂)和抑霉唑(IMZ,杀菌剂),以评估它们对 Caco-2 和 HepG2 细胞的细胞毒性。通过 Alamar Blue 测定法评估细胞活力,在不同浓度下暴露 24 和 48 小时后,计算 IC50 值。通过流式细胞术评估毒性的潜在机制,即细胞内活性氧(ROS)、谷胱甘肽(GSH)含量、脂质过氧化、线粒体膜电位(MMP)丧失和凋亡/坏死诱导。细胞毒性谱进一步与农药的分子物理化学参数相关联,即:水溶解度、在正辛醇/水(Log Pow)系统中的分配系数、拓扑极性表面积(TPSA)、氢键(供体/受体)的数量和可旋转键。体外结果得出以下毒性水平:IMZ(Caco-2:IC50 = 253.5 ± 3.37 μM,HepG2:IC50 = 94 ± 12 μM)> IMD(Caco-2:IC50 > 1 mM 和 HepG2:IC50 = 624 ± 24 μM)> GLY(IC50 >>1 mM,两种细胞系),24 小时处理后,毒性具有时间依赖性(48 小时时 IC50 值较低)。毒性可通过氧化应激来解释,因为 IMZ 诱导细胞内 ROS 增加和脂质过氧化作用更高,其次是 IMD,而 GLY 则不会改变这些标志物。然而,三种农药均导致 HepG2 细胞的 MMP 丧失,而 Caco-2 细胞中仅 IMZ 产生显著的 MMP 丧失。在 Caco-2 细胞中,ROS 的增加和 MMP 的丧失促进了 IMZ 处理的细胞凋亡,在 HepG2 细胞中,IMD 和 IMZ 暴露导致细胞凋亡,如 Annexin-V/PI 评估所示。农药的毒性谱与其 Log Pow 直接相关,因为亲脂环境的亲和力有利于与细胞膜相互作用,并且与它们的 TPSA 呈负相关;然而,较低的 TPSA 有利于膜渗透。IMZ 具有与膜相互作用和细胞渗透相关的最佳分子特性,即较高的 Log Pow、较低的 TPSA 和较低的氢键(H-bond)供体/受体,与其较高的毒性相关。总之,Log Pow、TPSA 和 H-bond 等分子物理化学因素可能与农药诱导的毒性直接相关,因此它们是预测其他化合物毒性的关键因素。