Biales Adam D, Bencic David C, Flick Robert W, Delacruz Armah, Gordon Denise A, Huang Weichun
U.S. Environmental Protection Agency, Office of Research and Development, Cincinnati, OH, 45268, USA.
U.S. Environmental Protection Agency, Office of Research and Development, Research Triangle Park, NC, 27709, USA.
Toxicon X. 2020 Oct 7;8:100060. doi: 10.1016/j.toxcx.2020.100060. eCollection 2020 Dec.
The canonical mode of action (MOA) of microcystins (MC) is the inhibition of protein phosphatases, but complete characterization of toxicity pathways is lacking. The existence of over 200 MC congeners complicates risk estimates worldwide. This work employed RNA-seq to provide an unbiased and comprehensive characterization of cellular targets and impacted cellular processes of hepatocytes exposed to either MC-LR or MC-RR congeners. The human hepatocyte cell line, HepaRG, was treated with three concentrations of MC-LR or -RR for 2 h. Significant reduction in cell survival was observed in LR1000 and LR100 treatments whereas no acute toxicity was observed in any MR-RR treatment. RNA-seq was performed on all treatments of MC-LR and -RR. Differentially expressed genes and pathways associated with oxidative and endoplasmic reticulum (ER) stress, and the unfolded protein response (UPR) were highly enriched by both congeners as were inflammatory pathways. Genes associated with both apoptotic and inflammatory pathways were enriched in LR1000. We present a model of MC toxicity that immediately causes oxidative stress and leads to ER stress and the activation of the UPR. Differential activation of the three arms of the UPR and the kinetics of JNK activation ultimately determine whether cell survival or apoptosis is favored. Extracellular exosomes were enrichment of by both congeners, suggesting a previously unidentified mechanism for MC-dependent extracellular signaling. The complement system was enriched only in MC-RR treatments, suggesting congener-specific differences in cellular effects. This study provided an unbiased snapshot of the early systemic hepatocyte response to MC-LR and MC-RR congeners and may explain differences in toxicity among MC congeners.
微囊藻毒素(MC)的典型作用模式(MOA)是抑制蛋白磷酸酶,但毒性途径的完整特征尚不明确。超过200种MC同系物的存在使全球范围内的风险评估变得复杂。这项工作采用RNA测序来无偏且全面地表征暴露于MC-LR或MC-RR同系物的肝细胞的细胞靶点和受影响的细胞过程。用人肝细胞系HepaRG分别用三种浓度的MC-LR或-RR处理2小时。在LR1000和LR100处理中观察到细胞存活率显著降低,而在任何MR-RR处理中均未观察到急性毒性。对所有MC-LR和-RR处理进行了RNA测序。与氧化应激和内质网(ER)应激以及未折叠蛋白反应(UPR)相关的差异表达基因和途径在两种同系物中均高度富集,炎症途径也是如此。与凋亡和炎症途径相关的基因在LR1000中富集。我们提出了一个MC毒性模型,该模型立即引起氧化应激并导致ER应激和UPR的激活。UPR三个分支的差异激活和JNK激活的动力学最终决定细胞存活还是凋亡占优势。两种同系物都富集了细胞外囊泡,这表明存在一种以前未被识别的MC依赖的细胞外信号传导机制。补体系统仅在MC-RR处理中富集,表明细胞效应存在同系物特异性差异。这项研究提供了早期系统性肝细胞对MC-LR和MC-RR同系物反应的无偏概况,并可能解释MC同系物之间毒性的差异。