Wolters Jarno E J, van Breda Simone G J, Caiment Florian, Claessen Sandra M, de Kok Theo M C M, Kleinjans Jos C S
Department of Toxicogenomics, GROW School for Oncology and Developmental Biology, Maastricht University , P.O. Box 616, Maastricht 6200 MD, The Netherlands.
Chem Res Toxicol. 2017 Oct 16;30(10):1847-1854. doi: 10.1021/acs.chemrestox.7b00171. Epub 2017 Sep 13.
Valproic acid (VPA) is one of the most widely prescribed antiepileptic drugs in the world. Despite its pharmacological importance, it may cause liver toxicity and steatosis through mitochondrial dysfunction. The aim of this study is to further investigate VPA-induced mechanisms of steatosis by analyzing changes in patterns of methylation in nuclear DNA (nDNA) and mitochondrial DNA (mtDNA). Therefore, primary human hepatocytes (PHHs) were exposed to an incubation concentration of VPA that was shown to cause steatosis without inducing overt cytotoxicity. VPA was administered daily for 5 days, and this was followed by a 3 day washout (WO). Methylated DNA regions (DMRs) were identified by using the methylated DNA immunoprecipitation-sequencing (MeDIP-seq) method. The nDNA DMRs after VPA treatment could indeed be classified into oxidative stress- and steatosis-related pathways. In particular, networks of the steatosis-related gene EP300 provided novel insight into the mechanisms of toxicity induced by VPA treatment. Furthermore, we suggest that VPA induces a crosstalk between nDNA hypermethylation and mtDNA hypomethylation that plays a role in oxidative stress and steatosis development. Although most VPA-induced methylation patterns appeared reversible upon terminating VPA treatment, 31 nDNA DMRs (including 5 zinc finger protein genes) remained persistent after the WO period. Overall, we have shown that MeDIP-seq analysis is highly informative in disclosing novel mechanisms of VPA-induced toxicity in PHHs. Our results thus provide a prototype for the novel generation of interesting methylation biomarkers for repeated dose liver toxicity in vitro.
丙戊酸(VPA)是世界上处方最广泛的抗癫痫药物之一。尽管其具有药理学重要性,但它可能通过线粒体功能障碍导致肝毒性和脂肪变性。本研究的目的是通过分析核DNA(nDNA)和线粒体DNA(mtDNA)甲基化模式的变化,进一步研究VPA诱导脂肪变性的机制。因此,将原代人肝细胞(PHH)暴露于已证明可导致脂肪变性而不引起明显细胞毒性的VPA孵育浓度下。每天给予VPA,持续5天,随后进行3天的洗脱期(WO)。通过使用甲基化DNA免疫沉淀测序(MeDIP-seq)方法鉴定甲基化DNA区域(DMR)。VPA处理后的nDNA DMR确实可分为氧化应激和脂肪变性相关途径。特别是,脂肪变性相关基因EP300的网络为VPA处理诱导的毒性机制提供了新的见解。此外,我们认为VPA诱导nDNA高甲基化和mtDNA低甲基化之间的串扰,这在氧化应激和脂肪变性发展中起作用。尽管在终止VPA处理后,大多数VPA诱导的甲基化模式似乎是可逆的,但在WO期后仍有31个nDNA DMR(包括5个锌指蛋白基因)持续存在。总体而言,我们已经表明,MeDIP-seq分析在揭示VPA诱导的PHH毒性新机制方面具有很高的信息量。因此,我们的结果为体外重复剂量肝毒性的新型有趣甲基化生物标志物的新一代提供了原型。