Jones Steven, Boisvert Annie, Francois Sade, Zhang Liandong, Culty Martine
Division of Experimental Medicine, The Research Institute of the McGill University Health Centre, McGill University, Montreal, Quebec, Canada.
Department of Medicine, The Research Institute of the McGill University Health Centre, McGill University, Montreal, Quebec, Canada.
Biol Reprod. 2015 Oct;93(4):92. doi: 10.1095/biolreprod.115.129098. Epub 2015 Aug 26.
Fetal exposure to endocrine disruptors (EDs) is believed to predispose males to reproductive abnormalities. Although males are exposed to combinations of chemicals, few studies have evaluated the effects of ED mixtures at environmentally relevant doses. Our previous work showed that fetal exposure to a mixture of the phytoestrogen genistein (GEN) and the plasticizer di-(2-ethylhexyl) phthalate (DEHP) induced unique alterations in adult testis. In this follow-up study, we examined Postnatal Day 3 (PND3) and PND6 male offspring exposed from Gestational Day 14 to parturition to corn oil, 10mg/kg GEN, DEHP, or their combination, to gain insight into the early molecular events driving long-term alterations. DEHP stimulated the mRNA and protein expression of the steroidogenic enzyme HSD3B, uniquely at PND3. DEHP also increased the mRNA expression of Nestin, a Leydig progenitor/Sertoli cell marker, and markers of Sertoli cell (Wt1), gonocyte (Plzf, Foxo1), and proliferation (Pcna) at PND3, while these genes were unchanged by the mixture. Redox (Nqo1, Sod2, Sod3, Trx, Gst, Cat) and xenobiotic transporter (Abcb1b, Abcg2) gene expression was also increased by DEHP at PND3, while attenuated when combined with GEN, suggesting the involvement of cellular stress in short-term DEHP effects and a protective effect of GEN. The direct effects of GEN and mono-(2-ethylhexyl) phthalate, the principal bioactive metabolite of DEHP, on testis were investigated in PND3 organ cultures, showing a stimulatory effect of 10 μM mono-(2-ethylhexyl) phthalate on basal testosterone production that was normalized by GEN. These effects contrasted with previous reports of androgen suppression and decreased gene expression in perinatal rat testis by high DEHP doses, implying that neonatal effects are not predictive of adult effects. We propose that GEN, through an antioxidant action, normalizes reactive oxygen species-induced neonatal effects of DEHP. The notion that these EDs do not follow classical dose-response effects and involve different mechanisms of toxicity from perinatal ages to adulthood highlights the importance of assessing impacts across a range of doses and ages.
胎儿暴露于内分泌干扰物(EDs)被认为会使男性易患生殖异常。尽管男性会接触多种化学物质的组合,但很少有研究评估环境相关剂量下ED混合物的影响。我们之前的研究表明,胎儿暴露于植物雌激素染料木黄酮(GEN)和增塑剂邻苯二甲酸二(2-乙基己基)酯(DEHP)的混合物会导致成年睾丸出现独特的改变。在这项后续研究中,我们检查了从妊娠第14天到分娩期间暴露于玉米油、10mg/kg GEN、DEHP或它们的组合的出生后第3天(PND3)和PND6雄性后代,以深入了解驱动长期改变的早期分子事件。DEHP在PND3时独特地刺激了类固醇生成酶HSD3B的mRNA和蛋白质表达。DEHP还增加了Nestin(一种睾丸间质祖细胞/支持细胞标志物)以及支持细胞(Wt1)、生殖母细胞(Plzf、Foxo1)和增殖(Pcna)标志物在PND3时的mRNA表达,而这些基因在混合物作用下未发生变化。氧化还原(Nqo1、Sod2、Sod3、Trx、Gst、Cat)和外源性物质转运蛋白(Abcb1b、Abcg2)基因表达在PND3时也因DEHP而增加,但与GEN联合时减弱,这表明细胞应激参与了DEHP的短期效应以及GEN的保护作用。在PND3器官培养物中研究了GEN和DEHP的主要生物活性代谢物单-(2-乙基己基)邻苯二甲酸酯对睾丸的直接影响,结果显示10μM单-(2-乙基己基)邻苯二甲酸酯对基础睾酮产生有刺激作用,而GEN可使其恢复正常。这些效应与之前关于高剂量DEHP抑制围产期大鼠睾丸雄激素并降低基因表达的报道形成对比,这意味着新生儿期的效应并不能预测成年期的效应。我们提出GEN通过抗氧化作用使活性氧诱导的DEHP新生儿期效应恢复正常。这些EDs不遵循经典剂量反应效应且从围产期到成年期涉及不同毒性机制的观点凸显了评估不同剂量和年龄范围影响的重要性。