Yu Shuping, Mu Yaming, Wang Kai, Wang Ling, Wang Chunying, Yang Zexin, Liu Yu, Li Shuxian, Zhang Meihua
School of Public Health, Weifang Medical University, Weifang, 261053, Shandong, China.
Children's Hospital Affiliated to Shandong University, Jinan, 250014, Shandong, China.
Chem Biol Interact. 2024 Jan 5;387:110812. doi: 10.1016/j.cbi.2023.110812. Epub 2023 Nov 20.
Fetal growth restriction (FGR) is a prevalent complication in obstetrics, yet its exact aetiology remains unknown. Numerous studies suggest that the degradation of the living environment is a significant risk factor for FGR. 1-Nitropyrene (1-NP) is a widespread environmental pollutant as a representative substance of nitro-polycyclic aromatic hydrocarbons. In this study, we revealed that 1-NP induced FGR in fetal mice by constructing 1-NP exposed pregnant mice models. Intriguingly, we found that placental trophoblasts of 1-NP exposed mice exhibited significant ferroptosis, which was similarly detected in placental trophoblasts from human FGR patients. In this regard, we established a 1-NP exposed cell model in vitro using two human trophoblast cell lines, HTR8/SVneo and JEG-3. We found that 1-NP not only impaired the proliferation, migration, invasion and angiogenesis of trophoblasts, but also induced severe cellular ferroptosis. Meanwhile, the ferroptosis inhibitor ferrostatin-1 (Fer-1) effectively rescued 1-NP-induced trophoblast biological function impairment. Mechanistically, we revealed that 1-NP regulated ferroptosis by activating the ERK signaling pathway. Moreover, we innovatively revealed that CYP1B1 was essential for the activation of ERK signaling pathway induced by 1-NP. Overall, our study innovatively identified ferroptosis as a significant contributor to 1-NP induced trophoblastic functional impairment leading to FGR and clarified the specific mechanism by which 1-NP induced ferroptosis via the CYP1B1/ERK signaling pathway. Our study provided novel insights into the aetiology of FGR and revealed new mechanisms of reproductive toxicity of environmental pollutants.
胎儿生长受限(FGR)是产科常见的并发症,但其确切病因尚不清楚。大量研究表明,生存环境的恶化是FGR的一个重要危险因素。1-硝基芘(1-NP)作为硝基多环芳烃的代表性物质,是一种广泛存在的环境污染物。在本研究中,我们通过构建1-NP暴露的孕鼠模型,揭示了1-NP可诱导胎鼠发生FGR。有趣的是,我们发现1-NP暴露小鼠的胎盘滋养层细胞表现出明显的铁死亡,在人类FGR患者的胎盘滋养层细胞中也检测到了类似情况。在这方面,我们使用两种人滋养层细胞系HTR8/SVneo和JEG-3建立了体外1-NP暴露细胞模型。我们发现1-NP不仅损害滋养层细胞的增殖、迁移、侵袭和血管生成,还诱导严重的细胞铁死亡。同时,铁死亡抑制剂铁抑素-1(Fer-1)有效地挽救了1-NP诱导的滋养层细胞生物学功能损伤。机制上,我们揭示了1-NP通过激活ERK信号通路调节铁死亡。此外,我们创新性地揭示了CYP1B1对于1-NP诱导的ERK信号通路激活至关重要。总体而言,我们的研究创新性地确定铁死亡是1-NP诱导滋养层细胞功能损伤导致FGR的一个重要因素,并阐明了1-NP通过CYP1B1/ERK信号通路诱导铁死亡的具体机制。我们的研究为FGR的病因提供了新的见解,并揭示了环境污染物生殖毒性的新机制。