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Maternal stress and the early embryonic microenvironment: investigating long-term cortisol effects on bovine oviductal epithelial cells using air–liquid interface culture
Journal of Animal Science and Biotechnology ( IF 6.3 ) Pub Date : 2024-10-03 , DOI: 10.1186/s40104-024-01087-4
Fiona Wahl, Jianchao Huo, Shuaizhi Du, Jennifer Schoen, Shuai Chen

The oviduct epithelium is the initial maternal contact site for embryos after fertilization, offering the microenvironment before implantation. This early gestation period is particularly sensitive to stress, which can cause reduced fertility and reproductive disorders in mammals. Nevertheless, the local impact of elevated stress hormones on the oviduct epithelium has received limited attention to date, except for a few reports on polyovulatory species like mice and pigs. In this study, we focused on the effects of chronic maternal stress on cattle, given its association with infertility issues in this monoovulatory species. Bovine oviduct epithelial cells (BOEC) differentiated at the air–liquid interface (ALI) were stimulated with 250 nmol/L cortisol for 1 or 3 weeks. Subsequently, they were assessed for morphology, bioelectrical properties, and gene expression related to oviduct function, glucocorticoid pathway, cortisol metabolism, inflammation, and apoptosis. Results revealed adverse effects of cortisol on epithelium structure, featured by deciliation, vacuole formation, and multilayering. Additionally, cortisol exposure led to an increase in transepithelial potential difference, downregulated mRNA expression of the major glucocorticoid receptor (NR3C1), upregulated the expression of cortisol-responsive genes (FKBP5, TSC22D3), and significant downregulation of oviductal glycoprotein 1 (OVGP1) and steroid receptors PGR and ESR1. The systematic comparison to a similar experiment previously performed by us in porcine oviduct epithelial cells, indicated that bovine cultures were more susceptible to elevated cortisol levels than porcine. The distinct responses between both species are likely linked to their divergence in the cortisol-induced expression changes of HSD11B2, an enzyme controlling the cellular capacity to metabolise cortisol. These findings provide insights into the species-specific reactions and reproductive consequences triggered by maternal stress.

中文翻译:


母体应激和早期胚胎微环境:利用气液界面培养研究皮质醇对牛输卵管上皮细胞的长期影响



输卵管上皮是受精后胚胎最初与母体接触的部位,为植入前提供微环境。妊娠早期对压力特别敏感,这可能导致哺乳动物的生育能力下降和生殖障碍。然而,除了一些关于小鼠和猪等多排卵物种的报道外,迄今为止,应激激素升高对输卵管上皮的局部影响受到的关注还很有限。在这项研究中,我们重点关注慢性母体压力对牛的影响,因为它与这种单排卵物种的不孕问题有关。用 250 nmol/L 皮质醇刺激在气液界面 (ALI) 分化的牛输卵管上皮细胞 (BOEC) 1 或 3 周。随后,对它们的形态、生物电特性以及与输卵管功能、糖皮质激素途径、皮质醇代谢、炎症和细胞凋亡相关的基因表达进行了评估。结果揭示了皮质醇对上皮结构的不利影响,其特征是脱落、液泡形成和多层化。此外,皮质醇暴露导致跨上皮电位差增加,主要糖皮质激素受体(NR3C1)的mRNA表达下调,皮质醇反应基因(FKBP5、TSC22D3)的表达上调,以及输卵管糖蛋白1(OVGP1)和输卵管糖蛋白1(OVGP1)的显着下调。类固醇受体 PGR 和 ESR1。与我们之前在猪输卵管上皮细胞中进行的类似实验的系统比较表明,牛培养物比猪更容易受到皮质醇水平升高的影响。 这两个物种之间的不同反应可能与它们在皮质醇诱导的 HSD11B2 表达变化方面的差异有关,HSD11B2 是一种控制细胞代谢皮质醇能力的酶。这些发现为了解母亲压力引发的物种特异性反应和生殖后果提供了见解。
更新日期:2024-10-03
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