Regulation of Porcine Oviduct Epithelium Functions via Progesterone and Estradiol Is Influenced by Cortisol

Abstract

Preimplantation maternal stress, characterized by elevated glucocorticoids (GCs), has been linked to reproductive failures caused by impaired oviduct functionality, which is known to be predominantly regulated by the sex steroids, progesterone (P4) and (17)estradiol (E2). Although steroid receptors share analogous structures and binding preferences, the interaction between GC and E2/P4 in the oviduct has attracted little attention. Using an air-liquid interface culture model, porcine oviduct epithelial cells were stimulated with single (cortisol, E2, P4) or hormone mixtures (cortisol/E2, cortisol/P4) for 12 h and 72 h. Cultures were subsequently assessed for epithelial morphometry, bioelectrical properties, and gene expression responses (steroid hormone signaling, oviductal function, immune response, and apoptosis). Results confirmed the suppressive role of P4 in regulating oviduct epithelium characteristics, which was partially opposed by E2. Besides increasing the ratio of ciliated cells, cortisol antagonized the effect of P4 on epithelial polarity and modified sex steroids-induced changes in trans-epithelial electrical properties. Both sex steroids affected the glucocorticoid receptor expression, while cortisol downregulated the expression of progesterone receptor. The overall gene expression pattern suggests that sex steroid dominates the co-treatment, but cortisol contributes by altering the gene responses to sex steroids. We conclude that besides its individual action, maternal cortisol interplays with sex steroids at phenotypic and molecular levels in the oviduct epithelium, thereby influencing the microenvironment of gametes and early embryos.

Oxygen levels affect oviduct epithelium functions in air–liquid interface culture

“…Among these, 23 were conducted under atmospheric conditions with 5% CO 2 in a humidified incubator, resulting in supraphysiological O 2 levels of around 18%. Exceptions include the study by Ferraz et al, which performed bovine oviduct and embryo co-culture on a chip under 7% O 2 , and our group’s investigations into the influence of elevated cortisol due to maternal stress on the oviduct microenvironment under 5% O 2 conditions (Ferraz et al 2018 ; Du et al 2020 , 2022 ).…”

“…Initially we checked the expression of epithelial sodium channels (ENaC) situated on the apical membrane. Since these channels are responsible for transporting Na + from the apical fluid into the cytoplasm of epithelial cells, causing water to flow in the same direction (Alexander et al 2019 ; Du et al 2022 ). However, we did not detect a significant influence of O 2 levels on the expression of SCNN1A (encoding the α subunit of ENaC).…”

“…In the past, our group has employed both the one-step and two-step media regimes to study the physiology of oviduct epithelial cells, consistently revealing gene expression changes that mimic in vivo responses towards steroid hormones (Chen et al 2013a , 2018 ; Du et al 2022 ). However, a direct comparison to assess the cell compositions and gene expression profiles of ALI-POEC under the two media regimes has yet to be undertaken.…”

Hypothalamic-Pituitary-Adrenal Hormones Impair Pig Fertilization and Preimplantation Embryo Development via Inducing Oviductal Epithelial Apoptosis: An In Vitro Study

“…In this study, the effective concentrations of CRH and cortisol that caused the significant apoptosis of pig OECs were higher than peak serum concentrations reported in stressed pigs. Du et al [ 53 , 54 ] observed no effect on pig OEC apoptosis by in vitro treatment with cortisol at a stress-induced concentration (2.5 × 10 −7 M). Our previous study [ 52 ] demonstrated that although culture with either 1 × 10 −8 M CRH or 1 mg/mL cortisol did not affect pig oocyte development into blastocysts, culture with both significantly decreased blastocyst rates.…”