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Programming of the Endometrial Immune Milieu by Interferon Gamma during Early Pregnancy in Pigs

ABSTRACT: Release of interferon-gamma (IFNG), a pro-inflammatory type II interferon, by the early conceptus is critical for pregnancy establishment in the pig. Yet, the cellular and molecular mechanisms underpinning conceptus-derived IFNG actions in maternal peripheral immune cells and at the embryo–maternal interface remain unclear. Here we show that pregnancy status up-regulates expression of IRF1, an IFNG target-gene, in peripheral blood mononuclear cells on day 15 of pregnancy in the pig. In a second study, loss-of-function IFNG (IFNG–/–) embryos were generated by using CRISPR/Cas9 gene editing and somatic cell nuclear transfer. Single-nuclei RNA sequencing of endometrium from gilts carrying wild-type (Control) or IFNG–/– conceptuses on day 15 of pregnancy revealed cell-type-specific signatures at the embryo–maternal interface in response to conceptus IFNG. Changes in the transcriptome of epithelial and IFNG receptor-expressing immune cells were evident between Control and IFNG–/– samples, along with a downregulation of IFNG target-genes involved with chemotaxis and immune cell differentiation in IFNG–/– recipient endometria. A notable reduction in monocytes and macrophages was observed in IFNG–/– samples, confirmed by immunohistochemistry for AIF1. Differential gene expression (DEG) analysis revealed 391 DEGs in monocytes, implicating IFNG in macrophage polarization, with evidence suggesting a shift toward an M2 phenotype. The study concludes that conceptus IFNG plays an important role in monocyte recruitment and macrophage polarization at the embryo–maternal interface for regulation of inflammation upon conceptus attachment. Insufficient numbers or skewed IFNG-activated macrophages within the endometrium may contribute to pregnancy failure in the IFNG–/– pig model.

ORGANISM(S): Sus scrofa

PROVIDER: GSE300400 | GEO | 2026/01/08

REPOSITORIES: GEO

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Project description:The female reproductive tract provides a unique environment for a successful pregnancy. It is imperative that the non-pregnant uterus be transformed into a capable environment for the establishment and maintenance of pregnancy. To achieve this, intimate cross-communication between the endometrium and the embryo is necessary at an early stage of life (Almiñana et al., 2012) a dialog which further influences subsequent fetal developmental potential (Fleming et al., 2004) and even post-natal performance. Initially, the trophoblast-derived estrogen is one of the most important embryonic signals to activate the maternal uterus for attachment (Pope & First 1985). Once the conceptus has established its position in the uterus (>d15), its development and growth also require many other maternal-embryonic cellular and molecular interactions to ensure substantial vascular changes in the endometrium and the chorioallantois, mainly development of capillaries under the lamina propriae, essential to provide full function to the pig epiteliochorial placenta required for a successful pregnancy. It is during the peri-attachment window between days 12-30 of gestation when most (20-30%) of the embryos produced in pig natural or artificial breeding die (reviewed by Edwards et al., 2012); embryonic death with a substantial impact on pig production efficiency, especially because it significantly limits litter size. Different studies have focused on the elucidation of the complex embryo-maternal communication network to reduce pregnancy loss. Among these, several studies examined gene expression during the peri-implantation stage, when the majority of embryonic losses occur, or have compared the transcriptomic profiles of pregnant and non- pregnant animals. Interestingly, these studies identified changes in the expression of genes that can -directly or indirectly- contribute to reproductive success such genes related to cell proliferation, hormone synthesis and metabolism, cell adhesion or those related to cytokine production and immune local response (Almiñana et al., 2012, Lin et al, 2015; Smolinska et al., 2019; Yang et al., 2020, Martinez et al., 2020, 2022). However, we should not forget that changes in gene expression do not always lead to a corresponding alteration in the expression of proteins, which are crucial components in all biological processes. The knowledge of the proteome is therefore equally relevant to gene expression changes, being able to help detecting both normal and abnormal physiological conditions. Proteome characterization can led to a better understanding of physiological processes and to identify proteins that may serve as potential biomarkers. To date, only a limited number of studies have unfortunately explored the protein expression profiles of the pig endometrium during the crucial period of maternal recognition of pregnancy, which occurs between day 9 and 13 (Jalali et al., 2015; Kaiser et al., 2006) or during mid/last-gestation, from 40 to 93 days of pregnancy (Chae et al., 2011; Wang et al., 2019). These studies have identified several proteins associated with endometrial function, which could play a role in maternal recognition and progression of pregnancy. Therefore, in order to fully understand the molecular interaction between the conceptus and its chorion with the endometrium, we have aimed to characterize the proteome profile of both, the non-pregnant (control) endometrium compared with that of the “pregnant”endometrium with present extraembryonic membranes between the 3rd and the 4th week period, when the major conceptus loss occurs.

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Programming of the Endometrial Immune Milieu by Interferon Gamma during Early Pregnancy in Pigs

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