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Micro-bulk RNA-seq of trilaminar omphalopleure of Monodelphis domestica to investigate placental cytokine signaling

ABSTRACT: The brief placental attachment of the gray short-tailed opossum Monodelphis domestica spans only the final two days of the 14-day pregnancy. During this time the fetus grows rapidly and a pronounced spike in inflammatory signaling occurs. It was recently discovered that these cytokines are produced primarily by fetal cells, the syncytial knots which develop at the end stage of placentation after day 13 of gestation. To investigate this further, we conducted laser microdissection on placental membranes (omphalopleure) at 13.5 days post copulation to compare to published transcriptomes at 12.5 days post copulation. Analysis revealed indeed a pronounced expression of inflammatory cytokines in the 13.5 samples. We hypothesized that placental cytokines act as solicitation signals benefitting the fetus by effects on maternal nutrient transfer. To test this, we administered anti-inflammatory drugs to pregnant opossums during the attachment phase targeted at three arms of this response: IL1A via the receptor inhibitor anakinra, IL6 via the receptor inhibitor tocilizumab, and prostaglandin E2 via the PTGS2 synthetase inhibitor meloxicam. Inhibition of IL-1 and IL-6 signaling resulted in significant increases in fetal biomass, suggesting that they impose a cost to biomass acquisition by offspring rather than acting in direct solicitation. However, in the case of anakinra, saline-treated control individuals showed a greater mean surviving litter size compared to IL-1-inhibited animals. Together, our results suggest that marsupial end-pregnancy inflammation has acquired a novel function modulating both fetal growth and survival during pregnancy.

ORGANISM(S): Monodelphis domestica

PROVIDER: GSE302731 | GEO | 2026/01/31

REPOSITORIES: GEO

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Project description:Activation of the maternal immune system during pregnancy can fetal development, which can lead to postnatal susceptibility to a wide range of diseases, including cardiovascular, metabolic and psychiatric disorders. During maternal immune activation (MIA), the maternal body must balance its ressources between mounting an immune response and investing resources into continued metabolism and growth : both essential for survival of the fetus and a successful pregnancy. How the placenta responds to MIA over time and how it can protect the fetus is not well understood, and neither are the fetal consequences of MIA. Here, we characterised the response to an induced acute inflammation in maternal lungs over time across maternal and fetal organs, using a combination of omics-methods, imaging and integrative computational analysis. We found that the placenta, unlike other maternal organs, did not react by inducing a typical inflammatory response, but instead initially induced genes associated to strengthen tissue integrity and simultaneously reduced growth to prevent exposure to potential infections. Afterwards, a return to homeostasis was observed, with heightened biosynthesis and expression of endoplasmic reticulum (ER) stress genes. This mechanism likely protects the fetus from inflammation, as we observed no immune response in the fetal liver transcriptome. Instead, we observed metabolic adaptations in the fetus, including a release of docosahexaenoic acid (DHA) Notably, DHA has a crucial function for fetal brain development , and levels of triglyceride and phosphatidylcholine lipids that are necessary for transportation of DHA to the brain were also increased. This metabolic response is likely a combination of the placental MIA response and temporary maternal fasting, caused by MIA-induced fever and lack of nutrient intake. Our study shows, for the first time, the temporal and systemic response to MIA in lungs across maternal and fetal organs.

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Micro-bulk RNA-seq of trilaminar omphalopleure of Monodelphis domestica to investigate placental cytokine signaling

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