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A longitudinal single-nucleus transcriptomic atlas of bovine placentation reveals dynamic cellular hierarchies and regulatory programs

ABSTRACT: Supporting healthy pregnancy outcomes requires a comprehensive understanding of the cellular hierarchy and underlying molecular mechanisms in the ruminant placenta during gestation. Here, we constructed a single-nucleus transcriptomic atlas of 304,726 placental nuclei spanning 13 developmental stages in cows, identifying 13 major cell types and 14 trophoblast subtypes. Bioinformatics analyses and multiple validation experiments suggested that placental trophoblast cells exhibited stage-specific differences across gestation, and identified HAND1 and DLX5 as novel key regulators of maternal recognition of pregnancy. We found that binucleate (BNC) cells arise from specific uninucleate (UNC) subpopulations at E24, with their differentiation trajectories co-regulated by imprinted genes and metabolic reprogramming. Integrated genome-wide association study (GWAS) analysis identified early trophoblast subtypes significantly associated with gestation length, along with key pathways and risk genes (e.g., CYCS, HMGA1, VDAC1), with these signals under strong evolutionary constraint. Furthermore, we found that placental macrophages originate at E30 in cow and are significantly associated with pregnancy loss in both cattle and humans, sharing common risk pathways. Collectively, this study provides a cross-stage cellular and molecular map of the ruminant placenta, delineates the key regulatory networks at the maternal–fetal interface, and offers a theoretical framework and potential molecular targets for understanding pregnancy maintenance and improving reproductive traits in ruminants.

ORGANISM(S): Bos taurus

PROVIDER: GSE306749 | GEO | 2026/06/12

REPOSITORIES: GEO

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Project description:Data on the temporal dynamics of human placental gene expression is scarce. We have completed the first whole-genome profiling of human placental gene expression dynamics (GeneChips, Affymetrix®) from early to mid- gestation (10 samples; gestational weeks 5 to 18) and report 154 genes with considerable change in transcript levels (FDR P<0.1). Functional enrichment analysis revealed >200 GO categories that are statistically over-represented among 105 genes with dynamically increasing transcript levels. Analysis in an extended sample (n=43; gestational weeks 5 to 41) conformed a highly significant (FDR P<0.05) expressional peak in mid-gestation placenta for ten genes: BMP5, CCNG2, CDH11, FST, GATM, GPR183, ITGBL1, PLAGL1, SLC16A10, STC1. A central hypothesis of our study states that the aberrant expression of genes characteristic to mid-gestation placenta may contribute to affected fetal growth, maternal preeclampsia (PE) or gestational diabetes (GD). The gene STC1 coding for Stanniocalcin 1 (STC1) was identified with a sharp placental expressional peak in mid-gestation, increased mRNA levels at term and significantly elevated STC1 protein levels in post-partum maternal plasma in all pregnancy complications. The highest STC1 levels were identified in women, who developed simultaneously PE and delivered an SGA baby (median 731 vs 418 pg/ml in controls; P=0.001). CCNG2 and LYPD6 exhibited significantly increased placental mRNA expression and enhanced intensity of immunohistochemistry staining in placental sections all studied in GD and PE cases. Aberrant expression of mid-gestation specific genes in pregnancy complications at term indicates the importance of the fine-scale tuning of the temporal dynamics of transcription regulation in placenta. Observed significantly elevated plasma STC1 in complicated pregnancies warrants further investigations of its potential as a biomarker. Interestingly, a majority of genes with high expression in mid-gestation placenta have also been implicated in adult complex disease. This observation promotes a recently opened discussion on the role of placenta in developmental programming. 4 samples; this submission is extension of our earlier study (accession GSE22490).

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A longitudinal single-nucleus transcriptomic atlas of bovine placentation reveals dynamic cellular hierarchies and regulatory programs

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