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Spatiotemporal insight into early pregnancy governed by immune-featured stromal cells [scRNA-seq]

ABSTRACT: Endometrial decidualization connecting embryo implantation and placentation is transient, but essential for successful pregnancy, which however is not systematically investigated. Here, by using a novel single-cell spatial transcriptomic profiling technology (scStereo-seq), we were able to visualize and define key and dynamic functional decidual hubs assembled by distinct immune, endothelial, trophoblast and decidual stromal cells (DSCs) during early pregnancy in mice. We classified DSC subclusters and described their transdifferentiation trajectory controlled by transcription factor cascades. Interestingly, we discovered a novel type of DSCs expressing immune cell-specific genes, termed immune DSCs (iDSCs). Whereas immature DSCs attracted immune cells and induced decidual angiogenesis at the mesenchymal-to-epithelial transition (MET) hub during decidualization initiation, iDSCs enabled immune cell recruitment, angiogenesis facilitation and cytotoxic effect induction to form immune cell assembling and angiogenesis hubs, which eventually allow decidual homeostasis maintenance and decidualization-to-placentation transition. We spatiotemporally decode mouse early pregnancy events controlled by immune DSCs.

ORGANISM(S): Mus musculus

PROVIDER: GSE226417 | GEO | 2023/09/12

REPOSITORIES: GEO

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Spatiotemporal insight into early pregnancy governed by immune-featured stromal cells [RNA-seq]

Project description:Endometrial decidualization connecting embryo implantation and placentation is transient, but essential for successful pregnancy, which however is not systematically investigated. Here, by using a novel single-cell spatial transcriptomic profiling technology (scStereo-seq), we were able to visualize and define key and dynamic functional decidual hubs assembled by distinct immune, endothelial, trophoblast and decidual stromal cells (DSCs) during early pregnancy in mice. We classified DSC subclusters and described their transdifferentiation trajectory controlled by transcription factor cascades. Interestingly, we discovered a novel type of DSCs expressing immune cell-specific genes, termed immune DSCs (iDSCs). Whereas immature DSCs attracted immune cells and induced decidual angiogenesis at the mesenchymal-to-epithelial transition (MET) hub during decidualization initiation, iDSCs enabled immune cell recruitment, angiogenesis facilitation and cytotoxic effect induction to form immune cell assembling and angiogenesis hubs, which eventually allow decidual homeostasis maintenance and decidualization-to-placentation transition. We spatiotemporally decode mouse early pregnancy events controlled by immune DSCs.

2023-09-12 | GSE226429 | GEO

Spatiotemporal insight into early pregnancy governed by immune-featured stromal cells [Spatial Transcriptomics]

Project description:Endometrial decidualization connecting embryo implantation and placentation is transient but essential for successful pregnancy, which, however, is not systematically investigated. Here, we use a scStereo-seq technology to spatially visualize and deﬁne the dynamic functional decidual hubs assembled by distinct immune, endothelial, trophoblast, and decidual stromal cells (DSCs) in early pregnant mice. We unravel the DSC transdifferentiation trajectory and surprisingly discover a dual-featured type of immune-featured DSCs (iDSCs). We ﬁnd that immature DSCs attract immune cells and induce decidual angiogenesis at the mesenchymalepithelial transition hub during decidualization initiation. iDSCs enable immune cell recruitment and suppression, govern vascularization, and promote cytolysis at immune cell assembling and vascular hubs, respectively, to establish decidual homeostasis at a later stage. Interestingly, dysfunctional and spatially disordered iDSCs cause abnormal accumulation of immune cells in the vascular hub, which disrupts decidual hub speciﬁcation and eventually leads to pregnancy complications in DBA/2-mated CBA/J mice.

2023-12-18 | GSE250503 | GEO

Bone marrow-derived progenitors become decidual cells and are essential for implantation and pregnancy maintenance

Project description:The pregnant decidua is infiltrated by many immune cells which are thought to originate in the bone marrow (BM) promoting pregnancy. In addition, BM-derived progenitor cells (BMDPCs) become non-hematopoietic endometrial cells. However, whether BMDPCs become non-immune decidual cells and their functional contribution to pregnancy were previously unknown. Here, we show that embryo implantation stimulates vast BMDPCs recruitment to decidua, where BMDPCs differentiate into non-hematopoietic stromal decidual cells. In addition, to determine the functional importance of BMDPCs to pregnancy, we used mice with endometrial stromal-specific defects precluding successful pregnancy. BM transplant (BMT) from wild-type (WT) into Hoxa11-/- mice, which lack decidualization, results in uterine transcriptional changes leading to stromal expansion, gland formation, and marked decidualization otherwise absent in Hoxa11-/- mice. By contrast, BMT from Hoxa11-/- into WT mice induces pregnancy loss. Importantly, in Hoxa11+/- mice, which have increased pregnancy losses, BMT from WT donors leads to normalized expression of numerous decidualization-related genes and rescue of pregnancy loss. Collectively, these findings reveal that BMDPCs have a novel non-hematopoietic physiologic contribution to decidual stroma, thereby playing indispensable roles in pregnancy establishment and maintenance.

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Novel biomarkers for distributed stem cells: asymmetric self-renewal associated (ASRA) genes identification by combined cDNA micro-array orthogonal intersection and sparse feature analysis

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Proteomic profiling of human decidual immune proteins during Toxoplasma gondii infection

Project description:A Toxoplasma gondii infection during pregnancy can result in spontaneous abortion, preterm labor, or congenital fetal defects. The decidual immune system plays a critical role in regulating the immune micro-environment and in the induction of immune tolerance. To better understand the factors that mediate the decidual immune response associated with the T. gondii infection, a large-scale study employing TMT proteomics was conducted to characterize the differential decidual immune proteomes from infected and uninfected human decidual immune cells samples. The decidual immune cells from 105 human voluntary abortion tissues were purified, and of the 5510 unique proteins identified, 181 proteins were found to be differentially abundant (>1.2-fold cutoff, P＜0.05) in the T. gondii-infected decidual immune cells. 11 proteins of 181 differentially expressed proteins associated with trophoblast invasion, placental development, intrauterine fetal growth, and immune tolerance were verified using a quantitative real-time polymerase chain reaction and western blotting. This systematic research identified a broad range of immune factors in human decidual immune cells, shedding a new insight into the decidual immune molecular mechanism for abnormal pregnancy outcomes associated with T. gondii infection.

2018-07-27 | PXD008448 | Pride

The mammalian decidual cell evolved from a cellular stress response

Project description:Among animal species, cell types vary greatly in terms of number and kind. The broad range of number of cell types among species suggests that cell type origination is a significant source of evolutionary novelty. The molecular mechanisms giving rise to novel cell types, however, are poorly understood. Here we show that a novel cell type of eutherians mammals, the decidual stromal cell (DSC), evolved by rewiring an ancestral cellular stress response. We isolated the precursor cell type of DSCs, endometrial stromal fibroblasts (ESFs), from the opossum Monodelphis domestica. We show that, in opossum ESF, the majority of decidual core regulatory genes respond to decidualizing signals, but do not regulate decidual effector genes. Rather, in opossum ESF, decidual transcription factors function in apoptotic and oxidative stress response. We propose that the rewiring of cellular stress responses could be a general mechanism for the evolution of novel cell types.

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Endometrial extracellular vesicle decidualization

Project description:Proper decidualization is vital in preparation for a potential embryo receptivity, placentation, menstrual health and subsequent endometrial regeneration. Given the importance of extracellular vesicles (EVs) in intercellular communication, and recently in embryo implantation and indicators of menstrual cycle and fertility, we investigated their role during decidualization. Overall, this study provides an insight into distinct variation in sEV composition depending upon the level of decidualization of endometrial stromal cells, with the signaling potential to coordinate endometrial health ranging from embryo implantation, facilitating placentation and subsequent endometrial regeneration.

2021-11-17 | PXD026342 | Pride

Transcriptomic profiling of canine decidualization and effects evoked by antigestagens on decidualized canine uterine stromal cells

Project description:Maternal-stroma derived decidual cells are the single population in the canine placenta expressing the nuclear progesterone (P4) receptor (PGR), rendering them crucial for the maintenance of canine pregnancy. Indeed, decreased circulating P4 levels or blockage of PGR function with antigestagens (e.g., aglepristone), culminates in the termination of canine pregnancy. As an in vitro model for canine decidualization, dog uterine stromal (DUS; Graubner et al., 2017) cells can be decidualized in vitro with cAMP. The antigestagens aglepristone and mifepristone ablate the expression of decidualization markers in DUS cells (e.g., PGR, PRLR, IGF1 or PTGES). In order to study the mechanisms involved in feto-maternal communication during pregnancy and induction of parturition, the goal of the present work was to assess transcriptional changes mediated by decidualization and antigestagens-induced effects in decidualized DUS cells. Decidualization led to the upregulation of 1841 differentially expressed genes (DEGs, P < 0.01, FDR < 0.01) involved in cellular proliferation and adhesion, mesenchymal-epithelial transition, extracellular matrix organization, and vaso- and immunomodulation. The 1475 DEGs downregulated after decidualization were mostly associated with apoptosis and cell migration. In decidualized DUS cells, aglepristone modulated 1400 DEGs and mifepristone 1558 DEGs. Interestingly, only around half of the identified DEGs were modulated uniquely by one of the antigestagens. In both situations, however, PGR-blockage was associated with an inversion of decidualization-induced effects. Comparison between antigestagens-mediated effects and transcriptional changes in the canine placenta at term allowed the identification of 191 DEGs associated with cell proliferation and adhesion, vascularization and immune activity. These findings emphasize the importance of P4/PGR signaling for decidual cells function.

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Disrupted PGR-B and ESR1 signaling underlies defective decidualization linked to severe preeclampsia

Project description:In the present study, we aimed to discern the preconception decidual transcriptomic signature associated with in vivo defective decidualization in women who suffered sPE in a previous pregnancy. First, we performed a comparative global transcriptional profiling of endometrium from women who developed sPE in a previous pregnancy and from women who never have had sPE. Then, we selected those genes that were significantly deregulated 1.4-fold higher (FDR<0.05) and have an EntrezID code. As a result, we formulate a transcriptional signature associated with defective decidualization composed by 120 genes.

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Overactivation of wound healing-associated TGF-beta responses in EZH2-deficient decidual stromal cells.

Project description:Our objective was to identify genes upregulated by TGF-beta in control and Ezh2 cKO decidual stromal cells (DSCs), and to compare this set of genes with a previously identified gene set of H3K27me3-marked decidual genes that are putatively silenced by EZH2/PRC2 (Nancy et al. JCI. 2018). We also wanted to assess baseline (BL) gene expression in control and Ezh2 cKO DSCs, and compare it to an RNA-seq analysis of differential gene expression in whole tissue Ezh2 cKO and control decidua. RNA was isolated from untreated and TGF-beta treated decidual stromal cells from control and Ezh2 cKO mice. Sequencing provided was 706 million total reads with an average of 82.2% of these reads aligning uniquely to the mouse genome. Reads uniquely mapped to known mRNAs were used to identify gene expression changes between housing conditions using DESeq2. TGF-beta induced 638 protein-coding genes in EZH2-deficient DSCs versus 480 in control DSCs (with a 295 gene overlap), demonstrating that EZH2-deficient DSCs are transcriptionally more responsive to TGF- (P=0.0025, Fisher’s exact test). Within the 638 genes, activated fibroblast signature genes were highly over-represented. TGF-target genes were 2.7-fold over-represented within the set of genes with higher expression in EZH2-deficient DSCs at baseline (BL; i.e., when neither EZH2-deficient nor control DSCs were treated with TGF-beta; P<1x10-20) . 741 genes were overexpressed in Ezh2 cKO DSCs compared to control DSCs, and 904 genes were underexpressed. Moreover, by comparing to our laboratory's previous CHIP-Seq analysis (Nancy et al. JCI 2018), we noted that genes overexpressed in cKO mice were enriched in previously identified H3K27me3-marked genes (P<1x10-26).

2022-01-11 | GSE171724 | GEO

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