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Adult bone marrow-derived progenitors give rise to decidual cells and are essential for implantation and pregnancy maintenance

ABSTRACT: Bone marrow (BM)-derived progenitor cells (BMDPCs) are known to migrate and give rise to endometrial cells however their functional contribution to implantation and pregnancy are unknown . Here we show that implantation and pregnancy are strong stimuli for BMDPCs recruitment to the uterine decidua where BMDPCs differentiate into functional non-hematopoietic prolactin-producing decidual cells. Transcriptome analysis of implantation sites demonstrated that Hoxa11+/- mice transplanted with WT BM clustered hierarchically more closely with normal WT mice than with control Hoxa11+/- mice, showing normalized expression of numerous implantation-related genes. These findings reveal that BMDPCs have a major non-hematopoietic physiologic contribution to the decidual stroma, and thereby play an essential and previously unproven role in the establishment and maintenance of pregnancy.

ORGANISM(S): Mus musculus

PROVIDER: GSE93743 | GEO | 2020/01/17

REPOSITORIES: GEO

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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.

2019-12-01 | GSE104842 | GEO

Reconstruction of the decidual pathway in human endometrial cells using single-cell RNA-Seq

Project description:The fate of the human endometrium is determined during the mid-luteal window of implantation, coinciding with differentiation of endometrial stromal cells (EnSCs) into specialized decidual cells. Upon embryo implantation, differentiating EnSCs transform the endometrium into the decidua of pregnancy; whereas falling progesterone levels in the absence of pregnancy lead to tissue breakdown and menstruation. We used single-cell RNA sequencing to map the transcriptomic changes in primary EnSCs along a decidual time-course and in response to withdrawal of differentiation signals. We demonstrate that decidual transformation starts with a precipitous transcriptional response, which is followed by synchronous transition of EnSCs through intermediate states before emerging as divergent subpopulations, representing decidual cells and senescent decidual cells. Single-cell analysis of timed luteal phase biopsies identified multiple endometrial epithelial subpopulations and immune cells, most prominently uterine NK cells. In the stroma, transition from receptive to post-receptive endometrial state was marked by progression of EnSCs along diverging transcriptional trajectories, involving genes with conserved branching dynamics in vivo and in vitro. Our findings indicate that specification of EnSCs into distinct decidual subpopulations underpins endometrial fate decisions during the window of implantation.

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Project description:Macrophages are abundant in uterine mucosa during the peri-implantation phase and early pregnancy. Decidual macrophages display dynamic changes alone with pregnancy progress: During the peri-implantation phase, macrophages displayed a pro-inflammatory phenotype which facilitates embryo implantation. While, In the late firster trimester and second trimester, decidual macrophages are anti-proinflammatory which are helpful to pregnancy maintenance. Alterations in the ratio of pro-inflammatory/anti-inflammatory decidual macrophages lead to abortion, preeclampsia, and preterm birth. Placenta-derived exosomes (pEXO) are critical in the immune cell modulation such as T cell apoptosis, NK activities, and T regulatory (Treg) differentiation. However, it is unknown whether placenta-derived exosomes contribute to decidual macrophage polarization during early pregnancy. Here we report that exosomes from the placenta explant stimulate M2 macrophage polarization via exosomal miRNA-30d-5p. Mechanistically, miRNA-30d-5p polarized macrophages to M2 phenotype by inhibiting HDAC9 expression. Furthermore, the conditioned medium of pEXO-treated macrophages promoted trophoblast migration and invasion. By contrast, conditioned medium impaired the ability of endothelial cell tube formation. However, pEXO-treated macrophages have no impact on T cell proliferation. Together, we demonstrated that pEXO promoted trophoblast migration and invasion, endothelial cell migration, and attenuation of endothelial cell tube formation by polarizing macrophage to decidua-like macrophage.

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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

multiomic snRNAseq/snATACseq of human implantation sites, placenta and decidua

Project description:These samples are part of a study to provide a spatially resolved single-cell multiomics map of human trophoblast differentiation in early pregnancy. Here we profiled human implantation sites, decidual and placental samples from 6-9 PCW by 10x multiome snRNA-seq/snATAC-seq.

2023-02-09 | E-MTAB-12595 | biostudies-arrayexpress

Single-cell RNA Sequencing of Endometrial Assembloid Cultures

Project description:Decidual remodelling of midluteal endometrium leads to a short implantation window after which the uterine mucosa either breaks down or is transformed into a robust matrix that accommodates the placenta throughout pregnancy. To gain insights into the underlying mechanisms, we established and characterised endometrial assembloids, consisting of gland organoids and primary stromal cells. Single-cell transcriptomics revealed that decidualized assembloids closely resemble midluteal endometrium, harbouring differentiated and senescent subpopulations in both glands and stroma. We show that acute senescence in glandular epithelium drives secretion of multiple canonical implantation factors, whereas in the stroma it calibrates the emergence of anti-inflammatory decidual cells and pro-inflammatory senescent decidual cells. Pharmacological inhibition of stress responses in pre-decidual cells accelerated decidualization by inhibiting senescence and mesenchymal-epithelial transition, processes involved in endometrial breakdown and regeneration, respectively. Accelerated decidualization resulted in entrapment of co-cultured human blastocysts in a largely static decidual matrix. By contrast, the presence of senescent decidual cells created a dynamic implantation environment, enabling embryo expansion and attachment, although their persistence led to gradual disintegration of assembloids. Together, our findings demonstrate that senescence controls endometrial fate decisions at implantation and highlight how endometrial assembloids may accelerate the discovery of new treatments to prevent reproductive failure.

2021-03-08 | GSE168405 | GEO

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 [scRNA-seq]

2023-09-12 | GSE226417 | GEO

scRNAseq/snucRNAseq of human implantation sites, placenta and decidua.

Project description:These samples are part of a study to provide a spatially resolved single-cell multiomics map of human trophoblast differentiation in early pregnancy. Here we profiled three human implantation sites (between 6 and 9 post-conceptional weeks, PCW) with snucRNAseq; five decidual and three placental samples from 8-13 PCW by scRNA-seq/snRNA-seq.

2023-02-09 | E-MTAB-12421 | biostudies-arrayexpress

EGAS00001004069-sc-2023-02-08T16:08:31Z - samples

Project description:This dataset is part of a study that aims to provide a spatially resolved single-cell multiomics map of human trophoblast differentiation in early pregnancy. This dataset contains 10x multiome snRNA-seq/snATAC-seq from human implantation sites, decidual and placental samples from 8-9 PCW.

| EGAD00001010038 | EGA

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