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Characterization of highly proliferative decidual precursor cells during the window of implantation in human endometrium

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Diniz-da-Costa, Maria, Kong, Chow-Seng, Fishwick, Katherine, Rawlings, Thomas, Brighton, Paul (Paul J.), Hawkes, Amelia, Odendaal, Joshua, Quenby, Siobhan, Ott, Sascha, Lucas, Emma S., Vrljicak, Pavle and Brosens, Jan J. (2021) Characterization of highly proliferative decidual precursor cells during the window of implantation in human endometrium. Stem Cells, 39 (8). pp. 1067-1080. doi:10.1002/stem.3367 ISSN 1066-5099.

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Official URL: https://doi.org/10.1002/stem.3367

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Abstract

Pregnancy depends on the wholesale transformation of the endometrium, a process driven by differentiation of endometrial stromal cells (EnSC) into specialist decidual cells. Upon embryo implantation, decidual cells impart the tissue plasticity needed to accommodate a rapidly growing conceptus and invading placenta, although the underlying mechanisms are unclear. Here we characterize a discrete population of highly proliferative mesenchymal cells (hPMC) in midluteal human endometrium, coinciding with the window of embryo implantation. Single-cell transcriptomics demonstrated that hPMC express genes involved in chemotaxis and vascular transmigration. Although distinct from resident EnSC, hPMC also express genes encoding pivotal decidual transcription factors and markers, most prominently prolactin. We further show that hPMC are enriched around spiral arterioles, scattered throughout the stroma, and occasionally present in glandular and luminal epithelium. The abundance of hPMC correlated with the in vitro colony-forming unit activity of midluteal endometrium and, conversely, clonogenic cells in culture express a gene signature partially conserved in hPMC. Cross-referencing of single-cell RNA-sequencing data sets indicated that hPMC differentiate into a recently discovered decidual subpopulation in early pregnancy. Finally, we demonstrate that recurrent pregnancy loss is associated with hPMC depletion. Collectively, our findings characterize midluteal hPMC as novel decidual precursors that are likely derived from circulating bone marrow-derived mesenchymal stem/stromal cells and integral to decidual plasticity in pregnancy.

Item Type: Journal Article
Subjects: Q Science > QM Human anatomy
Q Science > QP Physiology
Q Science > QR Microbiology
R Medicine > RG Gynecology and obstetrics
Divisions: Faculty of Science, Engineering and Medicine > Medicine > Warwick Medical School
Library of Congress Subject Headings (LCSH): B cells, Mesenchymal stem cells , Infertility, Female -- Treatment, Human embryo -- Transplantation, Endometrium , Miscarriage, Pregnancy , Pregnancy -- Complications
Journal or Publication Title: Stem Cells
Publisher: Oxford University Press
ISSN: 1066-5099
Official Date: August 2021
Dates:
DateEvent
August 2021Published
25 March 2021Available
19 February 2021Accepted
Volume: 39
Number: 8
Page Range: pp. 1067-1080
DOI: 10.1002/stem.3367
Status: Peer Reviewed
Publication Status: Published
Access rights to Published version: Open Access (Creative Commons)
Date of first compliant deposit: 25 May 2021
Date of first compliant Open Access: 26 May 2021
RIOXX Funder/Project Grant:
Project/Grant IDRIOXX Funder NameFunder ID
212233/Z/18/ZWellcome Trusthttp://dx.doi.org/10.13039/100010269
UNSPECIFIEDTommy'shttp://dx.doi.org/10.13039/501100009324
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