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Endocrinology. 2014 Nov;155(11):4542-53. doi: 10.1210/en.2014-1370. Epub 2014 Aug 13.

Decidualization induces a secretome switch in perivascular niche cells of the human endometrium.

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Division of Reproductive Health, Clinical Science Research Laboratories (K.M., E.S.L., R.P.D., B.K.T., S.Q., J.J.B.), Warwick Medical School, University of Warwick, Coventry CV2 2DX, United Kingdom; Department of Obstetrics and Gynaecology (K.M., S.T.), Juntendo University Faculty of Medicine, Tokyo, 113-8421, Japan; Interdisciplinary Research Groups of BioSystems and Micromechanics, and Infectious Diseases (Y.H.L.), Singapore-MIT Alliance for Research and Technology, Singapore 138602; Warwick Systems Biology Centre (Y.-W.C., J.D.M.), University of Warwick, Coventry CV4 7AL, United Kingdom; Department of Reproductive Medicine (J.K.Y.C.), KK Women's and Children's Hospital, Singapore 229899; Cancer and Stem Cell Biology Program (J.K.Y.C.), Duke-NUS Graduate Medical School, Singapore, 169857; and The Ritchie Centre (C.E.G.), Monash Institute of Medical Research-Prince Henry's Institute, Institute of Medical Research and Department of Obstetrics and Gynaecology, Monash University, Clayton, 3168, Australia.


The endometrial perivascular microenvironment is rich in mesenchymal stem-like cells that express type 1 integral membrane protein Sushi domain containing 2 (SUSD2) but the role of these cells in the decidual transformation of this tissue in pregnancy is unknown. We used an antibody directed against SUSD2 (W5C5) to isolate perivascular (W5C5(+)) and nonperivascular (W5C5(-)) fibroblasts from mid-luteal biopsies. We show that SUSD2 expression, and hence the ratio of W5C5(+):W5C5(-) cells, changes in culture depending on cell-cell contact and activation of the Notch signaling pathway. RNA sequencing revealed that cultures derived from W5C5(+) progenitor cells remain phenotypically distinct by the enrichment of novel and established endometrial perivascular signature genes. In an undifferentiated state, W5C5(+)-derived cells produced lower levels of various chemokines and inflammatory modulators when compared with their W5C5(-) counterparts. This divergence in secretomes was switched and became more pronounced upon decidualization, which transformed perivascular W5C5(+) cells into the dominant source of a range of chemokines and cytokines, including leukemia inhibitory factor and chemokine (C-C motif) ligand 7. Our findings suggest that the decidual response is spatially organized at the embryo-maternal interface with differentiating perivascular cells establishing distinct cytokine and chemokine profiles that could potentially direct trophoblast toward maternal vessels and govern local immune responses in pregnancy.

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