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Exometabolomic analysis of decidualizing human endometrial stromal and perivascular cells

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Harden, Sarah, Zhou, Jieliang, Gharanei, Seley, Diniz-da-Costa, Maria, Lucas, Emma S., Cui, Liang, Murakami, Keisuke, Fang, Jinling, Chen, Qingfeng, Brosens, Jan J. and Lee, Yie Hou (2021) Exometabolomic analysis of decidualizing human endometrial stromal and perivascular cells. Frontiers, 9 . 626619. doi:10.3389/fcell.2021.626619 ISSN 0160-9009.

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Official URL: https://doi.org/10.3389/fcell.2021.626619

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Abstract

Differentiation of endometrial fibroblasts into specialized decidual cells controls embryo implantation and transforms the cycling endometrium into a semi-permanent, immune-protective matrix that accommodates the placenta throughout pregnancy. This process starts during the midluteal phase of the menstrual cycle with decidual transformation of perivascular cells (PVC) surrounding the terminal spiral arterioles and endometrial stromal cells (EnSC) underlying the luminal epithelium. Decidualization involves extensive cellular reprogramming and acquisition of a secretory phenotype, essential for coordinated placental trophoblast invasion. Secreted metabolites are an emerging class of signalling molecules. Here, we used liquid chromatography-mass spectrometry to characterise the dynamic changes in metabolite secretion (exometabolome) of primary PVC and EnSC decidualized over 8 days. We identified 79 annotated metabolites differentially secreted upon decidualization, including prostaglandin, sphingolipid, and hyaluronic acid metabolites. Secreted metabolites encompassed 21 metabolic pathways, most prominently glycerolipid and pyrimidine metabolism. Although temporal exometabolome changes were comparable between decidualizing PVC and EnSC, 32 metabolites were differentially secreted across the decidualization time-course. Further, targeted metabolomics demonstrated a conspicuous difference in xanthine secretion between decidualized PVC and EnSC. Taken together, our findings indicate that the metabolic footprints generated by different decidual subpopulations encode spatiotemporal information that may be important for optimal embryo implantation.

Item Type:

Journal Article

Subjects:

Q Science > QH Natural history
Q Science > QP Physiology

Divisions:

Faculty of Science, Engineering and Medicine > Medicine > Warwick Medical School

Library of Congress Subject Headings (LCSH):

Endometrium, Metabolism, Reproduction -- Molecular aspects, Vascular smooth muscle

Journal or Publication Title:

Frontiers

Publisher:

University of Nebraska Press

ISSN:

0160-9009

Official Date:

28 January 2021

Dates:

Date	Event
28 January 2021	Published
11 January 2021	Accepted

Volume:

Article Number:

626619

DOI:

10.3389/fcell.2021.626619

Status:

Peer Reviewed

Publication Status:

Published

Access rights to Published version:

Open Access (Creative Commons)

Date of first compliant deposit:

15 January 2021

Date of first compliant Open Access:

17 February 2021

RIOXX Funder/Project Grant:

Project/Grant ID	RIOXX Funder Name	Funder ID
NMRC/CG/M003/2017	National Research Foundation Singapore	http://dx.doi.org/10.13039/501100001381
Fellowship : NRF-NRFF2017-03	National Research Foundation Singapore	http://dx.doi.org/10.13039/501100001381
Investigator Award : 212233/Z/18/Z	Wellcome Trust	http://dx.doi.org/10.13039/100010269
UNSPECIFIED	University of Warwick	http://dx.doi.org/10.13039/501100000741
A∗ STAR Research Attachment Program	Agency for Science, Technology and Research	http://dx.doi.org/10.13039/501100001348