Exometabolomic Analysis of Decidualizing Human Endometrial Stromal and Perivascular Cells
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 me...
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Published in | Frontiers in cell and developmental biology Vol. 9; p. 626619 |
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Main Authors | , , , , , , , , , , |
Format | Journal Article |
Language | English |
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28.01.2021
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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 signaling molecules, collectively known as the exometabolome. Here, we used liquid chromatography-mass spectrometry to characterize and analyze time-resolved changes in metabolite secretion (exometabolome) of primary PVC and EnSC decidualized over 8 days. PVC were isolated using positive selection of the cell surface marker SUSD2. 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 significant differences in secretion of purine pathway metabolites 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. |
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AbstractList | 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 signaling molecules, collectively known as the exometabolome. Here, we used liquid chromatography-mass spectrometry to characterize and analyze time-resolved changes in metabolite secretion (exometabolome) of primary PVC and EnSC decidualized over 8 days. PVC were isolated using positive selection of the cell surface marker SUSD2. 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 significant differences in secretion of purine pathway metabolites 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. |
Author | Zhou, Jieliang Harden, Sarah L Gharanei, Seley Lee, Yie Hou Diniz-da-Costa, Maria Fang, Jinling Chen, Qingfeng Brosens, Jan J Murakami, Keisuke Lucas, Emma S Cui, Liang |
AuthorAffiliation | 2 Singapore–MIT Alliance for Research and Technology , Singapore , Singapore 6 Tommy’s National Centre for Miscarriage Research, University Hospitals Coventry and Warwickshire , Coventry , United Kingdom 8 Department of Obstetrics and Gynecology, Faculty of Medicine, Juntendo University , Tokyo , Japan 4 Translational ‘Omics and Biomarkers Group, KK Research Centre, KK Women’s and Children’s Hospital , Singapore , Singapore 1 Division of Biomedical Sciences, Clinical Science Research Laboratories, Warwick Medical School, University of Warwick , Coventry , United Kingdom 3 Institute of Molecular and Cell Biology, Agency for Science, Technology and Research , Singapore , Singapore 7 Centre for Early Life, Warwick Medical School, University of Warwick , Coventry , United Kingdom 9 Obstetrics and Gynaecology Academic Clinical Programme, Duke-NUS Medical School , Singapore , Singapore 5 Warwickshire Institute for the Study of Diabetes, Endocrinology and Metabolism (WISDEM), University Hospitals Cov |
AuthorAffiliation_xml | – name: 1 Division of Biomedical Sciences, Clinical Science Research Laboratories, Warwick Medical School, University of Warwick , Coventry , United Kingdom – name: 4 Translational ‘Omics and Biomarkers Group, KK Research Centre, KK Women’s and Children’s Hospital , Singapore , Singapore – name: 3 Institute of Molecular and Cell Biology, Agency for Science, Technology and Research , Singapore , Singapore – name: 5 Warwickshire Institute for the Study of Diabetes, Endocrinology and Metabolism (WISDEM), University Hospitals Coventry and Warwickshire NHS Trust , Coventry , United Kingdom – name: 8 Department of Obstetrics and Gynecology, Faculty of Medicine, Juntendo University , Tokyo , Japan – name: 9 Obstetrics and Gynaecology Academic Clinical Programme, Duke-NUS Medical School , Singapore , Singapore – name: 2 Singapore–MIT Alliance for Research and Technology , Singapore , Singapore – name: 7 Centre for Early Life, Warwick Medical School, University of Warwick , Coventry , United Kingdom – name: 6 Tommy’s National Centre for Miscarriage Research, University Hospitals Coventry and Warwickshire , Coventry , United Kingdom |
Author_xml | – sequence: 1 givenname: Sarah L surname: Harden fullname: Harden, Sarah L organization: Institute of Molecular and Cell Biology, Agency for Science, Technology and Research, Singapore, Singapore – sequence: 2 givenname: Jieliang surname: Zhou fullname: Zhou, Jieliang organization: Translational 'Omics and Biomarkers Group, KK Research Centre, KK Women's and Children's Hospital, Singapore, Singapore – sequence: 3 givenname: Seley surname: Gharanei fullname: Gharanei, Seley organization: Warwickshire Institute for the Study of Diabetes, Endocrinology and Metabolism (WISDEM), University Hospitals Coventry and Warwickshire NHS Trust, Coventry, United Kingdom – sequence: 4 givenname: Maria surname: Diniz-da-Costa fullname: Diniz-da-Costa, Maria organization: Tommy's National Centre for Miscarriage Research, University Hospitals Coventry and Warwickshire, Coventry, United Kingdom – sequence: 5 givenname: Emma S surname: Lucas fullname: Lucas, Emma S organization: Centre for Early Life, Warwick Medical School, University of Warwick, Coventry, United Kingdom – sequence: 6 givenname: Liang surname: Cui fullname: Cui, Liang organization: Singapore-MIT Alliance for Research and Technology, Singapore, Singapore – sequence: 7 givenname: Keisuke surname: Murakami fullname: Murakami, Keisuke organization: Department of Obstetrics and Gynecology, Faculty of Medicine, Juntendo University, Tokyo, Japan – sequence: 8 givenname: Jinling surname: Fang fullname: Fang, Jinling organization: Singapore-MIT Alliance for Research and Technology, Singapore, Singapore – sequence: 9 givenname: Qingfeng surname: Chen fullname: Chen, Qingfeng organization: Institute of Molecular and Cell Biology, Agency for Science, Technology and Research, Singapore, Singapore – sequence: 10 givenname: Jan J surname: Brosens fullname: Brosens, Jan J organization: Centre for Early Life, Warwick Medical School, University of Warwick, Coventry, United Kingdom – sequence: 11 givenname: Yie Hou surname: Lee fullname: Lee, Yie Hou organization: Obstetrics and Gynaecology Academic Clinical Programme, Duke-NUS Medical School, Singapore, Singapore |
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Copyright | Copyright © 2021 Harden, Zhou, Gharanei, Diniz-da-Costa, Lucas, Cui, Murakami, Fang, Chen, Brosens and Lee. Copyright © 2021 Harden, Zhou, Gharanei, Diniz-da-Costa, Lucas, Cui, Murakami, Fang, Chen, Brosens and Lee. 2021 Harden, Zhou, Gharanei, Diniz-da-Costa, Lucas, Cui, Murakami, Fang, Chen, Brosens and Lee |
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Keywords | endometrial stromal cells endometrium metabolism decidualization exometabolome perivascular cells reproduction |
Language | English |
License | Copyright © 2021 Harden, Zhou, Gharanei, Diniz-da-Costa, Lucas, Cui, Murakami, Fang, Chen, Brosens and Lee. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Edited by: Biserka Mulac Jericevic, University of Rijeka, Croatia These authors have contributed equally to this work This article was submitted to Molecular Medicine, a section of the journal Frontiers in Cell and Developmental Biology Reviewed by: Maximilian Schuff, NEXTCLINIC IVF Zentren Prof. Zech, Austria; Philippa Saunders, University of Edinburgh, United Kingdom; Bruno Miguel Fonseca, University of Porto, Portugal |
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Title | Exometabolomic Analysis of Decidualizing Human Endometrial Stromal and Perivascular Cells |
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