The human placenta shapes the phenotype of decidual macrophages

Summary: During human pregnancy, placenta-derived extravillous trophoblasts (EVTs) invade the decidua and communicate with maternal immune cells. The decidua distinguishes into basalis (decB) and parietalis (decP). The latter remains unaffected by EVT invasion. By defining a specific gating strategy...

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Main Authors: Sigrid Vondra, Anna-Lena Höbler, Andreas Ian Lackner, Johanna Raffetseder, Zala Nikita Mihalic, Andrea Vogel, Leila Saleh, Victoria Kunihs, Peter Haslinger, Markus Wahrmann, Heinrich Husslein, Raimund Oberle, Julia Kargl, Sandra Haider, Paulina Latos, Gernot Schabbauer, Martin Knöfler, Jan Ernerudh, Jürgen Pollheimer
Format: Article
Language:English
Published: Elsevier 2023-01-01
Series:Cell Reports
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124722018812
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author Sigrid Vondra
Anna-Lena Höbler
Andreas Ian Lackner
Johanna Raffetseder
Zala Nikita Mihalic
Andrea Vogel
Leila Saleh
Victoria Kunihs
Peter Haslinger
Markus Wahrmann
Heinrich Husslein
Raimund Oberle
Julia Kargl
Sandra Haider
Paulina Latos
Gernot Schabbauer
Martin Knöfler
Jan Ernerudh
Jürgen Pollheimer
author_facet Sigrid Vondra
Anna-Lena Höbler
Andreas Ian Lackner
Johanna Raffetseder
Zala Nikita Mihalic
Andrea Vogel
Leila Saleh
Victoria Kunihs
Peter Haslinger
Markus Wahrmann
Heinrich Husslein
Raimund Oberle
Julia Kargl
Sandra Haider
Paulina Latos
Gernot Schabbauer
Martin Knöfler
Jan Ernerudh
Jürgen Pollheimer
author_sort Sigrid Vondra
collection DOAJ
description Summary: During human pregnancy, placenta-derived extravillous trophoblasts (EVTs) invade the decidua and communicate with maternal immune cells. The decidua distinguishes into basalis (decB) and parietalis (decP). The latter remains unaffected by EVT invasion. By defining a specific gating strategy, we report the accumulation of macrophages in decB. We describe a decidua basalis-associated macrophage (decBAM) population with a differential transcriptome and secretome compared with decidua parietalis-associated macrophages (decPAMs). decBAMs are CD11chi and efficient inducers of Tregs, proliferate in situ, and secrete high levels of CXCL1, CXCL5, M-CSF, and IL-10. In contrast, decPAMs exert a dendritic cell-like, motile phenotype characterized by induced expression of HLA class II molecules, enhanced phagocytosis, and the ability to activate T cells. Strikingly, EVT-conditioned media convert decPAMs into a decBAM phenotype. These findings assign distinct macrophage phenotypes to decidual areas depending on placentation and further highlight a critical role for EVTs in the induction of decB-associated macrophage polarization.
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spelling doaj.art-4e271b792790412c9f28f9a4f66eebd52023-01-12T04:18:59ZengElsevierCell Reports2211-12472023-01-01421111977The human placenta shapes the phenotype of decidual macrophagesSigrid Vondra0Anna-Lena Höbler1Andreas Ian Lackner2Johanna Raffetseder3Zala Nikita Mihalic4Andrea Vogel5Leila Saleh6Victoria Kunihs7Peter Haslinger8Markus Wahrmann9Heinrich Husslein10Raimund Oberle11Julia Kargl12Sandra Haider13Paulina Latos14Gernot Schabbauer15Martin Knöfler16Jan Ernerudh17Jürgen Pollheimer18Department of Obstetrics and Gynecology, Reproductive Biology Unit, Maternal-fetal Immunology Group, Medical University of Vienna, Vienna, AustriaDepartment of Obstetrics and Gynecology, Reproductive Biology Unit, Maternal-fetal Immunology Group, Medical University of Vienna, Vienna, AustriaDepartment of Obstetrics and Gynecology, Reproductive Biology Unit, Maternal-fetal Immunology Group, Medical University of Vienna, Vienna, AustriaDivision of Inflammation and Infection (II), Department of Biomedical and Clinical Sciences (BKV), Linköping University, Linköping, SwedenOtto Loewi Research Center, Division of Pharmacology, Medical University of Graz, Graz, AustriaInstitute for Vascular Biology, Center for Physiology and Pharmacology, Medical University Vienna, Vienna, Austria; Christian Doppler Laboratory for Arginine Metabolism in Rheumatoid Arthritis and Multiple Sclerosis, Vienna, AustriaDepartment of Obstetrics and Gynecology, Reproductive Biology Unit, Placental Development Group, Medical University of Vienna, Vienna, AustriaDepartment of Obstetrics and Gynecology, Reproductive Biology Unit, Placental Development Group, Medical University of Vienna, Vienna, AustriaDepartment of Obstetrics and Gynecology, Reproductive Biology Unit, Maternal-fetal Immunology Group, Medical University of Vienna, Vienna, AustriaDivision of Nephrology and Dialysis, Department of Medicine III, Medical University of Vienna, Vienna, AustriaDepartment of Obstetrics and Gynecology, Medical University of Vienna, Vienna, AustriaCenter for Pathobiochemistry and Genetics, Institute of Medical Chemistry, Medical University of Vienna, Vienna, AustriaOtto Loewi Research Center, Division of Pharmacology, Medical University of Graz, Graz, AustriaInstitute for Vascular Biology, Center for Physiology and Pharmacology, Medical University Vienna, Vienna, AustriaCenter for Anatomy and Cell Biology, Medical University of Vienna, Vienna, AustriaInstitute for Vascular Biology, Center for Physiology and Pharmacology, Medical University Vienna, Vienna, Austria; Christian Doppler Laboratory for Arginine Metabolism in Rheumatoid Arthritis and Multiple Sclerosis, Vienna, AustriaInstitute for Vascular Biology, Center for Physiology and Pharmacology, Medical University Vienna, Vienna, AustriaDepartment of Clinical Immunology and Transfusion Medicine, Department of Biomedical and Clinical Sciences, Linköping University, Linköping, SwedenDepartment of Obstetrics and Gynecology, Reproductive Biology Unit, Maternal-fetal Immunology Group, Medical University of Vienna, Vienna, Austria; Corresponding authorSummary: During human pregnancy, placenta-derived extravillous trophoblasts (EVTs) invade the decidua and communicate with maternal immune cells. The decidua distinguishes into basalis (decB) and parietalis (decP). The latter remains unaffected by EVT invasion. By defining a specific gating strategy, we report the accumulation of macrophages in decB. We describe a decidua basalis-associated macrophage (decBAM) population with a differential transcriptome and secretome compared with decidua parietalis-associated macrophages (decPAMs). decBAMs are CD11chi and efficient inducers of Tregs, proliferate in situ, and secrete high levels of CXCL1, CXCL5, M-CSF, and IL-10. In contrast, decPAMs exert a dendritic cell-like, motile phenotype characterized by induced expression of HLA class II molecules, enhanced phagocytosis, and the ability to activate T cells. Strikingly, EVT-conditioned media convert decPAMs into a decBAM phenotype. These findings assign distinct macrophage phenotypes to decidual areas depending on placentation and further highlight a critical role for EVTs in the induction of decB-associated macrophage polarization.http://www.sciencedirect.com/science/article/pii/S2211124722018812CP: Immunology
spellingShingle Sigrid Vondra
Anna-Lena Höbler
Andreas Ian Lackner
Johanna Raffetseder
Zala Nikita Mihalic
Andrea Vogel
Leila Saleh
Victoria Kunihs
Peter Haslinger
Markus Wahrmann
Heinrich Husslein
Raimund Oberle
Julia Kargl
Sandra Haider
Paulina Latos
Gernot Schabbauer
Martin Knöfler
Jan Ernerudh
Jürgen Pollheimer
The human placenta shapes the phenotype of decidual macrophages
Cell Reports
CP: Immunology
title The human placenta shapes the phenotype of decidual macrophages
title_full The human placenta shapes the phenotype of decidual macrophages
title_fullStr The human placenta shapes the phenotype of decidual macrophages
title_full_unstemmed The human placenta shapes the phenotype of decidual macrophages
title_short The human placenta shapes the phenotype of decidual macrophages
title_sort human placenta shapes the phenotype of decidual macrophages
topic CP: Immunology
url http://www.sciencedirect.com/science/article/pii/S2211124722018812
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