Fibrinoid-associated neutrophils promote invasive placentation and neutrophil reprogramming at the maternal-fetal interface

Successful early pregnancy depends on coordinated interactions between the placenta and maternal immune cells, but the mechanisms underlying this interplay remain incompletely understood. Placenta-derived extravillous trophoblasts (EVTs) invade the decidua basalis and remodel maternal vessels, yet the contribution of neutrophils to this process is unclear. Here, we analyzed first-trimester human decidual tissue together with blood samples and identified decidual fibrinoid-associated neutrophils (dFANs) localized to Rohr’s layer, a fibrinoid matrix between the decidua proper and the intervillous space. Flow cytometry and mass cytometry showed that dFANs differ phenotypically from donor-matched peripheral blood neutrophils (PBNs). Functionally, dFANs secreted high levels of matrix metalloproteinase-9 (MMP-9) and promoted EVT invasion, whereas PBNs induced EVT apoptosis. dFAN-derived MMP-9 enhanced activation of latent transforming growth factor-β (TGF-β), which suppressed PBN cytotoxicity and shifted PBNs toward an MMP-9–hypersecretory, proinvasive state. These findings define a dFAN-dependent MMP-9–TGF-β axis that supports invasive placentation at the maternal-fetal interface.

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Journal
Science Immunology
Published
2026-09-25
DOI
https://doi.org/10.1126/sciimmunol.aea4118
Primary Topic
Pregnancy and preeclampsia studies
Type
article
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article

Fibrinoid-associated neutrophils promote invasive placentation and neutrophil reprogramming at the maternal-fetal interface

Michael R. Angelo, Sandra Haider, Jasmin Wächter, Felix Kosta et al.
Science Immunology
Pregnancy and preeclampsia studies
article

Fibrinoid-associated neutrophils promote invasive placentation and neutrophil reprogramming at the maternal-fetal interface

Michael R. Angelo, Sandra Haider, Jasmin Wächter, Felix Kosta, Andreas Ian Lackner, Trevor Bruce, Anna-Lena Höbler, Gernot Schabbauer, Barbara Öhler, Laszlo Musiejovsky, Sean C. Bendall, Gudrun Meinhardt, Sigrid Vondra, Jürgen Pollheimer, Theresa Maxian, Christian Fiala, Hanna Waldhäusl, Peter Haslinger, Daniel Ho, Patricia M.B. Favaro, Leila Saleh, Martin Knöfler
article en

Abstract

Successful early pregnancy depends on coordinated interactions between the placenta and maternal immune cells, but the mechanisms underlying this interplay remain incompletely understood. Placenta-derived extravillous trophoblasts (EVTs) invade the decidua basalis and remodel maternal vessels, yet the contribution of neutrophils to this process is unclear. Here, we analyzed first-trimester human decidual tissue together with blood samples and identified decidual fibrinoid-associated neutrophils (dFANs) localized to Rohr’s layer, a fibrinoid matrix between the decidua proper and the intervillous space. Flow cytometry and mass cytometry showed that dFANs differ phenotypically from donor-matched peripheral blood neutrophils (PBNs). Functionally, dFANs secreted high levels of matrix metalloproteinase-9 (MMP-9) and promoted EVT invasion, whereas PBNs induced EVT apoptosis. dFAN-derived MMP-9 enhanced activation of latent transforming growth factor-β (TGF-β), which suppressed PBN cytotoxicity and shifted PBNs toward an MMP-9–hypersecretory, proinvasive state. These findings define a dFAN-dependent MMP-9–TGF-β axis that supports invasive placentation at the maternal-fetal interface.

Science ImmunologyVol. 11(123)
Karolinska Institutet (SE), Medical University of Vienna (AT), Stanford University (US)
Good health and well-being
Openalex Percentile: Top 9%
Pregnancy and preeclampsia studies
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