Pulmonary maternal immune activation does not cross the placenta but leads to fetal metabolic adaptation

Signe Schmidt Kjølner Hansen; Robert Krautz; Daria Rago; Jesper Havelund; Arnaud Stigliani; Nils J. Færgeman; Audrey Prézelin; Julie Rivière; Anne Couturier-Tarrade; Vyacheslav Akimov; Blagoy Blagoev; Betina Elfving; Ditte Neess; Ulla Vogel; Konstantin Khodosevich; Karin Sørig Hougaard; Albin Sandelin

doi:10.1038/s41467-024-48492-x

Pulmonary maternal immune activation does not cross the placenta but leads to fetal metabolic adaptation

Signe Schmidt Kjølner Hansen, Robert Krautz, Daria Rago, Jesper Havelund, Arnaud Stigliani, Nils J. Færgeman, Audrey Prézelin, Julie Rivière, Anne Couturier-Tarrade, Vyacheslav Akimov, Blagoy Blagoev, Betina Elfving, Ditte Neess, Ulla Vogel, Konstantin Khodosevich, Karin Sørig Hougaard, Albin Sandelin

Institut for Klinisk Medicin - Translational Neuropsychiatry Unit

Publikation: Bidrag til tidsskrift/Konferencebidrag i tidsskrift /Bidrag til avis › Tidsskriftartikel › Forskning › peer review

Abstract

The fetal development of organs and functions is vulnerable to perturbation by maternal inflammation which may increase susceptibility to disorders after birth. Because it is not well understood how the placenta and fetus respond to acute lung- inflammation, we characterize the response to maternal pulmonary lipopolysaccharide exposure across 24 h in maternal and fetal organs using multi-omics, imaging and integrative analyses. Unlike maternal organs, which mount strong inflammatory immune responses, the placenta upregulates immuno-modulatory genes, in particular the IL-6 signaling suppressor Socs3. Similarly, we observe no immune response in the fetal liver, which instead displays metabolic changes, including increases in lipids containing docosahexaenoic acid, crucial for fetal brain development. The maternal liver and plasma display similar metabolic alterations, potentially increasing bioavailability of docosahexaenoic acid for the mother and fetus. Thus, our integrated temporal analysis shows that systemic inflammation in the mother leads to a metabolic perturbation in the fetus.

Originalsprog	Engelsk
Artikelnummer	4711
Tidsskrift	Nature Communications
Vol/bind	15
Nummer	1
Sider (fra-til)	4711
Antal sider	1
ISSN	2041-1723
DOI	https://doi.org/10.1038/s41467-024-48492-x
Status	Udgivet - jun. 2024

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10.1038/s41467-024-48492-xLicens: CC BY

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Hansen, S. S. K., Krautz, R., Rago, D., Havelund, J., Stigliani, A., Færgeman, N. J., Prézelin, A., Rivière, J., Couturier-Tarrade, A., Akimov, V., Blagoev, B., Elfving, B., Neess, D., Vogel, U., Khodosevich, K., Hougaard, K. S., & Sandelin, A. (2024). Pulmonary maternal immune activation does not cross the placenta but leads to fetal metabolic adaptation. Nature Communications, 15(1), 4711. Artikel 4711. https://doi.org/10.1038/s41467-024-48492-x

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title = "Pulmonary maternal immune activation does not cross the placenta but leads to fetal metabolic adaptation",

abstract = "The fetal development of organs and functions is vulnerable to perturbation by maternal inflammation which may increase susceptibility to disorders after birth. Because it is not well understood how the placenta and fetus respond to acute lung- inflammation, we characterize the response to maternal pulmonary lipopolysaccharide exposure across 24 h in maternal and fetal organs using multi-omics, imaging and integrative analyses. Unlike maternal organs, which mount strong inflammatory immune responses, the placenta upregulates immuno-modulatory genes, in particular the IL-6 signaling suppressor Socs3. Similarly, we observe no immune response in the fetal liver, which instead displays metabolic changes, including increases in lipids containing docosahexaenoic acid, crucial for fetal brain development. The maternal liver and plasma display similar metabolic alterations, potentially increasing bioavailability of docosahexaenoic acid for the mother and fetus. Thus, our integrated temporal analysis shows that systemic inflammation in the mother leads to a metabolic perturbation in the fetus.",

author = "Hansen, {Signe Schmidt Kj{\o}lner} and Robert Krautz and Daria Rago and Jesper Havelund and Arnaud Stigliani and F{\ae}rgeman, {Nils J.} and Audrey Pr{\'e}zelin and Julie Rivi{\`e}re and Anne Couturier-Tarrade and Vyacheslav Akimov and Blagoy Blagoev and Betina Elfving and Ditte Neess and Ulla Vogel and Konstantin Khodosevich and Hougaard, {Karin S{\o}rig} and Albin Sandelin",

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year = "2024",

month = jun,

doi = "10.1038/s41467-024-48492-x",

language = "English",

volume = "15",

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Hansen, SSK, Krautz, R, Rago, D, Havelund, J, Stigliani, A, Færgeman, NJ, Prézelin, A, Rivière, J, Couturier-Tarrade, A, Akimov, V, Blagoev, B, Elfving, B, Neess, D, Vogel, U, Khodosevich, K, Hougaard, KS & Sandelin, A 2024, 'Pulmonary maternal immune activation does not cross the placenta but leads to fetal metabolic adaptation', Nature Communications, bind 15, nr. 1, 4711, s. 4711. https://doi.org/10.1038/s41467-024-48492-x

Pulmonary maternal immune activation does not cross the placenta but leads to fetal metabolic adaptation. / Hansen, Signe Schmidt Kjølner; Krautz, Robert; Rago, Daria et al.
I: Nature Communications, Bind 15, Nr. 1, 4711, 06.2024, s. 4711.

Publikation: Bidrag til tidsskrift/Konferencebidrag i tidsskrift /Bidrag til avis › Tidsskriftartikel › Forskning › peer review

TY - JOUR

T1 - Pulmonary maternal immune activation does not cross the placenta but leads to fetal metabolic adaptation

AU - Hansen, Signe Schmidt Kjølner

AU - Krautz, Robert

AU - Rago, Daria

AU - Havelund, Jesper

AU - Stigliani, Arnaud

AU - Færgeman, Nils J.

AU - Prézelin, Audrey

AU - Rivière, Julie

AU - Couturier-Tarrade, Anne

AU - Akimov, Vyacheslav

AU - Blagoev, Blagoy

AU - Elfving, Betina

AU - Neess, Ditte

AU - Vogel, Ulla

AU - Khodosevich, Konstantin

AU - Hougaard, Karin Sørig

AU - Sandelin, Albin

PY - 2024/6

Y1 - 2024/6

N2 - The fetal development of organs and functions is vulnerable to perturbation by maternal inflammation which may increase susceptibility to disorders after birth. Because it is not well understood how the placenta and fetus respond to acute lung- inflammation, we characterize the response to maternal pulmonary lipopolysaccharide exposure across 24 h in maternal and fetal organs using multi-omics, imaging and integrative analyses. Unlike maternal organs, which mount strong inflammatory immune responses, the placenta upregulates immuno-modulatory genes, in particular the IL-6 signaling suppressor Socs3. Similarly, we observe no immune response in the fetal liver, which instead displays metabolic changes, including increases in lipids containing docosahexaenoic acid, crucial for fetal brain development. The maternal liver and plasma display similar metabolic alterations, potentially increasing bioavailability of docosahexaenoic acid for the mother and fetus. Thus, our integrated temporal analysis shows that systemic inflammation in the mother leads to a metabolic perturbation in the fetus.

AB - The fetal development of organs and functions is vulnerable to perturbation by maternal inflammation which may increase susceptibility to disorders after birth. Because it is not well understood how the placenta and fetus respond to acute lung- inflammation, we characterize the response to maternal pulmonary lipopolysaccharide exposure across 24 h in maternal and fetal organs using multi-omics, imaging and integrative analyses. Unlike maternal organs, which mount strong inflammatory immune responses, the placenta upregulates immuno-modulatory genes, in particular the IL-6 signaling suppressor Socs3. Similarly, we observe no immune response in the fetal liver, which instead displays metabolic changes, including increases in lipids containing docosahexaenoic acid, crucial for fetal brain development. The maternal liver and plasma display similar metabolic alterations, potentially increasing bioavailability of docosahexaenoic acid for the mother and fetus. Thus, our integrated temporal analysis shows that systemic inflammation in the mother leads to a metabolic perturbation in the fetus.

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DO - 10.1038/s41467-024-48492-x

M3 - Journal article

C2 - 38830841

AN - SCOPUS:85195014674

SN - 2041-1723

VL - 15

SP - 4711

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 4711

ER -

Pulmonary maternal immune activation does not cross the placenta but leads to fetal metabolic adaptation

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