Alterations in the placental proteome in association with the presence of black carbon particles: a discovery study.

black carbon particles exposome mass spectrometry placental proteome prenatal air pollution exposure

Journal

Environmental research
ISSN: 1096-0953
Titre abrégé: Environ Res
Pays: Netherlands
ID NLM: 0147621

Informations de publication

Date de publication:
21 Oct 2024
Historique:
received: 10 07 2024
revised: 18 10 2024
accepted: 21 10 2024
medline: 24 10 2024
pubmed: 24 10 2024
entrez: 23 10 2024
Statut: aheadofprint

Résumé

Exposure to ambient air pollution is known to cause direct and indirect molecular expression changes in the placenta, on the DNA, mRNA, and protein levels. Ambient black carbon (BC) particles can be found in the human placenta already very early in gestation. However, the effect of in utero BC exposure on the entire placental proteome has never been studied to date. We explored whether placental proteome differs between mothers exposed to either high or low BC levels throughout the entire pregnancy. We used placental tissue samples from the ENVIRONAGE birth cohort, of 20 non-smoking, maternal- and neonate characteristic-matched women exposed to high (n=10) or low (n=10) levels of ambient BC throughout pregnancy. We modeled prenatal BC exposure levels based on the mother's home address and measured BC levels in the fetal side of the placenta. The placental proteome was analyzed by nano-liquid chromatography Q-TOF mass spectrometry. PEAKS software was used for protein identification and label-free quantification. Protein-protein interaction and functional pathway enrichment analyses were performed with the Search Tool for the Retrieval of Interacting Genes/Proteins (STRING) software. The accumulation of BC particles in placenta was 2.19 times higher in the high versus low exposure group (20943.4 vs 9542.7 particles/mm³; p=0.007). Thirteen proteins showed a ≥ 2-fold expression difference between the two exposure groups, all overexpressed in the placentas of women prenatally exposed to high BC levels. Three protein-protein interactions were enriched within this group, namely between TIMP3 and COL4A2, SERPINE2 and COL4A2, and SERPINE2 and GP1BB. Functional pathway enrichment analysis put forward pathways involved in extracellular matrix-receptor interaction, fibrin clot formation, and sodium ion transport regulation. Prenatal BC exposure affects the placental proteome. Future research should focus on the potential consequences of these alterations on placental functioning, and health and disease during early childhood development.

Sections du résumé

BACKGROUND BACKGROUND
Exposure to ambient air pollution is known to cause direct and indirect molecular expression changes in the placenta, on the DNA, mRNA, and protein levels. Ambient black carbon (BC) particles can be found in the human placenta already very early in gestation. However, the effect of in utero BC exposure on the entire placental proteome has never been studied to date.
OBJECTIVES OBJECTIVE
We explored whether placental proteome differs between mothers exposed to either high or low BC levels throughout the entire pregnancy.
METHODS METHODS
We used placental tissue samples from the ENVIRONAGE birth cohort, of 20 non-smoking, maternal- and neonate characteristic-matched women exposed to high (n=10) or low (n=10) levels of ambient BC throughout pregnancy. We modeled prenatal BC exposure levels based on the mother's home address and measured BC levels in the fetal side of the placenta. The placental proteome was analyzed by nano-liquid chromatography Q-TOF mass spectrometry. PEAKS software was used for protein identification and label-free quantification. Protein-protein interaction and functional pathway enrichment analyses were performed with the Search Tool for the Retrieval of Interacting Genes/Proteins (STRING) software.
RESULTS RESULTS
The accumulation of BC particles in placenta was 2.19 times higher in the high versus low exposure group (20943.4 vs 9542.7 particles/mm³; p=0.007). Thirteen proteins showed a ≥ 2-fold expression difference between the two exposure groups, all overexpressed in the placentas of women prenatally exposed to high BC levels. Three protein-protein interactions were enriched within this group, namely between TIMP3 and COL4A2, SERPINE2 and COL4A2, and SERPINE2 and GP1BB. Functional pathway enrichment analysis put forward pathways involved in extracellular matrix-receptor interaction, fibrin clot formation, and sodium ion transport regulation.
DISCUSSION CONCLUSIONS
Prenatal BC exposure affects the placental proteome. Future research should focus on the potential consequences of these alterations on placental functioning, and health and disease during early childhood development.

Identifiants

pubmed: 39442658
pii: S0013-9351(24)02121-2
doi: 10.1016/j.envres.2024.120214
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

120214

Informations de copyright

Copyright © 2024. Published by Elsevier Inc.

Déclaration de conflit d'intérêts

Declaration of Competing Interest ☐ The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. ☒ The authors declare the following financial interests/personal relationships which may be considered as potential competing interests: Tim S. Nawrot has patent "Method for detecting or quantifying carbon black and/or black carbon particles" issued to Katholieke Universiteit Leuven, Universiteit Hasselt. If there are other authors, they declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Auteurs

Joline L Millen (JL)

Unité de Recherche en Biologie Cellulaire (URBC) - Namur Research Institute for Life Sciences (Narilis), University of Namur (UNamur), Namur, Belgium; Centre for Environmental Sciences, Hasselt University (UHasselt), Diepenbeek, Belgium.

Leen J Luyten (LJ)

Unité de Recherche en Biologie Cellulaire (URBC) - Namur Research Institute for Life Sciences (Narilis), University of Namur (UNamur), Namur, Belgium; Centre for Environmental Sciences, Hasselt University (UHasselt), Diepenbeek, Belgium.

Marc Dieu (M)

Unité de Recherche en Biologie Cellulaire (URBC) - Namur Research Institute for Life Sciences (Narilis), University of Namur (UNamur), Namur, Belgium; MaSUN, Mass Spectrometry Facility, University of Namur (UNamur), Namur, Belgium.

Hannelore Bové (H)

Centre for Environmental Sciences, Hasselt University (UHasselt), Diepenbeek, Belgium.

Marcel Ameloot (M)

Biomedical Research Institute, Hasselt University (UHasselt), Diepenbeek, Belgium.

Eva Bongaerts (E)

Centre for Environmental Sciences, Hasselt University (UHasselt), Diepenbeek, Belgium.

Catherine Demazy (C)

Unité de Recherche en Biologie Cellulaire (URBC) - Namur Research Institute for Life Sciences (Narilis), University of Namur (UNamur), Namur, Belgium; MaSUN, Mass Spectrometry Facility, University of Namur (UNamur), Namur, Belgium.

Maude Fransolet (M)

Unité de Recherche en Biologie Cellulaire (URBC) - Namur Research Institute for Life Sciences (Narilis), University of Namur (UNamur), Namur, Belgium; MaSUN, Mass Spectrometry Facility, University of Namur (UNamur), Namur, Belgium.

Dries S Martens (DS)

Centre for Environmental Sciences, Hasselt University (UHasselt), Diepenbeek, Belgium.

Patricia Renard (P)

Unité de Recherche en Biologie Cellulaire (URBC) - Namur Research Institute for Life Sciences (Narilis), University of Namur (UNamur), Namur, Belgium; MaSUN, Mass Spectrometry Facility, University of Namur (UNamur), Namur, Belgium.

Brigitte Reimann (B)

Centre for Environmental Sciences, Hasselt University (UHasselt), Diepenbeek, Belgium.

Michelle Plusquin (M)

Centre for Environmental Sciences, Hasselt University (UHasselt), Diepenbeek, Belgium.

Tim S Nawrot (TS)

Centre for Environmental Sciences, Hasselt University (UHasselt), Diepenbeek, Belgium; Department of Public Health & Primary Care, Occupational and Environmental Medicine, Leuven University (KULeuven), Leuven, Belgium. Electronic address: tim.nawrot@uhasselt.be.

Florence Debacq-Chainiaux (F)

Unité de Recherche en Biologie Cellulaire (URBC) - Namur Research Institute for Life Sciences (Narilis), University of Namur (UNamur), Namur, Belgium.

Classifications MeSH