Cited by 264Tryptophan and brain disordersNeuroinflammation and Neurodegeneration MechanismsMaternal Mental Health During Pregnancy and Postpartum

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Maternal Inflammation Disrupts Fetal Neurodevelopment via Increased Placental Output of Serotonin to the Fetal Brain

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Goeden, Nick, Velasquez, Juan, Arnold, Kathryn A., Chan, Yen, Lund, Brett T., Anderson, George M., Bonnin, Alexandre·2016·The Journal of Neuroscience

DOI 10.1523/jneurosci.2534-15.2016PMC PMC4887568

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Abstract

UNLABELLED: Maternal inflammation during pregnancy affects placental function and is associated with increased risk of neurodevelopmental disorders in the offspring. The molecular mechanisms linking placental dysfunction to abnormal fetal neurodevelopment remain unclear. During typical development, serotonin (5-HT) synthesized in the placenta from maternal l-tryptophan (TRP) reaches the fetal brain. There, 5-HT modulates critical neurodevelopmental processes. We investigated the effects of maternal inflammation triggered in midpregnancy in mice by the immunostimulant polyriboinosinic-polyribocytidylic acid [poly(I:C)] on TRP metabolism in the placenta and its impact on fetal neurodevelopment. We show that a moderate maternal immune challenge upregulates placental TRP conversion rapidly to 5-HT through successively transient increases in substrate availability and TRP hydroxylase (TPH) enzymatic activity, leading to accumulation of exogenous 5-HT and blunting of endogenous 5-HT axonal outgrowth specifically within the fetal forebrain. The pharmacological inhibition of TPH activity blocked these effects. These results establish altered placental TRP conversion to 5-HT as a new mechanism by which maternal inflammation disrupts 5-HT-dependent neurogenic processes during fetal neurodevelopment. SIGNIFICANCE STATEMENT: The mechanisms linking maternal inflammation during pregnancy with increased risk of neurodevelopmental disorders in the offspring are poorly understood. In this study, we show that maternal inflammation in midpregnancy results in an upregulation of tryptophan conversion to serotonin (5-HT) within the placenta. Remarkably, this leads to exposure of the fetal forebrain to increased concentrations of this biogenic amine and to specific alterations of crucially important 5-HT-dependent neurogenic processes. More specifically, we found altered serotonergic axon growth resulting from increased 5-HT in the fetal forebrain. The data provide a new understanding of placental function playing a key role in fetal brain development and how this process is altered by adverse prenatal events such as maternal inflammation. The results uncover important future directions for understanding the early developmental origins of mental disorders.

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Authors: Goeden, N., Velasquez, J., Arnold, K. A., Chan, Y., Lund, B. T., Anderson, G. M., & Bonnin, A.
Affiliations: University of Southern California (US)
Yale University (US)
ORCID: Arnold, Kathryn A.
Lund, Brett T.
Anderson, George M.
Bonnin, Alexandre
Venue: The Journal of Neuroscience
Publisher: Society for Neuroscience
Published: 2016-06-01
Volume: 36
Issue: 22
Pages: 6041-6049
ISSN: 0270-6474 (ISSN-L)
1529-2401
DOI: 10.1523/jneurosci.2534-15.2016
PMC: PMC4887568
OpenAlex: W2409273775
Cited by: 264
References: 48
Citations by year: 2026: 16 · 2025: 28 · 2024: 25 · 2023: 32 · 2022: 31 · 2021: 36 · 2020: 30 · 2019: 20 · 2018: 29 · 2017: 13 · 2016: 4
FWCI: 7.51
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-sa
creativecommons.org/licenses/by-nc-sa/4.0/ (vor, 183 d)
Locations: Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: U.S. Department of Defense
University of Southern California
Autism Science Foundation
Rose Hills Foundation
National Institute of Mental Health (P50MH103222, P50MH096972)
Eunice Kennedy Shriver National Institute of Child Health and Human Development (R21HD065287)
Topics: Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Maternal Mental Health During Pregnancy and Postpartum
Keywords: maternal inflammation, fetal brain development, placenta, serotonin, tryptophan metabolism, tryptophan hydroxylase, poly(I:C), neurodevelopmental disorders, placental insufficiency, prenatal immune challenge
MeSH terms: Animals, Brain, Disease Models, Animal, Female, Fetal Diseases, 5-Hydroxytryptophan, Inflammation, Fenclonine, Placenta, Polydeoxyribonucleotides, Pregnancy, Prenatal Exposure Delayed Effects, Serotonin, Serotonin Antagonists, Cytokines, Gene Expression Regulation, Developmental, Statistics, Nonparametric, Fetal Development, Mice

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Maternal Inflammation Disrupts Fetal Neurodevelopment via Increased Placental Output of Serotonin to the Fetal Brain

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