Prenatal Stress-Induced Increases in Placental Inflammation and Offspring Hyperactivity Are Male-Specific and Ameliorated by Maternal Antiinflammatory Treatment
Open accessAbstract
Adverse experiences during gestation such as maternal stress and infection are known risk factors for neurodevelopmental disorders, including schizophrenia, autism, and attention deficit/hyperactivity disorder. The mechanisms by which these distinct exposures may confer similar psychiatric vulnerability remain unclear, although likely involve pathways common to both stress and immune responses at the maternal-fetal interface. We hypothesized that maternal stress-induced activation of immune pathways within the placenta, the sex-specific maternal-fetal intermediary, may contribute to prenatal stress programming effects on the offspring. Therefore, we assessed for markers indicative of stress-induced placental inflammation, and examined the ability of maternal nonsteroidal antiinflammatory drug (NSAID) treatment to ameliorate placental effects and thereby rescue the stress-dysregulation phenotype observed in our established mouse model of early prenatal stress (EPS). As expected, placental gene expression analyses revealed increased levels of immune response genes, including the proinflammatory cytokines IL-6 and IL-1β, specifically in male placentas. NSAID treatment partially ameliorated these EPS effects. Similarly, in adult offspring, males displayed stress-induced locomotor hyperactivity, a hallmark of dopaminergic dysregulation, which was ameliorated by maternal NSAID treatment. Fitting with these outcomes and supportive of dopamine pathway involvement, expression of dopamine D1 and D2 receptors was altered by EPS in males. These studies support an important interaction between maternal stress and a proinflammatory state in the long-term programming effects of maternal stress.
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Recent evidence from human and animal studies suggests that under stress, placental transfer of nutrients to the fetus is disrupted, and factors such as prenatal stress and placental inflammation increase hyperactivity in offspring.
“Recent evidence from human and animal studies suggests that under stress, placental transfer of nutrients to the fetus is disrupted, and factors such as prenatal stress and placental inflammation increase hyperactivity in offspring3536.”
From Fetal and postnatal metal dysregulation in autism (2017) · cites this paper as [35]
Prenatal stress-induced inflammation caused locomotor hyperactivity in a novel stressful environment in male but not female mouse offspring.
“male, but not female, mouse offspring exposed to inflammation induced by prenatal stress exhibited locomotor hyperactivity in a novel, stressful environment.”
From Neuroinflammation as a risk factor for attention deficit hyperactivity disorder (2019) · cites this paper as Bronson and Bale, 2014
The locomotor hyperactivity phenotype from prenatal stress was associated with alterations in D1 and D2 receptors.
“was associated with alterations in D1 and D2 receptors (Bronson and Bale, 2014).”
From Neuroinflammation as a risk factor for attention deficit hyperactivity disorder (2019) · cites this paper as Bronson and Bale, 2014
The locomotor hyperactivity phenotype from prenatal stress was ameliorated by maternal NSAID treatment.
“This behavioral phenotype was ameliorated by treatment of the mother with non-steroidal anti-inflammatory drugs”
From Neuroinflammation as a risk factor for attention deficit hyperactivity disorder (2019) · cites this paper as Bronson and Bale, 2014
Maternal NSAID administration ameliorated behaviors associated with dopamine dysregulation.
“administration of maternal non-steroidal anti-inflammatory drugs resulted in amelioration of behaviors associated with dopamine dysregulation (Bronson and Bale, 2014).”
From Neuroinflammation as a risk factor for attention deficit hyperactivity disorder (2019) · cites this paper as Bronson and Bale, 2014
Maternal stress-induced inflammation produced behaviors related to ADHD.
“a model of maternal stress-induced inflammation that produced behaviors related to ADHD.”
From Neuroinflammation as a risk factor for attention deficit hyperactivity disorder (2019) · cites this paper as Bronson and Bale, 2014
Altered expression of D1 and D2 dopamine transporters was observed in male offspring.
“This study also observed altered expression of the D1 and D2 dopamine transporters in male offspring”
From Neuroinflammation as a risk factor for attention deficit hyperactivity disorder (2019) · cites this paper as Bronson and Bale, 2014
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- Authors
- Bronson, S. L., & Bale, T. L.
- Affiliations
- University of Pennsylvania (US)
- Corresponding author
- Bale, Tracy L.
- ORCID
- Bale, Tracy L.
- Venue
- Endocrinology
- Publisher
- The Endocrine Society
- Published
- 2014-07-01
- Volume
- 155
- Issue
- 7
- Pages
- 2635-2646
- ISSN
- 0013-7227 (ISSN-L)
- 1945-7170
- PMC
- PMC4060181
- OpenAlex
- W2050044795
- Cited by
- 299
- References
- 103
- Citations by year
- 2026: 14 · 2025: 21 · 2024: 22 · 2023: 31 · 2022: 24 · 2021: 37 · 2020: 35 · 2019: 29 · 2018: 23 · 2017: 18 · 2016: 19 · 2015: 24 · 2014: 2
- FWCI
- 10.31
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Endocrinology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r01mh091258-05)
- National Institute of Mental Health (P50MH099910, MH087597, R01MH073030, R01 MH-091258, R01MH087597)
- National Institute of Diabetes and Digestive and Kidney Diseases (P30DK019525)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Maternal Mental Health During Pregnancy and Postpartum
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Keywords
- prenatal stress, placental inflammation, sex differences, maternal-fetal interface, nonsteroidal anti-inflammatory drugs, interleukin-6, IL-1β, dopamine D1 receptor, dopamine D2 receptor, dopaminergic dysfunction, neurodevelopmental disorders, attention deficit hyperactivity disorder, developmental programming, mouse model
- MeSH terms
- Animals, Anti-Inflammatory Agents, Non-Steroidal, Brain, Female, Humans, Male, Mice, Inbred C57BL, Motor Activity, Placenta, Pregnancy, Prenatal Exposure Delayed Effects, Sex Factors, Stress, Psychological, Tyrosine 3-Monooxygenase, Blotting, Western, Interleukin-6, Gene Expression, Receptors, Dopamine D1, Receptors, Dopamine D2, Maze Learning, Reverse Transcriptase Polymerase Chain Reaction, Mice, Interleukin-1beta
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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