Maternal immune activation by LPS selectively alters specific gene expression profiles of interneuron migration and oxidative stress in the fetus without triggering a fetal immune response
Open accessAbstract
Maternal immune activation (MIA) is a risk factor for the development of schizophrenia and autism. Infections during pregnancy activate the mother's immune system and alter the fetal environment, with consequential effects on CNS function and behavior in the offspring, but the cellular and molecular links between infection-induced altered fetal development and risk for neuropsychiatric disorders are unknown. We investigated the immunological, molecular, and behavioral effects of MIA in the offspring of pregnant Sprague-Dawley rats given an intraperitoneal (0.25 mg/kg) injection of lipopolysaccharide (LPS) on gestational day 15. LPS significantly elevated pro-inflammatory cytokine levels in maternal serum, amniotic fluid, and fetal brain at 4 h, and levels decreased but remained elevated at 24 h. Offspring born to LPS-treated dams exhibited reduced social preference and exploration behaviors as juveniles and young adults. Whole genome microarray analysis of the fetal brain at 4 h post maternal LPS was performed to elucidate the possible molecular mechanisms by which MIA affects the fetal brain. We observed dysregulation of 3285 genes in restricted functional categories, with increased mRNA expression of cellular stress and cell death genes and reduced expression of developmentally-regulated and brain-specific genes, specifically those that regulate neuronal migration of GABAergic interneurons, including the Distal-less (Dlx) family of transcription factors required for tangential migration from progenitor pools within the ganglionic eminences into the cerebral cortex. Our results provide a novel mechanism by which MIA induces the widespread down-regulation of critical neurodevelopmental genes, including those previously associated with autism.
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Gene expression alterations in MIA also involve neuronal migration processes that could underlie observed cortical layering defects, characterized by a 24% increase in neuron numbers in cortical layers II/III.
“Gene expression alterations also involve neuronal migration processes [128] that could underlie observed cortical layering defects, characterized by a 24% increase in neuron numbers in cortical layers II/III [131].”
From The ASD Living Biology: from cell proliferation to clinical phenotype (2019) · cites this paper as [128]
MIA strongly upregulates cell cycle gene expression and cell proliferation, and may cause brain overgrowth.
“MIA strongly upregulates cell cycle gene expression and cell proliferation, and may cause brain overgrowth [127–129].”
From The ASD Living Biology: from cell proliferation to clinical phenotype (2019) · cites this paper as [128]
Both poly(I:C) and LPS affect maternal cytokine signaling (e.g., interleukin-6) that passes through the placenta to affect fetal brain development.
“Both poly(I:C) and LPS affect maternal cytokine signaling (e.g., interleukin-6) that passes through the placenta to affect fetal brain development31”
From Maternal immune activation dysregulation of the fetal brain transcriptome and relevance to the pathophysiology of autism spectrum disorder (2018) · cites this paper as [31]
Maternal infection is a primary environmental risk factor for ASD.
“Maternal infection is a primary environmental risk factor for ASD based on numerous epidemiological, clinical and animal studies (93–98).”
From Emerging Roles for the Gut Microbiome in Autism Spectrum Disorder (2017) · cites this paper as [93]
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The Role of Redox Dysregulation in the Effects of Prenatal Stress on Embryonic Interneuron Migration
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- Authors
- Oskvig, D. B., Elkahloun, A. G., Johnson, K. R., Phillips, T. M., & Herkenham, M.
- Affiliations
- National Institutes of Health (US)
- Corresponding author
- Herkenham, Miles
- Venue
- Brain, Behavior, and Immunity
- Publisher
- Elsevier BV
- Published
- 2012-05
- Volume
- 26
- Issue
- 4
- Pages
- 623-634
- ISSN
- 0889-1591 (ISSN-L)
- PMC
- PMC3285385
- OpenAlex
- W2052297858
- Cited by
- 248
- References
- 117
- Citations by year
- 2026: 13 · 2025: 9 · 2024: 16 · 2023: 22 · 2022: 23 · 2021: 19 · 2020: 21 · 2019: 21 · 2018: 19 · 2017: 15 · 2016: 19 · 2015: 15 · 2014: 14 · 2013: 13 · 2012: 9
- FWCI
- 5.07
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Brain Behavior and Immunity (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health
- National Institute of Mental Health (ZIAMH001090)
- National Human Genome Research Institute (ZICHG200365)
- Topics
- Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- maternal immune activation, lipopolysaccharide, oxidative stress, inflammatory cytokines, autism risk, schizophrenia risk, social behavior, brain development, prenatal infection, cortical development
- MeSH terms
- Amniotic Fluid, Animals, Autistic Disorder, Brain, Cell Movement, Exploratory Behavior, Female, Fetus, Interneurons, Lipopolysaccharides, Pregnancy, Pregnancy Complications, Infectious, Prenatal Exposure Delayed Effects, RNA, Messenger, Social Behavior, Transcription Factors, Down-Regulation, Cytokines, Rats, Sprague-Dawley, Oxidative Stress, Gene Expression Profiling, Rats
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