Sex-Specific Neurodevelopmental Programming by Placental Insulin Receptors on Stress Reactivity and Sensorimotor Gating
Open accessAbstract
Background Diabetes, obesity, and overweight are prevalent pregnancy complications that predispose offspring to neurodevelopmental disorders, including autism, attention-deficit/hyperactivity disorder, and schizophrenia. Although male individuals are three to four times more likely than female individuals to develop these disorders, the mechanisms driving the sex specificity of disease vulnerability remain unclear. Because defective placental insulin receptor (InsR) signaling is a hallmark of pregnancy metabolic dysfunction, we hypothesized that it may be an important contributor and novel mechanistic link to sex-specific neurodevelopmental changes underlying disease risk.Methods We used Cre/loxP transgenic mice to conditionally target InsRs in fetally derived placental trophoblasts. Adult offspring were evaluated for effects of placental trophoblast-specific InsR deficiency on stress sensitivity, cognitive function, sensorimotor gating, and prefrontal cortical transcriptional reprogramming. To evaluate molecular mechanisms driving sex-specific outcomes, we assessed genome-wide expression profiles in the placenta and fetal brain.Results Male, but not female, mice with placental trophoblast-specific InsR deficiency showed a significantly increased hypothalamic-pituitary-adrenal axis stress response and impaired sensorimotor gating, phenotypic effects that were associated with dysregulated nucleotide metabolic processes in the male prefrontal cortex. Within the placenta, InsR deficiency elicited changes in gene expression, predominantly in male mice, reflecting potential shifts in vasculature, amino acid transport, serotonin homeostasis, and mitochondrial function. These placental disruptions were associated with altered gene expression profiles in the male fetal brain and suggested delayed cortical development.Conclusions Together, these data demonstrate the novel role of placental InsRs in sex-specific neurodevelopment and reveal a potential mechanism for neurodevelopmental disorder risk in pregnancies complicated by maternal metabolic disorders, including diabetes and obesity.
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Maternal metabolic disorders including diabetes and obesity can pose another threat to the unborn child as placental dysfunctioning alters the prenatal exposure to nutrients and toxins.
“Maternal metabolic disorders including diabetes and obesity can pose another threat to the unborn child as placental dysfunctioning alters the prenatal exposure to nutrients and toxins [312–314].”
From Development of prefrontal cortex (2022) · cites this paper as [312]
The Introduction passage labeled “Abstract > CONCLUSIONS” identifies diabetes and obesity as risks to offspring and says the placenta delivers nutrients and maintains a protective barrier. The Discussion links defective placental insulin signaling to adverse fetal outcomes and reports changes in placental nutrient-transport pathways. Our copy does not say that these disorders alter fetal exposure to toxins. (LLM, conf=0.86)
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Wilson, H. A., Creighton, C., Scharfman, H., Choleris, E., & MacLusky, N. J. (2021) · The Neuroscientist · doi:10.1177/1073858420952046 · Cited by 23 · see citing works
- Authors
- Bronson, S. L., Chan, J. C., & Bale, T. L.
- Affiliations
- University of Pennsylvania (US)
- Corresponding author
- Bale, Tracy L.
- Venue
- Biological Psychiatry
- Publisher
- Elsevier BV
- Published
- 2017-07
- Volume
- 82
- Issue
- 2
- Pages
- 127-138
- ISSN
- 0006-3223 (ISSN-L)
- PMC
- PMC5483189
- OpenAlex
- W2565663545
- Cited by
- 49
- References
- 96
- Citations by year
- 2026: 6 · 2025: 7 · 2024: 5 · 2023: 6 · 2022: 3 · 2021: 6 · 2020: 6 · 2019: 3 · 2018: 3 · 2017: 4
- FWCI
- 3.87
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Biological Psychiatry (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Ohio State University
- National Institutes of Health (5r01mh091258-05)
- National Institute of Mental Health (P50MH099910, R37MH108286, R01MH073030, R33MH104184, R01 MH-091258, R21MH104184, R01MH087597)
- National Institute of Diabetes and Digestive and Kidney Diseases (P30DK019525)
- Topics
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Health Sciences › Medicine › Obstetrics and Gynecology › Gestational Diabetes Research and Management
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Maternal Mental Health During Pregnancy and Postpartum
- Keywords
- trophoblast, sex differences, stress reactivity, sensorimotor gating, hypothalamic-pituitary-adrenal axis, prefrontal cortex, nucleotide metabolism, maternal diabetes, maternal obesity, autism spectrum disorder, attention deficit hyperactivity disorder, schizophrenia, fetal brain development, placental gene expression
- MeSH terms
- Animals, Disease Models, Animal, Female, Fetus, Hypothalamo-Hypophyseal System, Mice, Inbred C57BL, Mice, Transgenic, Pituitary-Adrenal System, Placenta, Pregnancy, Receptor, Insulin, Sex Characteristics, Trophoblasts, Prefrontal Cortex, Mice, Sensory Gating, Mice, 129 Strain, Transcriptome, Neurodevelopmental Disorders
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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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