The omniscient placenta: Metabolic and epigenetic regulation of fetal programming

Nugent, Bridget M.; Bale, Tracy L.

doi:10.1016/j.yfrne.2015.09.001

Cited by 222Birth, Development, and HealthEpigenetics and DNA MethylationPregnancy and preeclampsia studies

The omniscient placenta: Metabolic and epigenetic regulation of fetal programming

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Nugent, Bridget M., Bale, Tracy L.·2015·Frontiers in Neuroendocrinology

DOI 10.1016/j.yfrne.2015.09.001PMC PMC4681645

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Abstract

Fetal development could be considered a sensitive period wherein exogenous insults and changes to the maternal milieu can have long-term impacts on developmental programming. The placenta provides the fetus with protection and necessary nutrients for growth, and responds to maternal cues and changes in nutrient signaling through multiple epigenetic mechanisms. The X-linked enzyme O-linked-N-acetylglucosamine transferase (OGT) acts as a nutrient sensor that modifies numerous proteins to alter various cellular signals, including major epigenetic processes. This review describes epigenetic alterations in the placenta in response to insults during pregnancy, the potential links of OGT as a nutrient sensor to placental epigenetics, and the implications of placental epigenetics in long-term neurodevelopmental programming. We describe the role of placental OGT in the sex-specific programming of hypothalamic-pituitary-adrenal (HPA) axis programming deficits by early prenatal stress as an example of how placental signaling can have long-term effects on neurodevelopment.

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In animal models, prenatal stress has been shown to lower expression of 11β-HSD2 mRNA and 11B-HSD2 activity, both of which are associated with increased 11β-HSD2 methylation in the placenta.
“In animal models, prenatal stress has been shown to lower expression of 11β-HSD2 mRNA and 11B-HSD2 activity, both of which are associated with increased 11β-HSD2 methylation in the placenta 140 .”
From Intergenerational transmission of trauma effects: putative role of epigenetic mechanisms (2018) · cites this paper as [140]
Section 6.1 reports that prenatal stress decreases placental 11β-HSD2 mRNA in rats and that reduced expression is associated with increased promoter methylation. It also reports reduced 11β-HSD2 in female mouse placentas, but does not specify reduced enzyme activity or associate an activity measurement with methylation. No page number is available in our copy. (LLM, conf=0.87)
Experimental — accuracy not yet measured
Fetal sex, or trophoblast cells from the embryo reflecting fetal sex, may differentially regulate epigenetic signals in the placenta, leading to differential signaling that feeds back to the offspring.
“The importance of fetal sex, or more specifically, trophoblast cells from the embryo reflecting fetal sex, is that it may differentially regulate epigenetic signals in the placenta, leading to differential signaling that feeds back to the offspring 140”
From Intergenerational transmission of trauma effects: putative role of epigenetic mechanisms (2018) · cites this paper as [140]
The placenta is a central integrative organ because it senses and responds to maternal nutrients, hormones, inflammatory mediators and environmental agents through vascular, transport, endocrine and molecular functions.
“The placenta is a central integrative organ because it senses and responds to maternal nutrients, hormones, inflammatory mediators and environmental agents through vascular, transport, endocrine and molecular functions [140,141,142].”
From Placental Pathophysiology and Developmental Programming of Adult Cardiometabolic Risk: A Narrative Review of Pregnancy Exposures (2026) · cites this paper as [141]
There are many reports of changes in placental DNA methylation and histone proteins in response to environmental cues that have been associated with developmental programming of the offspring.
“Epigenetics is a rapidly expanding field, and there are now many reports of changes in placental DNA methylation and histone proteins in response to environmental cues that have been associated with developmental programming of the offspring (203, 417, 522).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [417]

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Authors: Nugent, B. M., & Bale, T. L.
Affiliations: University of Pennsylvania (US)
Corresponding author: Bale, Tracy L.
ORCID: Nugent, Bridget M.
Bale, Tracy L.
Venue: Frontiers in Neuroendocrinology
Publisher: Elsevier BV
Published: 2015-10
Volume: 39
Pages: 28-37
ISSN: 0091-3022 (ISSN-L)
DOI: 10.1016/j.yfrne.2015.09.001
PMC: PMC4681645
OpenAlex: W1755596772
Cited by: 222
References: 151
Citations by year: 2026: 7 · 2025: 16 · 2024: 15 · 2023: 30 · 2022: 17 · 2021: 35 · 2020: 24 · 2019: 23 · 2018: 30 · 2017: 10 · 2016: 15
FWCI: 2.78
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Frontiers in Neuroendocrinology (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health (5r01mh091258-05)
National Institute of Mental Health (P50MH099910, R37MH108286, MH087597, MH 104184, MH 091258, MH099910, R01MH073030, R33MH104184, MH 108286, R01 MH108286, R01 MH-091258, R21MH104184, R01MH087597)
Topics: Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
Keywords: placenta, fetal programming, epigenetics, O-GlcNAc transferase, nutrient sensing, prenatal stress, hypothalamic-pituitary-adrenal axis, brain development, sex differences, maternal nutrition, developmental origins of health and disease
MeSH terms: Adult, Animals, Female, Fetus, Humans, Placenta, Pregnancy, Epigenesis, Genetic, Fetal Development

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The omniscient placenta: Metabolic and epigenetic regulation of fetal programming

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