The Transcription Factor Nerve Growth Factor-Inducible Protein A Mediates Epigenetic Programming: Altering Epigenetic Marks by Immediate-Early Genes
Open accessAbstract
Maternal care alters epigenetic programming of glucocorticoid receptor (GR) gene expression in the hippocampus, and increased postnatal maternal licking/grooming (LG) behavior enhances nerve growth factor-inducible protein A (NGFI-A) transcription factor binding to the exon 1 7 GR promoter within the hippocampus of the offspring. We tested the hypothesis that NGFI-A binding to the exon 1 7 GR promoter sequence marks this sequence for histone acetylation and DNA demethylation and that such epigenetic alterations subsequently influence NGFI-A binding and GR transcription. We report that (1) NGFI-A binding to its consensus sequence is inhibited by DNA methylation, (2) NGFI-A induces the activity of exon 1 7 GR promoter in a transient reporter assay, (3) DNA methylation inhibits exon 1 7 GR promoter activity, and (4) whereas NGFI-A interaction with the methylated exon 1 7 GR promoter is reduced, NGFI-A overexpression induces histone acetylation, DNA demethylation, and activation of the exon 1 7 GR promoter in transient transfection assays. Site-directed mutagenesis assays demonstrate that NGFI-A binding to the exon 1 7 GR promoter is required for such epigenetic reprogramming.In vivo, enhanced maternal LG is associated with increased NGFI-A binding to the exon 1 7 GR promoter in the hippocampus of pups, and NGFI-A-bound exon 1 7 GR promoter is unmethylated compared with unbound exon 1 7 GR promoter. Knockdown experiments of NGFI-A in hippocampal primary cell culture show that NGFI-A is required for serotonin-induced DNA demethylation and increased exon 1 7 GR promoter expression. The data are consistent with the hypothesis that NGFI-A participates in epigenetic programming of GR expression.
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Most studies focused on the promoter region of NR3C1 exon 1F, which includes binding sites for NGFI-A that regulate NR3C1 gene expression.
“Most studies focused on the promoter region of exon 1 F , a particularly interesting genomic region since it includes binding sites for the nerve growth factor-inducible protein A (NGFI-A), which regulate NR3C1 gene expression (Weaver et al., 2007)”
From The applied implications of epigenetics in anxiety, affective and stress-related disorders - A review and synthesis on psychosocial stress, psychotherapy and prevention (2020) · cites this paper as Weaver et al., 2007
The section “Transcriptional activation from exon 1 7 GR promoter requires NGFI-A binding” reports that blocking NGFI-A binding abolished its effect on promoter-driven expression. However, the Methods identify the tested sequence as the rat exon 1₇ GR promoter, not the cited sentence’s NR3C1 exon 1F promoter. The paper therefore supports the regulatory mechanism, but not its assignment to exon 1F. (LLM, conf=0.84)
Experimental — accuracy not yet measuredIn cultured hippocampal neurons, the effect of 5-HT on GR expression is blocked by 5-HT7 antagonists or PKA inhibitors, mimicked by 5-HT7 agonists or cAMP analogs, and eliminated by NGFI-A knockdown.
“In cultured hippocampal neurons the effect of 5-HT on GR expression is: (i) blocked by 5-HT7 receptor antagonists or inhibitors of protein kinase A; (ii) mimicked by 5-HT7 receptor agonists or treatments with stable cAMP analogs; and (iii) eliminated by antisense or small interfering RNA (siRNA) knockdown of NGFI-A mRNA.82,83”
From Early life adversity and the epigenetic programming of hypothalamic-pituitary-adrenal function (2014) · cites this paper as [83]
In vitro, 5-HT acts through a 5-HT7 receptor to increase cAMP-dependent signaling in hippocampal neurons, resulting in elevated NGFI-A expression.
“In vitro, 5-HT acts through a 5-HT7 receptor to increase the activity of cyclic adenosine monophosphate (cAMP)-dependent signaling pathways in hippocampal neurons, resulting in elevated expression of NGFI-A.”
From Early life adversity and the epigenetic programming of hypothalamic-pituitary-adrenal function (2014) · cites this paper as [83]
The effect of NGFI-A is eliminated by a site-directed mutation within the NGFI-A response element of the exon 17 promoter, revealing that physical interaction of NGFI-A with its response element triggers increased transcriptional activity.
“The effect of NGFI-A is eliminated by a site-directed mutation within the NGFI-A response element of the exon 17 promoter83 revealing that it is the physical interaction of NGFI-A with its response element that triggers the increase in transcriptional activity.”
From Early life adversity and the epigenetic programming of hypothalamic-pituitary-adrenal function (2014) · cites this paper as [83]
T3 administration in the neonatal period mimics the effects of increased pup LG on NGFI-A expression and hippocampal GR programming.
“T3 administration in neonatal period, which regulates the 5-HT systems activity, mimics the effects of increased pup LG on both NGFI-A expression and hippocampal GR programming.82-84”
From Early life adversity and the epigenetic programming of hypothalamic-pituitary-adrenal function (2014) · cites this paper as [83]
Pup LG increases hippocampal NGFI-A expression and binding to the exon 17 promoter.
“Pup LG increases hippocampal NGFI-A expression and binding to the exon 17 promoter.70,82,83”
From Early life adversity and the epigenetic programming of hypothalamic-pituitary-adrenal function (2014) · cites this paper as [83]
There is increased H3K9ac of the exon 17 GR promoter in hippocampus from adult offspring of High compared with Low LG mothers.
“H3K9ac associates with increased transcription and we found increased H3K9ac of the exon 17 GR promoter in hippocampus from the adult offspring of High compared with Low LG mothers.70,83,92”
From Early life adversity and the epigenetic programming of hypothalamic-pituitary-adrenal function (2014) · cites this paper as [83]
Co-transfection of an NGFI-A vector and an exon 17-luciferase construct increases luciferase activity, reflecting NGFI-A-induced activation of transcription through the exon 17 promoter.
“Co-transfection of an NGFI-A vector and an exon 17 - luciferase construct shows increased luciferase activity, reflecting NGFI-A-induced activation of transcription through the exon 17 promoter.82,83”
From Early life adversity and the epigenetic programming of hypothalamic-pituitary-adrenal function (2014) · cites this paper as [83]
Increased pup LG enhances hippocampal expression of GR mRNA splice variants containing exon 17 sequence, which contains an NGFI-A response element.
“Increased pup LG enhances hippocampal expression of GR mRNA splice variants containing exon 17 sequence,70,82,83,86 which contains an NGFI-A response element.”
From Early life adversity and the epigenetic programming of hypothalamic-pituitary-adrenal function (2014) · cites this paper as [83]
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- Authors
- Weaver, I. C. G., D'Alessio, A. C., Brown, S. E., Hellstrom, I. C., Dymov, S., Sharma, S., Szyf, M., & Meaney, M. J.
- Affiliations
- Douglas Mental Health University Institute (CA)
- McGill University (CA)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2007-02-14
- Volume
- 27
- Issue
- 7
- Pages
- 1756-1768
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC2951014
- OpenAlex
- W1994674729
- Cited by
- 508
- References
- 9
- Citations by year
- 2026: 9 · 2025: 6 · 2024: 9 · 2023: 6 · 2022: 40 · 2021: 16 · 2020: 24 · 2019: 13 · 2018: 20 · 2017: 23 · 2016: 21 · 2015: 26 · 2014: 54 · 2013: 31 · 2012: 46
- FWCI
- 16.68
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- Canadian Institutes of Health Research
- National Cancer Institute
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD051897, HD-051897)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Keywords
- NGFI-A, glucocorticoid receptor, epigenetic programming, DNA methylation, histone acetylation, maternal care, hippocampus, transcription factor binding, serotonin, immediate early genes, glucocorticoid receptor expression
- MeSH terms
- Animals, Behavior, Animal, Cells, Cultured, Chromosome Mapping, Embryo, Mammalian, Exons, Female, Gene Expression Regulation, Hippocampus, Humans, Male, Maternal Behavior, Promoter Regions, Genetic, Protein Binding, Receptors, Glucocorticoid, Serotonin, Transfection, Genes, Immediate-Early, DNA Methylation, Rats, Long-Evans, Electrophoretic Mobility Shift Assay, Epigenesis, Genetic, Chromatin Immunoprecipitation, Rats, Early Growth Response Protein 1
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