Maternal licking regulates hippocampal glucocorticoid receptor transcription through a thyroid hormone–serotonin–NGFI-A signalling cascade
Open accessAbstract
Variations in parental care direct phenotypic development across many species. Variations in maternal pup licking/grooming (LG) in the rat regulate the development of individual differences in hypothalamic–pituitary–adrenal responses to stress. The adult offspring of mothers that show an increased frequency of pup LG have increased hippocampal glucocorticoid receptor (GR) expression and more modest pituitary–adrenal responses to stress. This parental effect is mediated by the epigenetic programming of a GR exon 1 promoter (exon 1 7 ) through the binding of the transcription factor nerve growth factor-inducible factor A (NGFI-A). In this paper, we report that: (i) the association of NGFI-A with the exon 1 7 GR promoter is dynamically regulated by mother–pup interactions; (ii) this effect is mimicked by artificial tactile stimulation comparable to that provided by pup LG; (iii) that serotonin (5-HT) induces an NGFI-A-dependent increase in GR transcription in hippocampal neurons and NGFI-A overexpression is sufficient for this effect; and (iv) that thyroid hormones and 5-HT are key mediators of the effects of pup LG and tactile stimulation on NGFI-A binding to the exon 1 7 GR promoter in hippocampus. These findings suggest that pup LG directly activates 5-HT systems to initiate intracellular signalling pathways in the hippocampus that regulate GR transcription.
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Maternal licking or direct tactile stimulation that mimics licking increases hippocampal expression of NGFI-A.
“Maternal licking or direct application of tactile stimulation that mimics the sensory effects of licking increases hippocampal expression of the transcription factor, nerve growth factor-inducible factor A (NGFI-A; AKA egr-1, zif268).82”
From Early life adversity and the epigenetic programming of hypothalamic-pituitary-adrenal function (2014) · cites this paper as [82]
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 [82]
Maternal effects on hippocampal GR expression are mediated by increases in hippocampal serotonin turnover and expression of the NGFI-A transcription factor.
“In vivo studies with rat pups or in vitro studies using cultured hippocampal neurons suggest that maternal effects on hippocampal GR expression are mediated by increases in hippocampal serotonin (5-HT) turnover and the expression of the nerve-growth factor-inducible factor-A (NGFI-A) transcription factor.78-82”
From Early life adversity and the epigenetic programming of hypothalamic-pituitary-adrenal function (2014) · cites this paper as [82]
In 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 [82]
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 [82]
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 [82]
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 [82]
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 [82]
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- Authors
- Hellstrom, I. C., Dhir, S. K., Diorio, J. C., & Meaney, M. J.
- Affiliations
- Douglas Mental Health University Institute (CA)
- Corresponding author
- Meaney, Michael J.
- Venue
- Philosophical Transactions of the Royal Society B: Biological Sciences
- Publisher
- The Royal Society
- Published
- 2012-09-05
- Volume
- 367
- Issue
- 1601
- Pages
- 2495-2510
- ISSN
- 0962-8436 (ISSN-L)
- 1471-2970
- PMC
- PMC3405683
- OpenAlex
- W2005902017
- Cited by
- 171
- References
- 47
- Citations by year
- 2026: 3 · 2025: 8 · 2024: 4 · 2023: 8 · 2022: 11 · 2021: 13 · 2020: 14 · 2019: 13 · 2018: 23 · 2017: 16 · 2016: 13 · 2015: 16 · 2014: 18 · 2013: 8 · 2012: 3
- FWCI
- 5.97
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Philosophical Transactions of the Royal Society B Biological Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Hope for Depression Research Foundation
- Canadian Institutes of Health Research
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- maternal licking, NGFI-A, serotonin, thyroid hormones, transcriptional regulation, hypothalamic-pituitary-adrenal axis, stress response, epigenetic programming, parental care, tactile stimulation, hippocampal neurons, rats
- MeSH terms
- Animals, Behavior, Animal, Exons, Female, Hippocampus, Male, Maternal Behavior, Promoter Regions, Genetic, Protein Binding, Receptors, Glucocorticoid, Serotonin, Thyroxine, Transcription, Genetic, Triiodothyronine, Signal Transduction, Lentivirus, Rats, Long-Evans, Rats, Early Growth Response Protein 1, Primary Cell Culture
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