Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse
Open accessAbstract
Maternal care influences hypothalamic-pituitary-adrenal (HPA) function in the rat through epigenetic programming of glucocorticoid receptor expression. In humans, childhood abuse alters HPA stress responses and increases the risk of suicide. We examined epigenetic differences in a neuron-specific glucocorticoid receptor (NR3C1) promoter between postmortem hippocampus obtained from suicide victims with a history of childhood abuse and those from either suicide victims with no childhood abuse or controls. We found decreased levels of glucocorticoid receptor mRNA, as well as mRNA transcripts bearing the glucocorticoid receptor 1F splice variant and increased cytosine methylation of an NR3C1 promoter. Patch-methylated NR3C1 promoter constructs that mimicked the methylation state in samples from abused suicide victims showed decreased NGFI-A transcription factor binding and NGFI-A-inducible gene transcription. These findings translate previous results from rat to humans and suggest a common effect of parental care on the epigenetic regulation of hippocampal glucocorticoid receptor expression.
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In the same group there was decreased NGF1-A transcription factor binding and NGF1-induced gene transcription.
“Also, in the same group there was decreased NGF1-A transcription factor binding and NGF1-induced gene transcription (137).”
From Epigenetic Modifications in Stress Response Genes Associated With Childhood Trauma (2019) · cites this paper as [137]
The Results sections on patch methylation and NGFI-A association report reduced NGFI-A binding and NGFI-A–induced transcription in methylated NR3C1 promoter constructs that mimicked the abused-suicide group’s methylation pattern. They do not report measuring those two decreases directly in that group. Page numbers were not provided in our copy. (LLM, conf=0.88)
Experimental — accuracy not yet measuredMcGowan et al. first demonstrated this in post-mortem hippocampal samples of suicide victims with a history of childhood abuse, showing methylation levels approximately 2-fold higher at key CpG sites than in controls.
“McGowan et al. first demonstrated this in post-mortem hippocampal samples of suicide victims with a history of childhood abuse, showing methylation levels approximately 2-fold higher at key CpG sites than in controls (55).”
From Exploring the neurobiological markers of suicidal behaviors in pediatric population: a narrative review (2026) · cites this paper as [55]
The Methods describe postmortem hippocampal samples from suicide victims with a history of childhood abuse and controls. The Results (Genotyping and methylation analysis; Patch methylation of the NR3C1 promoter) report increased methylation in the abused group at specific CpG sites, but the passages do not establish the claimed approximately two-fold difference at those sites. (LLM, conf=0.86)
Experimental — accuracy not yet measuredOne of the most consistent findings in suicide research is hypermethylation of specific CpG sites in the NR3C1 promoter region, particularly exon 1F, which reduces glucocorticoid receptor expression and disrupts negative feedback within the HPA axis.
“One of the most consistent findings in suicide research is hypermethylation of specific CpG sites in the NR3C1 promoter region, particularly exon 1F, which reduces glucocorticoid receptor expression and disrupts negative feedback within the HPA axis (55).”
From Exploring the neurobiological markers of suicidal behaviors in pediatric population: a narrative review (2026) · cites this paper as [55]
Split into 2 atoms — 0 confirmed, 2 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measuredGenetic liability and early-life adversity converge on glucocorticoid signaling; polymorphisms in NR3C1 and FKBP5 alter glucocorticoid receptor sensitivity, while childhood maltreatment produces stable hypermethylation of the NR3C1 promoter that further reduces glucocorticoid feedback.
“Genetic liability and early-life adversity converge on glucocorticoid signaling. Polymorphisms in NR3C1 and FKBP5 alter glucocorticoid receptor sensitivity, while childhood maltreatment produces stable hypermethylation of the NR3C1 promoter that further reduces glucocorticoid feedback (55).”
From Exploring the neurobiological markers of suicidal behaviors in pediatric population: a narrative review (2026) · cites this paper as [55]
Split into 2 atoms — 0 confirmed, 2 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measuredChildhood maltreatment, including abuse and neglect, represents a sustained early-life stressor associated with long-term biological and behavioral changes across generations.
“Childhood maltreatment, including abuse and neglect, represents a sustained early-life stressor associated with long-term biological and behavioral changes across generations.”
From Epigenetic changes associated with multi-generational trauma: characterization, mechanisms, and therapeutics (2026) · cites this paper as [119]
The Abstract reports biological differences in adults with a history of childhood abuse, and the Discussion links childhood adversity to altered stress responses and later behavioral risks. The Discussion suggests that vulnerability might pass from parent to offspring through epigenetic mechanisms, but it does not establish that maltreatment causes biological and behavioral changes across generations. (LLM, conf=0.86)
Experimental — accuracy not yet measured
Altered methylation of genes involved in HPA-axis feedback and glucocorticoid homeostasis, including NR3C1 and FKBP5, has been reported in individuals with histories of abuse or neglect.
“Altered methylation of genes involved in HPA-axis feedback and glucocorticoid homeostasis, including NR3C1 and FKBP5, has been reported in individuals with histories of abuse or neglect (118–120).”
From Epigenetic changes associated with multi-generational trauma: characterization, mechanisms, and therapeutics (2026) · cites this paper as [119]
The Discussion reports increased methylation of the NR3C1 promoter in hippocampal samples from suicide victims with a history of childhood abuse. This supports the NR3C1-and-abuse portion of the claim, but the paper does not report FKBP5 methylation or a finding specifically about neglect. (LLM, conf=0.88)
Experimental — accuracy not yet measuredEvidence suggests involvement of stress-response regulation, neurodevelopmental and emotional processing pathways, and epigenetic remodeling processes in shaping intergenerational outcomes.
“Evidence suggests involvement of stress-response regulation, neurodevelopmental and emotional processing pathways, and epigenetic remodeling processes in shaping intergenerational outcomes (116–124).”
From Epigenetic changes associated with multi-generational trauma: characterization, mechanisms, and therapeutics (2026) · cites this paper as [119]
The Discussion (page not provided) suggests that epigenetic modification of stress-response genes could contribute to transmission of depression vulnerability from parent to offspring. It also discusses altered hippocampal development after childhood abuse, but does not identify a distinct emotional-processing pathway shaping intergenerational outcomes. (LLM, conf=0.82)
Experimental — accuracy not yet measuredEarly-life stress, commonly experienced through childhood abuse, increases DNA methylation of stress-regulating genes (NR3C1, FKBP5), hypermethylating the glucocorticoid receptor and altering the HPA axis.
“In the case of early-life stress, commonly experienced through childhood abuse, DNA methylation of stress-regulating genes (i.e. NR3C1, FKBP5) increases, hypermethylating the glucocorticoid receptor and altering the HPA axis”
From The clinical use of epigenetics in psychiatry: a narrative review of epigenetic mechanisms, key candidate genes, and precision psychiatry (2025) · cites this paper as [10]
The Discussion reports increased methylation of the NR3C1 promoter in hippocampal samples from suicide victims with a history of childhood abuse. It does not report increased FKBP5 methylation, and it discusses a link between methylation and altered HPA activity as a possibility rather than demonstrating that causal chain in the human samples. Page numbers are not available in our copy. (LLM, conf=0.89)
Experimental — accuracy not yet measuredThe first documented study of the GR promoter in humans showed higher methylation of the hippocampal GR 1F promoter in post-mortem tissue of adult suicide victims with a history of childhood abuse, similar to findings in rodent pups raised by mothers who provided low levels of licking and grooming.
“The first documented study of the GR promoter in humans showed higher methylation of the hippocampal GR 1F promoter in post-mortem tissue of adult suicide victims with a history of childhood abuse, similar to findings in rodent pups raised by mothers who provided low levels of licking and grooming 121,122 .”
From Intergenerational transmission of trauma effects: putative role of epigenetic mechanisms (2018) · cites this paper as [121]
Split into 2 atoms — 0 confirmed, 2 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measuredIn postmortem brain tissue (hippocampus) from those who died by suicide, there was decreased expression of GRs, along with enhanced cytosine methylation of the NR3C1 promoter in those with a history of childhood trauma.
“In postmortem brain tissue (hippocampus) from those who have died by suicide, there was decreased expression of GRs, along with enhanced cytosine methylation of the NR3C1 promoter in those with a history of childhood trauma.”
From Epigenetic Modifications in Stress Response Genes Associated With Childhood Trauma (2019) · cites this paper as [137]
Binding of glucocorticoid to GRs regulates the stress response through both genetic and epigenetic mechanisms.
“and regulates the stress response through both genetic (136) and epigenetic mechanisms (137).”
From Epigenetic Modifications in Stress Response Genes Associated With Childhood Trauma (2019) · cites this paper as [137]
History of childhood abuse is associated with changes in DNA methylation related to the neuron-specific GR (NR3C1) promoter in the hippocampus.
“For example, in a recent human brain autopsy material study, history of childhood abuse was associated with changes in DNA methylation related to the neuron-specific GR (NR3C1) promoter in the hippocampus, suggesting distinct effects of ELS/CT on the epigenetic regulation of hippocampal GR expression (405).”
From Developmental Trajectories of Early Life Stress and Trauma: A Narrative Review on Neurobiological Aspects Beyond Stress System Dysregulation (2019) · cites this paper as [405]
Lower GR expression along with higher levels of cytosine methylation of the GR promoter exon 1F have been reported in suicide decedents with a history of childhood abuse than in suicide decedents without a history of abuse as well as in non-suicide controls.
“Lower GR expression along with higher levels of cytosine methylation of the GR promoter exon 1 F have been reported in suicide decedents with a history of childhood abuse than in suicide decedents without a history of abuse as well as in non-suicide controls.78”
From Epigenetic regulation in major depression and other stress-related disorders: molecular mechanisms, clinical relevance and therapeutic potential (2023) · cites this paper as [78]
Reduced hippocampal NR3C1 expression was linked to increased hippocampal NR3C1 1F promoter CpG methylation in suicide victims with maltreatment history.
“Reduced expression was linked to increased hippocampal NR3C1 1 F promoter CpG methylation in suicide victims with maltreatment history”
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 McGowan et al., 2009
McGowan et al. reported reduced hippocampal NR3C1 expression in suicide victims with a history of childhood abuse compared to suicide victims without such history and healthy controls.
“McGowan et al. reported reduced hippocampal NR3C1 expression in an all-male postmortem investigation comparing 12 suicide victims with a history of childhood abuse to 12 suicide victims without a history of childhood abuse as well as to 12 healthy control subjects (McGowan et al., 2009)”
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 McGowan et al., 2009
In vitro patch methylation mimicking this epigenetic state resulted in decreased NGFI-A binding and correspondingly reduced NGFI-A-induced gene transcription.
“in vitro patch methylation mimicking this epigenetic state resulted in decreased NGFI-A binding and correspondingly reduced NGFI-A-induced gene transcription (McGowan et al., 2009)”
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 McGowan et al., 2009
NR3C1 methylation is increased in suicide victims with a history of maltreatment.
“↑ NR3C1 methylation in suicide victims with maltreatment history”
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 McGowan et al., 2009
A history of severe childhood abuse was associated with increased NR3C1 methylation in the hippocampus in a post-mortem study of adult suicide victims.
“McGowan and colleagues found that a history of severe childhood abuse (ascertained with proxy-based interviews) was associated with increased NR3C1 methylation in the hippocampus.”
The findings concerning NR3C1 align with the animal studies and replicate the earlier observations with brain tissue.
“The findings concerning NR3C1 are of particular relevance given that they align with the animal studies and replicate the earlier observations with brain tissue.”
Increased methylation of the NR3C1 promoter and reduced glucocorticoid receptor expression have been observed in hippocampal tissue of suicide completers with histories of maltreatment.
“Increased methylation of the NR3C1 promoter and reduced glucocorticoid receptor expression have been observed in hippocampal tissue of suicide completers with histories of maltreatment (119, 120).”
From Epigenetic changes associated with multi-generational trauma: characterization, mechanisms, and therapeutics (2026) · cites this paper as [119]
Other studies have observed associations between childhood maltreatment and differences in DNA methylation in brain, blood, and gametes.
“Other studies have also observed associations between childhood maltreatment and differences in DNAm in the brain, 58 blood, 59 , 60 and even gametes. 61”
From Epigenetics and depression (2019) · cites this paper as [58]
Maternal care in infancy contributes to epigenetic regulation of the glucocorticoid receptor in the hippocampus and in peripheral immune cells.
“Maternal care in infancy contributes to epigenetic regulation of the glucocorticoid receptor in the hippocampus (Anacker et al., 2014; McGowan et al., 2009) as well as in peripheral immune cells (Miller et al., 2011; Tyrka et al., 2012).”
From Developmental psychoneuroendocrine and psychoneuroimmune pathways from childhood adversity to disease (2017) · cites this paper as McGowan et al., 2009
Abused suicide victims had increased CpG methylation of the NR3C1 promoter, concomitant with a decrease in NR3C1 gene expression.
“abused suicide victims had increased CpG methylation of the NR3C1 promoter, concomitant with a decrease in NR3C1 gene expression 126.”
From Resilience in mental health: linking psychological and neurobiological perspectives. (2013) · cites this paper as [126]
Embryonic development and early life are major susceptibility windows during which epigenetic programming is sensitive to environmental influences such as diet, temperature, toxins, maternal behaviour or childhood abuse.
“Embryonic development and early life are two major susceptibility windows during which epigenetic programming is sensitive to environmental influences, such as diet, temperature, environmental toxins, maternal behaviour or childhood abuse 137 .”
From Advances in epigenetics link genetics to the environment and disease (2019) · cites this paper as [137]
Hippocampal samples from individuals with a history of abuse or extreme neglect showed decreased hippocampal GR mRNA levels.
“Hippocampal samples from individuals with a history of abuse or extreme neglect showed decreased hippocampal GR mRNA levels.”
From Early life adversity and the epigenetic programming of hypothalamic-pituitary-adrenal function (2014) · cites this paper as [65]
There is direct evidence for an association between childhood maltreatment and hippocampal GR expression.
“Nevertheless, there is direct evidence for an association between childhood maltreatment and hippocampal GR expression.65”
From Early life adversity and the epigenetic programming of hypothalamic-pituitary-adrenal function (2014) · cites this paper as [65]
Decreased hippocampal GR expression was found in samples from suicide completers with histories of childhood maltreatment compared with controls.
“We65,120 showed decreased hippocampal GR expression in samples from suicide completers with histories of childhood maltreatment compared with controls (sudden, involuntary fatalities).”
From Early life adversity and the epigenetic programming of hypothalamic-pituitary-adrenal function (2014) · cites this paper as [65]
The exon 1F sequence is the homolog of rat exon 17, is highly expressed in brain, and contains an NGFI-A response element.
“The exon 1F sequence is of particular interest as it is the homolog of the rat exon 17, is highly expressed in brain and contains an NGFI-A response element.65,121”
From Early life adversity and the epigenetic programming of hypothalamic-pituitary-adrenal function (2014) · cites this paper as [65]
Suicide risk may be mediated by genetic and epigenetic effects of stress response genes.
“Suicide risk may be mediated by genetic and epigenetic effects of stress response genes (58-61).”
From A brain-centric model of suicidal behavior (2020) · cites this paper as [60]
Glucocorticoid receptors are subject to genetic effects via chaperone proteins such as SKA1 and FKBP5, as well as epigenetic changes observed after maternal deprivation in rats and in suicide decedents with childhood adversity.
“Glucocorticoid receptors are subject to genetic effects via chaperone proteins like SKA1 and FKBP5 (58, 148, 149), as well as epigenetic changes (i.e., methylation) observed in response to maternal deprivation in rats (150) and in suicide decedents with a history of childhood adversity (60).”
From A brain-centric model of suicidal behavior (2020) · cites this paper as [60]
Human parental care impacts epigenetic regulation of hippocampal glucocorticoid receptor gene (NR3C1) expression.
“A milestone study confirmed what had been previously shown in animal models: human parental care impacts epigenetic regulation of hippocampal glucocorticoid receptor gene (NR3C1) expression [138].”
From Food Addiction and Psychosocial Adversity: Biological Embedding, Contextual Factors, and Public Health Implications (2020) · cites this paper as [138]
Abnormal DNA methylation at specific genes has been observed in patients with neuropsychiatric disorders and in animal models of depression and anxiety.
“Abnormal DNA methylation at specific genes has been observed in patients with neuropsychiatric disorders and in animal models of depression and anxiety.”
From Epigenetic mechanisms of major depression: Targeting neuronal plasticity (2018) · cites this paper as [103]
In human post-mortem specimens, epigenetic differences were found in methylation of the neuron-specific NR3C1 promoter (GR1 F) in the hippocampus between suicide victims with a history of childhood abuse and those who committed suicide but had no abuse history and non-suicide controls.
“In human post-mortem specimens, epigenetic differences were found in methylation of the neuron-specific NR3C1 promoter (GR1 F ) in the hippocampus between suicide victims with a history of childhood abuse and those who committed suicide but had no abuse history and non-suicide controls.”
From Epigenetic mechanisms of major depression: Targeting neuronal plasticity (2018) · cites this paper as [103]
Lower levels of both glucocorticoid receptor mRNA and GR1 F splice variant mRNA but higher cytosine methylation of the GR1 F promoter were found in the group with abuse.
“The authors reported lower levels of both glucocorticoid receptor mRNA and GR1 F splice variant mRNA but higher cytosine methylation of the GR1 F promoter in the group with abuse.”
From Epigenetic mechanisms of major depression: Targeting neuronal plasticity (2018) · cites this paper as [103]
Early-life stress is reported to increase methylation of the same BDNF IV and GR17 regions by 95% and 135%, respectively.
“as compared to average reported increases for the same regions resulting from early-life stress of 95%32–34 and 135%29, 30, 47, respectively”
From Maternal and Early-Life Circadian Disruption Have Long-Lasting Negative Consequences on Offspring Development and Adult Behavior in Mice (2017) · cites this paper as [47]
Adversity-related increases in methylation in this region are associated with decreased gene expression in human postmortem brain tissue and increased physiological stress responding in infants.
“adversity-related increases in methylation in this region are associated with decreased gene expression in human postmortem brain tissue (McGowan et al., 2009) and increased physiological stress responding in infants (Oberlander et al., 2008).”
From Associations Between Early Life Stress and Gene Methylation in Children (2015) · cites this paper as McGowan et al., 2009
The current data replicate previously demonstrated associations between child maltreatment and methylation of the GR gene.
“The fact that the current data replicate previously demonstrated associations between child maltreatment and methylation of the GR gene”
From Associations Between Early Life Stress and Gene Methylation in Children (2015) · cites this paper as McGowan et al., 2009
Similar associations between early adversity and GR NR3C1 methylation have been demonstrated in humans, including in brain tissue of deceased adults who committed suicide following child abuse, cord blood of infants with depressed mothers, white blood cells of adults with borderline personality disorder or major depressive disorder with child sexual abuse, whole blood of adults with bipolar and a,
“Similar associations between early adversity and GR NR3C1 methylation have recently been demonstrated in humans who likely experienced severe stress or trauma. These samples have included brain tissue of deceased human adults who had committed suicide following a history of child abuse (McGowan et al., 2009), cord blood of infants with depressed mothers (Oberlander et al., 2008), white blood cells”
From Associations Between Early Life Stress and Gene Methylation in Children (2015) · cites this paper as McGowan et al., 2009
The results are consistent with previous research in adult humans demonstrating an association between child abuse and methylation differences.
“our results are consistent with previous research in adult humans demonstrating an association between child abuse and methylation differences, despite differences in sample characteristics”
From Associations Between Early Life Stress and Gene Methylation in Children (2015) · cites this paper as McGowan et al., 2009
Increased CpG methylation within the glucocorticoid receptor promoter is associated with a sluggish HPA stress response and is associated with poor maternal care in rodents and early life abuse in human suicide victims.
“Likewise the increased CpG methylation within the GR promotor is associated with a sluggish HPA stress response and is associated with poor maternal care in rodents and early life abuse in human suicide victims.”
From Neurobiological and Systemic Effects of Chronic Stress (2017) · cites this paper as [33]
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“Likewise the increased CpG methylation within the GR promotor is associated with a sluggish HPA stress response and is associated with poor maternal care in rodents and early life abuse in human suicide victims.(32,33) Glucocorticoid actions are biphasic, as illustrated above for mitochondria,(29) and timing is import…”
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“First, for example, past adversity can cause epigenetic modification of the glucocorticoid receptor gene in the neural transcriptome, especially in the hypothalamus and amygdala, thereby degrading HPA axis regulation of the inflammatory response (McGowan et al. 2009).”
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- Authors
- McGowan, P. O., Sasaki, A., D'Alessio, A. C., Dymov, S., Labonté, B., Szyf, M., Turecki, G., & Meaney, M. J.
- Affiliations
- Douglas Mental Health University Institute (CA)
- McGill University (CA)
- Corresponding author
- Turecki, Gustavo
- Meaney, Michael J
- Venue
- Nature Neuroscience
- Published
- 2009-02-22
- Volume
- 12
- Issue
- 3
- Pages
- 342-348
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC2944040
- OpenAlex
- W2148337554
- Cited by
- 3,531
- References
- 52
- Citations by year
- 2026: 112 · 2025: 100 · 2024: 108 · 2023: 143 · 2022: 123 · 2021: 146 · 2020: 248 · 2019: 213 · 2018: 209 · 2017: 197 · 2016: 274 · 2015: 270 · 2014: 308 · 2013: 260 · 2012: 278
- FWCI
- 103.35
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD051897)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Social Sciences › Psychology › Clinical Psychology › Child Abuse and Trauma
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Keywords
- glucocorticoid receptor, NR3C1, childhood abuse, child neglect, suicide, epigenetic regulation, DNA methylation, hippocampus, hypothalamic-pituitary-adrenal axis, NGFI-A, promoter methylation, maternal care, postmortem brain
- MeSH terms
- Adult, Base Sequence, Cell Line, Female, Hippocampus, Humans, Male, Middle Aged, Molecular Sequence Data, Promoter Regions, Genetic, Receptors, Glucocorticoid, Suicide, DNA Methylation, Epigenesis, Genetic, Adult Survivors of Child Abuse, Young Adult
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