The DOI matches its Crossref record; 52 of the 52 references it cites were found in a registry or an index.
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.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“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]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“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]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“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]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“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]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“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]
Experimental — accuracy not yet measured
The source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“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]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“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]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“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]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“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]
Experimental — accuracy not yet measuredThe cited source says what the claim attributes to it.
In the citing paper
“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]
The cited source says what the claim attributes to it.
In the citing paper
“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]
The cited source says what the claim attributes to it.
In the citing paper
“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]
The cited source says what the claim attributes to it.
In the citing paper
“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]
The cited source says what the claim attributes to it.
In the citing paper
“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
The cited source says what the claim attributes to it.
In the citing paper
“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
The cited source says what the claim attributes to it.
In the citing paper
“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
The cited source says what the claim attributes to it.
In the citing paper
“↑ 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
The cited source says what the claim attributes to it.
In the citing paper
“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 cited source says what the claim attributes to it.
In the citing paper
“The findings concerning NR3C1 are of particular relevance given that they align with the animal studies and replicate the earlier observations with brain tissue.”
The cited source says what the claim attributes to it.
In the citing paper
“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]
The cited source says what the claim attributes to it.
In the citing paper
“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]
In the citing paper
“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
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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 the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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
In the citing paper
“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
In the citing paper
“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
In the citing paper
“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
In the citing paper
“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]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Epigenetic programming by maternal behavior
Weaver, I. C. G., Cervoni, N., Champagne, F. A., D'Alessio, A. C., Sharma, S., Seckl, J. R., Dymov, S., Szyf, M., & Meaney, M. J. (2004) · Nature Neuroscience · doi:10.1038/nn1276 · Cited by 6,177
Self-citationStress and the brain: from adaptation to disease
de Kloet, E. R., Joëls, M., & Holsboer, F. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1683 · Cited by 4,621
The Structured Clinical Interview for DSM-III-R (SCID): I: History, Rationale, and Description
Spitzer, R. L. (1992) · Archives of General Psychiatry · doi:10.1001/archpsyc.1992.01820080032005 · Cited by 4,336
Frommer, M., McDonald, L. E., Millar, D. S., Collis, C. M., Watt, F., Grigg, G. W., Molloy, P. L., & Paul, C. L. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.5.1827 · Cited by 3,238
Liu, D., Diorio, J., Tannenbaum, B., Caldji, C., Francis, D., Freedman, A., Sharma, S., Pearson, D., Plotsky, P. M., & Meaney, M. J. (1997) · Science · doi:10.1126/science.277.5332.1659 · Cited by 3,170
Self-citationHeim, C., & Nemeroff, C. B. (2001) · Biological Psychiatry · doi:10.1016/s0006-3223(01)01157-x · Cited by 2,791
Meaney, M. J. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.1161 · Cited by 2,708
Self-citationThe Corticosteroid Receptor Hypothesis of Depression
Holsboer, F. (2000) · Neuropsychopharmacology · doi:10.1016/s0893-133x(00)00159-7 · Cited by 2,181
High sensitivity mapping of methylated cytosines
Susan, J. C., Harrison, J., Paul, C. L., & Frommer, M. (1994) · Nucleic Acids Research · doi:10.1093/nar/22.15.2990 · Cited by 1,862
Oberlander, T. F., Weinberg, J., Papsdorf, M., Grunau, R., Misri, S., & Devlin, A. M. (2008) · Epigenetics · doi:10.4161/epi.3.2.6034 · Cited by 1,432
Flagged first, then by citations
Cited by
Sorted by citations
Items 401–500 of 1,057
The involvement of audio–motor coupling in the music‐supported therapy applied to stroke patients
Rodríguez‐Fornells, A., Rojo, N., Amengual, J. L., Ripollés, P., ALTENMÜLLER, E. O., & Münte, T. F. (2012) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2011.06425.x · Cited by 152
Epigenetic transmission of Holocaust trauma: can nightmares be inherited?
Kellermann, N. P. F. (2013) · PubMed · Cited by 144
The epigenetic impacts of social stress: how does social adversity become biologically embedded?
Cunliffe, V. T. (2016) · Epigenomics · doi:10.2217/epi-2016-0075 · Cited by 141
Na, K., Chang, H. S., Won, E., Han, K., Choi, S., Tae, W., Yoon, H., Kim, Y., Joe, S., Jung, I., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0085425 · Cited by 144
Stress and Anxiety Across the Lifespan: Structural Plasticity and Epigenetic Regulation
Hunter, R. G., & McEwen, B. S. (2013) · Epigenomics · doi:10.2217/epi.13.8 · Cited by 142
Epidemiology of Stress and Asthma: From Constricting Communities and Fragile Families to Epigenetics
Wright, R. J. (2010) · Immunology and Allergy Clinics of North America · doi:10.1016/j.iac.2010.09.011 · Cited by 146
Glucocorticoid receptor protein expression in human hippocampus; stability with age
Wang, Q., Van Heerikhuize, J., Aronica, E., Kawata, M., Seress, L., Joels, M., Swaab, D. F., & Lucassen, P. J. (2013) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2012.11.019 · Cited by 144
Blunted HPA Axis Activity in Suicide Attempters Compared to those at High Risk for Suicidal Behavior
Melhem, N. M., Keilp, J. G., Porta, G., Oquendo, M. A., Burke, A., Stanley, B., Cooper, T. B., Mann, J. J., & Brent, D. A. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2015.309 · Cited by 143
Early-Life Stress Reduces DNA Methylation of the Pomc Gene in Male Mice
Wu, Y., Patchev, A. V., Daniel, G., Almeida, O. F. X., & Spengler, D. (2014) · Endocrinology · doi:10.1210/en.2013-1868 · Cited by 142
Dynamic regulation of glucocorticoid signalling in health and disease
Biddie, S. C., Conway-Campbell, B. L., & Lightman, S. L. (2012) · Rheumatology · doi:10.1093/rheumatology/ker215 · Cited by 143
Cognitive and social lifestyle: links with neuropathology and cognition in late life
Bennett, D. A., Arnold, S. E., Valenzuela, M., Brayne, C., & Schneider, J. A. (2013) · Acta Neuropathologica · doi:10.1007/s00401-013-1226-2 · Cited by 148
Diverse Epigenetic Mechanisms of Human Disease
Brookes, E., & Shi, Y. (2014) · Annual Review of Genetics · doi:10.1146/annurev-genet-120213-092518 · Cited by 145
Perinatal programming of emotional brain circuits: an integrative view from systems to molecules
Bock, J., Rether, K., Gröger, N., Xie, L., & Braun, K. (2014) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00011 · Cited by 152
Riem, M. M. E., Alink, L. R. A., Out, D., van IJzendoorn, M. H., & Bakermans‐Kranenburg, M. J. (2015) · Development and Psychopathology · doi:10.1017/s0954579415000127 · Cited by 161
Mortality after Parental Death in Childhood: A Nationwide Cohort Study from Three Nordic Countries
Li, J., Vestergaard, M., Cnattingius, S., Gissler, M., Bech, B. H., Obel, C., & Olsen, J. (2014) · PLoS Medicine · doi:10.1371/journal.pmed.1001679 · Cited by 150
Lavebratt, C., Åberg, E., Sjöholm, L. K., & Forsell, Y. (2010) · Journal of Affective Disorders · doi:10.1016/j.jad.2010.02.113 · Cited by 142
Roy, B., Shelton, R. C., & Dwivedi, Y. (2017) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2017.02.005 · Cited by 139
The social brain: Neurobiological basis of affiliative behaviours and psychological well-being
Walker, S. C., & McGlone, F. P. (2013) · Neuropeptides · doi:10.1016/j.npep.2013.10.008 · Cited by 145
Fryer, A. A., Emes, R. D., ISMAIL, K. M. K., Haworth, K. E., Mein, C. A., Carroll, W. D., & Farrell, W. E. (2011) · Epigenetics · doi:10.4161/epi.6.1.13392 · Cited by 140
Increased DNA methylation of neuropsychiatric genes occurs in borderline personality disorder
Dammann, G., Teschler, S., Haag, T., Altmüller, F., Tuczek, F., & Dammann, R. (2011) · Epigenetics · doi:10.4161/epi.6.12.18363 · Cited by 137
Obradović, J. (2012) · Development and Psychopathology · doi:10.1017/s0954579412000053 · Cited by 153
Lehnen, H., Zechner, U., & Haaf, T. (2013) · Molecular Human Reproduction · doi:10.1093/molehr/gat020 · Cited by 148
Mapping the new molecular landscape: social dimensions of epigenetics
Pickersgill, M. D., Niewöhner, J., Müller, R., Martin, P. A., & Cunningham‐Burley, S. (2013) · New Genetics and Society · doi:10.1080/14636778.2013.861739 · Cited by 143
Hakamata, Y., Suzuki, Y., Kobashikawa, H., & Hori, H. (2022) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2022.100994 · Cited by 159
Bick, J., Naumova, O., Hunter, S., Barbot, B., Lee, M., Luthar, S. S., Raefski, A., & Grigorenko, E. L. (2012) · Development and Psychopathology · doi:10.1017/s0954579412000806 · Cited by 140
Brauer, J., Xiao, Y., Poulain, T., Friederici, A. D., & Schirmer, A. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhw137 · Cited by 141
Flinn, M. V., Nepomnaschy, P. A., Muehlenbein, M. P., & Ponzi, D. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.01.005 · Cited by 125
Transcriptional enhancers in development and disease
Sakabe, N. J., Savic, D., & Nóbrega, M. A. (2012) · Genome biology · doi:10.1186/gb-2012-13-1-238 · Cited by 143
Adversity exposure during sensitive periods predicts accelerated epigenetic aging in children
Marini, S., Davis, K. A., Soare, T. W., Zhu, Y., Suderman, M. J., Simpkin, A. J., Smith, A. D. A. C., Wolf, E. J., Relton, C. L., & Dunn, E. C. (2019) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2019.104484 · Cited by 145
Epigenetic programming of the HPA axis: Early life decides
Murgatroyd, C., & Spengler, D. (2011) · Stress · doi:10.3109/10253890.2011.602146 · Cited by 138
Neurobiological correlates of illness progression in the recurrent affective disorders
Post, R. M., Fleming, J., & Kapczinski, F. P. (2012) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2012.02.004 · Cited by 142
Bevilacqua, L. (2012) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2011.152 · Cited by 137
“Genetic variation in FKBP5 may alter function of the stress-response pathway during development and thus alter CRH and AVP expression, predisposing those who had a significant history of child abuse to a higher risk of aggressive behavior through long-lasting traumainduced epigenetic changes.(59) Table 4.”
What Biological Functions Are and Why They Matter
Garson, J. (2019) · doi:10.1017/9781108560764 · Cited by 239
Epigenetic Regulations in Neuropsychiatric Disorders
Kuehner, J. N., Bruggeman, E. C., Wen, Z., & Yao, B. (2019) · Frontiers in Genetics · doi:10.3389/fgene.2019.00268 · Cited by 144
The intergenerational transmission of parenting: Closing comments for the special section.
Conger, R. D., Belsky, J., & Capaldi, D. M. (2009) · Developmental Psychology · doi:10.1037/a0016911 · Cited by 136
Prenatal maternal mood is associated with altered diurnal cortisol in adolescence
O’Donnell, K. J., Glover, V. A. S., Jenkins, J., Browne, D. T., Ben‐Shlomo, Y., Golding, J., & O’Connor, T. G. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.01.008 · Cited by 151
Early Life Stress Effects on Glucocorticoid—BDNF Interplay in the Hippocampus
Daskalakis, N. P., de Kloet, E. R., Yehuda, R., Malaspina, D., & Kranz, T. M. (2015) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2015.00068 · Cited by 141
Tyrka, A. R., Parade, S. H., Welch, E. S., Ridout, K. K., Price, L. H., Marsit, C., Philip, N. S., & Carpenter, L. L. (2016) · Translational Psychiatry · doi:10.1038/tp.2016.112 · Cited by 135
Mistry, K. B., Minkovitz, C. S., Riley, A. W., Johnson, S. B., Grason, H. A., Dubay, L. C., & Guyer, B. (2012) · American Journal of Public Health · doi:10.2105/ajph.2012.300687 · Cited by 142
S-Adenosyl Methionine and Transmethylation Pathways in Neuropsychiatric Diseases Throughout Life
Gao, J., Cahill, C. M., Huang, X., Roffman, J. L., Lamon‐Fava, S., D, M. F. M., Mischoulon, D., & Rogers, J. T. (2018) · Neurotherapeutics · doi:10.1007/s13311-017-0593-0 · Cited by 142
Barker, E. D., Walton, E., & Cecil, C. A. M. (2018) · Journal of Child Psychology and Psychiatry · doi:10.1111/jcpp.12782 · Cited by 134
Epigenetics and depression: return of the repressed
Dalton, V. S., Kolshus, E., & McLoughlin, D. M. (2013) · Journal of Affective Disorders · doi:10.1016/j.jad.2013.10.028 · Cited by 142
Olvera Alvarez, H. A., Kubzansky, L. D., Campen, M. J., & Slavich, G. M. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.06.002 · Cited by 133
“In human studies, early life stress has been associated with modifications of hypothalamic–pituitary–adrenal (HPA) axis- and neuroplasticity-related methylation patterns (Labonté et al., 2012; McGowan et al., 2009; Mehta et al., 2013).”
Steiger, H., Labonté, B., Groleau, P., Turecki, G., & Israël, M. (2013) · International Journal of Eating Disorders · doi:10.1002/eat.22113 · Cited by 133
Self-citationDrake, A. J., McPherson, R. C., Godfrey, K. M., Cooper, C. C., Lillycrop, K. A., Hanson, M. A., Meehan, R. R., Seckl, J. R., & Reynolds, R. M. (2012) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2012.04453.x · Cited by 137
DNA Methylation and Susceptibility to Autism Spectrum Disorder
Tremblay, M. W., & Jiang, Y. (2019) · Annual Review of Medicine · doi:10.1146/annurev-med-120417-091431 · Cited by 139
Genome-Wide DNA Methylation Scan in Major Depressive Disorder
Sabunciyan, S., Aryee, M. J., Irizarry, R. A., Rongione, M. A., Webster, M. J., Kaufmann, W. E., Murakami, P. N., Lessard, A., Yolken, R. H., Feinberg, A. P., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0034451 · Cited by 139
Perišić, T., Zimmermann, N., Kirmeier, T., Asmus, M., Tuorto, F., Uhr, M., Holsboer, F., Rein, T., & Zschocke, J. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2009.188 · Cited by 135
Role of glucocorticoid in developmental programming: Evidence from zebrafish
Nesan, D., & Vijayan, M. M. (2012) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2012.10.006 · Cited by 136
DNA Methylation, Behavior and Early Life Adversity
Szyf, M. (2013) · Journal of genetics and genomics/Journal of Genetics and Genomics · doi:10.1016/j.jgg.2013.06.004 · Cited by 147
Early life adversity: Lasting consequences for emotional learning
Krugers, H. J., Arp, J. M., Xiong, H., Kanatsou, S., Lesuis, S. L., Kőrösi, A., Joëls, M., & Lucassen, P. J. (2016) · Neurobiology of Stress · doi:10.1016/j.ynstr.2016.11.005 · Cited by 139
Culturing the adolescent brain: what can neuroscience learn from anthropology?
Choudhury, S. (2009) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsp030 · Cited by 137
Adverse Childhood Experiences and Trauma-Informed Care
Goddard, A. (2021) · Journal of Pediatric Health Care · doi:10.1016/j.pedhc.2020.09.001 · Cited by 132
Beauchaine, T. P., Neuhaus, E., Zalewski, M., Crowell, S. E., & Potapova, N. V. (2011) · Development and Psychopathology · doi:10.1017/s0954579411000459 · Cited by 134
Wingenfeld, K., Spitzer, C., Rullkötter, N., & Löwe, B. (2009) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2009.09.014 · Cited by 135
Grova, N., Schroeder, H., Olivier, J. L., & Turner, J. D. (2019) · International Journal of Genomics · doi:10.1155/2019/2085496 · Cited by 138
Radtke, K. M., Schauer, M., Gunter, H. M., Ruf-Leuschner, M., Sill, J., Meyer, A., & Elbert, T. (2015) · Translational Psychiatry · doi:10.1038/tp.2015.63 · Cited by 128
Redefining neuroendocrinology: Epigenetics of brain-body communication over the life course
McEwen, B. S. (2018) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2017.11.001 · Cited by 129
Duman, E. A., & Canli, T. (2015) · Biology of Mood & Anxiety Disorders · doi:10.1186/s13587-015-0017-x · Cited by 136
Vijayendran, M., Beach, S. R. H., Plume, J. M., Brody, G. H., & Philibert, R. A. (2012) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2012.00055 · Cited by 133
Epigenetic regulation of the expression of genes involved in steroid hormone biosynthesis and action
Martinez-Arguelles, D. B., & Papadopoulos, V. (2010) · Steroids · doi:10.1016/j.steroids.2010.02.004 · Cited by 130
Pratchett, L. C., & Yehuda, R. (2011) · Development and Psychopathology · doi:10.1017/s0954579411000186 · Cited by 142
Gassen, N. C., Chrousos, G. P., Binder, E. B., & Zannas, A. S. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.06.003 · Cited by 131
Blunted HPA axis activity prior to suicide attempt and increased inflammation in attempters
Melhem, N. M., Munroe, S., Marsland, A., Gray, K., Brent, D., Porta, G., Douaihy, A., Laudenslager, M. L., DePietro, F., Diler, R., et al. (2017) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2017.01.001 · Cited by 124
Zhu, Y., Wang, Y., Yao, R., Hao, T., Cao, J., Huang, H., Wang, L., & Wu, Y. (2017) · Journal of Neuroinflammation · doi:10.1186/s12974-016-0782-5 · Cited by 128
Glucocorticoid programming of the fetal male hippocampal epigenome
Crudo, A., Suderman, M., Moisiadis, V. G., Petropoulos, S., Kostaki, A., Hallett, M., Szyf, M., & Matthews, S. G. (2013) · Endocrinology · doi:10.1210/en.2012-1980 · Cited by 123
Okada, S., Morinobu, S., Fuchikami, M., Segawa, M., Yokomaku, K., Kataoka, T., Okamoto, Y., Yamawaki, S., Inoue, T., Kusumi, I., et al. (2014) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2014.02.002 · Cited by 125
Stress, Memory, and the Hippocampus
Wingenfeld, K., & Wolf, O. T. (2014) · Frontiers of Neurology and Neuroscience · doi:10.1159/000356423 · Cited by 139
Cultural trauma and epigenetic inheritance
Lehrner, A. L., & Yehuda, R. (2018) · Development and Psychopathology · doi:10.1017/s0954579418001153 · Cited by 144
Genetic approaches to understanding post-traumatic stress disorder
Almli, L. M., Fani, N., Smith, A. K., & Ressler, K. J. (2014) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145713001090 · Cited by 124
Martín-Blanco, A., Ferrer, M., Soler, J., Salazar, J., Vega, D., Andión, O., Sanchez-Mora, C., Arranz, M. J., Ribases, M., Feliu-Soler, A., et al. (2014) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2014.06.011 · Cited by 138
Kember, R. L., Dempster, E. L., Lee, T. H. A., Schalkwyk, L. C., Mill, J., & Fernandes, C. (2012) · Brain and Behavior · doi:10.1002/brb3.69 · Cited by 133
Glucocorticoids, epigenetic control and stress resilience
Reul, J. M. H. M., Collins, A., Saliba, R. S., Mifsud, K. R., Carter, S. D., Gutièrrez‐Mecinas, M., Qian, X., & Linthorst, A. C. E. (2014) · Neurobiology of Stress · doi:10.1016/j.ynstr.2014.10.001 · Cited by 124
Importance of epigenetic mechanisms in visceral pain induced by chronic water avoidance stress
Tran, L., Chaloner, A., Sawalha, A. H., & van-Meerveld, B. G. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.09.016 · Cited by 124
Epigenetic Biomarker Development
Bock, C. (2009) · Epigenomics · doi:10.2217/epi.09.6 · Cited by 129
Adverse Childhood Experiences and Disability in U.S. Adults
Rose, S. M. S., Xie, D., & Stineman, M. G. (2014) · PM&R · doi:10.1016/j.pmrj.2014.01.013 · Cited by 140
Agorastos, A., Pervanidou, P., Chrousos, G. P., & Kolaitis, G. A. (2018) · HORMONES · doi:10.1007/s42000-018-0065-x · Cited by 139
Childhood trauma, HPA axis activity and antidepressant response in patients with depression
Nikkheslat, N., McLaughlin, A. P., Hastings, C., Zajkowska, Z., Nettis, M. A., Mariani, N., Enache, D., Lombardo, G., Pointon, L., Cowen, P. J., et al. (2020) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2019.11.024 · Cited by 124
Surace, T., Fusar‐Poli, L., Vozza, L., Cavone, V., Arcidiacono, C., Mammano, R., Basile, L., Rodolico, A., Bisicchia, P., Caponnetto, P., et al. (2020) · European Child & Adolescent Psychiatry · doi:10.1007/s00787-020-01508-5 · Cited by 140
Principles of inflammasome priming and inhibition: implications for psychiatric disorders
Herman, F. J., & Pasinetti, G. M. (2018) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2018.06.010 · Cited by 115
Blaze, J., Scheuing, L., & Roth, T. L. (2013) · Developmental Neuroscience · doi:10.1159/000350716 · Cited by 123
Shumay, E., Logan, J., Volkow, N. D., & Fowler, J. S. (2012) · Epigenetics · doi:10.4161/epi.21976 · Cited by 120
A Cellular Memory of Developmental History Generates Phenotypic Diversity in C. elegans
Hall, S. E., Beverly, M., Russ, C., Nusbaum, C., & Sengupta, P. (2010) · Current Biology · doi:10.1016/j.cub.2009.11.035 · Cited by 126
Holloway, T. D., Moreno, J. L., Umali, A., Rayannavar, V., Hodes, G. E., Russo, S. J., & González‐Maeso, J. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.2331-12.2013 · Cited by 124
Watkeys, O. J., Kremerskothen, K., Quidé, Y., Fullerton, J. M., & Green, M. J. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.08.017 · Cited by 123
Childhood trauma in bipolar disorder
Watson, S., Gallagher, P., Dougall, D., Porter, R., Moncrieff, J., Ferrier, I. N., & Young, A. H. (2014) · Australian & New Zealand Journal of Psychiatry · doi:10.1177/0004867413516681 · Cited by 122
Sit, D. K. Y., Luther, J. F., Buysse, D. J., Dills, J. L., Eng, H. F., Okun, M. L., Wisniewski, S. R., & Wisner, K. L. (2015) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2015.04.021 · Cited by 128
A Review of Hypothalamic-Pituitary-Adrenal Axis Function in Chronic Fatigue Syndrome
Tomas, C., Newton, J. L., & Watson, S. (2013) · ISRN Neuroscience · doi:10.1155/2013/784520 · Cited by 128
Booij, L., Tremblay, R. E., Szyf, M., & Benkelfat, C. (2015) · Journal of Psychiatry and Neuroscience · doi:10.1503/jpn.140099 · Cited by 127
Molecular targets of epigenetic regulation and effectors of environmental influences☆☆☆
Choudhuri, S., Cui, Y., & Klaassen, C. D. (2010) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2010.03.022 · Cited by 125
Modulation of programmed cell death by medicinal plants.
Thatte, U. M., Bagadey, S., & Dahanukar, S. A. (2000) · PubMed · Cited by 122
Epigenetics in pain and analgesia: An imminent research field
Doehring, A., Geißlinger, G., & Lötsch, J. (2010) · European Journal of Pain · doi:10.1016/j.ejpain.2010.06.004 · Cited by 121
Post, R. M., & Kalivas, P. W. (2013) · The British Journal of Psychiatry · doi:10.1192/bjp.bp.112.116855 · Cited by 126
Lang, J., McKie, J., Smith, H. E., McLaughlin, A. L., Gillberg, C., Shiels, P. G., & Minnis, H. (2019) · European Child & Adolescent Psychiatry · doi:10.1007/s00787-019-01329-1 · Cited by 138
Bio-behavioral synchrony promotes the development of conceptualized emotions
Atzil, S., & Gendron, M. (2017) · Current Opinion in Psychology · doi:10.1016/j.copsyc.2017.07.009 · Cited by 120
Fruyt, F. D., & Clercq, B. J. D. (2014) · Annual Review of Clinical Psychology · doi:10.1146/annurev-clinpsy-032813-153634 · Cited by 126
The early‐life social environment and DNA methylation
Szyf, M. (2012) · Clinical Genetics · doi:10.1111/j.1399-0004.2012.01843.x · Cited by 124
The Impact of External Factors on the Epigenome:In Uteroand over Lifetime
Toraño, E. G., García, M. G., Fernández-Morera, J. L., García, P. N., & Fernández, A. F. (2016) · BioMed Research International · doi:10.1155/2016/2568635 · Cited by 130
Antoniou, G., Lambourg, E. J., Steele, J. D., & Colvin, L. (2023) · British Journal of Anaesthesia · doi:10.1016/j.bja.2023.03.008 · Cited by 133
Stress-induced mechanisms in mental illness: A role for glucocorticoid signalling
Cattaneo, A., & Riva, M. A. (2016) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2015.07.021 · Cited by 118
Metadata
- 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
About these checks
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.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
