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Lasting Epigenetic Influence of Early-Life Adversity on the BDNF Gene
Open accessAbstract
Background Childhood maltreatment and early trauma leave lasting imprints on neural mechanisms of cognition and emotion. Using a rat model of infant maltreatment by a caregiver, we investigated whether early-life adversity leaves lasting epigenetic marks at the Brain-derived Neurotrophic Factor (BDNF) gene in the CNS. Methods During the first postnatal week, we exposed infant rats to stressed caretakers that predominately displayed abusive behaviors. We then assessed DNA methylation patterns and gene expression throughout the life span, as well as DNA methylation patterns in the next generation of infants. Results Early maltreatment produced persisting changes in methylation of BDNF DNA that caused altered BDNF gene expression in the adult prefrontal cortex. Furthermore, we observed altered BDNF DNA methylation in offspring of females that had previously experienced the maltreatment regimen. Conclusions These results highlight an epigenetic molecular mechanism potentially underlying lifelong and transgenerational perpetuation of changes in gene expression and behavior incited by early abuse and neglect.
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“Furthermore, the findings suggested germ-line inheritance because cross-fostering could not completely erase these DNA methylation changes.”
From Biological Embedding of Early-Life Adversity and a Scoping Review of the Evidence for Intergenerational Epigenetic Transmission of Stress and Trauma in Humans (2023) · cites this paper as [73]
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“Other animal findings also suggested ELS/CT-related epigenetic changes in the CNS growth and differentiation-related BDNF gene expression (407), while in a genome-wide blood DNA methylation analysis study by Houtepen et al. (408), a locus in the Kit ligand gene (KITLG;”
From Developmental Trajectories of Early Life Stress and Trauma: A Narrative Review on Neurobiological Aspects Beyond Stress System Dysregulation (2019) · cites this paper as [407]
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“Early-life maltreatment of infant rats produced persistent changes in Bdnf DNA methylation that were passed to the next generation by maltreated mothers [73].”
In the citing paper
“Infant maltreatment increases DNA methylation and reduces BDNF gene expression in the PFC (191).”
From A brain-centric model of suicidal behavior (2020) · cites this paper as [191]
In the citing paper
“Differential levels of DNA methylation of genes related to stress reactivity have already been associated with PTSD and early life stress [93-95].”
From Efficacy of oxytocin administration early after psychotrauma in preventing the development of PTSD: study protocol of a randomized controlled trial (2014) · cites this paper as [94]
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“In a related study, adult rats exposed to mistreatment at an early age exhibited higher levels of DNA methylation at CpG sites within the Bdnf promoter as well as decreased levels of Bdnf mRNA.”
From Epigenetic mechanisms of major depression: Targeting neuronal plasticity (2018) · cites this paper as [124]
In the citing paper
“ELS results in hippocampal hypermethylation at the promoter regions of genes related to the stress axis and brain development, including glucocorticoid receptor (NR3c1) region 17 29–31 and brain derived neurotrophic factor (BDNF) region IV32–34.”
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 [32]
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 [32]
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Long-Term Brain and Behavioral Consequences of Early-Life Iron Deficiency
Kennedy, B. C., Wallin, D. J., Tran, P. V., & Georgieff, M. (2016) · Springer eBooks · doi:10.1007/978-3-319-22023-9_15 · Cited by 19
Milbocker, K. A., LeBlanc, G. L., Brengel, E. K., Hekmatyar, K. S., Kulkarni, P. P., Ferris, C. F., & Klintsova, A. Y. (2022) · Scientific Reports · doi:10.1038/s41598-022-14752-3 · Cited by 26
Morc1 knockout evokes a depression-like phenotype in mice
Schmidt, M., Brandwein, C., Luoni, A., Sandrini, P., Calzoni, T., Deuschle, M., Cirulli, F., Riva, M. A., & Gass, P. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.08.005 · Cited by 21
Gene-Environment Interactions in Geriatric Depression
Lotrich, F. E. (2011) · Psychiatric Clinics of North America · doi:10.1016/j.psc.2011.02.003 · Cited by 22
Epigenetic mechanisms in Alzheimer's disease: progress but much to do
Balázs, R., Vernon, J. D. R., & Hardy, J. (2011) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2011.02.024 · Cited by 21
Epigenetics in the nervous system: An overview of its essential role
Kannan, M., & Ravi, B. (2013) · Indian journal of human genetics · doi:10.4103/0971-6866.124357 · Cited by 22
Keller, S. M., Doherty, T. S., & Roth, T. L. (2018) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2018.00126 · Cited by 22
“Exposure to adversity during this time has lifelong implications for the brain and, consequently, behavior (Fride et al., 1985; Heim et al., 1997; Brunson et al., 2001; McEwen, 2003; Lupien et al., 2009; Roth et al., 2009; Blaze and Roth, 2013, 2017; Blaze et al., 2013; Doherty et al., 2017).”
BackgroundMethodResultInfluentialSelf-citationThe Kindling/Sensitization Model and Early Life Stress
Post, R. M. (2020) · Current topics in behavioral neurosciences · doi:10.1007/7854_2020_172 · Cited by 25
Darwin's Finches or Lamarck's Giraffe, Does International Relations Get Evolution Wrong?
Gilady, L., & Hoffmann, M. J. (2013) · International Studies Review · doi:10.1111/misr.12060 · Cited by 21
Elevated Familial Cardiovascular Burden Among Adolescents With Familial Bipolar Disorder
Toma, S., Fıksenbaum, L., Omrin, D. S., & Goldstein, B. I. (2019) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2019.00008 · Cited by 20
How to prevent the malignant progression of bipolar disorder
Post, R. M. (2020) · Brazilian Journal of Psychiatry · doi:10.1590/1516-4446-2020-0874 · Cited by 24
Li, Y., Wu, Z., Zhu, B., Wang, Y., Kan, Y.-Q., & Zeng, H. (2022) · Toxics · doi:10.3390/toxics10080413 · Cited by 22
Hernaus, D., van Winkel, R., Gronenschild, E. H. B. M., Habets, P., Kenis, G., Marcelis, M. C., van Os, J., Myin‐Germeys, I., Collip, D., & (G.R.O.U.P.), F. G. R. A. O. I. P. (2014) · PLoS ONE · doi:10.1371/journal.pone.0092722 · Cited by 25
“adversity, yet differences in the prefrontal cortex (PFC) were present [19].”
BackgroundAgnati, L. F., Barlow, P. W., Baluška, F., Tonin, P., Guescini, M., Leo, G., & Fuxé, K. (2011) · Communicative & Integrative Biology · doi:10.4161/cib.17602 · Cited by 21
PTSD, Endophenotypes, the RDoC, and the DSM-5
Young, G. C. (2014) · Psychological Injury and Law · doi:10.1007/s12207-014-9187-x · Cited by 25
“Sherin and Nemeroff (2011) continued to discuss the typical changes in brain structure, circuitry, and function found using brain-imaging methods in PTSD.”
BackgroundHamelin, S., & Depaulis, A. (2015) · Revue Neurologique · doi:10.1016/j.neurol.2015.01.560 · Cited by 20
“of BDNF following an early life stress [68,70], or a depression [63,119] may facilitate GCD.”
BackgroundNeuroepigenetics of Neurotrophin Signaling: Neurobiology of Anxiety and Affective Disorders
Règue, M., Lanfumey, L., & Mongeau, R. (2018) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2018.03.002 · Cited by 22
Biological determinants of depression following bereavement
Assareh, A. A., Sharpley, C. F., McFarlane, J. R., & Sachdev, P. S. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.12.013 · Cited by 23
Epigenetic Influence of the Social Environment
Champagne, F. A., & Curley, J. P. (2011) · Springer eBooks · doi:10.1007/978-3-642-17426-1_10 · Cited by 20
“2008), and a broad range of environmental exposures (Mueller and Bale 2008; Roth et al. 2009; Weaver et al. 2004) occurring during pre- and postnatal development have implicated epigenetic regulation of gene expression as a critical target of experiencedependent change.”
BackgroundInfluentialGee, D. G. (2022) · American Psychologist · doi:10.1037/amp0001107 · Cited by 22
“…provided novel insight into the role of epigenetic effects, such as regulation of gene expression, in linking early experiences with alterations in corticolimbic circuitry and behavior (McClelland et al., 2011; Roth et al., 2009; Short & Baram, 2019; Torres-Berrío et al., 2019;Weaver et al., 2004).”
BackgroundPalamarchuk, I. S., Slavich, G. M., Vaillancourt, T., & Rajji, T. K. (2023) · BMC Neuroscience · doi:10.1186/s12868-023-00831-2 · Cited by 26
Noncoding RNAs : Emerging regulators of behavioral complexity
Dayal, S., Chaubey, D., Joshi, D. C., Ranmale, S., & Pillai, B. (2024) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1847 · Cited by 22
“Many studies have related these behavioral alterations to experience-dependent epigenetic changes in brain regions such as the mPFC and infralimbic prefrontal cortex Roth et al., 2009; van Harmelen et al., 2010).”
BackgroundKim, J., Stewart, R. J., Kim, J.-W., Kang, H., Lee, J., Kim, S., Kim, S., Shin, I., Hong, Y. J., Ahn, Y., et al. (2019) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2019.06.038 · Cited by 20
Bearer, E. L., & Mulligan, B. S. (2018) · Current Genomics · doi:10.2174/1389202919666180307150508 · Cited by 19
“For physical harm, the adoptive dam model may prove the most promising model to harm by a parent on the child [111-114].”
Kumar, A., Kumar, P., Pareek, V., Faiq, M. A., Narayan, R. K., Raza, K., Prasoon, P., & Sharma, V. K. (2019) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2019.101688 · Cited by 18
The physiology of stress and the human body’s response to stress
Lee, R. S. (2022) · Elsevier eBooks · doi:10.1016/b978-0-12-823039-8.00017-4 · Cited by 22
Benatti, B. M., Adiletta, A., Sgadó, P., Malgaroli, A., Ferro, M., & Lamanna, J. (2024) · Behavioral Sciences · doi:10.3390/bs14100882 · Cited by 23
“It has been demonstrated that ELA can lead to abnormal BDNF methylation and mRNA expression patterns in the hippocampus, PFC, and amygdala [75,101].”
BackgroundMin, J., Lee, H., Lee, S., Park, Y.-M., Kang, S., & Chae, J. (2012) · Neuropsychobiology · doi:10.1159/000342384 · Cited by 21
Neurobiological disease etiology and inheritance: an epigenetic perspective
Saab, B. J., & Mansuy, I. M. (2013) · Journal of Experimental Biology · doi:10.1242/jeb.089995 · Cited by 18
“In this model, although induced by the mother, DNA methylation of the BDNF gene could not be completely reversed by cross-fostering, implying a contribution from epigenetic processes independent of maternal care (Roth et al., 2009).”
BackgroundMultigenerational effects of fetal-neonatal iron deficiency on hippocampal BDNF signaling
Blegen, M. B., Kennedy, B. C., Thibert, K. A., Gewirtz, J. C., Tran, P. V., & Georgieff, M. (2013) · Physiological Reports · doi:10.1002/phy2.96 · Cited by 19
“For example, rats subjected to early maltreatment showed more maltreatment behaviors to their own offspring (Roth et al. 2009) and the transmission of this behavior is accompanied by stable, epigenetic changes to the BDNF gene in the hippocampus and other brain areas (Roth et al. 2010).”
InfluentialSSTR4, childhood adversity, self-efficacy and suicide risk in alcoholics
Berent, D., Emilien, G., Podgórski, M. T., Kusideł, E., Kulczycka-Wojdala, D., Szymańska, B., Macander, M., & Pawłowska, Z. (2017) · Translational Neuroscience · doi:10.1515/tnsci-2017-0013 · Cited by 19
Metadata
- Authors
- Roth, T. L., Lubin, F. D., Funk, A. J., & Sweatt, J. D.
- Affiliations
- University of Alabama (US)
- University of Alabama at Birmingham (US)
- Venue
- Biological Psychiatry
- Publisher
- Elsevier BV
- Published
- 2009-05
- Volume
- 65
- Issue
- 9
- Pages
- 760-769
- ISSN
- 0006-3223 (ISSN-L)
- PMC
- PMC3056389
- OpenAlex
- W1965636455
- Semantic Scholar
- 73b25ed907cfc11b7dfd5f2e6c7e3f05afbe7148
- Cited by
- 1,273
- References
- 75
- Citations by year
- 2026: 26 · 2025: 27 · 2024: 37 · 2023: 38 · 2022: 39 · 2021: 68 · 2020: 78 · 2019: 77 · 2018: 90 · 2017: 91 · 2016: 107 · 2015: 100 · 2014: 145 · 2013: 105 · 2012: 91
- FWCI
- 86.14
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Biological Psychiatry (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute on Aging (R01AG031722)
- National Institute of Mental Health (MH 57014, R01MH057014)
- National Institute of Neurological Disorders and Stroke (NS048811, F32NS048811)
- Topics
- Social Sciences › Psychology › Clinical Psychology › Child Abuse and Trauma
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- childhood adversity, child abuse, brain-derived neurotrophic factor, DNA methylation, epigenetics, transgenerational transmission, prefrontal cortex, gene expression, infant rat model, caregiver abuse, neglect
- MeSH terms
- Animals, Animals, Newborn, Cytidine, Female, Hippocampus, Injections, Intraventricular, Male, Maternal Behavior, Stress, Psychological, Gene Expression, Prefrontal Cortex, DNA Methylation, Brain-Derived Neurotrophic Factor, Rats, Long-Evans, Models, Animal, Epigenesis, Genetic, Rats
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