Childhood maltreatment and methylation of FK506 binding protein 5 gene (FKBP5)

Tyrka, Audrey R.; Ridout, Kathryn K.; Parade, Stephanie H.; Paquette, Alison; Marsit, Carmen J.; Seifer, Ronald

doi:10.1017/s0954579415000991

Cited by 118Child Abuse and TraumaEpigenetics and DNA MethylationStress Responses and Cortisol

Childhood maltreatment and methylation of FK506 binding protein 5 gene (FKBP5)

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Tyrka, Audrey R., Ridout, Kathryn K., Parade, Stephanie H., Paquette, Alison, Marsit, Carmen J., Seifer, Ronald·2015·Development and Psychopathology

DOI 10.1017/s0954579415000991PMC PMC4870720

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Abstract

A growing body of evidence suggests that alterations of the stress response system may be a mechanism by which childhood maltreatment alters risk for psychopathology. FK506 binding protein 51 (FKBP5) binds to the glucocorticoid receptor and alters its ability to respond to stress signaling. The aim of the present study was to examine methylation of the FKBP5 gene (FKBP5), and the role of an FKBP5 genetic variant, in relation to childhood maltreatment in a sample of impoverished preschool-aged children. One hundred seventy-four families participated in this study, including 69 with child welfare documentation of moderate to severe maltreatment in the past 6 months. The children, who ranged in age from 3 to 5 years, were racially and ethnically diverse. Structured record review and interviews in the home were used to assess a history of maltreatment, other traumas, and contextual life stressors; and a composite variable assessed the number exposures to these adversities. Methylation of two sites in intron 7 of FKBP5 was measured via sodium bisulfite pyrosequencing. Maltreated children had significantly lower levels of methylation at both CpG sites (p < .05). Lifetime contextual stress exposure showed a trend for lower levels of methylation at one of the sites, and a trend for an interaction with the FKBP5 polymorphism. A composite adversity variable was associated with lower levels of methylation at one of the sites as well (p < .05). FKBP5 alters glucocorticoid receptor responsiveness, and FKBP5 gene methylation may be a mechanism of the biobehavioral effects of adverse exposures in young children.

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Polygenic scores for Environmental Sensitivity have been shown to moderate the beneficial outcomes of cognitive behavioural therapy on anxiety symptoms, and genome-wide and single locus variation in the SCL6A4 gene the impact of good parenting quality on youth psychopathology.
“Polygenic scores for Environmental Sensitivity have been shown to moderate the beneficial outcomes of cognitive behavioural therapy on anxiety symptoms,89 and genome-wide and single locus variation in the SCL6A4 gene the impact of good parenting quality on youth psychopathology.89,90”
From The role of epigenetics in psychological resilience (2021) · cites this paper as [89]

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González, A. (2013) · Paediatrics & Child Health · doi:10.1093/pch/18.8.415 · Cited by 110 · see citing works
A measure of glucocorticoid load provided by DNA methylation of Fkbp5 in mice
Lee, R. S., Tamashiro, K. L., Yang, X., Purcell, R. H., Huo, Y., Rongione, M. A., Potash, J. B., & Wand, G. S. (2011) · Psychopharmacology · doi:10.1007/s00213-011-2307-3 · Cited by 109 · see citing works
Cognitive deficits induced in young rats by long-term corticosterone administration
Dachir, S., Kadar, T., Robinzon, B., & Levy, A. (1993) · Behavioral and Neural Biology · doi:10.1016/0163-1047(93)90173-f · Cited by 105 · see citing works
Alterations in DNA methylation of Fkbp5 as a determinant of blood–brain correlation of glucocorticoid exposure
Ewald, E. R., Wand, G. S., Seifuddin, F., Yang, X., Tamashiro, K. L., Potash, J. B., Zandi, P., & Lee, R. S. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.03.003 · Cited by 105 · see citing works
Glucocorticoid Sensitivity in Mood Disorders
Spijker, A. T., & van Rossum, E. F. C. (2011) · Neuroendocrinology · doi:10.1159/000329846 · Cited by 102 · see citing works
Effects of childhood trauma on HPA-axis reactivity in women free of lifetime psychopathology
Klaassens, E. R., van Noorden, M. S., Giltay, E. J., van Pelt, J., van Veen, T., & Zitman, F. G. (2009) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2009.04.011 · Cited by 101 · cited 3× · see citing works
“…of adults with a history of early life stress show attenuated cortisol response to stress (Carpenter et al., 2007, 2009; Carpenter, Shattuck, Tyrka, Geracioti, & Price, 2011; Elzinga et al., 2008; Klaassens et al., 2009), suggesting that the physiologic effects of maltreatment are long lasting.”
Background
FKBP5 polymorphism is associated with major depression but not with bipolar disorder
Szczepankiewicz, A., Leszczyńska-Rodziewicz, A., Pawlak, J., Narozna, B., Rajewska-Rager, A., Wilkosc, M., Zaremba, D., Maciukiewicz, M., & Twarowska-Hauser, J. (2014) · Journal of Affective Disorders · doi:10.1016/j.jad.2014.04.002 · Cited by 100 · see citing works
Epigenetics and depressive disorders: a review of current progress and future directions
Januar, V., Saffery, R., & Ryan, J. (2015) · International Journal of Epidemiology · doi:10.1093/ije/dyu273 · Cited by 99 · see citing works
Longitudinal Patterns of Cortisol Regulation Differ in Maltreated and Nonmaltreated Children
Doom, J. R., Cicchetti, D., & Rogosch, F. A. (2014) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1016/j.jaac.2014.08.006 · Cited by 98 · see citing works
HPA-axis reactivity interacts with stage of pubertal development to predict the onset of depression
Colich, N. L., Kircanski, K., Foland‐Ross, L. C., & Gotlib, I. H. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2015.02.004 · Cited by 92 · see citing works
FKBP5 allele-specific epigenetic modification in gene by environment interaction
Klengel, T., & Binder, E. B. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2014.208 · Cited by 84 · see citing works
Child maltreatment, inflammation, and internalizing symptoms: Investigating the roles of C-reactive protein, gene variation, and neuroendocrine regulation
Cicchetti, D., Handley, E. D., & Rogosch, F. A. (2015) · Development and Psychopathology · doi:10.1017/s0954579415000152 · Cited by 76 · see citing works
FKBP5 genotype-dependent DNA methylation and mRNA regulation after psychosocial stress in remitted depression and healthy controls
Hohne, N., Poidinger, M., Merz, F., Pfister, H., Bruckl, T., Zimmermann, P., Uhr, M., Holsboer, F., & Ising, M. (2015) · International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyu087 · Cited by 74 · see citing works
Differences in the response to the combined DEX-CRH test between PTSD patients with and without co-morbid depressive disorder
de Kloet, C. S., Vermetten, E. H. G. J. M., Lentjes, E. G. W. M., Geuze, E., PELT, J. V., Manuel, R., Heijnen, C. J., & Westenberg, H. G. M. (2008) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2007.11.016 · Cited by 71 · see citing works
Exposure to childhood trauma is associated with altered n-back activation and performance in healthy adults: implications for a commonly used working memory task
Philip, N. S., Sweet, L. H., Tyrka, A. R., Carpenter, S. L., Albright, S. E., Price, L. H., & Carpenter, L. L. (2015) · Brain Imaging and Behavior · doi:10.1007/s11682-015-9373-9 · Cited by 67 · see citing works
Self-citation
Post-Dexamethasone Cortisol, Self-Inflicted Injury, and Suicidal Ideation Among Depressed Adolescent Girls
Beauchaine, T. P., Crowell, S. E., & Hsiao, R. C.-J. (2014) · Research on Child and Adolescent Psychopathology · doi:10.1007/s10802-014-9933-2 · Cited by 64 · see citing works
Organization and function of the FKBP52 and FKBP51 genes
Cioffi, D. L., Hubler, T. R., & Scammell, J. G. (2011) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2011.03.013 · Cited by 64 · see citing works
Methylation of exons 1D, 1F, and 1Hof the glucocorticoid receptor gene promoter and exposure to adversity in preschool-aged children
Tyrka, A. R., Parade, S. H., Eslinger, N. M., Marsit, C. J., Lesseur, C., Armstrong, D. A., Philip, N. S., Josefson, B., & Seifer, R. (2015) · Development and Psychopathology · doi:10.1017/s0954579415000176 · Cited by 60 · see citing works
Self-citation
Glucocorticoid receptor gene methylation and HPA-axis regulation in adolescents. The TRAILS study
van der Knaap, L. J., Oldehinkel, A. J., Verhulst, F. C., van Oort, F. V. A., & Riese, H. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2015.04.012 · Cited by 60 · see citing works
Self- or parent report of (co-occurring) internalizing and externalizing problems, and basal or reactivity measures of HPA-axis functioning: A systematic evaluation of the internalizing-hyperresponsivity versus externalizing-hyporesponsivity HPA-axis hypothesis
Hartman, C. A., Hermanns, V. W., de Jong, P. J., & Ormel, J. (2013) · Biological Psychology · doi:10.1016/j.biopsycho.2013.05.009 · Cited by 58 · see citing works
How Much Does “How Much” Matter? Assessing the Relationship Between Children’s Lifetime Exposure to Violence and Trauma Symptoms, Behavior Problems, and Parenting Stress
Hickman, L. J., Jaycox, L. H., Setodji, C. M., Kofner, A., Schultz, D. J., Barnes‐Proby, D., & Harris, R. (2012) · Journal of Interpersonal Violence · doi:10.1177/0886260512468239 · Cited by 57 · see citing works
FKBP5 moderation of depressive symptoms in peer victimized, post-institutionalized children
VanZomeren‐Dohm, A., Pitula, C. E., Koss, K. J., Thomas, K. M., & Gunnar, M. R. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.10.003 · Cited by 56 · see citing works
Role of epigenetic factors in the development of mental illness throughout life
Guintivano, J., & Kaminsky, Z. A. (2014) · Neuroscience Research · doi:10.1016/j.neures.2014.08.003 · Cited by 54 · see citing works
HPA-axis activity and externalizing behavior problems in early adolescents from the general population: The role of comorbidity and gender
Marsman, R., Willemsen‐Swinkels, S. H. N., Rosmalen, J. G. M., Oldehinkel, A. J., Ormel, J., & Buitelaar, J. K. (2008) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2008.03.005 · Cited by 54 · see citing works
Dissection of glucocorticoid receptor-mediated inhibition of the hypothalamic–pituitary–adrenal axis by gene targeting in mice
Laryea, G. N., Muglia, L. M., Arnett, M. G., & Muglia, L. J. (2014) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2014.09.002 · Cited by 53 · see citing works
Genetic fingerprinting in mouthwashes of patients after allogeneic bone marrow transplantation
Endler, G., Greinix, H., Winkler, K., Mitterbauer, G., & Mannhalter, C. (1999) · Bone Marrow Transplantation · doi:10.1038/sj.bmt.1701815 · Cited by 51 · see citing works
Telomeres, Early-Life Stress and Mental Illness
Ridout, S. J., Ridout, K. K., Kao, H., Carpenter, L. L., Philip, N. S., Tyrka, A. R., & Price, L. H. (2015) · Advances in psychosomatic medicine · doi:10.1159/000369088 · Cited by 47 · see citing works
Self-citation
Effect of the common functional FKBP5 variant (rs1360780) on the hypothalamic-pituitary-adrenal axis and peripheral blood gene expression
Fujii, T., Hori, H., Ota, M., Hattori, K., Teraishi, T., Sasayama, D., Yamamoto, N., Higuchi, T., & Kunugi, H. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.01.007 · Cited by 45 · see citing works
Childhood maltreatment and stress-related psychopathology: the epigenetic memory hypothesis
Lutz, P.-E., Almeida, D., Fiori, L., & Turecki, G. (2015) · Current Pharmaceutical Design · doi:10.2174/1381612821666150105124928 · Cited by 44 · see citing works
Neural plasticity, sensitive periods, and psychopathology
Cicchetti, D. (2015) · Development and Psychopathology · doi:10.1017/s0954579415000012 · Cited by 41 · see citing works
Methylation of NR3C1 and SLC6A4 and internalizing problems. The TRAILS study
van der Knaap, L. J., van Oort, F. V. A., Verhulst, F. C., Oldehinkel, A. J., & Riese, H. (2015) · Journal of Affective Disorders · doi:10.1016/j.jad.2015.03.056 · Cited by 40 · see citing works
Biological embedding in mental health: An epigenomic perspective
Sasaki, A., de Vega, W. C., & McGowan, P. O. (2013) · Biochemistry and Cell Biology · doi:10.1139/bcb-2012-0070 · Cited by 40 · see citing works
A role for synapsin in FKBP51 modulation of stress responsiveness: Convergent evidence from animal and human studies
Schmidt, U., Buell, D. R., Ionescu, I. A., Gassen, N. C., Holsboer, F., Cox, M. B., Novak, B., Huber, C. W., Hartmann, J., Schmidt, M. V., et al. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.11.005 · Cited by 32 · see citing works
Blunted stress cortisol reactivity and failure to acclimate to familiar stress in depressed and sub-syndromal children
Suzuki, H., Belden, A. C., Spitznagel, E. L., Dietrich, R., & Luby, J. L. (2013) · Psychiatry Research · doi:10.1016/j.psychres.2013.06.038 · Cited by 31 · see citing works
Interleukin 1B gene (IL1B) variation and internalizing symptoms in maltreated preschoolers
Ridout, K. K., Parade, S. H., Seifer, R., Price, L. H., Gelernter, J. E., Feliz, P., & Tyrka, A. R. (2014) · Development and Psychopathology · doi:10.1017/s0954579414001023 · Cited by 28 · see citing works
Self-citation
Cortisol response to cosyntropin administration in military veterans with or without posttraumatic stress disorder
Golier, J. A., Caramanica, K., Makotkine, I., Sher, L., & Yehuda, R. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.10.020 · Cited by 21 · see citing works
Possible association between haplotypes of the FKBP5 gene and suicidal bipolar disorder, but not with melancholic depression and psychotic features, in the course of bipolar disorder
Leszczyńska-Rodziewicz, A., Szczepankiewicz, A., Skibińska, M., Pawlak, J., Dmitrzak‐Węglarz, M., Hauser, J., & Narożna, B. (2014) · Neuropsychiatric Disease and Treatment · doi:10.2147/ndt.s54538 · Cited by 19 · see citing works
Relationship of the FKBP5 C/T polymorphism with dysfunctional attitudes predisposing to depression.
Suzuki, A., Matsumoto, Y., Sadahiro, R., Enokido, M., Goto, K., & Otani, K. (2014) · Comprehensive Psychiatry · doi:10.1016/j.comppsych.2014.04.019 · Cited by 10 · see citing works

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Understanding the Molecular Mechanisms Underpinning Gene by Environment Interactions in Psychiatric Disorders: The FKBP5 Model
Matosin, N., Halldorsdottir, T., & Binder, E. B. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.01.021 · Cited by 226 · see citing works
Epigenetic Pathways in Human Disease: The Impact of DNA Methylation on Stress-Related Pathogenesis and Current Challenges in Biomarker Development
Argentieri, M. A., Nagarajan, S., Seddighzadeh, B., Baccarelli, A., & Shields, A. E. (2017) · EBioMedicine · doi:10.1016/j.ebiom.2017.03.044 · Cited by 189 · see citing works
A systematic review of childhood maltreatment and DNA methylation: candidate gene and epigenome-wide approaches
Parade, S. H., Huffhines, L. P., Daniels, T. E., Stroud, L. R., Nugent, N. R., & Tyrka, A. R. (2021) · Translational Psychiatry · doi:10.1038/s41398-021-01207-y · Cited by 177 · see citing works
Self-citation
Childhood maltreatment and DNA methylation: A systematic review
Cecil, C. A. M., Zhang, Y., & Nolte, T. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.02.019 · Cited by 171 · see citing works
Epigenetic programming by stress and glucocorticoids along the human lifespan
Zannas, A. S., & Chrousos, G. P. (2017) · Molecular Psychiatry · doi:10.1038/mp.2017.35 · Cited by 158 · see citing works
Translating basic research knowledge on the biological embedding of early-life stress into novel approaches for the developmental programming of lifelong health
Heim, C. M., Entringer, S., & Buss, C. (2019) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2018.12.011 · Cited by 158 · see citing works
DNA methylation differences at the glucocorticoid receptor gene in depression are related to functional alterations in hypothalamic-pituitary-adrenal axis activity and to early life emotional abuse
Farrell, C., Doolin, K., O’ Leary, N., Jairaj, C., Roddy, D., Tozzi, L., Morris, D., Harkin, A., Frodl, T., Nemoda, Z., et al. (2018) · Psychiatry Research · doi:10.1016/j.psychres.2018.04.064 · Cited by 144 · see citing works
Hsp90 and FKBP51: complex regulators of psychiatric diseases
Criado‐Marrero, M., Rein, T., Binder, E. B., Porter, J. T., Koren, J., & Blair, L. J. (2017) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2016.0532 · Cited by 145 · see citing works
Adverse childhood experiences, epigenetics and telomere length variation in childhood and beyond: a systematic review of the literature
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 125 · see citing works
The role of epigenetics in psychological resilience
Smeeth, D., Beck, S., Karam, E. G., & Pluess, M. (2021) · The Lancet Psychiatry · doi:10.1016/s2215-0366(20)30515-0 · Cited by 108 · see citing works
DNA methylation at stress‐related genes is associated with exposure to early life institutionalization
Non, A. L., Hollister, B. M., Humphreys, K. L., Childebayeva, A., Esteves, K. C., Zeanah, C. H., Fox, N. A., Nelson, C. A., & Drury, S. S. (2016) · American Journal of Physical Anthropology · doi:10.1002/ajpa.23010 · Cited by 107 · see citing works
How Stress Gets Under the Skin: Early Life Adversity and Glucocorticoid Receptor Epigenetic Regulation
Liu, P. Z., & Nusslock, R. (2017) · Current Genomics · doi:10.2174/1389202919666171228164350 · Cited by 102 · see citing works
Associations among oxytocin receptor gene (OXTR) DNA methylation in adulthood, exposure to early life adversity, and childhood trajectories of anxiousness
Gouin, J.-P., Zhou, Q. Q., Booij, L., Boivin, M., Côté, S. M., Hébert, M., Ouellet‐Morin, I., Moshe Szyf, A., Tremblay, R. E., Turecki, G., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-07950-x · Cited by 102 · see citing works
Influence of FKBP5 polymorphism and DNA methylation on structural changes of the brain in major depressive disorder
Han, K., Won, E., Sim, Y., Kang, J. C., Han, C., Kim, Y., Kim, S., Joe, S.-H., Lee, M.-S., Tae, W., et al. (2017) · Scientific Reports · doi:10.1038/srep42621 · Cited by 96 · see citing works
Identification of dynamic glucocorticoid-induced methylation changes at the FKBP5 locus
Wiechmann, T., Röh, S., Sauer, S., Czamara, D., Arloth, J., Ködel, M., Beintner, M., Knop, L., Menke, A., Binder, E. B., et al. (2019) · Clinical Epigenetics · doi:10.1186/s13148-019-0682-5 · Cited by 81 · see citing works
Adverse Childhood Events and Health Biomarkers: A Systematic Review
Soares, S., Rocha, V., Kelly‐Irving, M., Stringhini, S., & Fraga, S. J. D. S. (2021) · Frontiers in Public Health · doi:10.3389/fpubh.2021.649825 · Cited by 91 · see citing works
Methylation of the glucocorticoid receptor gene, nuclear receptor subfamily 3, group C, member 1 ( NR3C1 ), in maltreated and nonmaltreated children: Associations with behavioral undercontrol, emotional lability/negativity, and externalizing and internalizing symptoms
Cicchetti, D., & Handley, E. D. (2017) · Development and Psychopathology · doi:10.1017/s0954579417001407 · Cited by 87 · see citing works
Advance in Stress for Depressive Disorder
Ding, Y., & Dai, J. (2019) · Advances in experimental medicine and biology · doi:10.1007/978-981-32-9271-0_8 · Cited by 82 · see citing works
The effects of childhood maltreatment on epigenetic regulation of stress-response associated genes: An intergenerational approach
Ramo-Fernández, L., Boeck, C., Koenig, A. M., Schury, K., Binder, E. B., Gündel, H., Fegert, J. M., Karabatsiakis, A., & Kolassa, I.-T. (2019) · Scientific Reports · doi:10.1038/s41598-018-36689-2 · Cited by 67 · see citing works
Cortisol and cardiometabolic disease: a target for advancing health equity
Ortiz, R., Kluwe, B., Lazarus, S. A., Teruel, M. N., & Joseph, J. J. (2022) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2022.08.002 · Cited by 73 · see citing works
Early Childhood Stress and Child Age Predict Longitudinal Increases in Obesogenic Eating Among Low-Income Children
Miller, A. L., Gearhardt, A. N., Retzloff, L., Sturza, J. S., Kaciroti, N., & Lumeng, J. C. (2018) · Academic Pediatrics · doi:10.1016/j.acap.2018.01.007 · Cited by 54 · see citing works
Childhood maltreatment, behavioral adjustment, and molecular markers of cellular aging in preschool-aged children: A cohort study
Ridout, K. K., Parade, S. H., Kao, H., Magnan, S., Seifer, R., Porton, B., Price, L. H., & Tyrka, A. R. (2019) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2019.05.015 · Cited by 51 · see citing works
Self-citation
FKBP5 DNA methylation does not mediate the association between childhood maltreatment and depression symptom severity in the Detroit Neighborhood Health Study
Bustamante, A. C., Aiello, A. E., Guffanti, G., Galea, S., Wildman, D. E., & Uddin, M. (2018) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2017.09.016 · Cited by 50 · see citing works
The Disease-Associated Chaperone FKBP51 Impairs Cognitive Function by Accelerating AMPA Receptor Recycling
Blair, L. J., Criado‐Marrero, M., Zheng, D., Wang, X., Kamath, S. G., Nordhues, B. A., Weeber, E. J., & Dickey, C. A. (2019) · eNeuro · doi:10.1523/eneuro.0242-18.2019 · Cited by 47 · see citing works
Harsh Parenting Predicts Novel HPA Receptor Gene Methylation and NR3C1 Methylation Predicts Cortisol Daily Slope in Middle Childhood
Lewis, C. R., Breitenstein, R. S., Henderson-Smith, A., Sowards, H., Piras, I. S., Huentelman, M. J., Doane, L. D., & Lemery‐Chalfant, K. (2020) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-020-00885-4 · Cited by 44 · see citing works
Childhood Maltreatment and Headache Disorders
Tietjen, G. E. (2016) · Current Pain and Headache Reports · doi:10.1007/s11916-016-0554-z · Cited by 43 · see citing works
Environmentally Induced Epigenetic Plasticity in Development: Epigenetic Toxicity and Epigenetic Adaptation
Tian, F., & Marsit, C. J. (2018) · Current Epidemiology Reports · doi:10.1007/s40471-018-0175-7 · Cited by 40 · see citing works
Self-citation
Targeted bisulfite sequencing: A novel tool for the assessment of DNA methylation with high sensitivity and increased coverage
Moser, D., Müller, S., Hummel, E. M., Limberg, A., Dieckmann, L., Frach, L., Pakusch, J., Flasbeck, V., Brüne, M., Beygo, J., et al. (2020) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2020.104784 · Cited by 39 · see citing works
Crack cocaine addiction, early life stress and accelerated cellular aging among women
Levandowski, M. L., Tractenberg, S. G., de Azeredo, L. A., Nardi, T. D., Rovaris, D. L., Bau, C. H. D., Rizzo, L. B., Maurya, P. K., Brietzke, E. M., Tyrka, A. R., et al. (2016) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2016.06.009 · Cited by 39 · see citing works
Self-citation
Bridging Basic and Clinical Research in Early Life Adversity, DNA Methylation, and Major Depressive Disorder
Brown, A., Fiori, L. M., & Turecki, G. (2019) · Frontiers in Genetics · doi:10.3389/fgene.2019.00229 · Cited by 39 · see citing works
Childhood Maltreatment and Longitudinal Epigenetic Aging
Chang, O. D., Meier, H. C. S., Maguire‐Jack, K., Davis-Kean, P. E., & Mitchell, C. M. (2024) · JAMA Network Open · doi:10.1001/jamanetworkopen.2024.21877 · Cited by 33 · see citing works
History of child maltreatment and telomere length in immune cell subsets: Associations with stress- and attachment-related hormones
Boeck, C., Krause, S., Karabatsiakis, A., Schury, K., Gündel, H., Waller, C., & Kolassa, I. (2017) · Development and Psychopathology · doi:10.1017/s0954579417001055 · Cited by 32 · see citing works
Adverse Childhood Experiences and Methylation of the FKBP5 Gene in Patients with Psychotic Disorders
Misiak, B., Karpiński, P., Szmida, E., Grąźlewski, T., Jabłoński, M., Cyranka, K., Rymaszewska, J., Piotrowski, P., Kotowicz, K., & Frydecka, D. (2020) · Journal of Clinical Medicine · doi:10.3390/jcm9123792 · Cited by 32 · see citing works
Peripheral DNA methylation of HPA axis-related genes in humans: Cross-tissue convergence, two-year stability and behavioural and neural correlates.
Sante, J. D., Ismaylova, E., Nemoda, Z., Gouin, J., Yu, W.-J., Caldwell, W., Vitaro, F., Szyf, M., Tremblay, R., & Booij, L. (2018) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2018.07.019 · Cited by 27 · see citing works
Childhood maltreatment and DNA methylation: A systematic review
Rubens, M., Bruenig, D., Adams, J. A. M., Suresh, S. M., Sathyanarayanan, A., Haslam, D. M., Shenk, C. E., Mathews, B., & Mehta, D. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105079 · Cited by 31 · see citing works
The effects of early trauma and the FKBP5 gene on PTSD and the HPA axis in a clinical sample of Gulf War veterans
Young, D. A., Inslicht, S. S., Metzler, T. J., Neylan, T. C., & Ross, J. A. (2018) · Psychiatry Research · doi:10.1016/j.psychres.2018.03.037 · Cited by 30 · see citing works
Dissecting the molecular mechanisms of gene x environment interactions: implications for diagnosis and treatment of stress-related psychiatric disorders
Binder, E. B. (2017) · European Journal of Psychotraumatology · doi:10.1080/20008198.2017.1412745 · Cited by 29 · see citing works
Medical morbidities and DNA methylation of NR3C1 in preterm infants
Giarraputo, J., DeLoach, J., Padbury, J. F., Uzun, A., Marsit, C. J., Hawes, K., & Lester, B. M. (2016) · Pediatric Research · doi:10.1038/pr.2016.185 · Cited by 29 · see citing works
Self-citation
Epigenetic Mechanisms Activated by Childhood Adversity
Krause, B. J., Artigas, R., Sciolla, A., & Hamilton, J. (2020) · Epigenomics · doi:10.2217/epi-2020-0042 · Cited by 29 · see citing works
360-Degree Perspectives on Obesity
Cuciureanu, M. D., Caratașu, C.-C., Gabrielian, L., Frăsinariu, O. E., Checheriță, L. E., Trandafir, L. M., Stanciu, G. D., Szilagyi, A., Pogonea, I., Bordeianu, G., et al. (2023) · Medicina · doi:10.3390/medicina59061119 · Cited by 31 · see citing works
Association between childhood maltreatment, psychopathology and DNA methylation of genes involved in stress regulation: Evidence from a study in Borderline Personality Disorder
Flasbeck, V., & Brüne, M. (2021) · PLoS ONE · doi:10.1371/journal.pone.0248514 · Cited by 29 · see citing works
Childhood Trauma and Epigenetics: State of the Science and Future
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Authors: Tyrka, A. R., Ridout, K. K., Parade, S. H., Paquette, A., Marsit, C. J., & Seifer, R.
Affiliations: Brown University (US)
Dartmouth College (US)
Corresponding author: Tyrka, Audrey R.
ORCID: Tyrka, Audrey R.
Ridout, Kathryn K.
Parade, Stephanie H.
Paquette, Alison
Marsit, Carmen J.
Seifer, Ronald
Venue: Development and Psychopathology
Publisher: Cambridge University Press (CUP)
Published: 2015-11
Volume: 27
Issue: 4pt2
Pages: 1637-1645
ISSN: 0954-5794 (ISSN-L)
1469-2198
DOI: 10.1017/s0954579415000991
PMC: PMC4870720
OpenAlex: W2163901153
Cited by: 118
References: 118
Citations by year: 2026: 6 · 2025: 15 · 2024: 10 · 2023: 12 · 2022: 9 · 2021: 10 · 2020: 11 · 2019: 11 · 2018: 11 · 2017: 16 · 2016: 7
FWCI: 14.07
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.cambridge.org/core/terms (unspecified, 3 d)
Locations: Development and Psychopathology (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute of Mental Health (R25MH101076, R01MH083704)
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: child abuse, FKBP5, DNA methylation, glucocorticoid receptor, epigenetics, contextual stress, adversity exposure, preschool children, child welfare, psychopathology risk, stress system
MeSH terms: Tacrolimus Binding Protein 5, Child Abuse, Child, Preschool, Female, Humans, Male, Polymorphism, Genetic, Poverty, Risk, Stress, Psychological, DNA Methylation, Tacrolimus Binding Proteins

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Childhood maltreatment and methylation of FK506 binding protein 5 gene (FKBP5)

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