Epigenetics and the regulation of stress vulnerability and resilience
Open accessAbstract
The human brain has a remarkable capacity to adapt to and learn from a wide range of variations in the environment. However, environmental challenges can also precipitate psychiatric disorders in susceptible individuals. Why any given experience should induce one brain to adapt while another is edged toward psychopathology remains poorly understood. Like all aspects of psychological function, both nature (genetics) and nurture (life experience) sculpt the brain's response to stressful stimuli. Here we review how these two influences intersect at the epigenetic regulation of neuronal gene transcription, and we discuss how the regulation of genomic DNA methylation near key stress-response genes may influence psychological susceptibility or resilience to environmental stressors. Our goal is to offer a perspective on the epigenetics of stress responses that works to bridge the gap between the study of this molecular process in animal models and its potential usefulness for understanding stress vulnerabilities in humans.
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
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?
Genes related to HPA axis regulation, especially NR3C1, are among the most promising epigenetic biomarkers for identifying individuals susceptible to maladaptive responses to psychological stressors and could serve as surrogate markers of HPA axis activity when comparing different treatment modalities.
“genes related to HPA axis regulation, especially NR3C1, are among the most promising epigenetic biomarkers, which are currently explored regarding their predictive potential at identifying individuals susceptible to maladaptive responses to psychological stressors, and could also serve as surrogate markers of HPA axis activity, when comparing different treatment modalities (Zannas & West, 2014)”
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 Zannas & West, 2014
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Diagnostic and Statistical Manual of Mental Disorders
Williams, J. B. W., & First, M. B. (2013) · Oxford University Press eBooks · doi:10.1093/acrefore/9780199975839.013.104 · Cited by 109,841 · see citing works
Diagnostic and Statistical Manual of Mental Disorders
(2012) · Springer eBooks · doi:10.1007/springerreference_121117 · Cited by 20,769 · see citing works
Diagnostic and Statistical Manual of Mental Disorders.
Widiger, T. A. (2000) · Oxford University Press eBooks · doi:10.1037/10518-009 · Cited by 19,767 · see citing works
Multiplex Genome Engineering Using CRISPR/Cas Systems
Cong, L., Ran, F. A., Cox, D., Lin, S., Barretto, R., Habib, N., Hsu, P. D., Wu, X., Jiang, W., Marraffini, L. A., et al. (2013) · Science · doi:10.1126/science.1231143 · Cited by 15,339 · see citing works
RNA-Guided Human Genome Engineering via Cas9
Mali, P., Yang, L., Esvelt, K. M., Aach, J., Guell, M., DiCarlo, J. E., Norville, J. E., & Church, G. M. (2013) · Science · doi:10.1126/science.1232033 · Cited by 9,210 · see citing works
Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene
Caspi, A., Sugden, K., Moffitt, T. E., Taylor, A., Craig, I. W., Harrington, H., McClay, J., Mill, J., Martin, J., Braithwaite, A., et al. (2003) · Science · doi:10.1126/science.1083968 · Cited by 8,120 · see citing works
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 · see citing works
Repurposing CRISPR as an RNA-Guided Platform for Sequence-Specific Control of Gene Expression
Qi, L. S., Larson, M. H., Gilbert, L. A., Doudna, J. A., Weissman, J. S., Arkin, A. P., & Lim, W. A. (2013) · Cell · doi:10.1016/j.cell.2013.02.022 · Cited by 5,016 · see citing works
Human DNA methylomes at base resolution show widespread epigenomic differences
Lister, R., Pelizzola, M., Dowen, R. H., Hawkins, R. D., Hon, G., Tonti-Filippini, J., Nery, J. R., Lee, L., Ye, Z., Ngo, Q.-M., et al. (2009) · Nature · doi:10.1038/nature08514 · Cited by 4,673 · see citing works
ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering
Gaj, T., Gersbach, C. A., & Barbas, C. F. (2013) · Trends in Biotechnology · doi:10.1016/j.tibtech.2013.04.004 · Cited by 3,820 · see citing works
CRISPR-Mediated Modular RNA-Guided Regulation of Transcription in Eukaryotes
Gilbert, L. A., Larson, M. H., Morsut, L., Liu, Z., Brar, G. A., Torres, S. E., Stern-Ginossar, N., Brandman, O., Whitehead, E. H., Doudna, J. A., et al. (2013) · Cell · doi:10.1016/j.cell.2013.06.044 · Cited by 3,696 · see citing works
Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse
McGowan, P. O., Sasaki, A., D'Alessio, A. C., Dymov, S., Labonté, B., Szyf, M., Turecki, G., & Meaney, M. J. (2009) · Nature Neuroscience · doi:10.1038/nn.2270 · Cited by 3,531 · see citing works
Nan, X., Ng, H.-H., Johnson, C. A., Laherty, C. D., Turner, B. M., Eisenman, R. N., & Bird, A. (1998) · Nature · doi:10.1038/30764 · Cited by 3,440 · see citing works
Genetic Epidemiology of Major Depression: Review and Meta-Analysis
Sullivan, P. F., Neale, M. C., & Kendler, K. S. (2000) · American Journal of Psychiatry · doi:10.1176/appi.ajp.157.10.1552 · Cited by 3,431 · see citing works
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 · see citing works
Psychological Stress and Disease
Cohen, S., Janicki-Deverts, D., & Miller, G. E. (2007) · JAMA · doi:10.1001/jama.298.14.1685 · Cited by 3,168 · see citing works
Efficient genome editing in zebrafish using a CRISPR-Cas system
Hwang, W. Y., Fu, Y., Reyon, D., Maeder, M. L., Tsai, S. Q., Sander, J. D., Peterson, R. T., Yeh, J.-R. J., & Joung, J. K. (2013) · Nature Biotechnology · doi:10.1038/nbt.2501 · Cited by 2,937 · see citing works
The Concepts of Stress and Stress System Disorders: Overview of Physical and Behavioral Homeostasis
Chrousos, G. P. (1992) · JAMA · doi:10.1001/jama.1992.03480090092034 · Cited by 2,689 · see citing works
Genome-scale DNA methylation maps of pluripotent and differentiated cells
Meissner, A., Mikkelsen, T. S., Gu, H., Wernig, M., Hanna, J., Sivachenko, A., Zhang, X., Bernstein, B. E., Nusbaum, C., Jaffe, D. B., et al. (2008) · Nature · doi:10.1038/nature07107 · Cited by 2,536 · see citing works
Causal Relationship Between Stressful Life Events and the Onset of Major Depression
Kendler, K. S., Karkowski, L. M., & Prescott, C. A. (1999) · American Journal of Psychiatry · doi:10.1176/ajp.156.6.837 · Cited by 2,486 · see citing works
RNA-guided editing of bacterial genomes using CRISPR-Cas systems
Jiang, W., Bikard, D., Cox, D., Zhang, F., & Marraffini, L. A. (2013) · Nature Biotechnology · doi:10.1038/nbt.2508 · Cited by 2,429 · see citing works
Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress
Berton, O., McClung, C. A., DiLeone, R. J., Krishnan, V., Renthal, W., Russo, S. J., Graham, D., Tsankova, N. M., Bolanos, C. A., Rios, M., et al. (2006) · Science · doi:10.1126/science.1120972 · Cited by 2,129 · see citing works
EUKARYOTIC CYTOSINE METHYLTRANSFERASES
Goll, M. G., & Bestor, T. H. (2005) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.74.010904.153721 · Cited by 2,066 · see citing works
McEwen, B. S. (2008) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2007.11.071 · Cited by 1,864 · see citing works
Targeted genome engineering in human cells with the Cas9 RNA-guided endonuclease
Cho, S. W., Kim, S., Kim, J. M., & Kim, J.-S. (2013) · Nature Biotechnology · doi:10.1038/nbt.2507 · Cited by 1,863 · see citing works
Global epigenomic reconfiguration during mammalian brain development
Lister, R., Mukamel, E. A., Nery, J. R., Urich, M., Puddifoot, C. A., Johnson, N. D., Lucero, J., Huang, Y., Dwork, A. J., Schultz, M. D., et al. (2013) · Science · doi:10.1126/science.1237905 · Cited by 1,830 · see citing works
The link between childhood trauma and depression: insights from HPA axis studies in humans
Heim, C., Newport, D. J., Mletzko, T., Miller, A. H., & Nemeroff, C. B. (2008) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2008.03.008 · Cited by 1,704 · see citing works
Cryan, J. F., Mombereau, C., & Vassout, A. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.03.009 · Cited by 1,674 · see citing works
Risch, N., Herrell, R., Lehner, T., Liang, K.-Y., Eaves, L., Hoh, J., Griem, A., Kovacs, M., Ott, J., & Merikangas, K. R. (2009) · JAMA · doi:10.1001/jama.2009.878 · Cited by 1,655 · see citing works
The global burden of disease, 1990–2020
López, A. D., & Murray, C. C. J. L. (1998) · Nature Medicine · doi:10.1038/3218 · Cited by 1,613 · see citing works
Allele-specific FKBP5 DNA demethylation mediates gene–childhood trauma interactions
Klengel, T., Mehta, D., Anacker, C., Rex-Haffner, M., Pruessner, J. C., Pariante, C. M., Pace, T. W. W., Mercer, K. B., Mayberg, H. S., Bradley, B., et al. (2013) · Nature Neuroscience · doi:10.1038/nn.3275 · Cited by 1,447 · see citing works
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 · see citing works
Binder, E. B. (2008) · JAMA · doi:10.1001/jama.299.11.1291 · Cited by 1,362 · see citing works
RNA-guided gene activation by CRISPR-Cas9-based transcription factors
Perez-Pinera, P., Kocak, D. D., Vockley, C. M., Adler, A. F., Kabadi, A. M., Polstein, L. R., Thakore, P. I., Glass, K. A., Ousterout, D. G., Leong, K. W., et al. (2013) · Nature Methods · doi:10.1038/nmeth.2600 · Cited by 1,328 · see citing works
The Epidemiology of Post-Traumatic Stress Disorder after Disasters
Galea, S., Nandi, A., & Vlahov, D. (2005) · Epidemiologic Reviews · doi:10.1093/epirev/mxi003 · Cited by 1,287 · see citing works
Lasting epigenetic influence of early-life adversity on the BDNF gene
Roth, T. L., Lubin, F. D., Funk, A. J., & Sweatt, J. D. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.11.028 · Cited by 1,273 · see citing works
The Story of Rett Syndrome: From Clinic to Neurobiology
Chahrour, M., & Zoghbi, H. Y. (2007) · Neuron · doi:10.1016/j.neuron.2007.10.001 · Cited by 1,265 · see citing works
Russo, S. J., Murrough, J. W., Han, M.-H., Charney, D. S., & Nestler, E. J. (2012) · Nature Neuroscience · doi:10.1038/nn.3234 · Cited by 1,206 · see citing works
Cas9 as a versatile tool for engineering biology
Mali, P., Esvelt, K. M., & Church, G. M. (2013) · Nature Methods · doi:10.1038/nmeth.2649 · Cited by 1,197 · see citing works
Covalent Modification of DNA Regulates Memory Formation
Miller, C. A., & Sweatt, J. D. (2007) · Neuron · doi:10.1016/j.neuron.2007.02.022 · Cited by 1,180 · see citing works
Dynamic DNA methylation programs persistent adverse effects of early-life stress
Murgatroyd, C., Patchev, A. V., Wu, Y., Micale, V., Bockmühl, Y., Fischer, D., Holsboer, F., Wotjak, C. T., Almeida, O. F. X., & Spengler, D. (2009) · Nature Neuroscience · doi:10.1038/nn.2436 · Cited by 1,162 · see citing works
A mega-analysis of genome-wide association studies for major depressive disorder
Major Depressive Disorder Working Group of the Psychiatric GWAS Consortium, Ripke, S., Wray, N. R., Lewis, C. M., Hamilton, S. P., Weissman, M. M., Breen, G., Byrne, E. M., Blackwood, D. H. R., Boomsma, D. I., et al. (2013) · Molecular Psychiatry · doi:10.1038/mp.2012.21 · Cited by 1,120 · see citing works
Dnmt1 and Dnmt3a maintain DNA methylation and regulate synaptic function in adult forebrain neurons
Feng, J., Zhou, Y., Campbell, S. L., Le, T., Li, E., Sweatt, J. D., Silva, A. J., & Fan, G. (2010) · Nature Neuroscience · doi:10.1038/nn.2514 · Cited by 1,019 · see citing works
The Methyl-CpG-binding Protein MeCP2 Links DNA Methylation to Histone Methylation
Fuks, F., Hurd, P. J., Wolf, D., Nan, X., Bird, A. P., & Kouzarides, T. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m210256200 · Cited by 994 · see citing works
Sex-Specific Programming of Offspring Emotionality after Stress Early in Pregnancy
Mueller, B. R., & Bale, T. L. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.1424-08.2008 · Cited by 988 · see citing works
Binder, E. B. (2009) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2009.05.021 · Cited by 968 · see citing works
The habenula: from stress evasion to value-based decision-making
Hikosaka, O. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2866 · Cited by 955 · see citing works
Mohn, F., Weber, M., Rebhan, M., Roloff, T. C., Richter, J., Stadler, M. B., Bibel, M., & Schübeler, D. (2008) · Molecular Cell · doi:10.1016/j.molcel.2008.05.007 · Cited by 912 · see citing works
Molecular Signals of Epigenetic States
Bonasio, R., Tu, S., & Reinberg, D. (2010) · Science · doi:10.1126/science.1191078 · Cited by 912 · see citing works
Weaver, I. C. G., Champagne, F. A., Brown, S. E., Dymov, S., Sharma, S., Meaney, M. J., & Szyf, M. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.3652-05.2005 · Cited by 905 · see citing works
TETonic shift: biological roles of TET proteins in DNA demethylation and transcription
Pastor, W. A., Aravind, L., & Rao, A. (2013) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3589 · Cited by 897 · cited 1× · see citing works
“Active demethylation of DNA can occur by at least two potentially non-exclusive enzymatic processes – base excision repair (BER) and oxidation (Niehrs and Schafer, 2012, Pastor et al., 2013).”
BackgroundZhou, Z., Hong, E. J., Cohen, S., Zhao, W.-N., Ho, H.-Y. H., Schmidt, L., Chen, W. G., Lin, Y., Savner, E., Griffith, E. C., et al. (2006) · Neuron · doi:10.1016/j.neuron.2006.09.037 · Cited by 877 · see citing works
Cheng, A. W., Wang, H., Yang, H., Shi, L., Yarden Katz, A., Theunissen, T. W., Rangarajan, S., Shivalila, C., Dadon, D. B., & Jaenisch, R. (2013) · Cell Research · doi:10.1038/cr.2013.122 · Cited by 743 · see citing works
Gene Body-Specific Methylation on the Active X Chromosome
Hellman, A., & Chess, A. J. (2007) · Science · doi:10.1126/science.1136352 · Cited by 732 · see citing works
Kendler, K. S., Thornton, L. M., & Gardner, C. O. (2000) · American Journal of Psychiatry · doi:10.1176/appi.ajp.157.8.1243 · Cited by 721 · see citing works
Dynamic DNA methylation across diverse human cell lines and tissuesPreprint
Varley, K. E., Gertz, J., Bowling, K. M., Parker, S. L., Reddy, T. E., Pauli, F., Cross, M. K., Williams, B. A., Stamatoyannopoulos, J. A., Crawford, G. E., et al. (2013) · Genome Research · doi:10.1101/gr.147942.112 · Cited by 693 · see citing works
Neuronal MeCP2 Is Expressed at Near Histone-Octamer Levels and Globally Alters the Chromatin State
Skene, P. J., Illingworth, R. S., Webb, S., Kerr, A. R. W., James, K. D., Turner, D. J., Andrews, R., & Bird, A. P. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.01.030 · Cited by 688 · see citing works
Neuronal activity modifies the DNA methylation landscape in the adult brain
Guo, J. U., Ma, D. K., Mo, H., Ball, M. P., Jang, M.-H., Bonaguidi, M. A., Balazer, J. A., Eaves, H. L., Xie, B., Ford, E., et al. (2011) · Nature Neuroscience · doi:10.1038/nn.2900 · Cited by 669 · see citing works
Epigenetic mechanisms of perinatal programming of hypothalamic-pituitary-adrenal function and health
Meaney, M. J., Moshe Szyf, A., & Seckl, J. R. (2007) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2007.05.003 · Cited by 660 · see citing works
Maternal care as a model for experience-dependent chromatin plasticity?
Meaney, M. J., & Szyf, M. (2005) · Trends in Neurosciences · doi:10.1016/j.tins.2005.07.006 · Cited by 658 · see citing works
Handbook of Disease Burdens and Quality of Life Measures
Bradley, C., Mitchell, J., & Woodcock, A. J. (2009) · Springer eBooks · doi:10.1007/978-0-387-78665-0 · Cited by 652 · see citing works
Synaptic potentiation onto habenula neurons in the learned helplessness model of depression
Li, B., Piriz, J., Mirrione, M., Chung, C., Proulx, C. D., Schulz, D., Henn, F., & Malinow, R. (2011) · Nature · doi:10.1038/nature09742 · Cited by 634 · cited 1× · see citing works
“…in neurons of the lateral habenula, which is a brain region strongly implicated in the regulation of stress-induced depressivelike behaviors via its ability to directly modulate the firing of dopaminergic and serotonergic neurons in brainstem nuclei (Hikosaka, 2010, Li et al., 2011).”
BackgroundDnmt3a regulates emotional behavior and spine plasticity in the nucleus accumbens
LaPlant, Q., Vialou, V., Covington, H. E., Dumitriu, D., Feng, J., Warren, B. L., Maze, I., Dietz, D. M., Watts, E. L., Iñiguez, S. D., et al. (2010) · Nature Neuroscience · doi:10.1038/nn.2619 · Cited by 612 · see citing works
Widespread plasticity in CTCF occupancy linked to DNA methylation
Wang, H., Maurano, M. T., Qu, H., Varley, K. E., Gertz, J., Pauli, F., Lee, K., Canfield, T., Weaver, M., Sandstrom, R., et al. (2012) · Genome Research · doi:10.1101/gr.136101.111 · Cited by 588 · cited 1× · see citing works
“This repression can occur either by recruiting the association of methyl-DNA binding proteins that scaffold chromatin repressors, or by inhibiting the association of transcriptional activators or architectural proteins such as CTCF with their regulatory elements (Wang et al., 2012).”
BackgroundDevelopmental determinants of sensitivity and resistance to stress
Levine, S. (2005) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2005.03.013 · Cited by 574 · see citing works
Animal Models of Depression: Molecular Perspectives
Krishnan, V., & Nestler, E. J. (2011) · Current Topics in Behavioral Neurosciences · doi:10.1007/7854_2010_108 · Cited by 528 · see citing works
Perroud, N., Paoloni-Giacobino, A., Prada, P., Olié, E., Salzmann, A., Nicastro, R., Guillaume, S., Mouthon, D., Stouder, C., Dieben, K., et al. (2011) · Translational Psychiatry · doi:10.1038/tp.2011.60 · Cited by 516 · see citing works
A Population-Based Twin Study of Lifetime Major Depression in Men and Women
Kendler, K. S., & Prescott, C. A. (1999) · Archives of General Psychiatry · doi:10.1001/archpsyc.56.1.39 · Cited by 512 · see citing works
van Winkel, R., Stefanis, N. C., & Myin-Germeys, I. (2008) · Schizophrenia Bulletin · doi:10.1093/schbul/sbn101 · Cited by 489 · see citing works
Morris, M. C., Compas, B. E., & Garber, J. (2012) · Clinical Psychology Review · doi:10.1016/j.cpr.2012.02.002 · Cited by 466 · cited 1× · see citing works
“On the other hand, excessive suppression of the HPA axis, an effect thought to result from GR hypersensitivity, has been associated with traumatic events and PTSD (Binder, 2009; Morris et al., 2012).”
BackgroundPsychobiological allostasis: resistance, resilience and vulnerability
Karatsoreos, I. N., & McEwen, B. S. (2011) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2011.10.005 · Cited by 458 · see citing works
Lu, N. Z., & Cidlowski, J. A. (2005) · Molecular Cell · doi:10.1016/j.molcel.2005.03.025 · Cited by 455 · see citing works
Resilience to social stress coincides with functional DNA methylation of the Crf gene in adult mice
Elliott, E., Ezra-Nevo, G., Regev, L., Neufeld-Cohen, A., & Chen, A. (2010) · Nature Neuroscience · doi:10.1038/nn.2642 · Cited by 436 · see citing works
The human glucocorticoid receptor: molecular basis of biologic function
Nicolaides, N. C., Galata, Z., Kino, T., Chrousos, G. P., & Charmandari, E. (2010) · Steroids · doi:10.1016/j.steroids.2009.09.002 · Cited by 436 · see citing works
Rett syndrome mutations abolish the interaction of MeCP2 with the NCoR/SMRT co-repressor
Lyst, M. J., Ekiert, R., Ebert, D. H., Merusi, C., Nowak, J., Selfridge, J., Guy, J., Kastan, N. R., Robinson, N. D., de Lima Alves, F., et al. (2013) · Nature Neuroscience · doi:10.1038/nn.3434 · Cited by 410 · see citing works
Uchida, S., Hara, K., Kobayashi, A., Otsuki, K., Yamagata, H., Hobara, T., Suzuki, T., Miyata, N., & Watanabe, Y. (2011) · Neuron · doi:10.1016/j.neuron.2010.12.023 · Cited by 398 · see citing works
Sinha, R. (2011) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2011.49 · Cited by 368 · see citing works
Roth, T. L., Zoladz, P. R., Sweatt, J. D., & Diamond, D. M. (2011) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2011.01.013 · Cited by 321 · see citing works
Early postnatal handling alters glucocorticoid receptor concentrations in selected brain regions.
Meaney, M. J., Aitken, D. H., Bodnoff, S. R., Iny, L. J., Tatarewicz, J. E., & Sapolsky, R. M. (2013) · Behavioral Neuroscience · doi:10.1037/a0034187 · Cited by 307 · see citing works
Cohen, S., Gabel, H. W., Hemberg, M., Hutchinson, A. N., Sadacca, L. A., Ebert, D. H., Harmin, D. A., Greenberg, R. S., Verdine, V. K., Zhou, Z., et al. (2011) · Neuron · doi:10.1016/j.neuron.2011.08.022 · Cited by 298 · see citing works
Self-citationEarly postnatal handling alters glucocorticoid receptor concentrations in selected brain regions.
Meaney, M. J., Aitken, D. H., Bodnoff, S. R., Iny, L. J., Tatarewicz, J. E., & Sapolsky, R. M. (1985) · Behavioral Neuroscience · doi:10.1037/0735-7044.99.4.765 · Cited by 295 · see citing works
Nan, X., Hou, J., Maclean, A. W., Nasir, J., Lafuente, M. J., Shu, X., Kriaučionis, S., & Bird, A. P. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0608056104 · Cited by 260 · see citing works
Active DNA demethylation by Gadd45 and DNA repair
Niehrs, C., & Schäfer, A. (2012) · Trends in Cell Biology · doi:10.1016/j.tcb.2012.01.002 · Cited by 248 · see citing works
Activity-dependent phosphorylation of MeCP2 threonine 308 regulates interaction with NCoR
Ebert, D. H., Gabel, H. W., Robinson, N. D., Kastan, N. R., Hu, L. S., Cohen, S., Navarro, A. J., Lyst, M. J., Ekiert, R., Bird, A. P., et al. (2013) · Nature · doi:10.1038/nature12348 · Cited by 227 · see citing works
Phosphorylation of MeCP2 at Serine 80 regulates its chromatin association and neurological function
Tao, J., Hu, K., Chang, Q., Wu, H., Sherman, N. E., Martinowich, K., Klose, R. J., Schanen, C., Jaenisch, R., Wang, W., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0811648106 · Cited by 226 · see citing works
An AT-hook domain in MeCP2 determines the clinical course of Rett syndrome and related disorders
Baker, S. A., Chen, L., Wilkins, A. D., Yu, P., Lichtarge, O., & Zoghbi, H. Y. (2013) · Cell · doi:10.1016/j.cell.2013.01.038 · Cited by 225 · see citing works
Sartor, C. E. (2012) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2011.1385 · Cited by 212 · see citing works
PTSD and gene variants: new pathways and new thinking
Skelton, K., Ressler, K. J., Norrholm, S. D., Jovanovic, T., & Bradley-Davino, B. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.02.013 · Cited by 191 · see citing works
Prospective investigation of stress inoculation in young monkeys
Parker, K. J., Buckmaster, C. L., Schatzberg, A. F., & Lyons, D. M. (2004) · Archives of General Psychiatry · doi:10.1001/archpsyc.61.9.933 · Cited by 185 · see citing works
Posttraumatic growth in adolescence: examining its components and relationship with PTSD.
Levine, S. Z., Laufer, A., Hamama‐Raz, Y., Stein, E., & Solomon, Z. (2008) · Journal of Traumatic Stress · doi:10.1002/jts.20361 · Cited by 154 · see citing works
Chapter 33. Neuroscience of Psychotherapy
Vaughan, S., & Ahmed, M. (2022) · American Psychiatric Association Publishing eBooks · doi:10.1176/appi.books.9781615375233.gg33 · Cited by 151 · see citing works
Regulation of chromatin structure in memory formation
Roth, T. L., & Sweatt, J. D. (2009) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2009.05.011 · Cited by 138 · see citing works
Stress and cardiovascular disease
Cho, J. J. (2013) · Journal of Korean Medical Association · doi:10.5124/jkma.2013.56.6.462 · Cited by 135 · see citing works
MBD family proteins: reading the epigenetic code
Fatemi, M., & Wade, P. A. (2006) · Journal of Cell Science · doi:10.1242/jcs.03099 · Cited by 117 · see citing works
Russell, G. M., Henley, D. E., Leendertz, J., Douthwaite, J. A., Wood, S. A., Stevens, A., Woltersdorf, W. W., Peeters, B. W. M. M., Ruigt, G. S. F., White, A., et al. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.5332-09.2010 · Cited by 111 · 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
Gonzales, M. L., Adams, S., Dunaway, K. W., & LaSalle, J. M. (2012) · Molecular and Cellular Biology · doi:10.1128/mcb.06728-11 · Cited by 94 · see citing works
Karg, K., Burmeister, M., Shedden, K., & Sen, S. (2011) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2010.189 · Cited by 87 · see citing works
DNA memories of early social life
Hoffmann, A. H., & Spengler, D. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.04.003 · Cited by 64 · see citing works
Animal Models of Stress Vulnerability and Resilience in Translational Research
Scharf, S. H., & Schmidt, M. V. (2012) · Current Psychiatry Reports · doi:10.1007/s11920-012-0256-0 · Cited by 54 · see citing works
Phosphorylation of MeCP2 at Ser421 Contributes to Chronic Antidepressant Action
Hutchinson, A. N., Deng, J. V., Cohen, S., & West, A. E. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.2156-12.2012 · Cited by 53 · see citing works
Self-citationVisualizing epigenetics: Current advances and advantages in HDAC PET imaging techniques
Wang, C., Schroeder, F. A., & Hooker, J. M. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2013.09.018 · Cited by 48 · see citing works
Differential Regulation of MeCP2 Phosphorylation in the CNS by Dopamine and Serotonin
Hutchinson, A. N., Deng, J. V., Aryal, D. K., Wetsel, W. C., & West, A. E. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2011.190 · Cited by 31 · see citing works
Self-citationTsolaki, M., Kounti, F., & Karamavrou, S. (2009) · American Journal of Alzheimer s Disease & Other Dementias® · doi:10.1177/1533317508329813 · Cited by 26 · see citing works
Hypothalamic–Pituitary–Adrenal Axis and Cardiovascular Disease
Kaltsas, G., Zannas, A. S., & Chrousos, G. P. (2011) · Springer eBooks · doi:10.1007/978-1-84882-419-5_5 · Cited by 11 · see citing works
Self-citationFreed, M. C., Goldberg, R., Gore, K. L., & Engel, C. C. (2009) · Springer eBooks · doi:10.1007/978-0-387-78665-0_89 · Cited by 10 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Gene–Stress–Epigenetic regulation of FKBP5: clinical and translational implications
Zannas, A. S., Wiechmann, T., Gassen, N. C., & Binder, E. B. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2015.235 · Cited by 622 · see citing works
Self-citationHerzog, J. I., & Schmahl, C. (2018) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2018.00420 · Cited by 583 · see citing works
Zannas, A. S., Arloth, J., Carrillo-Roa, T., Iurato, S., Röh, S., Ressler, K. J., Nemeroff, C. B., Smith, A. K., Bradley, B., Heim, C., et al. (2015) · Genome Biology · doi:10.1186/s13059-015-0828-5 · Cited by 469 · see citing works
Self-citationWhen pain gets stuck: the evolution of pain chronification and treatment resistance
Borsook, D., Youssef, A. M., Simons, L., Elman, I., & Eccleston, C. (2018) · Pain · doi:10.1097/j.pain.0000000000001401 · Cited by 281 · see citing works
Epigenetics of posttraumatic stress disorder: current evidence, challenges, and future directions
Zannas, A. S., Provençal, N., & Binder, E. B. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.04.003 · Cited by 218 · see citing works
Self-citationThe stressed synapse 2.0: pathophysiological mechanisms in stress-related neuropsychiatric disorders
Sanacora, G., Yan, Z., & Popoli, M. (2022) · Nature Reviews Neuroscience · doi:10.1038/s41583-021-00540-x · Cited by 197 · 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
Self-citationSchiele, M. A., Gottschalk, M. G., & Domschke, K. (2020) · Clinical Psychology Review · doi:10.1016/j.cpr.2020.101830 · Cited by 156 · see citing works
DNA methylation, early life environment, and health outcomes
Mitchell, C., Schneper, L. M., & Notterman, D. A. (2016) · Pediatric Research · doi:10.1038/pr.2015.193 · Cited by 146 · see citing works
Liu, R. T. (2015) · Journal of Abnormal Psychology · doi:10.1037/abn0000043 · Cited by 113 · see citing works
Duclot, F., & Kabbaj, M. (2015) · Journal of Experimental Biology · doi:10.1242/jeb.107086 · Cited by 103 · see citing works
Schneider, I., Kugel, H., Redlich, R., Grotegerd, D., Bürger, C., Bürkner, P.-C., Opel, N., Dohm, K., Zaremba, D., Meinert, S., et al. (2018) · Neuropsychopharmacology · doi:10.1038/npp.2017.273 · Cited by 86 · see citing works
Maternal caregiving and DNA methylation in human infants and children: systematic review
Provenzi, L., Brambilla, M., Scotto di Minico, G., Montirosso, R., & Borgatti, R. (2020) · Genes, Brain and Behavior · doi:10.1111/gbb.12616 · Cited by 60 · see citing works
Neonatal DNA methylation and early-onset conduct problems: A genome-wide, prospective study
Cecil, C. A. M., Walton, E., Jaffee, S. R., O'Connor, T., Maughan, B., Relton, C. L., Smith, R. G., McArdle, W., Gaunt, T. R., Ouellet-Morin, I., et al. (2018) · Development and Psychopathology · doi:10.1017/s095457941700092x · Cited by 46 · see citing works
Seo, J. H., Kim, S. T., Jeon, S., Kang, J. I., & Kim, S. J. (2023) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2023.106404 · Cited by 11 · see citing works
- Authors
- Zannas, A. S., & West, A. E.
- Affiliations
- Duke University (US)
- Corresponding author
- West, A.E.
- Venue
- Neuroscience
- Publisher
- Elsevier BV
- Published
- 2014-04
- Volume
- 264
- Pages
- 157-170
- ISSN
- 0306-4522 (ISSN-L)
- PMC
- PMC3959582
- OpenAlex
- W2115418898
- Cited by
- 211
- References
- 106
- Citations by year
- 2026: 16 · 2025: 20 · 2024: 7 · 2023: 9 · 2022: 17 · 2021: 17 · 2020: 23 · 2019: 14 · 2018: 21 · 2017: 20 · 2016: 19 · 2015: 18 · 2014: 10
- FWCI
- 1.47
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Mental Health (R21MH096310)
- National Institute on Drug Abuse (R01DA033610)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- epigenetics, stress vulnerability, resilience, DNA methylation, stress response, mental illness, environmental stressors, gene-environment interaction, brain adaptation
- MeSH terms
- Animals, Brain, Humans, Stress, Psychological, Epigenesis, Genetic, Mice, Rats, Resilience, Psychological
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