Glucocorticoid exposure during hippocampal neurogenesis primes future stress response by inducing changes in DNA methylation
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Significance: Prenatal stress exposure is associated with a wide range of health problems later in life. This may be mediated in part via glucocorticoid (GC) exposure during fetal development known to impact neurogenesis and induce epigenetic changes. Using a human fetal hippocampal progenitor cell line to assess the effects of GCs, we observe that exposure to GCs early during neurogenesis results in lasting changes in DNA methylation (DNAm). Lasting DNAm alterations are associated with significantly enhanced transcriptional response to a subsequent GC exposure. Our data suggest that early exposure to GCs changes the set point of future transcriptional responses to stress by inducing lasting DNAm changes. Such altered set points may relate to differential vulnerability to stress exposure later in life.
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Lasting changes in DNA methylation result in an altered set-point for transcriptional changes of FKBP5 upon subsequent GR activation.
“Such lasting changes in DNAm result in an altered set-point for transcriptional changes of FKBP5 upon subsequent GR activation. 55 , 69 , 72”
From Epigenetics and depression (2019) · cites this paper as [55]
Glucocorticoid-induced DNA methylation changes are long-lasting and prime the stress response for future exposure.
“Subsequent post-differentiation exposure to GCs resulted in robust transcriptional changes in the HPCs that were initially treated during proliferation and differentiation, indicating that GC induced DNAm changes are long-lasting and prime the stress response for future exposure.”
From Epigenetics and depression (2019) · cites this paper as [55]
The differentially methylated regions in that HPC model were enriched for the binding motif of the glucocorticoid receptor.
“Furthermore, the DMRs were enriched for the binding motif of the glucocorticoid receptor (GR), a key modulator of the hypothalamus-pituitary-adrenal (HPA) axis.”
From Epigenetics and depression (2019) · cites this paper as [55]
In a human hippocampal progenitor cell line model, exposure to glucocorticoids during differentiation and proliferation induced long-lasting DNA methylation changes.
“In a model of stress using a human hippocampal progenitor cell line (HPCs), exposure to glucocorticoids (GCs) during differentiation and proliferation induced long-lasting DNAm changes.”
From Epigenetics and depression (2019) · cites this paper as [55]
In human models, environmental factors can induce epigenetic changes.
“In human models, there is also evidence of environmental factors inducing epigenetic changes. 55”
From Epigenetics and depression (2019) · cites this paper as [55]
In a human hippocampal progenitor cell line, GR-induced demethylation can become stable when initiated during certain early developmental periods.
“However, as shown in a human hippocampal progenitor cell line, GR-induced demethylation can become stable when initiated during certain early developmental periods. 55”
From Epigenetics and depression (2019) · cites this paper as [55]
The DMRs with GR binding motifs were more commonly demethylated than hypermethylated.
“The DMRs with GR binding motifs were more commonly demethylated than hypermethylated.”
From Epigenetics and depression (2019) · cites this paper as [55]
Cites
Effects of stress throughout the lifespan on the brain, behaviour and cognition
Lupien, S. J., McEwen, B. S., Gunnar, M. R., & Heim, C. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2639 · Cited by 6,256 · see citing works
ChromHMM: automating chromatin-state discovery and characterization
Ernst, J., & Kellis, M. (2012) · Nature Methods · doi:10.1038/nmeth.1906 · Cited by 2,489 · see citing works
Spatio-temporal transcriptome of the human brain
Kang, H. J., Kawasawa, Y. I., Cheng, F., Zhu, Y., Xu, X., Li, M., Sousa, A. M. M., Pletikos, M., Meyer, K. A., Sedmak, G., et al. (2011) · Nature · doi:10.1038/nature10523 · Cited by 2,084 · see citing works
BOYCE, W. T., & ELLIS, B. J. (2005) · Development and Psychopathology · doi:10.1017/s0954579405050145 · Cited by 2,078 · see citing works
Fetal Origins of Mental Health: The Developmental Origins of Health and Disease Hypothesis
O’Donnell, K. J., & Meaney, M. J. (2017) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2016.16020138 · Cited by 608 · see citing works
Reynolds, R. M. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.08.012 · Cited by 497 · see citing works
Prenatal stress diminishes neurogenesis in the dentate gyrus of juvenile rhesus monkeys
Coe, C. L., Kramer, M., Czéh, B., Gould, E., Reeves, A. J., Kirschbaum, C., & Fuchs, E. (2003) · Biological Psychiatry · doi:10.1016/s0006-3223(03)00698-x · Cited by 477 · see citing works
Impact of Maternal Stress, Depression and Anxiety on Fetal Neurobehavioral Development
KINSELLA, M. T., & MONK, C. (2009) · Clinical Obstetrics & Gynecology · doi:10.1097/grf.0b013e3181b52df1 · Cited by 422 · see citing works
Anacker, C., Cattaneo, A., Musaelyan, K., Zunszain, P. A., Horowitz, M., Molteni, R., Luoni, A., Calabrese, F., Tansey, K., Gennarelli, M., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1300886110 · Cited by 319 · see citing works
Self-citationGlucocorticoid-Related Molecular Signaling Pathways Regulating Hippocampal Neurogenesis
Anacker, C., Cattaneo, A., Luoni, A., Musaelyan, K., Zunszain, P. A., Milanesi, E., Rybka, J., Berry, A., Cirulli, F., Thuret, S., et al. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2012.253 · Cited by 313 · see citing works
Self-citationMethylomic trajectories across human fetal brain development
Spiers, H., Hannon, E., Schalkwyk, L. C., Smith, R., Wong, C. C. Y., O’Donovan, M. C., Bray, N. J., & Mill, J. (2015) · Genome Research · doi:10.1101/gr.180273.114 · Cited by 287 · see citing works
Lee, R. S., Tamashiro, K. L. K., Yang, X., Purcell, R. H., Harvey, A., Willour, V. L., Huo, Y., Rongione, M., Wand, G. S., & Potash, J. B. (2010) · Endocrinology · doi:10.1210/en.2010-0225 · Cited by 275 · see citing works
The placental interleukin-6 signaling controls fetal brain development and behavior
Wu, W.-L., Hsiao, E. Y., Yan, Z., Mazmanian, S. K., & Patterson, P. H. (2017) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2016.11.007 · Cited by 275 · see citing works
The effects of early life stress on the epigenome: From the womb to adulthood and even before
Provençal, N., & Binder, E. B. (2015) · Experimental Neurology · doi:10.1016/j.expneurol.2014.09.001 · Cited by 255 · see citing works
Self-citationDNA methylation status predicts cell type‐specific enhancer activity
Wiench, M., John, S., Baek, S., Johnson, T. A., Sung, M., Escobar, T., Simmons, C. A., Pearce, K. H., Biddie, S. C., Sabo, P. J., et al. (2011) · The EMBO Journal · doi:10.1038/emboj.2011.210 · Cited by 245 · see citing works
11β-Hydroxysteroid dehydrogenases and the brain: From zero to hero, a decade of progress
Wyrwoll, C. S., Holmes, M. C., & Seckl, J. R. (2011) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2010.12.001 · Cited by 244 · see citing works
Sandman, C. A., Buss, C., Head, K., & Davis, E. P. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.06.025 · Cited by 219 · see citing works
Prenatal programing: At the intersection of maternal stress and immune activation
Howerton, C. L., & Bale, T. L. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.03.007 · Cited by 205 · see citing works
Rifkin-Graboi, A. E., Meaney, M. J., Chen, H., Bai, J., Hameed, W. B., Tint, M. T., Broekman, B. F. P., Chong, Y. S., Gluckman, P. D., Fortier, M. V., et al. (2015) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1016/j.jaac.2015.01.013 · Cited by 140 · see citing works
Set1/COMPASS and Mediator are repurposed to promote epigenetic transcriptional memory
D’Urso, A., Takahashi, Y.-H., Xiong, B., Marone, J., Coukos, R., Randise-Hinchliff, C., Wang, J.-P., Shilatifard, A., & Brickner, J. H. (2016) · eLife · doi:10.7554/elife.16691 · Cited by 133 · see citing works
Active cytosine demethylation triggered by a nuclear receptor involves DNA strand breaks
Kress, C., Thomassin, H., & Grange, T. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0601793103 · Cited by 121 · see citing works
Chikina, M. D., Zaslavsky, E., & Sealfon, S. C. (2015) · Bioinformatics · doi:10.1093/bioinformatics/btv015 · Cited by 118 · see citing works
Zheng, Y., Fan, W., Zhang, X., & Dong, E. (2016) · Epigenetics · doi:10.1080/15592294.2016.1146850 · Cited by 111 · see citing works
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
Pryce, C. R., Aubert, Y., Maier, C., Pearce, P. C., & Fuchs, E. (2010) · Psychopharmacology · doi:10.1007/s00213-010-1989-2 · Cited by 94 · see citing works
Impact of glucocorticoid on neurogenesis
Numakawa, T., Odaka, H., & Adachi, N. (2017) · Neural Regeneration Research · doi:10.4103/1673-5374.211174 · Cited by 93 · see citing works
CoGAPS: an R/C++ package to identify patterns and biological process activity in transcriptomic data
Fertig, E. J., Ding, J., Favorov, A. V., Parmigiani, G., & Ochs, M. F. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btq503 · Cited by 91 · see citing works
Johnson, T. A., Chereji, R. V., Stavreva, D. A., Morris, S. A., Hager, G. L., & Clark, D. J. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkx1044 · Cited by 76 · see citing works
Antenatal Glucocorticoid Treatment Affects Hippocampal Development in Mice
Noorlander, C. W., Tijsseling, D., Hessel, E. V. S., de Vries, W. B., Derks, J. B., Visser, G. H. A., & Graan, P. N. E. D. (2014) · PLoS ONE · doi:10.1371/journal.pone.0085671 · Cited by 71 · see citing works
Prediction and Prevention of Preeclampsia and Intrauterine Growth Restriction (PREDO) study
Girchenko, P. V., Hämäläinen, E. K., Kajantie, E., Pesonen, A., Villa, P., Laivuori, H. M., & Räikkönen, K. (2016) · International Journal of Epidemiology · doi:10.1093/ije/dyw154 · Cited by 71 · see citing works
Self-citationBose, R., Spulber, S. D., Kilian, P., Heldring, N., Lönnerberg, P., Johnsson, A., Conti, M., Hermanson, O., & Ceccatelli, S. (2015) · Cell Death and Disease · doi:10.1038/cddis.2015.159 · Cited by 52 · see citing works
Associations of antenatal glucocorticoid exposure with mental health in children
Wolford, E., Lahti‐Pulkkinen, M., Girchenko, P. V., Lipsanen, J. O., Tuovinen, S., Lahti, J. M. T., Heinonen, K., Hämäläinen, E. K., Kajantie, E., Pesonen, A., et al. (2019) · Psychological Medicine · doi:10.1017/s0033291718004129 · Cited by 48 · see citing works
Self-citationGirchenko, P., Lahti, M., Tuovinen, S., Savolainen, K., Lahti, J., Binder, E., Reynolds, R., Entringer, S., Buss, C., Wadhwa, P. D., et al. (2017) · MPG.PuRe (Max Planck Society) · Cited by 46 · see citing works
Self-citationGenome-wide Methyl-Seq analysis of blood-brain targets of glucocorticoid exposure
Seifuddin, F., Wand, G. S., Cox, O., Pirooznia, M., Moody, L., Yang, X., Tai, J., Boersma, G. J., Tamashiro, K. L., Zandi, P. P., et al. (2017) · Epigenetics · doi:10.1080/15592294.2017.1334025 · Cited by 43 · see citing works
Schroeder, M., Jakovcevski, M., Polacheck, T., Lebow, M., Drori, Y., Engel, M., Ben‐Dor, S., & Chen, A. (2017) · Cell Metabolism · doi:10.1016/j.cmet.2017.05.001 · Cited by 37 · see citing works
Neural stem cells respond to stress hormones: distinguishing beneficial from detrimental stress
Koutmani, Y., & Karalis, K. P. (2015) · Frontiers in Physiology · doi:10.3389/fphys.2015.00077 · Cited by 29 · see citing works
Chromatin structure and gene regulation: a dynamic view of enhancer function
Stavreva, D. A., & Hager, G. L. (2015) · Nucleus · doi:10.1080/19491034.2015.1107689 · Cited by 24 · see citing works
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Biological embedding of experience: a primer on epigenetics
Aristizabal, M. J., Anreiter, I., Halldorsdottir, T., Odgers, C. L., McDade, T. W., Goldenberg, A., Mostafavi, S., Kobor, M. S., Binder, E. B., Sokolowski, M. B., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1820838116 · Cited by 268 · see citing works
Self-citationPenner-Goeke, S., & Binder, E. B. (2019) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2019.21.4/ebinder · Cited by 254 · see citing works
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Malave, L., van Dijk, M. T., & Anacker, C. (2022) · Translational Psychiatry · doi:10.1038/s41398-022-02092-9 · Cited by 177 · see citing works
Self-citationThe cortisol switch between vulnerability and resilience
de Kloet, E. R., & Joëls, M. (2023) · Molecular Psychiatry · doi:10.1038/s41380-022-01934-8 · Cited by 153 · see citing works
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Boyce, W. T., Sokolowski, M. B., & Robinson, G. E. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2016710117 · Cited by 135 · see citing works
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 126 · see citing works
Glucocorticoids as Mediators of Adverse Outcomes of Prenatal Stress
Krontira, A. C., Cruceanu, C., & Binder, E. B. (2020) · Trends in Neurosciences · doi:10.1016/j.tins.2020.03.008 · Cited by 115 · see citing works
Self-citationMulti-omics data integration methods and their applications in psychiatric disorders
Sathyanarayanan, A., Mueller, T. T., Moni, M. A., Schueler, K., Baune, B. T., Lió, P., Mehta, D., Baune, B. T., Dierssen, M., Ebert, B., et al. (2023) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2023.01.001 · Cited by 90 · see citing works
Invited Review: Epigenetics in neurodevelopment
Salinas, R. D., Connolly, D. R., & Song, H. (2020) · Neuropathology and Applied Neurobiology · doi:10.1111/nan.12608 · Cited by 81 · see citing works
Harris, B. N. (2019) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2019.113355 · Cited by 76 · see citing works
Raineki, C., Opendak, M. M., Sarro, E. C., Showler, A., Bui, K., McEwen, B. S., Wilson, D. A., & Sullivan, R. M. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1907170116 · Cited by 76 · see citing works
Dammering, F., Martins, J., Dittrich, K., Czamara, D., Rex‐Haffner, M., Overfeld, J., de Punder, K., Buß, C., Entringer, S., Winter, S., et al. (2021) · Neurobiology of Stress · doi:10.1016/j.ynstr.2021.100394 · Cited by 75 · see citing works
Self-citationCruceanu, C., Dony, L., Krontira, A. C., Fischer, D. S., Roeh, S., Giaimo, R. D., Kyrousi, C., Kaspar, L., Arloth, J., Czamara, D., et al. (2021) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2021.21010095 · Cited by 70 · see citing works
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Leschik, J., Lutz, B., & Gentile, A. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22147339 · Cited by 63 · see citing works
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McGill, M. G., Pokhvisneva, I., Clappison, A. S., McEwen, L. M., Beijers, R., Tollenaar, M. S., Pham, H., Kee, M. Z. L., Garg, E., Filho, E. J. D. M., et al. (2021) · Biological Psychiatry · doi:10.1016/j.biopsych.2021.07.025 · Cited by 70 · see citing works
Seah, C., Breen, M. S., Rusielewicz, T., Bader, H. N., Xu, C., Hunter, C. J., McCarthy, B., Deans, P. J. M., Chattopadhyay, M., Goldberg, J., et al. (2022) · Nature Neuroscience · doi:10.1038/s41593-022-01161-y · Cited by 67 · see citing works
Cattane, N., Vernon, A. C., Borsini, A., Scassellati, C., Endres, D., Capuron, L., Tamouza, R., Benros, M. E., Leza, J. C., Pariante, C. M., et al. (2022) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2022.02.002 · Cited by 64 · see citing works
Self-citationThe epigenetically-encoded memory of the innate immune system
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Podgorny, O., & Gulyaeva, N. (2020) · Journal of Neurochemistry · doi:10.1111/jnc.15265 · Cited by 55 · see citing works
Marqués-Feixa, L., Palma‐Gudiel, H., Romero, S., Moya, J., Rapado‐Castro, M., Castro-Quintas, Á., Zorrilla, E. P., Muñoz, M. J., Ramírez, M., Mayoral, M., et al. (2021) · Psychological Medicine · doi:10.1017/s003329172100249x · Cited by 59 · see citing works
Matosin, N., Arloth, J., Czamara, D., Edmond, K. Z., Maitra, M., Fröhlich, A. S., Martinelli, S., Kaul, D., Bartlett, R., Curry, A. R., et al. (2023) · Acta Neuropathologica · doi:10.1007/s00401-023-02541-9 · Cited by 55 · see citing works
Self-citationBorsini, A., Giacobbe, J., Mandal, G., & Boldrini, M. (2023) · Molecular Psychiatry · doi:10.1038/s41380-023-02229-2 · Cited by 59 · see citing works
The epigenetics of perinatal stress
Moshe Szyf, A. (2019) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2019.21.4/mszyf · Cited by 58 · see citing works
Horowitz, M. A., Cattaneo, A., Cattane, N., Lopizzo, N., Tojo, L. M., Bakunina, N., Musaelyan, K., Borsini, A., Zunszain, P. A., & Pariante, C. M. (2020) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2020.03.012 · Cited by 57 · see citing works
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Eachus, H., Choi, M., & Ryu, S. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.657591 · Cited by 52 · see citing works
Borsini, A., Stangl, D., Jeffries, A. R., Pariante, C. M., & Thuret, S. (2020) · Translational Psychiatry · doi:10.1038/s41398-020-00908-0 · Cited by 50 · see citing works
Self-citationGalbally, M., Watson, S., van IJzendoorn, M. H., Saffery, R., Ryan, J. L., de Kloet, E. R., Oberlander, T. F., Lappas, M., & Lewis, A. J. (2020) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2020.104611 · Cited by 48 · see citing works
Soliai, M. M., Kato, A., Helling, B. A., Stanhope, C. T., Norton, J. E., Naughton, K. A., Klinger, A. I., Thompson, E. E., Clay, S. M., Kim, S., et al. (2021) · Genome Medicine · doi:10.1186/s13073-021-00967-y · Cited by 44 · see citing works
Palma‐Gudiel, H., Prather, A. A., Lin, J., Oxendine, J. D., Guintivano, J., Xia, K., Rubinow, D. R., Wolkowitz, O. M., Epel, E. S., & Zannas, A. S. (2020) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2020.11.027 · Cited by 43 · see citing works
Berretta, E., Guida, E., Forni, D., & Provenzi, L. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.03.003 · Cited by 44 · see citing works
Bentz, A. B., George, E., Wolf, S. E., Rusch, D. B., Podicheti, R., Buechlein, A. M., Nephew, K. P., & Rosvall, K. A. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2016154118 · Cited by 41 · see citing works
Human cortical neurogenesis is altered via glucocorticoid-mediated regulation of ZBTB16 expression
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Self-citationMulligan, C. J., Quinn, E. B., Hamadmad, D., Dutton, C. L., Nevell, L., Binder, A. M., Panter-Brick, C., & Dajani, R. (2025) · Scientific Reports · doi:10.1038/s41598-025-89818-z · Cited by 36 · see citing works
Telomere length and human hippocampal neurogenesis
Palmos, A., Duarte, R. R. R., Smeeth, D. M., Hedges, E. C., Nixon, D. F., Thuret, S., & Powell, T. R. (2020) · Neuropsychopharmacology · doi:10.1038/s41386-020-00863-w · Cited by 35 · see citing works
Lux, V., Non, A. L., Pexman, P. M., Stadler, W., Weber, L. A. E., & Krüger, M. (2021) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2021.672740 · Cited by 42 · see citing works
Glucocorticoid effects on the brain: from adaptive developmental plasticity to allostatic overload
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Social Epigenomics: Are we at an Impasse?
Non, A. L. (2021) · Epigenomics · doi:10.2217/epi-2020-0136 · Cited by 35 · see citing works
Lin, Y.-H., Lin, C., Lin, M., Hsu, Y.-C., & Hsu, C.-T. (2022) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2022.09.050 · Cited by 33 · see citing works
Epigenetics applied to child and adolescent mental health: Progress, challenges and opportunities
Cecil, C. A. M., Neumann, A., & Walton, E. (2022) · JCPP Advances · doi:10.1002/jcv2.12133 · Cited by 33 · see citing works
Mareckova, K., Marecek, R., Andryskova, L., Brazdil, M., & Nikolova, Y. S. (2020) · Cerebral Cortex · doi:10.1093/cercor/bhaa014 · Cited by 32 · see citing works
Leung, C. S., Kosyk, O., Welter, E. M., Dietrich, N., Archer, T., & Zannas, A. S. (2022) · iScience · doi:10.1016/j.isci.2022.104960 · Cited by 30 · see citing works
Arcego, D. M., Buschdorf, J. P., O’Toole, N., Wang, Z., Barth, B., Pokhvisneva, I., Rayan, N. A., Patel, S. H., Filho, E. J. D. M., Lee, P., et al. (2023) · Biological Psychiatry · doi:10.1016/j.biopsych.2023.06.028 · Cited by 31 · see citing works
Self-citationEpigenetic Mechanisms in Aging: Extrinsic Factors and Gut Microbiome
Borrego-Ruiz, A., & Borrego, J. J. (2024) · Genes · doi:10.3390/genes15121599 · Cited by 30 · see citing works
Czamara, D., Dieckmann, L., Röh, S., Kraemer, S., Rancourt, R. C., Sammallahti, S., Kajantie, E., Laivuori, H. M., Eriksson, J. G., Räikkönen, K., et al. (2021) · Clinical Epigenetics · doi:10.1186/s13148-021-01153-y · Cited by 31 · see citing works
Self-citationNieto-Quero, A., Chaves-Peña, P., Santín, L. J., Pérez‐Martín, M., & Pedraza, C. (2021) · Neurobiology of Stress · doi:10.1016/j.ynstr.2021.100356 · Cited by 31 · see citing works
In vitro modeling of the neurobiological effects of glucocorticoids: A review
Bassil, K. C., Krontira, A. C., Leroy, T., Escoto, A. I. H., Snijders, C., Pernia, C. D., Pasterkamp, R. J., de Nijs, L., van den Hove, D., Kenis, G., et al. (2023) · Neurobiology of Stress · doi:10.1016/j.ynstr.2023.100530 · Cited by 31 · see citing works
Self-citationPerinatal stress and epigenetics.
(2021) · Handbook of Clinical Neurology · doi:10.1016/b978-0-12-820107-7.00008-2 · Cited by 28 · see citing works
Hippocampal glucocorticoid target genes associated with enhancement of memory consolidation
Buurstede, J. C., van Weert, L. T. C. M., Colucci, P., Gentenaar, M., Viho, E. M. G., Koorneef, L. L., Schoonderwoerd, R. A., Lanooij, S. D., Moustakas, I., Balog, J., et al. (2021) · European Journal of Neuroscience · doi:10.1111/ejn.15226 · Cited by 28 · see citing works
Choi, G. E., Chae, C. W., Park, M. R., Yoon, J. H., Jung, Y. H., Lee, H. J., & Han, H. J. (2022) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-022-04313-2 · Cited by 27 · see citing works
Nold, V., Richter, N., Hengerer, B., Kolassa, I., & Allers, K. A. (2020) · European Journal of Neuroscience · doi:10.1111/ejn.14999 · Cited by 26 · see citing works
Sarid, E. B., Stoopler, M. L., Morency, A., & Garfinkle, J. (2022) · Pediatric Research · doi:10.1038/s41390-022-02135-3 · Cited by 27 · see citing works
DNA methylation signatures of early-life adversity are exposure-dependent in wild baboons
Anderson, J. A., Lin, D., Lea, A. J., Johnston, R. A., Voyles, T., Akinyi, M. Y., Archie, E. A., Alberts, S. C., & Tung, J. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2309469121 · Cited by 26 · see citing works
How is prenatal stress transmitted from the mother to the fetus?
Sze, Y., & Brunton, P. J. (2024) · Journal of Experimental Biology · doi:10.1242/jeb.246073 · Cited by 29 · see citing works
Comprehensive Review of the Impact of Maternal Stress on Fetal Development
Tadanki, D., Kaza, P., Meisinger, E., Syed, A., Johnson, A., Bainbridge, G., Cho, M., Anigbogu, C., & Gupta, G. (2025) · Pediatric Discovery · doi:10.1002/pdi3.70004 · Cited by 33 · see citing works
Glucocorticoid-Mediated Developmental Programming of Vertebrate Stress Responsivity
Gans, I. M., & Coffman, J. A. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.812195 · Cited by 27 · see citing works
SARS-CoV-2 (COVID-19) as a possible risk factor for neurodevelopmental disorders
Dubey, H., Sharma, R. K., Krishnan, S., & Knickmeyer, R. C. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.1021721 · Cited by 26 · see citing works
Huzard, D., Rappeneau, V., Meijer, O. C., Touma, C., Arango-Lievano, M., Garabedian, M. J., & Jeanneteau, F. D. (2020) · Stress · doi:10.1080/10253890.2020.1806226 · Cited by 23 · see citing works
Lobo, J. J., Ayoub, L. J., Moayedi, M., & Linnstaedt, S. D. (2022) · Scientific Reports · doi:10.1038/s41598-022-10411-9 · Cited by 24 · see citing works
Walton, E., Baltramonaityte, V., Calhoun, V. D., Heijmans, B. T., Thompson, P. M., & Cecil, C. A. M. (2023) · Molecular Psychiatry · doi:10.1038/s41380-023-02067-2 · Cited by 24 · see citing works
Silveira, P. P., & Meaney, M. J. (2023) · Neurobiology of Disease · doi:10.1016/j.nbd.2023.106008 · Cited by 24 · see citing works
Pubertal adversity alters chromatin dynamics and stress circuitry in the pregnant brain
Morrison, K. E., Cole, A. B., Kane, P. J., Meadows, V. E., Thompson, S. M., & Bale, T. L. (2020) · Neuropsychopharmacology · doi:10.1038/s41386-020-0634-y · Cited by 23 · see citing works
Cox, O., Song, H. Y., Garrison‐Desany, H. M., Gadiwalla, N., Carey, J. L., Menzies, J., & Lee, R. S. (2020) · Epigenetics · doi:10.1080/15592294.2020.1864169 · Cited by 22 · see citing works
Palma‐Gudiel, H., Córdova‐Palomera, A., Navarro, V., & Fañanás, L. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.02.017 · Cited by 21 · see citing works
Lei, L., Wu, X., Gu, H., Ji, M., & Yang, J. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.573107 · Cited by 21 · see citing works
The Long-Term Effects of Early Life Stress on the Modulation of miR-19 Levels
Mazzelli, M., Maj, C., Mariani, N., Mora, C., Begni, V., Pariante, C. M., Riva, M. A., Cattaneo, A., & Cattane, N. (2020) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2020.00389 · Cited by 21 · see citing works
Self-citationBentz, A. B., Niederhuth, C. E., Carruth, L. L., & Navara, K. J. (2021) · BMC Genomics · doi:10.1186/s12864-021-07466-9 · Cited by 18 · see citing works
Epigenetic Mechanisms Modulated by Glucocorticoids With a Focus on Cushing Syndrome
Paes, T., Feelders, R. A., & Hofland, L. J. (2024) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgae151 · Cited by 23 · see citing works
Dony, L., Krontira, A. C., Kaspar, L., Ahmad, R., Demirel, I. S., Grochowicz, M., Schäfer, T., Begum, F., Sportelli, V., Raimundo, C., et al. (2025) · Science Advances · doi:10.1126/sciadv.adn8631 · Cited by 19 · see citing works
Self-citationRim, C., Park, H., You, M., Yang, B., Kim, H.-J., Sung, S., & Kwon, M. (2022) · Schizophrenia · doi:10.1038/s41537-022-00280-6 · Cited by 19 · see citing works
Perret, L. C., Geoffroy, M.-C., Barr, E., Parnet, F., Provencal, N., Boivin, M., O’Donnell, K. J., Suderman, M., Power, C., Turecki, G., et al. (2023) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.1051556 · Cited by 19 · see citing works
Self-citationEnvironmental epigenetics: new horizons in redefining biological and health outcomes
Faraji, J., & Metz, G. A. S. (2026) · Environment International · doi:10.1016/j.envint.2026.110072 · Cited by 21 · see citing works
Suarez, A., Lahti, J. M. T., Lahti‐Pulkkinen, M., Girchenko, P. V., Czamara, D., Arloth, J., Malmberg, A., Hämäläinen, E. K., Kajantie, E., Laivuori, H. M., et al. (2020) · Neurobiology of Stress · doi:10.1016/j.ynstr.2020.100275 · Cited by 19 · see citing works
Self-citationLanshakov, D. A., Sukhareva, E. V., Bulygina, V. V., Bannova, A. V., Shaburova, E. V., & Kalinina, T. S. (2021) · Scientific Reports · doi:10.1038/s41598-021-87652-7 · Cited by 19 · see citing works
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 19 · see citing works
Comtois‐Cabana, M., Barr, E., Provençal, N., & Ouellet‐Morin, I. (2023) · PLoS ONE · doi:10.1371/journal.pone.0280203 · Cited by 18 · see citing works
Self-citationNeuroepigenetic Changes in DNA Methylation Affecting Diabetes-Induced Cognitive Impairment
Fernandes, V., Kumari, P., Sood, A., Nair, K. P., Khan, S. S., Rao, B. S. S., Khatri, D. K., & Singh, S. B. (2022) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-022-01278-5 · Cited by 17 · see citing works
From cellular to fear memory: An epigenetic toolbox to remember
Coda, D. M., & Gräff, J. (2023) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2023.102829 · Cited by 16 · see citing works
Vetrovoy, O. V., Tyulkova, E. I., Stratilov, V. A., Baranova, K. A., Nimiritsky, P., Макаревич, П. И., & Rybnikova, E. A. (2020) · Developmental Neuroscience · doi:10.1159/000512223 · Cited by 17 · see citing works
Leachman, J. R., Rea, M. D., Cohn, D. M., Xu, X. Q., Fondufe‐Mittendorf, Y. N., & Loria, A. S. (2020) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00243.2020 · Cited by 18 · see citing works
Kirkpatrick, M., Mandal, G., Elhadidy, I., Mariani, N., Priestley, K., Pariante, C. M., & Borsini, A. (2024) · Molecular Psychiatry · doi:10.1038/s41380-024-02866-1 · Cited by 18 · see citing works
Self-citationThe role of TET proteins in stress-induced neuroepigenetic and behavioural adaptations
Dick, A., & Chen, A. (2021) · Neurobiology of Stress · doi:10.1016/j.ynstr.2021.100352 · Cited by 16 · see citing works
Infant DNA methylation: an early indicator of intergenerational trauma?
Moore, S. R., Merrill, S. M., Sekhon, B., MacIsaac, J. L., Kobor, M. S., Giesbrecht, G. F., & Letourneau, N. L. (2021) · Early Human Development · doi:10.1016/j.earlhumdev.2021.105519 · Cited by 16 · see citing works
Treccani, G., Yiğit, H., Lingner, T., Schleuβner, V., Mey, F., van der Kooij, M. A., Wennström, M., Herzog, D. P., Linke, M., Fricke, M., et al. (2021) · Neurobiology of Stress · doi:10.1016/j.ynstr.2021.100338 · Cited by 14 · see citing works
Schwarze, C. E., von der Heiden, S., Wallwiener, S., & Pauen, S. (2023) · Journal of Affective Disorders · doi:10.1016/j.jad.2023.10.035 · Cited by 18 · see citing works
Coping with the multifaceted and multifunctional role of cortisol in the brain
de Kloet, E. R. (2024) · Neuroscience Applied · doi:10.1016/j.nsa.2024.104047 · Cited by 14 · see citing works
DNA methylation-environment interactions in the human genome
Johnston, R. A., Aracena, K. A., Barreiro, L. B., Lea, A. J., & Tung, J. (2024) · eLife · doi:10.7554/elife.89371.3 · Cited by 14 · see citing works
Tartour, A. I., Chivese, T., Eltayeb, S., Elamin, F. M., Fthenou, E., Ahmed, M. S., & Babu, G. R. (2024) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2024.107060 · Cited by 15 · see citing works
Littlejohn, B. P., Price, D. M., Neuendorff, D. A., Carroll, J. A., VANN, R. C., Riggs, P. K., Riley, D. G., Long, C. R., Randel, R. D., & Welsh, T. H. (2019) · Journal of Animal Science · doi:10.1093/jas/skz368 · Cited by 14 · see citing works
Stress system and related biomarkers in Parkinson's disease
Bougea, A. M., Stefanis, L., & Chrousos, G. P. (2022) · Advances in clinical chemistry · doi:10.1016/bs.acc.2022.07.004 · Cited by 13 · see citing works
DNA methylation patterns of FKBP5 regulatory regions in brain and blood of humanized mice and humans
Yusupov, N., Roeh, S., Elliott, L. S., Chang, S., Loganathan, S., Urbina-Treviño, L., Fröhlich, A. S., Sauer, S., Ködel, M., Matosin, N., et al. (2024) · Molecular Psychiatry · doi:10.1038/s41380-024-02430-x · Cited by 12 · see citing works
Self-citationIn utero exposure to glucocorticoids and risk of anxiety and depression in childhood or adolescence
Laugesen, K., Sørensen, H. T., Jørgensen, J. O. L., & Petersen, I. (2022) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2022.105766 · Cited by 13 · see citing works
Schaffner, S. L., Wassouf, Z., Lázaro, D. F., Xylaki, M., Gladish, N., Lin, D. T. S., MacIsaac, J. L., Ramadori, K. E., Hentrich, T., Schulze-Hentrich, J. M., et al. (2022) · Human Molecular Genetics · doi:10.1093/hmg/ddac104 · Cited by 13 · see citing works
Vetrovoy, O. V., Stratilov, V. A., Lomert, E. V., & Tyulkova, E. I. (2022) · Neurochemical Research · doi:10.1007/s11064-022-03837-0 · Cited by 13 · see citing works
Walton, E., Baltramonaityte, V., Calhoun, V. D., Heijmans, B. T., Thompson, P. M., & Cecil, C. A. M. (2020) · doi:10.31234/osf.io/4a8xn · Cited by 13 · see citing works
Wu, T., Zhou, K., Hua, Y., Zhang, W., & Li, Y. (2023) · Frontiers in Pharmacology · doi:10.3389/fphar.2023.1164487 · Cited by 12 · see citing works
Glucocorticoid feedback paradox: a homage to Mary Dallman
de Kloet, E. R. (2023) · Stress · doi:10.1080/10253890.2023.2247090 · Cited by 11 · see citing works
Stress Molecular Signaling in Interaction With Cognition
Lugenbühl, J. F., Viho, E. M. G., Binder, E. B., & Daskalakis, N. P. (2024) · Biological Psychiatry · doi:10.1016/j.biopsych.2024.09.023 · Cited by 12 · see citing works
Self-citation
- Authors
- Provençal, N., Arloth, J., Cattaneo, A., Anacker, C., Cattane, N., Wiechmann, T., Röh, S., Ködel, M., Klengel, T., Czamara, D., Müller, N. S., Lahti, J., PREDO team, Räikkönen, K., Pariante, C. M., Binder, E. B., Kajantie, E., Hämäläinen, E., Villa, P., & Laivuori, H.
- Affiliations
- Simon Fraser University (CA)
- Helmholtz Munich (DE)
- King's College London (GB)
- Research Foundation For Mental Hygiene (US)
- Centro San Giovanni di Dio Fatebenefratelli (IT)
- Max Planck Institute of Psychiatry (DE)
- Harvard University (US)
- University of Helsinki (FI)
- Emory University (US)
- ORCID
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2019-08-09
- Volume
- 117
- Issue
- 38
- Pages
- 23280-23285
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC7519233
- OpenAlex
- W2968811349
- Cited by
- 209
- References
- 37
- Citations by year
- 2026: 16 · 2025: 22 · 2024: 32 · 2023: 34 · 2022: 28 · 2021: 46 · 2020: 24 · 2019: 7
- FWCI
- 10.17
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Archivio Istituzionale della Ricerca (Universita Degli Studi Di Milano) (submittedVersion, other-oa)
- Työväentutkimus Vuosikirja (submittedVersion)
- Site cant be reached (submittedVersion, other-oa)
- GoeScholar The Publication Server of the Georg-August-Universität Göttingen (Georg-August-Universität Göttingen) (submittedVersion, cc-by)
- Funders
- National Institute for Health and Care Research (NIHR201376, NF-SI-0616-10074)
- Canadian Institutes of Health Research
- Medical Research Council (MR/N029488/1)
- National Institute of Mental Health (K99MH108719, R00MH108719)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (R21HD088931)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Keywords
- glucocorticoids, prenatal stress, hippocampal neurogenesis, DNA methylation, epigenetics, hippocampal progenitor cells, stress response, differentially methylated sites, umbilical cord blood, mental illness, fetal brain development
- MeSH terms
- Female, Gene Expression Regulation, Glucocorticoids, Hippocampus, Humans, Male, Pregnancy, Prenatal Exposure Delayed Effects, Stress, Physiological, Cohort Studies, DNA Methylation, Neurogenesis
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