Epigenomic profiling of men exposed to early-life stress reveals DNA methylation differences in association with current mental state
Open accessAbstract
Early-life stress (ELS) is known to be associated with an increased risk of neuropsychiatric and cardiometabolic disease in later life. One of the potential mechanisms underpinning this is through effects on the epigenome, particularly changes in DNA methylation. Using a well-phenotyped cohort of 83 men from the Helsinki Birth Cohort Study, who experienced ELS in the form of separation from their parents during childhood, and a group of 83 matched controls, we performed a genome-wide analysis of DNA methylation in peripheral blood. We found no differences in DNA methylation between men who were separated from their families and non-separated men; however, we did identify differences in DNA methylation in association with the development of at least mild depressive symptoms over the subsequent 5-10 years. Notably, hypomethylation was identified at a number of genes with roles in brain development and/or function in association with depressive symptoms. Pathway analysis revealed an enrichment of DNA methylation changes in pathways associated with development and morphogenesis, DNA and transcription factor binding and programmed cell death. Our results support the concept that DNA methylation differences may be important in the pathogenesis of psychiatric disease.
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Among the most significant findings were hypomethylations in LGI1 and LGI2 in addition to other genes related to brain functioning.
“Among the most significant findings were hypomethylations in the genes coding for the leucine-rich glioma-inactivated protein 1 (LGI1, chromosomal location 10q23.33)and 2 (LGI2, chromosomal location 4p15.2) in addition to other genes related to brain functioning.”
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 Khulan et al., 2014
Pathway analysis revealed an overrepresentation of hypomethylated genes representing biological processes related to morphology and development, as well as DNA and transcription factor binding.
“Pathway analysis revealed an overrepresentation of hypomethylated genes representing biological processes related to morphology and development, as well as DNA and transcription factor binding (Khulan et al., 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 Khulan et al., 2014
When evaluating the development of depressive symptoms over a 5-10 year period, significant associations for 491 CpG probes in 351 different genes were discovered.
“However, when evaluating the development of depressive symptoms over a 5-10 year period significant associations for 491 CpG probes in 351 different genes were discovered (Khulan et al., 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 Khulan et al., 2014
Comparing 83 males exposed to early life stress in the form of separation from their parents to 83 non-separated controls, no epigenome-wide changes were detected.
“Comparing 83 males exposed to early life stress in form of separation from their parents to 83 non-separated controls, no epigenomewide changes were detected.”
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 Khulan et al., 2014
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1 retracted
Perroud, N., Dayer, A., Piguet, C., Nallet, A., Favre, S., Malafosse, A., & Aubry, J.-M. (2014) · British Journal of Psychiatry · doi:10.1192/bjp.bp.112.120055 · Cited by 89 · see citing works
RetractedGene Ontology: tool for the unification of biology
Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., Davis, A. P., Dolinski, K., Dwight, S. S., Eppig, J. T., et al. (2000) · Nature Genetics · doi:10.1038/75556 · Cited by 43,206 · see citing works
KEGG: Kyoto Encyclopedia of Genes and Genomes
Ogata, H., Goto, S., Sato, K., Fujibuchi, W., Bono, H., & Kanehisa, M. (1999) · Nucleic Acids Research · doi:10.1093/nar/27.1.29 · Cited by 31,232 · see citing works
Bioconductor: open software development for computational biology and bioinformatics
Gentleman, R., Carey, V., Bates, D., Bolstad, B., Dettling, M., Dudoit, S., Ellis, B., Gautier, L., Ge, Y., Gentry, J., et al. (2004) · Genome Biology · doi:10.1186/gb-2004-5-10-r80 · Cited by 13,133 · see citing works
Smyth, G. K. (2004) · Statistical Applications in Genetics and Molecular Biology · doi:10.2202/1544-6115.1027 · Cited by 11,829 · see citing works
Psychometric properties of the Beck Depression Inventory: Twenty-five years of evaluation
Beck, A. T., Steer, R. A., & Carbin, M. G. (1988) · Clinical Psychology Review · doi:10.1016/0272-7358(88)90050-5 · Cited by 11,696 · 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
Self-citationEpigenetic 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
lumi : a pipeline for processing Illumina microarray
Du, P., Kibbe, W. A., & Lin, S. M. (2008) · Bioinformatics · doi:10.1093/bioinformatics/btn224 · Cited by 2,028 · 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
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
Danese, A., Moffitt, T. E., Harrington, H., Milne, B. J., Polanczyk, G., Pariante, C. M., Poulton, R., & Caspi, A. (2009) · Archives of Pediatrics & Adolescent Medicine · doi:10.1001/archpediatrics.2009.214 · Cited by 1,165 · 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
On the Validity of the Beck Depression Inventory
Richter, P., Werner, J., Heerlein, A., Kraus, A., & Sauer, H. (1998) · Psychopathology · doi:10.1159/000066239 · Cited by 1,113 · see citing works
Gluckman, P. D., Hanson, M. A., & Beedle, A. S. (2007) · American Journal of Human Biology · doi:10.1002/ajhb.20590 · Cited by 1,006 · see citing works
Early growth and coronary heart disease in later life: longitudinal study
Eriksson, J. G., Forsén, T., Tuomilehto, J., Osmond, C., & Barker, D. J. P. (2001) · BMJ · doi:10.1136/bmj.322.7292.949 · Cited by 1,004 · see citing works
Self-citationDNA methylation and body-mass index: a genome-wide analysis
Dick, K. J., Nelson, C. P., Tsaprouni, L., Sandling, J. K., Aïssi, D., Wahl, S., Meduri, E., Morange, P.-E., Gagnon, F., Grallert, H., et al. (2014) · The Lancet · doi:10.1016/s0140-6736(13)62674-4 · Cited by 778 · see citing works
Epigenomic Profiling Reveals DNA-Methylation Changes Associated with Major Psychosis
Mill, J., Tang, T., Kaminsky, Z., Khare, T., Yazdanpanah, S., Bouchard, L., Jia, P., Assadzadeh, A., Flanagan, J., Schumacher, A., et al. (2008) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2008.01.008 · Cited by 773 · see citing works
Davies, M. N., Volta, M., Pidsley, R., Lunnon, K., Dixit, A., Lovestone, S., Coarfa, C., Harris, R. A., Milosavljevic, A., Troakes, C., et al. (2012) · Genome Biology · doi:10.1186/gb-2012-13-6-r43 · Cited by 630 · see citing works
Afifi, T. O., Enns, M. W., Cox, B. J., Asmundson, G. J. G., Stein, M. B., & Sareen, J. (2008) · American Journal of Public Health · doi:10.2105/ajph.2007.120253 · Cited by 558 · see citing works
Mehta, D., Klengel, T., Conneely, K. N., Smith, A. K., Altmann, A., Pace, T. W., Rex-Haffner, M., Loeschner, A., Gonik, M., Mercer, K. B., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1217750110 · Cited by 548 · see citing works
Genome-wide epigenetic regulation by early-life trauma
Labonté, B., Suderman, M., Maussion, G., Navaro, L., Yerko, V., Mahar, I., Bureau, A., Mechawar, N., Szyf, M., Meaney, M. J., et al. (2012) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2011.2287 · Cited by 488 · see citing works
Tyrka, A. R., Price, L. H., Marsit, C., Walters, O. C., & Carpenter, L. L. (2012) · PLoS ONE · doi:10.1371/journal.pone.0030148 · Cited by 486 · see citing works
Essex, M. J., Thomas Boyce, W., Hertzman, C., Lam, L. L., Armstrong, J. M., Neumann, S. M. A., & Kobor, M. S. (2013) · Child Development · doi:10.1111/j.1467-8624.2011.01641.x · Cited by 462 · see citing works
Dempster, E. L., Pidsley, R., Schalkwyk, L. C., Owens, S., Georgiades, A., Kane, F., Kalidindi, S., Picchioni, M., Kravariti, E., Toulopoulou, T., et al. (2011) · Human Molecular Genetics · doi:10.1093/hmg/ddr416 · Cited by 460 · see citing works
Broad Epigenetic Signature of Maternal Care in the Brain of Adult Rats
McGowan, P. O., Suderman, M., Sasaki, A., Huang, T. C. T., Hallett, M., Meaney, M. J., & Szyf, M. (2011) · PLoS ONE · doi:10.1371/journal.pone.0014739 · Cited by 452 · see citing works
DNA methylome profiling of human tissues identifies global and tissue-specific methylation patterns
Lokk, K., Modhukur, V., Rajashekar, B., Märtens, K., Mägi, R., Kolde, R., Koltšina, M., Nilsson, T. K., Vilo, J., Salumets, A., et al. (2014) · Genome Biology · doi:10.1186/gb-2014-15-4-r54 · Cited by 444 · see citing works
Depression in Ambulatory Medical Patients
Nielsen, A. C. (1980) · Archives of General Psychiatry · doi:10.1001/archpsyc.1980.01780220037003 · Cited by 421 · see citing works
Associations with early-life socio-economic position in adult DNA methylation
Borghol, N., Suderman, M. J., McArdle, W. L., Racine, A., Hallett, M. T., Pembrey, M. E., Hertzman, C., Power, C., & Moshe Szyf, A. (2011) · International Journal of Epidemiology · doi:10.1093/ije/dyr147 · Cited by 415 · see citing works
Pryce, C. R., Rüedi‐Bettschen, D., Dettling, A. C., Weston, A. A., Russig, H. D., Ferger, B., & Feldon, J. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.03.011 · Cited by 414 · see citing works
Rakyan, V. K., Down, T. A., Thorne, N., Flicek, P., Kulesha, E., Gräf, S., Tomazou, E. M., Bäckdahl, L., Johnson, N., Herberth, M., et al. (2008) · Genome Research · doi:10.1101/gr.077479.108 · Cited by 379 · see citing works
Differential immune system DNA methylation and cytokine regulation in post-traumatic stress disorder
Smith, A. K., Conneely, K. N., Kilaru, V., Mercer, K. B., Weiss, T. E., Bradley, B., Tang, Y., Gillespie, C. F., Cubells, J. F., & Ressler, K. J. (2011) · American Journal of Medical Genetics Part B: Neuropsychiatric Genetics · doi:10.1002/ajmg.b.31212 · Cited by 355 · see citing works
From promises to practical strategies in epigenetic epidemiology
Mill, J. S., & Heijmans, B. T. (2013) · Nature Reviews Genetics · doi:10.1038/nrg3405 · Cited by 347 · see citing works
Labonte, B., Yerko, V., Gross, J., Mechawar, N., Meaney, M. J., Szyf, M., & Turecki, G. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.01.034 · Cited by 345 · see citing works
Wang, Y., & Gorenstein, C. (2013) · Clinics · doi:10.6061/clinics/2013(09)15 · Cited by 295 · see citing works
Naumova, O. Y., Lee, M., Koposov, R. A., Moshe Szyf, A., Dozier, M., & Grigorenko, E. L. (2011) · Development and Psychopathology · doi:10.1017/s0954579411000605 · Cited by 251 · see citing works
DNA methylation: A mechanism for embedding early life experiences in the genome
Szyf, M., & Bick, J. (2013) · Child Development · doi:10.1111/j.1467-8624.2012.01793.x · Cited by 251 · see citing works
On the outside, looking in: A review and evaluation of the comparability of blood and brain “‐omes”
Tylee, D. S., Kawaguchi, D. M., & Glatt, S. J. (2013) · American Journal of Medical Genetics Part B: Neuropsychiatric Genetics · doi:10.1002/ajmg.b.32150 · Cited by 243 · see citing works
Sapienza, C., Lee, J. Y. H., Powell, J., Erinle, O., Yafai, F., Reichert, J., Siraj, E. S., & Madaio, M. P. (2011) · Epigenetics · doi:10.4161/epi.6.1.13362 · Cited by 208 · see citing works
Ouellet-Morin, I., Wong, C. C. Y., Danese, A., Pariante, C. M., Papadopoulos, A. S., Mill, J., & Arseneault, L. (2013) · Psychological Medicine · doi:10.1017/s0033291712002784 · Cited by 207 · see citing works
Beach, S. R. H., Brody, G. H., Todorov, A. A., Gunter, T. D., & Philibert, R. A. (2011) · Psychosomatic Medicine · doi:10.1097/psy.0b013e3181fdd074 · Cited by 195 · see citing works
Sareen, J., Henriksen, C. A., Bolton, S.-L., Afifi, T. O., Stein, M. B., & Asmundson, G. J. G. (2013) · Psychological Medicine · doi:10.1017/s003329171200102x · Cited by 163 · see citing works
Properties of the beck depression inventory as a screening instrument for adolescent depression
Barrera, M., & Garrison-Jones, C. V. (1988) · Research on Child and Adolescent Psychopathology · doi:10.1007/bf00913799 · Cited by 162 · see citing works
Pesonen, A.-K., Räikkönen, K., Feldt, K., Heinonen, K., Osmond, C., Phillips, D. I. W., Barker, D. J. P., Eriksson, J. G., & Kajantie, E. (2010) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2009.10.017 · Cited by 147 · see citing works
Self-citationGenome-Wide DNA Methylation Scan in Major Depressive Disorder
Sabunciyan, S., Aryee, M. J., Irizarry, R. A., Rongione, M. A., Webster, M. J., Kaufmann, W. E., Murakami, P. N., Lessard, A., Yolken, R. H., Feinberg, A. P., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0034451 · Cited by 132 · see citing works
Vijayendran, M., Beach, S. R. H., Plume, J. M., Brody, G. H., & Philibert, R. A. (2012) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2012.00055 · Cited by 126 · see citing works
Pesonen, A., Räikkönen, K., Heinonen, K., Kajantie, E., Forsén, T., & Eriksson, J. G. (2007) · American Journal of Epidemiology · doi:10.1093/aje/kwm254 · Cited by 118 · see citing works
Self-citationCardiovascular health of Finnish war evacuees 60 years later
Alastalo, H., Räikkönen, K., Pesonen, A.-K., Osmond, C., Barker, D. J. P., Kajantie, E., Heinonen, K., Forsén, T. J., & Eriksson, J. G. (2009) · Annals of Medicine · doi:10.1080/07853890802301983 · Cited by 116 · see citing works
Self-citationAberrant promoter methylation of multiple genes in oligodendrogliomas and ependymomas
Alonso, M. E., Bello, M. J., González‐Gómez, P., Arjona, D., Lomas, J., de Campos, J. M., Isla, A., Sarasa, J. L., & REY, J. A. (2003) · Cancer Genetics and Cytogenetics · doi:10.1016/s0165-4608(02)00928-7 · Cited by 115 · see citing works
Pesonen, A., Räikkönen, K., Heinonen, K., Kajantie, E., Forsén, T., & Eriksson, J. G. (2008) · American Journal of Human Biology · doi:10.1002/ajhb.20735 · Cited by 105 · see citing works
Self-citationGenes associated with autism spectrum disorder
Li, X., Zou, H., & Brown, W. T. (2012) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2012.05.017 · Cited by 102 · see citing works
Hoyer, D., & Bartfai, T. (2012) · Chemistry & Biodiversity · doi:10.1002/cbdv.201200288 · Cited by 102 · see citing works
Byrne, E. M., Carrillo‐Roa, T., Henders, A. K., Bowdler, L. M., McRae, A. F., Heath, A. C., Martin, N. G., Montgomery, G. W., Krause, L., & Wray, N. R. (2013) · Translational Psychiatry · doi:10.1038/tp.2013.45 · Cited by 100 · see citing works
Draxin Inhibits Axonal Outgrowth through the Netrin Receptor DCC
Ahmed, G., Shinmyo, Y., Ohta, K., Islam, S. M., Hossain, M., Naser, I. B., Riyadh, M. A., Su, Y., Zhang, S., Tessier‐Lavigne, M., et al. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.0943-11.2011 · Cited by 97 · see citing works
LGI Proteins in the Nervous System
Kegel, L., Aunin, E., Meijer, D., & Bermingham, J. R. (2013) · ASN NEURO · doi:10.1042/an20120095 · Cited by 96 · see citing works
Leukocyte DNA Methylation Signature Differentiates Pancreatic Cancer Patients from Healthy Controls
Pedersen, K. S., Bamlet, W. R., Oberg, A. L., de Andrade, M., Matsumoto, M., Tang, H. D., Thibodeau, S. N., Petersen, G. M., & Wang, L. (2011) · PLoS ONE · doi:10.1371/journal.pone.0018223 · Cited by 80 · see citing works
Räikkönen, K., Lahti‐Pulkkinen, M., Heinonen, K., Pesonen, A., Wahlbeck, K., Kajantie, E., Osmond, C., Barker, D. J. P., & Eriksson, J. G. (2010) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2010.07.003 · Cited by 77 · see citing works
Self-citationLack of Pur-alpha alters postnatal brain development and causes megalencephaly
Hokkanen, S. R. K., Feldmann, H.-J., Ding, H., Jung, C. K. E., Bojarski, Ł., Renner‐Müller, I., Schüller, U., Kretzschmar, H. A., Wolf, E., & Herms, J. W. (2011) · Human Molecular Genetics · doi:10.1093/hmg/ddr476 · Cited by 75 · see citing works
Cognitive ability and decline after early life stress exposure
Pesonen, A., Eriksson, J. G., Heinonen, K., Kajantie, E., Tuovinen, S., Alastalo, H., HENRIKSSON, M. M., Leskinen, J. T., Osmond, C., Barker, D. J. P., et al. (2013) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2012.12.012 · Cited by 64 · see citing works
Self-citationOhta, K., Ito, A., Kuriyama, S., Lupo, G., Kosaka, M., Ohnuma, S., Nakagawa, S., & Tanaka, H. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1100513108 · Cited by 63 · see citing works
Use of the Beck Depression Inventory-II with African American primary care patients
Dutton, G. R., Grothe, K. B., Jones, G. N., Whitehead, D., Kendra, K. E., & Brantley, P. J. (2004) · General Hospital Psychiatry · doi:10.1016/j.genhosppsych.2004.06.002 · Cited by 60 · see citing works
González-Cano, L., Herreros‐Villanueva, M., Fernández-Alonso, R., Ayuso‐Sacido, Á., Meyer, G., García‐Verdugo, J. M., Silva, A. D. N., Marqués, M. M., & Marín, M. C. (2010) · Cell Death and Disease · doi:10.1038/cddis.2010.87 · Cited by 60 · see citing works
Early Life Stress and Physical and Psychosocial Functioning in Late Adulthood
Alastalo, H., von Bonsdorff, M. B., Räikkönen, K., Pesonen, A., Osmond, C., Barker, D. J. P., Heinonen, K., Kajantie, E., & Eriksson, J. G. (2013) · PLoS ONE · doi:10.1371/journal.pone.0069011 · Cited by 58 · see citing works
Self-citationUddin, M., Galea, S., Chang, S. C., Koenen, K. C., Goldmann, E., Wildman, D. E., & Aiello, A. E. (2013) · Biodemography and Social Biology · doi:10.1080/19485565.2013.774627 · Cited by 39 · see citing works
Alastalo, H., Räikkönen, K., Pesonen, A.-K., Osmond, C., Barker, D. J. P., Heinonen, K., Kajantie, E., & Eriksson, J. G. (2012) · Psychosomatic Medicine · doi:10.1097/psy.0b013e31825b3d76 · Cited by 32 · see citing works
Self-citationHossain, M., Ahmed, G., Naser, I. B., Shinmyo, Y., Ito, A., Riyadh, M. A., Felemban Athary Abdulhaleem, M., Song, X., Ohta, K., & Tanaka, H. (2012) · Developmental Biology · doi:10.1016/j.ydbio.2012.11.029 · Cited by 30 · see citing works
Kortleven, C., Bruneau, L. C., & Trudeau, L. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.07.037 · Cited by 29 · see citing works
Epilepsy GeneLGI1Regulates Postnatal Developmental Remodeling of Retinogeniculate Synapses
Zhou, Y., Zhang, D., Özkaynak, E., Wang, X., Kasper, E. M., Leguern, É., Baulac, S., & Anderson, M. P. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.5191-11.2012 · Cited by 29 · see citing works
Identification of the promoter, genomic structure, and mouse ortholog of LGI1
Somerville, R. P. T., Chernova, O. B., Liu, S., Shoshan, Y., & Cowell, J. K. (2000) · Mammalian Genome · doi:10.1007/s0033500101280 · Cited by 28 · see citing works
Apolipoprotein CI Knock-Out Mice Display Impaired Memory Functions
Berbée, J. F. P., Vanmierlo, T., Abildayeva, K., Blokland, A., Jansen, P. J., Lütjohann, D., Gautier, T., Sijbrands, E. J. G., Prickaerts, J., Hadfoune, M., et al. (2011) · Journal of Alzheimer s Disease · doi:10.3233/jad-2010-100576 · Cited by 23 · see citing works
DNA demethylation of neuronal cell death genes in depression
Xin, Y., O’Donell, A., Ge, Y., Chanrion, B., Dwork, A. J., Arango, V., Mann, J. J., & Haghighi, F. G. (2013) · Epigenetics & Chromatin · doi:10.1186/1756-8935-6-s1-p113 · Cited by 3 · see citing works
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Jawahar, M. C., Murgatroyd, C., Harrison, E. L., & Baune, B. T. (2015) · Clinical Epigenetics · doi:10.1186/s13148-015-0156-3 · Cited by 165 · see citing works
Schiele, M. A., Gottschalk, M. G., & Domschke, K. (2020) · Clinical Psychology Review · doi:10.1016/j.cpr.2020.101830 · Cited by 156 · see citing works
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Noyes, B. K., Munoz, D. P., Khalid‐Khan, S., Brietzke, E. M., & Booij, L. (2022) · Journal of Affective Disorders · doi:10.1016/j.jad.2022.04.067 · Cited by 103 · see citing works
Sparrow, S. A., Manning, J. R., Cartier, J., Anblagan, D., Bastin, M. E., Piyasena, C., Pataky, R., Moore, E. J., Semple, S. I., Wilkinson, A. G., et al. (2016) · Translational Psychiatry · doi:10.1038/tp.2015.210 · Cited by 85 · see citing works
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Jones, M. J., Moore, S. R., & Kobor, M. S. (2017) · Annual Review of Psychology · doi:10.1146/annurev-psych-122414-033653 · Cited by 88 · see citing works
Huang, Y., Ollikainen, M., Muniandy, M., Zhang, T., van Dongen, J., Hao, G., van der Most, P. J., Pan, Y., Pervjakova, N., Sun, Y. V., et al. (2020) · Hypertension · doi:10.1161/hypertensionaha.120.14973 · Cited by 78 · see citing works
Self-citationSakharkar, A. J., Kyzar, E. J., Gavin, D. P., Zhang, H., Chen, Y., Krishnan, H. R., Grayson, D. R., & Pandey, S. C. (2019) · Neuropharmacology · doi:10.1016/j.neuropharm.2019.107679 · Cited by 75 · see citing works
Holmes, L., Shutman, E., Chinaka, C., Deepika, K., Pelaez, L., & DABNEY, K. W. (2019) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph16214280 · Cited by 75 · see citing works
Nöthling, J., Malan-Müller, S., Abrahams, N., Hemmings, S. M. J., & Seedat, S. (2020) · The World Journal of Biological Psychiatry · doi:10.1080/15622975.2019.1583369 · Cited by 74 · see citing works
Humphreys, K. L., Moore, S. R., Davis, E., MacIsaac, J. L., Lin, D. T. S., Kobor, M. S., & Gotlib, I. H. (2019) · Translational Psychiatry · doi:10.1038/s41398-019-0582-7 · Cited by 67 · see citing works
Blaze, J., & Roth, T. L. (2015) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2015.04.004 · Cited by 62 · see citing works
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Blaze, J., Asok, A., & Roth, T. L. (2015) · Stress · doi:10.3109/10253890.2015.1071790 · Cited by 52 · see citing works
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Tomassi, S., & Tosato, S. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.10.018 · Cited by 51 · see citing works
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Lahti, J., Ala-Mikkula, H., Kajantie, E., Haljas, K., Eriksson, J. G., & Räikkönen, K. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.10.022 · Cited by 37 · see citing works
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Mehta, D., Pelzer, E. S., Bruenig, D., Lawford, B., McLeay, S., Morris, C. P., Gibson, J. N., Young, R. M., Voisey, J., McLeay, S., et al. (2019) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2019.06.001 · Cited by 37 · see citing works
Hao, G., Youssef, N. A., Davis, C. L., & Su, S. (2017) · International Journal of Cardiology · doi:10.1016/j.ijcard.2017.12.063 · Cited by 36 · see citing works
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DNA methylation profiles of elderly individuals subjected to indentured childhood labor and trauma
Marinova, Z., Maercker, A. R. A., Küffer, A., Robinson, M. D., Wojdacz, T. K., Walitza, S., Grünblatt, E., & Burri, A. V. (2017) · BMC Medical Genetics · doi:10.1186/s12881-017-0370-2 · Cited by 31 · see citing works
Løkhammer, S., Stavrum, A.-K., Polushina, T. V., Aas, M., Ottesen, A. A., Andreassen, O. A., Melle, I. S., & Hellard, S. L. (2022) · Translational Psychiatry · doi:10.1038/s41398-022-01936-8 · Cited by 29 · see citing works
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Rana, A. K. (2018) · Egyptian Journal of Forensic Sciences · doi:10.1186/s41935-018-0042-1 · Cited by 29 · see citing works
Kim, A. W., Adam, E. K., Bechayda, S. A., & Kuzawa, C. W. (2020) · American Journal of Physical Anthropology · doi:10.1002/ajpa.24105 · Cited by 23 · see citing works
Steyn, A. W., Crowther, N. J., Norris, S. A., Rabionet, R., Estivill, X., & Ramsay, M. (2019) · Epigenomics · doi:10.2217/epi-2018-0206 · Cited by 25 · see citing works
Investigating epigenetic consequences of early-life adversity: some methodological considerations
Fiori, L. M., & Turecki, G. (2016) · European Journal of Psychotraumatology · doi:10.3402/ejpt.v7.31593 · Cited by 20 · see citing works
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Holmes, L., Chinaka, C., Elmi, H., Deepika, K., Pelaez, L., Enwere, M., Akinola, O., & DABNEY, K. W. (2019) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph16214123 · Cited by 18 · see citing works
Zhang, Y., & Liu, C. (2022) · Epigenomics · doi:10.2217/epi-2021-0190 · Cited by 17 · see citing works
DNA Methylation: A Mediator Between Parenting Stress and Adverse Child Development?
Mulder, R. H., Rijlaarsdam, J., & van IJzendoorn, M. H. (2017) · Springer eBooks · doi:10.1007/978-3-319-55376-4_7 · Cited by 15 · see citing works
Schang, A., Sabéran‐Djoneidi, D., & Mezger, V. (2017) · Clinical Genetics · doi:10.1111/cge.13097 · Cited by 15 · see citing works
Musazzi, L., Paoli, C., Misztak, P., & Mazzini, G. (2022) · Current Neuropharmacology · doi:10.2174/1570159x20666220201084536 · Cited by 15 · see citing works
Khaw, Y. M., Majid, D., Oh, S., Kang, E., & Inoue, M. (2021) · Nature Communications · doi:10.1038/s41467-020-20302-0 · Cited by 12 · see citing works
Watamura, S. E., & Roth, T. L. (2018) · Developmental Psychobiology · doi:10.1002/dev.21796 · Cited by 11 · see citing works
Cartier, J., Piyasena, C., Sparrow, S. A., Boardman, J. P., & Drake, A. J. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.13825 · Cited by 9 · see citing works
Self-citationSaygıdeğer, Y., Özkan, H., Baydar, O., & Yılmaz, Ö. (2022) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s2040174422000083 · Cited by 8 · see citing works
Carlos, J., Holuka, C., Menta, G., Turner, J. D., Vögele, C., & D’Ambrosio, C. (2022) · Biological Psychology · doi:10.1016/j.biopsycho.2022.108463 · Cited by 7 · see citing works
Xiao, Y., Wang, J., Siegel, P. B., Cline, M. A., & Gilbert, E. R. (2020) · Life · doi:10.3390/life10050051 · Cited by 5 · see citing works
Inaba, Y., Iwamoto, S., & Nakayama, K. (2022) · Journal of PHYSIOLOGICAL ANTHROPOLOGY · doi:10.1186/s40101-022-00305-0 · Cited by 4 · see citing works
Stojkov, N. J., Bjelic, M. M., Pletikosic, S. M. R., Mihajlović, A. I., Sokanovic, S. J., Baburski, A. Z., Janjic, M. M., Kostic, T. S., & Andrić, S. A. (2015) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2015.05.019 · Cited by 4 · see citing works
Pigatto, F., Grant, C. C., Marks, E. J., Walker, C. G., Fletcher, B., & Waldie, K. E. (2024) · Journal of Affective Disorders · doi:10.1016/j.jad.2024.09.143 · Cited by 3 · see citing works
Trauma and Gene Expression: Understanding the Connections
Pilkay, S. R., & Combs-Orme, T. D. (2020) · Social Work Research · doi:10.1093/swr/svz024 · Cited by 2 · see citing works
Korobkova, L., Thornton, M. E., Collin, M. A., Morin, E. L., Aoued, H. S., Sannigrahi, S., Bhinderwala, N., Garza, K. M., Siebert, E. R., Walum, H., et al. (2025) · Biological Psychiatry · doi:10.1016/j.biopsych.2025.08.020 · Cited by 1 · see citing works
Psychosocial Impact of Epigenetics in Pediatrics
Gong, X., & Rubin, L. P. (2019) · Springer eBooks · doi:10.1007/978-3-319-55530-0_100 · Cited by 1 · see citing works
Epigenetics of major depressive disorder
Braun, P., & Potash, J. (2021) · Epigenetics in Psychiatry · doi:10.1016/b978-0-12-823577-5.00002-7
Korobkova, L., Morin, E. L., Aoued, H. S., Sannigrahi, S., Garza, K., Siebert, E. R., Walum, H., Cabeen, R. P., Sánchez, M. M., & Dias, B. G. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.02.23.529808 · Cited by 1 · see citing works
Lawford‐Smith, H. (2015)
Psychosocial Impact of Epigenetics in Pediatrics
Gong, X., & Rubin, L. P. (2017) · Springer eBooks · doi:10.1007/978-3-319-31143-2_100-1
Mediation and Moderation of Intergenerational Epigenetic Effects of Trauma
Pilkay, S. R. (2017)
Ünal, M. (2021) · Biochemistry · doi:10.5772/intechopen.99964
New insights into the link between childhood adversity and epigenetic changes
Lin, P., & Eapen, V. (2023) · The Lancet Child & Adolescent Health · doi:10.1016/s2352-4642(23)00106-2
Epigenetics in neurobehavioral disease
Løkhammer, S. (2023) · Elsevier eBooks · doi:10.1016/b978-0-443-18661-5.00012-9
Inaba, Y., Iwamoto, S., & Nakayama, K. (2022) · Figshare · doi:10.6084/m9.figshare.20521140
- Authors
- Khulan, B., Manning, J. R., Dunbar, D. R., Seckl, J. R., Raikkonen, K., Eriksson, J. G., & Drake, A. J.
- Affiliations
- The Queen's Medical Research Institute (GB)
- University of Helsinki (FI)
- Corresponding author
- Drake, A J
- Venue
- Translational Psychiatry
- Published
- 2014-09-23
- Volume
- 4
- Issue
- 9
- Pages
- e448-e448
- ISSN
- 2158-3188 (ISSN-L)
- PMC
- PMC4203020
- OpenAlex
- W2039214507
- Cited by
- 59
- References
- 71
- Citations by year
- 2025: 1 · 2024: 1 · 2023: 3 · 2022: 8 · 2021: 5 · 2020: 6 · 2019: 10 · 2018: 4 · 2017: 8 · 2016: 5 · 2015: 8
- FWCI
- 2.87
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Translational Psychiatry (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, cc-by-nc-nd)
- Työväentutkimus Vuosikirja (submittedVersion)
- STM:n Hallinnonalan avoin julkaisuarkisto (Julkari) (submittedVersion)
- Funders
- Finska Läkaresällskapet
- Wellcome Trust (104036/Z/14/Z, 104036)
- British Heart Foundation (104036/Z/14/Z)
- European Commission (278603)
- Signe ja Ane Gyllenbergin Säätiö
- Samfundet Folkhälsan
- Medical Research Council (104036/Z/14/Z, EU FP7)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Social Sciences › Psychology › Clinical Psychology › Child Abuse and Trauma
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Maternal Mental Health During Pregnancy and Postpartum
- Keywords
- early life stress, DNA methylation, epigenomics, depressive symptoms, brain development genes, programmed cell death, men, Helsinki Birth Cohort Study
- MeSH terms
- Aged, Mental Disorders, Female, Finland, Humans, Male, Men, Middle Aged, Stress, Psychological, Cohort Studies, DNA Methylation, Epigenesis, Genetic, Epigenomics
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