Differential impact of prenatal PTSD symptoms and preconception trauma exposure on placental NR3C1 and FKBP5 methylation

References

• ACOG. (2019). ACOG committee opinion No. 777: Sexual assault. Obstetrics & Gynecology, 133(4), 1–10. https://doi.org/10.1097/AOG.0000000000003178
   Web of Science ®Google Scholar
• American Psychiatric Association. (1994). Diagnostic and statistical manual of mental disorders (4th ed.). https://search.library.wisc.edu/catalog/999733358502121
   Google Scholar
• Appleton, A. A., Lester, B. M., Armstrong, D. A., Lesseur, C., & Marsit, C. J. (2015). Examining the joint contribution of placental NR3C1 and HSD11B2 methylation for infant neurobehavior. Psychoneuroendocrinology, 52, 32–42. https://doi.org/10.1016/j.psyneuen.2014.11.004
   PubMed Web of Science ®Google Scholar
• Bierer, L. M., Bader, H. N., Daskalakis, N. P., Lehrner, A., Provençal, N., Wiechmann, T., Klengel, T., Makotkine, I., Binder, E. B., & Yehuda, R. (2020). Intergenerational effects of maternal holocaust exposure on FKBP5 methylation. The American Journal of Psychiatry, 177(8), 744–753. https://doi.org/10.1176/appi.ajp.2019.19060618
   PubMed Web of Science ®Google Scholar
• Bonnin, A., & Levitt, P. (2011). Fetal, maternal, and placental sources of serotonin and new implications for developmental programming of the brain. Neuroscience, 197, 1–7. https://doi.org/10.1016/j.neuroscience.2011.10.005
   PubMed Web of Science ®Google Scholar
• Bowers, M. E., & Yehuda, R. (2016). Intergenerational transmission of stress in humans. Neuropsychopharmacology, 41(1), 232–244. https://doi.org/10.1038/npp.2015.247
   PubMed Web of Science ®Google Scholar
• Bromer, C., Marsit, C. J., Armstrong, D. A., Padbury, J. F., & Lester, B. (2013). Genetic and epigenetic variation of the glucocorticoid receptor (NR3C1) in placenta and infant neurobehavior. Developmental Psychobiology, 55(7), 673–683. https://doi.org/10.1002/dev.21061
   PubMed Web of Science ®Google Scholar
• Bulka, C. M., Everson, T. M., Burt, A. A., Marsit, C. J., Karagas, M. R., Boyle, K. E., Niemiec, S., Kechris, K., Davidson, E. J., Yang, I. V., Feinberg, J. I., Volk, H. E., Ladd-Acosta, C., Breton, C. V., O’Shea, T. M., & Fry, R. C. (2023). Sex-based differences in placental DNA methylation profiles related to gestational age: An NIH ECHO meta-analysis. Epigenetics, 18(1), 2179726. https://doi.org/10.1080/15592294.2023.2179726
   PubMed Web of Science ®Google Scholar
• Capron, L. E., Ramchandani, P. G., & Glover, V. (2018). Maternal prenatal stress and placental gene expression of NR3C1 and HSD11B2: The effects of maternal ethnicity. Psychoneuroendocrinology, 87, 166–172. https://doi.org/10.1016/j.psyneuen.2017.10.019
   PubMed Web of Science ®Google Scholar
• Caspi, A., Hariri, A. R., Holmes, A., Uher, R., & Moffitt, T. E. (2010). Genetic sensitivity to the environment: The case of the serotonin transporter gene and its implications for studying complex diseases and traits. The American Journal of Psychiatry, 167(5), 509–527. https://doi.org/10.1176/appi.ajp.2010.09101452
   PubMed Web of Science ®Google Scholar
• Conradt, E., Fei, M., LaGasse, L., Tronick, E., Guerin, D., Gorman, D., Marsit, C. J., & Lester, B. M. (2015). Prenatal predictors of infant self-regulation: The contributions of placental DNA methylation of NR3C1 and neuroendocrine activity. Frontiers in Behavioral Neuroscience, 9, 130. https://doi.org/10.3389/fnbeh.2015.00130
   PubMed Web of Science ®Google Scholar
• Conradt, E., Lester, B. M., Appleton, A. A., Armstrong, D. A., & Marsit, C. J. (2013). The roles of DNA methylation of NR3C1 and 11beta-HSD2 and exposure to maternal mood disorder in utero on newborn neurobehavior. Epigenetics, 8(12), 1321–1329. https://doi.org/10.4161/epi.26634
   PubMed Web of Science ®Google Scholar
• Conradt, E., Ostlund, B., Guerin, D., Armstrong, D. A., Marsit, C. J., Tronick, E., LaGasse, L., & Lester, B. M. (2019). DNA methylation of NR3c1 in infancy: Associations between maternal caregiving and infant sex. Infant Mental Health Journal, 40(4), 513–522. https://doi.org/10.1002/imhj.21789
   PubMed Web of Science ®Google Scholar
• Cook, N., Ayers, S., & Horsch, A. (2018). Maternal posttraumatic stress disorder during the perinatal period and child outcomes: A systematic review. Journal of Affective Disorders, 225, 18–31. https://doi.org/10.1016/j.jad.2017.07.045
   PubMed Web of Science ®Google Scholar
• Dereix, A. E., Ledyard, R., Redhunt, A. M., Bloomquist, T. R., Brennan, K. J., Baccarelli, A. A., Hacker, M. R., & Burris, H. H. (2021). Maternal anxiety and depression in pregnancy and DNA methylation of the NR3C1 glucocorticoid receptor gene. Epigenomics, 13(21), 1701–1709. https://doi.org/10.2217/epi-2020-0022
   PubMed Web of Science ®Google Scholar
• Finik, J., Buthmann, J., Zhang, W., Go, K., & Nomura, Y. (2020). Placental gene expression and offspring temperament trajectories: Predicting negative affect in early childhood. Journal of Abnormal Child Psychology, 48(6), 783–795. https://doi.org/10.1007/s10802-020-00632-9
   PubMed Web of Science ®Google Scholar
• Fransquet, P. D., Hjort, L., Rushiti, F., Wang, S. J., Krasniqi, S. P., Çarkaxhiu, S. I., Arifaj, D., Xhemaili, V. D., Salihu, M., Leku, N. A., & Ryan, J. (2022). DNA methylation in blood cells is associated with cortisol levels in offspring of mothers who had prenatal post-traumatic stress disorder. Stress and Health, 38(4), 755–766. https://doi.org/10.1002/smi.3131
   PubMed Web of Science ®Google Scholar
• Gokhale, P., Young, M. R., Williams, M. N., Reid, S. N., Tom, L. S., O’Brian, C. A., & Simon, M. A. (2020). Refining trauma-informed perinatal care for urban prenatal care patients with multiple lifetime traumatic exposures: A qualitative study. Journal of Midwifery & Women’s Health, 65(2), 224–230. https://doi.org/10.1111/jmwh.13063
   PubMed Web of Science ®Google Scholar
• González Ramírez, C., Villavicencio Queijeiro, A., Jiménez Morales, S., Bárcenas López, D., Hidalgo Miranda, A., Ruiz Chow, A., Tellez Cárdenas, L., & Guardado Estrada, M. (2020). The NR3C1 gene expression is a potential surrogate biomarker for risk and diagnosis of posttraumatic stress disorder. Psychiatry Research, 284, 112797. https://doi.org/10.1016/j.psychres.2020.112797
   PubMed Web of Science ®Google Scholar
• Gottfried, A. W. (1985). Measures of socioeconomic status in child development research: Data and recommendations. Merrill Palmer Q, 31, 85–92.
   Web of Science ®Google Scholar
• Harris-Britt, A., Martin, S. L., Li, Y., Casanueva, C., & Kupper, L. L. (2004). Posttraumatic stress disorder and associated functional impairments during pregnancy: Some consequences of violence against women. Journal of Clinical Psychology in Medical Settings, 11(4), 253–264. https://doi.org/10.1023/B:JOCS.0000045345.72671.5e
   Web of Science ®Google Scholar
• Heim, C., & Binder, E. B. (2012). Current research trends in early life stress and depression: Review of human studies on sensitive periods, gene-environment interactions, and epigenetics. Experimental Neurology, 233(1), 102–111. https://doi.org/10.1016/j.expneurol.2011.10.032
   PubMed Web of Science ®Google Scholar
• Kaouane, N., Porte, Y., Vallée, M., Brayda-Bruno, L., Mons, N., Calandreau, L., Marighetto, A., Piazza, P. V., & Desmedt, A. (2012). Glucocorticoids can induce PTSD-like memory impairments in mice. Science, 335(6075), 1510–1513. https://doi.org/10.1126/science.1207615
   PubMed Web of Science ®Google Scholar
• Kertes, D. A., Kamin, H. S., Hughes, D. A., Rodney, N. C., Bhatt, S., & Mulligan, C. J. (2016). Prenatal maternal stress predicts methylation of genes regulating the hypothalamic-pituitary-adrenocortical system in mothers and newborns in the democratic republic of Congo. Child Development, 87(1), 61–72. https://doi.org/10.1111/cdev.12487
   PubMed Web of Science ®Google Scholar
• Klengel, T., Mehta, D., Anacker, C., Rex-Haffner, M., Pruessner, J. C., Pariante, C. M., Pace, T. W., Mercer, K. B., Mayberg, H. S., Bradley, B., Nemeroff, C. B., Holsboer, F., Heim, C. M., Ressler, K. J., Rein, T., & Binder, E. B. (2013). Allele-specific FKBP5 DNA demethylation mediates gene-childhood trauma interactions. Nature Neuroscience, 16(1), 33–41. https://doi.org/10.1038/nn.3275
   PubMed Web of Science ®Google Scholar
• Kubo, K. Y., Suzuki, A., Iinuma, M., Sato, Y., Nagashio, R., Ohta, E., & Azuma, K. (2019). Vulnerability to stress in mouse offspring is ameliorated when pregnant dams are provided a chewing stick during prenatal stress. Archives of Oral Biology, 97, 150–155. https://doi.org/10.1016/j.archoralbio.2018.10.014
   PubMed Web of Science ®Google Scholar
• Liu, H., Petukhova, M. V., Sampson, N. A., Aguilar-Gaxiola, S., Alonso, J., Andrade, L. H., Bromet, E. J., de Girolamo, G., Haro, J. M., Hinkov, H., Kawakami, N., Koenen, K. C., Kovess-Masfety, V., Lee, S., Medina-Mora, M. E., Navarro-Mateu, F., O’Neill, S., Piazza, M., Posada-Villa, J., … Kessler, R. C. (2017). Association of DSM-IV posttraumatic stress disorder with traumatic experience type and history in the World Health Organization World Mental Health Surveys. JAMA Psychiatry, 74(3), 270–281. https://doi.org/10.1001/jamapsychiatry.2016.3783
   PubMed Web of Science ®Google Scholar
• Maccani, M. A., & Marsit, C. J. (2009). Epigenetics in the placenta. American Journal of Reproductive Immunology (New York, NY: 1989), 62(2), 78–89. https://doi.org/10.1111/j.1600-0897.2009.00716.x
   PubMed Web of Science ®Google Scholar
• Meaney, M. J., Szyf, M., & Seckl, J. R. (2007). Epigenetic mechanisms of perinatal programming of hypothalamic-pituitary-adrenal function and health. Trends in Molecular Medicine, 13(7), 269–277. https://doi.org/10.1016/j.molmed.2007.05.003
   PubMed Web of Science ®Google Scholar
• Mulligan, C. J., D’Errico, N. C., Stees, J., & Hughes, D. A. (2012). Methylation changes at NR3C1 in newborns associate with maternal prenatal stress exposure and newborn birth weight. Epigenetics, 7(8), 853–857. https://doi.org/10.4161/epi.21180
   PubMed Web of Science ®Google Scholar
• National Center for Posttraumatic Stress Disorder. (2021). How common is PTSD in adults? https://www.ptsd.va.gov/understand/common/common_adults.asp
   Google Scholar
• Nomura, Y., Rompala, G., Pritchett, L., Aushev, V., Chen, J., & Hurd, Y. L. (2021). Natural disaster stress during pregnancy is linked to reprogramming of the placenta transcriptome in relation to anxiety and stress hormones in young offspring. Molecular Psychiatry, 26(11), 6520–6530. https://doi.org/10.1038/s41380-021-01123-z
   PubMed Web of Science ®Google Scholar
• Ostlund, B. D., Conradt, E., Crowell, S. E., Tyrka, A. R., Marsit, C. J., & Lester, B. M. (2016). Prenatal stress, fearfulness, and the epigenome: Exploratory analysis of sex differences in DNA methylation of the glucocorticoid receptor gene. Frontiers in Behavioral Neuroscience, 10, 147. https://doi.org/10.3389/fnbeh.2016.00147
   PubMed Web of Science ®Google Scholar
• Palma-Gudiel, H., Cirera, F., Crispi, F., Eixarch, E., & Fañanás, L. (2018). The impact of prenatal insults on the human placental epigenome: A systematic review. Neurotoxicology and Teratology, 66, 80–93. https://doi.org/10.1016/j.ntt.2018.01.001
   PubMed Web of Science ®Google Scholar
• Palma-Gudiel, H., Córdova-Palomera, A., Eixarch, E., Deuschle, M., & Fañanás, L. (2015). Maternal psychosocial stress during pregnancy alters the epigenetic signature of the glucocorticoid receptor gene promoter in their offspring: A meta-analysis. Epigenetics, 10(10), 893–902. https://doi.org/10.1080/15592294.2015.1088630
   PubMed Web of Science ®Google Scholar
• Palma-Gudiel, H., Córdova-Palomera, A., Leza, J. C., & Fañanás, L. (2015). Glucocorticoid receptor gene (NR3C1) methylation processes as mediators of early adversity in stress-related disorders causality: A critical review. Neuroscience and Biobehavioral Reviews, 55, 520–535. https://doi.org/10.1016/j.neubiorev.2015.05.016
   PubMed Web of Science ®Google Scholar
• Paquette, A. G., Lester, B. M., Koestler, D. C., Lesseur, C., Armstrong, D. A., & Marsit, C. J. (2014). Placental FKBP5 genetic and epigenetic variation is associated with infant neurobehavioral outcomes in the RICHS cohort. PLoS One, 9(8), e104913. https://doi.org/10.1371/journal.pone.0104913
   PubMed Web of Science ®Google Scholar
• Paquette, A. G., Lester, B. M., Lesseur, C., Armstrong, D. A., Guerin, D. J., Appleton, A. A., & Marsit, C. J. (2015). Placental epigenetic patterning of glucocorticoid response genes is associated with infant neurodevelopment. Epigenomics, 7(5), 767–779. https://doi.org/10.2217/epi.15.28
   PubMed Web of Science ®Google Scholar
• Parade, S. H., Huffhines, L., Daniels, T. E., Stroud, L. R., Nugent, N. R., & Tyrka, A. R. (2021). A systematic review of childhood maltreatment and DNA methylation: Candidate gene and epigenome-wide approaches. Translational Psychiatry, 11(1), 134. https://doi.org/10.1038/s41398-021-01207-y
   PubMed Web of Science ®Google Scholar
• Perez, M. F., & Lehner, B. (2019). Intergenerational and transgenerational epigenetic inheritance in animals. Nature Cell Biology, 21(2), 143–151. https://doi.org/10.1038/s41556-018-0242-9
   PubMed Web of Science ®Google Scholar
• Racine, N., Plamondon, A., Madigan, S., McDonald, S., & Tough, S. (2018). Maternal adverse childhood experiences and infant development. Pediatrics, 141(4), e20172495. https://doi.org/10.1542/peds.2017-2495
   PubMed Web of Science ®Google Scholar
• Robinson, S. M., Sobell, L. C., Sobell, M. B., & Leo, G. I. (2014). Reliability of the Timeline Followback for cocaine, cannabis, and cigarette use. Psychology of Addictive Behaviors, 28(1), 154–162. https://doi.org/10.1037/a0030992
   PubMed Web of Science ®Google Scholar
• Rosenblum, K. L., Muzik, M., Morelen, D. M., Alfafara, E. A., Miller, N. M., Waddell, R. M., Schuster, M. M., & Ribaudo, J. (2017). A community-based randomized controlled trial of Mom Power parenting intervention for mothers with interpersonal trauma histories and their young children. Archives of Women’s Mental Health, 20(5), 673–686. https://doi.org/10.1007/s00737-017-0734-9
   PubMed Web of Science ®Google Scholar
• Sapolsky, R. M., Romero, L. M., & Munck, A. U. (2000). How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Reviews, 21(1), 55–89. https://doi.org/10.1210/edrv.21.1.0389
   PubMed Web of Science ®Google Scholar
• Seng, J. S., Rauch, S. A., Resnick, H., Reed, C. D., King, A., Low, L. K., McPherson, M., Muzik, M., Abelson, J., & Liberzon, I. (2010). Exploring posttraumatic stress disorder symptom profile among pregnant women. Journal of Psychosomatic Obstetrics and Gynaecology, 31(3), 176–187. https://doi.org/10.3109/0167482X.2010.486453
   PubMed Web of Science ®Google Scholar
• Sheerin, C. M., Lind, M. J., Bountress, K. E., Marraccini, M. E., Amstadter, A. B., Bacanu, S. A., & Nugent, N. R. (2020). Meta-analysis of associations between hypothalamic-pituitary-adrenal axis genes and risk of posttraumatic stress disorder. Journal of Traumatic Stress, 33(5), 688–698. https://doi.org/10.1002/jts.22484
   PubMed Web of Science ®Google Scholar
• Szeszko, P. R., Lehrner, A., & Yehuda, R. (2018). Glucocorticoids and hippocampal structure and function in PTSD. Harvard Review of Psychiatry, 26(3), 142–157. https://doi.org/10.1097/HRP.0000000000000188
   PubMed Web of Science ®Google Scholar
• Szyf, M., Weaver, I., & Meaney, M. (2007). Maternal care, the epigenome and phenotypic differences in behavior. Reproductive Toxicology (Elmsford, NY), 24(1), 9–19. https://doi.org/10.1016/j.reprotox.2007.05.001
   PubMed Web of Science ®Google Scholar
• Tyrka, A. R., Price, L. H., Marsit, C., Walters, O. C., & Carpenter, L. L. (2012). Childhood adversity and epigenetic modulation of the leukocyte glucocorticoid receptor: Preliminary findings in healthy adults. PLoS One. 7(1), e30148. https://doi.org/10.1371/journal.pone.0030148
   PubMed Web of Science ®Google Scholar
• van Zuiden, M., Kavelaars, A., Geuze, E., Olff, M., & Heijnen, C. J. (2013). Predicting PTSD: Pre-existing vulnerabilities in glucocorticoid-signaling and implications for preventive interventions. Brain, Behavior, and Immunity, 30, 12–21. https://doi.org/10.1016/j.bbi.2012.08.015
   PubMed Web of Science ®Google Scholar
• Ward, L. G. (2020). Trauma-informed perinatal healthcare for survivors of sexual violence. The Journal of Perinatal & Neonatal Nursing, 34(3), 199–202. https://doi.org/10.1097/JPN.0000000000000501
   PubMed Web of Science ®Google Scholar
• Watkeys, O. J., Kremerskothen, K., Quidé, Y., Fullerton, J. M., & Green, M. J. (2018). Glucocorticoid receptor gene (NR3C1) DNA methylation in association with trauma, psychopathology, transcript expression, or genotypic variation: A systematic review. Neuroscience and Biobehavioral Reviews, 95, 85–122. https://doi.org/10.1016/j.neubiorev.2018.08.017
   PubMed Web of Science ®Google Scholar
• Yehuda, R. (2009). Status of glucocorticoid alterations in post-traumatic stress disorder. Annals of the New York Academy of Sciences, 1179(1), 56–69. https://doi.org/10.1111/j.1749-6632.2009.04979.x
   PubMedGoogle Scholar
• Yehuda, R., Daskalakis, N. P., Bierer, L. M., Bader, H. N., Klengel, T., Holsboer, F., & Binder, E. B. (2016). Holocaust exposure induced intergenerational effects on FKBP5 methylation. Biological Psychiatry, 80(5), 372–380. https://doi.org/10.1016/j.biopsych.2015.08.005
   PubMed Web of Science ®Google Scholar
• Yildiz, P. D., Ayers, S., & Phillips, L. (2017). The prevalence of posttraumatic stress disorder in pregnancy and after birth: A systematic review and meta-analysis. Journal of Affective Disorders, 208, 634–645. https://doi.org/10.1016/j.jad.2016.10.009
   PubMed Web of Science ®Google Scholar
• Zhang, W., Ham, J., Li, Q., Deyssenroth, M. A., Lambertini, L., Huang, Y., Tsuchiya, K. J., Chen, J., & Nomura, Y. (2020). Moderate prenatal stress may buffer the impact of Superstorm Sandy on placental genes: Stress in Pregnancy (SIP) Study. PLoS One, 15(1), e0226605. https://doi.org/10.1371/journal.pone.0226605
   PubMed Web of Science ®Google Scholar
• Zimmerman, M., & Mattia, J. I. (2001). A self-report scale to help make psychiatric diagnoses: The Psychiatric Diagnostic Screening Questionnaire. Archives of General Psychiatry, 58(8), 787–794. https://doi.org/10.1001/archpsyc.58.8.787
   PubMed Web of Science ®Google Scholar