Female HPA axis displays heightened sensitivity to pre-pubertal stress

References

• Agorastos, A., Pervanidou, P., Chrousos, G.P., & Baker, D.G. (2019). Developmental trajectories of early life stress and trauma: A narrative review on neurobiological aspects beyond stress system dysregulation. Frontiers in Psychiatry, 10, 1–25. doi:10.3389/fpsyt.2019.00118
   PubMed Web of Science ®Google Scholar
• Aisa, B., Tordera, R., Lasheras, B., Del Rio, J., & Ramirez, M.J. (2008). Effects of maternal separation on hypothalamic-pituitary-adrenal responses, cognition and vulnerability to stress in adult female rats. Neuroscience, 154, 1218–1226. doi:10.1016/j.neuroscience.2008.05.011
   PubMed Web of Science ®Google Scholar
• Albers, H.E. (2015). Species, sex and individual differences in the vasotocin/vasopressin system: Relationship to neurochemical signaling in the social behavior neural network. Frontiers in Neuroendocrinology, 36, 49–71. doi:10.1016/j.yfrne.2014.07.001
   PubMed Web of Science ®Google Scholar
• Albrecht, A., Müller, I., Ardi, Z., Çalışkan, G., Gruber, D., Ivens, S., … Richter-Levin, G. (2017). Neurobiological consequences of juvenile stress: A GABAergic perspective on risk and resilience. Neuroscience & Biobehavioral Reviews, 74, 21–43. doi:10.1016/j.neubiorev.2017.01.005
   PubMed Web of Science ®Google Scholar
• Alteba, S., Korem, N., & Akirav, I. (2016). Cannabinoids reverse the effects of early stress on neurocognitive performance in adulthood. Learning & Memory, 23, 349–358. doi:10.1101/lm.041608.116
   PubMed Web of Science ®Google Scholar
• Bale, T.L., & Dorsa, D.M. (1995). Sex-differences in and effects of estrogen on oxytocin receptor messenger-ribonucleic-acid expression in the ventromedial hypothalmaus. S. Endocrinology, 136, 27–32. doi:10.1210/en.136.1.27
   PubMed Web of Science ®Google Scholar
• Barfield, E.T., & Gourley, S.L. (2018). Prefrontal cortical trkB, glucocorticoids, and their interactions in stress and developmental contexts. Neuroscience & Biobehavioral Reviews, 95, 535–558. doi:10.1016/j.neubiorev.2018.10.015
   PubMed Web of Science ®Google Scholar
• Binder, E.B. (2009). The role of FKBP5, a co-chaperone of the glucocorticoid receptor in the pathogenesis and therapy of affective and anxiety disorders. Psychoneuroendocrinology, 34, S186–S195. doi:10.1016/j.psyneuen.2009.05.021
   PubMed Web of Science ®Google Scholar
• Bourke, C.H., & Neigh, G.N. (2011). Behavioral effects of chronic adolescent stress are sustained and sexually dimorphic. Hormones and Behavior, 60, 112–120. doi:10.1016/j.yhbeh.2011.03.011
   PubMed Web of Science ®Google Scholar
• Brunton, P.J., & Russell, J.A. (2010). Prenatal social stress in the rat programmes neuroendocrine and behavioural responses to stress in the adult offspring: Sex-specific effects. Journal of Neuroendocrinology, 22, 258–271. doi:10.1111/j.1365-2826.2010.01969.x
   PubMed Web of Science ®Google Scholar
• Brydges , et al. in review. Brydges, N.M., Hall, J., Best, C., Rule, L, Watkin, H., Drake, A.J., Lewis, C., Thomas, K.L. & Hall, J. Early life stress impairs social function through AVP-dependent mechanisms.
   Google Scholar
• Brydges, N.M. (2016). Pre-pubertal stress and brain development in rodents. Current Opinion in Behavioral Sciences, 7, 8–14. doi:10.1016/j.cobeha.2015.08.003
   Web of Science ®Google Scholar
• Brydges, N.M., Jin, R.W., Seckl, J., Holmes, M.C., Drake, A.J., & Hall, J. (2014). Juvenile stress enhances anxiety and alters corticosteroid receptor expression in adulthood. Brain and Behavior, 4, 4–13. doi:10.1002/brb3.182
   PubMed Web of Science ®Google Scholar
• Brydges, N.M., Moon, A., Rule, L., Watkin, H., Thomas, K.L., & Hall, J. (2018). Sex specific effects of pre-pubertal stress on hippocampal neurogenesis and behaviour. Translational Psychiatry, 8, 1–12. doi:10.1038/s41398-018-0322-4
   PubMed Web of Science ®Google Scholar
• Bunea, I.M., Szentágotai-Tătar, A., & Miu, A.C. (2017). Early-life adversity and cortisol response to social stress: A meta-analysis. Translational Psychiatry, 7, 1–8. doi:10.1038/s41398-017-0032-3
   Web of Science ®Google Scholar
• Christiansen, D.M., & Hansen, M. (2015). Accounting for sex differences in PTSD: A multi-variable mediation model. European Journal of Psychotraumatology, 6, 26068. doi:10.3402/ejpt.v6.26068
   PubMed Web of Science ®Google Scholar
• de Kloet, E.R., Joels, M., & Holsboer, F. (2005). Stress and the brain: From adaptation to disease. Nature Reviews Neuroscience, 6, 463–475. doi:10.1038/nrn1683
   PubMed Web of Science ®Google Scholar
• Desbonnet, L., Garrett, L., Daly, E., McDermott, K.W., & Dinan, T.G. (2008). Sexually dimorphic effects of maternal separation stress on corticotrophin-releasing factor and vasopressin systems in the adult rat brain. International Journal of Developmental Neuroscience, 26, 259–268. doi:10.1016/j.ijdevneu.2008.02.004
   PubMed Web of Science ®Google Scholar
• Dumais, K.M., Bredewold, R., Mayer, T.E., & Veenema, A.H. (2013). Sex differences in oxytocin receptor binding in forebrain regions: Correlations with social interest in brain region- and sex- specific ways. Hormones and Behavior, 64, 693–701. doi:10.1016/j.yhbeh.2013.08.012
   PubMed Web of Science ®Google Scholar
• Francis, D.D., Young, L.J., Meaney, M.J., & Insel, T.R. (2002). Naturally occurring differences in maternal care are associated with the expression of oxytocin and vasopressin (V1a) receptors: Gender differences. Journal of Neuroendocrinology, 14, 349–353. doi:10.1046/j.0007-1331.2002.00776.x
   PubMed Web of Science ®Google Scholar
• Fuentes, S., Carrasco, J., Armario, A., & Nadal, R. (2014). Behavioral and neuroendocrine consequences of juvenile stress combined with adult immobilization in male rats. Hormones and Behavior, 66, 475–486. doi:10.1016/j.yhbeh.2014.07.003
   PubMed Web of Science ®Google Scholar
• Gjerstad, J.K., Lightman, S.L., & Spiga, F. (2018). Role of glucocorticoid negative feedback in the regulation of HPA axis pulsatility. Stress, 21, 403–416. doi:10.1080/10253890.2018.1470238
   PubMed Web of Science ®Google Scholar
• Gobinath, A.R., Mahmoud, R., & Galea, L.A.M. (2015). Influence of sex and stress exposure across the lifespan on endophenotypes of depression: Focus on behavior glucocorticoids, and hippocampus. Frontiers in Neuroscience, 8, 1–18. doi:10.3389/fnins.2014.00420
   Web of Science ®Google Scholar
• Grigoryan, G., Ardi, Z., Albrecht, A., Richter-Levin, G., & Segal, M. (2015). Juvenile stress alters LTP in ventral hippocampal slices: Involvement of noradrenergic mechanisms. Behavioural Brain Research, 278, 559–562. doi:10.1016/j.bbr.2014.09.047
   PubMed Web of Science ®Google Scholar
• Harms, M.B., Birn, R., Provencal, N., Wiechmann, T., Binder, E.B., Giakas, S.W., … Pollak, S.D. (2017). Early life stress, FK506 binding protein 5 gene (FKBP5) methylation, and inhibition-related prefrontal function: A prospective longitudinal study. Development and Psychopathology, 29, 1895–1903. doi:10.1017/S095457941700147X
   PubMed Web of Science ®Google Scholar
• Heck, A.L., & Handa, R.J. (2019). Sex differences in the hypothalamic-pituitary-adrenal axis' response to stress: An important role for gonadal hormones. Neuropsychopharmacology, 44, 45–58. doi:10.1038/s41386-018-0167-9
   PubMed Web of Science ®Google Scholar
• Heim, C., & Nemeroff, C.B. (2001). The role of childhood trauma in the neurobiology of mood and anxiety disorders: Preclinical and clinical studies. Biological Psychiatry, 49, 1023–1039. doi:10.1016/S0006-3223(01)01157-X
   PubMed Web of Science ®Google Scholar
• Herman, J.P. (1993). Regulation of adrenocorticosteroid receptor messenger-RNA expression in the central nervous system. Cellular and Molecular Neurobiology, 13, 349–372. doi:10.1007/BF00711577
   PubMed Web of Science ®Google Scholar
• Isgor, C., Kabbaj, M., Akil, H., & Watson, S.J. (2004). Delayed effects of chronic variable stress during peripubertal-juvenile period on hippocampal morphology and on cognitive and stress axis functions in rats. Hippocampus, 14, 636–648. doi:10.1002/hipo.10207
   PubMed Web of Science ®Google Scholar
• Jacobson-Pick, S., & Richter-Levin, G. (2010). Differential impact of juvenile stress and corticosterone in juvenility and in adulthood, in male and female rats. Behavioural Brain Research, 214, 268–276. doi:10.1016/j.bbr.2010.05.036
   PubMed Web of Science ®Google Scholar
• Juruena, M.F., Baes, C.V., Menezes, I.C., & Graeff, F.G. (2015). Early life stress in depressive patients: Role of glucocorticoid and mineralocorticoid receptors and of hypothalamic-pituitary-adrenal axis activity. Current Pharmaceutical Design, 21, 1369–1378. doi:10.2174/1381612821666150105125500
   PubMed Web of Science ®Google Scholar
• Juruena, M.F., Cleare, A.J., & Young, A.H. (2018). The role of early life stress in HPA axis and depression. In Understanding depression (pp. 71–80). Amsterdam, Netherland: Springer.
   Google Scholar
• Kapoor, A., Dunn, E., Kostaki, A., Andrews, M.H., & Matthews, S.G. (2006). Fetal programming of hypothalamo-pituitary-adrenal function: Prenatal stress and glucocorticoids. The Journal of Physiology, 572, 31–44. doi:10.1113/jphysiol.2006.105254
   PubMed Web of Science ®Google Scholar
• Kessler, R.C., Berglund, P., Demler, O., Jin, R., Koretz, D., Merikangas, K.R., … Wang, P.S. (2003). The epidemiology of major depressive disorder – Results from the National Comorbidity Survey Replication (NCS-R). JAMA, 289, 3095–3105. doi:10.1001/jama.289.23.3095
   PubMed Web of Science ®Google Scholar
• Kessler, R.C., Chiu, W.T., Demler, O., Merikangas, K.R., & Walters, E.E. (2005). Prevalence, severity, and comorbidity of 12-month DSM-IV disorders in the national comorbidity survey replication (vol 62, pg 617, 2005). Archives of General Psychiatry, 62, 709–709. doi:10.1001/archpsyc.62.6.617
   Web of Science ®Google Scholar
• Kessler, R.C., McGonagle, K.A., Swartz, M., Blazer, D.G., & Nelson, C.B. (1993). Sex and depression in the national comorbidity survey.1. lifetime prevelance, chronicity and recurrence. Journal of Affective Disorders, 29, 85–96. doi:10.1016/0165-0327(93)90026-G
   PubMed Web of Science ®Google Scholar
• Kinlein, S.A., Wilson, C.D., & Karatsoreos, I.N. (2015). Dysregulated hypothalamic-pituitary-adrenal axis function contributes to altered endocrine and neurobehavioral responses to acute stress. Frontiers in Psychiatry, 6, 1–9. doi:10.3389/fpsyt.2015.00031
   PubMed Web of Science ®Google Scholar
• Lee, P.R., Brady, D.L., Shapiro, R.A., Dorsa, D.M., & Koenig, J.I. (2007). Prenatal stress generates deficits in rat social behavior: Reversal by oxytocin. Brain Research, 1156, 152–167. doi:10.1016/j.brainres.2007.04.042
   PubMed Web of Science ®Google Scholar
• Lehmann, J., Russig, H., Feldon, J., & Pryce, C.R. (2002). Effect of a single maternal separation at different pup ages on the corticosterone stress response in adult and aged rats. Pharmacology Biochemistry and Behavior, 73, 141–145. doi:10.1016/S0091-3057(02)00788-8
   PubMed Web of Science ®Google Scholar
• Lesse, A., Rether, K., Groger, N., Braun, K., & Bock, J. (2017). Chronic postnatal stress induces depressive-like behavior in male mice and programs second-hit stress-induced gene expression patterns of OxtR and AvpR1a in adulthood. Molecular Neurobiology, 54, 4813–4819. doi:10.1007/s12035-016-0043-8
   PubMed Web of Science ®Google Scholar
• Levitt, N.S., Lindsay, R.S., Holmes, M.C., & Seckl, J.R. (1996). Dexamethasone in the last week of pregnancy attenuates hippocampal glucocorticoid receptor gene expression and elevates blood pressure in the adult offspring in the rat. Neuroendocrinology, 64, 412–418. doi:10.1159/000127146
   PubMed Web of Science ®Google Scholar
• Liston, C., & Gan, W.B. (2011). Glucocorticoids are critical regulators of dendritic spine development and plasticity in vivo. Proceedings of the National Academy of Sciences of Sciences, 108, 16074–16079. doi:10.1073/pnas.1110444108
   PubMed Web of Science ®Google Scholar
• Llorente, R., Miguel-Blanco, C., Aisa, B., Lachize, S., Borcel, E., Meijer, O.C., … Viveros, M.P. (2011). Long term sex-dependent psychoneuroendocrine effects of maternal deprivation and juvenile unpredictable stress in rats. Journal of Neuroendocrinology, 23, 329–344. doi:10.1111/j.1365-2826.2011.02109.x
   PubMed Web of Science ®Google Scholar
• Lukas, M., Bredewold, R., Neumann, I.D., & Veenema, A.H. (2010). Maternal separation interferes with developmental changes in brain vasopressin and oxytocin receptor binding in male rats. Neuropharmacology, 58, 78–87. doi:10.1016/j.neuropharm.2009.06.020
   PubMed Web of Science ®Google Scholar
• Lupien, S.J., McEwen, B.S., Gunnar, M.R., & Heim, C. (2009). Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nature Reviews Neuroscience, 10, 434–445. doi:10.1038/nrn2639
   PubMed Web of Science ®Google Scholar
• Maccari, S., Piazza, P.V., Kabbaj, M., Barbazanges, A., Simon, H., & Le Moal, M. (1995). Adoption reverses the long-term impairment in glucocorticoid feedback induced by prenatal stress. The Journal of Neuroscience, 15, 110–116. doi:10.1523/JNEUROSCI.15-01-00110.1995
   PubMed Web of Science ®Google Scholar
• Mak, P., Broussard, C., Vacy, K., & Broadbear, J.H. (2012). Modulation of anxiety behavior in the elevated plus maze using peptidic oxytocin and vasopressin receptor ligands in the rat. Journal of Psychopharmacology, 26, 532–542. doi:10.1177/0269881111416687
   PubMed Web of Science ®Google Scholar
• Matosin, N., Halldorsdottir, T., & Binder, E.B. (2018). Understanding the molecular mechanisms underpinning gene by environment interactions in psychiatric disorders: The FKBP5 Model. Biological Psychiatry, 83, 821–830. doi:10.1016/j.biopsych.2018.01.021
   PubMed Web of Science ®Google Scholar
• McLaughlin, K.A., Conron, K.J., Koenen, K.C., & Gilman, S.E. (2010). Childhood adversity, adult stressful life events, and risk of past-year psychiatric disorder: A test of the stress sensitization hypothesis in a population-based sample of adults. Psychological Medicine, 40, 1647–1658. doi:10.1017/S0033291709992121
   PubMed Web of Science ®Google Scholar
• Misiak, B., Stramecki, F., Gawęda, Ł., Prochwicz, K., Sąsiadek, M.M., Moustafa, A.A., & Frydecka, D. (2018). Interactions between variation in candidate genes and environmental factors in the etiology of schizophrenia and bipolar disorder: A systematic review. Molecular Neurobiology, 55, 5075–5100. doi:10.1007/s12035-017-0708-y
   PubMed Web of Science ®Google Scholar
• Murgatroyd, C., Patchev, A.V., Wu, Y., Micale, V., Bockmühl, Y., Fischer, D., … Spengler, D. (2009). Dynamic DNA methylation programs persistent adverse effects of early-life stress. Nature Neuroscience, 12, 1559–U1108. doi:10.1038/nn.2436
   PubMed Web of Science ®Google Scholar
• Murri, M.B., Prestia, D., Mondelli, V., Pariante, C., Patti, S., Olivieri, B., … Amore, M. (2016). The HPA axis in bipolar disorder: Systematic review and meta-analysis. Psychoneuroendocrinology, 63, 327–342. doi:10.1016/j.psyneuen.2015.10.014
   PubMed Web of Science ®Google Scholar
• Nettles, K.W., Pesold, C., & Goldman, M.B. (2000). Influence of the ventral hippocampal formation on plasma vasopressin, hypothalamic-pituitary-adrenal axis, and behavioral responses to novel acoustic stress. Brain Research, 858, 181–190. doi:10.1016/S0006-8993(99)02281-7
   PubMed Web of Science ®Google Scholar
• Neumann, I.D., & Landgraf, R. (2012). Balance of brain oxytocin and vasopressin: Implications for anxiety, depression, and social behaviors. Trends in Neurosciences, 35, 649–659. doi:10.1016/j.tins.2012.08.004
   PubMed Web of Science ®Google Scholar
• Neumann, I.D., & Landgraf, R. (2019). Tracking oxytocin functions in the rodent brain during the last 30 years: From push-pull perfusion to chemogenetic silencing. Journal of Neuroendocrinology, 31, e12695. doi:10.1111/jne.12695
   PubMed Web of Science ®Google Scholar
• Neumann, I.D., & Slattery, D.A. (2016). Oxytocin in general anxiety and social fear: A translational approach. Biological Psychiatry, 79, 213–221. doi:10.1016/j.biopsych.2015.06.004
   PubMed Web of Science ®Google Scholar
• Nicol, K., Pope, M., Romaniuk, L., & Hall, J. (2015). Childhood trauma, midbrain activation and psychotic symptoms in borderline personality disorder. Translational Psychiatry, 5, e559. doi:10.1038/tp.2015.53
   PubMed Web of Science ®Google Scholar
• Nowacka-Chmielewska, M.M., Kasprowska-Liśkiewicz, D., Barski, J.J., Obuchowicz, E., & Małecki, A. (2017). The behavioral and molecular evaluation of effects of social instability stress as a model of stress-related disorders in adult female rats. Stress, 20, 549–561. doi:10.1080/10253890.2017.1376185
   PubMed Web of Science ®Google Scholar
• Oitzl, M.S., Champagne, D.L., van der Veen, R., & de Kloet, E.R. (2010). Brain development under stress: Hypotheses of glucocorticoid actions revisited. Neuroscience & Biobehavioral Reviews, 34, 853–866. doi:10.1016/j.neubiorev.2009.07.006
   PubMed Web of Science ®Google Scholar
• Palmier-Claus, J., Berry, K., Darrell-Berry, H., Emsley, R., Parker, S., Drake, R., & Bucci, S. (2016). Childhood adversity and social functioning in psychosis: Exploring clinical and cognitive mediators. Psychiatry Research, 238, 25–32. doi:10.1016/j.psychres.2016.02.004
   PubMed Web of Science ®Google Scholar
• Patel, P.D., Katz, M., Karssen, A.M., & Lyons, D.M. (2008). Stress-induced changes in corticosteroid receptor expression in primate hippocampus and prefrontal cortex. Psychoneuroendocrinology, 33, 360–367. doi:10.1016/j.psyneuen.2007.12.003
   PubMed Web of Science ®Google Scholar
• Plotsky, P.M., & Meaney, M.J. (1993). Early postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) messenger-RNA, median eminence CRF content and stress-indiced release in adult rats. Molecular Brain Research, 18, 195–200. doi:10.1016/0169-328X(93)90189-V
   PubMedGoogle Scholar
• Remes, O., Brayne, C., van der Linde, R., & Lafortune, L. (2016). A systematic review of reviews on the prevalence of anxiety disorders in adult populations. Brain and Behavior, 6, e00497. doi:10.1002/brb3.497
   PubMed Web of Science ®Google Scholar
• Roman, E., Gustafsson, L., Berg, M., & Nylander, I. (2006). Behavioral profiles and stress-induced corticosteroid secretion in male Wistar rats subjected to short and prolonged periods of maternal separation. Hormones and Behavior, 50, 736–747. doi:10.1016/j.yhbeh.2006.06.016
   PubMed Web of Science ®Google Scholar
• Sandi, C., & Haller, J. (2015). Stress and the social brain: Behavioural effects and neurobiological mechanisms. Nature Reviews Neuroscience, 16, 290–304. doi:10.1038/nrn3918
   PubMed Web of Science ®Google Scholar
• Schmidt, M., Braun, K., Brandwein, C., Rossetti, A.C., Guara Ciurana, S., Riva, M.A., … Gröger, N. (2018). Maternal stress during pregnancy induces depressive-like behavior only in female offspring and correlates to their hippocampal Avp and Oxt receptor expression. Behavioural Brain Research, 353, 1–10. doi:10.1016/j.bbr.2018.06.027
   PubMed Web of Science ®Google Scholar
• Schroeder, A., Notaras, M., Du, X., & Hill, R.A. (2018). On the developmental timing of stress: Delineating sex-specific effects of stress across development on adult behavior. Brain Sciences, 8, 1–29. doi:10.3390/brainsci8070121
   Web of Science ®Google Scholar
• Seale, J.V., Wood, S.A., Atkinson, H.C., Bate, E., Lightman, S.L., Ingram, C.D., … Harbuz, M.S. (2004). Gonadectomy reverses the sexually diergic patterns of circadian and stress-induced hypothalamic-pituitary-adrenal axis activity in male and female rats. Journal of Neuroendocrinology, 16, 516–524. doi:10.1111/j.1365-2826.2004.01195.x
   PubMed Web of Science ®Google Scholar
• Smith, C.J.W., Poehlmann, M.L., Li, S., Ratnaseelan, A.M., Bredewold, R., & Veenema, A.H. (2017). Age and sex differences in oxytocin and vasopressin V1a receptor binding densities in the rat brain: Focus on the social decision-making network. Brain Structure and Function, 222, 981–1006. doi:10.1007/s00429-016-1260-7
   PubMed Web of Science ®Google Scholar
• Song, Z.M., & Albers, H.E. (2018). Cross-talk among oxytocin and arginine-vasopressin receptors: Relevance for basic and clinical studies of the brain and periphery. Frontiers in Neuroendocrinology, 51, 14–24. doi:10.1016/j.yfrne.2017.10.004
   PubMed Web of Science ®Google Scholar
• Spencer, S.J., Buller, K.M., & Day, T.A. (2005). Medial prefrontal cortex control of the Paraventricular hypothalamic nucleus response to psychological stress: Possible role of the bed nucleus of the stria terminalis. The Journal of Comparative Neurology, 481, 363–376. doi:10.1002/cne.20376
   PubMed Web of Science ®Google Scholar
• Szymanska, M., Budziszewska, B., Jaworska-Feil, L., Basta-Kaim, A., Kubera, M., Leskiewicz, M., … Lason, W. (2009). The effect of antidepressant drugs on the HPA axis activity, glucocorticoid receptor level and FKBP51 concentration in prenatally stressed rats. Psychoneuroendocrinology, 34, 822–832. doi:10.1016/j.psyneuen.2008.12.012
   PubMed Web of Science ®Google Scholar
• Tasker, J.G., & Herman, J.P. (2011). Mechanisms of rapid glucocorticoid feedback inhibition of the hypothalamic–pituitary–adrenal axis. Stress, 14, 398–406. doi:10.3109/10253890.2011.586446
   PubMed Web of Science ®Google Scholar
• Teicher, M.H., & Samson, J.A. (2016). Annual research review: Enduring neurobiological effects of childhood abuse and neglect. Journal of Child Psychology and Psychiatry, 57, 241–266. doi:10.1111/jcpp.12507
   PubMed Web of Science ®Google Scholar
• Teicher, M.H., Samson, J.A., Anderson, C.M., & Ohashi, K. (2016). The effects of childhood maltreatment on brain structure, function and connectivity. Nature Reviews Neuroscience, 17, 652. doi:10.1038/nrn.2016.111
   PubMed Web of Science ®Google Scholar
• Tiwari, A., & Gonzalez, A. (2018). Biological alterations affecting risk of adult psychopathology following childhood trauma: A review of sex differences. Clinical Psychology Review, 66, 69–79. doi:10.1016/j.cpr.2018.01.006
   PubMed Web of Science ®Google Scholar
• Tobon, A., Jeffrey, N., & Nemeroff, C.B. (2018). The role of oxytocin in early life adversity and later psychopathology: A review of preclinical and clinical studies. Current Treatment Options in Psychiatry, 5, 401–415. doi:10.1007/s40501-018-0158-9
   Google Scholar
• Touma, C., Gassen, N.C., Herrmann, L., Cheung-Flynn, J., Büll, D.R., Ionescu, I.A., … Rein, T. (2011). FK506 binding protein 5 shapes stress responsiveness: Modulation of neuroendocrine reactivity and coping behavior. Biological Psychiatry, 70, 928–936. doi:10.1016/j.biopsych.2011.07.023
   PubMed Web of Science ®Google Scholar
• Turner, B.B. (1990). Sex difference in glucocorticoid binding in rat pituitary is estrogen dependent. Life Sciences, 46, 1399–1406. doi:10.1016/0024-3205(90)90340-W
   PubMed Web of Science ®Google Scholar
• van Bodegom, M., Homberg, J.R., & Henckens, M. (2017). Modulation of the hypothalamic-pituitary-adrenal axis by early life stress exposure. Frontiers in Cellular Neuroscience, 11, 33. doi:10.3389/fncel.2017.00087
   PubMed Web of Science ®Google Scholar
• van der Doelen, R.H.A., Calabrese, F., Guidotti, G., Geenen, B., Riva, M.A., Kozicz, T., & Homberg, J.R. (2014). Early life stress and serotonin transporter gene variation interact to affect the transcription of the glucocorticoid and mineralocorticoid receptors, and the co-chaperone FKBP5, in the adult rat brain. Frontiers in Behavioral Neuroscience, 8, 1–11. doi:10.3389/fnbeh.2014.00355
   PubMed Web of Science ®Google Scholar
• Veenema, A.H., Bredewold, R., & Neumann, I.D. (2007). Opposite effects of maternal separation on intermale and maternal aggression in C57BL/6 mice: Link to hypothalamic vasopressin and oxytocin immunoreactivity. Psychoneuroendocrinology, 32, 437–450. doi:10.1016/j.psyneuen.2007.02.008
   PubMed Web of Science ®Google Scholar
• Veenema, A.H., & Neumann, I.D. (2009). Maternal separation enhances offensive play-fighting, basal corticosterone and hypothalamic vasopressin mRNA expression in juvenile mate rats. Psychoneuroendocrinology, 34, 463–467. doi:10.1016/j.psyneuen.2008.10.017
   PubMed Web of Science ®Google Scholar
• Wang, Q.Z., Shelton, R.C., & Dwivedi, Y. (2018). Interaction between early-life stress and FKBP5 gene variants in major depressive disorder and post-traumatic stress disorder: A systematic review and meta-analysis. Journal of Affective Disorders, 225, 422–428. doi:10.1016/j.jad.2017.08.066
   PubMed Web of Science ®Google Scholar
• Welberg, L.A.M., Seckl, J.R., & Holmes, M.C. (2001). Prenatal glucocorticoid programming of brain corticosteroid receptors and corticotrophin-releasing hormone: Possible implications for behaviour. Neuroscience, 104, 71–79. doi:10.1016/S0306-4522(01)00065-3
   PubMed Web of Science ®Google Scholar
• Wochnik, G.M., Ruegg, J., Abel, G.A., Schmidt, U., Holsboer, F., & Rein, T. (2005). FK506-binding proteins 51 and 52 differentially regulate dynein interaction and nuclear translocation of the glucocorticoid receptor in mammalian cells. Journal of Biological Chemistry, 280, 4609–4616. doi:10.1074/jbc.M407498200
   PubMed Web of Science ®Google Scholar
• Wulsin, A.C., Wick-Carlson, D., Packard, B.A., Morano, R., & Herman, J.P. (2016). Adolescent chronic stress causes hypothalamo-pituitary-adrenocortical hypo-reponsiveness and depression-like behavior in adult female rats. Psychoneuroendocrinology, 65, 109–117. doi:10.1016/j.psyneuen.2015.12.004
   PubMed Web of Science ®Google Scholar
• Xu, J.J., Wang, R., Liu, Y., Liu, D.X., Jiang, H., & Pan, F. (2017). FKBP5 and specific microRNAs via glucocorticoid receptor in the basolateral amygdala involved in the susceptibility to depressive disorder in early adolescent stressed rats. Journal of Psychiatric Research, 95, 102–113. doi:10.1016/j.jpsychires.2017.08.010
   PubMed Web of Science ®Google Scholar
• Xu, J.J., Wang, R., Liu, Y., Wang, W., Liu, D.X., Jiang, H., & Pan, F. (2019). Short- and long-term alterations of FKBP5-GR and specific microRNAs in the prefrontal cortex and hippocampus of male rats induced by adolescent stress contribute to depression susceptibility. Psychoneuroendocrinology, 101, 204–215. doi:10.1016/j.psyneuen.2018.11.008
   PubMed Web of Science ®Google Scholar
• Zannas, A.S., Wiechmann, T., Gassen, N.C., & Binder, E.B. (2016). Gene-stress-epigenetic regulation of FKBP5: Clinical and translational implications. Neuropsychopharmacology, 41, 261–274. doi:10.1038/npp.2015.235
   PubMed Web of Science ®Google Scholar
• Zhang, L., & Hernandez, V.S. (2013). Synaptic innervation to rat hippocampus by vasopressin-immuno-positive fibres from the hypothalmaic supraoptic and paraventricular nuclei. Neuroscience, 228, 139–162. doi:10.1016/j.neuroscience.2012.10.010
   PubMed Web of Science ®Google Scholar
• Zorn, J.V., Schur, R.R., Boks, M.P., Kahn, R.S., Joels, M., & Vinkers, C.H. (2017). Cortisol stress reactivity across psychiatric disorders: A systematic review and meta-analysis. Psychoneuroendocrinology, 77, 25–36. doi:10.1016/j.psyneuen.2016.11.036
   PubMed Web of Science ®Google Scholar