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Original Article

Long-term programing of psychopathology-like behaviors in male rats by peripubertal stress depends on individual’s glucocorticoid responsiveness to stress

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Pages 433-442 | Received 09 Nov 2017, Accepted 28 Jan 2018, Published online: 07 Feb 2018

References

  • Beach, S.R., Brody, G.H., Gunter, T.D., Packer, H., Wernett, P., & Philibert, R.A. (2010). Child maltreatment moderates the association of MAOA with symptoms of depression and antisocial personality disorder. Journal of Family Psychology, 24, 12–20. doi:10.1037/a0018074
  • Bevilacqua, L., Carli, V., Sarchiapone, M., George, D.K., Goldman, D., Roy, A., & Enoch, M.A. (2012). Interaction between FKBP5 and childhood trauma and risk of aggressive behavior. Archives of General Psychiatry, 69, 62–70. doi:10.1001/archgenpsychiatry.2011.152
  • 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 Suppl. 1, S186–S195. doi:10.1016/j.psyneuen.2009.05.021
  • Binder, E.B., Bradley, R.G., Liu, W., Epstein, M.P., Deveau, T.C., Mercer, K.B., … Ressler, K.J. (2008). Association of FKBP5 polymorphisms and childhood abuse with risk of posttraumatic stress disorder symptoms in adults. JAMA, 299, 1291–1305. doi:10.1001/jama.299.11.1291
  • Bryushkova, L., Zai, C., Chen, S., Pappa, I., Mileva, V., Tiemeier, H., … Beitchman, J.H. (2016). FKBP5 interacts with maltreatment in children with extreme, pervasive, and persistent aggression. Psychiatry Research, 242, 277–280. doi:10.1016/j.psychres.2015.09.052
  • Casey, B.J., Jones, R.M., & Hare, T.A. (2008). The adolescent brain. Annals of the New York Academy of Sciences, 1124, 111–126. doi:10.1196/annals.1440.010
  • Caspi, A., & Moffitt, T.E. (2006). Gene-environment interactions in psychiatry: Joining forces with neuroscience. Nature Reviews Neuroscience, 7, 583–590. doi:10.1038/nrn1925
  • Clinton, S.M., Watson, S.J., & Akil, H. (2014). High novelty-seeking rats are resilient to negative physiological effects of the early life stress. Stress, 17, 97–107. doi:10.3109/10253890.2013.850670
  • Cohen, H., Zohar, J., Gidron, Y., Matar, M.A., Belkind, D., Loewenthal, U., … Kaplan, Z. (2006). Blunted HPA axis response to stress influences susceptibility to posttraumatic stress response in rats. Biological Psychiatry, 59, 1208–1218. doi:10.1016/j.biopsych.2005.12.003
  • Contractor, A.A., Elhai, J.D., Fine, T.H., Tamburrino, M.B., Cohen, G., Shirley, E., … Calabrese, J.R. (2015). Latent profile analyses of posttraumatic stress disorder, depression and generalized anxiety disorder symptoms in trauma-exposed soldiers. Journal of Psychiatric Research, 68, 19–26. doi:10.1016/j.jpsychires.2015.05.014
  • de Kloet, E.R. (2014). From receptor balance to rational glucocorticoid therapy. Endocrinology, 155, 2754–2769. doi:10.1210/en.2014-1048
  • Durham, T.A., Byllesby, B.M., Armour, C., Forbes, D., & Elhai, J.D. (2016). Relations between anger and DSM-5 posttraumatic stress disorder symptoms. Psychiatry Research, 244, 403–409. doi:10.1016/j.psychres.2016.08.004
  • Federenko, I.S., Nagamine, M., Hellhammer, D.H., Wadhwa, P.D., & Wust, S. (2004). The heritability of hypothalamus pituitary adrenal axis responses to psychosocial stress is context dependent. Journal of Clinical Endocrinology & Metabolism, 89, 6244–6250. doi:10.1210/jc.2004-0981
  • Ferenczi, E.A., Zalocusky, K.A., Liston, C., Grosenick, L., Warden, M.R., Amatya, D., … Deisseroth, K. (2016). Prefrontal cortical regulation of brainwide circuit dynamics and reward-related behavior. Science, 351, aac9698. doi:10.1126/science.aac9698
  • Gerra, G., Zaimovic, A., Mascetti, G.G., Gardini, S., Zambelli, U., Timpano, M., … Brambilla, F. (2001). Neuroendocrine responses to experimentally-induced psychological stress in healthy humans. Psychoneuro-endocrinology, 26, 91–107. doi:10.1016/S0306-4530(00)00046-9
  • Haller, J. (2013). The neurobiology of abnormal manifestations of aggression – A review of hypothalamic mechanisms in cats, rodents, and humans. Brain Research Bulletin, 93, 97–109. doi:10.1016/j.brainresbull.2012.10.003
  • 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, 102–111. doi:10.1016/j.expneurol.2011.10.032
  • Joels, M., Pasricha, N., & Karst, H. (2013). The interplay between rapid and slow corticosteroid actions in brain. European Journal of Pharmacology, 719, 44–52. doi:10.1016/j.ejphar.2013.07.01
  • Klengel, T., Mehta, D., Anacker, C., Rex-Haffner, M., Pruessner, J.C., Pariante, C.M., … Binder, E.B. (2013). Allele-specific FKBP5 DNA demethylation mediates gene-childhood trauma interactions. Nature Neuroscience, 16, 33–41. doi:10.1038/nn.3275
  • Koch, S.B., van Zuiden, M., Nawijn, L., Frijling, J.L., Veltman, D.J., & Olff, M. (2016). Aberrant resting-state brain activity in posttraumatic stress disorder: A meta-analysis and systematic review. Depress Anxiety, 33, 592–605. doi:10.1002/da.22478
  • Koolhaas, J.M., Coppens, C.M., de Boer, S.F., Buwalda, B., Meerlo, P., & Timmermans, P.J. (2013). The resident–intruder paradigm: A standardized test for aggression, violence and social stress. Journal of Visualized Experiments, e4367. doi:10.3791/4367
  • Marquez, C., Poirier, G.L., Cordero, M.I., Larsen, M.H., Groner, A., Marquis, J., … Sandi, C. (2013). Peripuberty stress leads to abnormal aggression, altered amygdala and orbitofrontal reactivity and increased prefrontal MAOA gene expression. Translational Psychiatry, 3, e216. doi:10.1038/tp.2012.144
  • McBurnett, K., Lahey, B.B., Rathouz, P.J., & Loeber, R. (2000). Low salivary cortisol and persistent aggression in boys referred for disruptive behavior. Archives of General Psychiatry, 57, 38–43. doi:10.1001/archpsyc.57.1.38
  • McEwen, B.S. (1998). Stress, adaptation, and disease. Allostasis and allostatic load. Annals of the New York Academy of Sciences, 840, 33–44. doi:10.1111/j.1749-6632.1998.tb09546.x
  • McEwen, B.S. (2007). Physiology and neurobiology of stress and adaptation: Central role of the brain. Physiological Reviews, 87, 873–904. doi:10.1152/physrev.00041.2006
  • McIlwrick, S., Rechenberg, A., Matthes, M., Burgstaller, J., Schwarzbauer, T., Chen, A., & Touma, C. (2016). Genetic predisposition for high stress reactivity amplifies effects of early-life adversity. Psychoneuroendocrino-logy, 70, 85–97. doi:10.1016/j.psyneuen.2016.04.023
  • New, A.S., Hazlett, E.A., Newmark, R.E., Zhang, J., Triebwasser, J., Meyerson, D., … Buchsbaum, M.S. (2009). Laboratory induced aggression: A positron emission tomography study of aggressive individuals with borderline personality disorder. Biological Psychiatry, 66, 1107–1114. doi:10.1016/j.biopsych.2009.07.015
  • Nugent, N.R., Tyrka, A.R., Carpenter, L.L., & Price, L.H. (2011). Gene-environment interactions: Early life stress and risk for depressive and anxiety disorders. Psychopharmacology (Berl), 214, 175–196. doi:10.1007/s00213-010-2151-x
  • O'Leary, M.M., Loney, B.R., & Eckel, L.A. (2007). Gender differences in the association between psychopathic personality traits and cortisol response to induced stress. Psychoneuroendocrinology, 32, 183–191. doi:10.1016/j.psyneuen.2006.12.004
  • Rabasa, C., Gagliano, H., Pastor-Ciurana, J., Fuentes, S., Belda, X., Nadal, R., & Armario, A. (2015). Adaptation of the hypothalamus–pituitary–adrenal axis to daily repeated stress does not follow the rules of habituation: A new perspective. Neuroscience & Biobehavioral Reviews, 56, 35–49. doi:10.1016/j.neubiorev.2015.06.013
  • Raine, A. (1996). Autonomic nervous system factors underlying disinhibited, antisocial, and violent behavior. Biosocial perspectives and treatment implications. Annals of the New York Academy of Sciences, 794, 46–59. doi:10.1111/j.1749-6632.1996.tb32508.x
  • Rana, S., Nam, H., Glover, M.E., Akil, H., Watson, S.J., Clinton, S.M., & Kerman, I.A. (2016). Protective effects of chronic mild stress during adolescence in the low-novelty responder rat. Stress, 19, 133–138. doi:10.3109/10253890.2015.1108304
  • Ritov, G., Boltyansky, B., & Richter-Levin, G. (2016). A novel approach to PTSD modeling in rats reveals alternating patterns of limbic activity in different types of stress reaction. Molecular Psychiatry, 21, 630–641. doi:10.1038/mp.2015.169
  • Spear, L.P. (2000). The adolescent brain and age-related behavioral manifestations. Neuroscience & Biobehavioral Reviews, 24, 417–463. doi:10.1016/S0149-7634(00)00014-2
  • Stedenfeld, K.A., Clinton, S.M., Kerman, I.A., Akil, H., Watson, S.J., & Sved, A.F. (2011). Novelty-seeking behavior predicts vulnerability in a rodent model of depression. Physiology & Behavior, 103, 210–216. doi:10.1016/j.physbeh.2011.02.001
  • Tzanoulinou, S., Garcia-Mompo, C., Castillo-Gomez, E., Veenit, V., Nacher, J., & Sandi, C. (2014). Long-term behavioral programming induced by peripuberty stress in rats is accompanied by GABAergic-related alterations in the Amygdala. PLoS One, 9, e94666. doi:10.1371/journal.pone.0094666
  • Tzanoulinou, S., Garcia-Mompo, C., Riccio, O., Grosse, J., Zanoletti, O., Dedousis, P., … Sandi, C. (2016). Neuroligin-2 expression in the prefrontal cortex is involved in attention deficits induced by peripubertal stress. Neuropsychopharmacology, 41, 751–761. doi:10.1038/npp.2015.200
  • Tzanoulinou, S., Riccio, O., de Boer, M.W., & Sandi, C. (2014). Peripubertal stress-induced behavioral changes are associated with altered expression of genes involved in excitation and inhibition in the amygdala. Translational Psychiatry, 4, e410. doi:10.1038/tp.2014.54
  • Walker, S.E., Papilloud, A., Huzard, D., & Sandi, C. (2016). The link between aberrant hypothalamic-pituitary-adrenal axis activity during development and the emergence of aggression-animal studies. Neuroscience & Biobehavioral Reviews. doi:10.1016/j.neubiorev.2016.10.008
  • Walker, S.E., Zanoletti, O., Guillot de Suduiraut, I., & Sandi, C. (2017). Constitutive differences in glucocorticoid responsiveness to stress are related to variation in aggression and anxiety-related behaviors. Psychoneuroendocrinology, 84, 1–10. doi:10.1016/j.psyneuen.2017.06.011
  • Weder, N., Yang, B.Z., Douglas-Palumberi, H., Massey, J., Krystal, J.H., Gelernter, J., & Kaufman, J. (2009). MAOA genotype, maltreatment, and aggressive behavior: The changing impact of genotype at varying levels of trauma. Biological Psychiatry, 65, 417–424. doi:10.1016/j.biopsych.2008.09.013
  • Widom, C.S., & Maxfield, M.G. (1996). A prospective examination of risk for violence among abused and neglected children. Annals of the New York Academy of Sciences, 794, 224–237. doi:10.1111/j.1749-6632.1996.tb32523.x
  • Yehuda, R., Boisoneau, D., Lowy, M.T., & Giller, E.L. Jr. (1995). Dose–response changes in plasma cortisol and lymphocyte glucocorticoid receptors following dexamethasone administration in combat veterans with and without posttraumatic stress disorder. Archives of General Psychiatry, 52, 583–593. doi:10.1001/archpsyc.1995.03950190065010
  • Yizhar, O., Fenno, L.E., Prigge, M., Schneider, F., Davidson, T.J., O'Shea, D.J., … Deisseroth, K. (2011). Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature, 477, 171–178. doi:10.1038/nature10360

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