Stress and the brain: from adaptation to disease (original) (raw)

• Selye, H. Syndrome produced by diverse nocuous agents. Nature 138, 32 (1936).
  Google Scholar
• Levine, S. & Ursin, H. in Stress Neurobiology and Neuroendocrinology (eds Brown, M. R. & Koob, G. F.) 3–21 (Rivier Marcel Dekker, Inc., New York, 1991).
  Google Scholar
• Chrousos, G. P. & Gold, P. W. The concepts of stress and stress system disorders. Overview of physical and behavioral homeostasis. JAMA 267, 1244–1252 (1992).
  CAS PubMed Google Scholar
• De Kloet, E. R., Vreugdenhil, E., Oitzl, M. S. & Joëls, M. Brain corticosteroid receptor balance in health and disease. Endocr. Rev. 19, 269–301 (1998).
  CAS PubMed Google Scholar
• McEwen, B. in Encyclopedia of Stress Vol. 3 (ed. Fink, G.) 508–509 (Academic, San Diego, USA, 2000).
  Google Scholar
• Sapolsky, R. M., Romero, L. M. & Munck, A. U. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr. Rev. 21, 55–89 (2000).
  CAS PubMed Google Scholar
• Tausk, M. Das Hormon: Hat die Nebennierrinde tatsächlich eine Verteidigungsfunktion? Vol. 3 (Organon International BV, Oss, The Netherlands, 1952).
  Google Scholar
• McEwen, B. S. Mood disorders and allostatic load. Biol. Psychiatry 54, 200–207 (2003).
  PubMed Google Scholar
• Holsboer, F. The corticosteroid receptor hypothesis of depression. Neuropsychopharmacology 23, 477–501 (2000).
  CAS PubMed Google Scholar
• Van Praag, H. M., de Kloet, E. R. & van Os, J. Stress, the Brain and Depression (Cambridge Univ. Press, 2004).
  Google Scholar
• Yehuda, R. Post-traumatic stress disorder. N. Engl. J. Med. 346, 108–114 (2002).
  CAS PubMed Google Scholar
• Reul, J. M. & de Kloet, E. R. Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation. Endocrinology 117, 2505–2511 (1985). The first account of two distinct nuclear receptor systems that bind naturally occurring glucocorticoids with a tenfold difference in affinity.
  CAS PubMed Google Scholar
• Arriza, J. L., Simerly, R. B., Swanson, L. W. & Evans, R. M. The neuronal mineralocorticoid receptor as a mediator of glucocorticoid response. Neuron 1, 887–900 (1988).
  CAS PubMed Google Scholar
• Young, E. A., Abelson, J. & Lightman, S. L. Cortisol pulsatility and its role in stress regulation and health. Front. Neuroendocrinol. 25, 69–76 (2004).
  CAS PubMed Google Scholar
• Kitchener, P., Di Blasi, F., Borrelli, E. & Piazza, P. V. Differences between brain structures in nuclear translocation and DNA binding of the glucocorticoid receptor during stress and the circadian cycle. Eur. J. Neurosci. 19, 1837–1846 (2004).
  PubMed Google Scholar
• Miklos, I. H. & Kovacs, K. J. GABAergic innervation of corticotropin-releasing hormone (CRH)-secreting parvocellular neurons and its plasticity as demonstrated by quantitative immunoelectron microscopy. Neuroscience 113, 581–592 (2002).
  CAS PubMed Google Scholar
• Herman, J. P. et al. Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo–pituitary–adrenocortical responsiveness. Front. Neuroendocrinol. 24, 151–180 (2003).
  CAS PubMed Google Scholar
• Patel, P. D. et al. Glucocorticoid and mineralocorticoid receptor mRNA expression in squirrel monkey brain. J. Psychiatr. Res. 34, 383–392 (2000).
  CAS PubMed Google Scholar
• Trapp, T., Rupprecht, R., Castren, M., Reul, J. M. & Holsboer, F. Heterodimerization between mineralocorticoid and glucocorticoid receptor: a new principle of glucocorticoid action in the CNS. Neuron 13, 1457–1462 (1994).
  CAS PubMed Google Scholar
• Nishi, M., Ogawa, H., Ito, T., Matsuda, K. I. & Kawata, M. Dynamic changes in subcellular localization of mineralocorticoid receptor in living cells: in comparison with glucocorticoid receptor using dual-color labeling with green fluorescent protein spectral variants. Mol. Endocrinol. 15, 1077–1092 (2001).
  CAS PubMed Google Scholar
• Gesing, A. et al. Psychological stress increases hippocampal mineralocorticoid receptor levels: involvement of corticotropin-releasing hormone. J. Neurosci. 21, 4822–4829 (2001).
  CAS PubMed PubMed Central Google Scholar
• Datson, N. A., van der Perk, J., de Kloet, E. R. & Vreugdenhil, E. Identification of corticosteroid-responsive genes in rat hippocampus using serial analysis of gene expression. Eur. J. Neurosci. 14, 675–689 (2001). This paper describes a comprehensive database of MR- and GR-responsive gene patterns in the hippocampus.
  CAS PubMed Google Scholar
• Sabban, E. L. & Kvetnansky, R. Stress-triggered activation of gene expression in catecholaminergic systems: dynamics of transcriptional events. Trends Neurosci. 24, 91–98 (2001).
  CAS PubMed Google Scholar
• Schaaf, M. J., Hoetelmans, R. W., de Kloet, E. R. & Vreugdenhil, E. Corticosterone regulates expression of BDNF and trkB but not NT-3 and trkC mRNA in the rat hippocampus. J. Neurosci. Res. 48, 334–341 (1997).
  CAS PubMed Google Scholar
• Hansson, A. C. et al. Gluco- and mineralocorticoid receptor-mediated regulation of neurotrophic factor gene expression in the dorsal hippocampus and the neocortex of the rat. Eur. J. Neurosci. 12, 2918–2934 (2000).
  CAS PubMed Google Scholar
• Sandi, C. Stress, cognitive impairment and cell adhesion molecules. Nature Rev. Neurosci. 5, 917–930 (2004).
  CAS Google Scholar
• Kole, M. H., Costoli, T., Koolhaas, J. M. & Fuchs, E. Bidirectional shift in the cornu ammonis 3 pyramidal dendritic organization following brief stress. Neuroscience 125, 337–347 (2004).
  CAS PubMed Google Scholar
• Wossink, J., Karst, H., Mayboroda, O. & Joëls, M. Morphological and functional properties of rat dentate granule cells after adrenalectomy. Neuroscience 108, 263–272 (2001).
  CAS PubMed Google Scholar
• Garcia, A., Steiner, B., Kronenberg, G., Bick-Sander, A. & Kempermann, G. Age-dependent expression of glucocorticoid- and mineralocorticoid receptors on neural precursor cell populations in the adult murine hippocampus. Aging Cell 3, 363–371 (2004).
  CAS PubMed Google Scholar
• Woolley, C. S., Gould, E., Sakai, R. R., Spencer, R. L. & McEwen, B. S. Effects of aldosterone or RU28362 treatment on adrenalectomy-induced cell death in the dentate gyrus of the adult rat. Brain Res. 554, 312–315 (1991).
  CAS PubMed Google Scholar
• Hu, Z., Yuri, K., Ozawa, H., Lu, H. & Kawata, M. The in vivo time course for elimination of adrenalectomy-induced apoptotic profiles from the granule cell layer of the rat hippocampus. J. Neurosci. 17, 3981–3989 (1997).
  CAS PubMed PubMed Central Google Scholar
• Nair, S. M. et al. Gene expression profiles associated with survival of individual rat dentate cells after endogenous corticosteroid deprivation. Eur. J. Neurosci. 20, 3233–3243 (2004).
  CAS PubMed Google Scholar
• Almeida, O. F. et al. Subtle shifts in the ratio between pro- and antiapoptotic molecules after activation of corticosteroid receptors decide neuronal fate. FASEB J. 14, 779–790 (2000).
  CAS PubMed Google Scholar
• Tanapat, P., Hastings, N. B., Rydel, T. A., Galea, L. A. & Gould, E. Exposure to fox odor inhibits cell proliferation in the hippocampus of adult rats via an adrenal hormone-dependent mechanism. J. Comp. Neurol. 437, 496–504 (2001). This report describes how stressful experiences rapidly diminish cell proliferation by increasing adrenal hormone levels, which results in a transient decrease in the number of adult-generated immature granule neurons.
  CAS PubMed Google Scholar
• Crochemore, C., Michaelidis, T. M., Fischer, D., Loeffler, J. P. & Almeida, O. F. Enhancement of p53 activity and inhibition of neural cell proliferation by glucocorticoid receptor activation. FASEB J. 16, 761–770 (2002).
  CAS PubMed Google Scholar
• Heine, V. M., Maslam, S., Zareno, J., Joëls, M. & Lucassen, P. J. Suppressed proliferation and apoptotic changes in the rat dentate gyrus after acute and chronic stress are reversible. Eur. J. Neurosci. 19, 131–144 (2004).
  PubMed Google Scholar
• Joëls, M. Steroid hormones and excitability in the mammalian brain. Front. Neuroendocrinol. 18, 2–48 (1997).
  PubMed Google Scholar
• Joëls, M. & de Kloet, E. R. Effects of glucocorticoids and norepinephrine on the excitability in the hippocampus. Science 245, 1502–1505 (1989). This paper shows that glucocorticoids can reduce transmitter-evoked excitability in the hippocampus, presumably through receptor-mediated genomic actions.
  PubMed Google Scholar
• Joëls, M., Hesen, W. & de Kloet, E. R. Mineralocorticoid hormones suppress serotonin-induced hyperpolarization of rat hippocampal CA1 neurons. J. Neurosci. 11, 2288–2294 (1991).
  PubMed PubMed Central Google Scholar
• Beck, S. G., Choi, K. C., List, T. J., Okuhara, D. Y. & Birnsteil, S. Corticosterone alters 5-HT1A receptor-mediated hyperpolarization in area CA1 hippocampal pyramidal neurons. Neuropsychopharmacology 14, 27–33 (1996).
  CAS PubMed Google Scholar
• Kerr, D. S., Campbell, L. W., Thibault, O. & Landfield, P. W. Hippocampal glucocorticoid receptor activation enhances voltage-dependent Ca2+ conductances: relevance to brain aging. Proc. Natl Acad. Sci. USA 89, 8527–8531 (1992).
  CAS PubMed PubMed Central Google Scholar
• Karst, H. et al. Corticosteroid actions in hippocampus require DNA binding of glucocorticoid receptor homodimers. Nature Neurosci. 3, 977–978 (2000).
  CAS PubMed Google Scholar
• Venero, C. & Borrell, J. Rapid glucocorticoid effects on excitatory amino acid levels in the hippocampus: a microdialysis study in freely moving rats. Eur. J. Neurosci. 11, 2465–2473 (1999).
  CAS PubMed Google Scholar
• Di, S., Malcher-Lopes, R., Halmos, K. C. & Tasker, J. G. Nongenomic glucocorticoid inhibition via endocannabinoid release in the hypothalamus: a fast feedback mechanism. J. Neurosci. 23, 4850–4857 (2003). This study presents evidence for rapid glucocorticoid feedback inhibition of hypothalamic hormone secretion by endocannabinoid release in the PVN.
  CAS PubMed PubMed Central Google Scholar
• Dong, Y. et al. Cocaine-induced potentiation of synaptic strength in dopamine neurons: Behavioral correlates in GluRA (−/−) mice. Proc. Natl Acad. Sci. USA 101, 14282–14287 (2004).
  CAS PubMed PubMed Central Google Scholar
• Diamond, D. M., Bennett, M. C., Fleshner, M. & Rose, G. M. Inverted-U relationship between the level of peripheral corticosterone and the magnitude of hippocampal primed burst potentiation. Hippocampus 2, 421–430 (1992). This research shows that corticosterone exerts a concentration-dependent biphasic influence on the expression of hippocampal plasticity.
  CAS PubMed Google Scholar
• Martin, S. J., Grimwood, P. D. & Morris, R. G. Synaptic plasticity and memory: an evaluation of the hypothesis. Annu. Rev. Neurosci. 23, 649–711 (2000).
  CAS PubMed Google Scholar
• Kim, J. J. & Diamond, D. The stressed hippocampus, synaptic plasticity and lost memories. Nature Rev. Neurosci. 3, 453–462 (2002).
  CAS Google Scholar
• Pavlides, C., Ogawa, S., Kimura, A. & McEwen, B. S. Role of adrenal steroid mineralocorticoid and glucocorticoid receptors in long-term potentiation in the CA1 field of hippocampal slices. Brain Res. 738, 229–235 (1996).
  CAS PubMed Google Scholar
• Xu, L., Anwyl, R. & Rowan, M. J. Spatial exploration induces a persistent reversal of long-term potentiation in rat hippocampus. Nature 394, 891–894 (1998).
  CAS PubMed Google Scholar
• Kim, J. J., Foy, M. R. & Thompson. Behavioral stress modifies hippocampal plasticity through _N_-methyl-D-aspartate receptor activation. Proc. Natl Acad. Sci. USA 93, 4750–4753 (1996).
  CAS PubMed PubMed Central Google Scholar
• Blank, T., Nijholt, I., Eckart, K. & Spiess, J. Priming of long-term potentiation in mouse hippocampus by corticotropin-releasing factor and acute stress: implications for hippocampus-dependent learning. J. Neurosci. 22, 3788–3794 (2002).
  CAS PubMed PubMed Central Google Scholar
• Rupprecht, R. et al. Progesterone receptor-mediated effects of neuroactive steroids. Neuron 11, 523–530 (1993).
  CAS PubMed Google Scholar
• Korz, V. & Frey, J. U. Stress-related modulation of hippocampal long-term potentiation in rats: involvement of adrenal steroid receptors. J. Neurosci. 23, 7281–7287 (2003).
  CAS PubMed PubMed Central Google Scholar
• Diamond, D. M., Park, C. R. & Woodson, J. C. Stress generates emotional memories and retrograde amnesia by inducing an endogenous form of hippocampal LTP. Hippocampus 14, 281–291 (2004).
  PubMed Google Scholar
• Oitzl, M. S. & de Kloet, E. R. Selective corticosteroid antagonists modulate specific aspects of spatial orientation learning. Behav. Neurosci. 106, 62–71 (1992). This paper shows that corticosteroids affect behavioural strategies and the storage of spatial information through MR and GR in a differential and coordinated manner.
  CAS PubMed Google Scholar
• Oitzl, M. S., Reichardt, H. M., Joëls, M. & de Kloet, E. R. Point mutation in the mouse glucocorticoid receptor preventing DNA binding impairs spatial memory. Proc. Natl Acad. Sci. USA 98, 12790–12795 (2001).
  CAS PubMed PubMed Central Google Scholar
• Sandi, C., Loscertales, M. & Guaza, C. Experience-dependent facilitating effect of corticosterone on spatial memory formation in the water maze. Eur. J. Neurosci. 9, 637–642 (1997).
  CAS PubMed Google Scholar
• Quirarte, G. L., Roozendaal, B. & McGaugh, J. L. Glucocorticoid enhancement of memory storage involves noradrenergic activation in the basolateral amygdala. Proc. Natl Acad. Sci. USA 94, 14048–14053 (1997). This study shows that β-adrenergic activation seems to be an essential step in mediating glucocorticoid effects on memory storage and that the BLA is a locus of interaction for these two systems.
  CAS PubMed PubMed Central Google Scholar
• De Quervain, D. J., Roozendaal, B. & McGaugh, J. L. Stress and glucocorticoids impair retrieval of long-term spatial memory. Nature 394, 787–790 (1998).
  CAS PubMed Google Scholar
• Myers, K. M. & Davis, M. Behavioral and neural analysis of extinction. Neuron 36, 567–584 (2002).
  CAS PubMed Google Scholar
• Cordero, M. I., Merino, J. J. & Sandi, C. Correlational relationship between shock intensity and corticosterone secretion on the establishment and subsequent expression of contextual fear conditioning. Behav. Neurosci. 112, 885–891 (1998).
  CAS PubMed Google Scholar
• Karst, H. et al. Glucocorticoids alter calcium conductances and calcium channel subunit expression in basolateral amygdala neurons. Eur. J. Neurosci. 16, 1083–1089 (2002).
  PubMed Google Scholar
• Vouimba, R. M., Yaniv, D., Diamond, D. & Richter-Levin, G. Effects of inescapable stress on LTP in the amygdala versus the dentate gyrus of freely behaving rats. Eur. J. Neurosci. 19, 1887–1894 (2004).
  PubMed Google Scholar
• Kim, J. J., Lee, H. J., Han, J. S. & Packard, M. G. Amygdala is critical for stress-induced modulation of hippocampal long-term potentiation and learning. J. Neurosci. 21, 5222–5228 (2001).
  CAS PubMed PubMed Central Google Scholar
• Akirav, I. & Richter-Levin, G. Mechanisms of amygdala modulation of hippocampal plasticity. J. Neurosci. 22, 912–921 (2002).
  Google Scholar
• Maroun, M. & Richter-Levin, G. Exposure to acute stress blocks the induction of long-term potentiation of the amygdala-prefrontal cortex pathway in vivo. J. Neurosci. 23, 4406–4409 (2003).
  CAS PubMed PubMed Central Google Scholar
• Amat, J. et al. Medial prefrontal cortex determines how stressor controllability affects behavior and dorsal raphe nucleus. Nature Neurosci. 8, 365–371 (2005).
  CAS PubMed Google Scholar
• Conrad, C. D., LeDoux, J. E., Magarinos, A. M. & McEwen, B. S. Repeated restraint stress facilitates fear conditioning independently of causing hippocampal CA3 dendritic atrophy. Behav. Neurosci. 113, 902–913 (1999).
  CAS PubMed Google Scholar
• Bowman, R. E., Beck, K. D. & Luine, V. N. Chronic stress effects on memory: sex differences in performance and monoaminergic activity. Horm. Behav. 43, 48–59 (2003).
  CAS PubMed Google Scholar
• Woolley, C. S., Gould, E. & McEwen, B. S. Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons. Brain Res. 531, 225–231 (1990). In this study, changes in dendritic morphology were observed that might have been indicative of neurons in the early stages of degeneration
  CAS PubMed Google Scholar
• Magarinos, A. M., McEwen, B. S., Flugge, G. & Fuchs, E. Chronic psychosocial stress causes apical dendritic atrophy of hippocampal CA3 pyramidal neurons in subordinate tree shrews. J. Neurosci. 16, 3534–3540 (1996). These results indicate that a naturalistic psychosocial stressor induces specific structural changes in the hippocampal neurons of subordinate male tree shrews.
  CAS PubMed PubMed Central Google Scholar
• Sandi, C. et al. Rapid reversal of stress induced loss of synapses in CA3 of rat hippocampus following water maze training. Eur. J. Neurosci. 17, 2447–2456 (2003).
  PubMed Google Scholar
• Wellman, C. L. Dendritic reorganization in pyramidal neurons in medial prefrontal cortex after chronic corticosterone administration. J. Neurobiol. 49, 245–253 (2001).
  CAS PubMed Google Scholar
• Vyas, A., Mitra, R., Shankaranarayana Rao, B. S. & Chattarji, S. Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. J. Neurosci. 22, 6810–6818 (2002). The data presented here indicate that chronic stress can cause contrasting patterns of dendritic remodelling in neurons of the amygdala and hippocampus.
  CAS PubMed PubMed Central Google Scholar
• Magarinos, A. M., Verdugo, J. M. & McEwen, B. S. Chronic stress alters synaptic terminal structure in hippocampus. Proc. Natl Acad. Sci. USA 94, 14002–14008 (1997).
  CAS PubMed PubMed Central Google Scholar
• Kole, M. H., Swan, L. & Fuchs, E. The antidepressant tianeptine persistently modulates glutamate receptor currents of the hippocampal CA3 commissural associational synapse in chronically stressed rats. Eur. J. Neurosci. 16, 807–816 (2002).
  PubMed Google Scholar
• Karst, H. & Joëls, M. Effect of chronic stress on synaptic currents in rat hippocampal dentate gyrus neurons. J. Neurophysiol. 89, 625–633 (2003).
  PubMed Google Scholar
• Alfarez, D. N., Joëls, M. & Krugers, H. J. Chronic unpredictable stress impairs long-term potentiation in rat hippocampal CA1 area and dentate gyrus in vitro. Eur. J. Neurosci. 17, 1928–1934 (2003).
  PubMed Google Scholar
• Pham, K., Nacher, J., Hof, P. R. & McEwen, B. S. Repeated restraint stress suppresses neurogenesis and induces biphasic PSA-NCAM expression in the adult rat dentate gyrus. Eur. J. Neurosci. 17, 879–886 (2003).
  PubMed Google Scholar
• Czeh, B. et al. Stress-induced changes in cerebral metabolites, hippocampal volume, and cell proliferation are prevented by antidepressant treatment with tianeptine. Proc. Natl Acad. Sci. USA 98, 12796–12801 (2001).
  CAS PubMed PubMed Central Google Scholar
• Wong, E. Y. & Herbert, J. The corticoid environment: a determining factor for neural progenitors' survival in the adult hippocampus. Eur. J. Neurosci. 20, 2491–2498 (2004).
  PubMed PubMed Central Google Scholar
• Malberg, J. E., Eisch, A. J., Nestler, E. J. & Duman, R. S. Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J. Neurosci. 20, 9104–9110 (2000).
  CAS PubMed PubMed Central Google Scholar
• Alonso, R. et al. Blockade of CRF(1) or V(1b) receptors reverses stress-induced suppression of neurogenesis in a mouse model of depression. Mol. Psychiatry 9, 278–286 (2004).
  CAS PubMed Google Scholar
• Santarelli, L. et al. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301, 805–809 (2003). The authors show that the behavioural effects of chronic antidepressant use might be mediated by the stimulation of neurogenesis in the hippocampus.
  CAS PubMed Google Scholar
• Saravia, F. E. et al. Increased astrocyte reactivity in the hippocampus of murine models of type 1 diabetes: the nonobese diabetic (NOD) and streptozotocin-treated mice. Brain Res. 957, 345–353 (2002).
  CAS PubMed Google Scholar
• De Kloet, E. R. Brain corticosteroid balance and homeostatic control. Front. Neuroendocrinol. 12, 95–164 (1991).
  Google Scholar
• Herman, J. P., Watson, S. J. & Spencer, R. L. Defense of adrenocorticosteroid receptor expression in rat hippocampus: effects of stress and strain. Endocrinology 140, 3981–3991 (1999).
  CAS PubMed Google Scholar
• Obradovic, D. et al. DAXX, FLASH, and FAF-1 modulate mineralocorticoid and glucocorticoid receptor mediated transcription in hippocampal cells: toward a basis for the opposite actions elicited by two nuclear receptors? Mol. Pharmacol. 65, 761–769 (2004).
  CAS PubMed Google Scholar
• Meijer, O. C. et al. Steroid receptor coactivator-1 splice variants differentially affect corticosteroid receptor signaling. Endocrinology 146, 1438–1448 (2005).
  CAS PubMed Google Scholar
• Karten, Y. J., Nair, S. M., van Essen, L., Sibug, R. & Joëls, M. Long-term exposure to high corticosterone levels attenuates serotonin responses in rat hippocampal CA1 neurons. Proc. Natl Acad. Sci. USA 96, 13456–13461 (1999). This study shows that prolonged elevation of the corticosteroid concentration, which is a possible causative factor for depression in humans, gradually attenuates responsiveness to serotonin without necessarily decreasing serotonin-1A receptor mRNA levels in pyramidal neurons.
  CAS PubMed PubMed Central Google Scholar
• Froger, N. et al. Neurochemical and behavioral alterations in glucocorticoid receptor-impaired transgenic mice after chronic mild stress. J. Neurosci. 24, 2787–2796 (2004).
  CAS PubMed PubMed Central Google Scholar
• Lopez, J. F., Chalmers, D. T., Little, K. Y. & Watson, S. J. A. E. Bennett Research Award. Regulation of serotonin1A, glucocorticoid, and mineralocorticoid receptor in rat and human hippocampus: implications for the neurobiology of depression. Biol. Psychol. 43, 547–573 (1998).
  CAS Google Scholar
• Dunn, A. J., Swiergiel, A. H. & Palamarchouk, V. Brain circuits involved in corticotropin-releasing factor-norepinephrine interactions during stress. Ann. NY Acad. Sci. 1018, 25–34 (2004).
  CAS PubMed Google Scholar
• Cabib, S. & Puglisi-Allegra, S. Opposite responses of mesolimbic dopamine system to controllable and uncontrollable aversive experiences. J. Neurosci. 14, 3333–3340 (1994).
  CAS PubMed PubMed Central Google Scholar
• Yau, J. L., Kelly, P. A. & Seckl, J. R. Increased glucocorticoid receptor gene expression in the rat hippocampus following combined serotonergic and medial septal cholinergic lesions. Brain Res. Mol. Brain Res. 27, 174–178 (1994).
  CAS PubMed Google Scholar
• Maccari, S. et al. Hippocampal type I and type II corticosteroid receptors are modulated by central noradrenergic systems. Psychoneuroendocrinology 17, 103–112 (1992).
  CAS PubMed Google Scholar
• Reul, J. M., Stec, I., Soder, M. & Holsboer, F. Chronic treatment of rats with the antidepressant amitriptyline attenuates the activity of the hypothalamic-pituitary-adrenocortical system. Endocrinology 133, 312–320 (1993). This paper indicates that during amitriptyline treatment, a rise in limbic MR might be the initial phenomenon in a successively adjusting HPA system, as evidenced by the decreasing plasma hormone concentrations, declining adrenal size and upregulation of GR in particular brain regions.
  CAS PubMed Google Scholar
• Lai, M. et al. Differential regulation of corticosteroid receptors by monoamine neurotransmitters and antidepressant drugs in primary hippocampal culture. Neuroscience 118, 975–984 (2003).
  CAS PubMed Google Scholar
• Hugin-Flores, M. E., Steimer, T., Aubert, M. L. & Schulz, P. Mineralo- and glucocorticoid receptor mRNAs are differently regulated by corticosterone in the rat hippocampus and anterior pituitary. Neuroendocrinology 79, 174–184 (2004).
  PubMed Google Scholar
• Gass, P. et al. Genetic disruption of mineralocorticoid receptor leads to impaired neurogenesis and granule cell degeneration in the hippocampus of adult mice. EMBO Rep. 1, 447–451 (2000).
  CAS PubMed PubMed Central Google Scholar
• Edwards, E., King, J. A. & Fray, J. C. Increased basal activity of the HPA axis and renin angiotensin system in congenital learned helpless rats exposed to stress early in development. Int. J. Dev. Neurosci. 17, 805–812 (1999).
  CAS PubMed Google Scholar
• Degen, S. B., Verheij, M. M. & Cools, A. R. Genetic background, nature of event, and time of exposure to event direct the phenotypic expression of a particular genotype. A study with apomorphine-(un)susceptible Wistar rats. Behav. Brain Res. 154, 107–112 (2004).
  CAS PubMed Google Scholar
• Keck, M. E. et al. Vasopressin mediates the response of the combined dexamethasone/CRH test in hyper-anxious rats: implications for pathogenesis of affective disorders. Neuropsychopharmacology 26, 94–105 (2002).
  CAS PubMed Google Scholar
• Landgraf, R. & Wigger, A. Born to be anxious: neuroendocrine and genetic correlates of trait anxiety in HAB rats. Stress 6, 111–119 (2003).
  CAS PubMed Google Scholar
• Murgatroyd, C. et al. Impaired repression at a vasopressin promoter polymorphism underlies overexpression of vasopressin in a rat model of trait anxiety. J. Neurosci. 24, 7762–7770 (2004).
  CAS PubMed PubMed Central Google Scholar
• Bohus, B. et al. Neuroendocrine states and behavioral and physiological stress responses. Prog. Brain Res. 72, 57–70 (1987).
  CAS PubMed Google Scholar
• Korte, S. M., Koolhaas, J. M., Wingfield, J. C. & McEwen, B. S. The Darwinian concept of stress: benefits of allostasis and costs of allostatic load and the trade-offs in health and disease. Neurosci. Biobehav. Rev. 29, 3–38 (2005).
  PubMed Google Scholar
• Veenema, A. H., Meijer, O. C., de Kloet, E. R. & Koolhaas, J. M. Genetic selection for coping style predicts stressor susceptibility. J. Neuroendocrinol. 15, 256–267 (2003).
  CAS PubMed Google Scholar
• Feldker, D. E. et al. Serial analysis of gene expression predicts structural differences in hippocampus of long attack latency and short attack latency mice. Eur. J. Neurosci. 17, 379–387 (2003).
  PubMed Google Scholar
• Seckl, J. R. & Meaney, M. J. Glucocorticoid programming. Ann. NY Acad. Sci. 1032, 63–84 (2004).
  CAS PubMed Google Scholar
• Francis, D., Diorio, J., Liu, D. & Meaney, M. J. Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 286, 1155–1158 (1999).
  CAS PubMed Google Scholar
• Levine, S. Infantile experience and resistance to physiological stress. Science 126, 405 (1957).
  CAS PubMed Google Scholar
• Levine, S., Dent, G. W. & de Kloet, E. R. in Encyclopedia of Stress 518–526 (Academic, San Diego, USA, 2000).
  Google Scholar
• Meaney, M. J., Aitken, D. H., van Berkel, C., Bhatnagar, S. & Sapolsky, R. M. Effect of neonatal handling on age-related impairments associated with the hippocampus. Science 239, 766–768 (1988).
  CAS PubMed Google Scholar
• Liu, D. et al. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 277, 1659–1662 (1997).
  CAS PubMed Google Scholar
• Weaver, I. C. G. et al. Epigenetic programming by maternal behavior. Nature Neurosci. 7, 847–854 (2004). These data indicate that a potentially reversible epigenomic state of a gene can be established through behavioural programming.
  CAS PubMed Google Scholar
• Ladd, C. O., Huot, R. L., Thrivikraman, K. V., Nemeroff, C. B. & Plotsky, P. M. Long-term adaptations in glucocorticoid receptor and mineralocorticoid receptor mRNA and negative feedback on the hypothalamo–pituitary–adrenal axis following neonatal maternal separation. Biol. Psychiatry 55, 367–375 (2004).
  CAS PubMed Google Scholar
• Oitzl, M. S., Workel, J. O., Fluttert, M., Frosch, F. & de Kloet, E. R. Maternal deprivation affects behaviour from youth to senescence: amplification of individual differences in spatial learning and memory in senescent Brown Norway rats. Eur. J. Neurosci. 12, 3771–3780 (2000).
  CAS PubMed Google Scholar
• Van Riel, E., van Gemert, N. G., Meijer, O. C. & Joëls, M. Effect of early life stress on serotonin responses in the hippocampus of young adult rats. Synapse 53, 11–19 (2004).
  CAS PubMed Google Scholar
• Coplan, J. D. et al. Persistent elevations of cerebrospinal fluid concentrations of corticotrophin releasing factor in adult nonhuman primates exposed to early-life stressors: implications for the pathophysiology of mood and anxiety disorders. Proc. Natl Acad. Sci. USA 93, 1619–1623 (1996). These data indicate a potential neurobiological mechanism in non-human primates by which early-life stressors might contribute to adult psychopathology.
  CAS PubMed PubMed Central Google Scholar
• Kendler, K. S. et al. Stressful life events, genetic liability, and onset of an episode of major depression in women. Am. J. Psychiatry 152, 833–842 (1995).
  CAS PubMed Google Scholar
• Brown, E. S., Varghese, F. P. & McEwen, B. S. Association of depression with medical illness: does cortisol play a role? Biol. Psychiatry 55, 1–9 (2004).
  CAS PubMed Google Scholar
• Lupien, S. J. et al. Cortisol levels during human aging predict hippocampal atrophy and memory deficits. Nature Neurosci. 1, 69–73 (1998). This study presents evidence that basal cortisol elevation might cause hippocampal damage and impair hippocampus-dependent learning and memory in humans.
  CAS PubMed Google Scholar
• Sheline, Y. I., Sanghavi, M., Mintun, M. A. & Gado, M. H. Depression duration but not age predicts hippocampal volume loss in medically healthy women with recurrent major depression. J. Neurosci. 19, 5034–5043 (1999).
  CAS PubMed PubMed Central Google Scholar
• Müller, M. B. et al. Neither major depression nor glucocorticoid treatment affects the cellular integrity of the human hippocampus. Eur. J. Neurosci. 14, 1603–1612 (2001).
  PubMed Google Scholar
• Tronche, F. et al. Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety. Nature Genet. 23, 99–103 (1999). The authors show that conditional mutagenesis of GR in the nervous system provides genetic evidence for the importance of GR signalling in emotional behaviour
  CAS PubMed Google Scholar
• Boyle, M. P. et al. Acquired deficit of forebrain glucocorticoid receptor produces depression-like changes in adrenal axis regulation and behavior. Proc. Natl Acad. Sci. USA 102, 473–478 (2005).
  CAS PubMed Google Scholar
• Wei, Q. et al. Glucocorticoid receptor overexpression in forebrain: a mouse model of increased emotional lability. Proc. Natl Acad. Sci. USA 101, 11851–11856 (2004).
  CAS PubMed PubMed Central Google Scholar
• Smith, G. W. et al. Corticotropin releasing factor receptor 1-deficient mice display decreased anxiety, impaired stress response, and aberrant neuroendocrine development. Neuron 20, 1093–1102 (1998).
  CAS PubMed Google Scholar
• Timpl, P. et al. Impaired stress response and reduced anxiety in mice lacking a functional corticotropin-releasing hormone receptor 1. Nature Genet. 19, 162–166 (1998).
  CAS PubMed Google Scholar
• Müller, M. B. et al. Limbic corticotropin-releasing hormone receptor 1 mediates anxiety-related behavior and hormonal adaptation to stress. Nature Neurosci. 6, 1100–1107 (2003). This study presents evidence that limbic CRHR1 modulates anxiety-related behaviour independent of HPA-axis function.
  PubMed Google Scholar
• Pepin, M. C., Pothier, F. & Barden, N. Antidepressant drug action in a transgenic mouse model of the endocrine changes seen in depression. Mol. Pharmacol. 42, 991–995 (1992).
  CAS PubMed Google Scholar
• Heuser, I., Yassouridis, A. & Holsboer, F. The combined dexamethasone/CRH test: a refined laboratory test for psychiatric disorders. J. Psychiatr. Res. 28, 341–356 (1994).
  CAS PubMed Google Scholar
• Meijer, O. C. et al. Penetration of dexamethasone into brain glucocorticoid targets is enhanced in mdr1A P-glycoprotein knockout mice. Endocrinology 139, 1789–1793 (1998).
  CAS PubMed Google Scholar
• Purba, J. S., Hoogendijk, W. J., Hofman, M. A. & Swaab, D. F. Increased number of vasopressin- and oxytocin-expressing neurons in the paraventricular nucleus of the hypothalamus in depression. Arch. Gen. Psychiatry 53, 137–143 (1996).
  CAS PubMed Google Scholar
• Zobel, A. W. et al. Cortisol response in the combined dexamethasone/CRH test as predictor of relapse in patients with remitted depression. A prospective study. J. Psychiatr. Res. 35, 83–94 (2001).
  CAS PubMed Google Scholar
• Modell, S. et al. Hormonal response pattern in the combined DEX-CRH test is stable over time in subjects at high familial risk for affective disorders. Neuropsychopharmacology 18, 253–262 (1998).
  CAS PubMed Google Scholar
• Pariante, C. M. et al. Antidepressants enhance glucocorticoid receptor function in vitro by modulating the membrane steroid transporters. Br. J. Pharmacol. 134, 1335–1343 (2001).
  CAS PubMed PubMed Central Google Scholar
• Sullivan, P. F., Neale, M. C. & Kendler, K. S. Genetic epidemiology of major depression: review and meta-analysis. Am. J. Psychiatry 157, 1552–1562 (2000).
  CAS PubMed Google Scholar
• Heim, C. & Nemeroff, C. B. The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biol. Psychiatry 49, 1023–1039 (2001).
  CAS PubMed Google Scholar
• Rinne, T. et al. Hyperresponsiveness of hypothalamic–pituitary–adrenal axis to combined dexamethasone/corticotropin-releasing hormone challenge in female borderline personality disorder subjects with a history of sustained childhood abuse. Biol. Psychiatry 52, 1102–1112 (2002).
  CAS PubMed Google Scholar
• Davidson, J. R., Stein, D. J., Shalev, A. Y. & Yehuda, R. Posttraumatic stress disorder: acquisition, recognition, course, and treatment. J. Neuropsychiatry Clin. Neurosci. 16, 135–147 (2004).
  PubMed Google Scholar
• Lindley, S. E., Carlson, E. B. & Benoit, M. Basal and dexamethasone suppressed salivary cortisol concentrations in a community sample of patients with posttraumatic stress disorder. Biol. Psychiatry 55, 940–945 (2004).
  CAS PubMed Google Scholar
• Binder, E. B. et al. Polymorphisms in FKBP5 are associated with increased recurrence of depressive episodes and rapid response to antidepressant treatment. Nature Genet. 36, 1319–1325 (2004). Individuals carrying a polymorphism in FKBP5, a GR-regulating co-chaperone, showed less HPA axis hyperactivity and a significant association with the response to antidepressants.
  CAS PubMed Google Scholar
• Wochnik, G. M. et al. FKBP51 and FKBP52 differentially regulate dynein interaction and nuclear translocation of the glucocorticoid receptor in mammalian cells. J. Biol. Chem. (in the press).
• van Rossum, E. F. & Lamberts, S. W. Polymorphisms in the glucocorticoid receptor gene and their associations with metabolic parameters and body composition. Recent Prog. Horm. Res. 59, 333–357 (2004).
  CAS PubMed Google Scholar
• Stevens, A. et al. Glucocorticoid sensitivity is determined by a specific glucocorticoid receptor haplotype. J. Clin. Endocrinol. Metab. 89, 892–897 (2004).
  CAS PubMed Google Scholar
• Wüst, S. et al. Common polymorphisms in the glucocorticoid receptor gene are associated with adrenocortical responses to psychosocial stress. J. Clin. Endocrinol. Metab. 89, 565–573 (2004). This was the first report to document an effect of GR gene polymorphisms on cortisol responses to psychosocial stress that might contribute to individual vulnerability to HPA-related disorders.
  PubMed Google Scholar
• Caspi, A. et al. Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science 301, 386–389 (2003). An epidemiological study that provides evidence of a gene-by-environment interaction, in which the response of an individual to environmental insults is moderated by genetic makeup.
  CAS PubMed Google Scholar
• Kaufer, D. et al. Restructuring the neuronal stress response with anti-glucocorticoid gene delivery. Nature Neurosci. 7, 947–953 (2004). In this study, a genetic strategy diminished the neurological damage inflicted by glucocorticoids in the hippocampus. In particular, a chimeric receptor combining the ligand-binding domain of the glucocorticoid receptor and the DNA-binding domain of the oestrogen receptor seemed effective.
  CAS PubMed Google Scholar
• Seckl, J. R. & Walker, B. R. 11β-hydroxysteroid dehydrogenase type 1 as a modulator of glucocorticoid action: from metabolism to memory. Trends Endocrinol. Metab. 15, 418–424 (2004).
  CAS PubMed Google Scholar
• Young, A. H. et al. Improvements in neurocognitive function and mood following adjunctive treatment with mifepristone (RU-486) in bipolar disorder. Neuropsychopharmacology 29, 1538–1545 (2004).
  CAS PubMed Google Scholar
• Zobel, A. W. et al. Effects of the high-affinity corticotropin-releasing hormone receptor 1 antagonist R121919 in major depression: the first 20 patients treated. J. Psychiatr. Res. 34, 171–181 (2000).
  CAS PubMed Google Scholar
• Schatzberg, A. F., Rothschild, A. J., Langlais, P. J., Bird, E. D. & Cole, J. O. A corticosteroid/dopamine hypothesis for psychotic depression and related states. Psychiatr. Res. 19, 57–64 (1985).
  CAS Google Scholar
• Belanoff, J. K. et al. An open label trial of C-1073 (mifepristone) for psychotic major depression. Biol. Psychiatry 52, 386–392 (2002).
  CAS PubMed Google Scholar
• van der Lely, A. J., Foeken, K., van der Mast, R. C. & Lamberts, S. W. Rapid reversal of acute psychosis in the Cushing syndrome with the cortisol-receptor antagonist mifepristone (RU 486). Ann. Intern. Med. 114, 143–144 (1991).
  CAS PubMed Google Scholar
• Oitzl, M. S., Fluttert, M., Sutanto, W. & de Kloet, E. R. Continuous blockade of brain glucocorticoid receptors facilitates spatial learning and memory in rats. Eur. J. Neurosci. 10, 3759–3766 (1998).
  CAS PubMed Google Scholar
• Bachmann, C. G., Linthorst, A. C., Holsboer, F. & Reul, J. M. Effect of chronic administration of selective glucocorticoid receptor antagonists on the rat hypothalamic–pituitary–adrenocortical axis. Neuropsychopharmacology 28, 1056–1067 (2003).
  CAS PubMed Google Scholar
• Holsboer, F. The rationale for corticotropin-releasing hormone receptor (CRH-R) antagonists to treat depression and anxiety. J. Psychiatr. Res. 33, 181–214 (1999).
  CAS PubMed Google Scholar
• Aerni, A. et al. Low-dose cortisol for symptoms of posttraumatic stress disorder. Am. J. Psychiatry 161, 1488–1490 (2004).
  PubMed Google Scholar
• Schelling, G. et al. Stress doses of hydrocortisone, traumatic memories, and symptoms of posttraumatic stress disorder in patients after cardiac surgery: a randomized study. Biol. Psychiatry 55, 627–633 (2004).
  CAS PubMed Google Scholar
• Hsu, S. Y. & Hsueh, A. J. Human stresscopin and stresscopin-related peptide are selective ligands for the type corticotropin-releasing hormone receptor. Nature Med. 7, 605–611 (2001).
  CAS PubMed Google Scholar
• Reyes, T. M. et al. Urocortin II: a member of the corticotropin-releasing factor (CRF) neuropeptide family that is selectively bound by type 2 CRF receptors. Proc. Natl Acad. Sci. USA 98, 2843–2848 (2001).
  CAS PubMed PubMed Central Google Scholar
• Heinrichs, S. C. & Koob, G. F. Corticotropin-releasing factor in brain: a role in activation, arousal, and affect regulation. J. Pharmacol. Exp. Ther. 311, 427–440 (2004).
  CAS PubMed Google Scholar
• De Bosscher, K., Vanden Berghe, W. & Haegeman, G. The interplay between the glucocorticoid receptor and nuclear factor-κB or activator protein-1: molecular mechanisms for gene repression. Endocr. Rev. 24, 488–522 (2003).
  CAS PubMed Google Scholar