Publication Cover
Stress
The International Journal on the Biology of Stress
Volume 17, 2014 - Issue 3
513
Views
8
CrossRef citations to date
0
Altmetric
Research Article

A double-hit model of stress dysregulation in rats: implications for limbic corticosteroid receptors and anxious behavior under amitriptyline treatment

, &
Pages 235-246 | Received 03 Aug 2013, Accepted 29 Mar 2014, Published online: 01 Apr 2014

References

  • Aguilera G. (1994). Regulation of pituitary ACTH secretion during chronic stress. Front Neuroendocrinol 15:321–50
  • Ahima RS, Harlan RE. (1990). Charting of type II glucocorticoid receptor-like immunoreactivity in the rat central nervous system. Neuroscience 39:579–604
  • Ahima RS, Krozowski Z, Harlan RE. (1991). Type I corticosteroid receptor-like immunoreactivity in the rat CNS: distribution and regulation by Corticosteroids. J Comp Neurol 313:522–38
  • Ashina S, Bendtsen L, Jensen R. (2004). Analgesic effect of amitriptyline in chronic tension-type headache is not directly related to serotonin reuptake inhibition. Pain 108(1–2):108–14
  • Aubry J-M, Pozzoli G, Vale W. (1999). Chronic treatment with the antidepressant amitriptyline decreases CRF-R1 receptor mRNA levels in the rat amygdala. Neurosci Lett 266:197–200
  • Bitran D, Shiekh M, Dowd JA, Dugan MM, Renda P. (1998). Corticosterone is permissive to the anxiolytic effect that results from the blockade of hippocampal mineralocorticoid receptors. Pharmacol Biochem Behav 60:879–87
  • Calfa G, Bussolino D, Molina VA. (2007). Involvement of the lateral septum and the ventral Hippocampus in the emotional sequelae induced by social defeat: role of glucocorticoid receptors. Behav Brain Res 181:23–34
  • Calfa G, Volosin M, Molina VA. (2006). Glucocorticoid receptors in lateral septum are involved in the modulation of the emotional sequelae induced by social defeat. Behav Brain Res 172:324–32
  • Cotella EM, Mestres Lascano I, Franchioni L, Levin GM, Suárez MM. (2013). Long-term effects of maternal separation on chronic stress response suppressed by amitriptyline treatment. Stress 16:477–81
  • Cotella EM, Mestres Lascano I, Levin GM, Suárez M, Lascano I. (2009). Amitriptyline treatment under chronic stress conditions: effect on circulating catecholamines and anxiety in early maternally separated rats. Int J Neurosci 119:664–80
  • De Kloet ER. (2008). About stress hormones and resilience to psychopathology. J Neuroendocrinol 20:885–92
  • De Kloet ER, Joëls M, Holsboer F. (2005). Stress and the brain: from adaptation to disease. Nat Rev Neurosci 6:463–75
  • De Kloet ER, Vreugdenhil E, Oitzl MS, Joëls M. (1998). Brain corticosteroid receptor balance in health and disease. Endocr Rev 19:269–301
  • Degroot A, Treit D. (2004). Anxiety is functionally segregated within the septo-hippocampal system. Brain Res 1001:60–71
  • Diefenbacher ME, Litfin M, Herrlich P, Kassel O. (2010). The nuclear isoform of the LIM domain protein Trip6 integrates activating and repressing signals at the promoter-bound glucocorticoid receptor. Mol Cell Endocrinol 320:58–66
  • Gesing A, Bilang-Bleuel A, Droste SK, Linthorst A C, Holsboer F, Reul JM. (2001). Psychological stress increases hippocampal mineralocorticoid receptor levels: involvement of corticotropin-releasing hormone. J Neurosci 21:4822–9
  • Gillespie CF, Nemeroff CB. (2005). Hypercortisolemia and depression. Psychosom Med 67:S26–8
  • Gómez F, Lahmame A, de Kloet R, Armario A. (1996). Hypothalamic-pituitary-adrenal response to chronic stress in five inbred rat strains: differential responses are mainly located at the adrenocortical level. Neuroendocrinology 63:327–37
  • Gomez-Sanchez CE, de Rodriguez AF, Romero DG, Estess J, Warden MP, Gomez-Sanchez MT, Gomez-Sanchez EP. (2006). Development of a panel of monoclonal antibodies against the mineralocorticoid receptor. Endocrinology 147:1343–8
  • Gould GG, Altamirano AV, Javors MA, Frazer AA. (2006). Comparison of the chronic treatment effects of venlafaxine and other antidepressants on serotonin and norepinephrine transporters. Biol Psychiatry 59(5):408–14
  • Gray J, McNaughton N. (2000). The neuropsychology of anxiety: an enquiry into the functions of the septo-hippocampal system. Second. In: Mackintosh NJ, McGaugh JL, Shallice T, Schacter D, Treisman A, Weiskrantz L, editors. Oxford Psychology Series. Oxford: Oxford University Press. p 440
  • Hassan A H, Patchev VK, von Rosenstiel P, Holsboer F, Almeida OF. (1999). Plasticity of hippocampal corticosteroid receptors during aging in the rat. FASEB J 13:115–22
  • Herman JP, Ostrander MM, Mueller NK, Figueiredo H. (2005). Limbic system mechanisms of stress regulation: hypothalamo-pituitary-adrenocortical axis. Prog Neuropsychopharmacol Biol Psychiatry 29:1201–13
  • Hong W, Chen L, Liu Y, Gao W. (2009). ATP hydrolysis is essential for Bag-1M-mediated inhibition of the DNA binding by the glucocorticoid receptor. Biochem Biophys Res Commun 390:77–81
  • Joëls M. (2001). Corticosteroid actions in the hippocampus. J Neuroendocrinol 13:657–69
  • Katz RJ, Hersh S. (1981). Amitriptyline and scopolamine in an animal model of depression. Neurosci Biobehav Rev 5:265–71
  • Kitraki E, Kremmyda O, Youlatos D, Alexis MN, Kittas C. (2004). Gender-dependent alterations in corticosteroid receptor status and spatial performance following 21 days of restraint stress. Neuroscience 125:47–55
  • Korte SM. (2001). Corticosteroids in relation to fear, anxiety and psychopathology. Neurosci Biobehav Rev 25:117–42
  • Ladd CO, Huot RL, Thrivikraman K V, Nemeroff CB, Plotsky PM. (2004). 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 55:367–75
  • Ladd CO, Thrivikraman K V, Huot RL, Plotsky PM. (2005). Differential neuroendocrine responses to chronic variable stress in adult Long Evans rats exposed to handling-maternal separation as neonates. Psychoneuroendocrinology 30:520–33
  • Lai M, Horsburgh K, Bae S-E, Carter RN, Stenvers DJ, Fowler JH, Yau JL, et al. (2007). Forebrain mineralocorticoid receptor overexpression enhances memory, reduces anxiety and attenuates neuronal loss in cerebral ischaemia. Eur J Neurosci 25:1832–42
  • Llorente R, Miguel-Blanco C, Aisa B, Lachize S, Borcel E, Meijer OC, Ramirez MJ, et al. (2011). Long term sex-dependent psychoneuroendocrine effects of maternal deprivation and juvenile unpredictable stress in rats. J Neuroendocrinol 23:329–44
  • Macrì S, Chiarotti F, Würbel H. (2008). Maternal separation and maternal care act independently on the development of HPA responses in male rats. Behav Brain Res 191(2):227–34
  • Macrì S, Mason GJ, Würbel H. (2004). Dissociation in the effects of neonatal maternal separations on maternal care and the offspring’s HPA and fear responses in rats. Eur J Neurosci 20(4):1017–24
  • Makino S, Hashimoto K, Gold PW. (2002). Multiple feedback mechanisms activating corticotropin-releasing hormone system in the brain during stress. Pharmacol Biochem Behav 73:147–58
  • Mamalaki E, Kvetnansky R, Brady LS, Gold PW, Herkenham M. (1992). Repeated immobilization stress alters tyrosine hydroxylase, corticotropin-releasing hormone and corticosteroid receptor messenger ribonucleic Acid levels in rat brain. J Neuroendocrinol 4:689–99
  • Maynard TM, Sikich L, Lieberman JA, LaMantia AS. (2001). Neural development, cell-cell signaling, and the “two-hit” hypothesis of schizophrenia. Schizophr Bull 27:457–76
  • McEwen B. (2001). Plasticity of the hippocampus: adaptation to chronic stress and allostatic load. Ann N Y Acad Sci 933:265–77
  • McEwen B. (2003). Early life influences on life-long patterns of behavior and health. Ment Retard Dev Disabil Res Rev 9:149–54
  • Meaney M. (2001). Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu Rev Neurosci 24:1161–92
  • Meaney M. (2010). Epigenetics and the biological definition of gene × environment interactions. Child Dev 81:41–79
  • Miller G, Chen E, Cole SW. (2009). Health psychology: developing biologically plausible models linking the social world and physical health. Annu Rev Psychol 60:501–24
  • Mitra R, Ferguson D, Sapolsky RM. (2009). Mineralocorticoid receptor overexpression in basolateral amygdala reduces corticosterone secretion and anxiety. Biol Psychiatry 66:686–90
  • Mizoguchi K, Yuzurihara M, Ishige A, Sasaki H, Chui DH, Tabira T. (2001). Chronic stress differentially regulates glucocorticoid negative feedback response in rats. Psychoneuroendocrinology 26:443–59
  • Mongiat LA, Schinder AF. (2011). Adult neurogenesis and the plasticity of the dentate gyrus network. Eur J Neurosci 33:1055–61
  • Mostalac-Preciado CR, de Gortari P, López-Rubalcava C. (2011). Antidepressant-like effects of mineralocorticoid but not glucocorticoid antagonists in the lateral septum: interactions with the serotonergic system. Behav Brain Res 223:88–98
  • Ogawa T, Mikuni M, Kuroda Y, Muneoka K, Mori KJ, Takahashi K. (1994). Periodic maternal deprivation alters stress response in adult offspring: potentiates the negative feedback regulation of restraint stress-induced adrenocortical response and reduces the frequencies of open field-induced behaviors. Pharmacol Biochem Behav 49(4):961–7
  • Oitzl MS, Champagne DL, van der Veen R, De Kloet ER. (2010). Brain development under stress: hypotheses of glucocorticoid actions revisited. Neurosci Biobehav Rev 34:853–66
  • Pariante C. (2004). Do antidepressants regulate how cortisol affects the brain? Psychoneuroendocrinology 29(4):423–47
  • Paskitti ME, McCreary BJ, Herman JP. (2000). Stress regulation of adrenocorticosteroid receptor gene transcription and mRNA expression in rat hippocampus: time-course analysis. Brain Res Mol Brain Res 80:142–52
  • Paxinos G, Watson C. (2007). The rat brain in stereotaxic coordinates6. San Diego: Elsevier Academic Press
  • Pittenger C, Duman RS. (2008). Stress, depression, and neuroplasticity: a convergence of mechanisms. Neuropsychopharmacology 33:88–109
  • Renard GM, Rivarola MA, Suárez M. (2007). Sexual dimorphism in rats: effects of early maternal separation and variable chronic stress on pituitary-adrenal axis and behavior. Int J Dev Neurosci 25:373–9
  • Reul JM, De Kloet ER. (1985). Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation. Endocrinology 117:2505–11
  • Reul JM, Stec I, Söder M, Holsboer F. (1993). Chronic treatment of rats with the antidepressant amitriptyline attenuates the activity of the hypothalamic-pituitary-adrenocortical system. Endocrinology 133:312–20
  • Risold PY, Swanson LW. (1997). Connections of the rat lateral septal complex. Brain Res Brain Res Rev 24:115–95
  • Roth KA, Katz RJ. (1981). Further studies on a novel animal model of depression: Therapeutic effects of a tricyclic antidepressant. Neurosci Biobehav Rev 5:253–8
  • Sah P, Faber ESL, Lopez De Armentia M, Power J. (2003). The amygdaloid complex: anatomy and physiology. Physiol Rev 83:803–34
  • Singewald GM, Rjabokon A, Ebner K. (2011). The modulatory role of the lateral septum on neuroendocrine and behavioral stress responses. Neuropsychopharmacology 36:793–804
  • Soblosky JS, Thurmond JB. (1986). Biochemical and behavioral correlates of chronic stress: effects of tricyclic antidepressants. Pharmacol Biochem Behav 24:1361–8
  • Steffensen SC, Yeckel MF, Miller DR, Henriksen SJ. (1993). Ethanol-induced suppression of hippocampal long-term potentiation is blocked by lesions of the septohippocampal nucleus. Alcohol Clin Exp Res 17:655–9
  • Sutanto W, Rosenfeld P, De Kloet ER, Levine S. (1996). Long-term effects of neonatal maternal deprivation and ACTH on hippocampal mineralocorticoid and glucocorticoid receptors. Brain Res Dev Brain Res 92:156–63
  • Vyas A, Mitra R, Shankaranarayana Rao BS, Chattarji S. (2002). Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. J Neurosci 22:6810–18
  • Wang Q, Joels M, Swaab DF, Lucassen PJ. (2012). Hippocampal GR expression is increased in elderly depressed females. Neuropharmacology 62:527–33
  • Wang Q, Van Heerikhuize J, Aronica E, Kawata M, Seress L, Joels M, Swaab DF, Lucassen PJ. (2013). Glucocorticoid receptor protein expression in human hippocampus; stability with age. Neurobiol Aging 34:1662–73
  • Witter MP, Amaral DG. (2004). Hippocampal formation. In: Paxinos G, editor. The rat nervous system. 3rd edition. Burlington: Academic Press. p 635–704
  • Yau JL, Olsson T, Morris RGM, Meaney M, Seckl JR. (1995). Glucocorticoids, hippocampal corticosteroid receptor gene expression and antidepressant treatment: relationship with spatial learning in young and aged rats. Neuroscience 66:571–81

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.