Psychoneuroendocrinology
Volume 32, Issue 5 , Pages 417-429 , June 2007

Persistent neuroendocrine and behavioral effects of a novel, etiologically relevant mouse paradigm for chronic social stress during adolescence

Received 21 July 2006 ,Revised 9 February 2007 ,Accepted 18 February 2007.

References 

  1. Ader R. Early experiences accelerate maturation of the 24-h adrenocortical rhythm. Science. 1969;163:1225–1226
  2. Ader R, Grota LJ. Rhytmicity in the maternal behaviour of Rattus norvegicus. Anim. Behav. 1970;18:144–150
  3. Aguilera G. Regulation of pituitary ACTH secretion during chronic stress. Front. Neuroendocrinol. 1994;15:321–350
  4. Aguilera G, Rabadan-Diehl C, Nikodemova M. Regulation of pituitary corticotropin releasing hormone receptors. Peptides. 2001;22:769–774
  5. Ahima RS, Prabakaran D, Flier JS. Postnatal leptin surge and regulation of circadian rhythm of leptin by feeding. Implications for energy homeostasis and neuroendocrine function. J. Clin. Invest. 1998;101:1020–1027
  6. Albeck DS, McKittrick CR, Blanchard DC, Blanchard RJ, Nikulina J, McEwen BS, et al. Chronic social stress alters levels of corticotropin-releasing factor and arginine vasopressin mRNA in rat brain. J. Neurosci. 1997;17:4895–4903
  7. Amat J, Baratta MV, Paul E, Bland ST, Watkins LR, Maier SF. Medial prefrontal cortex determines how stressor controllability affects behavior and dorsal raphe nucleus. Nat. Neurosci. 2005;8:365–371
  8. Anisman H, Zacharko RM. Depression as a consequence of inadequate neurochemical adaptation in response to stressors. Br. J. Psychiatry. 1992;(Suppl.):36–43
  9. Anisman H, Zaharia MD, Meaney MJ, Merali Z. Do early-life events permanently alter behavioral and hormonal responses to stressors?. Int. J. Dev. Neurosci. 1998;16:149–164
  10. Arai M, Widmaier EP. Steroidogenesis in isolated adrenocortical cells during development in rats. Mol. Cell. Endocrinol. 1993;92:91–97
  11. Avital A, Ram E, Maayan R, Weizman A, Richter-Levin G. Effects of early-life stress on behavior and neurosteroid levels in the rat hypothalamus and entorhinal cortex. Brain Res. Bull. 2006;68:419–424
  12. Bartolomucci A, Palanza P, Gaspani L, Limiroli E, Panerai AE, Ceresini G, et al. Social status in mice: behavioral, endocrine and immune changes are context dependent. Physiol. Behav. 2001;73:401–410
  13. Bartolomucci A, Palanza P, Parmigiani S, Pederzani T, Merlot E, Neveu PJ, et al. Chronic psychosocial stress down-regulates central cytokines mRNA. Brain Res. Bull. 2003;62:173–178
  14. Bartolomucci A, Palanza P, Sacerdote P, Ceresini G, Chirieleison A, Panerai AE, et al. Individual housing induces altered immuno-endocrine responses to psychological stress in male mice. Psychoneuroendocrinology. 2003;28:540–558
  15. Bartolomucci A, Chirieleison A, Gioiosa L, Ceresini G, Parmigiani S, Palanza P. Age at group formation alters behavior and physiology in male but not female CD-1 mice. Physiol. Behav. 2004;82:425–434
  16. Bartolomucci A, Palanza P, Sacerdote P, Panerai AE, Sgoifo A, Dantzer R, et al. Social factors and individual vulnerability to chronic stress exposure. Neurosci. Biobehav. Rev. 2005;29:67–81
  17. Beijamini V, Andreatini R. Effects of Hypericum perforatum and paroxetine in the mouse defense test battery. Pharmacol. Biochem. Behav. 2003;74:1015–1024
  18. Blanchard DC, Spencer RL, Weiss SM, Blanchard RJ, McEwen B, Sakai RR. Visible burrow system as a model of chronic social stress: behavioral and neuroendocrine correlates. Psychoneuroendocrinology. 1995;20:117–134
  19. Brown GW, Prudo R. Psychiatric disorder in a rural and an urban population, 1: aetiology of depression. Psychol. Med. 1981;11:581–599
  20. Conrad CD, Galea LA, Kuroda Y, McEwen BS. Chronic stress impairs rat spatial memory on the Y maze, and this effect is blocked by tianeptine pretreatment. Behav. Neurosci. 1996;110:1321–1334
  21. Dettling AC, Feldon J, Pryce CR. Early deprivation and behavioral and physiological responses to social separation/novelty in the marmoset. Pharmacol. Biochem. Behav. 2002;73:259–269
  22. Deuschle M, Schweiger U, Weber B, Gotthardt U, Korner A, Schmider J, et al. Diurnal activity and pulsatility of the hypothalamus–pituitary–adrenal system in male depressed patients and healthy controls. J. Clin. Endocrinol. Metab. 1997;82:234–238
  23. Ducottet C, Belzung C. Correlations between behaviours in the elevated plus-maze and sensitivity to unpredictable subchronic mild stress: evidence from inbred strains of mice. Behav. Brain Res. 2005;156:153–162
  24. Fluttert M, Dalm S, Oitzl MS. A refined method for sequential blood sampling by tail incision in rats. Lab. Anim. 2000;34:372–378
  25. Fuchs E. Social stress in tree shrews as an animal model of depression: an example of a behavioral model of a CNS disorder. CNS Spectr. 2005;10:182–190
  26. Geyer MA, Markou A. Animal models of psychiatric disorders. In:  Bloom FE,  Kupfer DJ editor. Psychopharmacology: The Fourth Generation of Progress. New York: Raven Press; 1995;p. 787–798
  27. Goeldner FO, Pigatto G, Ribeiro AF, Machado HB, Boerngen-Lacerda R. Influence of fluoxetine and paroxetine in behavioral sensitization induced by ethanol in mice. Pharm. Biochem. Behav. 2005;82:388–396
  28. Heim C, Nemeroff CB. The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biol. Psychiatry. 2001;49:1023–1039
  29. Henry JP, Stephens PM. The social environment and essential hypertension in mice: possible role of the innervation of the adrenal cortex. Prog. Brain. Res. 1977;47:263–276263–276
  30. Herman JP, Spencer R. Regulation of hippocampal glucocorticoid receptor gene transcription and protein expression in vivo. J. Neurosci. 1998;18:7462–7473
  31. Holsboer F. The rationale for corticotropin-releasing hormone receptor (CRH-R) antagonists to treat depression and anxiety. J. Psychiatr. Res. 1999;33:181–214
  32. Holsboer F. The corticosteroid receptor hypothesis of depression. Neuropsychopharmacology. 2000;23:477–501
  33. Keck ME, Holsboer F. Hyperactivity of CRH neuronal circuits as a target for therapeutic interventions in affective disorders. Peptides. 2001;22:835–844
  34. Keck ME, Welt T, Müller MB, Uhr M, Ohl F, Wigger A, et al. Reduction of hypothalamic vasopressinergic hyperdrive contributes to clinically relevant behavioral and neuroendocrine effects of chronic paroxetine treatment in a psychopathological rat model. Neuropsychopharmacology. 2003;28:235–243
  35. Klein F, Lemaire V, Sandi C, Vitiello S, Van der LJ, Laurent PE, et al. Prolonged increase of corticosterone secretion by chronic social stress does not necessarily impair immune functions. Life Sci. 1992;50:723–731
  36. Koolhaas JM, Meerlo P, De Boer SF, Strubbe JH, Bohus B. The temporal dynamics of the stress response. Neurosci. Biobehav. Rev. 1997;21:775–782
  37. Levine S, Mody T. The long-term psychobiological consequences of intermittent postnatal separation in the squirrel monkey. Neurosci. Biobehav. Rev. 2003;27:83–89
  38. Li YW, Hill G, Wong H, Kelly N, Ward K, Pierdomenico M, et al. Receptor occupancy of nonpeptide corticotropin-releasing factor 1 antagonist DMP696: correlation with drug exposure and anxiolytic efficacy. J. Pharmacol. Exp. Ther. 2003;305:86–96
  39. Li YW, Fitzgerald L, Wong H, Lelas S, Zhang G, Lindner MD, et al. The pharmacology of DMP696 and DMP904, non-peptidergic CRF1 receptor antagonists. CNS Drug Rev. 2005;11:21–52
  40. Lopez JF, Chalmers DT, Little KY, Watson SJ. Regulation of serotonin1A, glucocorticoid, and mineralocorticoid receptor in rat and human hippocampus: implications for the neurobiology of depression. Biol. Psychiatry. 1998;43:547–573
  41. Merali Z, Levac C, Anisman H. Validation of a simple, ethologically relevant paradigm for assessing anxiety in mice. Biol. Psychiatry. 2003;54:552–565
  42. Meyer U, van Kampen M, Isovich E, Flugge G, Fuchs E. Chronic psychosocial stress regulates the expression of both GR and MR mRNA in the hippocampal formation of tree shrews. Hippocampus. 2001;11:329–336
  43. Mineur YS, Prasol DJ, Belzung C, Crusio WE. Agonistic behavior and unpredictable chronic mild stress in mice. Behav. Genet. 2003;33:513–519
  44. Müller MB, Zimmermann S, Sillaber I, Hagemeyer TP, Deussing JM, Timpl P, et al. Limbic corticotropin-releasing hormone receptor 1 mediates anxiety-related behavior and hormonal adaptation to stress. Nat. Neurosci. 2003;6:1100–1107
  45. Nickel T, Sonntag A, Schill J, Zobel AW, Ackl N, Brunnauer A, et al. Clinical and neurobiological effects of tianeptine and paroxetine in major depression. J. Clin. Psychopharmacol. 2003;23:155–168
  46. Ottenweller JE, Natelson BH, Pitman DL, Drastal SD. Adrenocortical and behavioral responses to repeated stressors: toward an animal model of chronic stress and stress-related mental illness. Biol. Psychiatry. 1989;26:829–841
  47. Pariante CM, Thomas SA, Lovestone S, Makoff A, Kerwin RW. Do antidepressants regulate how cortisol affects the brain?. Psychoneuroendocrinology. 2004;29:423–447
  48. Parker KJ, Buckmaster CL, Justus KR, Schatzberg AF, Lyons DM. Mild early life stress enhances prefrontal-dependent response inhibition in monkeys. Biol. Psychiatry. 2005;57:848–855
  49. Pickering TG. Mental stress as a causal factor in the development of hypertension and cardiovascular disease. Curr. Hypertens. Rep. 2001;3:249–254
  50. Plamondon H, Khan S. Characterization of anxiety and habituation profile following global ischemia in rats. Physiol. Behav. 2005;84:543–552
  51. Post A, Ohl F, Almeida OFX, Binder EB, Rücker M, Welt S, et al. Identification of molecules potentially involved in mediating the in vivo actions of the corticotropin-releasing hormone receptor 1 antagonist, NBI30775 (R121919). Psychopharmacology. 2005;180:150–158
  52. Post RM. Transduction of psychosocial stress into the neurobiology of recurrent affective disorder. Am. J. Psychiatry. 1992;149:999–1010
  53. Rex A, Voigt JP, Voits M, Fink H. Pharmacological evaluation of a modified open-field test sensitive to anxiolytic drugs. Pharmacol. Biochem. Behav. 1998;59:677–683
  54. Rodgers RJ, Boullier E, Chatzimichalaki P, Cooper GD, Shorten A. Contrasting phenotypes of C57BL/6JOlaHsd, 129S2/SvHsd and 129/SvEv mice in two exploration-based tests of anxiety-related behaviour. Physiol. Behav. 2002;77:301–310
  55. Rodgers RJ, Dalvi A. Anxiety, defence and the elevated plus-maze. Neurosci. Biobehav. Rev. 1997;21:801–810
  56. Sachser N, Durschlag M, Hirzel D. Social relationships and the management of stress. Psychoneuroendocrinology. 1998;23:891–904
  57. Schmidt MV, Oitzl MS, Levine S, De Kloet ER. The HPA system during the postnatal development of CD1 mice and the effects of maternal deprivation. Brain Res. Dev. Brain Res. 2002;139:39–49
  58. Spencer SJ, Martin S, Mouihate A, Pittman QJ. Early-life immune challenge: defining a critical window for effects on adult responses to immune challenge. Neuropsychopharmacology. 2006;31:1910–1918
  59. Stefanski V. Social stress in laboratory rats: hormonal responses and immune cell distribution. Psychoneuroendocrinology. 2000;25:389–406
  60. Stefanski V. Social stress in laboratory rats: behavior, immune function, and tumor metastasis. Physiol. Behav. 2001;73:385–391
  61. Tennant C. Life stress and hypertension. J. Cardiovasc. Risk. 2001;8:51–56
  62. Tsankova NM, Berton O, Renthal W, Kumar A, Neve RL, Nestler EJ. Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action. Nat. Neurosci. 2006;9:519–525
  63. Tsoory M, Cohen H, Richter-Levin G. Juvenile stress induces a predisposition to either anxiety or depressive-like symptoms following stress in adulthood. Eur. Neuropsychopharmacol. 2007;17:245–256
  64. Veenema AH, Meijer OC, De Kloet ER, Koolhaas JM. Genetic selection for coping style predicts stressor susceptibility. J. Neuroendocrinol. 2003;15:256–267
  65. Weber B, Lewicka S, Deuschle M, Colla M, Vecsei P, Heuser I. Increased diurnal plasma concentrations of cortisone in depressed patients. J. Clin. Endocrinol. Metab. 2000;85:1133–1136
  66. Willner P. Chronic mild stress (CMS) revisited: consistency and behavioural-neurobiological concordance in the effects of CMS. Neuropsychobiology. 2005;52:90–110
  67. Yau JLW, Hibberd C, Noble J, Seckl JR. The effect of chronic fluoxetine treatment on brain corticosteroid receptor mRNA expression and spatial memory in young and aged rats. Mol. Brain Res. 2002;106:117–123
  68. Zobel AW, Nickel T, Kunzel HE, Ackl N, Sonntag A, Ising M, 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. 2000;34:171–181

PII: S0306-4530(07)00037-6

doi: 10.1016/j.psyneuen.2007.02.011

Psychoneuroendocrinology
Volume 32, Issue 5 , Pages 417-429 , June 2007