Chronic Subordinate Colony Housing (CSC) as a Model of Chronic Psychosocial Stress in Male Rats

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Nyuyki, Kewir D ^a   Beiderbeck, Daniela I ^a   Lukas, Michael ^a   Neumann, Inga D ^a   Reber, Stefan O ^a  

^a UNIVERSITY OF REGENSBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CORTICOSTERONE; CORTICOTROPIN;

ADRENAL HYPERPLASIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY DISORDER; ARTICLE; CHRONIC STRESS; CHRONIC SUBORDINATE COLONY HOUSING; COLON DISEASE; CONTROLLED STUDY; COPING BEHAVIOR; CORTICOSTERONE BLOOD LEVEL; CORTICOTROPIN BLOOD LEVEL; FEMALE; HYPOTHALAMUS HYPOPHYSIS SYSTEM; IMMUNOLOGY; MALE; MENTAL STRESS; NONHUMAN; RAT; SOCIAL BEHAVIOR; THYMUS; WEIGHT GAIN; WISTAR RAT;

ADRENAL GLANDS; ADRENOCORTICOTROPIC HORMONE; AGGRESSION; ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; BODY WEIGHT; CORTICOSTERONE; DEPRESSION; FEMALE; HOUSING, ANIMAL; INTERFERON-GAMMA; MALE; MESENTERY; MICE; MUCUS; ORGAN SIZE; RATS; STRESS, PSYCHOLOGICAL; THYMUS GLAND; TIME FACTORS;

MUS; RATTUS; RATTUS NORVEGICUS; RODENTIA;

EID: 84871562199     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0052371     Document Type: Article

References (64)

1. Heim C, Ehlert U, Hellhammer DH, (2000) The potential role of hypocortisolism in the pathophysiology of stress-related bodily disorders. Psychoneuroendocrinology 25: 1-35.
2. Kessler RC, (1997) The effects of stressful life events on depression. Annu Rev Psychol 48: 191-214.
3. Amat J, Baratta MV, Paul E, Bland ST, Watkins LR, et al. (2005) Medial prefrontal cortex determines how stressor controllability affects behavior and dorsal raphe nucleus. Nat Neurosci 8: 365-71.
4. Berton O, McClung CA, Dileone RJ, Krishnan V, Renthal W, et al. (2006) Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science 311: 864-8.
5. Schmidt MV, Sterlemann V, Ganea K, Liebl C, Alam S, et al. (2007) Persistent neuroendocrine and behavioral effects of a novel, etiologically relevant mouse paradigm for chronic social stress during adolescence. Psychoneuroendocrinology 32: 417-29.
6. Stefanski V, (2001) Social stress in laboratory rats: behavior, immune function, and tumor metastasis. Physiol Behav 73: 385-91.
7. Tsankova NM, Berton O, Renthal W, Kumar A, Neve RL, et al. (2006) Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action. Nat Neurosci 9: 519-25.
8. Post RM, (1992) Transduction of psychosocial stress into the neurobiology of recurrent affective disorder. Am J Psychiatry 149: 999-1010.
9. Tennant C, (2002) Life events, stress and depression: a review of recent findings. Aust N Z J Psychiatry 36: 173-82.
10. Blanchard DC, Spencer RL, Weiss SM, Blanchard RJ, McEwen B, et al. (1995) Visible burrow system as a model of chronic social stress: behavioral and neuroendocrine correlates. Psychoneuroendocrinology 20: 117-34.
11. Stefanski V, Peschel A, Reber S, (2003) Social stress affects migration of blood T cells into lymphoid organs. J Neuroimmunol 138: 17-24.
12. Reber SO, Birkeneder L, Veenema AH, Obermeier F, Falk W, et al. (2007) Adrenal insufficiency and colonic inflammation after a novel chronic psycho-social stress paradigm in mice: implications and mechanisms. Endocrinology 148: 670-82.
13. Reber SO, Obermeier F, Straub RH, Veenema AH, Neumann ID, (2008) Aggravation of DSS-induced colitis after chronic subordinate colony (CSC) housing is partially mediated by adrenal mechanisms. Stress 11: 225-34.
14. Singewald GM, Nguyen NK, Neumann ID, Singewald N, Reber SO, (2009) Effect of chronic psychosocial stress-induced by subordinate colony (CSC) housing on brain neuronal activity patterns in mice. Stress 12: 58-69.
15. Slattery DA, Uschold N, Magoni M, Bar J, Popoli M, et al. (2012) Behavioural consequences of two chronic psychosocial stress paradigms: Anxiety without depression. Psychoneuroendocrinology 37: 702-14.
16. Reber SO, Peters S, Slattery DA, Hofmann C, Scholmerich J, et al. (2011) Mucosal immunosuppression and epithelial barrier defects are key events in murine psychosocial stress-induced colitis. Brain Behav Immun 25: 1153-61.
17. Peters S, Grunwald N, Rummele P, Endlicher E, Lechner A, et al. (2011) Chronic psychosocial stress increases the risk for inflammation-related colon carcinogenesis in male mice. Stress 15: 403-15.
18. Uschold-Schmidt N, Nyuyki KD, Fuchsl AM, Neumann ID, Reber SO, (2012) Chronic psychosocial stress results in sensitization of the HPA axis to acute heterotypic stressors despite a reduction of adrenal in vitro ACTH responsiveness. Psychoneuroendocrinology 37: 1676-87.
19. Aguilera G, (1994) Regulation of pituitary ACTH secretion during chronic stress. Front Neuroendocrinol 15: 321-50.
20. Spiga F, Harrison LR, MacSweeney CP, Thomson FJ, Craighead M, et al. (2009) Effect of vasopressin 1b receptor blockade on the hypothalamic-pituitary-adrenal response of chronically stressed rats to a heterotypic stressor. J Endocrinol 200: 285-91.
21. Chen J, Young S, Subburaju S, Sheppard J, Kiss A, et al. (2008) Vasopressin does not mediate hypersensitivity of the hypothalamic pituitary adrenal axis during chronic stress. Ann N Y Acad Sci 1148: 349-59.
22. Belda X, Rotllant D, Fuentes S, Delgado R, Nadal R, et al. (2008) Exposure to severe stressors causes long-lasting dysregulation of resting and stress-induced activation of the hypothalamic-pituitary-adrenal axis. Ann N Y Acad Sci 1148: 165-73.
23. Keeney A, Jessop DS, Harbuz MS, Marsden CA, Hogg S, et al. (2006) Differential effects of acute and chronic social defeat stress on hypothalamic-pituitary-adrenal axis function and hippocampal serotonin release in mice. J Neuroendocrinol 18: 330-8.
24. Barnum CJ, Blandino P Jr, Deak T, (2007) Adaptation in the corticosterone and hyperthermic responses to stress following repeated stressor exposure. J Neuroendocrinol 19: 632-42.
25. Flannelly K, Lore R, (1977) The influence of females upon aggression in domesticated male rats (Rattus norvegicus). Anim Behav 25: 654-9.
26. Neumann ID, Johnstone HA, Hatzinger M, Liebsch G, Shipston M, et al. (1998) Attenuated neuroendocrine responses to emotional and physical stressors in pregnant rats involve adenohypophysial changes. J Physiol 508 (Pt 1): 289-300.
27. Waldherr M, Nyuyki K, Maloumby R, Bosch OJ, Neumann ID, (2010) Attenuation of the neuronal stress responsiveness and corticotrophin releasing hormone synthesis after sexual activity in male rats. Horm Behav 57: 222-9.
28. Pellow S, Chopin P, File SE, Briley M, (1985) Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J Neurosci Methods 14: 149-67.
29. Nyuyki KD, Waldherr M, Baeuml S, Neumann ID (2011) Yes, I am ready now: differential effects of paced versus unpaced mating on anxiety and central oxytocin release in female rats. PLoS One 6: doi:10.1371/journal.pone.0023599.
30. Costall B, Jones BJ, Kelly ME, Naylor RJ, Tomkins DM, (1989) Exploration of mice in a black and white test box: validation as a model of anxiety. Pharmacol Biochem Behav 32: 777-85.
31. Waldherr M, Neumann ID, (2007) Centrally released oxytocin mediates mating-induced anxiolysis in male rats. Proc Natl Acad Sci U S A 104: 16681-4.
32. Lukas M, Toth I, Reber SO, Slattery DA, Veenema AH, et al. (2011) The Neuropeptide Oxytocin Facilitates Pro-Social Behavior and Prevents Social Avoidance in Rats and Mice. Neuropsychopharmacology 36: 2159-68.
33. Slattery DA, Neumann ID, (2010) Chronic icv oxytocin attenuates the pathological high anxiety state of selectively bred Wistar rats. Neuropharmacology 58: 56-61.
34. Porsolt RD, Le Pichon M, Jalfre M, (1977) Depression: a new animal model sensitive to antidepressant treatments. Nature 266: 730-2.
35. Veenema AH, Bredewold R, Neumann ID, (2007) Opposite effects of maternal separation on intermale and maternal aggression in C57BL/6 mice: link to hypothalamic vasopressin and oxytocin immunoreactivity. Psychoneuroendocrinology 32: 437-50.
36. Beiderbeck DI, Neumann ID, Veenema AH, (2007) Differences in intermale aggression are accompanied by opposite vasopressin release patterns within the septum in rats bred for low and high anxiety. Eur J Neurosci 26: 3597-605.
37. Koolhaas JM, Schuurman T, Wiepkema PR, (1980) The organization of intraspecific agonistic behaviour in the rat. Prog Neurobiol 15: 247-68.
38. Beiderbeck DI, Reber SO, Havasi A, Bredewold R, Veenema AH, et al. (2012) High and abnormal forms of aggression in rats with extremes in trait anxiety- Involvement of the dopamine system in the nucleus accumbens. Psychoneuroendocrinology 37: 1969-80.
39. Bartolomucci A, Palanza P, Sacerdote P, Ceresini G, Chirieleison A, et al. (2003) Individual housing induces altered immuno-endocrine responses to psychological stress in male mice. Psychoneuroendocrinology 28: 540-58.
40. Gasparotto OC, Lopes DM, Carobrez SG, (2005) Pair housing affects anxiety-like behaviors induced by a social but not by a physiological stressor in male Swiss mice. Physiol Behav 85: 603-12.
41. Wallace DL, Han MH, Graham DL, Green TA, Vialou V, et al. (2009) CREB regulation of nucleus accumbens excitability mediates social isolation-induced behavioral deficits. Nat Neurosci 12: 200-9.
42. Ahmed SH, Stinus L, Le Moal M, Cador M, (1995) Social deprivation enhances the vulnerability of male Wistar rats to stressor- and amphetamine-induced behavioral sensitization. Psychopharmacology (Berl) 117: 116-24.
43. Barrot M, Wallace DL, Bolanos CA, Graham DL, Perrotti LI, et al. (2005) Regulation of anxiety and initiation of sexual behavior by CREB in the nucleus accumbens. Proc Natl Acad Sci U S A 102: 8357-62.
44. Hall FS, Huang S, Fong GF, Pert A, (1998) The effects of social isolation on the forced swim test in Fawn hooded and Wistar rats. J Neurosci Methods 79: 47-51.
45. Brown KJ, Grunberg NE, (1995) Effects of housing on male and female rats: crowding stresses male but calm females. Physiol Behav 58: 1085-9.
46. Weiss IC, Pryce CR, Jongen-Relo AL, Nanz-Bahr NI, Feldon J, (2004) Effect of social isolation on stress-related behavioural and neuroendocrine state in the rat. Behav Brain Res 152: 279-95.
47. Sachser N, Lick C, (1989) Social stress in guinea pigs. Physiol Behav 46: 137-44.
48. Reber SO, Obermeier F, Straub HR, Falk W, Neumann ID, (2006) Chronic intermittent psychosocial stress (social defeat/overcrowding) in mice increases the severity of an acute DSS-induced colitis and impairs regeneration. Endocrinology 147: 4968-76.
49. Stefanski V, Engler H, (1999) Social stress, dominance and blood cellular immunity. J Neuroimmunol 94: 144-52.
50. Engler H, Stefanski V, (2003) Social stress and T cell maturation in male rats: transient and persistent alterations in thymic function. Psychoneuroendocrinology 28: 951-69.
51. De Goeij DC, Dijkstra H, Tilders FJ, (1992) Chronic psychosocial stress enhances vasopressin, but not corticotropin-releasing factor, in the external zone of the median eminence of male rats: relationship to subordinate status. Endocrinology 131: 847-53.
52. Ashwell JD, Lu FW, Vacchio MS, (2000) Glucocorticoids in T cell development and function*. Annu Rev Immunol 18: 309-45.
53. Kendall MD, al-Shawaf AA, (1991) Innervation of the rat thymus gland. Brain Behav Immun 5: 9-28.
54. Schwartzman RA, Cidlowski JA, (1994) Glucocorticoid-induced apoptosis of lymphoid cells. Int Arch Allergy Immunol 105: 347-54.
55. Stefanski V, (2000) Social stress in laboratory rats: hormonal responses and immune cell distribution. Psychoneuroendocrinology 25: 389-406.
56. Koolhaas JM, Meerlo P, De Boer SF, Strubbe JH, Bohus B, (1997) The temporal dynamics of the stress response. Neurosci Biobehav Rev 21: 775-82.
57. Haller J, Fuchs E, Halasz J, Makara GB, (1999) Defeat is a major stressor in males while social instability is stressful mainly in females: towards the development of a social stress model in female rats. Brain Res Bull 50: 33-9.
58. Hillerer KM, Reber SO, Neumann ID, Slattery DA, (2011) Exposure to chronic pregnancy stress reverses peripartum-associated adaptations: implications for postpartum anxiety and mood disorders. Endocrinology 152: 3930-40.
59. Landgraf R, Wigger A, Holsboer F, Neumann ID, (1999) Hyper-reactive hypothalamo-pituitary-adrenocortical axis in rats bred for high anxiety-related behaviour. J Neuroendocrinol 11: 405-7.
60. Vicario M, Guilarte M, Alonso C, Yang P, Martinez C, et al. (2010) Chronological assessment of mast cell-mediated gut dysfunction and mucosal inflammation in a rat model of chronic psychosocial stress. Brain Behav Immun 24: 1166-75.
61. Vicario M, Alonso C, Guilarte M, Serra J, Martinez C, et al. (2012) Chronic psychosocial stress induces reversible mitochondrial damage and corticotropin-releasing factor receptor type-1 upregulation in the rat intestine and IBS-like gut dysfunction. Psychoneuroendocrinology 37: 65-77.
62. Reber SO, Neumann ID, (2008) Defensive behavioral strategies and enhanced state anxiety during chronic subordinate colony housing are accompanied by reduced hypothalamic vasopressin, but not oxytocin, expression. Ann N Y Acad Sci 1148: 184-95.
63. Veenema AH, Reber SO, Selch S, Obermeier F, Neumann ID, (2008) Early life stress enhances the vulnerability to chronic psychosocial stress and experimental colitis in adult mice. Endocrinology 149: 2727-36.
64. McCormick CM, Smith C, Mathews IZ, (2008) Effects of chronic social stress in adolescence on anxiety and neuroendocrine response to mild stress in male and female rats. Behav Brain Res 187: 228-38.