Individual differences in chronically defeated male mice: Behavioral, endocrine, immune, and neurotrophic changes as markers of vulnerability to the effects of stress

Stress

Volumn 14, Issue 5, 2011, Pages 537-548

  Gómez Lzaro, Eneritz ^a   Arregi, Amaia ^a   Beitia, Garikoitz ^a   Vegas, Oscar ^a   Azpiroz, Arantza ^a   Garmendia, Larraitz ^a  

^a UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

Author keywords

BDNF; chronic defeat; corticosterone; individual differences; proinflammatory cytokines; proliferative capacity of splenocytes

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CORTICOSTERONE; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR CHANGE; CLUSTER ANALYSIS; COMPARATIVE STUDY; CONDITIONING; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; DEPRESSION; DISCRIMINANT ANALYSIS; HIPPOCAMPUS; IMMOBILIZATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; SOCIAL STRESS; SPLEEN;

ANIMALS; B-LYMPHOCYTES; BEHAVIOR, ANIMAL; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL PROLIFERATION; CORTICOSTERONE; DOMINANCE-SUBORDINATION; HIPPOCAMPUS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; INDIVIDUALITY; INTERLEUKIN-6; MALE; MICE; PITUITARY-ADRENAL SYSTEM; SPLEEN; STRESS, PSYCHOLOGICAL; SWIMMING; T-LYMPHOCYTES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 80051772007     PISSN: 10253890     EISSN: 16078888     Source Type: Journal    
DOI: 10.3109/10253890.2011.562939     Document Type: Article

References (68)

1. Anisman H. 2009. Cascading effects of stressors and inflammatory immune system activation: Implications for major depressive disorder. J Psychiatry Neurosci 34:4-20.
2. Anisman H, Merali Z. 2002. Cytokines, stress, and depressive illness. Brain Behav Immun 16:513-524. (Pubitemid 35333731)
3. Antonijevic I A. 2006. Depressive disorders: Is it time to endorse different pathophysiologies? Psychoneuroendocrinology 31: 1-15. (Pubitemid 41668888)
4. Avitsur R, Stark JL, Sheridan J F. 2001. Social stress induces glucocorticoid resistance in subordinate animals. Horm Behav 39:247-257. (Pubitemid 32548016)
5. Barbany G, Persson H. 1992. Regulation of neurotrophin messenger-RNA expression in the rat-brain by glucocorticoids. Eur J Neurosci 4:396-403.
6. Bartolomucci A, Palanza P, Gaspani L, Limiroli E, Panerai AE, Ceresini G, Poli MD, Parmigiani S. 2001. Social status in mice: Behavioral, endocrine and immune changes are context dependent. Physiol Behav 73:401-410. (Pubitemid 32595715)
7. Bartolomucci A, Palanza P, Sacerdote P, Panerai AE, Sgoifo A, Dantzer R, Parmigiani S. 2005. Social factors and individual vulnerability to chronic stress exposure. Neurosci Biobehav Rev 29:67-81. (Pubitemid 40094579)
8. Beitia G, Garmendia L, Azpiroz A, Vegas O, Brain PF, Arregi A. 2005. Time-dependent behavioral, neurochemical, and immune consequences of repeated experiences of social defeat stress in male mice and the ameliorative effects of fluoxetine. Brain Behav Immun 19:530-539. (Pubitemid 41408582)
9. Berton O, McClung CA, DiLeone RJ, Krishnan V, Renthal W, Russo SJ, Graham D, Tsankova NM, Bolanos CA, Rios M, Monteggia LM, Self DW, Nestler E J. 2006. Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science 311:864-868. (Pubitemid 43228853)
10. Bielajew C, Konkle AT M, Kentner AC, Baker SL, Stewart A, Hutchins AA, Santa-Maria Barbagallo L, Fouriezos G. 2003. Strain and gender specific effects in the forced swim test: Effects of previous stress exposure. Stress 6:269-280. (Pubitemid 38101486)
11. Blanchard RJ, McKittrick CR, Blanchard D C. 2001. Animal models of social stress: Effects on behavior and brain neurochemical systems. Physiol Behav 73:261-271. (Pubitemid 32595699)
12. Brain PF, McAllister KH, Walmsley S V. 1989. Drug effects on social behavior: Methods in ethopharmacology. In: Boulton AA, Baker GB, Greenshaw AJ, editors. Neuromethods. Totowa, NJ: The Humana Press Inc. p 687-739.
13. Butterweck V, Winterhoff H, Herkenham M. 2001. St. John's wort, hypericin, and imipramine: A comparative analysis of mRNA levels in brain areas involved in HPA axis control following short-term and long-term administration in normal and stressed rats. Psychiatry 6:547-564. (Pubitemid 32772564)
14. Buwalda B, Kole MH P, Veenema AH, Huininga M, de Boer SF, Korte SM, Koolhaas J M. 2005. Long-term effects of social stress on brain and behavior: A focus on hippocampal functioning. Neurosci Biobehav Rev 29:83-97. (Pubitemid 40094580)
15. Chen MJ, Nguyen TV, Pike CJ, Russo-Neustadt A A. 2007. Norepinephrine induces BDNF and activates the PI-3K and MAPK cascades in embryonic hippocampal neurons. Cell Signal 19:114-128. (Pubitemid 44880248)
16. Conner JM, Lauterborn JC, Yan Q, Gall CM, Varon S. 1997. Distribution of brain-derived neurotrophic factor (BDNF) protein and mRNA in the normal adult rat CNS: Evidence for anterograde axonal transport. J Neurosci 17:2295-2313. (Pubitemid 27137397)
17. Dantzer R, O'Connor JC, Freund GG, Johnson RW, Kelley K W. 2008. From inflammation to sickness and depression: When the immune system subjugates the brain. Nat Rev Neurosci 9: 46-56. (Pubitemid 350295688)
18. De Kloet ER, Vreugdenhil E, Oitzl MS, Joels M. 1998. Brain corticosteroid receptor balance in health and disease. Endocr Rev 19:269-301. (Pubitemid 29117816)
19. De Kloet ER, Joels M, Holsboer F. 2005. Stress and the brain: From adaptation to disease. Nat Rev Neurosci 6:463-475. (Pubitemid 40769171)
20. Duarte FS, Andrade ES, Vieira RA, Uieara M, Nunes RJ, de Lima TC M. 2006. Synthesis and antidepressant-like action of stereoisomers of imidobenzenesulfonylaziridines in mice evaluated in the forced swimming test. Bioorg Med Chem 14: 5397-5401. (Pubitemid 43903245)
21. Duman RS, Monteggia L M. 2006. A neurotrophic model for stress-related mood disorders. Biol Psychiatry 59:1116-1127.
22. Fries E, Hesse J, Hellhammer J, Hellhammer D H. 2005.A new view on hypocortisolism. Psychoneuroendocrinology 30:1010-1016. (Pubitemid 40982486)
23. Gasparotto OC, Ignacio ZM, Lin K, Goncalves S. 2002. The effect of different psychological profiles and timings of stress exposure on humoral immune response. Physiol Behav 76:321-326. (Pubitemid 34607239)
24. Gold PW, Chrousos G P. 2002. Organization of the stress system and its dysregulation in melancholic and atypical depression: High vs low CRH/NE states. Mol Psychiatry 7:254-275. (Pubitemid 34280634)
25. Golde WT, Gollobin P, Rodriguez L L. 2005. A rapid, simple, and humane method for submandibular bleeding of mice using a lancet. Lab Anim 34:39-43. (Pubitemid 44662092)
26. Gupta S, Aslakson E, Gurbaxani B, Vernon S D. 2007. Inclusion of the glucocorticoid receptor in a hypothalamic pituitary adrenal axis model reveals bistability. Theor Biol Med Model 4:8.
27. Hayley S, Poulter MO, Merali Z, Anisman H. 2005. The pathogenesis of clinical depression: Stressor-and cytokine-induced alterations of neuroplasticity. Neuroscience 135: 659-678. (Pubitemid 41407732)
28. Hellhammer DH, Wade S. 1993. Endocrine correlates of stress vulnerability. Psychother Psychosom 60:8-17. (Pubitemid 23295473)
29. Hofer M, Pagliusi SR, Hohn A, Leibrock J, Barde Y A. 1990. Regional distribution of brain-derived neurotrophic factor mRNA in the adult mouse brain. EMBO J 9:2459-2464.
30. Huang EJ, Reichardt L F. 2001. Neurotrophins: Roles in neuronal development and function. Annu Rev Neurosci 24:677-736. (Pubitemid 32695243)
31. Jacobsen JP R, Mørk A. 2006. Chronic corticosterone decreases brain-derived neurotrophic factor (BDNF) mRNA and protein in the hippocampus, but not in the frontal cortex, of the rat. Brain Res 1110:221-225. (Pubitemid 44344611)
32. Johnson JD, Campisi J, Sharkey CM, Kennedy SL, Nickerson M, Greenwood BN, Fleshner M. 2005. Catecholamines mediate stress-induced increases in peripheral and central inflammatory cytokines. Neuroscience 135:1295-1307. (Pubitemid 41416690)
33. Kalsbeek A, vanHeerikhuize JJ, Wortel J, Buijs R M. 1996. A diurnal rhythm of stimulatory input to the hypothalamo-pituitary-adrenal system as revealed by timed intrahypothalamic administration of the vasopressin V-1 antagonist. J Neurosci 16:5555-5565. (Pubitemid 26277883)
34. Katoh-Semba R, Takeuchi IK, Inaguma Y, Ichisaka S, Hata Y, Tsumoto T, Iwai M, Mikoshiba K, Kato K. 2001. Induction of brain-derived neurotrophic factor by convulsant drugs in the rat brain: Involvement of region-specific voltage-dependent calcium channels. J Neurochem 77:71-83. (Pubitemid 32245081)
35. Kinsey SG, Bailey MT, Sheridan JF, Padgett D A. 2008. The inflammatory response to social defeat is increased in older mice. Physiol Behav 93:628-636. (Pubitemid 351208446)
36. Koolhaas JM, Korte SM, De Boer SF, Van Der Vegt BJ, Van Reenen CG, Hopster H, De Jong IC, Ruis MA W, Blokhuis H J. 1999. Coping styles in animals: Current status in behavior and stress-physiology. Neurosci Biobehav Rev 23:925-935. (Pubitemid 29502398)
37. Koolhaas JM, de Boer SF, Coppens CM, Buwalda B. 2010. Neuroendocrinology of coping styles: Towards understanding the biology of individual variation. Front Neuroendocrinol 31: 307-321.
38. Korte SM, Koolhaas JM, Wingfield JC, McEwen B S. 2005. 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. (Pubitemid 40094575)
39. Krishnan V, Han MH, Graham DL, Berton O, Renthal W, Russo SJ, LaPlant Q, Graham A, Lutter M, Lagace DC, Ghose S, Reister R, Tannous P, Green TA, Neve RL, Chakravarty S, Kumar A, Eisch AJ, Self DW, Lee FS, Tamminga CA, Cooper DC, Gershenfeld HK, Nestler E J. 2007. Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions. Cell 131:391-404. (Pubitemid 47576141)
40. Kudielka BM, Hellhammer DH, Wüst S. 2009. Why do we respond so differently? Reviewing determinants of human salivary cortisol responses to challenge. Psychoneuroendocrinology 34: 2-18.
41. Kudryavtseva NN, Bakshtanovskaya IV, Koryakina L A. 1991. Social model of depression in mice of C57BL/6J strain. Pharmacol Biochem Behav 38:315-320.
42. McEwen B S. 2008. Central effects of stress hormones in health and disease: Understanding the protective and damaging effects of stress and stress mediators. Eur J Pharmacol 583:174-185.
43. Meaney M J. 2001. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu Rev Neurosci 24:1161-1192. (Pubitemid 32695257)
44. Meerlo P, Sgoifo A, De Boer SF, Koolhaas J M. 1999. Long-lasting consequences of a social conflict in rats: Behavior during the interaction predicts subsequent changes in daily rhythms of heart rate, temperature, and activity. Behav Neurosci 113:1283-1290. (Pubitemid 30013835)
45. Miczek K A. 1979. New test for aggression in rats without aversive-stimulation: Differential effects of D-amphetamine and cocaine. Psychopharmacology 60:253-259. (Pubitemid 9147474)
46. Miller A H. 2010. Depression and immunity: A role for T cell? Brain Behav Immun 24:1-8.
47. Murakami S, Imbe H, Morikawa Y, Kubo C, Senba E. 2005. Chronic stress, as well as acute stress, reduces BDNF mRNA expression in the rat hippocampus but less robustly. Neurosci Res 53:129-139. (Pubitemid 41219528)
48. Nibuya M, Morinobu S, Duman R S. 1995. Regulation of BDNF and Trkb messenger-RNA in rat-brain by chronic electrocon-vulsive seizure and antidepressant drug treatments. J Neurosci 15:7539-7547.
49. Pang TY C, Stam NC, Nithianantharajah J, Howard ML, Hannan A J. 2006. Differential effects of voluntary physical exercise on behavioral and brain-derived neurotrophic factor expression deficits in Huntington's disease transgenic mice. Neuroscience 141:569-584. (Pubitemid 44066652)
50. Porsolt RD, Lepichon M, Jalfre M. 1977. Depression: New animal-model sensitive to antidepressant treatments. Nature 266: 730-732. (Pubitemid 8073804)
51. Raab A, Dantzer R, Michaud B, Mormede P, Taghzouti K, Simon H, Le Moal M. 1986. Behavioural, physiological and immunological consequences of social status and aggression in chronically coexisting resident-intruder dyads of male rats. Physiol Behav 36:223-228. (Pubitemid 16188261)
52. Raison CL, Miller A H. 2003. When not enough is too much: The role of insufficient glucocorticoid signaling in the pathophysiol-ogy of stress-related disorders. Am J Psychiatry 160:1554-1565. (Pubitemid 41079539)
53. Raison CL, Capuron L, Miller A H. 2006. Cytokines sing the blues: Inflammation and the pathogenesis of depression. Trends Immunol 27:24-31. (Pubitemid 43083561)
54. Rasmussen A, Shi L, Duman R S. 2002. Down-regulation of BDNF mRNA in the hippocampal dentate gyrus after re-exposure to cues previously associated with footshock. Neuropsychophar-macology 27:133-142. (Pubitemid 34686965)
55. Rygula R, Abumaria N, Flügge G, Fuchs E, Rüther E, Havemann-Reinecke U. 2005. Anhedonia and motivational deficits in rats: Impact of chronic social stress. Behav Brain Res 162:127-134. (Pubitemid 40731540)
56. Sapolsky R M. 1992. Neuroendocrinology of stress-response. In: Becker S, Bredlove S, Crews D, editors. Behavioral Endocrinology. Cambridge: MIT Press. p 287-324.
57. Schaaf MJ M, de Jong J, de Kloet ER, Vreugdenhil E. 1998. Downregulation of BDNF mRNA and protein in the rat hippocampus by corticosterone. Brain Res 813:112-120. (Pubitemid 29012524)
58. Schmidt-Kastner R, Wetmore C, OlsonL.1996. Comparative study of brain-derived neurotrophic factor messenger RNA and protein at the cellular level suggests multiple roles in hippocampus, striatum and cortex. Neuroscience 74:161-183. (Pubitemid 26291156)
59. Sorrells SF, Sapolsky R M. 2007. An inflammatory review of glucocorticoid actions in the CN S. Brain Behav Immun 21: 259-272.
60. Stefanski V. 1998. Social stress in loser rats: Opposite immunologi-cal effects in submissive and subdominant males. Physiol Behav 63:605-613. (Pubitemid 28119196)
61. Sternberg EM, Young WS, Bernardini R, Calogero AE, Chrousos GP, Gold PW, Wilder R L. 1989. A central nervous-system defect in biosynthesis of corticotropin-releasing hormone is associated with susceptibility to streptococcal cell wall-induced arthritis in Lewis rats. Proc Natl Acad Sci USA 86:4771-4775. (Pubitemid 19164631)
62. Touma C, Bunck M, Glasl L, Nussbaumer M, Palme R, Stein H, Wolf er s t ätter M, Zeh R, Zimbelmann M, Holsboer F, Landgraf R. 2008. Mice selected for high versus low stress reactivity: A new animal model for affective disorders. Psychoneuroendocrinology 33:839-862.
63. Veenema AH, Meijer OC, de Kloet ER, Koolhaas JM, Bohus B G. 2003. Differences in basal and stress-induced HPA regulation of wild house mice selected for high and low aggression. Horm Behav 43:197-204. (Pubitemid 36293290)
64. Veenema AH, Cremers TIF H, Jongsma ME, Steenbergen PJ, de Boer SF, Koolhaas J M. 2005. Differences in the effects of 5-HT(1A) receptor agonists on forced swimming behavior and brain 5-HT metabolism between low and high aggressive mice. Psychopharmacology 178:151-160. (Pubitemid 40379209)
65. Walker FR, Hinwood M, Masters LM, Deilenberg RA, Day T A. 2008. Individual differences predict susceptibility to conditioned fear arising from psychosocial trauma. J Psychiatry Res 42: 371-383. (Pubitemid 351253574)
66. Walker FR, Masters LM, Dielenberg RA, Day T A. 2009. Coping with defeat: Acute glucocorticoid and forebrain responses to social defeat vary with defeat episode behaviour. Neuroscience 162:244-253.
67. Yehuda R. 2001. Biology of posttraumatic stress disorder. J Clin Psichiatry 62:41-46. (Pubitemid 32720665)
68. Zorrilla EP, Luborsky L, McKay JR, Rosenthal R, Houldin A, Tax A, McCorkle R, Seligman DA, Schmidt K. 2001. The relationship of depression and stressors to immunological assays: A meta-analytic review. Brain Behav Immun 15:199-226. (Pubitemid 33070955)