Social defeat stress induces a depression-like phenotype in adolescent male c57BL/6 mice

Stress

Volumn 17, Issue 3, 2014, Pages 247-255

  Iñiguez, Sergio D ^a   Riggs, Lace M ^a   Nieto, Steven J ^a   Dayrit, Genesis ^a   Zamora, Norma N ^a   Shawhan, Kristi L ^a   Cruz, Bryan ^a   Warren, Brandon L ^b  

^a CALIFORNIA STATE UNIVERSITY   (United States)

^b NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

Author keywords

Anhedonia; Animal model; Anxiety; Bullying; Depression; Forced swim test; Juvenile; Mood disorders

Indexed keywords

CORTICOSTERONE; CARBOHYDRATE DIET; SUCROSE;

ADOLESCENT; ADULT; ANIMAL EXPERIMENT; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; DEPRESSION; FORCED SWIM TEST; IMMUNOASSAY; LATENT PERIOD; LOCOMOTION; MALE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SOCIAL BEHAVIOR; SOCIAL DEFEAT STRESS; SOCIAL INTERACTION; SOCIAL INTERACTION TEST; SOCIAL STRESS; WEIGHT CHANGE; WEIGHT GAIN; ADMINISTRATION AND DOSAGE; AGING; ANIMAL; ANXIETY; BLOOD; C57BL MOUSE; CARBOHYDRATE DIET; DEPRESSIVE DISORDER; ETIOLOGY; FOOD PREFERENCE; HUMAN RELATION; SOCIAL DOMINANCE; SWIMMING;

AGING; ANIMALS; ANXIETY; CORTICOSTERONE; DEPRESSION; DEPRESSIVE DISORDER; DIETARY CARBOHYDRATES; DOMINANCE-SUBORDINATION; FOOD PREFERENCES; INTERPERSONAL RELATIONS; MALE; MICE, INBRED C57BL; PHENOTYPE; SUCROSE; SWIMMING;

EID: 84899030471     PISSN: 10253890     EISSN: 16078888     Source Type: Journal    
DOI: 10.3109/10253890.2014.910650     Document Type: Article

References (56)

1. APA. (2000). Diagnostic and Statistical Manual of Mental Disorders. DSM-IV Edition. Washington, DC: American Psychiatric Association.
2. Axelson DA, Birmaher B. (2001). Relation between anxiety and depressive disorders in childhood and adolescence. Depress Anxiety 14:67-78. (Pubitemid 32937480)
3. Backström T, Winberg S. (2013). Central corticotropin releasing factor and social stress. Front Neurosci 7:117. doi: 10.3389/ fnins.2013.00117.
4. Berton O, McClung CA, Dileone RJ, Krishnan V, Renthal W, Russo SJ, Graham D, et al. (2006). Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science 311:864-8. (Pubitemid 43228853)
5. Beuke CJ, Fischer R, McDowall J. (2003). Anxiety and depression: why and how to measure their separate effects. Clin Psychol Rev 23: 831-48. (Pubitemid 37188651)
6. Burke KC, Burke Jr JD, Regier DA, Rae DS. (1990). Age at onset of selected mental disorders in five community populations. Arch Gen Psychiatry 47:511-18. (Pubitemid 20189962)
7. Buwalda B, Stubbendorff C, Zickert N, Koolhaas JM. (2013). Adolescent social stress does not necessarily lead to a compromised adaptive capacity during adulthood: a study on the consequences of social stress in rats. Neuroscience 249:258-70.
8. Buwalda B, de Boer SF, Schmidt ED, Felszeghy K, Nyakas C, Sgoifo A, Van der Vegt BJ, et al. (1999). Long-lasting deficient dexamethasone suppression of hypothalamic-pituitary-adrenocortical activation following peripheral CRF challenge in socially defeated rats. J Neuroendocrinol 11:513-20. (Pubitemid 29312844)
9. Charney DS, Manji HK. (2004). Life stress, genes, and depression: multiple pathways lead to increased risk and new opportunities for intervention. Sci STKE 225:re5. doi: 10.1126/stke.2252004re5.
10. Das-Munshi J, Goldberg D, Bebbington PE, Bhugra DK, Brugha TS, Dewey ME, Jenkins R, et al. (2008). Public health significance of mixed anxiety and depression: beyond current classification. Br J Psychiatry 192:171-7. (Pubitemid 351347374)
11. Doremus-Fitzwater TL, Varlinskaya EI, Spear LP. (2010). Motivational systems in adolescence: possible implications for age differences in substance abuse and other risk-taking behaviors. Brain Cogn 72: 114-23.
12. Eiland L, Romeo RD. (2013). Stress and the developing adolescent brain. Neuroscience 249:162-71.
13. Eisch AJ, Bolaños CA, de Wit J, Simonak RD, Pudiak CM, Barrot M, Verhaagen J, Nestler EJ. (2003). Brain-derived neurotrophic factor in the ventral midbrain-nucleus accumbens pathway: a role in depression. Biol Psychiatry 54:994-1005. (Pubitemid 37415034)
14. Findling RL, McNamara NK, Stansbrey RJ, Feeny NC, Young CM, Peric FV, Youngstrom EA. (2006). The relevance of pharmacokinetic studies in designing efficacy trials in juvenile major depression. J Child Adolesc Psychopharmacol 16:131-45.
15. Gladstone GL, Parker GB, Malhi GS. (2006). Do bullied children become anxious and depressed adults?: a cross-sectional investigation of the correlates of bullying and anxious depression. J Nerv Ment Dis 194:201-8.
16. Golden SA, Covington 3rd HE, Berton O, Russo SJ. (2011). A standardized protocol for repeated social defeat stress in mice. Nat Protoc 6:1183-91.
17. Hankin BL, Abramson LY, Moffitt TE, Silva PA, McGee R, Angell KE. (1998). Development of depression from preadolescence to young adulthood: emerging gender differences in a 10-year longitudinal study. J Abnorm Psychol 107:128-40. (Pubitemid 28102960)
18. Heinrichs SC, Koob GF. (2006). Application of experimental stressors in laboratory rodents. Curr Protoc Neurosci Chapter 8: Unit8.4.
19. Huang GB, Zhao T, Muna SS, Bagalkot TR, Jin HM, Chae HJ, Chung YC. (2013). Effects of chronic social defeat stress on behaviour, endoplasmic reticulum proteins and choline acetyltransferase in adolescent mice. Int J Neuropsychopharmacol 16: 1635-47.
20. Iñiguez SD, Warren BL, Bolaños-Guzmán CA. (2010a). Short- and longterm functional consequences of fluoxetine exposure during adolescence in male rats. Biol Psychiatry 67:1057-66.
21. Iñiguez SD, Warren BL, Parise EM, Alcantara LF, Schuh B, Maffeo ML, Manojlovic Z, Bolaños-Guzmán CA. (2009). Nicotine exposure during adolescence induces a depression-like state in adulthood. Neuropsychopharmacology 34:1609-24.
22. Iñiguez SD, Vialou V, Warren BL, Cao JL, Alcantara LF, Davis LC, Manojlovic Z, et al. (2010b). Extracellular signal-regulated kinase-2 within the ventral tegmental area regulates responses to stress. J Neurosci 30:7652-63.
23. Iñiguez SD, Alcantara LF, Warren BL, Riggs LM, Parise EM, Vialou V, Wright KN, et al. (2014). Fluoxetine exposure during adolescence alters responses to aversive stimuli in adulthood. J Neurosci 34: 1007-21.
24. Jiang C, Salton SR. (2013). The role of neurotrophins in major depressive disorder. Transl Neurosci 4:46-58.
25. Kessler RC, Avenevoli S, Ries Merikangas K. (2001). Mood disorders in children and adolescents: an epidemiologic perspective. Biol Psychiatry 49:1002-14.
26. Krishnan V, Nestler EJ. (2008). The molecular neurobiology of depression. Nature 455:894-902.
27. Krishnan V, Nestler EJ. (2011). Animal models of depression: molecular perspectives. Curr Top Behav Neurosci 7:121-47.
28. Krishnan V, Han MH, Mazei-Robison M, Iñiguez SD, Ables JL, Vialou V, Berton O, et al. (2008). AKT signaling within the ventral tegmental area regulates cellular and behavioral responses to stressful stimuli. Biol Psychiatry 64:691-700.
29. Krishnan V, Han MH, Graham DL, Berton O, Renthal W, Russo SJ, Laplant Q, et al. (2007). Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions. Cell 131: 391-404. (Pubitemid 47576141)
30. Kudryavtseva NN, Bakshtanovskaya IV, Koryakina LA. (1991). Social model of depression in mice of C57BL/6J strain. Pharmacol Biochem Behav 38:315-20.
31. Kupfer DJ, Frank E, Phillips ML. (2012). Major depressive disorder: new clinical, neurobiological, and treatment perspectives. Lancet 379: 1045-55.
32. Laviola G, Macri S, Adriani W, Morley Fletcher S. (2002). Psychobiological determinants of risk behavior in adolescence. Ann Ist Super Sanita 38:279-87.
33. Lewinsohn PM, Hops H, Roberts RE, Seeley JR, Andrews JA. (1993). Adolescent psychophathology: I. Prevalence and incidence of depression and other DSM-III-R disorders in high school students. J Abnorm Psychol 102:133-44. (Pubitemid 23089571)
34. Malkesman O, Weller A. (2009). Two different putative genetic animal models of childhood depression - a review. Prog Neurobiol 88: 153-69.
35. McCormick CM, Mathews IZ, Thomas C, Waters P. (2010). Investigations of HPA function and the enduring consequences of stressors in adolescence in animal models. Brain Cogn 72:73-85.
36. Miczek KA. (1979). A new test for aggression in rats without aversive stimulation: differential effects of d-amphetamine and cocaine. Psychopharmacology (Berl) 60:253-9. (Pubitemid 9147474)
37. Montgomery KC. (1955). The relation between fear induced by novel stimulation and exploratory behavior. J Comp Physiol Psychol 48: 254-60.
38. Niwa M, Jaaro-Peled H, Tankou S, Seshadri S, Hikida T, Matsumoto Y, Cascella NG, et al. (2013). Adolescent stress-induced epigenetic control of dopaminergic neurons via glucocorticoids. Science 339: 335-9.
39. Papp M, Willner P, Muscat R. (1991). An animal model of anhedonia: attenuation of sucrose consumption and place preference conditioning by chronic unpredictable mild stress. Psychopharmacology (Berl) 104: 255-9.
40. Parmigiani S, Palanza P, Rogers J, Ferrari PF. (1999). Selection, evolution of behavior and animal models in behavioral neuroscience. Neurosci Biobehav Rev 23:957-69.
41. Paus T, Keshavan M, Giedd JN. (2008). Why do many psychiatric disorders emerge during adolescence? Nat Rev Neurosci 9:947-57.
42. 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. (Pubitemid 16239568)
43. Porsolt RD, Le Pichon M, Jalfre M. (1977). Depression: a new animal model sensitive to antidepressant treatments. Nature 266:730-2. (Pubitemid 8073804)
44. Richards JM, Plate RC, Ernst M. (2012). Neural systems underlying motivated behavior in adolescence: implications for preventative medicine. Prev Med 55:s7-16.
45. Spear LP. (2000). The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 24:417-63. (Pubitemid 30243061)
46. Stone EA, Quartermain D. (1997). Greater behavioral effects of stress in immature as compared to mature male mice. Physiol Behav 63:143-5. (Pubitemid 27499955)
47. Tirelli E, Laviola G, Adriani W. (2003). Ontogenesis of behavioral sensitization and conditioned place preference induced by psychostimulants in laboratory rodents. Neurosci Biobehav Rev 27:163-78. (Pubitemid 36535398)
48. Trainor BC, Pride MC, Villalon Landeros R, Knoblauch NW, Takahashi EY, Silva AL, Crean KK. (2011). Sex differences in social interaction behavior following social defeat stress in the monogamous California mouse (Peromyscus californicus). PLoS One 6:e17405.
49. Tsoory M, Cohen H, Richter-Levin G. (2007). Juvenile stress induces a predisposition to either anxiety or depressive-like symptoms following stress in adulthood. Eur Neuropsychopharmacol 17:245-56. (Pubitemid 46135931)
50. Ver Hoeve ES, Kelly G, Luz S, Ghanshani S, Bhatnagar S. (2013). Shortterm and long-term effects of repeated social defeat during adolescence or adulthood in female rats. Neuroscience 249:63-73.
51. Wals M, Verhulst F. (2005). Child and adolescent antecedents of adult mood disorders. Curr Opin Psychiatry 18:15-19. (Pubitemid 40332013)
52. Warren BL, Iñiguez SD, Alcantara LF, Wright KN, Parise EM, Weakley SK, Bolaños-Guzmán CA. (2011). Juvenile administration of concomitant methylphenidate and fluoxetine alters behavioral reactivity to reward- and mood-related stimuli and disrupts ventral tegmental area gene expression in adulthood. J Neurosci 31:10347-58.
53. Warren BL, Vialou VF, Iñiguez SD, Alcantara LF, Wright KN, Feng J, Kennedy PJ, et al. (2013). Neurobiological sequelae of witnessing stressful events in adult mice. Biol Psychiatry 73:7-14.
54. Watt MJ, Burke AR, Renner KJ, Forster GL. (2009). Adolescent male rats exposed to social defeat exhibit altered anxiety behavior and limbic monoamines as adults. Behav Neurosci 123:564-76.
55. Willner P, Towell A, Sampson D, Sophokleous S, Muscat R. (1987). Reduction of sucrose preference by chronic unpredictable mild stress, and its restoration by a tricyclic antidepressant. Psychopharmacology (Berl) 93:358-64. (Pubitemid 17160661)
56. Zito JM, Tobi H, de Jong-van den Berg LT, Fegert JM, Safer DJ, Janhsen K, Hansen DG, et al. (2006). Antidepressant prevalence for youths: a multi-national comparison. Pharmacoepidemiol Drug Saf 15:793-8. (Pubitemid 44762710)