Social defeat during adolescence and adulthood differentially induce BDNF-regulated immediate early genes

Frontiers in Behavioral Neuroscience

Volumn , Issue NOVEMBER, 2011, Pages

  Coppens, Caroline M ^a   Sipornmongcolchai, Taweeporn ^b   Wibrand, Karin ^b   Alme, Maria Nordheim ^b   Buwalda, Bauke ^a   de Boer, Sietse F ^a   Koolhaas, Jaap M ^a   Bramham, Clive R ^b  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b UNIVERSITY OF BERGEN   (Norway)

Author keywords

Adolescence; BDNF; Hippocampus; Mesocorticolimbic system; Rat; Social defeat; Stress; Synaptic plasticity

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; IMMEDIATE EARLY PROTEIN; MESSENGER RNA;

ADOLESCENCE; ADULTHOOD; AGGRESSION; ANIMAL EXPERIMENT; ANXIETY DISORDER; ARC GENE; ARTICLE; CARP GENE; CONTROLLED STUDY; COPING BEHAVIOR; DEPRESSION; GENE; GENE EXPRESSION; HIPPOCAMPUS; LATENT PERIOD; LIFE EVENT; LIFE STRESS; LONG TERM POTENTIATION; MALE; MENTAL STRESS; NERVE CELL PLASTICITY; NONHUMAN; NUCLEUS ACCUMBENS; POLYMERASE CHAIN REACTION; PREFRONTAL CORTEX; QUANTITATIVE ANALYSIS; RAT; SIGNAL TRANSDUCTION; SOCIAL DEFEAT; SOCIAL INTERACTION; SOCIAL STRESS; TIEG1 GENE; UPREGULATION;

EID: 84855324726     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2011.00072     Document Type: Article

References (69)

1. Adachi, M., Barrot, M., Autry, A. E., Theobald, D., and Monteggia, L. M. (2008). Selective loss of brainderived neurotrophic factor in the dentate gyrus attenuates antidepressant efficacy. Biol. Psychiatry 63, 642-649.
2. Aid, T., Kazantseva, A., Piirsoo, M., Palm, K., and Timmusk, T. (2007). Mouse and rat BDNF gene structure and expression revisited. J. Neurosci. Res. 85, 525-535.
3. Alme, M. N., Wibrand, K., Dagestad, G., and Bramham, C. R. (2007). Chronic fluoxetinetreatment inducesbrainregion-specific upregulation of genes associated with BDNF-induced long-term potentiation. Neural Plast. 2007, 26496.
4. Andersen, S. L. (2003). Trajectories of brain development: point of vulnerability or window of opportunity? Neurosci. Biobehav. Rev. 27, 3-18.
5. Andersen, S. L., Thompson, A. T., Rutstein, M., Hostetter, J. C., and Teicher, M. H. (2000). Dopamine receptor pruning in prefrontal cortex during the periadolescent period in rats. Synapse 37, 167-169.
6. Artola, A., Von Frijtag, J. C., Fermont, P. C., Gispen, W. H., Schrama, L. H., Kamal, A., and Spruijt, B. M. (2006). Long-lasting modulation of the induction of LTD and LTP in rat hippocampal CA1 by behavioural stress and environmental enrichment. Eur. J. Neurosci. 23, 261-272.
7. Berke, J. D., Paletzki, R. F., Aronson, G. J., Hyman, S. E., and Gerfen, C. R. (1998). A complex program of striatal gene expression induced by dopaminergic stimulation. J. Neurosci. 18, 5301-5310.
8. Bernstein, D. P., Cohen, P., Skodol, A., Bezirganian, S., and Brook, J. S. (1996). Childhood antecedents of adolescent personality disorders. Am. J. Psychiatry 153, 907-913.
9. Berton, O., Mcclung, C. A., Dileone, R. J., Krishnan, V., Renthal, W., Russo, S. J., Graham, D., Tsankova, N. M., Bolanos, C. A., Rios, M., Monteggia, L. M., Self, D. W., and Nestler, E. J. (2006). Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science 311, 864-868.
10. Björkqvist, K. (2001). Social defeat as a stressor in humans. Physiol. Behav. 73, 435-442.
11. Blair, R. J. R. (2004). The roles of orbital frontal cortex in the modulation of antisocial behavior. Brain Cogn. 55, 198-208.
12. Bramham, C. R., Alme, M. N., Bittins, M., Kuipers, S. D., Nair, R. R., Pai, B., Panja, D., Schubert, M., Soule, J., Tiron, A., and Wibrand, K. (2010). The arc of synaptic memory. Exp. Brain Res. 200, 125-140.
13. Bramham, C. R., and Messaoudi, E. (2005). BDNF function in adult synaptic plasticity: the synaptic consolidation hypothesis. Prog. Neurobiol. 76, 99-125.
14. Bramham, C. R., Worley, P. F., Moore, M. J., and Guzowski, J. F. (2008). The immediate early gene arc/arg3.1: regulation, mechanisms, and function. J. Neurosci. 28, 11760-11767.
15. Buwalda, B., Kole, M. H. P., Veenema, A. H., Huininga, M., De Boer, S. F., Korte, S. M., and 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.
16. Cressman, V. L., Balaban, J., Steinfeld, S., Shemyakin, A., Graham, P., Parisot, N., and Moore, H. (2010). Prefrontal cortical inputs to the basal amygdala undergo pruning during late adolescence in the rat. J. Comp. Neurol. 518, 2693-2709.
17. Dagestad, G., Kuipers, S. D., Messaoudi, E., and Bramham, C. R. (2006). Chronic fluoxetine induces region-specific changes in translation factor eIF4E and eEF2 activity in the rat brain. Eur. J. Neurosci. 23, 2814-2818.
18. De Boer, S., Caramaschi, D., Natarajan, D., and Koolhaas, J. (2010). The vicious cycle towards violence: focus on the negative feedback mechanisms of brain serotonin neurotransmission. Front. Behav. Neurosci.3:52. doi:10.3389/neuro.08.052.2009
19. De Boer, S. F., Van der Vegt, B. J., and Koolhaas, J. M. (2003). Individual variation in aggression of feral rodent strains: a standard for the genetics of aggression and violence? Behav. Genet. 33, 485-501.
20. De Jong, J. G., Van der Vegt, B. J., Buwalda, B., and Koolhaas, J. M. (2005). Social environment determines the long-term effects of social defeat. Physiol. Behav. 84, 87-95.
21. Duman, R. S., and Monteggia, L. M. (2006). A neurotrophic model for stress-related mood disorders. Biol. Psychiatry 59, 1116-1127.
22. Feder, A., Nestler, E. J., and Charney, D. S. (2009). Psychobiology and molecular genetics of resilience. Nat. Rev. Neurosci. 10, 446-457.
23. Feldker, D. E., Datson, N. A., Veenema, A. H., Meulmeester, E., De Kloet, E. R., and Vreugdenhil, E. (2003). Serial analysis of gene expression predicts structural differences in hippocampus of long attack latency and short attack latency mice. Eur. J. Neurosci. 17, 379-387.
24. Gelbard, H. A., Teicher, M. H., Faedda, G., and Baldessarini, R. J. (1989). Postnatal development of dopamine D1 and D2 receptor sites in rat striatum. Brain Res. Dev. Brain Res. 49, 123-130.
25. Giedd, J. N., Blumenthal, J., Jeffries, N. O., Castellanos, F. X., Liu, H., Zijdenbos, A., Paus, T., Evans, A. C., and Rapoport, J. L. (1999). Brain development during childhood and adolescence: a longitudinal MRI study. Nat. Neurosci. 2, 861-863.
26. Greenberg, M. E., Xu, B., Lu, B., and Hempstead, B. L. (2009). New insights in the biology of BDNF synthesis and release: implications in CNS function. J. Neurosci. 29, 12764-12767.
27. Grønli, J., Bramham, C., Murison, R., Kanhema, T., Fiske, E., Bjorvatn, B., Ursin, R., and Portas, C. M. (2006). Chronic mild stress inhibits BDNF protein expression and CREB activation in the dentate gyrus but not in the hippocampus proper. Pharmacol. Biochem. Behav. 85, 842-849.
28. Hankin, B. L., Abramson, L. Y., Moffitt, T. E., Silva, P. A., Mcgee, R., and Angell, K. E. (1998). Development of depression from preadolescence to young adulthood: emerging gender differences in a 10-year longitudinal study. J. Abnorm. Psychol. 107, 128-140.
29. Ito, W., Chehab, M., Thakur, S., Li, J., and Morozov, A. (2011). BDNFrestricted knockout mice as an animal model for aggression. Genes Brain Behav. 10, 365-374.
30. Johnsen, S. A., Subramaniam, M., Katagiri, T., Janknecht, R., and Spelsberg, T. C. (2002). Transcriptional regulation of Smad2 is required for enhancement of TGFbeta/Smad signaling by TGFbeta inducible early gene. J. Cell. Biochem. 87, 233-241.
31. Kalsbeek, A., Voorn, P., Buijs, R. M., Pool, C. W., and Uylings, H. B. (1988). Development of the dopaminergic innervation in the prefrontal cortex of the rat. J. Comp. Neurol. 269, 58-72.
32. Kole, M. H. P., Costoli, T., Koolhaas, J. M., and Fuchs, E. (2004). Bidirectional shift in the cornuammonis 3 pyramidal dendritic organization following brief stress. Neuroscience 125, 337-347.
33. Koolhaas, J. M., De Boer, S. F., Coppens, C. M., and Buwalda, B. (2010). Neuroendocrinology of coping styles: towards understanding the biology of individual variation. Front. Neuroendocrinol. 31:307-321.
34. Koolhaas, J. M., Korte, S. M., De Boer, S. F., Van Der Vegt, B. J., Van Reenen, C. G., Hopster, H., De Jong, I. C., Ruis, M. A. W., and Blokhuis, H. J. (1999). Coping styles in animals: current status in behavior and stressphysiology. Neurosci. Biobehav. Rev. 23, 925-935.
35. Krishnan, V., Han, M.-H., Graham, D. L., Berton, O., Renthal, W., Russo, S. J., Laplant, Q., Graham, A., Lutter, M., Lagace, D. C., Ghose, S., Reister, R., Tannous, P., Green, T. A., Neve, R. L., Chakravarty, S., Kumar, A., Eisch, A. J., Self, D. W., Lee, F. S., Tamminga, C. A., Cooper, D. C., Gershenfeld, H. K., and Nestler, E. J. (2007). Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions. Cell 131, 391-404.
36. Landsheer, J. A., and Hart, H. (1999). Age and adolescent delinquency the changing relationship among age, delinquent attitude, and delinquent activity. Crim. Justice Behav. 26, 373-388.
37. Lauterborn, J. C., Rivera, S., Stinis, C. T., Hayes, V. Y., Isackson, P. J., and Gall, C. M. (1996). Differential effects of protein synthesis inhibition on the activity-dependent expression of BDNF transcripts: evidence for immediate-early gene responses from specific promoters. J. Neurosci. 16, 7428-7436.
38. Leslie, C. A., Robertson, M. W., Cutler, A. J., and Bennett, J. P. Jr. (1991). Postnatal development of D1 dopamine receptors in the medial prefrontal cortex, striatum and nucleus accumbens of normal and neonatal 6-hydroxydopamine treated rats: a quantitative autoradiographic analysis. Brain Res. Dev. Brain Res. 62, 109-114.
39. McCurry, C. L., Shepherd, J. D., Tropea, D., Wang, K. H., Bear, M. F., and Sur, M. (2010). Loss of Arc renders the visual cortex impervious to the effects of sensory experience or deprivation. Nat. Neurosci. 13, 450-457.
40. Meerlo, P., Overkamp, G. J., Daan, S., Van Den Hoofdakker, R. H., and Koolhaas, J. M. (1996). Changes in behaviour and body weight following a single or double social defeat in rats. Stress 1, 21-32.
41. Meerlo, P., Sgoifo, A., De Boer, S. F., and 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.
42. Messaoudi, E., Kanhema, T., Soule, J., Tiron, A., Dagyte, G., Da Silva, B., and Bramham, C. R. (2007). Sustained Arc/Arg3.1 synthesis controls long-term potentiation consolidation through regulation of local actin polymerization in the dentate gyrus in vivo. J. Neurosci. 27, 10445-10455.
43. Mikkelsen, J. D., and Larsen, M. H. (2006). Effects of stress and adrenalectomy on activity-regulated cytoskeleton protein (Arc) gene expression. Neurosci. Lett. 403, 239-243.
44. Miller, E. K. (2000). The prefrontal cortex and cognitive control. Nat. Rev. Neurosci. 1, 59-65.
45. Miller, E. K., and Cohen, J. D. (2001). An integrative theory of prefrontal cortex function. Annu. Rev. Neurosci. 24, 167-202.
46. Minichiello, L. (2009). TrkB signalling pathways in LTP and learning. Nat. Rev. Neurosci. 10, 850-860.
47. Ons, S., Marti, O., and Armario, A. (2004). Stress-induced activation of the immediate early gene Arc (activity-regulated cytoskeletonassociated protein) is restricted to telencephalic areas in the rat brain: relationship to c-fos mRNA. J. Neurochem. 89, 1111-1118.
48. Ons, S., Rotllant, D., Marin-Blasco, I. J., and Armario, A. (2010). Immediateearly gene response to repeated immobilization: Fos protein and arc mRNA levels appear to be less sensitive than c-fos mRNA to adaptation. Eur. J. Neurosci. 31, 2043-2052.
49. Quirk, G. J., and Beer, J. S. (2006). Prefrontal involvement in the regulation of emotion: convergence of rat and human studies. Curr. Opin. Neurobiol. 16, 723-727.
50. Rantamaki, T., Hendolin, P., Kankaanpaa, A., Mijatovic, J., Piepponen, P., Domenici, E., Chao, M. V., Mannisto, P. T., and Castren, E. (2007). Pharmacologically diverse antidepressants rapidly activate brainderived neurotrophic factor receptor TrkB and induce phospholipaseCgamma signaling pathways in mouse brain. Neuropsychopharmacology 32, 2152-2162.
51. Rial Verde, E. M., Lee-Osbourne, J., Worley, P. F., Malinow, R., and Cline, H. T. (2006). Increased expression of the immediate-early gene arc/arg3.1 reduces AMPA receptor-mediated synaptic transmission. Neuron 52, 461-474.
52. Romeo, R. D., and McEwen, B. S. (2006). Stress and the adolescent brain. Ann. N. Y. Acad. Sci. 1094, 202-214.
53. Ruis, M. A., Te Brake, J. H., Buwalda, B., De Boer, S. F., Meerlo, P., Korte, S. M., Blokhuis, H. J., and Koolhaas, J. M. (1999). Housing familiar male wildtype rats together reduces the longterm adverse behavioural and physiological effects of social defeat. Psychoneuroendocrinology 24, 285-300.
54. Shepherd, J. D., Rumbaugh, G., Wu, J., Chowdhury, S., Plath, N., Kuhl, D., Huganir, R. L., and Worley, P. F. (2006). Arc/Arg3.1 mediates homeostatic synaptic scaling of AMPA receptors. Neuron 52, 475-484.
55. Siever, L. J. (2008). Neurobiology of aggression and violence. Am. J. Psychiatry 165, 429-442.
56. Sluyter, F., Jamot, L., Van Oortmerssen, G. A., and Crusio, W. E. (1994). Hippocampal mossy fiber distributions in mice selected for aggression. Brain Res. 646, 145-148.
57. Smith, M. A., Makino, S., Kvetnansky, R., and Post, R. M. (1995). Stress and glucocorticoids affect the expression of brain-derived neurotrophic factor and neurotrophin-3 mRNAs in the hippocampus. J. Neurosci. 15, 1768-1777.
58. Subramaniam, M., Harris, S. A., Oursler, M. J., Rasmussen, K., Riggs, B. L., and Spelsberg, T. C. (1995). Identification of a novel TGF-beta-regulated gene encoding a putative zinc finger protein in human osteoblasts. Nucleic Acids Res. 23, 4907-4912.
59. Suske, G., Bruford, E., and Philipsen, S. (2005). Mammalian SP/KLF transcription factors: bring in the family. Genomics 85, 551-556.
60. Taliaz, D., Loya, A., Gersner, R., Haramati, S., Chen, A., and Zangen, A. (2011). Resilience to chronic stress is mediated by hippocampal brainderived neurotrophic factor. J. Neurosci. 31, 4475-4483.
61. Tarazi, F. I., Tomasini, E. C., and Baldessarini, R. J. (1998). Postnatal development of dopamine D4-like receptors in rat forebrain regions: comparison with D2-like receptors. Brain Res. Dev. Brain Res. 110, 227-233.
62. Tarazi, F. I., Tomasini, E. C., and Baldessarini, R. J. (1999). Postnatal development of dopamine D1-like receptors in rat cortical and striatolimbic brain regions: an autoradiographic study. Dev. Neurosci. 21, 43-49.
63. Teicher, M. H., Andersen, S. L., and Hostetter, J. C. Jr. (1995). Evidence for dopamine receptor pruning between adolescence and adulthood in striatum but not nucleus accumbens. Brain Res. Dev. Brain Res. 89, 167-172.
64. Tornatzky, W., and Miczek, K. A. (1994). Behavioral and autonomic responses to intermittent social stress: differential protection by clonidine and metoprolol. Psychopharmacology (Berl.) 116, 346-356.
65. Toth, E., Gersner, R., Wilf-Yarkoni, A., Raizel, H., Dar, D. E., Richter-Levin, G., Levit, O., and Zangen, A. (2008). Age-dependent effects of chronic stress on brain plasticity and depressive behavior. J. Neurochem. 107, 522-532.
66. Veenema, A. H., and Neumann, I. D. (2007). Neurobiological mechanisms of aggression and stress coping: a comparative study in mouse and rat selection lines. Brain Behav. Evol. 70, 274-285.
67. Waung, M. W., Pfeiffer, B. E., Nosyreva, E. D., Ronesi, J. A., and Huber, K. M. (2008). Rapid translation of Arc/Arg3.1 selectively mediates mGluR-dependent LTD through persistent increases in AMPAR endocytosis rate. Neuron 59, 84-97.
68. WHO International Consortium in Psychiatric Epidemiology. (2000). Cross-national comparisons of the prevalences and correlates of mental disorders. Bull. World Health Organ. 78, 413-426.
69. Wibrand, K., Messaoudi, E., Havik, B., Steenslid, V., Lovlie, R., Steen, V. M., and Bramham, C. R. (2006). Identification of genes co-upregulated with Arc during BDNF-induced longterm potentiation in adult rat dentate gyrus in vivo. Eur. J. Neurosci. 23, 1501-1511.