Chronic mild stress inhibits BDNF protein expression and CREB activation in the dentate gyrus but not in the hippocampus proper

Pharmacology Biochemistry and Behavior

Volumn 85, Issue 4, 2006, Pages 842-849

  Grønli, Janne ^a,b   Bramham, Clive ^a   Murison, Robert ^a   Kanhema, Tambudzai ^a   Fiske, Eldbjørg ^a   Bjorvatn, Bjørn ^a,b   Ursin, Reidun ^a,b   Portas, Chiara M ^a,b  

^a UNIVERSITY OF BERGEN   (Norway)

^b HAUKELAND UNIVERSITY HOSPITAL   (Norway)

Author keywords

Anhedonia; Animal model of depression; CMS; Neurotrophins; Sucrose intake

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; SUCROSE;

ANHEDONIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARBOHYDRATE INTAKE; CHRONIC STRESS; CONTROLLED STUDY; DENTATE GYRUS; DEPRESSION; DISEASE MODEL; DOWN REGULATION; HIPPOCAMPUS; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RAT; SYMPTOM;

ANIMALS; APPETITE REGULATION; BRAIN-DERIVED NEUROTROPHIC FACTOR; CHRONIC DISEASE; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DENTATE GYRUS; HIPPOCAMPUS; MALE; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; STRESS, PSYCHOLOGICAL; SUCROSE;

ANIMALIA; RATTUS;

EID: 33846433505     PISSN: 00913057     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbb.2006.11.021     Document Type: Article

References (83)

1. Alfonso J., Frick L.R., Silberman D.M., Palumbo M.L., Genaro A.M., and Frasch A.C. Regulation of hippocampal gene expression is conserved in two species subjected to different stressors and antidepressant treatments. Biol Psychiatry 59 3 (2006) 244-251
2. Alonso R, Griebel G, Pavone G, Stemmelin J, Le Fur G, Soubrie P. Blockade of CRF(1) or V(1b) receptors reverses stress-induced suppression of neurogenesis in a mouse model of depression. Mol Psychiatry 2004;9(3): 278-86, 24.
3. Altar C.A. Neurotrophins and depression. Trends Pharmacol Sci 20 2 (1999) 59-61
4. Altman J., and Bayer S.A. Mosaic organization of the hippocampal neuroepithelium and the multiple germinal sources of dentate granule cells. J Comp Neurol 301 3 (1990) 325-342
5. Altman J., and Das G.D. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124 3 (1965) 319-335
6. Angelucci F., Aloe L., Vasquez P.J., and Mathe A.A. Mapping the differences in the brain concentration of brain-derived neurotrophic factor (BDNF) and nerve growth factor (NGF) in an animal model of depression. Neuroreport 11 6 (2000) 1369-1373
7. Angelucci F., Aloe L., Jimenez-Vasquez P., and Mathe A.A. Electroconvulsive stimuli alter nerve growth factor but not brain-derived neurotrophic factor concentrations in brains of a rat model of depression. Neuropeptides 37 1 (2003) 51-56
8. Badia-Elder N., Kiefer S.W., and Dess N.K. Taste reactivity in rats selectively bred for high vs. low saccharin consumption. Physiol Behav 59 4-5 (1996) 749-755
9. Baker S.L., Kentner A.C., Konkle A.T., Santa-Maria Barbagallo L., and Bielajew C. Behavioral and physiological effects of chronic mild stress in female rats. Physiol Behav 87 2 (2006) 314-322
10. Bartesaghi R. Effect of early isolation on the synaptic function in the dentate gyrus and field CA1 of the guinea pig. Hippocampus 14 4 (2004) 482-498
11. Becker S. A computational principle for hippocampal learning and neurogenesis. Hippocampus 15 6 (2005) 722-738
12. Benca R.M. Sleep in psychiatric disorders. Neurol Clin 14 4 (1996) 739-764
13. Benelli A., Filaferro M., Bertolini A., and Genedani S. Influence of S-adenosyl-l-methionine on chronic mild stress-induced anhedonia in castrated rats. Br J Pharmacol 127 3 (1999) 645-654
14. Berntson G.G., Sarter M., and Cacioppo J.T. Ascending visceral regulation of cortical affective information processing. Eur J Neurosci 18 8 (2003) 2103-2109
15. Blum R., and Konnerth A. Neurotrophin-mediated rapid signaling in the central nervous system: mechanisms and functions. Physiology (Bethesda) 20 (2005) 70-78
16. Bramham C.R., and Messaoudi E. BDNF function in adult synaptic plasticity: the synaptic consolidation hypothesis. Prog Neurobiol 76 2 (2005) 99-125
17. Castren E. Is mood chemistry?. Nat Rev Neurosci 6 3 (2005) 241-246
18. Chen A.C., Shirayama Y., Shin K.H., Neve R.L., and Duman R.S. Expression of the cAMP response element binding protein (CREB) in hippocampus produces an antidepressant effect. Biol Psychiatry 49 9 (2001) 753-762
19. Chen B., Dowlatshahi D., MacQueen G.M., Wang J.F., and Young L.T. Increased hippocampal BDNF immunoreactivity in subjects treated with antidepressant medication. Biol Psychiatry 50 4 (2001) 260-265
20. Collier T.J., and Routtenberg A. Electrical self-stimulation of dentate gyrus granule cells. Behav Neural Biol 42 1 (1984) 85-90
21. Conner J.M., Lauterborn J.C., Yan Q., Gall C.M., and Varon S. Distribution of brain-derived neurotrophic factor (BDNF) protein and mRNA in the normal adult rat CNS: evidence for anterograde axonal transport. J Neurosci 17 7 (1997) 2295-2313
22. Conti A.C., Cryan J.F., Dalvi A., Lucki I., and Blendy J.A. cAMP response element-binding protein is essential for the upregulation of brain-derived neurotrophic factor transcription, but not the behavioral or endocrine responses to antidepressant drugs. J Neurosci 22 8 (2002) 3262-3268
23. Dowlatshahi D., MacQueen G.M., Wang J.F., and Young L.T. Increased temporal cortex CREB concentrations and antidepressant treatment in major depression. Lancet 352 9142 (1998) 1754-1755
24. Duman R.S. Synaptic plasticity and mood disorders. Mol Psychiatry 7 Suppl 1 (2002) S29-S34
25. Duman R.S., Heninger G.R., and Nestler E.J. Molecular psychiatry. Adaptations of receptor-coupled signal transduction pathways underlying stress- and drug-induced neural plasticity. J Nerv Ment Dis 182 12 (1994) 692-700
26. Duman R.S., Heninger G.R., and Nestler E.J. A molecular and cellular theory of depression. Arch Gen Psychiatry 54 7 (1997) 597-606
27. Finkbeiner S., Tavazoie S.F., Maloratsky A., Jacobs K.M., Harris K.M., and Greenberg M.E. CREB: a major mediator of neuronal neurotrophin responses. Neuron 19 5 (1997) 1031-1047
28. Forbes N.F., Stewart C.A., Matthews K., and Reid I.C. Chronic mild stress and sucrose consumption: validity as a model of depression. Physiol Behav 60 6 (1996) 1481-1484
29. Franklin T.B., and Perrot-Sinal T.S. Sex and ovarian steroids modulate brain-derived neurotrophic factor (BDNF) protein levels in rat hippocampus under stressful and non-stressful conditions. Psychoneuroendocrinology 31 1 (2006) 38-48
30. Golarai G., and Sutula T.P. Bilateral organization of parallel and serial pathways in the dentate gyrus demonstrated by current-source density analysis in the rat. J Neurophysiol 75 1 (1996) 329-342
31. Grewal S.S., York R.D., and Stork P.J. Extracellular-signal-regulated kinase signalling in neurons. Curr Opin Neurobiol 9 5 (1999) 544-553
32. Gronli J., Murison R., Bjorvatn B., Sorensen E., Portas C.M., and Ursin R. Chronic mild stress affects sucrose intake and sleep in rats. Behav Brain Res 150 1-2 (2004) 139-147
33. Gronli J., Murison R., Fiske E., Bjorvatn B., Sorensen E., Portas C.M., et al. Effects of chronic mild stress on sexual behavior, locomotor activity and consumption of sucrose and saccharine solutions. Physiol Behav 84 4 (2005) 571-577
34. Gronli J, Murison R, Fiske E, Bjorvatn B, Sorensen E, Portas CM, et al. Extracellular levels of Serotonin and GABA in the hippocampus of CMS treated rats. A microdialysis study in an animal model of depression. submitted for publication.
35. Haidkind R., Eller M., Harro M., Kask A., Rinken A., Oreland L., et al. Effects of partial locus coeruleus denervation and chronic mild stress on behaviour and monoamine neurochemistry in the rat. Eur Neuropsychopharmacol 13 1 (2003) 19-28
36. Hashimoto K., Shimizu E., and Iyo M. Critical role of brain-derived neurotrophic factor in mood disorders. Brain Res Brain Res Rev 45 2 (2004) 104-114
37. Herman J.P., and Cullinan W.E. Neurocircuitry of stress: central control of the hypothalamo-pituitary-adrenocortical axis. Trends Neurosci 20 2 (1997) 78-84
38. Hillegaart V., and Ahlenius S. Time course for synchronization of spontaneous locomotor activity in the rat following reversal of the daylight (12:12 h) cycle. Physiol Behav 55 1 (1994) 73-75
39. Ho Y.J., Chang Y.C., Liu T.M., Tai M.Y., Wong C.S., and Tsai Y.F. Striatal glutamate release during novelty exposure-induced hyperactivity in olfactory bulbectomized rats. Neurosci Lett 287 2 (2000) 117-120
40. Jaako-Movits K., and Zharkovsky A. Impaired fear memory and decreased hippocampal neurogenesis following olfactory bulbectomy in rats. Eur J Neurosci 22 11 (2005) 2871-2878
41. Jacobsen J.P., and Mork A. The effect of escitalopram, desipramine, electroconvulsive seizures and lithium on brain-derived neurotrophic factor mRNA and protein expression in the rat brain and the correlation to 5-HT and 5-HIAA levels. Brain Res 1024 1-2 (2004) 183-192
42. Jayatissa M.N., Bisgaard C., Tingstrom A., Papp M., and Wiborg O. Hippocampal cytogenesis correlates to escitalopram-mediated recovery in a chronic mild stress rat model of depression. Neuropsychopharmacology 31 11 (2006) 2395-2404 [Nov]
43. Karege F., Perret G., Bondolfi G., Schwald M., Bertschy G., and Aubry J.M. Decreased serum brain-derived neurotrophic factor levels in major depressed patients. Psychiatry Res 109 2 (2002) 143-148
44. Kesner R.P., Lee I., and Gilbert P. A behavioral assessment of hippocampal function based on a subregional analysis. Rev Neurosci 15 5 (2004) 333-351
45. Kirschenbaum B., and Goldman S.A. Brain-derived neurotrophic factor promotes the survival of neurons arising from the adult rat forebrain subependymal zone. Proc Natl Acad Sci U S A 92 1 (1995) 210-214
46. Kuipers S.D., and Bramham C.R. Brain-derived neurotrophic factor mechanisms and function in adult synaptic plasticity: new insights and implications for therapy. Curr Opin Drug Discov Devel 9 5 (2006) 580-586
47. Kuroda Y., and McEwen B.S. Effect of chronic restraint stress and tianeptine on growth factors, growth-associated protein-43 and microtubule-associated protein 2 mRNA expression in the rat hippocampus. Brain Res Mol Brain Res 59 1 (1998) 35-39
48. Lang U.E., Hellweg R., and Gallinat J. BDNF serum concentrations in healthy volunteers are associated with depression-related personality traits. Neuropsychopharmacology 29 4 (2004) 795-798
49. Lee K.S., Lim B.V., Chang H.K., Yang H.Y., Bahn G.H., Paik E.K., et al. Liuweidihuang-tang improves spatial memory function and increases neurogenesis in the dentate gyrus in rats. Fitoterapia 76 6 (2005) 514-519
50. Lesch K.P., and Manji H.K. Signal-transducing G proteins and antidepressant drugs: evidence for modulation of alpha subunit gene expression in rat brain. Biol Psychiatry 32 7 (1992) 549-579
51. Lewin G.R., and Barde Y.A. Physiology of the neurotrophins. Annu Rev Neurosci 19 (1996) 289-317
52. Lisman J.E., and Grace A.A. The hippocampal-VTA loop: controlling the entry of information into long-term memory. Neuron 46 5 (2005) 703-713
53. Matthews K., Forbes N., and Reid I.C. Sucrose consumption as an hedonic measure following chronic unpredictable mild stress. Physiol Behav 57 2 (1995) 241-248
54. Montminy M.R., Gonzalez G.A., and Yamamoto K.K. Regulation of cAMP-inducible genes by CREB. Trends Neurosci 13 5 (1990) 184-188
55. Moreau J.L., Jenck F., Martin J.R., Mortas P., and Haefely W.E. Antidepressant treatment prevents chronic unpredictable mild stress-induced anhedonia as assessed by ventral tegmentum self-stimulation behavior in rats. Eur Neuropsychopharmacol 2 1 (1992) 43-49
56. Muscat R., and Willner P. Suppression of sucrose drinking by chronic mild unpredictable stress: a methodological analysis. Neurosci Biobehav Rev 16 4 (1992) 507-517
57. Nibuya M., Morinobu S., and Duman R.S. Regulation of BDNF and trkB mRNA in rat brain by chronic electroconvulsive seizure and antidepressant drug treatments. J Neurosci 15 11 (1995) 7539-7547
58. Nibuya M., Nestler E.J., and Duman R.S. Chronic antidepressant administration increases the expression of cAMP response element binding protein (CREB) in rat hippocampus. J Neurosci 16 7 (1996) 2365-2372
59. Nielsen C.K., Arnt J., and Sanchez C. Intracranial self-stimulation and sucrose intake differ as hedonic measures following chronic mild stress: interstrain and interindividual differences. Behav Brain Res 107 1-2 (2000) 21-33
60. Papp M., Willner P., and Muscat R. An animal model of anhedonia: attenuation of sucrose consumption and place preference conditioning by chronic unpredictable mild stress. Psychopharmacology 104 2 (1991) 255-259
61. Pucilowski O., Overstreet D.H., Rezvani A.H., and Janowsky D.S. Chronic mild stress-induced anhedonia: greater effect in a genetic rat model of depression. Physiol Behav 54 6 (1993) 1215-1220
62. Rasmusson A.M., Shi L., and Duman R. Downregulation of BDNF mRNA in the hippocampal dentate gyrus after re-exposure to cues previously associated with footshock. Neuropsychopharmacology 27 2 (2002) 133-142
63. Russo-Neustadt A., Beard R.C., and Cotman C.W. Exercise, antidepressant medications, and enhanced brain derived neurotrophic factor expression. Neuropsychopharmacology 21 5 (1999) 679-682
64. Russo-Neustadt A.A., Beard R.C., Huang Y.M., and Cotman C.W. Physical activity and antidepressant treatment potentiate the expression of specific brain-derived neurotrophic factor transcripts in the rat hippocampus. Neuroscience 101 2 (2000) 305-312
65. Russo-Neustadt A., Ha T., Ramirez R., and Kesslak J.P. Physical activity-antidepressant treatment combination: impact on brain-derived neurotrophic factor and behavior in an animal model. Behav Brain Res 120 1 (2001) 87-95
66. Saarelainen T., Hendolin P., Lucas G., Koponen E., Sairanen M., MacDonald E., et al. Activation of the TrkB neurotrophin receptor is induced by antidepressant drugs and is required for antidepressant-induced behavioral effects. J Neurosci 23 1 (2003) 349-357
67. Sairanen M., Lucas G., Ernfors P., Castren M., and Castren E. Brain-derived neurotrophic factor and antidepressant drugs have different but coordinated effects on neuronal turnover, proliferation, and survival in the adult dentate gyrus. J Neurosci 25 5 (2005) 1089-1094
68. Schildkraut J.J. The catecholamine hypothesis of affective disorders: a review of supporting evidence. Am J Psychiatry 122 5 (1965) 509-522
69. Shabsigh R., Zakaria L., Anastasiadis A.G., and Seidman A.S. Sexual dysfunction and depression: etiology, prevalence, and treatment. Curr Urol Rep 2 6 (2001) 463-467
70. Shirayama Y., Chen A.C., Nakagawa S., Russell D.S., and Duman R.S. Brain-derived neurotrophic factor produces antidepressant effects in behavioral models of depression. J Neurosci 22 8 (2002) 3251-3261
71. Siuciak J.A., Lewis D.R., Wiegand S.J., and Lindsay R.M. Antidepressant-like effect of brain-derived neurotrophic factor (BDNF). Pharmacol Biochem Behav 56 1 (1997) 131-137
72. Smith M.A., Makino S., Kvetnansky R., and Post R.M. Stress and glucocorticoids affect the expression of brain-derived neurotrophic factor and neurotrophin-3 mRNAs in the hippocampus. J Neurosci 15 3 Pt 1 (1995) 1768-1777
73. Tabuchi E., Mulder A.B., and Wiener S.I. Reward value invariant place responses and reward site associated activity in hippocampal neurons of behaving rats. Hippocampus 13 1 (2003) 117-132
74. Tao X., Finkbeiner S., Arnold D.B., Shaywitz A.J., and Greenberg M.E. Ca2+ influx regulates BDNF transcription by a CREB family transcription factor-dependent mechanism. Neuron 20 4 (1998) 709-726
75. Thome J., Sakai N., Shin K., Steffen C., Zhang Y.J., Impey S., et al. cAMP response element-mediated gene transcription is upregulated by chronic antidepressant treatment. J Neurosci 20 11 (2000) 4030-4036
76. Tsankova N.M., Berton O., Renthal W., Kumar A., Neve R.L., and Nestler E.J. Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action. Nat Neurosci 9 4 (2006) 519-525
77. Willner P. Validity, reliability and utility of the chronic mild stress model of depression: a 10-year review and evaluation. Psychopharmacology (Berl) 134 4 (1997) 319-329
78. Willner P. Chronic mild stress (CMS) revisited: consistency and behavioural-neurobiological concordance in the effects of CMS. Neuropsychobiology 52 2 (2005) 90-110
79. Willner P., Towell A., Sampson D., Sophokleous S., and Muscat R. Reduction of sucrose preference by chronic unpredictable mild stress, and its restoration by a tricyclic antidepressant. Psychopharmacology 93 3 (1987) 358-364
80. Witgen B.M., Lifshitz J., Smith M.L., Schwarzbach E., Liang S.L., Grady M.S., et al. Regional hippocampal alteration associated with cognitive deficit following experimental brain injury: a systems, network and cellular evaluation. Neuroscience 133 1 (2005) 1-15
81. Wong M.L., and Licinio J. From monoamines to genomic targets: a paradigm shift for drug discovery in depression. Nat Rev Drug Discov 3 2 (2004) 136-151
82. Yamamoto T., and Sawa K. Comparison of c-fos-like immunoreactivity in the brainstem following intraoral and intragastric infusions of chemical solutions in rats. Brain Res 866 1-2 (2000) 144-151
83. Ying S.W., Futter M., Rosenblum K., Webber M.J., Hunt S.P., Bliss T.V., et al. Brain-derived neurotrophic factor induces long-term potentiation in intact adult hippocampus: requirement for ERK activation coupled to CREB and upregulation of Arc synthesis. J Neurosci 22 5 (2002) 1532-1540