Resistance to the development of stress-induced behavioral despair in the forced swim test associated with elevated hippocampal Bcl-xl expression

Behavioural Brain Research

Volumn 213, Issue 2, 2010, Pages 218-224

  Shishkina, Galina T ^a   Kalinina, Tatyana S ^a   Berezova, Inna V ^a   Bulygina, Veta V ^a   Dygalo, Nikolay N ^a  

^a INSTITUTE OF CYTOLOGY AND GENETICS   (Russian Federation)

Author keywords

Bax; Bcl xl; BDNF; Forced swim test; Hippocampus; Immobility

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; MESSENGER RNA; PROTEIN BAX; PROTEIN BCL XL; BCL2L1 PROTEIN, RAT; CORTICOSTERONE; CORTICOTROPIN; PROTEIN BCL X;

ANIMAL BEHAVIOR; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; CORRELATION ANALYSIS; DOWN REGULATION; FORCED SWIMMING TEST; FRONTAL CORTEX; GENE EXPRESSION; HIPPOCAMPUS; HOPELESSNESS; IMMUNOHISTOCHEMISTRY; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; STRESS; ANIMAL; BIOSYNTHESIS; BLOOD; DEPRESSION; DISEASE MODEL; FRONTAL LOBE; GENE EXPRESSION REGULATION; MENTAL STRESS; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOLOGY; SWIMMING; TIME;

ADRENOCORTICOTROPIC HORMONE; ANIMALS; BCL-2-ASSOCIATED X PROTEIN; BCL-X PROTEIN; BRAIN-DERIVED NEUROTROPHIC FACTOR; CORTICOSTERONE; DEPRESSION; DISEASE MODELS, ANIMAL; FRONTAL LOBE; GENE EXPRESSION REGULATION; HIPPOCAMPUS; MALE; RATS; STRESS, PSYCHOLOGICAL; SWIMMING; TIME FACTORS;

EID: 77953913795     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2010.05.003     Document Type: Article

References (65)

1. Adachi M., Barrot M., Autry A.E., Theobald D., Monteggia L.M. Selective loss of brain-derived neurotrophic factor in the dentate gyrus attenuates antidepressant efficacy. Biol Psychiatry 2008, 63:642-649.
2. Almeida O.F., Condé G.L., Crochemore C., Demeneix B.A., Fischer D., Hassan A.H., et al. Subtle shifts in the ratio between pro- and antiapoptotic molecules after activation of corticosteroid receptors decide neuronal fate. FASEB J 2000, 14:779-790.
3. Arunrut T., Alejandre H., Chen M., Cha J., Russo-Neustadt A. Differential behavioral and neurochemical effects of exercise, reboxetine and citalopram with the forced swim test. Life Sci 2009, 84:584-589.
4. Bachis A., Cruz M.I., Nosheny R.L., Mocchetti I. Chronic unpredictable stress promotes neuronal apoptosis in the cerebral cortex. Neurosci Lett 2008, 442:104-108.
5. Banasr M., Valentine G.W., Li X.Y., Gourley S.L., Taylor J.R., Duman R.S. Chronic unpredictable stress decreases cell proliferation in the cerebral cortex of the adult rat. Biol Psychiatry 2007, 62:496-504.
6. Bergström A., Jayatissa M.N., Mørk A., Wiborg O. Stress sensitivity and resilience in the chronic mild stress rat model of depression, an in situ hybridization study. Brain Res 2008, 1196:41-52.
7. Bilang-Bleuel A., Rech J., De Carli S., Holsboer F., Reul J.M. Forced swimming evokes a biphasic response in CREB phosphorylation in extrahypothalamic limbic and neocortical brain structures in the rat. Eur J Neurosci 2002, 15:1048-1060.
8. Bittigau P., Sifringer M., Genz K., Reith E., Pospischil D., Govindarajalu S., et al. Antiepileptic drugs and apoptotic neurodegeneration in the developing brain. Proc Natl Acad Sci USA 2002, 99:15089-15094.
9. Boise L.H., González-García M., Postema C.E., Ding L., Lindsten T., Turka L.A., et al. bcl-x, a bcl-2-related gene that functions as a dominant regulator of apoptotic cell death. Cell 1993, 74:597-608.
10. Bravo J.A., Díaz-Veliz G., Mora S., Ulloa J.L., Berthoud V.M., Morales P., et al. Desipramine prevents stress-induced changes in depressive-like behavior and hippocampal markers of neuroprotection. Behav Pharmacol 2009, 20:273-285.
11. Chalovich E.M., Zhu J.H., Caltagarone J., Bowser R., Chu C.T. Functional repression of cAMP response element in 6-hydroxydopamine-treated neuronal cells. J Biol Chem 2006, 281:17870-17881.
12. Champagne D.L., Bagot R.C., van Hasselt F., Ramakers G., Meaney M.J., de Kloet E.R., et al. Maternal care and hippocampal plasticity: evidence for experience-dependent structural plasticity, altered synaptic functioning, and differential responsiveness to glucocorticoids and stress. J Neurosci 2008, 28:6037-6045.
13. Czéh B., Müller-Keuker J.I., Rygula R., Abumaria N., Hiemke C., Domenici E., et al. Chronic social stress inhibits cell proliferation in the adult medial prefrontal cortex: hemispheric asymmetry and reversal by fluoxetine treatment. Neuropsychopharmacology 2007, 32:1490-1503.
14. Czéh B., Welt T., Fischer A.K., Erhardt A., Schmitt W., Müller M.B., et al. Chronic psychosocial stress and concomitant repetitive transcranial magnetic stimulation: effects on stress hormone levels and adult hippocampal neurogenesis. Biol Psychiatry 2002, 52:1057-1065.
15. de Kloet E.R. About stress hormones and resilience to psychopathology. J Neuroendocrinol 2008, 20:885-892.
16. Droste S.K., de Groote L., Atkinson H.C., Lightman S.L., Reul J.M., Linthorst A.C. Corticosterone levels in the brain show a distinct ultradian rhythm but a delayed response to forced swim stress. Endocrinology 2008, 149:3244-3253.
17. Du J., McEwen B., Manji H.K. Glucocorticoid receptors modulate mitochondrial function: a novel mechanism for neuroprotection. Commun Integr Biol 2009, 2:350-352.
18. Dygalo N.N., Kalinina T.S., Shishkina G.T. Neonatal programming of rat behavior by downregulation of alpha2A-adrenoreceptor gene expression in the brain. Ann N Y Acad Sci 2008, 1148:409-414.
19. Feder A., Nestler E.J., Charney D.S. Psychobiology and molecular genetics of resilience. Nat Rev Neurosci 2009, 10:446-457.
20. Fuchikami M., Morinobu S., Kurata A., Yamamoto S., Yamawaki S. Single immobilization stress differentially alters the expression profile of transcripts of the brain-derived neurotrophic factor (BDNF) gene and histone acetylation at its promoters in the rat hippocampus. Int J Neuropsychopharmacol 2009, 12:73-82.
21. Gascoyne D.M., Kypta R.M., Vivanco M.M. Glucocorticoids inhibit apoptosis during fibrosarcoma development by transcriptionally activating Bcl-xL. J Biol Chem 2003, 278:18022-18029.
22. Gould E., McEwen B.S., Tanapat P., Galea L.A., Fuchs E. Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation. J Neurosci 1997, 17:2492-2498.
23. Gould E., Tanapat P., McEwen B.S., Flügge G., Fuchs E. Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proc Natl Acad Sci USA 1998, 95:3168-3171.
24. Gourley S.L., Kiraly D.D., Howell J.L., Olausson P., Taylor J.R. Acute hippocampal brain-derived neurotrophic factor restores motivational and forced swim performance after corticosterone. Biol Psychiatry 2008, 64:884-890.
25. Haack D., Luu H., Cho J., Chen M.J., Russo-Neustadt A. Exercise reverses chronic stress-induced Bax oligomer formation in the cerebral cortex. Neurosci Lett 2008, 438:290-294.
26. Hajszan T., Dow A., Warner-Schmidt J.L., Szigeti-Buck K., Sallam N.L., Parducz A., et al. Remodeling of hippocampal spine synapses in the rat learned helplessness model of depression. Biol Psychiatry 2009, 65:392-400.
27. Hansson A.C., Sommer W.H., Metsis M., Strömberg I., Agnati L.F., Fuxe K. Corticosterone actions on the hippocampal brain-derived neurotrophic factor expression are mediated by exon IV promoter. J Neuroendocrinol 2006, 18:104-114.
28. Hansson A.C., Sommer W., Rimondini R., Andbjer B., Strömberg I., Fuxe K. c-fos reduces corticosterone-mediated effects on neurotrophic factor expression in the rat hippocampal CA1 region. J Neurosci 2003, 23:6013-6022.
29. Heine V.M., Maslam S., Zareno J., Joëls M., Lucassen P.J. Suppressed proliferation and apoptotic changes in the rat dentate gyrus after acute and chronic stress are reversible. Eur J Neurosci 2004, 19:131-144.
30. Jonas E. BCL-xL regulates synaptic plasticity. Mol Interv 2006, 6:208-222.
31. Kendler K.S., Karkowski L.M., Prescott C.A. Causal relationship between stressful life events and the onset of major depression. Am J Psychiatry 1999, 156:837-841.
32. Kosten T.A., Galloway M.P., Duman R.S., Russell D.S., D'Sa C. Repeated unpredictable stress and antidepressants differentially regulate expression of the bcl-2 family of apoptotic genes in rat cortical, hippocampal, and limbic brain structures. Neuropsychopharmacology 2008, 33:1545-1558.
33. Krishnan V., Nestler E.J. The molecular neurobiology of depression. Nature 2008, 455:894-902.
34. Lee J., Duan W., Mattson M.P. Evidence that brain-derived neurotrophic factor is required for basal neurogenesis and mediates, in part, the enhancement of neurogenesis by dietary restriction in the hippocampus of adult mice. J Neurochem 2002, 82:1367-1375.
35. Lee T., Saruta J., Sasaguri K., Sato S., Tsukinoki K. Allowing animals to bite reverses the effects of immobilization stress on hippocampal neurotrophin expression. Brain Res 2008, 1195:43-49.
36. Li H., Chen Y., Jones A.F., Sanger R.H., Collis L.P., Flannery R., et al. Bcl-xL induces Drp1-dependent synapse formation in cultured hippocampal neurons. Proc Natl Acad Sci USA 2008, 105:2169-2174.
37. Lucassen P.J., Heine V.M., Muller M.B., van der Beek E.M., Wiegant V.M., De Kloet E.R., et al. Stress, depression and hippocampal apoptosis. CNS Neurol Disord Drug Targets 2006, 5:531-546.
38. Luo C., Xu H., Li X.M. Post-stress changes in BDNF and Bcl-2 immunoreactivities in hippocampal neurons: effect of chronic administration of olanzapine. Brain Res 2004, 1025:194-202.
39. Manji H.K., Duman R.S. Impairments of neuroplasticity and cellular resilience in severe mood disorders: implications for the development of novel therapeutics. Psychopharmacol Bull 2001, 35:5-49.
40. McEwen B.S. Glucocorticoids, depression, and mood disorders: structural remodeling in the brain. Metabolism 2005, 54:20-23.
41. McEwen B.S. Central effects of stress hormones in health and disease: understanding the protective and damaging effects of stress and stress mediators. Eur J Pharmacol 2008, 583:174-185.
42. McEwen B.S., Magarinos A.M. Stress effects on morphology and function of the hippocampus. Ann N Y Acad Sci 1997, 821:271-284.
43. Meaney M.J. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu Rev Neurosci 2001, 24:1161-1192.
44. Monteggia L.M., Barrot M., Powell C.M., Berton O., Galanis V., Gemelli T., et al. Essential role of brain-derived neurotrophic factor in adult hippocampal function. Proc Natl Acad Sci USA 2004, 101:10827-10832.
45. Murakami S., Imbe H., Morikawa Y., Kubo C., Senba E. Chronic stress, as well as acute stress, reduces BDNF mRNA expression in the rat hippocampus but less robustly. Neurosci Res 2005, 53:129-139.
46. Nahas Z., Jiang Y., Zeidan Y.H., Bielawska A., Szulc Z., Devane L., et al. Anti-ceramidase LCL385 acutely reduces BCL-2 expression in the hippocampus but is not associated with an increase of learned helplessness in rats. Behav Brain Res 2009, 197:41-44.
47. Nair A., Vadodaria K.C., Banerjee S.B., Benekareddy M., Dias B.G., Duman R.S., et al. Stressor-specific regulation of distinct brain-derived neurotrophic factor transcripts and cyclic AMP response element-binding protein expression in the postnatal and adult rat hippocampus. Neuropsychopharmacology 2007, 32:1504-1519.
48. Nudel U., Zakut R., Shani M., Neuman S., Levy Z., Yaffe D. The nucleotide sequence of the rat cytoplasmic beta-actin gene. Nucleic Acids Res 1983, 11:1759-1771.
49. Panickar K.S., Nonner D., Barrett J.N. Overexpression of Bcl-xl protects septal neurons from prolonged hypoglycemia and from acute ischemia-like stress. Neuroscience 2005, 135:73-80.
50. Pizarro J.M., Lumley L.A., Medina W., Robison C.L., Chang W.E., Alagappan A., et al. Acute social defeat reduces neurotrophin expression in brain cortical and subcortical areas in mice. Brain Res 2004, 1025:10-20.
51. Porsolt R.D., Anton G., Blavet N., Jalfre M. Behavioural despair in rats: a new model sensitive to antidepressant treatments. Eur J Pharmacol 1978, 47:379-391.
52. Sairanen M., Lucas G., Ernfors P., Castrén M., Castrén 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 2005, 25:1089-1094.
53. Santarelli L., Saxe M., Gross C., Surget A., Battaglia F., Dulawa S., et al. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 2003, 301:805-809.
54. Scharfman H., Goodman J., Macleod A., Phani S., Antonelli C., Croll S. Increased neurogenesis and the ectopic granule cells after intrahippocampal BDNF infusion in adult rats. Exp Neurol 2005, 192:348-356.
55. Schmidt M.V., Sterlemann V., Müller M.B. Chronic stress and individual vulnerability. Ann N Y Acad Sci 2008, 1148:174-183.
56. Shindler K.S., Latham C.B., Roth K.A. Bax deficiency prevents the increased cell death of immature neurons in bcl-x-deficient mice. J Neurosci 1997, 17:3112-3119.
57. Shirayama Y., Chen A.C., Nakagawa S., Russell D.S., Duman R.S. Brain-derived neurotrophic factor produces antidepressant effects in behavioral models of depression. J Neurosci 2002, 22:3251-3261.
58. Shishkina G.T., Kalinina T.S., Dygalo N.N. Up-regulation of tryptophan hydroxylase-2 mRNA in the rat brain by chronic fluoxetine treatment correlates with its antidepressant effect. Neuroscience 2007, 150:404-412.
59. Shishkina G.T., Kalinina T.S., Dygalo N.N. Serotonergic changes produced by repeated exposure to forced swimming: correlation with behavior. Ann N Y Acad Sci 2008, 1148:148-153.
60. Smith M.A., Makino S., Kvetnansky R., Post R.M. Stress and glucocorticoids affect the expression of brain-derived neurotrophic factor and neurotrophin-3 mRNAs in the hippocampus. J Neurosci 1995, 15:1768-1777.
61. Sun W., Winseck A., Vinsant S., Park O.H., Kim H., Oppenheim R.W. Programmed cell death of adult-generated hippocampal neurons is mediated by the proapoptotic gene Bax. J Neurosci 2004, 24:11205-11213.
62. Tamatani M., Che Y.H., Matsuzaki H., Ogawa S., Okado H., Miyake S., et al. Tumor necrosis factor induces Bcl-2 and Bcl-x expression through NFkappaB activation in primary hippocampal neurons. J Biol Chem 1999, 274:8531-8538.
63. Tanapat P., Hastings N.B., Rydel T.A., Galea L.A., Gould E. Exposure to fox odor inhibits cell proliferation in the hippocampus of adult rats via an adrenal hormone-dependent mechanism. J Comp Neurol 2001, 437:496-504.
64. Viegas L.R., Vicent G.P., Barañao J.L., Beato M., Pecci A. Steroid hormones induce bcl-X gene expression through direct activation of distal promoter P4. J Biol Chem 2004, 279:9831-9839.
65. Wann B.P., Bah T.M., Boucher M., Courtemanche J., Le Marec N., Rousseau G., et al. Vulnerability for apoptosis in the limbic system after myocardial infarction in rats: a possible model for human postinfarct major depression. J Psychiatry Neurosci 2007, 32:11-16.