Beneficial effects of benzodiazepine diazepam on chronic stress-induced impairment of hippocampal structural plasticity and depression-like behavior in mice

Behavioural Brain Research

Volumn 228, Issue 2, 2012, Pages 339-350

  Zhao, Yunan ^a   Wang, Zhongli ^a   Dai, Jianguo ^a   Chen, Lin ^a   Huang, Yufang ^a   Zhan, Zhen ^a  

^a NANJING UNIVERSITY OF CHINESE MEDICINE   (China)

Author keywords

Benzodiazepine; Depression like behavior; Diazepam; Hippocampus; Stress; Structural plasticity

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; DIAZEPAM; GLUCOCORTICOID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY SPECIFICITY; ARTICLE; CHRONIC STRESS; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; DEPRESSION; DRUG ACTIVITY; DRUG DOSE COMPARISON; DRUG EFFICACY; DRUG MEGADOSE; FORCED SWIMMING TEST; HIPPOCAMPUS; IMMOBILIZATION; LOW DRUG DOSE; MALE; MOUSE; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TREATMENT DURATION; TREATMENT RESPONSE;

ANALYSIS OF VARIANCE; ANIMALS; ANTI-ANXIETY AGENTS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CORTICOSTERONE; DEPRESSION; DIAZEPAM; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; HINDLIMB SUSPENSION; HIPPOCAMPUS; MALE; MICE; MICE, INBRED C57BL; NEURONAL PLASTICITY; NEURONS; STRESS, PSYCHOLOGICAL; SWIMMING; SYNAPTOPHYSIN; TIME FACTORS;

EID: 84856228680     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2011.12.013     Document Type: Article

References (65)

1. Stout S.C., Nemeroff C.B. Stress and psychiatric disorders. Semin Neurosci 1994, 6:271-280.
2. Meyer S.E., Chrousos G.P., Gold P.W. Major depression and the stress system: a life span perspective. Dev Psychopathol 2001, 13:565-580.
3. Stam R. PTSD and stress sensitisation: a tale of brain and body. Part 1: human studies. Neurosci Biobehav Rev 2007, 31:530-557.
4. Liu R.T., Allogy L.B. Stress generation in depression: a systematic review of the empirical literature and recommendations for future study. Clin Psychol Rev 2010, 30:582-593.
5. Dunčko R., Kiss A., Škultétyová I., Škultétyová M., Ježová D. Corticotropin-releasing hormone mRNA levels in response to chronic mild stress rise in male but not in female rats while tyrosine hydroxylase mRNA levels decrease in both sexes. Psychoneuroendocrinology 2001, 26:77-89.
6. Grønli J., Murison R., Bjorvatn B., Sørensen E., Portas C.M., Ursin R. Chronic mild stress affects sucrose intake and sleep in rats. Behav Brain Res 2004, 150:139-147.
7. Mineur Y.S., Belzung C., Crusio W.E. Effects of unpredictable chronic mild stress on anxiety and depression-like behavior in mice. Behav Brain Res 2006, 175:43-50.
8. Zhao Y., Ma R., Shen J., Su H., Xing D., Du L. A mouse model of depression induced by repeated corticosterone injections. Eur J Pharmacol 2008, 581:113-120.
9. Radley J.J., Morrison J.H. Repeated stress and structural plasticity in the brain. Ageing Res Rev 2005, 4:271-287.
10. Pittenger C., Duman R.S. Stress, depression, and neuroplasticity: a convergence of mechanisms. Neuropsychopharmacology 2008, 33:88-109.
11. Calabrese F., Molteni R., Racagni G., Riva M.A. Neuronal plasticity: a link between stress and mood disorders. Psychoneuroendocrinology 2009, 34(Suppl. 1):S208-S216.
12. Smith M.E. Bilateral hippocampal volume reduction in adults with post-traumatic stress disorder: a meta-analysis of structural MRI studies. Hippocampus 2005, 15:798-807.
13. Czéh B., Sinon M., Schmelting B., Hiemke C., Fuchs E. Astroglial plasticity in the hippocampus is affected by chronic psychosocial stress and concomitant fluoxetine treatment. Neuropsychopharmacology 2006, 31:1616-1626.
14. Sapolsky R.M., Krey L., McEwen B.S. Prolonged glucocorticoid exposure reduces hippocampal neuron number: implications for aging. J Neurosci 1985, 5:1221-1227.
15. Zhao H., Xu H., Xu X., Young D. Predatory stress induces hippocampal cell death by apoptosis in rats. Neurosci Lett 2007, 421:115-120.
16. Magariños A.M., McEwen B.S., Flügge G., Fuchs E. Chronic psychosocial stress causes apical dendritic atrophy of hippocampal CA3 pyramidal neurons in subordinate tree shrews. J Neurosci 1996, 16:3534-3540.
17. Stockmeier C.A., Mahajan G.J., Konick L.C., Overholser J.C., Jurjus G.J., Meltzer H.Y., et al. Cellular changes in the postmortem hippocampus in major depression. Biol Psychiatry 2004, 56:640-650.
18. Tata D.A., Marciano V.A., Anderson B.J. Synapse loss from chronically elevated glucocorticoids: relationship to neuropil volume and cell number in hippocampal area CA3. J Comp Neurol 2006, 498:363-374.
19. Cerseto M., Reinés A., Ferrero A., Sifonios L., Rubio M., Wikinske S. Chronic treatment with high doses of corticosterone decreases cytoskeletal proteins in the rat hippocampus. Eur J Neurosci 2006, 24:3354-3364.
20. Zhao Y., Xie W., Dai J., Wang Z., Huang Y. The varying effects of short-term and long-term corticosterone injections on depression-like behavior in mice. Brain Res 2009, 1261:82-90.
21. Duman R.S. Depression: a case of neuronal life and death. Biol Psychiatry 2004, 56:140-145.
22. Henn F., Vollmayr B., Sartorius A. Mechanisms of depression: the role of neurogenesis. Drug Discov Today Dis Mech 2004, 1:407-411.
23. Dranovsky A., Hen R. Hippocampal neurogenesis: regulation by stress and antidepressants. Biol Psychiatry 2006, 59:1136-1143.
24. Yuluĝ B., Ozan E., Gönül A.S., Kilic E. Brain-derived neurotrophic factor, stress and depression: a minireview. Brain Res Bull 2009, 78:267-269.
25. Seckl J.R., Olsson T. Glucocorticoid hypersecretion and the age-impaired hippocampus: cause or effect. J Endocrinol 1995, 145:201-211.
26. Woolley C.S., Gould E., McEwen B.S. Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons. Brain Res 1990, 531:225-231.
27. Jacobsen J.P.R., Mørk A. 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 2006, 1110:221-225.
28. Krugers H.J., Goltstein P.M., van der Linden S., Joëls M. Blockade of glucocorticoid receptors rapidly restores hippocampal CA1 synaptic plasticity after exposure to chronic stress. Eur J Neurosci 2006, 23:3051-3055.
29. Dumas T.C., Gillette T., Ferguson D., Hamilton K., Sapolsky R.M. Anti-glucocorticoid gene therapy reverses the impairing effects of elevated corticosterone on spatial memory, hippocampal neuronal excitability, and synaptic plasticity. J Neurosci 2010, 30:1712-1720.
30. Mandrioli R., Mercolini L., Raggi M.A. Benzodiazepine metabolism: an analytical perspective. Curr Drug Metab 2008, 9:827-844.
31. Davidson J.R. Use of benzodiazepines in social anxiety disorder, generalized anxiety disorder, and posttraumatic stress disorder. J Clin Psychiatry 2004, 65(Suppl. 5):29-33.
32. Divac N., Jasović M., Djukić L., Vujnović M., Babić D., Bajcetić M., et al. Benzodiazepines utilization and self-medication as correlates of stress in the population of Serbia. Pharmacoepidemiol Drug Saf 2004, 13:315-322.
33. Ravindran L.N., Stein M.B. The pharmacologic treatment of anxiety disorders: a review of progress. J Clin Psychiatry 2010, 71:839-854.
34. Gamaro G.D., Manoli L.P., Torres I.L.S., Silveira R., Dalmaz C. Effects of chronic variate stress on feeding behavior and on monoamine levels in different rat brain structures. Neurochem Int 2003, 42:107-114.
35. Swiergiel A.H., Leskov I.L., Dunn A.J. Effects of chronic and acute stressors and CRF on depression-like behavior in mice. Behav Brain Res 2008, 186:32-40.
36. Porsolt R.D., Le Pichon M., Jalfre M. Depression: a new animal model sensitive to antidepressant treatments. Nature 1977, 266:730-732.
37. Steru L., Chermat R., Thierry B., Simon P. The tail suspension test: a new method for screening antidepressants in mice. Psychopharmacology (Berl) 1985, 85:367-370.
38. Yang C., Wang G., Wang H., Liu Z., Wang X. Cytoskeletal alterations in rat hippocampus following chronic unpredictable mild stress and re-exposure to acute and chronic unpredictable mild stress. Behav Brain Res 2009, 205:518-524.
39. Dagyte G., Van der Zee E.A., Postema F., Luiten P.G., Den Boe J.A., Trentani A., et al. Chronic but not acute foot-shock stress leads to temporary suppression of cell proliferation in rat hippocampus. Neuroscience 2009, 162:904-913.
40. Molteni R., Calabrese F., Cattaneo A., Mancini M., Gennarelli M., Racagni G., et al. Acute stress responsiveness of the neurotrophin BDNF in the rat hippocampus is modulated by chronic treatment with the antidepressant duloxetine. Neuropsychopharmacology 2009, 34:1523-1532.
41. Shi S.S., Shao S.H., Yuan B.P., Pan F., Li Z.L. Acute stress and chronic stress change brain-derived neurotrophic factor (BDNF) and tyrosine kinase-coupled receptor (TrkB) expression in both young and aged rat hippocampus. Yonsei Med J 2010, 51:661-671.
42. Badowska-Szalewska E., Spodnik E., Klejbor I., Ludkiewicz B., Moryś J. Do two models of acute and chronic stress stimulation influence the amount of nerve growth factor (NGF) and its receptor TrkA in the hippocampal neurons of middle aged rats. Brain Res 2011, 1384:97-109.
43. Keeney A., Jessop D.S., Harbuz M.S., Marsden C.A., Hogg S., Blackburn-Munro R.E. Differential effects of acute and chronic social defeat stress on hypothalamic-pituitary-adrenal axis function and hippocampal serotonin release in mice. J Neuroendocrinol 2006, 18:330-338.
44. Xu H., Luo C., Richardson J.S., Li X.M. Recovery of hippocampal cell proliferation and BDNF levels, both of which are reduced by repeated restraint stress, is accelerated by chronic venlafaxine. Pharmacogenomics J 2004, 4:322-331.
45. Vyas A., Pillai A.G., Chatarji S. Recovery after chronic stress fails to reverse amygdaloid neuronal hypertrophy and enhanced anxiety-like behavior. Neuroscience 2004, 128:667-673.
46. Mizoguchi K., Kunishita T., Chui D.H., Tabira T. Stress induces neuronal death in the hippocampus of castrated rats. Neurosci Lett 1992, 138:157-216.
47. Willner P., Towell A., Sampson D., Sophokleous S., Muscat R. Reduction of sucrose preference by chronic unpredictable mild stress, and its restoration by a tricyclic antidepressant. Psychopharmacology (Berl) 1987, 93:358-364.
48. Papp M., Willner P., Muscat R. An animal model of anhedonia: attenuation of sucrose consumption and place preference conditioning by chronic unpredictable mild stress. Psychopharmacology (Berl) 1991, 104:255-259.
49. Cryan J.F., Markou A., Lucki I. Assessing antidepressant activity in rodents: recent developments and future needs. Trends Pharmacol Sci 2002, 23:238-245.
50. Brotto L.A., Gorzalka B.B., Barr A.M. Paradoxical effects of chronic corticosterone on forced swim behaviours in aged male and female rats. Eur J Pharmacol 2001, 424:203-209.
51. Kalynchuk L.E., Gregus A., Boudreau D., Perrot-Sinal T.S. Corticosterone increases depression-like behavior, with some effects on predator odor-induced defensive behavior, in male and female rats. Behav Neurosci 2004, 118:1365-1377.
52. Gregus A., Wintink A.J., Davis A.C., Kalynchuk L.E. Effect of repeated corticosterone injections and restraint stress on anxiety and depression-like behavior in male rats. Behav Brain Res 2005, 156:105-114.
53. Sousa N., Lukoyanov N.V., Madeira M.D., Almeida O.F., Paula-Barboosa M.M. Reorganization of the morphology of hippocampal neuritis and synapses after stress-induced damage correlates with behavioral improvement. Neuroscience 2000, 97:253-266.
54. Magariños A.M., Deslandes A., McEwen B.S. Effects of antidepressants and benzodiazepine treatments on the dendritic structure of CA3 pyramidal neurons after chronic stress. Eur J Pharmacol 1999, 371:113-122.
55. Kampen M.V., Schmitt U., Hiemke C., Fuchs E. Diazepam has no beneficial effects on stress-induced behavioural and endocrine changes in male tree shrews. Pharmacol Biochem Behav 2000, 65:539-546.
56. Li S., Murakami Y., Wang M., Maeda K., Matsumoto K. The effects of chronic valproate and diazepam in a mouse model of posttraumatic stress disorder. Pharmacol Biochem Behav 2006, 85:324-331.
57. Kalman B.A., Kim P.J., Cole M.A., Chi M.S., Spencer R.L. Diazepam attenuation of restraint stress-induced corticosterone levels is enhanced by prior exposure to repeated restraint. Psychoneuroendocrinology 1997, 22:349-360.
58. Fries E., Hellhammer D.H., Hellhammer J. Attenuation of the hypothalamic-pituitary-adrenal axis responsivity to the trier social stress test by the benzodiazepine alprazolam. Psychoneuroendocrinology 2006, 31:1278-1288.
59. Welt T., Engelmann M., Renner U., Erhardt A., Müller M.B., Landgraf R., et al. Temazepam triggers the release of vasopressin into the rat hypothalamic paraventricular nucleus: novel insight into benzodiazepine action on hypothalamic-pituitary-adrenocortical system activity during stress. Neuropsychopharmacology 2006, 31:2573-2579.
60. Matar M.A., Zohar J., Kaplan Z., Cohen H. Alprazolam treatment immediately after stress exposure interferes with normal HPA-stress response and increases vulnerability to subsequent stress in an animal model of PTSD. Eur Neuropsychopharmacol 2009, 19:283-295.
61. Manthey L., Giltay E.J., Van Veen T., Neven A.K., Vreeburg S.A., Penninx B.W., et al. Long-term benzodiazepine use and salivary cortisol: the Netherlands study of depression and anxiety (NESDA). J Clin Psychopharmacol 2010, 30:160-168.
62. Obrietan K., Gao X.B., Van Den Pol A.N. Excitatory actions of GABA increase BDNF expression via a MAPK-CREB-dependent mechanism-a positive feedback circuit in developing neurons. J Neurophysiol 2002, 88:1005-1015.
63. Mantelas A., Stamatakis A., Kazanis I., Philippidis H., Stylianopoulou F. Control of neuronal nitric oxide synthase and brain-derived neurotrophic factor levels by GABA-A receptors in the developing rat cortex. Brain Res Dev Brain 2003, 145:185-195.
64. Fiorentino H., Kuczewski N., Diabira D., Ferrand N., Pangalos M.N., Porcher C., et al. GABA(B) receptor activation triggers BDNF release and promotes the maturation of GABAergic synapses. J Neurosci 2009, 29:11650-11661.
65. Kuczewski N., Fuchs C., Ferrand N., Jovanovic J.N., Gaiarsa J.L., Porcher C. Mechanism of GABA(B) receptor-induced BDNF secretion and promotion of GABA(A) receptor membrane expression. J Neurochem 2011, 118:533-545.