Effects of antidepressants and benzodiazepine treatments on the dendritic structure of CA3 pyramidal neurons after chronic stress

European Journal of Pharmacology

Volumn 371, Issue 2-3, 1999, Pages 113-122

  Magariños, Ana M ^a   Deslandes, Antoine ^b   McEwen, Bruce S ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b INSTITUT DE RECHERCHES INTERNATIONALES SERVIER   (France)

Author keywords

5 HT (5 hydroxytryptamine, serotonin) reuptake inhibitor, selective; Adinazolam; Dendritic atrophy; Hippocampus; Stress; Tianeptine

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; ADINAZOLAM; ANTIDEPRESSANT AGENT; BENZODIAZEPINE; BENZODIAZEPINE RECEPTOR; CORTICOSTERONE; FLUOXETINE; FLUVOXAMINE; SEROTONIN; SEROTONIN RECEPTOR; SEROTONIN UPTAKE INHIBITOR; TIANEPTINE;

ANIMAL EXPERIMENT; ARTICLE; BRAIN ATROPHY; CONTROLLED STUDY; HIPPOCAMPUS; IMMOBILIZATION STRESS; INTRAPERITONEAL DRUG ADMINISTRATION; MALE; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; STRESS;

ANIMALS; ANTIDEPRESSIVE AGENTS, SECOND-GENERATION; ANTIDEPRESSIVE AGENTS, TRICYCLIC; DENDRITIC CELLS; FLUOXETINE; FLUVOXAMINE; GOLGI APPARATUS; HIPPOCAMPUS; MALE; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-A; RECEPTORS, SEROTONIN; RESTRAINT, PHYSICAL; STRESS; THIAZEPINES;

EID: 0345465716     PISSN: 00142999     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0014-2999(99)00163-6     Document Type: Article

References (66)

1. Amsterdam J.D., Kaplan M., Potter L., Bloom L., Rickels K. Adinazolam, a new triazolobenzodiazepine, and imipramine in the treatment of major depressive disorder. Psychopharmacology. 88:1986;484-488.
2. Azmitia E., McEwen B.S. Corticosterone regulation of tryptophan hydroxylase in rat midbrain. Science. 166:1969;1274-1276.
3. Beck S.G., Choi K.C., List T.J., Okuhara D.Y., Birnstiel S. Corticosterone alters 5-HT 1A receptor-mediated hyperpolarization in area CA1 hippocampal pyramidal neurons. Neuropsychopharmacology. 14:1996;27-33.
4. Ben Shachar D., Klein E., Tabak A., Finberg J.P.M. Effect of single and repeated administration of fluvoxamine on noradrenaline release in rat brain. Eur. J. Pharmacol. 332:1997;237-243.
5. Bremner D.J., Randall P., Scott T.M., Bronen R.A., Seibyl J.P., Southwick S.M., Delaney R.C., McCarthy G., Charney D.S., Innis R.B. MRI-based measurement of hippocampal volume in patients with combat-related posttraumatic stress disorder. Am. J. Psychiatry. 152:1995;973-981.
6. Broderick P.A., Hope O., Jeannot P. Mechanism of triazolo-benzodiazepine and benzodiazepine action in anxiety and depression: behavioral studies with concomitant in vivo CA1 hippocampal norepineprine and serotonin release detection in the behaving animal. Prog. Neuropharmacol. Biol. Psychiatry. 22:1998;353-386.
7. Chaouloff F. Physiopharmacological interactions between stress hormones and central serotonergic systems. Brain Res. Rev. 18:1993;1-32.
8. Conrad C.D., Galea L.A.M., Kuroda Y., McEwen B.S. Chronic stress impairs rat spatial memory on the Y-Maze and this effect is blocked by tianeptine pre-treatment. Behav. Neurosci. 110:1996;1321-1334.
9. Convit A., de Leon M.J., Tarshish C., De Santi S., Tsui W., Rusinek H., George A. Specific hippocampal volume reductions in individuals at risk for Alzheimer's disease. Neurobiol. Aging. 18:1997;131-138.
10. De Bellis M.D., Gold P.W., Geracioti T.D., Listwak S.J., Kling M.A. Association of fluoxetine treatment with reductions in CSF concentrations of corticotropin-releasing hormone and arginine vasopressin in patients with major depression. Am. J. Psychiatry. 150:1993;656-657.
11. De Bruin L.A., Schasfoort M.C., Stefens A.B., Korf J. Effects of stress and exercise on rat hippocampus and striatum extracellular lactate. Am. J. Physiol. 259:1994;R773-R779.
12. De Kloet E.R., Vreugdenhil E., Oitzl M.S., Joëls M. Brain corticosteroid receptor balance in heath and disease. Endocrine Reviews. 19:1998;269-301.
13. Delbende C., Contesse V., Mocaër E., Vaudry H. The novel antidepressant tianeptine reduces stress-evoked stimulation of the HPA axis. Eur. J. Pharmacol. 202:1991;391-396.
14. Duncan G.E., Knapp D.S., Carson S.W., Breese G.R. Differential effect of chronic antidepressant treatment on swim stress and fluoxetine-induced secretion of corticosterone and progesterone. J. Pharmacol. Exp. Ther. 285(2):1998;579-587.
15. Fitch J.M., Juraska J.M., Washington L.W. The dendritic morphology of pyramidal neurons in the rat hippocampal CA3 area: I. Cell types. Brain Res. 479:1989;105-114.
16. Freund T.F., Buzsaki G. Interneurons in the hippocampus. Hippocampus. 6:1996;347-470.
17. Gabbott P.L., Somogyi J. The 'single' section Golgi-impregnation procedure: methodological description. J. Neurosci. Methods. 11:1984;221-230.
18. Gurvits T.V., Shenton M.E., Hokama H., Ohta H., Lasko N.B., Gilbertson M.W., Orr S.P., Kikinis R., Jolesz F.A., McCarley R.W., Pitman R.K. Magnetic resonance imaging study of hippocampal volume in chronic, combat-related posttraumatic stress disorder. Biol. Psychiatry. 40:1996;1091-1099.
19. Hwang E.C., Magnussen I., Van Woert M.H. Effects of chronic fluoxetine on serotonin metabolism. Res. Commun. Chem. Pathol. Pharmacol. 29:1980;79-98.
20. Hyttel J. Pharmacological characterization of selective serotonin reuptake inhibitors (SSRIs). Int. Clin. Psychopharmacol. 9:1994;19-26. Suppl. 1.
21. Kelley M.S., Steward O. Injury-induced physiological events that may modulate gene expression in neurons and glia. Rev. Neurosci. 8:1997;147-177.
22. Kelly J.P., Leonard B.E. The effect of tianeptine and sertraline in three animal models of depression. Neuropharmacology. 33(8):1994;1011-1016.
23. Kennett G.A., Dickinson S.L., Curzon G. Enhancement of some 5-HT-dependent behavioral responses following repeated immobilization in rats. Brain Res. 330:1985;253-263.
24. Koshikawa N., Kitamura M., Tomiyama K., Stephenson J.D. Chronic treatment with tianeptine attenuates the behavioural effects induced by 5-HTP, but not the effects on hippocampal 5-HT concentrations. Neurosci. Res. Commun. 22:1998;107-116.
25. Lacroix P., Rocher N., Deslandes A. Antidepressant effects of tianeptine, of its two enantiomers and its predominant metabolite in the learned helplessness in rats. Eur. Neuropsychopharmacol. 6(S4-70):1996;1.029.
26. Lahti R.A., Sethy V.H., Barsuhn C., Hester J.B. Pharmachological profile of the antidepressant adinazolam, a triazolobenzodiazepine. Neuropharmacology. 22:1983;1277-1282.
27. A, glucocorticoid, and mineralocorticoid receptor in rat and human hippocampus: implications for the neurobiology of depression. Biol. Psychiatry. 43:1998;547-573.
28. Lowy M.T., Gault L., Yamamoto B.K. Adrenalectomy attenuates stress-induced elevations in extracellular glutamate concentrations in the hippocampus. J. Neurochem. 61:1993;1957-1960.
29. Luine V., Villegas M., Martinez C., McEwen B.S. Repeated stress causes reversible impairments of spatial memory performance. Brain Res. 639:1994;167-170.
30. Magariños A.M., McEwen B.S. Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: comparison of stressors. Neuroscience. 69:1995;83-88.
31. Magariños A.M., McEwen B.S. Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: involvement of glucocorticoid secretion and excitatory amino acid receptors. Neuroscience. 69:1995;89-98.
32. Magariños A.M., McEwen B.S. Differential effects of chronic stress and oral corticosterone on the hippocampal mossy fiber terminals ultrastructure: prevention by tianeptine. Abstr. Soc. Neurosci. 23(720.4):1997;1849.
33. 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. 16:1996;3534-3540.
34. Magariños A.M., Garcia Verdugo J.M., McEwen B.S. Chronic stress alters synaptic terminal structure in the hippocampus. Proc. Natl. Acad. Sci. USA. 94:1997;14002-14008.
35. Magariños A.M., Orchinik M., McEwen B.S. Morphological changes in the hippocampal CA3 region induced by non-invasive glucocorticoid administration: a paradox. Brain Res. 809:1998;314-318.
36. McEwen B.S. Possible mechanisms for atrophy of the human hippocampus. Mol. Psychiatry. 2:1997;255-262.
37. McKittrick, C.R., McEwen, B.S., 1996. Regulation of serotonergic function in the CNS by steroid hormones and stress. In: Stone, T.W. (Ed.), CNS Neurotransmitters and Neuromodulators: Neuroactive Steroids. CRC Press, Boca Raton, FL, pp. 37-76.
38. McKittrick C.R., Magariños A.M., Blanchard D.C., Blanchard R.J., McEwen B.S., Sakai R.R. Chronic social stress decreases binding to 5-HT transporter sites and reduces dendritic arbors in CA3 of hippocampus. Abstr. Soc. Nerurosci. 22(809.18):1996;2060.
39. 1A receptor expression in adrenally intact rats: implication for the pathogenesis of depression. Neuroscience. 80:1997;419-426.
40. Mendelson S.D., McEwen B.S. Autoradiographic analyses of the effects of adrenalectomy and corticosterone on 5-HT1A and 5-HT1B receptors in the dorsal hippocampus and cortex of the rat. Neuroendocrinology. 55:1992;444-450.
41. Mocaër E., Rettori M.C., Kamoun A. Pharmacological antidepressive effects and tianeptine-induced 5-HT uptake increase. Clin. Neuropharmacol. 11:1988;S32-S42.
42. Moghaddam B., Bolinao M.L., Stein-Behrens B., Sapolsky R. Glucocorticoids mediate the stress-induced extracellular accumulation of glutamate. Brain Res. 655:1994;251-254.
43. Mongeau R., Blier P., de Montigny C. The serotonergic and noradrenergic systems of the hippocampus: their interactions and the effects of antidepressants treatments. Brain Res. Rev. 23:1997;145-195.
44. Mück-Seler D., Jevric-Causevic A., Diksic M. Influence of fluoxetine on regional serotonin synthesis in the rat brain. J. Neurochem. 67:1996;24324-24342.
45. Nadler V., Perry W.P., Cotman C.W. Selective reinnervation of hippocampal area CA1 and the fascia dentata after destruction of CA3-CA4 afferents with kainic acid. Brain Res. 182:1980;1-9.
46. O'Connor W.T., Earley B., Leonard B.E. Antidepressant properties of the triazolobenzodiazepines alprazolam and adinazolam: studies on the olfactory bulbectomized rat model of depression. Br. J. Clin. Pharmacol. 19:1985;45S-56S.
47. Ohi K., Mikuni M., Takahashi Stress adaptation and hypersensitivity in 5-HT neuronal systems after repeated foot shock. Pharmacol. Biochem. Behav. 34:1989;603-608.
48. Oluyomi A.O., Datla K.P., Curzon G. Effects of the (+) and (-) enantiomers of the antidepressant drug tianeptine on 5-HTP induced behavior. Neuropharmacology. 36:1997;383-387.
49. Page M.E., Abercrombie E.D. An analysis of the effects of acute and chronic fluoxetine on extracellular norepinephrine in the rat hippocampus during stress. Neuropsychopharmacology. 16:1997;419-425.
50. Post R.M. Transduction of psychosocial stress into the neurobiology of recurrent affective disorder. Am. J. Psychiatry. 149:1992;999-1010.
51. Pyapali G.K., Turner D.A. Denervation-induced alterations in CA1 pyramidal neurons following kainic acid lesions in rats. Brain Res. 652:1994;279-290.
52. Rahman S., Neuman R.S. Activation of 5-HT2 receptors facilitates depolarization of neocortical neurons by N-methyl-D-aspartate. Eur. J. Pharmacol. 231:1993;347-354.
53. Rutter J.J., Gundlah C., Auerbach S.B. Increase in extracellular serotonin produced by uptake inhibitors is enhanced after chronic treatment with fluoxetine. Neurosci. Lett. 171:1994;183-186.
54. Sapolsky R.M. Why stress is bad for your brain? Science. 273(5276):1996;749-750.
55. Sheline Y.I., Wang P.W., Gado M.H., Csernansky J.C., Vannier M.W. Hippocampal atrophy in recurrent major depression. Proc. Natl. Acad. Sci. USA. 93:1996;3908-3913.
56. Singh V., Corley K., Phan T., Boadle-Biber M. Increases in the activity of tryptophan hydroxylase from rat cortex and midbrain in response to acute or repeated sound stress are blocked by adrenalectomy and restored by dexamethasone treatment. Brain Res. 516:1990;66-76.
57. Sunanda R.M.S., Raju T.R. Effect of chronic restraint stress on dendritic spines and excrescences of hippocampal CA3 pyramidal neurons - a quantitative study. Brain Res. 694:1995;312-317.
58. Trouvin J.H., Gardier A.M., Chanut E., Pages N., Jacquot C. Time course of brain serotonin metabolism after cessation of long-term fluoxetine treatment in the rat. Life Sci. 52:1993;187-192.
59. Turmel A., De Montigny C. Sensitization of rat forebrain neurons to serotonin by adinazolam, an antidepressant triazolobenzodiazepine. Eur. J. Pharmacol. 99:1984;241-244.
60. Turner D.A., Buhl E.H., Hailer N.P., Nitsch R. Morphological features of the entorhinal-hippocampal connection. Progress in Neurobiology. 55:1998;537-562.
61. Watanabe Y., Gould E., McEwen B.S. Stress induces atrophy of apical dendrites of hippocampus CA3 pyramidal neurons. Brain Res. 588:1992;341-344.
62. Watanabe Y., Gould E., Cameron H., Daniels D., McEwen B.S. Tianeptine attenuates stress-induced morphological changes in the hippocampus. Eur. J. Pharmacol. 222:1992;157-162.
63. Watanabe Y., Weiland N.G., McEwen B.S. Effects of adrenal steroid manipulations and repeated restraint stress on dynorphin mRNA levels and excitatory amino acid receptor binding in hippocampus. Brain Res. 680:1995;217-225.
64. Weiland N.G., Orchinik M., Tanapat P. Chronic corticosterone treatment induces parallel changes in N-methyl-D-aspartate receptor subunit messenger RNA levels and antagonist binding sites in the hippocampus. Neuroscience. 78:1997;653-662.
65. Wilde M.I., Benfield P. Tianeptine. A review of its pharmacodynamic and pharmacokinetic properties, and therapeutic efficacy in depression and coexisting anxiety and depression. Drugs. 49:1995;411-439.
66. Woolley C.S., Gould E., McEwen B.S. Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons. Brain Res. 531:1990;225-231.