Fluoxetine affects hippocampal plasticity, apoptosis and depressive-like behavior of chronically isolated rats

Progress in Neuro-Psychopharmacology and Biological Psychiatry

Volumn 36, Issue 1, 2012, Pages 92-100

  Djordjevic, Ana ^b   Djordjevic, Jelena ^a   Elaković, Ivana ^b   Adzic, Miroslav ^a   Matić, Gordana ^b   Radojcic, Marija B ^a  

^a UNIVERSITY OF BELGRADE   (Serbia)

^b UNIVERSITY OF BELGRADE   (Serbia)

Author keywords

Antidepressant fluoxetine; Apoptosis; Forced swimming test; Hippocampus; Plasticity; Stress

Indexed keywords

BIOLOGICAL MARKER; FLUOXETINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN BAX; PROTEIN BCL 2; SYNAPTOSOMAL POLYSIALIC NERVE CELL ADHESION MOLECULE; SYNTAXIN 1; UNCLASSIFIED DRUG;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL COMPARTMENTALIZATION; CELL STRESS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; DEPRESSION; DRUG MECHANISM; FORCED SWIMMING TEST; HIPPOCAMPUS; LONG TERM CARE; MALE; MITOCHONDRION; MOLECULAR DYNAMICS; NERVE CELL PLASTICITY; NONHUMAN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; REGULATORY MECHANISM; SOCIAL ISOLATION;

ANIMALS; APOPTOSIS; DEPRESSION; FLUOXETINE; HIPPOCAMPUS; MALE; NEURONAL PLASTICITY; RATS; RATS, WISTAR; SOCIAL ISOLATION; SYNAPTOSOMES;

EID: 82555170339     PISSN: 02785846     EISSN: 18784216     Source Type: Journal    
DOI: 10.1016/j.pnpbp.2011.10.006     Document Type: Article

References (106)

1. Adzic M., Djordjevic A., Demonacos C., Krstic-Demonacos M., Radojcic M.B. The role of phosphorylated glucocorticoid receptor in mitochondrial functions and apoptotic signalling in brain tissue of stressed Wistar rats. Int J Biochem Cell Biol 2009, 41:2181-2188.
2. Arantes-Goncalves F., Coelho R. Depression and treatment. Apoptosis, neuroplasticity and antidepressants. Acta Med Port 2006, 19:9-20.
3. 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.
4. Bilici M., Efe H., Koroglu M.A., Uydu H.A., Bekaroglu M., Deger O. Antioxidative enzyme activities and lipid peroxidation in major depression: alterations by antidepressant treatments. J Affect Disord 2001, 64:43-51.
5. Bonfanti L. PSA-NCAM in mammalian structural plasticity and neurogenesis. Prog Neurobiol 2006, 80:129-164.
6. 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.
7. Bremner J., Narayan M., Anderson E.R., Staib L.H., Miller H.L., Charney D.S. Hippocampal volume reduction in major depression. Am J Psychiatry 2000, 157:115-118.
8. Brenes J.C., Fornaguera J. The effect of chronic fluoxetine on social isolation induced changes on sucrose consumption, immobility behavior, and on serotonin and dopamine function in hippocampus and ventral striatum. Behav Brain Res 2009, 198:199-205.
9. Bruses J.L., Chauvet N., Rubio M.E., Rutishauser U. Polysialic acid and the formation of oculomotor synapses on chick ciliary neurons. J Comp Neurol 2002, 446:244-256.
10. Calakos N., Scheller R.H. Vesicle-associated membrane protein and synaptophysin are associated on the synaptic vesicle. J Biol Chem 1994, 269:24534-24537.
11. Cameron H.A., Gould E. Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neuroscience 1994, 61:203-209.
12. Cameron H.A., McKay R.D. Restoring production of hippocampal neurons in old age. Nat Neurosci 1999, 2:894-897.
13. Cao G., Minami M., Pei W., Yan C., Chen D., O'Horo C., et al. Intracellular Bax translocation after transient cerebral ischemia: implications for a role of the mitochondrial apoptotic signaling pathway in ischemic neuronal death. J Cereb Blood Flow Metab 2001, 21:321-333.
14. Castren E. Is mood chemistry?. Nat Rev Neurosci 2005, 6:241-246.
15. Chen D.F., Schneider G.E., Martinou J.C., Tonegawa S. Bcl-2 promotes regeneration of severed axons in mammalian CNS. Nature 1997, 385:434-439.
16. Chiou S.H., Chen S.J., Peng C.H., Chang Y.L., Ku H.H., Hsu W.M., et al. Fluoxetine up-regulates expression of cellular FLICE-inhibitory protein and inhibits LPS-induced apoptosis in hippocampus-derived neural stem cell. Biochem Biophys Res Commun 2006, 343:391-400.
17. Chiou S.H., Ku H.H., Tsai T.H., Lin H.L., Chen L.H., Chien C.S., et al. Moclobemide upregulated Bcl-2 expression and induced neural stem cell differentiation into serotoninergic neuron via extracellular-regulated kinase pathway. Br J Pharmacol 2006, 148:587-598.
18. Cogswell P.C., Kashatus D.F., Keifer J.A., Guttridge D.C., Reuther J.Y., Bristow C., et al. NF-kappa B and I kappa B alpha are found in the mitochondria. Evidence for regulation of mitochondrial gene expression by NF-kappa B. J Biol Chem 2003, 278:2963-2968.
19. Cory S., Adams J.M. The Bcl2 family: regulators of the cellular life-or-death switch. Nat Rev Cancer 2002, 2:647-656.
20. Cryan J.F., Markou A., Lucki I. Assessing antidepressant activity in rodents: recent developments and future needs. Trends Pharmacol Sci 2002, 22:238-245.
21. Cryan J.F., Page M.E., Lucki I. Differential behavioral effects of the antidepressants reboxetine, fluoxetine, and moclobemide in a modified forced swim test following chronic treatment. Psychopharmacology (Berl) 2005, 182:335-344.
22. Cryan J.F., Valentino R.J., Lucki I. Assessing substrates underlying the behavioral effects of antidepressants using the modified rat forced swimming test. Neurosci Biobehav Rev 2005, 29:547-569.
23. Dandekar M.P., Singru P.S., Kokare D.M., Subhedar N.K. Cocaine- and amphetamine-regulated transcript peptide (CART) plays a role in the manifestation of depression: social isolation and olfactory bulbectomy models reveal unifying principles. Neuropsychopharmacology 2009, 34:1288-1300.
24. Davies A.M. The Bcl-2 family of proteins, and the regulation of neuronal survival. Trends Neurosci 1995, 18:355-358.
25. Djordjevic A., Adzic M., Djordjevic J., Radojcic M.B. Chronic social isolation is related to both upregulation of plasticity genes and initiation of proapoptotic signaling in Wistar rat hippocampus. J Neural Transm 2009, 116:1579-1589.
26. Djordjevic J., Djordjevic A., Adzic M., Elaković I., Matić G., Radojcic M.B. Fluoxetine affects antioxidant system and promotes apoptotic signaling in Wistar rat liver. Eur J Pharmacol 2011, 659:61-66.
27. D'Sa C., Duman R.S. Antidepressants and neuroplasticity. Bipolar Disord 2002, 4:183-194.
28. Duman R.S. A case of neuronal life and death?. Biol Psychiatry 2004, 56:140-145.
29. Duman R.S., Monteggia L.M. A neurotrophic model for stress-related mood disorders. Biol Psychiatry 2006, 59:1116-1127.
30. Fatemi S.H., Earle J.A., Stary J.M., Lee S., Sedgewick J. Altered levels of the synaptosomal associated protein SNAP-25 in hippocampus of subjects with mood disorders and schizophrenia. Neuroreport 2001, 12:3257-3262.
31. Fuchs E., Flugge G. Cellular consequences of stress and depression. Dialogues Clin Neurosci 2004, 6:171-183.
32. Gao Y., Bezchlibnyk Y.B., Sun X., Wang J.F., McEwen B.S., Young L.T. Effects of restraint stress on the expression of proteins involved in synaptic vesicle exocytosis in the hippocampus. Neuroscience 2006, 141:1139-1148.
33. Gascon E., Vutskits L., Kiss J.Z. Polysialic acid-neural cell adhesion molecule in brain plasticity: from synapses to integration of new neurons. Brain Res Rev 2007, 56:101-118.
34. Gelder M., Mayou R., Geddes J. Psychiatry 2005, Oxford University Press, New York. 3rd ed.
35. Grippo A.J., Trahanas D.M., Zimmerman R.R., Porges S.W., Carter C.S. Oxytocin protects against negative behavioral and autonomic consequences of long-term social isolation. Psychoneuroendocrinology 2009, 34:1542-1553.
36. Guirado R., Varea E., Castillo-Gomez E., Gomez-Climent M.A., Rovira-Esteban L., Blasco-Ibanez J.M., et al. Effects of chronic fluoxetine treatment on the rat somatosensory cortex: activation and induction of neuronal structural plasticity. Neurosci Lett 2009, 457:12-15.
37. Gupta G.L., Rana A.C. Effect of Withania somnifera Dunal in ethanol-induced anxiolysis and withdrawal anxiety in rats. Indian J Exp Biol 2008, 46:470-475.
38. Hajszan T., MacLusky N.J., Leranth C. Short-term treatment with the antidepressant fluoxetine triggers pyramidal dendritic spine synapse formation in rat hippocampus. Eur J Neurosci 2005, 21:1299-1303.
39. Haynes L.E., Barber D., Mitchell I.J. Chronic antidepressant medication attenuates dexamethasone-induced neuronal death and sublethal neuronal damage in the hippocampus and striatum. Brain Res 2004, 1026:157-167.
40. Henn F.A., Vollmayr B. Neurogenesis and depression: etiology or epiphenomenon?. Biol Psychiatry 2004, 56:146-150.
41. Heritch A.J., Henderson K., Westfall T.C. Effects of social isolation on brain catecholamines and forced swimming in rats: prevention by antidepressant treatment. J Psychiatr Res 1990, 24:251-258.
42. Huether G., Schuff-Werner P. Platelet serotonin acts as a locally releasable antioxidant. Adv Exp Med Biol 1996, 398:299-306.
43. Jorgensen O.S., Riederer P. Increased synaptic markers in hippocampus of depressed patients. J Neural Transm 1985, 64:55-66.
44. Kaltschmidt C., Kaltschmidt B., Baeuerle P.A. Brain synapses contain inducible forms of the transcription factor NF-kappa B. Mech Dev 1993, 43:135-147.
45. Karim A., Arslan M.I. Isolation modifies the behavioural response in rats. Bangladesh Med Res Counc Bull 2000, 26:27-32.
46. Keuker J., Vollmann-Honsdorf G.K., Fuchs E. How to use the optical frac- tionator: an example based on the estimation of neurons in the hippocampal CA1 and CA3 regions of tree shrews. Brain Res. Protocols. 2001, 2001:211-221.
47. Kirkova M., Tzvetanova E., Vircheva S., Zamfirova R., Grygier B., Kubera M. Antioxidant activity of fluoxetine: studies in mice melanoma model. Cell Biochem Funct 2010, 28:497-502.
48. Kokare D.M., Dandekar M.P., Singru P.S., Gupta G.L., Subhedar N.K. Involvement of alpha-MSH in the social isolation induced anxiety- and depression-like behaviors in rat. Neuropharmacology 2010, 58:1009-1018.
49. Kucharczak J., Simmons M.J., Fan Y., Gelinas C. To be, or not to be: NF-kappaB is the answer-role of Rel/NF-kappaB in the regulation of apoptosis. Oncogene 2003, 22:8961-8982.
50. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
51. Lee H.J., Kim J.W., Yim S.V., Kim M.J., Kim S.A., Kim Y.J., et al. Fluoxetine enhances cell proliferation and prevents apoptosis in dentate gyrus of maternally separated rats. Mol Psychiatry 2001, 6:725-728.
52. Levkovitz Y., Gil-Ad I., Zeldich E., Dayag M., Weizman A. Differential induction of apoptosis by antidepressants in glioma and neuroblastoma cell lines: evidence for p-c-Jun, cytochrome c, and caspase-3 involvement. J Mol Neurosci 2005, 27:29-42.
53. Lindsten T., Zong W.X., Thompson C.B. Defining the role of the Bcl-2 family of proteins in the nervous system. Neuroscientist 2005, 11:10-15.
54. Lirk P., Haller I., Hausott B., Ingorokva S., Deibl M., Gerner P., et al. The neurotoxic effects of amitriptyline are mediated by apoptosis and are effectively blocked by inhibition of caspase activity. Anesth Analg 2006, 102:1728-1733.
55. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. Protein measurement with the Folin phenol reagent. J Biol Chem 1951, 193:265-267.
56. 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.
57. Lucassen P.J., Vollmann-Honsdorf G.K., Gleisberg M., Czeh B., De Kloet E.R., Fuchs E. Chronic psychosocial stress differentially affects apoptosis in hippocampal subregions and cortex of the adult tree shrew. Eur J Neurosci 2001, 14:161-166.
58. 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.
59. Lynch M.A., Voss K.L. Presynaptic changes in long-term potentiation: elevated synaptosomal calcium concentration and basal phosphoinositide turnover in dentate gyrus. J Neurochem 1991, 56:113-118.
60. MacQueen G., Frodl T. The hippocampus in major depression: evidence for the convergence of the bench and bedside in psychiatric research?. Mol Psychiatry 2011, 16:252-264.
61. Magarinos 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.
62. Magarinos A.M., Verdugo J.M., McEwen B.S. Chronic stress alters synaptic terminal structure in hippocampus. Proc Natl Acad Sci U S A 1997, 94:14002-14008.
63. Manji H.K., Drevets W.C., Charney D.S. The cellular neurobiology of depression. Nat Med 2001, 7:541-547.
64. Mattson M.P. NF-kappaB in the survival and plasticity of neurons. Neurochem Res 2005, 30:883-893.
65. McEwen B.S. Glucocorticoids, depression, and mood disorders: structural remodeling in the brain. Metabolism 2005, 54:20-23.
66. 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.
67. McKernan D.P., Dinan T.G., Cryan J.F. "Killing the Blues": a role for cellular suicide (apoptosis) in depression and the antidepressant response?. Prog Neurobiol 2009, 88:246-263.
68. McKittrick C.R., Magarinos A.M., Blanchard D.C., Blanchard R.J., McEwen B.S., Sakai R.R. Chronic social stress reduces dendritic arbors in CA3 hippocampus and decreases binding to serotonin transporter sites. Synapse 2000, 236:85-94.
69. Meffert M.K., Baltimore D. Physiological functions for brain NF-kappaB. Trends Neurosci 2005, 28:37-43.
70. Meffert M.K., Chang J.M., Wiltgen B.J., Fanselow M.S., Baltimore D. NF-kappa B functions in synaptic signaling and behavior. Nat Neurosci 2003, 6:1072-1078.
71. Moutsatsou P., Psarra A.M.G., Tsiapara A., Paraskevakou H., Davaris P., Sekeris C.E. Localization of the glucocorticoid receptor in rat brain mitochondria. Arch Biochem Biophys 2001, 386:69-78.
72. Muller H.K., Wegener G., Popoli M., Elfving B. Differential expression of synaptic proteins after chronic restraint stress in rat prefrontal cortex and hippocampus. Brain Res 2011, 1385:26-37.
73. Nacher J., Blasco-Ibanez J.M., McEwen B.S. Non-granule PSA-NCAM immunoreactive neurons in the rat hippocampus. Brain Res 2002, 930:1-11.
74. O'Neill L.A., Kaltschmidt C. NF-kappa B: a crucial transcription factor for glial and neuronal cell function. Trends Neurosci 1997, 20:252-258.
75. Pham K., Nacher J., Hof P.R., McEwen B.S. Repeated restraint stress suppresses neurogenesis and induces biphasic PSA-NCAM expression in the adult rat dentate gyrus. Eur J Neurosci 2003, 17:879-886.
76. Piccotti J.R., LaGattuta M.S., Knight S.A., Gonzales A.J., Bleavins M.R. Induction of apoptosis by cationic amphiphilic drugs amiodarone and imipramine. Drug Chem Toxicol 2005, 28:117-133.
77. 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.
78. Porsolt R.D., Pichon M.L., Jalfre M. Depression: a new model sensitive to the antidepresant treatment. Nature 1977, 266:730-742.
79. Prabhakar A.H., Patel V.B., Giridhar R. Spectrophotometric determination of fluoxetine hydrochloride in bulk and in pharmaceutical formulations. J Pharm Biomed Anal 1999, 20:427-432.
80. Qi H., Chen H.Z., Jin Z.J. Caspase 3 gene expression and [Ca2+]i homeostasis underlying desipramine-induced C6 glioma cell apoptosis. Acta Pharmacol Sin 2002, 23:803-807.
81. Rapp S., Baader M., Hu M., Jennen-Steinmetz C., Henn F.A., Thome J. Differential regulation of synaptic vesicle proteins by antidepressant drugs. Pharmacogenomics J 2004, 4:110-113.
82. Reif A., Fritzen S., Finger M., Strobel A., Lauer M., Schmitt A., et al. Neural stem cell proliferation is decreased in schizophrenia, but not in depression. Mol Psychiatry 2006, 11:514-522.
83. Ryu V., Yoo S.B., Kang D.W., Lee J.H., Jahng J.W. Post-weaning isolation promotes food intake and body weight gain in rats that experienced neonatal maternal separation. Brain Res 2009, 1295:127-134.
84. Sandi C. Stress, cognitive impairment and cell adhesion molecules. Nat Rev Neurosci 2004, 5:917-930.
85. Sandi C., Merino J.J., Cordero M.I., Touyarot K., Venero C. Effects of chronic stress on contextual fear conditioning and the hippocampal expression of the neural cell adhesion molecule, its polysialylation, and L1. Neuroscience 2001, 102:329-339.
86. 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.
87. Sapolsky R.M. Why stress is bad for your brain. Science 1996, 273:749-750.
88. Sapolsky R.M. Stress and plasticity in the limbic system. Neurochem Res 2003, 28:1735-1742.
89. Schreck R., Meier B., Maennel D.N., Droge W., Baeuerle P.A. Dithiocarbamates as potent inhibitors of nuclear factor ΚB activation in intact cells. J Exp Med 1992, 175:1181-1194.
90. Seki T., Arai Y. Highly polysialylated neural cell adhesion molecule (NCAM-H) is expressed by newly generated granule cells in the dentate gyrus of the adult rat. J Neurosci 1993, 13:2351-2358.
91. Serafeim A., Holder M.J., Grafton G., Chamba A., Drayson M.T., Luong Q.T., et al. Selective serotonin reuptake inhibitors directly signal for apoptosis in biopsy-like Burkitt lymphoma cells. Blood 2003, 101:3212-3219.
92. Sheline Y., Sanghavi M., Mintun M.A., Gado M.H. Depression duration but not age predicts hippocampal volume loss in medically healthy women with recurrent major depression. J Neurosci 1999, 19:5034-5043.
93. Sollner T., Whiteheart S.W., Brunner M., Erdjument-Bromage H., Geromanos S., Tempst P., et al. SNAP receptors implicated in vesicle targeting and fusion. Nature 1993, 362:318-324.
94. Spencer R.L., Kalman B.A., Cotter C.S., Deak T. Discrimination between changes in glucocorticoid receptor expressionand activation in rat brain using western blot analysis. Brain Res 2000, 868:275-286.
95. Sudhof T.C. The synaptic vesicle cycle. Annu Rev Neurosci 2004, 27:509-547.
96. Varea E., Blasco-Ibanez J.M., Gomez-Climent M.A., Castillo-Gomez E., Crespo C., Martinez-Guijarro F.J., et al. Chronic fluoxetine treatment increases the expression of PSA-NCAM in the medial prefrontal cortex. Neuropsychopharmacology 2007, 32:803-812.
97. Varea E., Castillo-Gomez E., Gomez-Climent M.A., Blasco-Ibanez J.M., Crespo C., Martinez-Guijarro F.J., et al. Chronic antidepressant treatment induces contrasting patterns of synaptophysin and PSA-NCAM expression in different regions of the adult rat telencephalon. Eur Neuropsychopharmacol 2007, 17:546-557.
98. Wang D., Shu Cheng An S., Zhang X. Prevention of chronic stress-induced depression-like behavior by inducible nitric oxide inhibitor. Neurosci Lett 2008, 433:59-64.
99. Watanabe Y., Gould E., McEwen B.S. Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Res 1992, 588:341-345.
100. Wellmann H., Kaltschmidt B., Kaltschmidt C. Retrograde transport of transcription factor NF-kappa B in living neurons. J Biol Chem 2001, 276:11821-11829.
101. Willner P. Validity, reliability and utility of the chronic mild stress model of depression: a 10-year review and evaluation. Psychopharmacology (Berl) 1997, 134:319-329.
102. Wilson B.E., Mochon E., Boxer L.M. Induction of bcl-2 expression by phosphorylated CREB proteins during B-cell activation and rescue from apoptosis. Mol Cell Biol 1996, 16:5546-5556.
103. Wong D.T., Bymaster F.P., Engleman E.A. Prozac (Fluoxetine, Lilly 11040), the first selective serotonin uptake inhibitor and an antidepressant drug: twenty years since its first publication. Life Sci 1995, 57:411-441.
104. Xu H., Richardson J.S., Li X.M. Dose-related effects of chronic antidepressants on neuroprotective proteins BDNF, Bcl-2 and Cu/Zn-SOD in rat hippocampus. Neuropsychopharmacology 2003, 28:53-62.
105. Zafir A., Banu N. Antioxidant potential of fluoxetine in comparison to Curcuma longa in restraint-stressed rats. Eur J Pharmacol 2007, 572:23-31.
106. Zink M., Rapp S., Gebicke-Haerter P.J., Henn F.A., Thome J. Antidepressants differentially affect expression of complexin I and II RNA in rat hippocampus. Psychopharmacology (Berl) 2005, 181:560-565.