Chronic fluoxetine treatment increases expression of synaptic proteins in the hippocampus of the ovariectomized rat: Role of BDNF signalling

Psychoneuroendocrinology

Volumn 34, Issue 3, 2009, Pages 367-381

  O'Leary, Olivia F ^a   Wu, Xuefei ^a   Castren, Eero ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

Author keywords

AMPA; Antidepressant; BDNF; Ovariectomy; Plasticity; PSD 95

Indexed keywords

AMPA RECEPTOR; BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; FLUOXETINE; NERVE PROTEIN; PHOSPHOSYNAPSIN; POSTSYNAPTIC DENSITY PROTEIN 95; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; CHRONIC DRUG ADMINISTRATION; CONTROLLED STUDY; FEMALE; GENOTYPE; HIPPOCAMPUS; NERVE CELL PLASTICITY; NERVE CONDUCTION; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; SYNAPSE; TRANSGENIC MOUSE; WESTERN BLOTTING; WILD TYPE;

ANIMALS; ANTIDEPRESSIVE AGENTS, SECOND-GENERATION; BODY WEIGHT; FEMALE; FLUOXETINE; HIPPOCAMPUS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; ORGAN SIZE; OVARIECTOMY; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, TRKB; RECEPTORS, AMPA; RECEPTORS, NEUROTRANSMITTER; SIGNAL TRANSDUCTION; SYNAPSINS; UTERUS;

EID: 59249099507     PISSN: 03064530     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2008.09.015     Document Type: Article

References (83)

1. Adachi M., Barrot M., Autry A.E., Theobald D., and Monteggia L.M. Selective loss of brain-derived neurotrophic factor in the dentate gyrus attenuates antidepressant efficacy. Biol. Psychiatry 63 (2008) 642-649
2. Alt A., Nisenbaum E.S., Bleakman D., and Witkin J.M. A role for AMPA receptors in mood disorders. Biochem. Pharmacol. 71 (2006) 1273-1288
3. Alves S.E., Hoskin E., Lee S.J., Brake W.G., Ferguson D., Luine V., Allen P.B., Greengard P., and McEwen B.S. Serotonin mediates CA1 spine density but is not crucial for ovarian steroid regulation of synaptic plasticity in the adult rat dorsal hippocampus. Synapse 45 (2002) 143-151
4. Bai F., Bergeron M., and Nelson D.L. Chronic AMPA receptor potentiator (LY451646) treatment increases cell proliferation in adult rat hippocampus. Neuropharmacology 44 (2003) 1013-1021
5. Barbiero V.S., Giambelli R., Musazzi L., Tiraboschi E., Tardito D., Perez J., Drago F., Racagni G., and Popoli M. Chronic antidepressants induce redistribution and differential activation of alphaCaM kinase II between presynaptic compartments. Neuropsychopharmacology 32 (2007) 2511-2519
6. Bats C., Groc L., and Choquet D. The interaction between Stargazin and PSD-95 regulates AMPA receptor surface trafficking. Neuron 53 (2007) 719-734
7. Bresler T., Ramati Y., Zamorano P.L., Zhai R., Garner C.C., and Ziv N.E. The dynamics of SAP90/PSD-95 recruitment to new synaptic junctions. Mol. Cell. Neurosci. 18 (2001) 149-167
8. Caldeira M.V., Melo C.V., Pereira D.B., Carvalho R., Correia S.S., Backos D.S., Carvalho A.L., Esteban J.A., and Duarte C.B. Brain-derived neurotrophic factor regulates the expression and synaptic delivery of alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptor subunits in hippocampal neurons. J. Biol. Chem. 282 (2007) 12619-12628
9. Carboni L., Vighini M., Piubelli C., Castelletti L., Milli A., and Domenici E. Proteomic analysis of rat hippocampus and frontal cortex after chronic treatment with fluoxetine or putative novel antidepressants: CRF1 and NK1 receptor antagonists. Eur. Neuropsychopharmacol. 16 (2006) 521-537
10. Castren E. Is mood chemistry?. Nat. Rev. Neurosci. 6 (2005) 241-246
11. Castren E., Voikar V., and Rantamaki T. Role of neurotrophic factors in depression. Curr. Opin. Pharmacol. 7 (2007) 18-21
12. Charney D.S., and Manji H.K. Life stress, genes, and depression: multiple pathways lead to increased risk and new opportunities for intervention. Sci. STKE 2004 (2004) re5
13. Chen L., Chetkovich D.M., Petralia R.S., Sweeney N.T., Kawasaki Y., Wenthold R.J., Bredt D.S., and Nicoll R.A. Stargazin regulates synaptic targeting of AMPA receptors by two distinct mechanisms. Nature 408 (2000) 936-943
14. Chen X., Vinade L., Leapman R.D., Petersen J.D., Nakagawa T., Phillips T.M., Sheng M., and Reese T.S. Mass of the postsynaptic density and enumeration of three key molecules. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 11551-11556
15. Cheng D., Hoogenraad C.C., Rush J., Ramm E., Schlager M.A., Duong D.M., Xu P., Wijayawardana S.R., Hanfelt J., Nakagawa T., Sheng M., and Peng J. Relative and absolute quantification of postsynaptic density proteome isolated from rat forebrain and cerebellum. Mol. Cell. Proteomics 5 (2006) 1158-1170
16. Czeh B., Muller-Keuker J.I., Rygula R., Abumaria N., Hiemke C., Domenici E., and Fuchs E. Chronic social stress inhibits cell proliferation in the adult medial prefrontal cortex: hemispheric asymmetry and reversal by fluoxetine treatment. Neuropsychopharmacology 32 (2007) 1490-1503
17. D'Souza D.N., Zhang Y., Garcia F., Battaglia G., and Van de Kar L.D. Fluoxetine-induced changes in body weight and 5-HT1A receptor-mediated hormone secretion in rats on a tryptophan-deficient diet. Am. J. Physiol. Regul. Integr. Comp. Physiol. 286 (2004) R390-397
18. De Camilli P., Cameron R., and Greengard P. Synapsin I (protein I), a nerve terminal-specific phosphoprotein. I. Its general distribution in synapses of the central and peripheral nervous system demonstrated by immunofluorescence in frozen and plastic sections. J. Cell. Biol. 96 (1983) 1337-1354
19. Derkach V.A., Oh M.C., Guire E.S., and Soderling T.R. Regulatory mechanisms of AMPA receptors in synaptic plasticity. Nat. Rev. Neurosci. 8 (2007) 101-113
20. Du J., Suzuki K., Wei Y., Wang Y., Blumenthal R., Chen Z., Falke C., Zarate Jr. C.A., and Manji H.K. The anticonvulsants lamotrigine, riluzole, and valproate differentially regulate AMPA receptor membrane localization: relationship to clinical effects in mood disorders. Neuropsychopharmacology 32 (2007) 793-802
21. Ehrlich I., Klein M., Rumpel S., and Malinow R. PSD-95 is required for activity-driven synapse stabilization. Proc. Natl. Acad. Sci. U.S.A. 104 (2007) 4176-4181
22. Ehrlich I., and Malinow R. Postsynaptic density 95 controls AMPA receptor incorporation during long-term potentiation and experience-driven synaptic plasticity. J. Neurosci. 24 (2004) 916-927
23. El-Husseini A.E., Schnell E., Chetkovich D.M., Nicoll R.A., and Bredt D.S. PSD-95 involvement in maturation of excitatory synapses. Science (New York, NY) 290 (2000) 1364-1368
24. El-Husseini Ael D., Schnell E., Dakoji S., Sweeney N., Zhou Q., Prange O., Gauthier-Campbell C., Aguilera-Moreno A., Nicoll R.A., and Bredt D.S. Synaptic strength regulated by palmitate cycling on PSD-95. Cell 108 (2002) 849-863
25. Elias G.M., and Nicoll R.A. Synaptic trafficking of glutamate receptors by MAGUK scaffolding proteins. Trends Cell. Biol. 17 (2007) 343-352
26. Fdez E., and Hilfiker S. Vesicle pools and synapsins: new insights into old enigmas. Brain Cell. Biol. 35 (2006) 107-115
27. Ferreira A., and Rapoport M. The synapsins: beyond the regulation of neurotransmitter release. Cell. Mol. Life Sci. 59 (2002) 589-595
28. Gamaro G.D., Prediger M.E., Lopes J., Bassani M.G., and Dalmaz C. Fluoxetine alters feeding behavior and leptin levels in chronically-stressed rats. Pharmacol. Biochem. Behav. 90 (2008) 312-317
29. Gould E., Woolley C.S., Frankfurt M., and McEwen B.S. Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J. Neurosci. 10 (1990) 1286-1291
30. Gould T.D., O'Donnell K.C., Dow E.R., Du J., Chen G., and Manji H.K. Involvement of AMPA receptors in the antidepressant-like effects of lithium in the mouse tail suspension test and forced swim test. Neuropharmacology 54 (2008) 577-587
31. Greengard P., Valtorta F., Czernik A.J., and Benfenati F. Synaptic vesicle phosphoproteins and regulation of synaptic function. Science (New York, NY) 259 (1993) 780-785
32. Grippo A.J., Beltz T.G., Weiss R.M., and Johnson A.K. The effects of chronic fluoxetine treatment on chronic mild stress-induced cardiovascular changes and anhedonia. Biol. Psychiatry 59 (2006) 309-316
33. Hajszan T., MacLusky N.J., and Leranth C. Short-term treatment with the antidepressant fluoxetine triggers pyramidal dendritic spine synapse formation in rat hippocampus. Eur. J. Neurosci. 21 (2005) 1299-1303
34. Holderbach R., Clark K., Moreau J.L., Bischofberger J., and Normann C. Enhanced long-term synaptic depression in an animal model of depression. Biol. Psychiatry 62 (2007) 92-100
35. Hosaka M., Hammer R.E., and Sudhof T.C. A phospho-switch controls the dynamic association of synapsins with synaptic vesicles. Neuron 24 (1999) 377-387
36. Iwata M., Shirayama Y., Ishida H., and Kawahara R. Hippocampal synapsin I, growth-associated protein-43, and microtubule-associated protein-2 immunoreactivity in learned helplessness rats and antidepressant-treated rats. Neuroscience 141 (2006) 1301-1313
37. Ji Y., Pang P.T., Feng L., and Lu B. Cyclic AMP controls BDNF-induced TrkB phosphorylation and dendritic spine formation in mature hippocampal neurons. Nat. Neurosci. 8 (2005) 164-172
38. Jourdi H., Iwakura Y., Narisawa-Saito M., Ibaraki K., Xiong H., Watanabe M., Hayashi Y., Takei N., and Nawa H. Brain-derived neurotrophic factor signal enhances and maintains the expression of AMPA receptor-associated PDZ proteins in developing cortical neurons. Dev. Biol. 263 (2003) 216-230
39. Jovanovic J.N., Czernik A.J., Fienberg A.A., Greengard P., and Sihra T.S. Synapsins as mediators of BDNF-enhanced neurotransmitter release. Nat. Neurosci. 3 (2000) 323-329
40. Law A.J., Weickert C.S., Hyde T.M., Kleinman J.E., and Harrison P.J. Reduced spinophilin but not microtubule-associated protein 2 expression in the hippocampal formation in schizophrenia and mood disorders: molecular evidence for a pathology of dendritic spines. Am. J. Psychiatry 161 (2004) 1848-1855
41. Lebrun B., Bariohay B., Moyse E., and Jean A. Brain-derived neurotrophic factor (BDNF) and food intake regulation: a minireview. Auton. Neurosci. 126-127 (2006) 30-38
42. Li C., Brake W.G., Romeo R.D., Dunlop J.C., Gordon M., Buzescu R., Magarinos A.M., Allen P.B., Greengard P., Luine V., and McEwen B.S. Estrogen alters hippocampal dendritic spine shape and enhances synaptic protein immunoreactivity and spatial memory in female mice. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 2185-2190
43. Liu F., Day M., Muniz L.C., Bitran D., Arias R., Revilla-Sanchez R., Grauer S., Zhang G., Kelley C., Pulito V., Sung A., Mervis R.F., Navarra R., Hirst W.D., Reinhart P.H., Marquis K.L., Moss S.J., Pangalos M.N., and Brandon N.J. Activation of estrogen receptor-beta regulates hippocampal synaptic plasticity and improves memory. Nat. Neurosci. 11 (2008) 334-343
44. Lu B., Pang P.T., and Woo N.H. The yin and yang of neurotrophin action. Nat. Rev. Neurosci. 6 (2005) 603-614
45. Lustig R.H., Sudol M., Pfaff D.W., and Federoff H.J. Estrogenic regulation and sex dimorphism of growth-associated protein 43 kDa (GAP-43) messenger RNA in the rat. Brain Res. Mol. Brain Res. 11 (1991) 125-132
46. Mackowiak M., O'Neill M.J., Hicks C.A., Bleakman D., and Skolnick P. An AMPA receptor potentiator modulates hippocampal expression of BDNF: an in vivo study. Neuropharmacology 43 (2002) 1-10
47. Magarinos A.M., Deslandes A., and McEwen B.S. Effects of antidepressants and benzodiazepine treatments on the dendritic structure of CA3 pyramidal neurons after chronic stress. Eur. J. Pharmacol. 371 (1999) 113-122
48. Marrs G.S., Green S.H., and Dailey M.E. Rapid formation and remodeling of postsynaptic densities in developing dendrites. Nat. Neurosci. 4 (2001) 1006-1013
49. Martinez-Turrillas R., Del Rio J., and Frechilla D. Sequential changes in BDNF mRNA expression and synaptic levels of AMPA receptor subunits in rat hippocampus after chronic antidepressant treatment. Neuropharmacology 49 (2005) 1178-1188
50. Martinez-Turrillas R., Frechilla D., and Del Rio J. Chronic antidepressant treatment increases the membrane expression of AMPA receptors in rat hippocampus. Neuropharmacology 43 (2002) 1230-1237
51. Martinowich K., Manji H., and Lu B. New insights into BDNF function in depression and anxiety. Nat. Neurosci. 10 (2007) 1089-1093
52. Matsumoto T., Numakawa T., Yokomaku D., Adachi N., Yamagishi S., Numakawa Y., Kunugi H., and Taguchi T. Brain-derived neurotrophic factor-induced potentiation of glutamate and GABA release: different dependency on signaling pathways and neuronal activity. Mol. Cell. Neurosci. 31 (2006) 70-84
53. Matsuzaki M., Ellis-Davies G.C., Nemoto T., Miyashita Y., Iino M., and Kasai H. Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nat. Neurosci. 4 (2001) 1086-1092
54. Maya Vetencourt J.F., Sale A., Viegi A., Baroncelli L., De Pasquale R., O'Leary O.F., Castren E., and Maffei L. The antidepressant fluoxetine restores plasticity in the adult visual cortex. Science (New York, NY) 320 (2008) 385-388
55. Mueller K., and Hsiao S. Estrus- and ovariectomy-induced body weight changes: evidence for two estrogenic mechanisms. J. Comp. Physiol. Psychol. 94 (1980) 1126-1134
56. Nakata H., and Nakamura S. Brain-derived neurotrophic factor regulates AMPA receptor trafficking to post-synaptic densities via IP3R and TRPC calcium signaling. FEBS Lett. 581 (2007) 2047-2054
57. Narisawa-Saito M., Carnahan J., Araki K., Yamaguchi T., and Nawa H. Brain-derived neurotrophic factor regulates the expression of AMPA receptor proteins in neocortical neurons. Neuroscience 88 (1999) 1009-1014
58. Norrholm S.D., and Ouimet C.C. Altered dendritic spine density in animal models of depression and in response to antidepressant treatment. Synapse 42 (2001) 151-163
59. Palizvan M.R., Sohya K., Kohara K., Maruyama A., Yasuda H., Kimura F., and Tsumoto T. Brain-derived neurotrophic factor increases inhibitory synapses, revealed in solitary neurons cultured from rat visual cortex. Neuroscience 126 (2004) 955-966
60. Pittenger C., and Duman R.S. Stress, depression, and neuroplasticity: a convergence of mechanisms. Neuropsychopharmacology 33 (2008) 88-109
61. Rapp S., Baader M., Hu M., Jennen-Steinmetz C., Henn F.A., and Thome J. Differential regulation of synaptic vesicle proteins by antidepressant drugs. Pharmacogenomics J. 4 (2004) 110-113
62. Reines A., Cereseto M., Ferrero A., Sifonios L., Podesta M.F., and Wikinski S. Maintenance treatment with fluoxetine is necessary to sustain normal levels of synaptic markers in an experimental model of depression: correlation with behavioral response. Neuropsychopharmacology 33 (2008) 1896-1908
63. Reyna-Neyra A., Camacho-Arroyo I., Ferrera P., and Arias C. Estradiol and progesterone modify microtubule associated protein 2 content in the rat hippocampus. Brain Res. Bull. 58 (2002) 607-612
64. Rios M., Fan G., Fekete C., Kelly J., Bates B., Kuehn R., Lechan R.M., and Jaenisch R. Conditional deletion of brain-derived neurotrophic factor in the postnatal brain leads to obesity and hyperactivity. Mol. Endocrinol. 15 (2001) 1748-1757
65. Rosoklija G., Toomayan G., Ellis S.P., Keilp J., Mann J.J., Latov N., Hays A.P., and Dwork A.J. Structural abnormalities of subicular dendrites in subjects with schizophrenia and mood disorders: preliminary findings. Arch. Gen. Psychiatry 57 (2000) 349-356
66. Rygula R., Abumaria N., Domenici E., Hiemke C., and Fuchs E. Effects of fluoxetine on behavioral deficits evoked by chronic social stress in rats. Behav. Brain Res. 174 (2006) 188-192
67. Saarelainen T., Pussinen R., Koponen E., Alhonen L., Wong G., Sirvio J., and Castren E. Transgenic mice overexpressing truncated trkB neurotrophin receptors in neurons have impaired long-term spatial memory but normal hippocampal LTP. Synapse 38 (2000) 102-104
68. Sairanen M., O'Leary O.F., Knuuttila J.E., and Castren E. Chronic antidepressant treatment selectively increases expression of plasticity-related proteins in the hippocampus and medial prefrontal cortex of the rat. Neuroscience 144 (2007) 368-374
69. Santarelli L., Saxe M., Gross C., Surget A., Battaglia F., Dulawa S., Weisstaub N., Lee J., Duman R., Arancio O., Belzung C., and Hen R. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science (New York, NY) 301 (2003) 805-809
70. Sato K., Morimoto K., Suemaru S., Sato T., and Yamada N. Increased synapsin I immunoreactivity during long-term potentiation in rat hippocampus. Brain Res. 872 (2000) 219-222
71. Schnell E., Sizemore M., Karimzadegan S., Chen L., Bredt D.S., and Nicoll R.A. Direct interactions between PSD-95 and stargazin control synaptic AMPA receptor number. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 13902-13907
72. Shepherd J.D., and Huganir R.L. The cell biology of synaptic plasticity: AMPA receptor trafficking. Annu. Rev. Cell Dev. Biol. 23 (2007) 613-643
73. Spencer J.L., Waters E.M., Milner T.A., and McEwen B.S. Estrous cycle regulates activation of hippocampal Akt, LIM kinase, and neurotrophin receptors in C57BL/6 mice. Neuroscience 155 (2008) 1106-1119
74. Spencer J.L., Waters E.M., Romeo R.D., Wood G.E., Milner T.A., and McEwen B.S. Uncovering the mechanisms of estrogen effects on hippocampal function. Front. Neuroendocrinol. 29 (2008) 219-237
75. Svenningsson P., Bateup H., Qi H., Takamiya K., Huganir R.L., Spedding M., Roth B.L., McEwen B.S., and Greengard P. Involvement of AMPA receptor phosphorylation in antidepressant actions with special reference to tianeptine. Eur. J. Neurosci. 26 (2007) 3509-3517
76. Tomita S., Shenoy A., Fukata Y., Nicoll R.A., and Bredt D.S. Stargazin interacts functionally with the AMPA receptor glutamate-binding module. Neuropharmacology 52 (2007) 87-91
77. Wallace M., Luine V., Arellanos A., and Frankfurt M. Ovariectomized rats show decreased recognition memory and spine density in the hippocampus and prefrontal cortex. Brain Res. 1126 (2006) 176-182
78. Xu X., and Zhang Z. Effects of estradiol benzoate on learning-memory behavior and synaptic structure in ovariectomized mice. Life Sci. 79 (2006) 1553-1560
79. Yao W.D., Gainetdinov R.R., Arbuckle M.I., Sotnikova T.D., Cyr M., Beaulieu J.M., Torres G.E., Grant S.G., and Caron M.G. Identification of PSD-95 as a regulator of dopamine-mediated synaptic and behavioral plasticity. Neuron 41 (2004) 625-638
80. Yen T.T., Wong D.T., and Bemis K.G. Reduction of food consumption and body weight of normal and obese mice by chronic treatment with fluoxetine: a serotonin reuptake inhibitor. Drug Dev. Res. 10 (1987) 37-45
81. Yoshii A., and Constantine-Paton M. BDNF induces transport of PSD-95 to dendrites through PI3K-AKT signaling after NMDA receptor activation. Nat. Neurosci. 10 (2007) 702-711
82. Zamanillo D., Sprengel R., Hvalby O., Jensen V., Burnashev N., Rozov A., Kaiser K.M., Koster H.J., Borchardt T., Worley P., Lubke J., Frotscher M., Kelly P.H., Sommer B., Andersen P., Seeburg P.H., and Sakmann B. Importance of AMPA receptors for hippocampal synaptic plasticity but not for spatial learning. Science (New York, NY) 284 (1999) 1805-1811
83. Zarate Jr. C.A., Singh J., and Manji H.K. Cellular plasticity cascades: targets for the development of novel therapeutics for bipolar disorder. Biol. Psychiatry 59 (2006) 1006-1020