Fluoxetine suppresses synaptically induced [Ca2+]i spikes and excitotoxicity in cultured rat hippocampal neurons

Brain Research

Volumn 1490, Issue , 2013, Pages 23-34

  Kim, Hee Jung ^a   Kim, Tae Hyeong ^b   Choi, Se Joon ^b   Hong, Yi Jae ^b   Yang, Ji Seon ^b   Sung, Ki Wug ^b   Rhie, Duck Joo ^b   Hahn, Sang June ^b   Yoon, Shin Hee ^b  

^a Dankook University   (South Korea)

^b The Catholic University of Korea   (South Korea)

Author keywords

Epilepsy; Exocytosis; Glutamate receptor; Serotonin reuptake inhibitor

Indexed keywords

3,5 DIHYDROXYPHENYLGLYCINE; ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; CAFFEINE; CALCIUM CHANNEL; CHLORAMPHETAMINE; CITALOPRAM; FLUOXETINE; GLUTAMIC ACID; MAGNESIUM; N METHYLASPARTIC ACID; PAROXETINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTROSTIMULATION; EXCITOTOXICITY; EXTRACELLULAR SPACE; FETUS; HIPPOCAMPUS; NERVE CELL CULTURE; NERVE CELL NECROSIS; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRESYNAPTIC NERVE; PRIORITY JOURNAL; RAT; SPIKE; SYNAPSE;

ANIMALS; CALCIUM CHANNEL BLOCKERS; CALCIUM SIGNALING; CELL DEATH; CELLS, CULTURED; CITALOPRAM; EXCITATORY AMINO ACID AGONISTS; EXOCYTOSIS; FEMALE; FLUOXETINE; HIPPOCAMPUS; MAGNESIUM DEFICIENCY; NEURONS; NEUROPROTECTIVE AGENTS; NEUROTRANSMITTER AGENTS; P-CHLOROAMPHETAMINE; PAROXETINE; PATCH-CLAMP TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, METABOTROPIC GLUTAMATE; SEROTONIN AGENTS; SEROTONIN UPTAKE INHIBITORS; SYNAPSES;

RATTUS;

EID: 84871334105     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2012.10.062     Document Type: Article

References (70)

1. A.E. Abele, K.P. Scholz, W.K. Scholz, and R.J. Miller Excitotoxicity induced by enhanced excitatory neurotransmission in cultured hippocampal pyramidal neurons Neuron 4 1990 413 419
2. S.H. Ahn, H.J. Kim, I. Jeong, Y.J. Hong, M.J. Kim, D.J. Rhie, Y.H. Jo, S.J. Hahn, and S.H. Yoon Grape seed proanthocyanidin extract inhibits glutamate-induced cell death through inhibition of calcium signals and nitric oxide formation in cultured rat hippocampal neurons BMC Neurosci. 12 2011 1 12
3. G. Bagdy, V. Kecskemeti, P. Riba, and R. Jakus Serotonin and epilepsy J. Neurochem. 100 2007 857 873
4. H. Benveniste, J. Drejer, A. Schousboe, and N.H. Diemer Elevation of the extracellular concentrations of glutamate and aspartate in rat hippocampus during transient cerebral ischemia monitored by intracerebral microdialysis J. Neurochem. 43 1984 1369 1374
5. W.J. Betz, F. Mao, and G.S. Bewick Activity-dependent fluorescent staining and destaining of living vertebrate motor nerve terminals J. Neurosci. 12 1992 363 375
6. G. Bonanno, R. Giambelli, L. Raiteri, E. Tiraboschi, S. Zappettini, L. Musazzi, M. Raiteri, G. Racagni, and M. Popoli Chronic antidepressants reduce depolarization-evoked glutamate release and protein interactions favoring formation of SNARE complex in hippocampus J. Neurosci. 25 2005 3270 3279
7. D.J. Borys, S.C. Setzer, L.J. Ling, J.J. Reisdorf, L.C. Day, and E.P. Krenzelok Acute fluoxetine overdose: a report of 234 cases Am. J. Emerg. Med. 10 1992 115 120
8. D.W. Choi, M. Maulucci-Gedde, and A.R. Kriegstein Glutamate neurotoxicity in cortical cell culture J. Neurosci. 7 1987 357 368
9. J.S. Choi, B.H. Choi, H.S. Ahn, M.J. Kim, D.J. Rhie, S.H. Yoon, Min do, S. Jo, Y.H. Kim, M.S. Sung, and K.W. Hahn, S.J. Mechanism of block by fluoxetine of 5-hydroxytryptamine3 (5-HT3)-mediated currents in NCB-20 neuroblastoma cells Biochem. Pharmacol. 66 2003 2125 2132
10. F. Deak, B. Lasztoczi, P. Pacher, G.L. Petheo, V. Kecskemeti, and A. Spat Inhibition of voltage-gated calcium channels by fluoxetine in rat hippocampal pyramidal cells Neuropharmacology 39 2000 1029 1036
11. L.S. Deshpande, J.K. Lou, A. Mian, R.E. Blair, S. Sombati, E. Attkisson, and R.J. DeLorenzo Time course and mechanism of hippocampal neuronal death in an in vitro model of status epilepticus: role of NMDA receptor activation and NMDA dependent calcium entry Eur. J. Pharmacol. 583 2008 73 83
12. B. Eisensamer, G. Rammes, G. Gimpl, M. Shapa, U. Ferrari, G. Hapfelmeier, B. Bondy, C. Parsons, K. Gilling, W. Zieglgansberger, F. Holsboer, and R. Rupprecht Antidepressants are functional antagonists at the serotonin type 3 (5-HT3) receptor Mol. Psychiatry 8 2003 994 1007
13. P. Fan Effects of antidepressants on the inward current mediated by 5-HT3 receptors in rat nodose ganglion neurones Br. J. Pharmacol. 112 1994 741 744
14. G. Farrugia Modulation of ionic currents in isolated canine and human jejunal circular smooth muscle cells by fluoxetine Gastroenterology 110 1996 1438 1445
15. E. Favale, V. Rubino, P. Mainardi, G. Lunardi, and C. Albano Anticonvulsant effect of fluoxetine in humans Neurology 45 1995 1926 1927
16. J. Garcia-Colunga, J.N. Awad, and R. Miledi Blockage of muscle and neuronal nicotinic acetylcholine receptors by fluoxetine (Prozac) Proc. Nat. Acad. Sci. U.S.A. 94 1997 2041 2044
17. J.W. Gibbs 3rd, S. Sombati, R.J. DeLorenzo, and D.A. Coulter Physiological and pharmacological alterations in postsynaptic GABAA receptor function in a hippocampal culture model of chronic spontaneous seizures J. Neurophysiol. 77 1997 2139 2152
18. G.L. Gilbert, H.J. Kim, J.J. Waataja, and S.A. Thayer Delta9-tetrahydrocannabinol protects hippocampal neurons from excitotoxicity Brain Res. 1128 2007 61 69
19. 2+ indicators with greatly improved fluorescence properties J. Biol. Chem. 260 1985 3440 3450
20. S.J. Hahn, J.S. Choi, D.J. Rhie, C.S. Oh, Y.H. Jo, and M.S. Kim Inhibition by fluoxetine of voltage-activated ion channels in rat PC12 cells Eur. J. Pharmacol. 367 1999 113 118
21. E.J. Hernandez, P.A. Williams, and F.E. Dudek Effects of fluoxetine and TFMPP on spontaneous seizures in rats with pilocarpine-induced epilepsy Epilepsia 43 2002 1337 1345
22. Y. Jin, C.M. Lim, S.W. Kim, J.Y. Park, J.S. Seo, P.L. Han, S.H. Yoon, and J.K. Lee Fluoxetine attenuates kainic acid-induced neuronal cell death in the mouse hippocampus Brain Res. 1281 2009 108 116
23. P.C. Jobe, and R.A. Browning The serotonergic and noradrenergic effects of antidepressant drugs are anticonvulsant, not proconvulsant Epilepsy Behav. 7 2005 602 619
24. C.N. Karson, J.E. Newton, R. Livingston, J.B. Jolly, T.B. Cooper, J. Sprigg, and R.A. Komoroski Human brain fluoxetine concentrations J. Neuropsychiatry Clin. Neurosci. 5 1993 322 329
25. 2+ channel blocking potencies Brain Res. Bull. 67 2005 126 132
26. D.J. Kim, and S.A. Thayer Activation of CB1 cannabinoid receptors inhibits neurotransmitter release from identified synaptic sites in rat hippocampal cultures Brain Res. 852 2000 398 405
27. 2+ release from intracellular stores Neuropharmacology 49 2005 265 274
28. J.P. Kiss, B.K. Szasz, L. Fodor, A. Mike, N. Lenkey, D. Kurko, J. Nagy, and E.S. Vizi GluN2B-containing NMDA receptors as possible targets for the neuroprotective and antidepressant effects of fluoxetine Neurochem. Int. 60 2012 170 176
29. N. Lenkey, R. Karoly, J.P. Kiss, B.K. Szasz, E.S. Vizi, and A. Mike The mechanism of activity-dependent sodium channel inhibition by the antidepressants fluoxetine and desipramine Mol. Pharmacol. 70 2006 2052 2063
30. Y.F. Li, Y.Z. Zhang, Y.Q. Liu, H.L. Wang, J.B. Cao, T.T. Guan, and Z.P. Luo Inhibition of N-methyl-d-aspartate receptor function appears to be one of the common actions for antidepressants J. Psychopharmacol. 20 2006 629 635
31. C.M. Lim, S.W. Kim, J.Y. Park, C. Kim, S.H. Yoon, and J.K. Lee Fluoxetine affords robust neuroprotection in the postischemic brain via its anti-inflammatory effect J. Neurosci. Res. 87 2009 1037 1045
32. Y. Liu, T.P. Wong, M. Aarts, A. Rooyakkers, L. Liu, T.W. Lai, D.C. Wu, J. Lu, M. Tymianski, A.M. Craig, and Y.T. Wang NMDA receptor subunits have differential roles in mediating excitotoxic neuronal death both in vitro and in vivo J. Neurosci. 27 2007 2846 2857
33. I. Llano, R. DiPolo, and A. Marty Calcium-induced calcium release in cerebellar Purkinje cells Neuron 12 1994 663 673
34. K.T. Lu, and P.W. Gean Endogenous serotonin inhibits epileptiform activity in rat hippocampal CA1 neurons via 5-hydroxytryptamine1A receptor activation Neuroscience 86 1998 729 737
35. J.I. Luebke, K. Dunlap, and T.J. Turner Multiple calcium channel types control glutamatergic synaptic transmission in the hippocampus Neuron 11 1993 895 902
36. R. Lujan, Z. Nusser, J.D. Roberts, R. Shigemoto, and P. Somogyi Perisynaptic location of metabotropic glutamate receptors mGluR1 and mGluR5 on dendrites and dendritic spines in the rat hippocampus Eur. J. Neurosci. 8 1996 1488 1500
37. L.J. Martin, C.D. Blackstone, R.L. Huganir, and D.L. Price Cellular localization of a metabotropic glutamate receptor in rat brain Neuron 9 1992 259 270
38. J.R. McLeod Jr.; M. Shen, D.J. Kim, and S.A. Thayer Neurotoxicity mediated by aberrant patterns of synaptic activity between rat hippocampal neurons in culture J. Neurophysiol. 80 1998 2688 2698
39. I. Mody, J.D. Lambert, and U. Heinemann Low extracellular magnesium induces epileptiform activity and spreading depression in rat hippocampal slices J. Neurophysiol. 57 1987 869 888
40. J.W. Olney, R.C. Collins, and R.S. Sloviter Excitotoxic mechanisms of epileptic brain damage Adv. Neurol. 44 1986 857 877
41. P.J. Orsulak, J.T. Kenney, J.R. Debus, G. Crowley, and P.D. Wittman Determination of the antidepressant fluoxetine and its metabolite norfluoxetine in serum by reversed-phase HPLC with ultraviolet detection Clin. Chem. 34 1988 1875 1878
42. P. Pacher, J. Magyar, P. Szigligeti, T. Banyasz, C. Pankucsi, Z. Korom, Z. Ungvari, V. Kecskemeti, and P.P. Nanasi Electrophysiological effects of fluoxetine in mammalian cardiac tissues Naunyn Schmiedebergs Arch. Pharmacol. 361 2000 67 73
43. J.J. Pancrazio, G.L. Kamatchi, A.K. Roscoe, and C. Lynch 3rd Inhibition of neuronal Na+ channels by antidepressant drugs J. Pharmacol. Exp. Ther. 284 1998 208 214
44. D. Pericic, J. Lazic, and D. Svob Strac Anticonvulsant effects of acute and repeated fluoxetine treatment in unstressed and stressed mice Brain Res. 1033 2005 90 95
45. S.B. Pinnock, A.M. Blake, N.J. Platt, and J. Herbert The roles of BDNF, pCREB and Wnt3a in the latent period preceding activation of progenitor cell mitosis in the adult dentate gyrus by fluoxetine PLoS One 5 2010 e13652
46. T.M. Piser, R.A. Lampe, R.A. Keith, and S.A. Thayer Complete and reversible block by omega-grammotoxin SIA of glutamatergic synaptic transmission between cultured rat hippocampal neurons Neurosci. Lett. 201 1995 135 138
47. S. Prendiville, and K. Gale Anticonvulsant effect of fluoxetine on focally evoked limbic motor seizures in rats Epilepsia 34 1993 381 384
48. J.L. Rae, A. Rich, A.C. Zamudio, and O.A. Candia Effect of Prozac on whole cell ionic currents in lens and corneal epithelia Am. J. Physiol. 269 1995 C250 C256
49. S.S. Raju, A.R. Noor, S. Gurthu, C.R. Giriyappanavar, S.B. Acharya, H.C. Low, and S.H. Quah Effect of fluoxetine on maximal electroshock seizures in mice: acute vs chronic administration Pharmacol. Res. 39 1999 451 454
50. K. Rose, C.W. Christine, and D.W. Choi Magnesium removal induces paroxysmal neuronal firing and NMDA receptor-mediated neuronal degeneration in cortical cultures Neurosci. Lett. 115 1990 313 317
51. V.M. Sandler, and J.G. Barbara Calcium-induced calcium release contributes to action potential-evoked calcium transients in hippocampal CA1 pyramidal neurons J. Neurosci. 19 1999 4325 4336
52. M. Shen, T.M. Piser, V.S. Seybold, and S.A. Thayer Cannabinoid receptor agonists inhibit glutamatergic synaptic transmission in rat hippocampal cultures J. Neurosci. 16 1996 4322 4334
53. M.X. Shen, and S.A. Thayer Cannabinoid receptor agonists protect cultured rat hippocampal neurons fom excitotoxicity Mol. Pharmacol. 54 1998 459 462
54. R. Shigemoto, S. Nomura, H. Ohishi, H. Sugihara, S. Nakanishi, and N. Mizuno Immunohistochemical localization of a metabotropic glutamate receptor, mGluR5, in the rat brain Neurosci. Lett. 163 1993 53 57
55. E.Y. Shim, H.J. Kim, M.J. Kim, D.J. Rhie, Y.H. Jo, M.S. Kim, J.S. Hahn, M.Y. Lee, and S.H. Yoon Desensitization of somatostatin-induced inhibition of low extracellular magnesium concentration-induced calcium spikes in cultured rat hippocampal neurons Brain Res. 1111 2006 61 71
56. 2+ release by group I metabotropic glutamate receptors in acutely dissociated rat hippocampal neurons PLoS One 6 2011 e26625
57. S. Sombati, and R.J. Delorenzo Recurrent spontaneous seizure activity in hippocampal neuronal networks in culture J. Neurophysiol. 73 1995 1706 1711
58. 2+-channel inhibition Life Sci. 50 1992 2125 2138
59. B.K. Szasz, A. Mike, R. Karoly, Z. Gerevich, P. Illes, E.S. Vizi, and J.P. Kiss Direct inhibitory effect of fluoxetine on N-methyl-d-aspartate receptors in the central nervous system Biol. Psychiatry 62 2007 1303 1309
60. B.K. Szasz, E.S. Vizi, and J.P. Kiss Nicotinic acetylcholine receptor antagonistic property of the selective dopamine uptake inhibitor, GBR-12909 in rat hippocampal slices Neuroscience 145 2007 344 349
61. G.C. Terstappen, A. Pellacani, L. Aldegheri, F. Graziani, C. Carignani, G. Pula, and C. Virginio The antidepressant fluoxetine blocks the human small conductance calcium-activated potassium channels SK1, SK2 and SK3 Neurosci. Lett. 346 2003 85 88
62. C.G. Thomas, A.J. Miller, and G.L. Westbrook Synaptic and extrasynaptic NMDA receptor NR2 subunits in cultured hippocampal neurons J. Neurophysiol. 95 2006 1727 1734
63. J. Tytgat, C. Maertens, and P. Daenens Effect of fluoxetine on a neuronal, voltage-dependent potassium channel (Kv1.1) Br. J. Pharmacol. 122 1997 1417 1424
64. R.R. Ugale, N. Mittal, K. Hirani, and C.T. Chopde Essentiality of central GABAergic neuroactive steroid allopregnanolone for anticonvulsant action of fluoxetine against pentylenetetrazole-induced seizures in mice Brain Res. 1023 2004 102 111
65. Y. Wada, J. Shiraishi, M. Nakamura, and H. Hasegawa Prolonged but not acute fluoxetine administration produces its inhibitory effect on hippocampal seizures in rats Psychopharmacology 118 1995 305 309
66. 2+ channels Synapse 48 2003 170 177
67. J.F. Wernicke Safety and side effect profile of fluoxetine Expert Opin. Drug Saf. 3 2004 495 504
68. 2+ channels in supporting hippocampal synaptic transmission Science 264 1994 107 111
69. D.T. Wong, J.S. Horng, F.P. Bymaster, K.L. Hauser, and B.B. Molloy A selective inhibitor of serotonin uptake: lilly 110140, 3-(p- trifluoromethylphenoxy)-N-methyl-3-phenylpropylamine Life Sci. 15 1974 471 479
70. Q.S. Yan, P.C. Jobe, J.H. Cheong, K.H. Ko, and J.W. Dailey Role of serotonin in the anticonvulsant effect of fluoxetine in genetically epilepsy-prone rats Naunyn Schmiedebergs Arch. Pharmacol. 350 1994 149 152