The tricyclic antidepressant desipramine inhibited the neurotoxic, kainate-induced [Ca2+]i increases in CA1 pyramidal cells in acute hippocampal slices

Brain Research Bulletin

Volumn 104, Issue , 2014, Pages 42-51

  Koncz, István ^a   Szász, Bernadett K ^b   Szabó, Szilárd I ^b   Kiss, János P ^c   Mike, Árpád ^b   Lendvai, Balázs ^d   Sylvester Vizi, E ^b   Zelles, Tibor ^b,e  

^a UNIVERSITY OF SZEGED   (Hungary)

^b INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^c Servier   (Hungary)

^d GEDEON RICHTER LTD   (Hungary)

^e SEMMELWEIS UNIVERSITY   (Hungary)

Author keywords

AMPA receptors; CA1 pyramidal cells; Desipramine; Kainic acid; Rat hippocampal slices

Indexed keywords

1 (4 AMINOPHENYL) 3,4 DIHYDRO 4 METHYL 3 METHYLCARBAMOYL 7,8 METHYLENEDIOXY 5H 2,3 BENZODIAZEPINE; 2 AMINO 5 PHOSPHONOVALERIC ACID; 6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; AMPA RECEPTOR; DESIPRAMINE; KAINIC ACID; NICKEL CHLORIDE; NIFEDIPINE; OMEGA CONOTOXIN MVIIC; TETRODOTOXIN; VOLTAGE GATED CALCIUM CHANNEL; VOLTAGE GATED SODIUM CHANNEL; AMINO ACID RECEPTOR STIMULATING AGENT; CALCIUM; TRICYCLIC ANTIDEPRESSANT AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CONTROLLED STUDY; DRUG INHIBITION; EVOKED RESPONSE; FETUS; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL NEURONAL CULTURE; NERVE CELL MEMBRANE STEADY POTENTIAL; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; ANIMAL; DRUG EFFECTS; METABOLISM; TOXICITY; WISTAR RAT;

ANIMALS; ANTIDEPRESSIVE AGENTS, TRICYCLIC; CA1 REGION, HIPPOCAMPAL; CALCIUM; DESIPRAMINE; EXCITATORY AMINO ACID AGONISTS; KAINIC ACID; PYRAMIDAL CELLS; RATS; RATS, WISTAR;

EID: 84899843792     PISSN: 03619230     EISSN: 18732747     Source Type: Journal    
DOI: 10.1016/j.brainresbull.2014.04.003     Document Type: Article

References (83)

1. Abushik P.A., Sibarov D.A., Eaton M.J., Skatchkov S.N., Antonov S.M. Kainate-induced calcium overload of cortical neurons in vitro: dependence on expression of AMPAR GluA2-subunit and down-regulation by subnanomolar ouabain. Cell Calcium 2013, 54:95-104.
2. Andó R.D., Sperlágh B. The role of glutamate release mediated by extrasynaptic P2X7 receptors in animal models of neuropathic pain. Brain Res. Bull. 2013, 93:80-85.
3. Argenti D., D'Mello A.P. The pharmacodynamics of desipramine and desmethyldesipramine in rats. J. Pharmacol. Exp. Ther. 1994, 270:512-519.
4. Barbon A., Popoli M., La Via L., Moraschi S., Vallini I., Tardito D., Tiraboschi E., Musazzi L., Giambelli R., Gennarelli M., Racagni G., Barlati S. Regulation of editing and expression of glutamate alpha-amino-propionic-acid (AMPA)/kainate receptors by antidepressant drugs. Biol. Psychiatry 2006, 59:713-720.
5. Beauchamp G., Lavoie P.A., Elie R. Differential effect of desipramine and 2-hydroxydesipramine on depolarization-induced calcium uptake in synaptosomes from rat limbic sites. Can. J. Physiol. Pharmacol. 1995, 73:619-623.
6. Ben-Ari Y. Limbic seizure and brain damage produced by kainic acid: mechanisms and relevance to human temporal lobe epilepsy. Neuroscience 1985, 14:375-403.
7. Besret L., Debruyne D., Rioux P., Bonvalot T., Moulin M., Zarifian E., Baron J.C. A comprehensive investigation of plasma and brain regional pharmacokinetics of imipramine and its metabolites during and after chronic administration in the rat. J. Pharm. Sci. 1996, 85:291-295.
8. Bouron A., Chatton J.Y. Acute application of the tricyclic antidepressant desipramine presynaptically stimulates the exocytosis of glutamate in the hippocampus. Neuroscience 1999, 90:729-736.
9. Bredt D.S., Nicoll R.A. AMPA receptor trafficking at excitatory synapses. Neuron 2003, 40:361-379.
10. Burnashev N., Zhou Z., Neher E., Sakmann B. Fractional calcium currents through recombinant GluR channels of the NMDA, AMPA and kainate receptor subtypes. J. Physiol. 1995, 485(Pt 2):403-418.
11. 2+ levels in neuronal culture. Eur. J. Pharmacol. 1992, 219:53-57.
12. Chang P.K.-Y., Verbich D., McKinney R.A. AMPA receptors as drug targets in neurological disease - advantages, caveats, and future outlook. Eur. J. Neurosci. 2012, 35:1908-1916.
13. Cheng Y., Sun A.Y. Oxidative mechanisms involved in kainate-induced cytotoxicity in cortical neurons. Neurochem. Res. 1994, 19:1557-1564.
14. Choi J.J., Huang G.J., Shafik E., Wu W.H., McArdle J.J. Imipramine's selective suppression of an L-type calcium channel in neurons of murine dorsal root ganglia involves G proteins. J. Pharmacol. Exp. Ther. 1992, 263:49-53.
15. Coyle J.T., Ferkany J.W., Zaczek R. Kainic acid: insights from a neurotoxin into the pathophysiology of Huntington's disease. Neurobehav. Toxicol. Teratol. 1983, 5:617-624.
16. Coyle J.T., Schwarcz R. Lesion of striatal neurones with kainic acid provides a model for Huntington's chorea. Nature 1976, 263:244-246.
17. 2+-permeable AMPA receptors: synaptic plasticity and beyond. Curr. Opin. Neurobiol. 2006, 16:288-297.
18. Danysz W., Parsons C.G. Neuroprotective potential of ionotropic glutamate receptor antagonists. Neurotox. Res. 2002, 4:119-126.
19. Degracia D.J. Towards a dynamical network view of brain ischemia and reperfusion. Part III: Therapeutic implications. J. Exp. Stroke Transl. Med. 2010, 3:90-103.
20. Fekete A., Franklin L., Ikemoto T., Rózsa B., Lendvai B., Sylvester Vizi E., Zelles T. Mechanism of the persistent sodium current activator veratridine-evoked Ca elevation: implication for epilepsy. J. Neurochem. 2009, 111:745-756.
21. Fekete A., Vizi E.S., Kovács K.J., Lendvai B., Zelles T. Layer-specific differences in reactive oxygen species levels after oxygen-glucose deprivation in acute hippocampal slices. Free Radic. Biol. Med. 2008, 44:1010-1022.
22. Fisher R.S., Alger B.E. Electrophysiological mechanisms of kainic acid-induced epileptiform activity in the rat hippocampal slice. J. Neurosci. 1984, 4:1312-1323.
23. 2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 1985, 260:3440-3450.
24. 2+ accumulation in cortical cell culture correlates with subsequent neuronal degeneration. J. Neurosci. 1993, 13:1993-2000.
25. Hartwick A.T.E., Hamilton C.M., Baldridge W.H. Glutamatergic calcium dynamics and deregulation of rat retinal ganglion cells. J. Physiol. 2008, 586:3425-3446.
26. Heilbrunn S.M., Shah P., Bristow M.R., Valantine H.A., Ginsburg R., Fowler M.B. Increased beta-receptor density and improved hemodynamic response to catecholamine stimulation during long-term metoprolol therapy in heart failure from dilated cardiomyopathy. Circulation 1989, 79:483-490.
27. Hennings E.C., Kiss J.P., De Oliveira K., Toth P.T., Vizi E.S. Nicotinic acetylcholine receptor antagonistic activity of monoamine uptake blockers in rat hippocampal slices. J. Neurochem. 1999, 73:1043-1050.
28. Hinkle P.M., Shanshala E.D., Nelson E.J. Measurement of intracellular cadmium with fluorescent dyes. Further evidence for the role of calcium channels in cadmium uptake. J. Biol. Chem. 1992, 267:25553-25559.
29. Hoehn K., Watson T.W., MacVicar B.A. Multiple types of calcium channels in acutely isolated rat neostriatal neurons. J. Neurosci. 1993, 13:1244-1257.
30. Ishibashi H., Eto K., Kajiwara M., Noda M. Facilitation of spontaneous glutamate release by antidepressant drugs in rat locus coeruleus. Neurosci. Lett. 2005, 374:152-156.
31. Iwata S., Wakita M., Shin M.-C., Fukuda A., Akaike N. Modulation of allopregnanolone on excitatory transmitters release from single glutamatergic terminal. Brain Res. Bull. 2013, 93:39-46.
32. Jane D.E., Lodge D., Collingridge G.L. Kainate receptors: pharmacology, function and therapeutic potential. Neuropharmacology 2009, 56:90-113.
33. Kiss J.P., Szasz B.K., Fodor L., Mike A., Lenkey N., Kurkó D., Nagy J., Vizi E.S. GluN2B-containing NMDA receptors as possible targets for the neuroprotective and antidepressant effects of fluoxetine. Neurochem. Int. 2012, 60:170-176.
34. Kobayashi M., Kojima M., Koyanagi Y., Adachi K., Imamura K., Koshikawa N. Presynaptic and postsynaptic modulation of glutamatergic synaptic transmission by activation of alpha(1)- and beta-adrenoceptors in layer V pyramidal neurons of rat cerebral cortex. Synapse 2009, 63:269-281.
35. Kwak S., Weiss J.H. Calcium-permeable AMPA channels in neurodegenerative disease and ischemia. Curr. Opin. Neurobiol. 2006, 16:281-287.
36. 2+-model in guinea pig hippocampal slices. Eur. Neuropsychopharmacol. 1998, 8:209-212.
37. Lauterbach E.C. Neuroprotective effects of psychotropic drugs in Huntington's disease. Int. J. Mol. Sci. 2013, 14:22558-22603.
38. 2+ exchange in rat brain cortex synaptosomes. Can. J. Physiol. Pharmacol. 1990, 68:1414-1418.
39. Leng Y., Fessler E.B., Chuang D.-M. Neuroprotective effects of the mood stabilizer lamotrigine against glutamate excitotoxicity: roles of chromatin remodelling and Bcl-2 induction. Int. J. Neuropsychopharmacol. 2013, 16:607-620.
40. Lenkey N., Karoly R., Kiss J.P., Szasz B.K., Vizi E.S., Mike A. The mechanism of activity-dependent sodium channel inhibition by the antidepressants fluoxetine and desipramine. Mol. Pharmacol. 2006, 70:2052-2063.
41. Lenkey N., Karoly R., Lukacs P., Vizi E.S., Sunesen M., Fodor L., Mike A. Classification of drugs based on properties of sodium channel inhibition: a comparative automated patch-clamp study. PLoS ONE 2010, 5:e15568.
42. Lerma J., Paternain A.V., Rodríguez-Moreno A., López-García J.C. Molecular physiology of kainate receptors. Physiol. Rev. 2001, 81:971-998.
43. Li H., Dong H., Li J., Liu H., Liu Z., Li Z. Neuroprotective effect of insulin-like growth factor-1: effects on tyrosine kinase receptor (Trk) expression in dorsal root ganglion neurons with glutamate-induced excitotoxicity in vitro. Brain Res. Bull. 2013, 97:86-95.
44. Lipton P. Ischemic cell death in brain neurons. Physiol. Rev. 1999, 79:1431-1568.
45. Liu D., Yang Q., Li S. Activation of extrasynaptic NMDA receptors induces LTD in rat hippocampal CA1 neurons. Brain Res. Bull. 2013, 93:10-16.
46. Liu S., Lau L., Wei J., Zhu D., Zou S., Sun H.-S., Fu Y., Liu F., Lu Y. Expression of Ca(2+)-permeable AMPA receptor channels primes cell death in transient forebrain ischemia. Neuron 2004, 43:43-55.
47. Liu S., Zhao M. Neuroprotective effect of estrogen: role of nonsynaptic NR2B-containing NMDA receptors. Brain Res. Bull. 2013, 93:27-31.
48. Magazanik L.G., Buldakova S.L., Samoilova M.V., Gmiro V.E., Mellor I.R., Usherwood P.N. Block of open channels of recombinant AMPA receptors and native AMPA/kainate receptors by adamantane derivatives. J. Physiol. 1997, 505(Pt 3):655-663.
49. 2+ channels in apical dendrites of rat CA1 pyramidal neurons. J. Physiol. 1995, 487(Pt 1):67-90.
50. Martinez-Turrillas R., Frechilla D., Del Río J. Chronic antidepressant treatment increases the membrane expression of AMPA receptors in rat hippocampus. Neuropharmacology 2002, 43:1230-1237.
51. Mayer A., Szasz B.K., Kiss J.P. Inhibitory effect of antidepressants on the NMDA-evoked [(3)H]noradrenaline release from rat hippocampal slices. Neurochem. Int. 2009, 55:383-388.
52. McDonald J.W., Althomsons S.P., Hyrc K.L., Choi D.W., Goldberg M.P. Oligodendrocytes from forebrain are highly vulnerable to AMPA/kainate receptor-mediated excitotoxicity. Nat. Med. 1998, 4:291-297.
53. Milnerwood A.J., Gladding C.M., Pouladi M.A., Kaufman A.M., Hines R.M., Boyd J.D., Ko R.W.Y., Vasuta O.C., Graham R.K., Hayden M.R., Murphy T.H., Raymond L.A. Early increase in extrasynaptic NMDA receptor signaling and expression contributes to phenotype onset in Huntington's disease mice. Neuron 2010, 65:178-190.
54. Musazzi L., Treccani G., Mallei A., Popoli M. The action of antidepressants on the glutamate system: regulation of glutamate release and glutamate receptors. Biol. Psychiatry 2013, 73:1180-1188.
55. Nadler J.V. Minireview. Kainic acid as a tool for the study of temporal lobe epilepsy. Life Sci. 1981, 29:2031-2042.
56. Noh K.-M., Yokota H., Mashiko T., Castillo P.E., Zukin R.S., Bennett M.V.L. Blockade of calcium-permeable AMPA receptors protects hippocampal neurons against global ischemia-induced death. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:12230-12235.
57. Novelli A., Lysko P.G., Henneberry R.C. Uptake of imipramine in neurons cultured from rat cerebellum. Brain Res. 1987, 411:291-297.
58. Nozaki H., Tanaka K., Gomi S., Mihara B., Nogawa S., Nagata E., Kondo T., Fukuuchi Y. Role of the ryanodine receptor in ischemic brain damage - localized reduction of ryanodine receptor binding during ischemia in hippocampus CA1. Cell. Mol. Neurobiol. 1999, 19:119-131.
59. O'Brien F.E., Clarke G., Fitzgerald P., Dinan T.G., Griffin B.T., Cryan J.F. Inhibition of P-glycoprotein enhances transport of imipramine across the blood-brain barrier: microdialysis studies in conscious freely moving rats. Br. J. Pharmacol. 2012, 166:1333-1343.
60. Ogata N., Yoshii M., Narahashi T. Psychotropic drugs block voltage-gated ion channels in neuroblastoma cells. Brain Res. 1989, 476:140-144.
61. 2+-permeable AMPA/kainate channel expression in hippocampal pyramidal neurons: fluorescence imaging and immunocytochemical assessment. J. Neurosci. 2003, 23:10521-10530.
62. Rego A.C., Ward M.W., Nicholls D.G. Mitochondria control ampa/kainate receptor-induced cytoplasmic calcium deregulation in rat cerebellar granule cells. J. Neurosci. 2001, 21:1893-1901.
63. Rodriguez M., Sabate M., Rodriguez-Sabate C., Morales I. The role of non-synaptic extracellular glutamate. Brain Res. Bull. 2013, 93:17-26.
64. Sánchez-Gómez M.V., Matute C. AMPA and kainate receptors each mediate excitotoxicity in oligodendroglial cultures. Neurobiol. Dis. 1999, 6:475-485.
65. Sattler R., Tymianski M. Molecular mechanisms of glutamate receptor-mediated excitotoxic neuronal cell death. Mol. Neurobiol. 2001, 24:107-129.
66. Sernagor E., Kuhn D., Vyklicky L., Mayer M.L. Open channel block of NMDA receptor responses evoked by tricyclic antidepressants. Neuron 1989, 2:1221-1227.
67. Stoll L., Gentile L. Linking tricyclic antidepressants to ionotropic glutamate receptors. Biochem. Biophys. Res. Commun. 2005, 333:622-627.
68. Stoll L., Seguin S., Gentile L. Tricyclic antidepressants, but not the selective serotonin reuptake inhibitor fluoxetine, bind to the S1S2 domain of AMPA receptors. Arch. Biochem. Biophys. 2007, 458:213-219.
69. Sun H.Y., Bartley A.F., Dobrunz L.E. Calcium-permeable presynaptic kainate receptors involved in excitatory short-term facilitation onto somatostatin interneurons during natural stimulus patterns. J. Neurophysiol. 2009, 101:1043-1055.
70. Szasz B.K., Mike A., Karoly R., Gerevich Z., Illes P., Vizi E.S., Kiss J.P. Direct inhibitory effect of fluoxetine on N-methyl-d-aspartate receptors in the central nervous system. Biol. Psychiatry 2007, 62:1303-1309.
71. Takebayashi M., Kagaya A., Inagaki M., Kozuru T., Jitsuiki H., Kurata K., Okamoto Y., Yamawaki S. Effects of antidepressants on gamma-aminobutyric acid- and N-methyl-d-aspartate-induced intracellular Ca(2+) concentration increases in primary cultured rat cortical neurons. Neuropsychobiology 2000, 42:120-126.
72. 2+ signaling and apoptosis of medium spiny neurons in Huntington's disease. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:2602-2607.
73. Vécsei L., Beal M.F. Comparative behavioral and neurochemical studies with striatal kainic acid- or quinolinic acid-lesioned rats. Pharmacol. Biochem. Behav. 1991, 39:473-478.
74. Vizi E.S., Kisfali M., Lorincz T. Role of nonsynaptic GluN2B-containing NMDA receptors in excitotoxicity: evidence that fluoxetine selectively inhibits these receptors and may have neuroprotective effects. Brain Res. Bull. 2013, 93:32-38.
75. Wang Q., Yu S., Simonyi A., Sun G.Y., Sun A.Y. Kainic acid-mediated excitotoxicity as a model for neurodegeneration. Mol. Neurobiol. 2005, 31:3-16.
76. Wang S., Jia Z., Roder J., Murphy T.H. AMPA receptor-mediated miniature synaptic calcium transients in GluR2 null mice. J. Neurophysiol. 2002, 88:29-40.
77. Wei X.-W., Yan H., Xu B., Wu Y.-P., Li C., Zhang G.-Y. Neuroprotection of co-activation of GABA receptors by preventing caspase-3 denitrosylation in KA-induced seizures. Brain Res. Bull. 2012, 88:617-623.
78. Yin H.Z., Sensi S.L., Carriedo S.G., Weiss J.H. Dendritic localization of Ca(2+)-permeable AMPA/kainate channels in hippocampal pyramidal neurons. J. Comp. Neurol. 1999, 409:250-260.
79. 2+ accumulation and neuronal loss in hippocampal pyramidal neurons. J. Neurosci. 2002, 22:1273-1279.
80. Zádori D., Geisz A., Vámos E., Vécsei L., Klivényi P. Valproate ameliorates the survival and the motor performance in a transgenic mouse model of Huntington's disease. Pharmacol. Biochem. Behav. 2009, 94:148-153.
81. i increase in rat hippocampal CA1 pyramidal cells. Neurochem. Res. 2001, 26:1095-1100.
82. 2+ release from mitochondria. J. Neurosci. 1999, 19:3307-3315.
83. Zheng X.-Y., Zhang H.-L., Luo Q., Zhu J. Kainic acid-induced neurodegenerative model: potentials and limitations. J. Biomed. Biotechnol. 2011, 2011:457079.