Chronic benzodiazepine-induced reduction in GABAA receptor-mediated synaptic currents in hippocampal CA1 pyramidal neurons prevented by prior nimodipine injection

Neuroscience

Volumn 157, Issue 1, 2008, Pages 153-163

  Xiang, K ^a   Tietz, E I ^a  

^a MEDICAL COLLEGE OF OHIO   (United States)

Author keywords

BAPTA; flurazepam; L type voltage gated calcium channels; tolerance; unitary channel conductance; zolpidem

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; BENZODIAZEPINE; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; NIMODIPINE; VOLTAGE GATED CALCIUM CHANNEL; ZOLPIDEM;

ANIMAL EXPERIMENT; ARTICLE; BRAIN NERVE CELL; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CONTROLLED STUDY; HIPPOCAMPUS; IN VITRO STUDY; IN VIVO STUDY; MALE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SYNAPSE; SYNAPTIC TRANSMISSION;

ANIMALS; BENZODIAZEPINES; BRAIN; CALCIUM CHANNEL BLOCKERS; CALCIUM CHANNELS, L-TYPE; CALCIUM SIGNALING; CHELATING AGENTS; EGTAZIC ACID; EXCITATORY POSTSYNAPTIC POTENTIALS; FLURAZEPAM; GABA ANTAGONISTS; GABA MODULATORS; HIPPOCAMPUS; HYPNOTICS AND SEDATIVES; MALE; NIMODIPINE; PATCH-CLAMP TECHNIQUES; PRESYNAPTIC TERMINALS; PYRAMIDAL CELLS; PYRIDINES; RATS; RECEPTORS, GABA-A;

EID: 54949116487     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2008.08.049     Document Type: Article

References (46)

1. A receptors in mouse cortical neurons. Pflügers Arch 435 (1998) 382-387
2. Bateson A.N. Basic pharmacologic mechanisms involved in benzodiazepine tolerance and withdrawal. Curr Pharm Des 8 (2002) 5-21
3. Benke T.A., Lüthi A., Palmer M.J., Wikström M.A., Anderson W.W., Isaac J.T., and Collingridge G.L. Mathematical modeling of non-stationary fluctuation analysis for studying channel properties of synaptic AMPA receptors. J Physiol 537 (2001) 407-420
4. A receptor desensitization and deactivation. J Physiol 584 (2007) 769-787
5. Churn S.B., and DeLorenzo R.J. Modulation of GABAergic receptor function is regulated by phosphorylation in acutely dissociated guinea pig hippocampal neurons. J Physiol (Lond) 420 (1998) 207-221
6. Das P., Bell-Horner C.L., Huang R.Q., Raut A., Gonzales E.B., Chen Z.L., Covey D.F., and Dillon G.H. Inhibition of type A GABA receptors by L-type calcium channel blockers. Neuroscience 124 (2004) 195-206
7. A receptor channels. Abstract Viewer/Itinerary Planner. Washington, DC, Society for Neuroscience. Abstr 531.18 http://www.abstractsonline.com.
8. Das P., Lilly S.M., Zerda R., Gunning W.T., Alvarez F.J., and Tietz E.I. Increased AMPA receptor GluR1 subunit incorporation in rat hippocampal CA1 synapses during benzodiazepine withdrawal. J Comp Neurol (2008) doi: 10.1002/cne.21866
9. A receptor channels. Neuropharmacology 35 (1996) 1365-1374
10. Gallager D.W., Malcolm A.B., Anderson S.A., and Gonsalves S.F. Continuous release of diazepam: electrophysiological, biochemical and behavioral consequences. Brain Res 342 (1985) 26-36
11. Ghavanini A.A., Isbasescu I.M., Mathers D.A., and Puil E. Optimizing fluctuation analysis of GABAergic IPSCs for accurate unitary currents. J Neurosci Methods 158 (2006) 150-156
12. Gravielle M.C., Faris R., Russek S.J., and Farb D.H. GABA induces activity dependent delayed-onset uncoupling of GABA/Benzodiazepine site interactions in neocortical neurons. J Biol Chem 280 (2005) 20954-20960
13. Hell J.W., Westenbroek R.E., Warner C., Ahlijanian M.K., Prystay W., Gilbert M.M., Snutch T.P., and Catterall W.A. Identification and differential subcellular localization of the neuronal class C and class D L-type calcium channel alpha 1 subunits. J Cell Biol 123 (1993) 949-962
14. Houston C.M., Lee H.C., Hosie A.M., Moss S.J., and Smart T.G. Identification of the sites for CaMK-II-dependent phosphorylation of GABA(A) receptors. J Biol Chem 282 (2006) 17855-17866
15. Houston C.M., and Smart T.G. CaMK-II modulation of GABA(A) receptors expressed in HEK293, NG108-15 and rat cerebellar granule neurons. Eur J Neurosci 24 (1996) 2504-2514
16. Ishizawa Y., Furuya K., Yamagishi S., and Dohi S. Non-GABAergic effects of midazolam, diazepam and flumazenil on voltage-dependent ion currents in NG108-15 cells. Neuroreport 8 (1997) 2635-2638
17. Itier V., Granger P., Perrault C., Depoortere H., Scatton B., and Avenet P. Protracted treatment with diazepam reduces benzodiazepine receptor-mediated potentiation of γ-amino butyric acid-induced currents in dissociated rat hippocampal neurons. J Pharmacol Exp Ther 279 (1996) 1092-1099
18. Katsura M., Shibasaki M., Kurokawa K., Tsujimura A., and Ohkuma S. Up-regulation of L-type high voltage-gated calcium channel subunits by sustained exposure to 1,4- and 1,5-benzodiazepines in cerebrocortical neurons. J Neurochem 103 (2007) 2518-2528
19. Lavoie A.M., and Twyman R.E. Direct evidence for diazepam modulation of GABAA receptor microscopic affinity. Neuropharmacology 35 9-10 (1996) 1383-1392
20. Lyons H.R., Land M.B., Gibbs T.T., and Farb D.H. Distinct signal transduction pathways for GABA-induced GABA(A) receptor down-regulation and uncoupling in neuronal culture: a role for voltage-gated calcium channels. J Neurochem 78 (2001) 1114-1126
21. B recognition sites in rat brain. Mol Pharmacol 25 (1984) 352-359
22. Maruhn D., Siefert H.M., Weber H., Rämsch K., and Suwelack D. Pharmacokinetics of nimodipine. I. Communication: absorption, concentration in plasma and excretion after single administration of [14C]nimodipine in rat, dog and monkey. Arzneimittelforschung 35 (1985) 1781-1786
23. Megias M., Emri Z., Freund T.F., and Gulyás A.I. Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells. Neuroscience 102 (2001) 527-540
24. Perrais D., and Ropert N. Effect of zolpidem on miniature IPSCs and occupancy of postsynaptic GABAA receptors in central synapses. J Neurosci 19 (1999) 578-588
25. Poisbeau P., Williams S.R., and Mody I. Silent GABAA synapses during flurazepam withdrawal are region-specific in the hippocampal formation. J Neurosci 17 (1997) 3467-3475
26. A receptor function by PKA and PKC in adult hippocampal neurons. J Neurosci 19 (1999) 674-683
27. Regehr W.G., and Tank D.W. Calcium concentration dynamics produced by synaptic activation of CA1 hippocampal pyramidal cells. J Neurosci 12 (1992) 4202-4023
28. Reuveny E., Twombly D.A., and Narahashi T. Chlordiazepoxide block of two types of calcium channels in neuroblastoma cells. J Pharmacol Exp Ther 264 (1993) 22-28
29. 2+ channel than corresponding cerebral vessels. Clin Exp Hypertens 24 (2002) 715-726
30. Rosenberg H.C., Tietz E.I., and Chiu T.H. Tolerance to the anticonvulsant action of benzodiazepines. Relationship to decreased receptor density. Neuropharmacology 24 (1985) 639-644
31. Sanchez R.M., Dai W., Levada R.E., Lippman J.J., and Jensen F.E. AMPA/kainate receptor-mediated downregulation of GABAergic synaptic transmission by calcineurin after seizures in the developing rat brain. J Neurosci 25 (2005) 3442-3451
32. Smart T.G. Regulation of excitatory and inhibitory neurotransmitter-gated ion channels by protein phosphorylation. Curr Opin Neurobiol 7 (1997) 358-367
33. Song J., Shen G., Greenfield Jr. L.J., and Tietz E.I. Benzodiazepine withdrawal-induced glutamatergic plasticity involves up-regulation of GluR1-containing alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptors in hippocampal CA1 neurons. J Pharmacol Exp Ther 322 (2007) 569-581
34. A-receptor function in hippocampal cells is maintained by phosphorylation factors. Science 241 (1998) 339-341
35. Taft W.C., and DeLorenzo R.J. Micromolar-affinity benzodiazepine receptors regulate voltage-sensitive calcium channels in nerve terminal preparations. Proc Natl Acad Sci U S A 81 (1984) 3118-3122
36. i and L-type calcium channel activity in aged hippocampal neurons: relationship to impaired synaptic plasticity. J Neurosci 21 (2001) 9744-9756
37. Tietz E.I., Zeng X.J., Chen S., Lilly S.M., Rosenberg H.C., and Kometiani P. Antagonist-induced reversal of functional and structural measures of hippocampal benzodiazepine tolerance. J Pharmacol Exp Ther 291 (1999) 932-942
38. Van Sickle B., Xiang K., and Tietz E.I. Transient plasticity of hippocampal CA1 neuron glutamate receptors contributes to benzodiazepine withdrawal anxiety. Neuropsychopharmacology 29 (2004) 1994-2006
39. A receptor subtypes: any clues to the mechanism of benzodiazepine dependence?. Curr Opin Pharmacol 5 (2005) 47-52
40. A receptor function require L-type voltage-gated calcium channel activation. Neuropharmacology, in press.
41. Watson W.P., and Little H.J. Selectivity of the protective effects of dihydropyridine calcium channel antagonist against the ethanol withdrawal syndrome. Brain Res 930 (2002) 111-122
42. Weiland G.A., and Oswald R.E. The mechanism of binding of dihydropyridine calcium channel blockers to rat brain membranes. J Biol Chem 260 (1985) 8456-8464
43. Xiang K., Earl D.E., Davis K.M., Giovannucci D.R., Greenfield Jr. L.J., and Tietz E.I. Chronic benzodiazepine administration potentiates high voltage-activated calcium currents in hippocampal CA 1 neurons. J Pharmacol Exp Ther (2008) doi: 10.1124/jpet.108.144444. http://jpet.aspetjournals.org/papbyrecent.shtml
44. Xiang K., and Tietz E.I. Benzodiazepine-induced hippocampal CA1 neuron AMPA receptor plasticity linked to severity of withdrawal-anxiety: Differential role of voltage-gated calcium channels and NMDA receptors. Behav Pharmacol 18 (2007) 447-460
45. Xie X.H., and Tietz E.I. Reduction in potency of selective gamma-aminobutyric acid A agonists and diazepam in CA1 region of in vitro hippocampal slices from chronic flurazepam-treated rats. J Pharmacol Exp Ther 262 (1992) 204-211
46. Zeng X.J., and Tietz E.I. Benzodiazepine tolerance at GABAergic synapses on hippocampal CA1 pyramidal cells. Synapse 31 (1999) 263-277