Dual effects of gabapentin and pregabalin on glutamate release at rat entorhinal synapses in vitro

European Journal of Neuroscience

Volumn 20, Issue 6, 2004, Pages 1566-1576

  Cunningham, Mark O ^a,b   Woodhall, Gavin L ^a,c   Thompson, Sarah E ^a,d   Dooley, David J ^a,e   Jones, Roland S G ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b UNIVERSITY OF LEEDS   (United Kingdom)

^c ASTON UNIVERSITY   (United Kingdom)

^d MCGILL UNIVERSITY   (Canada)

^e PFIZER INC   (United States)

Author keywords

Ca channels; Evoked currents; Spontaneous currents

Indexed keywords

AMINO ACID TRANSPORTER; ANTICONVULSIVE AGENT; CALCIUM CHANNEL P TYPE; CALCIUM CHANNEL Q TYPE; GABAPENTIN; GLUTAMIC ACID; ISOLEUCINE; PREGABALIN; TETRODOTOXIN; VALPROIC ACID; VOLTAGE GATED CALCIUM CHANNEL;

AMPLITUDE MODULATION; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; ELECTROSTIMULATION; ENTORHINAL CORTEX; EXCITATORY POSTSYNAPTIC POTENTIAL; MALE; MINIATURE ENDPLATE POTENTIAL; NERVE ENDING; NEUROTRANSMITTER RELEASE; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; RAT; SYNAPSE;

AMINES; ANALYSIS OF VARIANCE; ANIMALS; ANTICONVULSANTS; BICUCULLINE; CALCIUM CHANNEL BLOCKERS; CYCLOHEXANECARBOXYLIC ACIDS; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; ELECTRIC STIMULATION; ENTORHINAL CORTEX; EXCITATORY POSTSYNAPTIC POTENTIALS; GABA ANTAGONISTS; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; ISOLEUCINE; MALE; NEURONS; OMEGA-CONOTOXIN GVIA; PATCH-CLAMP TECHNIQUES; RATS; RATS, WISTAR; SPIDER VENOMS; STATISTICS, NONPARAMETRIC; TETRODOTOXIN;

EID: 4644259036     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2004.03625.x     Document Type: Article

References (65)

1. Alden, K.J. & Garcia, J. (2001) Differential effect of gabapentin on neuronal and muscle calcium currents. J. Pharmacol. Exp. Ther., 297, 727-735.
2. Ben-Ari, Y., Tremblay, E., Riche, D., Ghilini, G. & Naquet, R. (1981) Electrographic, clinical and pathological alterations following systemic administration of kainic acid, bicuculline, or pentylenetetrazole: metabolic mapping using the deoxyglucose method with special reference to the pathology of epilepsy. Neuroscience, 6, 1361-1391.
3. Ben-Menachem., E., Persson, L.I. & Hedner, T. (1992) Selected CSF biochemistry and gabapentin concentrations in the CSF and plasma in patients with partial seizures after a single oral dose of gabapentin. Epilepsy Res., 11, 45-49.
4. Berretta, N. & Jones, R.S.G. (1996) A comparison of spontaneous synaptic EPSCs in layer V and layer II neurones in the rat entorhinal cortex in vitro. J. Neurophysiol., 76, 1089-1100.
5. Bryans, J.S. & Wustrow, D.J. (1999) 3-Substituted GABA analogs with central nervous system activity: a review. Med. Res. Rev., 19, 149-177.
6. Buchheim, K., Weissinger, F., Siegmund, H., Holtkamp, M., Schuchmann, S. & Meierkord, H. (2002) Intrinsic optical imaging reveals regionally different manifestation of spreading depression in hippocampal and entorhinal structures in vitro. Exp. Neurol., 175, 76-86.
7. Calabresi, P., Centonze, D., Marfia, G.A., Pisani, A. & Bernardi, G. (1999) An in vitro electrophysiological study on the effects of phenytoin, lamotrigine and gabapentin on striatal neurones. Br. J. Pharmacol., 126, 689-696.
8. 3H]-acetylcholine release from rat cortical slices and guinea-pig myenteric plexus. Br. J. Pharmacol., 120, 88-92.
9. Cunningham, M.O., Dhillon, A., Wood, S.J. & Jones, R.S.G. (2000) Reciprocal modulation of glutamate and GABA release may underlie the anticonvulsant effect of phenytoin. Neuroscience, 95, 343-351.
10. Cunningham, M.O., Dooley, D.J. & Jones, R.S.G. (2001) Gabapentin reduces spontaneous glutamate release in the entorhinal cortex. Soc. Neurosci. Abstr., 31, 711.4.
11. Cunningham, M.O. & Jones, R.S.G. (2000) Lamotrigine decreases spontaneous glutamate release and increases GABA release in the rat entorhinal cortex in vitro. Neuropharmacology, 39, 2139-2146.
12. Cunningham, M.O., Woodhall, G.L. & Jones, R.S.G. (2003) Valproate modifies spontaneous excitation and inhibition at cortical synapses in vitro. Neuropharmacol., 45, 907-917.
13. Cunningham, M.O., Thompson, S.E., Dooley, D.J. & Jones, R.S.G. (2002) Whole-cell patch-clamp studies of pregabalin and gabapentin on spontaneous glutamate release in the entorhinal cortex. Soc. Neurosci. Abstr., 32, 549.6.
14. D'Arcangelo, G., Tancredi, V. & Avoli, M. (2001) Intrinsic optical signals and electrographic seizures in the rat limbic system. Neurobiol. Dis., 8, 993-1005.
15. Debanne, D., Guerineau, N.C., Gahwiler, B.H. & Thompson, S.M. (1996) Paired-pulse facilitation and depression at unitary synapses in rat hippocampus: quantal fluctuation affects subsequent release. J. Physiol. (Lond.), 491, 163-176.
16. DeLorenzo, R.J. (1986) A molecular approach to the calcium signal in brain: relationship to synaptic modulation and seizure discharge. Adv. Neurol., 44, 435-464.
17. 3H]- norepinephrine release from rat neocortical slices. Synapse, 45, 171-190.
18. +-evoked glutamate release from rat neocortical and hippocampal slices by gabapentin. Neurosci. Lett., 280, 107-110.
19. 2+ entry, and spontaneous transmitter release. Neuron, 29, 197-208.
20. 2+ influx by gabapentin and pregabilin in the human neocortex. Neuropharmacology, 42, 229-236.
21. 2+ influx by gabapentin and subsequent reduction of neurotransmitter release from rat neocortical slices. Br. J. Pharmacol., 130, 900-906.
22. 2δ subunit of a calcium channel. J. Biol Chem., 271, 5768-5776.
23. 2+ influx and synaptic transmission in rat hippocampus and neocortex. Eur. J. Pharmacol., 449, 221-228.
24. Jones, R.S.G. & Heinemann, U. (1988) Synaptic and intrinsic responses of medial entorhinal cortical cells in normal and magnesium free medium in vitro. J. Neurophysiol., 59, 1476-1497.
25. Jones, R.S.G. & Lambert, J.D.C. (1990) The role of excitatory amino acid receptors in the propagation of epileptiform discharges from the entorhinal cortex to the dentate gyrus in vitro. Exp. Brain Res., 80, 310-322.
26. 2δ subunit. J. Neurosci., 19, 684-691.
27. Llano, I., Gonzalez, J., Caputo, C., Lai, F.A., Blayney, L.M., Tan, Y.P. & Marty. A. (2000) Presynaptic calcium stores underlie large-amplitude miniature IPSCs and spontaneous calcium transients. Nat. Neurosci., 3, 1256-1265.
28. Macdonald, R.L. & Kelly, K.M. (1994) Mechanisms of action of currently prescribed and newly developed antiepileptic drugs. Epilepsia, 35, 41-50.
29. Maneuf, Y.P., Gonzalez, M.I., Sutton, K.S., Chung, F.Z., Pinnock, R.D. & Lee, K. (2003) Cellular and molecular action of the putative GABA-mimetic, gabapentin. Cell. Mol. Life Sci., 60, 742-750.
30. 3H]-glutamate from rat caudal trigeminal nucleus slices. Pain, 93, 191-196.
31. Maneuf, Y.P. & McKnight, A.T. (2001) Block by gabapentin of the facilitation of glutamate release from rat trigeminal nucleus following activation of protein kinase C or adenylyl cyclase. Br. J. Pharmacol., 134, 237-240.
32. 2δ subunits ñ structure and gabapentin binding. Mol. Pharmacol., 59, 1243-1248.
33. Martin, D.J., McClelland, D., Herd, M.B., Sutton, K.G., Hall, M. & Lee, K. (2002) Gabapentin mediated inhibition of voltage activated calcium channel currents in cultured sensory neurones is dependent on culture conditions and channel subunit expression. Neuropharmacology, 42, 353-366.
34. +-induced calcium influx by gabapentin. Brain Res., 875, 157-159.
35. Moore, K.A., Baba, H. & Woolf, C.J. (2002) Gabapentin - actions on adult superficial dorsal horn neurones. Neuropharmacology, 43, 1077-1081.
36. Patel, M.K., Gonzalez, I., Bramwell, S., Pinnock, R.D. & Lee, K. (2000) Gabapentin inhibits excitatory synaptic transmission in the hyperalgesic spinal cord. Br. J. Pharmacol., 130, 1731-1734.
37. Rock, D.M., Kelly, K.M. & Macdonald, R.L. (1993) Gabapentin actions on ligand and voltage gated responses in cultured rodent neurones. Epilepsy Res., 16, 89-98.
38. Rutecki, P.A., Grossman, R.G., Armstrong, D. & Irish-Loewen, S. (1989) Electrophysiological connections between the hippocampus and entorhinal cortex in patients with complex partial seizures. J. Neurosurg., 70, 667-675.
39. Savic, N. & Sciancalepore, M. (1998) Intracellular calcium stores modulate miniature GABA-mediated synaptic currents in neonatal rat hippocampal neurons. Eur. J. Neurosci., 10, 3379-3386.
40. 2+ channels involved? Neuropharmacology, 34, 1549-1557.
41. Scanziani, M., Capogna, M.G., ‰hwiler, B.H. & Thompson, S.M. (1992) Presynaptic inhibition of miniature excitatory synaptic currents by baclofen and adenosine in the hippocampus. Neuron, 9, 919-927.
42. Schlicker, E., Reimann, W. & Gothert, M. (1985) Gabapentin decreases monoamine release without affecting acetylcholine release in the brain. Arzneim-Forsch. Drug Res., 35, 1347-1349.
43. Schumacher, T.B., Beck, H., Steinhauser, C., Schramm, J. & Elger, C.E. (1998) Effects of carbamazepine and gabapentin on calcium channels in hippocampal granule cells from patients with temporal lobe epilepsy. Epilepsia, 39, 355-363.
44. Shimoyama, M., Shimoyama, N. & Hori, Y. (2000) Gabapentin affects glutamate excitatory neurotransmission in the rat dorsal horn. Pain, 85, 405-414.
45. Siegel, A.N., Wieser, H.G., Wichnann, W. & Yasargil, G.M. (1990) Relationships between MR imaged total amount of tissue removed, resection scores of specific mediobasal limbic sub-compartments and clinical outcome following selective amygdala-hippocampectomy. Epilepsy Res., 63, 56-65.
46. Simkus, C.R. & Stricker, C. (2002) The contribution of intracellular calcium stores to mEPSCs recorded in layer II neurones of rat barrel cortex. J. Physiol. (Lond.), 545, 521-535.
47. Spencer, S.S. & Spencer, D.D. (1994) Entorhinal-hippocampal interactions in medial temporal lobe epilepsy syndrome. Epilepsia, 35, 721-727.
48. Stacey, A.E., Woodhall, G.L. & Jones, R.S.G. (2002) Tachykinin receptor mediated depolarisation of cortical neurones elicits a self-sustaining increase in glutamate release at cortical synapses. Eur. J. Neurosci., 16, 1896-1906.
49. Stefani, A., Spadoni, F. & Bernardi, G. (1998) Gabapentin inhibits calcium currents in isolated rat brain neurons. Neuropharmacology, 37, 83-91.
50. Stefani, A., Spadoni, F., Giacomini, P., Lavaroni, F. & Bernardi, G. (2001) The effects of gabapentin on different ligand- and voltage-gated currents in isolated cortical neurones. Epilepsy Res., 43, 239-248.
51. Stewart, B.H., Kugler, A.R., Thompson, P.R. & Bockbader, H.N. (1993) A saturable transport mechanism in the intestinal absorption of gabapentin in the underlying cause of a lack of proportionality between increasing dose and drug levels in plasma. Pharmacol. Res., 10, 276-281.
52. Su, T.Z., Lunnet, E., Campbell, G. & Oxender, D.L. (1995) Transport of gabapentin, a g-amino acid drug, by System L a-amino acid transporters: a comparative study in astrocytes, synaptosomes, and CHO cells. J. Neurochem., 64, 2125-2131.
53. Sugaya, E., Kishii, K. & Onozuka, M. (1985a) Inhibitory effect of phenytoin on intracellular cyclic nucleotide and calcium changes during pentylenetetrazole-induced bursting activity in snail neurons. Brain Res., 341, 313-319.
54. Sugaya, E., Onozuka, M., Furuichi, H., Kishii, K., Imai, S. & Sugaya, A. (1985b) Effect of phenytoin on intracellular calcium and intracellular protein changes during penrylenetetrazole-induced bursting activity in snail neurons. Brain Res., 327, 161-168.
55. 3H]-gabapentin binding to a novel site in rat brain: homogenate binding studies. Eur. J. Pharmacol., 244, 293-301.
56. Sutton, K.G., Martin, D.J., Pinnock, R.D., Lee, K. & Scott, R.H. (2002) Gabapentin inhibits high-threshold calcium channel currents in cultured rat dorsal root ganglion neurones. Br. J. Pharmacol., 135, 257-265.
57. Taylor, C.P., Gee, N.S., Su, T.-Z., Kocsis, J.D., Welty, D.F., Brown, J.P., Dooley, D.J., Boden, P. & Singh, L. (1998) A summary of mechanistic hypotheses of gabapentin pharmacology. Epilepsy Res., 29, 233-249.
58. Taylor, C.P., Vartanian, M.G., Yuen, P., Bigge, C., Suman-Chauhan, N. & Hill, D.R. (1993) Potent and stereoselective anticonvulsant activity of 3-isobutyl GABA relates to in vitro binding at a novel site labelled by tritiated gabapentin. Epilepsy Res., 14, 11-15.
59. 3H]-gabapentin binding may label a system-L like neutral amino acid carrier in brain. Eur. J. Pharmacol., 247, 341-345.
60. 3H]-gabapentin with excitatory amino acid receptor and amino acid uptake site distributions in rat brain. Br. J. Pharmacol., 118, 457-465.
61. 3H]- leucine into rat brain synaptosomes. Br. J. Pharmacol., 118, 449-456.
62. Upton, N. (1994) Mechanisms of action of new antiepileptic drugs: rational design and serendipitous findings. Trends Pharmacol. Sci., 15, 456-463.
63. Weissinger, F., Buchheim, K., Siegmund, H., Heinemann, U. & Meierkord, H. (2000) Optical imaging reveals characteristic seizure onsets, spread patterns, and propagation velocities in hippocampal-entorhinal cortex slices of juvenile rats. Neurobiol. Dis, 7, 286-298.
64. Wennberg, R., Arruda, F., Quesney, L.F. & Olivier, A. (2002) Pre-eminence of extra-hippocampal structures in the generation of mesial temporal seizures: evidence from human depth electrode recordings. Epilepsia, 4, 716-726.
65. +-channels expressed in a stable cell line. Pflugers Arch., 441, 425-433.