Antiepileptic drug-resistant rats differ from drug-responsive rats in hippocampal neurodegeneration and GABAA receptor ligand binding in a model of temporal lobe epilepsy

Neurobiology of Disease

Volumn 21, Issue 3, 2006, Pages 633-646

  Volk, Holger A ^a,b   Arabadzisz, Dimitrula ^c   Fritschy, Jean Marc ^c   Brandt, Claudia ^a   Bethmann, Kerstin ^a   Löscher, Wolfgang ^a,d  

^a UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^b ROYAL VETERINARY COLLEGE   (United Kingdom)

^c UNIVERSITY OF ZURICH   (Switzerland)

^d CENTER FOR SYSTEMS NEUROSCIENCE   (Germany)

Author keywords

Dentate gyrus; Drug resistance; Hippocampus; Phenobarbital; Refractory epilepsy

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; ANTICONVULSIVE AGENT; CLONAZEPAM; DIAZEPAM; FLUMAZENIL; PHENOBARBITAL;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTICONVULSANT THERAPY; ARTICLE; AUTORADIOGRAPHY; BRAIN NERVE CELL; CEREBROVASCULAR ACCIDENT; CONTROLLED STUDY; DENTATE GYRUS; DISEASE DURATION; DISEASE SEVERITY; DRUG RECEPTOR BINDING; DRUG RESPONSE; DRUG SENSITIVITY; ELECTROENCEPHALOGRAM; ELECTROSTIMULATION; EPILEPTIC STATE; EXPERIMENTAL MODEL; HIPPOCAMPUS; MAXIMUM TOLERATED DOSE; MORBIDITY; MORPHOLOGY; NERVE CELL NECROSIS; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; RAT; RECURRENT DISEASE; SEIZURE; TEMPORAL LOBE EPILEPSY; VIDEORECORDING;

ANIMALS; ANTICONVULSANTS; AUTORADIOGRAPHY; DISEASE MODELS, ANIMAL; DRUG RESISTANCE; ELECTROENCEPHALOGRAPHY; EPILEPSY, TEMPORAL LOBE; HIPPOCAMPUS; LIGANDS; NERVE DEGENERATION; PHENOBARBITAL; RATS; RECEPTORS, GABA-A;

EID: 33244481273     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2005.09.006     Document Type: Article

References (67)

1. C.E. Adkins, G.V. Pillai, J. Kerby, T.P. Bonnert, C. Haldon, R.M. Mckernan, J.E. Gonzalez, K. Oades, P.J. Whiting, and P.B. Simpson Alpha4beta3delta GABA(A) receptors characterized by fluorescence resonance energy transfer-derived measurements of membrane potential J. Biol. Chem. 276 2001 38934 38939
2. M. Baulac Phenobarbital and other barbiturates: clinical efficacy and use in epilepsy R.H. Levy R.H. Mattson B.S. Meldrum E. Perucca Antiepileptic Drugs 5th ed. 2002 Lippincott Williams & Wilkins Philadelphia 514 521
3. D.J. Begley ABC transporters and the blood-brain barrier Curr. Pharm. Des 10 2004 1295 1312
4. R.A. Bender, S.V. Soleymani, A.L. Brewster, S.T. Nguyen, H. Beck, G.W. Mathern, and T.Z. Baram Enhanced expression of a specific hyperpolarization- activated cyclic nucleotide-gated cation channel (HCN) in surviving dentate gyrus granule cells of human and experimental epileptic hippocampus J. Neurosci. 23 2003 6826 6836
5. D. Benke, P. Fakitsas, C. Roggenmoser, C. Michel, U. Rudolph, and H. Mohler Analysis of the presence and abundance of GABAA receptors containing two different types of alpha subunits in murine brain using point-mutated alpha subunits J. Biol. Chem. 279 2004 43654 43660
6. A. Binaschi, G. Bregola, and M. Simonato On the role of somatostatin in seizure control: clues from the hippocampus Rev. Neurosci. 14 2003 285 301
7. C. Brandt, M. Glien, H. Potschka, H. Volk, and W. Löscher Epileptogenesis and neuropathology after different types of status epilepticus induced by prolonged electrical stimulation of the basolateral amygdala in rats Epilepsy Res. 55 2003 83 103
8. C. Brandt, H.A. Volk, and W. Löscher Striking differences in individual anticonvulsant response to phenobarbital in rats with spontaneous seizures after status epilepticus Epilepsia 45 2004 1488 1497
9. A.R. Brooks-Kayal, M.D. Shumate, H. Jin, T.Y. Rikhter, and D.A. Coulter Selective changes in single cell GABAA receptor subunit expression and function in temporal lobe epilepsy Nat. Med. 4 1998 1166 1172
10. P.S. Buckmaster, and A.L. Jongen-Relo Highly specific neuron loss preserves lateral inhibitory circuits in the dentate gyrus of kainate-induced epileptic rats J. Neurosci. 19 1999 9519 9529
11. E.H. Buhl, T.S. Otis, and I. Mody Zinc-induced collapse of augmented inhibition by GABA in a temporal lobe epilepsy model Science 271 1996 369 373
12. G.D. Cascino Clinical correlations with hippocampal atrophy Magn. Reson. Imaging 13 1995 1133 1136
13. M.R. Cilio, A.R. Bolanos, Z. Liu, R. Schmid, Y. Yang, C.E. Stafstrom, M.A. Mikati, and G.L. Holmes Anticonvulsant action and long-term effects of gabapentin in the immature brain Neuropharmacology 40 2001 139 147
14. A.S. Cohen, D.D. Lin, G.L. Quirk, and D.A. Coulter Dentate granule cell GABA(A) receptors in epileptic hippocampus: enhanced synaptic efficacy and altered pharmacology Eur. J. Neurosci. 17 2003 1607 1616
15. D.A. Coulter Chronic epileptogenic cellular alterations in the limbic system after status epilepticus Epilepsia 40 1999 S23 S33
16. D.A. Coulter Mossy fiber zinc and temporal lobe epilepsy: pathological association with altered "epileptic" gamma-aminobutyric acid A receptors in dentate granule cells Epilepsia 41 Suppl. 6 2000 S96 S99
17. D.A. Coulter Epilepsy-associated plasticity in gamma-aminobutyric acid receptor expression, function, and inhibitory synaptic properties Int. Rev. Neurobiol. 45 2001 237 252
18. D.A. Coulter, D.C. McIntyre, and W. Löscher Animal models of limbic epilepsies: what can they tell us? Brain Pathol. 12 2002 240 256
19. N.C. de Lanerolle, M. Brines, A. Williamson, J.H. Kim, and D.D. Spencer Neurotransmitters and their receptors in human temporal lobe epilepsy Epilepsy Res., Suppl. 7 1992 235 250
20. R.K. Ellerkmann, S. Remy, J. Chen, D. Sochivko, C.E. Elger, B.W. Urban, A. Becker, and H. Beck Molecular and functional changes in voltage-dependent Na(+) channels following pilocarpine-induced status epilepticus in rat dentate granule cells Neuroscience 119 2003 323 333
21. J. Engel Introduction to temporal lobe epilepsy Epilepsy Res. 26 1996 141 150
22. J. Engel Mesial temporal lobe epilepsy: what have we learned? Neuroscientist 7 2001 340 352
23. P.D. Fisher, E.F. Sperber, and S.L. Moshe Hippocampal sclerosis revisited Brain Dev. 20 1998 563 573
24. D.G. Fujikawa, H.H. Itabashi, A. Wu, and S.S. Shinmei Status epilepticus-induced neuronal loss in humans without systemic complications or epilepsy Epilepsia 41 2000 981 991
25. M. Glien, C. Brandt, H. Potschka, and W. Löscher Effects of the novel antiepileptic drug levetiracetam on spontaneous recurrent seizures in the rat pilocarpine model of temporal lobe epilepsy Epilepsia 43 2002 350 357
26. J.A. Gorter, E.A. van Vliet, E. Aronica, and F.H. Lopes Da Silva Progression of spontaneous seizures after status epilepticus is associated with mossy fibre sprouting and extensive bilateral loss of hilar parvalbumin and somatostatin-immunoreactive neurons Eur. J. Neurosci. 13 2001 657 669
27. T. Halonen, J. Nissinen, and A. Pitkänen Chronic elevation of brain GABA levels beginning two days after status epilepticus does not prevent epileptogenesis in rats Neuropharmacology 40 2001 536 550
28. P. Kwan, and M.J. Brodie Refractory epilepsy: a progressive, intractable but preventable condition? Seizure 11 2002 77 84
29. J.P. Leite, and E.A. Cavalheiro Effects of conventional antiepileptic drugs in a model of spontaneous recurrent seizures in rats Epilepsy Res. 20 1995 93 104
30. F. Loup, H.G. Wieser, Y. Yonekawa, A. Aguzzi, and J.M. Fritschy Selective alterations in GABAA receptor subtypes in human temporal lobe epilepsy J. Neurosci. 20 2000 5401 5419
31. W. Löscher Animal models of drug resistant epilepsy V. Ling Mechanisms of Drug Resistance in Epilepsy: Lessons from Oncology 2002 Wiley Chichester 149 158
32. W. Löscher Current status and future directions in the pharmacotherapy of epilepsy Trends Pharmacol. Sci. 23 2002 113 118
33. W. Löscher, and D. Hönack Comparison of the anticonvulsant efficacy of primidone and phenobarbital during chronic treatment of amygdala-kindled rats Eur. J. Pharmacol. 162 1989 309 322
34. W. Löscher, and H. Potschka Role of multidrug transporters in pharmacoresistance to antiepileptic drugs J. Pharmacol. Exp. Ther. 301 2002 7 14
35. W. Löscher, and H. Potschka Drug resistance in brain diseases and the role of drug efflux transporters Nat. Rev., Neurosci. 6 2005 591 602
36. W. Löscher, and H. Potschka Role of drug efflux transporters in the brain for drug disposition and treatment of brain diseases Prog. Neurobiol. 76 2005 22 76
37. M. Marroni, N. Marchi, L. Cucullo, N.J. Abbott, K. Signorelli, and D. Janigro Vascular and parenchymal mechanisms in multiple drug resistance: a lesson from human epilepsy Curr. Drug Targets 4 2003 297 304
38. L.M. Masukawa, L.J. Burdette, P. McGonigle, H. Wang, W. O'Connor, M.R. Sperling, M.J. O'Connor, and K. Uruno Physiological and anatomical correlates of the human dentate gyrus: consequences or causes of epilepsy Adv. Neurol. 79 1999 781 794
39. K. Morimoto, M. Fahnestock, and R.J. Racine Kindling and status epilepticus models of epilepsy: rewiring the brain Prog. Neurobiol. 73 2004 1 60
40. J.V. Nadler The recurrent mossy fiber pathway of the epileptic brain Neurochem. Res. 28 2003 1649 1658
41. J. Nissinen, T. Halonen, E. Koivisto, and A. Pitkänen A new model of chronic temporal lobe epilepsy induced by electrical stimulation of the amygdala in rat Epilepsy Res. 38 2000 177 205
42. G. Paxinos, and C. Watson The rat brain in stereotaxic coordinates 4th ed. 1998 Academic Press Sydney
43. Z. Peng, C.S. Huang, B.M. Stell, I. Mody, and C.R. Houser Altered expression of the delta subunit of the GABAA receptor in a mouse model of temporal lobe epilepsy J. Neurosci. 24 2004 8629 8639
44. H. Potschka, M. Fedrowitz, and W. Löscher P-Glycoprotein-mediated efflux of phenobarbital, lamotrigine, and felbamate at the blood-brain barrier: evidence from microdialysis experiments in rats Neurosci. Lett. 327 2002 173 176
45. H. Potschka, H.A. Volk, and W. Löscher Pharmacoresistance and expression of multidrug transporter P-glycoprotein in kindled rats NeuroReport 19 2004 1657 1661
46. R.J. Racine Modification of seizure activity by electrical stimulation: II. Motor seizure Electroencephalogr. Clin. Neurophysiol. 32 1972 281 294
47. A.H. Ratzliff, V. Santhakumar, A. Howard, and I. Soltesz Mossy cells in epilepsy: rigor mortis or vigor mortis? Trends Neurosci. 25 2002 140 144
48. A.H. Ratzliff, A.L. Howard, V. Santhakumar, I. Osapay, and I. Soltesz Rapid deletion of mossy cells does not result in a hyperexcitable dentate gyrus: implications for epileptogenesis J. Neurosci. 24 2004 2259 2269
49. G. Regesta, and P. Tanganelli Clinical aspects and biological bases of drug-resistant epilepsies Epilepsy Res. 34 1999 109 122
50. S. Remy, B.W. Urban, C.E. Elger, and H. Beck Anticonvulsant pharmacology of voltage-gated Na+ channels in hippocampal neurons of control and chronically epileptic rats Eur. J. Neurosci. 17 2003 2648 2658
51. S. Remy, S. Gabriel, B.W. Urban, D. Dietrich, T.N. Lehmann, C.E. Elger, U. Heinemann, and H. Beck A novel mechanism underlying drug resistance in chronic epilepsy Ann. Neurol. 53 2003 469 479
52. C.E. Ribak, C.M. Gall, and I. Mody The dentate gyrus and its role in seizures 1992 Elsevier Amsterdam
53. M. Rizzi, S. Caccia, G. Guiso, C. Richichi, J.A. Gorter, E. Aronica, M. Aliprandi, R. Bagnati, R. Fanelli, M. D'Incalci, R. Samanin, and A. Vezzani Limbic seizures induce P-glycoprotein in rodent brain: functional implications for pharmacoresistance J. Neurosci. 22 2002 5833 5839
54. R.J. Robbins, M.L. Brines, J.H. Kim, T. Adrian, N. de Lanerolle, S. Welsh, and D.D. Spencer A selective loss of somatostatin in the hippocampus of patients with temporal lobe epilepsy Ann. Neurol. 29 1991 325 332
55. M.A. Rogawski, and W. Löscher The neurobiology of antiepileptic drugs Nat. Rev., Neurosci. 5 2004 553 564
56. D. Schmidt, and W. Löscher Drug resistance in epilepsy: putative neurobiological and clinical mechanisms Epilepsia 46 2005 858 877
57. S.M. Sisodiya Mechanisms of antiepileptic drug resistance Curr. Opin. Neurol. 16 2003 197 201
58. R.S. Sloviter The functional organization of the hippocampal dentate gyrus and its relevance to the pathogenesis of temporal lobe epilepsy Ann. Neurol. 35 1994 640 654
59. R.S. Sloviter Hippocampal pathology and pathophysiology in temporal lobe epilepsy Neurologia 11 Suppl. 4 1996 29 32
60. R.S. Sloviter, and G. Nilaver Immunocytochemical localization of GABA-, cholecystokinin-, vasoactive intestinal polypeptide-, and somatostatin-like immunoreactivity in the area dentata and hippocampus of the rat J. Comp. Neurol. 256 1987 42 60
61. P. Somogyi, A.J. Hodgson, A.D. Smith, M.G. Nunzi, A. Gorio, and J.Y. Wu Different populations of GABAergic neurons in the visual cortex and hippocampus of cat contain somatostatin- or cholecystokinin-immunoreactive material J. Neurosci. 4 1984 2590 2603
62. B.M. Stell, and I. Mody Receptors with different affinities mediate phasic and tonic GABA(A) conductances in hippocampal neurons J. Neurosci. 22 2002 RC223
63. W.H. Theodore Surgical Treatment of Epilepsy 1992 Elsevier Amsterdam
64. H.A. Volk, K. Burkhardt, H. Potschka, J. Chen, A. Becker, and W. Löscher Neuronal expression of the drug efflux transporter P-glycoprotein in the rat hippocampus after limbic seizures Neuroscience 123 2004 751 759
65. H.A. Volk, and W. Löscher Multidrug resistance in epilepsy: rats with drug-resistant seizures exhibit enhanced brain expression of P-glycoprotein compared with rats with drug-responsive seizures Brain 128 2005 1358 1368
66. W. Wei, N. Zhang, Z. Peng, C.R. Houser, and I. Mody Perisynaptic localization of delta subunit-containing GABA(A) receptors and their activation by GABA spillover in the mouse dentate gyrus J. Neurosci. 23 2003 10650 10661
67. P.J. Whiting, K.A. Wafford, and R.M. Mckernan Pharmacological subtypes of GABAA receptors based on subunit composition D.L. Martin R.W. Olsen GABA in the Nervous System: the View at Fifty Years 2000 Lippincott Williams & Wilkins Philadelphia 113 126