Carbamazepine-resistance in the epileptic dentate gyrus of human hippocampal slices

Brain

Volumn 129, Issue 12, 2006, Pages 3290-3306

  Jandová, Katerina ^a,c   Päsler, Dennis ^a   Antonio, Leandro Leite ^a,d   Raue, Claudia ^a   Ji, Shengbo ^a   Njunting, Marleisje ^a   Kann, Oliver ^a   Kovács, Richard ^a   Meencke, Heinz Joachim ^e   Cavalheiro, Esper A ^d   Heinemann, Uwe ^a,b   Gabriel, Siegrun ^a   Lehmann, Thomas Nicolas ^b  

^a Institute of Neurophysiology   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c CHARLES UNIVERSITY   (Czech Republic)

^d FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^e Evangelisches Krankhs Konigin E H   (Germany)

Author keywords

Drug resistance; Electrophysiology; Epilepsy; Hippocampus; Human

Indexed keywords

CARBAMAZEPINE; POTASSIUM;

ARTICLE; BLOOD BRAIN BARRIER; BRAIN ELECTROPHYSIOLOGY; BRAIN SLICE; BRAIN TUMOR; CLINICAL EXAMINATION; CONTROLLED STUDY; DATA ANALYSIS; DENTATE GYRUS; DRUG EFFECT; EPILEPTIC DISCHARGE; EXTRACELLULAR FLUID; HIPPOCAMPUS; HUMAN; HUMAN TISSUE; NEUROPATHOLOGY; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; TEMPORAL LOBE EPILEPSY; TISSUE SECTION;

ACTION POTENTIALS; ADULT; AGE FACTORS; ANTICONVULSANTS; BLOOD-BRAIN BARRIER; BRAIN NEOPLASMS; CARBAMAZEPINE; DENTATE GYRUS; DRUG ADMINISTRATION SCHEDULE; DRUG RESISTANCE; ELECTRIC STIMULATION; EPILEPSY, TEMPORAL LOBE; FEMALE; HUMANS; MALE; POTASSIUM; TIME FACTORS;

EID: 33845302656     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awl218     Document Type: Article

References (73)

1. Abbott NJ, Romero IA. Transporting therapeutics across the blood-brain barrier. Mol Med Today 1996; 2: 106-13.
2. Abbott NJ, Khan EU, Rollinson CM, Reichel A, Janigro D, Dombrowski SM, et al. Drug resistance in epilepsy: the role of the blood-brain barrier. Novartis Found Symp 2002; 243: 38-47.
3. Arias RL, Bowlby MR. Pharmacological characterization of antiepileptic drugs and experimental analgesics on low magnesium-induced hyperexcitability in rat hippocampal slices. Brain Res 2005; 1047: 233-44.
4. Aronica E, Gorter JA, Jansen GH, van Veelen CW, van Rijen PC, Leenstra S, et al. Expression and cellular distribution of multidrug transporter proteins in two major causes of medically intractable epilepsy: focal cortical dysplasia and glioneuronal tumours. Neuroscience 2003a; 118: 417-29.
5. Aronica E, Gorter JA, Van Vliet EA, Spliet WG, van Veelen CW, van Rijen PC, et al. Overexpression of the human major vault protein in gangliogliomas. Epilepsia 2003b; 44: 1166-75.
6. Aronica E, Gorter JA, Ramkema M, Redeker S, Ozbas-Gerceker F, Van Vliet EA, et al. Expression and cellular distribution of multidrug resistance-related proteins in the hippocampus of patients with mesial temporal lobe epilepsy. Epilepsia 2004; 45: 441-51.
7. Babb TL, Pretorius JK, Kupfer WR, Crandall PH. Glutamate decarboxylase-immunoreactive neurons are preserved in human epileptic hippocampus. J Neurosci 1989; 9: 2562-74.
8. Baumgartner C, Elger CE, Hufnagel A, Oppel F, Runge U, Schramm J, et al. Qualitätsrichtlinien auf dem Gebiet der prächirurgischen Epilepsiediagnostik und operativen Epilepsietherapie. Akt Neurol 2000; 27: 88-9.
9. Calatozzolo C, Gelati M, Ciusani E, Sciacca FL, Pollo B, Cajola L, et al. Expression of drug resistance proteins Pgp, MRP1, MRP3, MRP5 and GST-pi in human glioma. J Neurooncol 2005; 74: 113-21.
10. Colom LV, Saggau P. Spontaneous interictal-like activity originates in multiple areas of the CA2-CA3 region of hippocampal slices. J Neurophysiol 1994; 71: 1574-85.
11. de Lanerolle NC, Kim JH, Robbins RJ, Spencer DD. Hippocampal interneuron loss and plasticity in human temporal lobe epilepsy. Brain Res 1989; 495: 387-95.
12. Dlugos DJ. The early identification of candidates for epilepsy surgery. Arch Neurol 2001; 58: 1543-6.
13. Dombrowski SM, Desai SY, Marroni M, Cucullo L, Goodrich K, Bingaman W, et al. Overexpression of multiple drug resistance genes in endothelial cells from patients with refractory epilepsy. Epilepsia 2001; 42: 1501-6.
14. Dreier JP, Heinemann U. Regional and time dependent variations of low magnesium induced epileptiform activity in rat temporal cortex. Exp Brain Res 1991; 87: 581-96.
15. Engel J Jr. Outcome with respect to epileptic seizures. In: Engel J Jr, editor. Surgical treatment of the epilepsies. New York: Raven Press; 1987. p. 553-72.
16. Engel J Jr. Surgery for seizures. N Engl J Med 1996; 334: 647-52.
17. European Federation of Neurological Societies Task Force (2000), Pre-surgical evaluation for epilepsy surgery - European Standards. Eur J Neurol 2000; 7: 119-22.
18. 0 and field potentials in dentate gyrus and area CA1 of human epileptic hippocampus. Neurosci Lett 1998; 249: 91-4.
19. Gabriel S, Njunting M, Pomper JK, Merschhemke M, Sanabria ER, Eilers A, et al. Stimulus and potassium-induced epileptiform activity in the human dentate gyrus from patients with and without hippocampal sclerosis. J Neurosci 2004; 24: 10416-30.
20. Golden PL, Pardridge WM. Brain microvascular P-glycoprotein and a revised model of multidrug resistance in brain. Cell Mol Neurobiol 2000; 20: 165-81.
21. Hermanns G, Noachtar S, Tuxhorn I, Holthausen H, Ebner A, Wolf P. Systematic testing of medical intractability for carbamazepine, phenytoin, and phenobarbital or primidone in monotherapy for patients considered for epilepsy surgery. Epilepsia 1996; 37: 675-9.
22. Houser CR, Miyashiro JE, Swartz BE, Walsh GO, Rich JR, Delgado-Escueta AV. Altered patterns of dynorphin immunoreactivity suggest mossy fiber reorganization in human hippocampal epilepsy. J Neurosci 1990; 10: 267-82.
23. Jensen MS, Yaari Y. Role of intrinsic burst firing, potassium accumulation, and electrical coupling in the elevated potassium model of hippocampal epilepsy. J Neurophysiol 1997; 77: 1224-33.
24. Kann O, Kovacs R, Njunting M, Behrens CJ, Otahal J, Lehmann TN, et al. Metabolic dysfunction during neuronal activation in the ex vivo hippocampus from chronic epileptic rats and humans. Brain 2005; 128: 2396-407.
25. Korn SJ, Giacchino JL, Chambering NL, Dingledine R. Epileptiform burst activity induced by potassium in the hippocampus and its regulation by GABA-mediated inhibition. J Neurophysiol 1987; 57: 325-40.
26. Kubota H, Ishihara H, Langmann T, Schmitz G, Stieger B, Wieser H-G, et al. Distribution and functional activity of P-glycoprotein and multidrug resistance-associated proteins in human brain microvascular endothelial cells in hippocampal sclerosis. Epilepsy Res 2006; 68: 213-28.
27. Kuo CC. A common anticonvulsant binding site for phenytoin, carbamazepine, and lamotrigine in neuronal Na+ channels. Mol Pharmacol 1998; 54: 712-21.
28. Kwan P, Brodie MJ. Potential role of drug transporters in the pathogenesis of medically intractable epilepsy. Epilepsia 2005; 46: 224-35.
29. Lazarowski A, Sevlever G, Taratuto A, Massaro M, Rabinowicz A. Tuberous sclerosis associated with MDR1 gene expression and drug-resistant epilepsy. Pediatr Neurol 1999; 21: 731-34.
30. Lazarowski A, Lubieniecki F, Camarero S, Pomata H, Bartuluchi M, Sevlever G, et al. Multidrug resistance proteins in tuberous sclerosis and refractory epilepsy. Pediatr Neurol 2004; 30: 102-6.
31. Lee G, Dallas S, Hong M, Bendayan R. Drug transporters in the central nervous system: brain barriers and brain parenchyma considerations. Pharmacol Rev 2001; 53: 569-96.
32. Lehmann TN, Gabriel S, Kovacs R, Eilers A, Kivi A, Schulze K, et al. Alterations of neuronal connectivity in area CA1 of hippocampal slices from temporal lobe epilepsy patients and from pilocarpine-treated epileptic rats. Epilepsia 2000; 41 (Suppl 6): S190-4.
33. 2+ concentration in rat hippocampal slices. Exp Brain Res 1993; 96: 230-40.
34. Löscher W, Potschka H. Role of multidrug transporters in pharmacoresistance to antiepileptic drugs. J Pharmacol Exp Ther 2002; 301: 7-14.
35. Löscher W, Potschka H. Blood-brain barrier active efflux transporters: ATP-binding cassette gene family. NeuroRx 2005a; 2: 86-98.
36. Löscher W, Potschka H. Drug resistance in brain diseases and the role of drug efflux transporters. Nat Rev Neurosci 2005b; 6: 591-602.
37. Löscher W, Potschka H. Role of drug efflux transporters in the brain for drug disposition and treatment of brain diseases. Prog Neurobiol 2005c; 76: 22-76.
38. Lux HD, Neher E. The equilibration time course of (K + 0) in cat cortex. Exp Brain Res 1973; 17: 190-205.
39. Magloczky Z, Freund TF. Impaired and repaired inhibitory circuits in the epileptic human hippocampus. Trends Neurosci 2005; 28: 334-40.
40. Magloczky Z, Wittner L, Borhegyi Z, Halasz P, Vajda J, Czirjak S, et al. Changes in the distribution and connectivity of interneurons in the epileptic human dentate gyrus. Neuroscience 2000; 96: 7-25.
41. Maines LW, Antonetti DA, Wolpert EB, Smith CD. Evaluation of the role of P-glycoprotein in the uptake of paroxetine, clozapine, phenytoin and carbamazapine by bovine retinal endothelial cells. Neuropharmacology 2005; 49: 610-17.
42. Marchi N, Hallene KL, Kight KM, Cucullo L, Moddel G, Bingaman W, et al. Significance of MDR I and multiple drug resistance in refractory human epileptic brain. BMC Med 2004; 2: 37.
43. Marchi N, Guiso G, Rizzi M, Pirker R, Novak K, Czech T, et al. A pilot study on brain-to-plasma partition of 10,11-dyhydro-10-hydroxy-5Hdibenzo(b,f) azepine-5-carboxamide and MDR1 brain expression in epilepsy patients not responding to oxcarbazepine. Epilepsia 2005; 46: 1613-9.
44. Masukawa LM, O'Connor WM, Lynott J, Burdette LJ, Uruno K, McGonigle P, et al. Longitudinal variation in cell density and mossy fiber reorganization in the dentate gyrus from temporal lobe epileptic patients. Brain Res 1995; 678: 65-75.
45. Neels HM, Sierens AC, Naelaerts K, Scharpe SL, Hatfield GM, Lambert WE. Therapeutic drug monitoring of old and newer anti-epileptic drugs. Clin Chem Lab Med 2004; 42: 1228-55.
46. Nies AT, Jedlitschky G, Konig J, Herold-Mende C, Steiner HH, Schmitt H-P, et al. Expression and immunolocalization of the multidrug resistance proteins, MRP1-MRP6 (ABCC1-ABCC6), in human brain. Neuroscience 2004; 129: 349-60.
47. Owen A, Pirmohamed M, Tettey JN, Morgan P, Chadwick D, Park BK. Carbamazepine is not a substrate for P-glycoprotein. Br J Clin Pharmacol 2001; 51: 345-9.
48. Potschka H, Fedrowitz M, Löscher W. P-glycoprotein and multidrug resistance-associated protein are involved in the regulation of extracellular levels of the major antiepileptic drug carbamazepine in the brain. Neuroreport 2001; 12: 3557-60.
49. Potschka H, Fedrowitz M, Löscher W. Brain access and anticonvulsant efficacy of carbamazepine, lamotrigine, and felbamate in ABCC2/MRP2-deficient TR- rats. Epilepsia 2003; 44: 1479-86.
50. Ragsdale DS, Avoli M. Sodium channels as molecular targets for antiepileptic drugs. Brain Res Brain Res Rev 1998; 26: 16-28.
51. Reckziegel G, Beck H, Schramm J, Urban BW, Elger CE. Carbamazepine effects on Na+ currents in human dentate granule cells from epileptogenic tissue. Epilepsia 1999; 40: 401-7.
52. Remy S, Beck H. Molecular and cellular mechanisms of pharmacoresistance in epilepsy. Brain 2006; 129: 18-35.
53. Remy S, Gabriel S, Urban BW, Dietrich D, Lehmann TN, Elger CE, et al. A novel mechanism underlying drug resistance in chronic epilepsy. Ann Neurol 2003a; 53: 469-79.
54. Remy S, Urban BW, Elger CE, Beck H. Anticonvulsant pharmacology of voltage-gated Na+ channels in hippocampal neurons of control and chronically epileptic rats. Eur J Neurosci 2003b; 17: 2648-58.
55. Rutecki PA, Lebeda FJ, Johnston D. Epileptiform activity induced by changes in extracellular potassium in hippocampus. J Neurophysiol 1985; 54: 1363-74.
56. Schwarz JR, Grigat G. Phenytoin and carbamazepine: potential- and frequency-dependent block of Na currents in mammalian myelinated nerve fibers. Epilepsia 1989; 30: 286-94.
57. Semah F, Gimenez F, Longer E, Laplane D, Thuillier A, Baulac M. Carbamazepine and its epoxide: an open study of efficacy and side effects after carbamazepine dose increment in refractory partial epilepsy. Ther Drug Monit 1994; 16: 537-40.
58. Semah F, Picot MC, Adam C, Broglin D, Arzimanoglou A, Bazin B, et al. Is the underlying cause of epilepsy a major prognostic factor for recurrence? Neurology 1998; 51: 1256-62.
59. Sisodiya SM, Lin WR, Squier MV, Thom M. Multidrug-resistance protein 1 in focal cortical dysplasia. Lancet 2001; 357: 42-3.
60. Sisodiya SM, Lin WR, Harding BN, Squier MV, Thom M. Drug resistance in epilepsy: expression of drug resistance proteins in common causes of refractory epilepsy. Brain 2002; 125: 22-31.
61. Sisodiya SM, Martinian L, Scheffer GL, van der Valk P, Scheper RJ, Harding BN, et al. Vascular colocalization of P-glycoprotein, multidrug-resistance associated protein 1, breast cancer resistance protein and major vault protein in human epileptogenic pathologies. Neuropathol Appl Neurobiol 2006; 32: 51-63.
62. Strandjord RE, Johannessen SI. Single-drug therapy with carbamazepine in patients with epilepsy: serum levels and clinical effect. Epilepsia 1980; 21: 655-62.
63. Sutula T, Cascino G, Cavazos J, Parada I, Ramirez L. Mossy fiber synaptic reorganization in the epileptic human temporal lobe. Ann Neurol 1989; 26: 321-30.
64. Tishler DM, Weinberg KI, Hinton DR, Barbaro N, Annett GM, Raffel C. MDR1 gene expression in brain of patients with medically intractable epilepsy. Epilepsia 1995; 36: 1-6.
65. Traynelis SF, Dingledine R. Potassium-induced spontaneous electrographic seizures in the rat hippocampal slice. J Neurophysiol 1988; 59: 259-76.
66. Vogelgesang S, Kunert-Keil C, Cascorbi I, Mosyagin I, Schroder E, Runge U, et al. Expression of multidrug transporters in dysembryoplastic neuroepithelial tumours causing intractable epilepsy. Clin Neuropathol 2004; 23: 223-31.
67. Vreugdenhil M, van Veelen CW, van Rijen PC, Lopes da Silva FH, Wadman WJ. Effect of valproic acid on sodium currents in cortical neurons from patients with pharmaco-resistant temporal lobe epilepsy. Epilepsy Res 1998; 32: 309-20.
68. Vreugdenhil M, Wadman WJ. Modulation of sodium currents in rat CA1 neurons by carbamazepine and valproate after kindling epileptogenesis. Epilepsia 1999; 40: 1512-22.
69. Weiss J, Kerpen CJ, Lindenmaier H, Dormann SM, Haefeli WE. Interaction of antiepileptic drugs with human P-glycoprotein in vitro. J Pharmacol Exp Ther 2003; 307: 262-7.
70. Wieser HG, Häne A. Antiepileptic drug treatment before and after selective amygdalohippocampectomy. Epilepsy Res 2003; 55: 211-23.
71. Willow M, Gonoi T, Catterall WA. Voltage clamp analysis of the inhibitory actions of diphenylhydantoin and carbamazepine on voltage-sensitive sodium channels in neuroblastoma cells. Mol Pharmacol 1985; 27: 549-58.
72. Wittner L, Magloczky Z, Borhegyi Z, Halasz SZ, Toth L, Eross Z, et al. Preservation of perisomatic inhibitory input of granule cells in the epileptic human dentate gyrus. Neuroscience 2001; 108: 587-600.
73. Wyler AR, Dohan FC, Schweitzer JB, Berry AD. A grading system for mesial temporal pathology (hippocampal sclerosis) from anterior temporal lobectomy. J Epilepsy 1992; 5: 220-5.