Glutamate is critically involved in seizure-induced overexpression of P-glycoprotein in the brain

Neuropharmacology

Volumn 54, Issue 6, 2008, Pages 1006-1016

  Bankstahl, Jens P ^a,b   Hoffmann, Katrin ^a,b   Bethmann, Kerstin ^a,b   Loscher W ^a,b  

^a UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^b CENTER FOR SYSTEMS NEUROSCIENCE   (Germany)

Author keywords

Antiepileptic drugs; Epilepsy; MK 801; Pharmacoresistance; Pilocarpine; Tariquidar

Indexed keywords

DIAZEPAM; DIZOCILPINE; GLUTAMIC ACID; GLYCOPROTEIN P; PILOCARPINE; TARIQUIDAR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CAPILLARY; COMBINATION CHEMOTHERAPY; CONTROLLED STUDY; DRUG EFFECT; DYSPNEA; ENDOTHELIUM CELL; EPILEPTIC STATE; FEMALE; HIPPOCAMPUS; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REFLEX DISORDER; REPEATED DRUG DOSE; RIGHTING REFLEX; SEIZURE;

ANIMALS; APOPTOSIS; BRAIN CHEMISTRY; CAPILLARIES; DIZOCILPINE MALEATE; EPILEPSY, TEMPORAL LOBE; EXCITATORY AMINO ACID ANTAGONISTS; FEMALE; GLUTAMIC ACID; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; MUSCARINIC AGONISTS; NERVE DEGENERATION; P-GLYCOPROTEIN; PILOCARPINE; QUINOLINES; RATS; RATS, WISTAR; SEIZURES; STATUS EPILEPTICUS;

EID: 41949126379     PISSN: 00283908     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2008.02.008     Document Type: Article

References (61)

1. Bankstahl J.P., Potschka H., and Löscher W. Functional Impact of Overexpression of the Multidrug Transporter P-glycoprotein 48 h After Pilocarpine Induced Status Epilepticus. 2007 Neuroscience Meeting Planner (2007), Society for Neuroscience Program No. 166.21, San Diego, CA
2. Bauer B., Hartz A.M., Pekcec A., Toellner K., Miller D.S., and Potschka H. Seizure-induced upregulation of P-glycoprotein at the blood-brain barrier through glutamate and COX-2 signaling. Mol. Pharmacol. (2007) Epub ahead of print (Dec. 19, 2007)
3. Brandt C., Potschka H., Löscher W., and Ebert U. N-methyl-d-aspartate receptor blockade after status epilepticus protects against limbic brain damage but not against epilepsy in the kainate model of temporal lobe epilepsy. Neuroscience 118 (2003) 727-740
4. Brandt C., Bethmann K., Gastens A.M., and Löscher W. The multidrug transporter hypothesis of drug resistance in epilepsy: proof-of-principle in a rat model of temporal lobe epilepsy. Neurobiol. Dis. 24 (2006) 202-211
5. Carlson H., Ronne-Engstrom E., Ungerstedt U., and Hillered L. Seizure related elevations of extracellular amino acids in human focal epilepsy. Neurosci. Lett. 140 (1992) 30-32
6. Cavalheiro E.A., Naffah-Mazacoratti M.G., Mello L.E., and Leite J.P. The pilocarpine model of seizures. In: Pitkänen A., Schwartzkroin P.A., and Moshé S.L. (Eds). Models of Seizures and Epilepsy (2006), Elsevier, Amsterdam 433-448
7. Cilio M.R., Bolanos A.R., Liu Z., Schmid R., Yang Y., Stafstrom C.E., Mikati M.A., and Holmes G.L. Anticonvulsant action and long-term effects of gabapentin in the immature brain. Neuropharmacology 40 (2001) 139-147
8. Clifford D.B., Olney J.W., Benz A.M., Fuller T.A., and Zorumski C.F. Ketamine, phencyclidine, and MK-801 protect against kainic acid-induced seizure-related brain damage. Epilepsia 31 (1990) 382-390
9. Costa M.S., Rocha J.B., Perosa S.R., Cavalheiro E.A., and Naffah-Mazzacoratti M.G. Pilocarpine-induced status epilepticus increases glutamate release in rat hippocampal synaptosomes. Neurosci. Lett. 356 (2004) 41-44
10. de Lanerolle N.C., and Lee T.S. New facets of the neuropathology and molecular profile of human temporal lobe epilepsy. Epilepsy Behav. 7 (2005) 190-203
11. Dhar R., and Mirsattari S.M. Current approach to the diagnosis and treatment of refractory status epilepticus. Adv. Neurol. 97 (2006) 245-254
12. During M.J., and Spencer D.D. Extracellular hippocampal glutamate and spontaneous seizure in the conscious human brain. Lancet 341 (1993) 1607-1610
13. Fox E., and Bates S.E. Tariquidar (XR9576): a P-glycoprotein drug efflux pump inhibitor. Expert Rev. Anticancer Ther. 7 (2007) 447-459
14. Freitas R.M., Vasconcelos S.M., Souza F.C., Viana G.S., and Fonteles M.M. Oxidative stress in the hippocampus after pilocarpine-induced status epilepticus in Wistar rats. FEBS J. 272 (2005) 1307-1312
15. Fujikawa D.G. Neuroprotective effect of ketamine administered after status epilepticus onset. Epilepsia 36 (1995) 186-195
16. Fujikawa D.G. Prolonged seizures and cellular injury: understanding the connection. Epilepsy Behav. 7 Suppl. 3 (2005) S3-S11
17. Fujikawa D.G., Daniels A.H., and Kim J.S. The competitive NMDA receptor antagonist CGP 40116 protects against status epilepticus-induced neuronal damage. Epilepsy Res. 17 (1994) 207-219
18. Fujikawa D.G., Itabashi H.H., Wu A., and Shinmei S.S. Status epilepticus-induced neuronal loss in humans without systemic complications or epilepsy. Epilepsia 41 (2000) 981-991
19. Glien M., Brandt C., Potschka H., Voigt H., Ebert U., and Löscher W. Repeated low-dose treatment of rats with pilocarpine: low mortality but high proportion of rats developing epilepsy. Epilepsy Res. 46 (2001) 111-119
20. Gröticke I., Hoffmann K., and Löscher W. Behavioral alterations in the pilocarpine model of temporal lobe epilepsy in mice. Exp. Neurol. 207 (2007) 329-349
21. Halonen T., Nissinen J., and Pitkänen A. Chronic elevation of brain GABA levels beginning two days after status epilepticus does not prevent epileptogenesis in rats. Neuropharmacology 40 (2001) 536-550
22. Hao Y., Wu X.Y., Ren H.M., Ding D., Zhu G.X., Yu H., and Hong Z. [Effect of dizocilpine on P-glycoprotein expression in hippocampus in limbic seizure: experiment with rats]. Zhonghua Yi. Xue. Za Zhi. 87 (2007) 1641-1645
23. Hoffmann K., and Löscher W. Upregulation of brain expression of P-glycoprotein in MRP2-deficient TR(-) rats resembles seizure-induced up-regulation of this drug efflux transporter in normal rats. Epilepsia 48 (2007) 631-645
24. Holmes G.L. Seizure-induced neuronal injury: animal data. Neurology 59 (2002) S3-S6
25. Hong H., Lu Y., Ji Z.N., and Liu G.Q. Up-regulation of P-glycoprotein expression by glutathione depletion-induced oxidative stress in rat brain microvessel endothelial cells. J. Neurochem. 98 (2006) 1465-1473
26. Johnstone R.W., Ruefli A.A., Tainton K.M., and Smyth M.J. A role for P-glycoprotein in regulating cell death. Leuk. Lymphoma 38 (2000) 1-11
27. Johnstone R.W., Ruefli A.A., and Smyth M.J. Multiple physiological functions for multidrug transporter P-glycoprotein?. Trends Biochem. Sci. 25 (2000) 1-6
28. Kovacs R., Schuchmann S., Gabriel S., Kann O., Kardos J., and Heinemann U. Free radical-mediated cell damage after experimental status epilepticus in hippocampal slice cultures. J. Neurophysiol. 88 (2002) 2909-2918
29. Kwan P., and Brodie M.J. Potential role of drug transporters in the pathogenesis of medically intractable epilepsy. Epilepsia 46 (2005) 224-235
30. Lee T.S., Mane S., Eid T., Zhao H., Lin A., Guan Z., Kim J.H., Schweitzer J., King-Stevens D., Weber P., Spencer S.S., Spencer D.D., and de Lanerolle N.C. Gene expression in temporal lobe epilepsy is consistent with increased release of glutamate by astrocytes. Mol. Med. 13 (2007) 1-13
31. Lipton S.A., Gu Z., and Nakamura T. Inflammatory mediators leading to protein misfolding and uncompetitive/fast off-rate drug therapy for neurodegenerative disorders. Int. Rev. Neurobiol. 82 (2007) 1-27
32. Liu X.D., and Liu G.Q. P glycoprotein regulated transport of glutamate at blood brain barrier. Acta Pharmacol. Sin. 22 (2001) 111-116
33. Liu Z., Stafstrom C.E., Sarkisian M.R., Yang Y., Hori A., Tandon P., and Holmes G.L. Seizure-induced glutamate release in mature and immature animals: an in vivo microdialysis study. Neuroreport 8 (1997) 2019-2023
34. Löscher W., and Potschka H. Drug resistance in brain diseases and the role of drug efflux transporters. Nat. Rev. Neurosci. 6 (2005) 591-602
35. Löscher W., and Potschka H. Role of drug efflux transporters in the brain for drug disposition and treatment of brain diseases. Prog. Neurobiol. 76 (2005) 22-76
36. Marchi N., Hallene K.L., Kight K.M., Cucullo L., Moddel G., Bingaman W., Dini G., Vezzani A., and Janigro D. Significance of MDR1 and multiple drug resistance in refractory human epileptic brain. BMC Med. 2 (2004) 37
37. Marroni M., Agrawal M.L., Kight K., Hallene K.L., Hossain M., Cucullo L., Signorelli K., Namura S., Bingaman W., and Janigro D. Relationship between expression of multiple drug resistance proteins and p53 tumor suppressor gene proteins in human brain astrocytes. Neuroscience 121 (2003) 605-617
38. Millan M.H., Chapman A.G., and Meldrum B.S. Extracellular amino acid levels in hippocampus during pilocarpine-induced seizures. Epilepsy Res. 14 (1993) 139-148
39. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates. 4th ed. (1998), Academic Press, Sydney
40. Prasad A., Williamson J.M., and Bertram E.H. Phenobarbital and MK-801, but not phenytoin, improve the long-term outcome of status epilepticus. Ann. Neurol. 51 (2002) 175-181
41. Robakis T.K., and Hirsch L.J. Literature review, case report, and expert discussion of prolonged refractory status epilepticus. Neurocrit. Care 4 (2006) 35-46
42. Schmued L.C., Stowers C.C., Scallet A.C., and Xu L. Fluoro-Jade C results in ultra high resolution and contrast labeling of degenerating neurons. Brain Res. 1035 (2005) 24-31
43. Seegers U., Potschka H., and Löscher W. Transient increase of P-glycoprotein expression in endothelium and parenchyma of limbic brain regions in the kainate model of temporal lobe epilepsy. Epilepsy Res. 51 (2002) 257-268
44. Sherwin A.L. Neuroactive amino acids in focally epileptic human brain: a review. Neurochem. Res. 24 (1999) 1385-1395
45. Sisodiya S.M. Mechanisms of antiepileptic drug resistance. Curr. Opin. Neurol. 16 (2003) 197-201
46. Smolders I., Khan G.M., Manil J., Ebinger G., and Michotte Y. NMDA receptor-mediated pilocarpine-induced seizures: characterization in freely moving rats by microdialysis. Br. J. Pharmacol. 121 (1997) 1171-1179
47. Sorokin A. Cyclooxygenase-2: potential role in regulation of drug efflux and multidrug resistance phenotype. Curr. Pharm. Des. 10 (2004) 647-657
48. Sperk G. Kainic acid seizures in the rat. Progr. Neurobiol. 42 (1994) 1-32
49. Tate S.K., and Sisodiya S.M. Multidrug resistance in epilepsy: a pharmacogenomic update. Expert. Opin. Pharmacother 8 (2007) 1441-1449
50. Tejada S., Sureda A., Roca C., Gamundi A., and Esteban S. Antioxidant response and oxidative damage in brain cortex after high dose of pilocarpine. Brain Res. Bull. 71 (2007) 372-375
51. van Vliet E.A., van Schaik R., Edelbroek P.M., Redeker S., Aronica E., Wadman W.J., Marchi N., Vezzani A., and Gorter J.A. Inhibition of the multidrug transporter P-glycoprotein improves seizure control in phenytoin-treated chronic epileptic rats. Epilepsia 47 (2006) 672-680
52. van Vliet E.A., van Schaik R., Edelbroek P.M., Voskuyl R.A., Redeker S., Aronica E., Wadman W.J., and Gorter J.A. Region-specific overexpression of P-glycoprotein at the blood-brain barrier affects brain uptake of phenytoin in epileptic rats. J. Pharmacol. Exp. Ther. 322 (2007) 141-147
53. Vezzani A., and Granata T. Brain inflammation in epilepsy: experimental and clinical evidence. Epilepsia 46 (2005) 1724-1743
54. Volk H.A., and Löscher W. 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
55. Volk H.A., Burkhardt K., Potschka H., Chen J., Becker A., and Löscher W. Neuronal expression of the drug efflux transporter P-glycoprotein in the rat hippocampus after limbic seizures. Neuroscience 123 (2004) 751-759
56. Volk H.A., Potschka H., and Löscher W. Increased expression of the multidrug transporter P-glycoprotein in limbic brain regions after amygdala-kindled seizures in rats. Epilepsy Res. 58 (2004) 67-79
57. Volk H., Potschka H., and Löscher W. Immunohistochemial localization of P-glycoprotein in rat brain and detection of its increased expression by seizures are sensitive to fixation and staining variables. J. Histochem. Cytochem. 53 (2005) 517-531
58. Wilson C.L., Maidment N.T., Shomer M.H., Behnke E.J., Ackerson L., Fried I., and Engel Jr. J. Comparison of seizure related amino acid release in human epileptic hippocampus versus a chronic, kainate rat model of hippocampal epilepsy. Epilepsy Res. 26 (1996) 245-254
59. Yen W., Williamson J., Bertram E.H., and Kapur J. A comparison of three NMDA receptor antagonists in the treatment of prolonged status epilepticus. Epilepsy Res. 59 (2004) 43-50
60. Zhang L., Ong W.Y., and Lee T. Induction of P-glycoprotein expression in astrocytes following intracerebroventricular kainate injections. Exp. Brain Res. 126 (1999) 509-516
61. Zhu H.J., and Liu G.Q. Glutamate up-regulates P-glycoprotein expression in rat brain microvessel endothelial cells by an NMDA receptor-mediated mechanism. Life Sci. 75 (2004) 1313-1322