Changes in the sensitivity of GABAA current rundown to drug treatments in a model of temporal lobe epilepsy

Frontiers in Cellular Neuroscience

Volumn , Issue JUNE, 2013, Pages

  Cifelli, Pierangelo ^a,b   Palma, Eleonora ^c,d   Roseti, Cristina ^c   Verlengia, Gianluca ^a   Simonato, Michele ^a  

^a UNIVERSITY OF FERRARA   (Italy)

^b RiMED Foundation   (Italy)

^c IRCCS SAN RAFFAELE PISANA   (Italy)

^d SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

BDNF; GABA; Hippocampus; Levetiracetam; Neocortex; Pilocarpine

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; BRAIN DERIVED NEUROTROPHIC FACTOR; ETIRACETAM; PILOCARPINE;

AMINO ACID TRANSPORT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; DISEASE COURSE; DRUG EFFECT; DRUG SENSITIVITY; GABA CURRENT; HIPPOCAMPUS; MALE; MESIAL TEMPORAL LOBE EPILEPSY; NONHUMAN; RAT; RECEPTOR SENSITIVITY; SEIZURE; SIGNAL TRANSDUCTION; TREATMENT OUTCOME;

EID: 84879715037     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2013.00108     Document Type: Article

References (35)

1. Brooks-Kayal, A.R., Shumate, M.D., Jin, H., Rikhter, T.Y., Coulter, D.A. (1998). Selective changes in single cell GABA(A) receptor subunit expression and function in temporal lobe epilepsy. Nat Med 4, 1166-1172.
2. Brooks-Kayal, A.R., Russek, S.J. (2012). Regulation of GABAA receptor gene expression and epilepsy, in Jasper's Basic Mechanisms of the Epilepsies, ed. J.L. Noebels, M. Avoli, M.A. Rogawski, R.W. Olsen and A.V. Delgado-Escueta. (Oxford University Press).
3. Custer, K.L., Austin, N.S., Sullivan, J.M., Bajjalieh, S.M. (2006). Synaptic vesicle protein 2 enhances release probability at quiescent synapses. J Neurosci 26, 1303-1313.
4. Glauser, T.A., Ayala, R., Elterman, R.D., Mitchel, W.G., Van Orman, C.B., Gauer, L.J., Lu, Z. (2006). Double-blind placebo-controlled trial of adjunctive levetiracetam in pediatric partial seizures. Neurology 66, 1654-1660.
5. He, X.P., Kotloski, R., Nef, S., Luikart, B.W., Parada, L.F., McNamara, J.O. (2004). Conditional deletion of TrkB but not BDNF prevents epileptogenesis in the kindling model. Neuron 43, 31-42.
6. Lagrange, A.H., Botzolakis, E.J., Macdonald, R.L. (2007) Enhanced macroscopic desensitization shapes the response of alpha4 subtype-containing GABAA receptors to synaptic and extrasynaptic GABA. J Physiol 578, 655-676.
7. Lee, C.H., Lee, C.Y., Tsai, T.S., Liou, H.H. (2008). PKA-mediated phosphorylation is a novel mechanism for levetiracetam, an antiepileptic drug, activating ROMK1 channels. Biochem Pharmacol 76, 225-235.
8. Lewis, D., Ashwal, S., Hershey, A., Hirtz, D., Yonker, M., Silberstein, S. (2004). Practice parameters: pharmacological treatment of migraine headache in children and adolescent: report of the American Academy of Neurology Quality Standards Subcommitte and the Practice Committee of the child Neurology Society. Neurology 63, 2215-2224.
9. Lynch, B.A., Lambeng, N., Nocka, K., Kensel-Hammes, P., Bajjalieh, S.M., Matagne, A., Fuks, B. (2004). The synaptic vesicle protein SV2A is the binding site for the antiepileptic drug levetiracetam. Proc Natl Acad Sci U S A 101, 9861-9866.
10. Mazzuferi, M., Palma, E., Martinello, K., Maiolino, F., Roseti, C., Fucile, S., Fabene, P.F., Schio, F., Pellitteri, M., Sperk, G., Miledi, R., Eusebi, F., Simonato, M. (2010). Enhancement of GABA(A)-current run-down in the hippocampus occurs at the first spontaneous seizure in a model of temporal lobe epilepsy. Proc Natl Acad Sci U S A 107, 3180-3185.
11. Miledi, R., Palma, E., Eusebi, F. (2006). Microtransplantation of neurotransmitter receptors from cells to Xenopus oocyte membranes: new procedure for ion channel studies. Methods Mol Biol 322, 347-355.
12. Nishimura, T., Schwarzer, C., Gasser, E., Kato, N., Vezzani, A., Sperk, G. (2005). Altered expression of GABA(A) and GABA(B) receptor subunit mRNAs in the hippocampus after kindling and electrically induced status epilepticus. Neuroscience 134, 691-704.
13. Palma, E., Ragozzino, A., Di Angelantonio, S., Spinelli, G., Trettel, F., Martinez-Torres, A., Torchia, G., Arcella, A., Di Gennaro, G., Quarato, P.P., Esposito, V., Cantore, G., Miledi, R., Eusebi, F. (2004). Phosphatase inhibitors remove the run-down of gamma-aminobutyric acid type A receptors in the human epileptic brain. Proc Natl Acad Sci USA 101, 10183-10188.
14. Palma, E., Spinelli, G., Torchia, G., Martinez-Torres, A., Ragozzino, D., Miledi, R., Eusebi, F. (2005a). Abnormal GABAA receptors from the human epileptic hippocampal subiculum microtransplanted to Xenopus oocytes. Proc Natl Acad Sci USA 102, 2514-2518.
15. Palma, E., Torchia, G., Limatola, C., Trettel, F., Arcella, A., Cantore, G., Di Gennaro, G., Manfredi, M., Esposito, V., Quarato, P.P., Miledi, R., Eusebi, F. (2005b). BDNF modulates GABAA receptors microtransplanted from the human epileptic brain to Xenopus oocytes. Proc Natl Acad Sci USA 102, 1667-1672.
16. Palma, E., Ragozzino, D., Di Angelantonio, S., Mascia, A., Maiolino, F., Manfredi, M., Manfredi, M., Cantore, G., Esposito, V., Di Gennaro, G., Quarato, P., Miledi, R., Eusebi, F. (2007a). The antiepileptic drug levetiracetam stabilizes the human epileptic GABAA receptors upon repetitive activation. Epilepsia 48, 1842-1849.
17. Palma, E., Roseti, C., Maiolino, F., Fucile, S., Martinello, K., Mazzuferi, M., Aronica, E., Manfredi, M., Esposito, V., Cantore, G., Miledi, R., Simonato, M., Eusebi, F. (2007b). GABAA-current rundown of temporal lobe epilepsy is associated with repetitive activation of GABAA"phasic" receptors Proc Natl Acad Sci USA 104, 20944-20948.
18. Paradiso, B., Marconi, P., Zucchini, S., Berto, E., Binaschi, A., Bozac, A., Buzzi, A., Mazzuferi, M., Magri, E., Navarro Mora, G., Rodi, D., Su, T., Volpi, I., Zanetti, L., Marzola, A., Manservigi, R., Fabene, P.F., Simonato, M. (2009) Localized delivery of fibroblast growth factor-2 and brain-derived neurotrophic factor reduces spontaneous seizures in an epilepsy model. Proc Natl Acad Sci U S A 106, 7191-7196.
19. Paradiso, B., Zucchini, S., Su, T., Bovolenta, R., Berto, E., Marconi, P., Marzola, A., Navarro Mora, G., Fabene, P.F., Simonato, M. (2011). Localized overexpression of FGF-2 and BDNF in hippocampus reduces mossy fiber sprouting and spontaneous seizures up to 4 weeks after pilocarpine-induced status epilepticus. Epilepsia 52, 572-578.
20. Peng, Z., Houser, C.R. (2005). Temporal patterns of fos expression in the dentate gyrus after spontaneous seizures in a mouse model of temporal lobe epilepsy. J Neurosci 25, 7210-7220.
21. Pitkänen, A., Lukasiuk, K. (2011). Mechanisms of epileptogenesis and potential treatment targets. Lancet Neurol 10, 173-186.
22. Pitkänen, A., Sutula, T.P. (2002). Is epilepsy a progressive disorder? Prospects for new therapeutic approaches in temporal-lobe epilepsy. Lancet Neurol 1, 173-181.
23. Poulter, M.O., Brown, L.A., Tynan, S., Willick, G., William, R., McIntyre, D.C. (1999). Differential expression of alpha1, alpha2, alpha3 and alpha5 GABAA receptor subunits in seizure-prone and seizure-resistant rat model of temporal lobe epilepsy. J Neurosci 19, 4654-4661.
24. Racine, R.J. (1972). Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol 32, 281-294.
25. Ragozzino, D., Palma, E., Di Angelantonio, S., Amici, M., Mascia, A., Arcella, A., Giangaspero, F., Cantore, G., Di Gennaro, G., Manfredi, M., Esposito, V., Quarato, P.P., Miledi, R., and Eusebi, F. (2005). Run-down of GABAA-receptors is a dysfunction associated with human temporal lobe epilepsy lacking temporal cortex lesions. Proc. Natl. Acad. Sci. 102, 15219-15223
26. Raol, Y.H., Lund, I.V., Bandyopadhyay, S., Zhang, G., Roberts, D.S., Wolfe, J.H., Russek, S.J., Brooks-Kayal, A.R. (2006). Enhancing GABA(A) receptor alpha 1 subunit levels in hippocampal dentate gyrus inhibits epilepsy development in an animal model of temporal lobe epilepsy. J Neurosci 26:11342-11346.
27. Schimdt, D., Löscher, W. (2005). Drug resistance in epilepsy: putative neurobiologic and clinical mechanisms. Epilepsia 46, 858-877
28. Schwarzer, C., Tsunashima, K., Wanzenböck, C., Fuchs, K., Sieghart, W., Sperk, G. (1997). GABA(A) receptor subunits in the rat hippocampus II: Altered distribution in kainic acidinduced temporal lobe epilepsy. Neuroscience 80, 1001-1017.
29. Simonato, M., Tongiorgi, E., Kokaia, M. (2006). Angels and demons: neurotrophic factors and epilepsy. Trends Pharmacol Sci 27, 631-638.
30. Sperk, G. (2007) Changes in GABAA receptors in status epilepticus. Epilepsia 48 (Suppl. 8), 11-13.
31. Sperk, G., Furtinger, S., Schwarzer, C., Pirker, S. (2004). GABA and its receptors in epilepsy. Adv Exp Med Biol 103, 548-592.
32. Williams, P.A., White, A.M., Clark, S., Ferraro, D.J., Swiercz, W., Staley, K.J., Dudek, F.E. (2009). Development of spontaneous recurrent seizures after kainate-induced status epilepticus. J Neurosci 29, 2103-2112.
33. Yang, X.F., Weisenfeld, A., Rothman, S.M. (2007). Prolonged exposure to levetiracetam reveals a presynaptic effect on neurotransmission. Epilepsia 48, 1861-1869.
34. Zhang, G., Raol, Y.H., Hsu, F.C., Coulter, D.A., Brooks-Kayal, A.R. (2004) Effects of status epilepticus on hippocampal GABAA receptors are age-dependent. Neuroscience 125, 299-303.
35. Zhang, N., Wei, W., Mody, I., Houser, C.R. (2007). Altered localization of GABA(A) receptor subunits on dentate granule cell dendrites influences tonic and phasic inhibition in a mouse model of epilepsy. J Neurosci 27, 7520-7531.