Altered GABAA receptor expression during epileptogenesis

Neuroscience Letters

Volumn 497, Issue 3, 2011, Pages 218-222

  González, Marco I ^a   Brooks Kayal, Amy ^a,b  

^a Children's Hospital Colorado   (United States)

^b CHILDREN S HOSPITAL COLORADO   (United States)

Author keywords

Epilepsy; Epileptogenesis; GABA receptors; Receptor expression; Transcriptional regulation

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR ALPHA1; 4 AMINOBUTYRIC ACID A RECEPTOR ALPHA2; 4 AMINOBUTYRIC ACID A RECEPTOR BETA1; 4 AMINOBUTYRIC ACID A RECEPTOR BETA2; 4 AMINOBUTYRIC ACID A RECEPTOR BETA3; 4 AMINOBUTYRIC ACID A RECEPTOR GAMMA1; BENZODIAZEPINE; BRAIN DERIVED NEUROTROPHIC FACTOR; CLONAZEPAM; DNA; JANUS KINASE; MESSENGER RNA; STAT PROTEIN; NERVE PROTEIN;

DENTATE GYRUS; EPILEPSY; EPILEPTIC STATE; EPILEPTOGENESIS; GENE CONTROL; HUMAN; IMMUNOREACTIVITY; LATENT PERIOD; NERVE CELL EXCITABILITY; NEUROTRANSMISSION; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; TEMPORAL LOBE EPILEPSY; TRANSCRIPTION REGULATION; ANIMAL; BRAIN; GENE EXPRESSION REGULATION; METABOLISM; TISSUE DISTRIBUTION;

ANIMALS; BRAIN; EPILEPSY; GENE EXPRESSION REGULATION; HUMANS; NERVE TISSUE PROTEINS; RECEPTORS, GABA-A; TISSUE DISTRIBUTION;

EID: 79957813883     PISSN: 03043940     EISSN: 18727972     Source Type: Journal    
DOI: 10.1016/j.neulet.2011.02.052     Document Type: Review

References (59)

1. Aaronson D.S., Horvath C.M. A road map for those who don't know JAK-STAT. Science 2002, 296:1653-1655.
2. Banerjee P.N., Filippi D., Allen Hauser W. The descriptive epidemiology of epilepsy-a review. Epilepsy Res. 2009, 85:31-45.
3. Beck H., Yaari Y. Plasticity of intrinsic neuronal properties in CNS disorders. Nat. Rev. Neurosci. 2008, 9:357-369.
4. Blair R.E., Sombati S., Lawrence D.C., McCay B.D., DeLorenzo R.J. Epileptogenesis causes acute and chronic increases in GABA(A) receptor endocytosis that contributes to the induction and maintenance of seizures in the hippocampal culture model of acquired epilepsy. J. Pharmacol. Exp. Ther. 2004, 310:871-880.
5. Bouilleret V., Loup F., Kiener T., Marescaux C., Fritschy J.-M. Early loss of interneurons and delayed subunit-specific changes in GABA(A)-receptor expression in a mouse model of mesial temporal epilepsy. Hippocampus 2000, 10:305-324.
6. Boulland J.L., Ferhat L., Tallak Solbu T., Ferrand N., Chaudhry F.A., Storm-Mathisen J., Esclapez M. Changes in vesicular transporters for gamma-aminobutyric acid and glutamate reveal vulnerability and reorganization of hippocampal neurons following pilocarpine-induced seizures. J. Comp. Neurol. 2007, 503:466-485.
7. Brooks-Kayal A.R., Raol Y.H., Russek S.J. Alteration of epileptogenesis genes. Neurotherapeutics 2009, 6:312-318.
8. Brooks-Kayal A.R., Shumate M.D., Jin H., Rikhter T.Y., Coulter D.A. Selective changes in single cell GABA(A) receptor subunit expression and function in temporal lobe epilepsy. Nat. Med. 1998, 4:1166-1172.
9. Bumanglag A.V., Sloviter R.S. Minimal latency to hippocampal epileptogenesis and clinical epilepsy after perforant pathway stimulation-induced status epilepticus in awake rats. J. Comp. Neurol. 2008, 510:561-580.
10. Chen J.W., Naylor D.E., Wasterlain C.G. Advances in the pathophysiology of status epilepticus. Acta Neurol. Scand. Suppl. 2007, 186:7-15.
11. Choi J.S., Kim S.Y., Park H.J., Cha J.H., Choi Y.S., Kang J.E., Chung J.W., Chun M.H., Lee M.Y. Upregulation of gp130 and differential activation of STAT and p42/44 MAPK in the rat hippocampus following kainic acid-induced seizures. Brain Res. Mol. Brain Res. 2003, 119:10-18.
12. Cossart R., Bernard C., Ben-Ari Y. Multiple facets of GABAergic neurons and synapses: multiple fates of GABA signalling in epilepsies. Trends Neurosci. 2005, 28:108-115.
13. Cossart R., Dinocourt C., Hirsch J.C., Merchan-Perez A., De Felipe J., Ben-Ari Y., Esclapez M., Bernard C. Dendritic but not somatic GABAergic inhibition is decreased in experimental epilepsy. Nat. Neurosci. 2001, 4:52-62.
14. Darnell J.E., Kerr I.M., Stark G.R. Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science 1994, 264:1415-1421.
15. Dichter M.A. Emerging insights into mechanisms of epilepsy: implications for new antiepileptic drug development. Epilepsia 1994, 35(Suppl. 4):S51-S57.
16. El-Hassar L., Milh M., Wendling F., Ferrand N., Esclapez M., Bernard C. Cell domain-dependent changes in the glutamatergic and GABAergic drives during epileptogenesis in the rat CA1 region. J. Physiol. 2007, 578:193-211.
17. Feng H.J., Mathews G.C., Kao C., Macdonald R.L. Alterations of GABA(A)-receptor function and allosteric modulation during development of status epilepticus. J. Neurophysiol. 2008, 99:1285-1293.
18. Fritschy K.T., Bouilleret J.-M., Loup V.F. GABAergic neurons and GABA(A)-receptors in temporal lobe epilepsy. Neurochem. Int. 1999, 34:435-445.
19. Fritschy J.M. Epilepsy, E/I balance and GABA(A) receptor plasticity. Front. Mol. Neurosci. 2008, 1:5.
20. Gibbs J., Shumate M., Coulter D. Differential epilepsy-associated alterations in postsynaptic GABAA receptor function in dentate granule and CA1 neurons. J. Neurophysiol. 1997, 77:1924-1938.
21. Goodkin H.P., Joshi S., Mtchedlishvili Z., Brar J., Kapur J. Subunit-specific trafficking of GABA(A) receptors during status epilepticus. J. Neurosci. 2008, 28:2527-2538.
22. Goodkin H.P., Yeh J.L., Kapur J. Status epilepticus increases the intracellular accumulation of GABA(A) receptors. J. Neurosci. 2005, 25:5511-5520.
23. Hauser W.A., Kurland L.T. The epidemiology of epilepsy in Rochester, Minnesota, 1935 through 1967. Epilepsia 1975, 16:1-66.
24. Ihle J.N. STATs: signal transducers and activators of transcription. Cell 1996, 84:331-334.
25. Isokawa M. Decrement of GABAA receptor-mediated inhibitory postsynaptic currents in dentate granule cells in epileptic hippocampus. J. Neurophysiol. 1996, 75:1901-1908.
26. Jacob T.C., Moss S.J., Jurd R. GABA(A) receptor trafficking and its role in the dynamic modulation of neuronal inhibition. Nat. Rev. Neurosci. 2008, 9:331-343.
27. Jung S., Jones T.D., Lugo J.N., Sheerin A.H., Miller J.W., D'Ambrosio R., Anderson A.E., Poolos N.P. Progressive dendritic HCN channelopathy during epileptogenesis in the rat pilocarpine model of epilepsy. J. Neurosci. 2007, 27:13012-13021.
28. Kapur J., Macdonald R.L. Rapid seizure-induced reduction of benzodiazepine and Zn2+ sensitivity of hippocampal dentate graule cell GABAA receptors. J. Neurosci. 1997, 17:7532-7540.
29. Kobayashi M., Buckmaster P.S. Reduced inhibition of dentate granule cells in a model of temporal lobe epilepsy. J. Neurosci. 2003, 23:2440-2452.
30. Leroy C., Poisbeau P., Keller A.F., Nehlig A. Pharmacological plasticity of GABA(A) receptors at dentate gyrus synapses in a rat model of temporal lobe epilepsy. J. Physiol. 2004, 557:473-487.
31. Loup F., Wieser H.G., Yonekawa Y., Aguzzi A., Fritschy J.M. Selective Alterations in GABA(A) receptor subtypes in human temporal lobe epilepsy. J. Neurosci. 2000, 20:5401-5419.
32. Lowenstein D.H., Alldredge B.K. Status epilepticus. N. Engl. J. Med. 1998, 338:970-976.
33. Lund I.V., Hu Y., Raol Y.H., Benham R.S., Faris R., Russek S.J., Brooks-Kayal A.R. BDNF selectively regulates GABAA receptor transcription by activation of the JAK/STAT pathway. Sci. Signal. 2008, 1:ra9.
34. McNamara J.O., Huang Y.Z., Leonard A.S. Molecular signaling mechanisms underlying epileptogenesis. Sci. STKE 2006, 2006:re12.
35. Naylor D.E., Liu H., Wasterlain C.G. Trafficking of GABA(A) receptors, loss of inhibition, and a mechanism for pharmacoresistance in status epilepticus. J. Neurosci. 2005, 25:7724-7733.
36. O'Donovan K.J, Tourtellotte W.G., Millbrandt J., Baraban J.M. The EGR family of transcription-regulatory factors: progress at the interface of molecular and systems neuroscience. Trends Neurosci. 1999, 22:167-173.
37. Peng Z., Huang C.S., Stell B.M., Mody I., Houser C.R. Altered expression of the delta subunit of the GABAA receptor in a mouse model of temporal lobe epilepsy. J. Neurosci. 2004, 24:8629-8639.
38. Perlin J.B., Gerwin C.M., Panchision D.M., Vick R.S., Jakoi E.R., DeLorenzo R.J. Kindling produces long-lasting and selective changes in gene expression of hippocampal neurons. Proc. Natl. Acad. Sci. U.S.A. 1993, 90:1741-1745.
39. Pirker S.C., Czech S., Baumgartner T., Pockberger C., Maier H., Hauer H., Sieghart B., Furtinger W., Sperk S.G. Increased expression of GABA(A) receptor beta-subunits in the hippocampus of patients with temporal lobe epilepsy. J. Neuropathol. Exp. Neurol. 2003, 62:820-834.
40. Pitkanen A., Immonen R.J., Grohn O.H., Kharatishvili I. From traumatic brain injury to posttraumatic epilepsy: what animal models tell us about the process and treatment options. Epilepsia 2009, 50(Suppl. 2):21-29.
41. Planas A.M., Soriano M.A., Berruezo M., Justicia C., Estrada A., Pitarch S., Ferrer I. Induction of Stat3, a signal transducer and transcription factor, in reactive microglia following transient focal cerebral ischaemia. Eur. J. Neurosci. 1996, 8:2612-2618.
42. Rakhade S.N., Jensen F.E. Epileptogenesis in the immature brain: emerging mechanisms. Nat. Rev. Neurol. 2009, 5:380-391.
43. Raol Y.H., Lund I.V., Bandyopadhyay S., Zhang G., Roberts D.S., Wolfe J.H., Russek S.J., Brooks-Kayal A.R. 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. 2006, 26:11342-11346.
44. Roberts D.S., Hu Y., Lund I.V., Brooks-Kayal A.R., Russek S.J. Brain-derived neurotrophic factor (BDNF)-induced synthesis of early growth response factor 3 (Egr3) controls the levels of type A GABA receptor alpha 4 subunits in hippocampal neurons. J. Biol. Chem. 2006, 281:29431-29435.
45. Roberts D.S., Raol Y.H., Bandyopadhyay S., Lund I.V., Budreck E.C., Passini M.A., Wolfe J.H., Brooks-Kayal A.R., Russek S.J. Egr3 stimulation of GABRA4 promoter activity as a mechanism for seizure-induced up-regulation of GABA(A) receptor alpha4 subunit expression. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:11894-11899.
46. Sanabria E.R., Su H., Yaari Y. Initiation of network bursts by Ca2+-dependent intrinsic bursting in the rat pilocarpine model of temporal lobe epilepsy. J. Physiol. 2001, 532:205-216.
47. Scorza F.A., Arida R.M., Naffah-Mazzacoratti Mda G., Scerni D.A., Calderazzo L., Cavalheiro E.A. The pilocarpine model of epilepsy: what have we learned?. An. Acad. Bras. Cienc. 2009, 81:345-365.
48. Shumate M., Lin D., Gibbs J., Holloway K., Coulter D. GABAA receptor function in epileptic human dentate granule cells: comparison to epileptic and control rat. Epilepsy Res. 1998, 32:114-128.
49. Sloviter R.S. Hippocampal epileptogenesis in animal models of mesial temporal lobe epilepsy with hippocampal sclerosis: the importance of the "latent period" and other concepts. Epilepsia 2008, 49(Suppl. 9):85-92.
50. Staley K.J. Role of the depolarizing GABA response in epilepsy. Adv. Exp. Med. Biol. 2004, 548:104-109.
51. Suzuki S., Tanaka K., Nogawa S., Dembo T., Kosakai A., Fukuuchi Y. Phosphorylation of signal transducer and activator of transcription-3 (Stat3) after focal cerebral ischemia in rats. Exp. Neurol. 2001, 170:63-71.
52. Terunuma M., Xu J., Vithlani M., Sieghart W., Kittler J., Pangalos M., Haydon P.G., Coulter D.A., Moss S.J. Deficits in phosphorylation of GABA(A) receptors by intimately associated protein kinase C activity underlie compromised synaptic inhibition during status epilepticus. J. Neurosci. 2008, 28:376-384.
53. Thind K.K., Yamawaki R., Phanwar I., Zhang G., Wen X., Buckmaster P.S. Initial loss but later excess of GABAergic synapses with dentate granule cells in a rat model of temporal lobe epilepsy. J. Comp. Neurol. 2010, 518:647-667.
54. Wallace R.H., Marini C., Petrou S., Harkin L.A., Bowser D.N., Panchal R.G., Williams D.A., Sutherland G.R., Mulley J.C., Scheffer I.E., Berkovic S.F. Mutant GABA(A) receptor gamma2-subunit in childhood absence epilepsy and febrile seizures. Nat. Genet. 2001, 28:49-52.
55. Williams P.A., White A.M., Clark S., Ferraro D.J., Swiercz W., Staley K.J., Dudek F.E. Development of spontaneous recurrent seizures after kainate-induced status epilepticus. J. Neurosci. 2009, 29:2103-2112.
56. Zhang G., Raol Y.H., Hsu F.C., Coulter D.A., Brooks-Kayal A.R. Effects of status epilepticus on hippocampal GABAA receptors are age-dependent. Neuroscience 2004, 125:299-303.
57. Zhang N., Wei W., Mody I., Houser C.R. 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. 2007, 27:7520-7531.
58. Zhong Z., Wen Z., Darnell J.E. STAT3 and STAT4: members of the family of signal transducers and activators of transcription. Proc. Natl. Acad. Sci. U.S.A. 1994, 91:4806-4810.
59. Zhong Z., Wen Z., Darnell J.E. STAT3: a STAT family member activated by tyrosine phosphorylation in response to epidermal growth factor and interleukin-6. Science 1994, 264:95-98.