Down-regulation of gephyrin and GABAA receptor subunits during epileptogenesis in the CA1 region of hippocampus

Epilepsia

Volumn 54, Issue 4, 2013, Pages 616-624

  González, Marco I ^a   Cruz Del Angel, Yasmin ^a   Brooks Kayal, Amy ^a,b  

^a Children's Hospital Colorado   (United States)

^b CHILDREN S HOSPITAL COLORADO   (United States)

Author keywords

Epileptogenesis; GABAAR; Gephyrin; Receptor trafficking

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; DIAZEPAM; GEPHYRIN; PILOCARPINE; REAGENT; SCAFFOLD PROTEIN; SCOPOLAMINE METHYL NITRATE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BIOTINYLATION; CELL MEMBRANE; CELL SURFACE; CONTROLLED STUDY; EPILEPTIC STATE; EPILEPTOGENESIS; HIPPOCAMPAL CA1 REGION; IMMUNOPRECIPITATION; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TRANSPORT; RAT; RECEPTOR BINDING; RECEPTOR DOWN REGULATION; WESTERN BLOTTING;

ANIMALS; BIOTINYLATION; BLOTTING, WESTERN; CA1 REGION, HIPPOCAMPAL; CARRIER PROTEINS; CELL MEMBRANE; DOWN-REGULATION; ELECTROPHORESIS, POLYACRYLAMIDE GEL; EPILEPSY; FLUORESCENT ANTIBODY TECHNIQUE; GAMMA-AMINOBUTYRIC ACID; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MALE; MEMBRANE PROTEINS; MICROSCOPY, CONFOCAL; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, CELL SURFACE; RECEPTORS, GABA-A; STATUS EPILEPTICUS; SYNAPTIC TRANSMISSION;

EID: 84875842718     PISSN: 00139580     EISSN: 15281167     Source Type: Journal    
DOI: 10.1111/epi.12063     Document Type: Article

References (51)

1. Brooks-Kayal AR, Shumate MD, Jin H, Rikhter TY, Coulter DA,. (1998) Selective changes in single cell GABA(A) receptor subunit expression and function in temporal lobe epilepsy. Nat Med 4: 1166-1172.
2. Charych EI, Yu W, Miralles CP, Serwanski DR, Li X, Rubio M, De Blas AL,. (2004) The brefeldin A-inhibited GDP/GTP exchange factor 2, a protein involved in vesicular trafficking, interacts with the beta subunits of the GABA receptors. J Neurochem 90: 173-189.
3. Chauviere L, Rafrafi N, Thinus-Blanc C, Bartolomei F, Esclapez M, Bernard C,. (2009) Early deficits in spatial memory and theta rhythm in experimental temporal lobe epilepsy. J Neurosci 29: 5402-5410.
4. Chen ZW, Olsen RW,. (2007) GABAA receptor associated proteins: a key factor regulating GABAA receptor function. J Neurochem 100: 279-294.
5. Chen JW, Naylor DE, Wasterlain CG,. (2007) Advances in the pathophysiology of status epilepticus. Acta Neurol Scand Suppl 186: 7-15.
6. Curia G, Longo D, Biagini G, Jones RS, Avoli M,. (2008) The pilocarpine model of temporal lobe epilepsy. J Neurosci Methods 172: 143-157.
7. El-Hassar L, Esclapez M, Bernard C,. (2007) Hyperexcitability of the CA1 hippocampal region during epileptogenesis. Epilepsia 48 (Suppl. 5): 131-139.
8. Esclapez M, Hirsch JC, Ben-Ari Y, Bernard C,. (1999) Newly formed excitatory pathways provide a substrate for hyperexcitability in experimental temporal lobe epilepsy. J Comp Neurol 408: 449-460.
9. Essrich C, Lorez M, Benson JA, Fritschy JM, Luscher B,. (1998) Postsynaptic clustering of major GABAA receptor subtypes requires the gamma 2 subunit and gephyrin. Nat Neurosci 1: 563-571.
10. Falconer M, Serafetinides E, Corsellis J,. (1964) Etiology and pathogenesis of temporal lobe epilepsy. Arch Neurol 10: 233-248.
11. Fang M, Shen L, Yin H, Pan YM, Wang L, Chen D, Xi ZQ, Xiao Z, Wang XF, Zhou SN,. (2011) Downregulation of gephyrin in temporal lobe epilepsy neurons in humans and a rat model. Synapse 65: 1006-1014.
12. Fritschy JM,. (2008) Epilepsy, E/I balance and GABA(A) receptor plasticity. Front Mol Neurosci 1: 5.
13. Fritschy JM, Harvey RJ, Schwarz G,. (2008) Gephyrin: where do we stand, where do we go? Trends Neurosci 31: 257-264.
14. A receptor function in dentate granule and CA1 neurons. J Neurophysiol 77: 1924-1938.
15. Gonzalez MI, Krizman-Genda E, Robinson MB,. (2007) Caveolin-1 regulates the delivery and endocytosis of the glutamate transporter, excitatory amino acid carrier 1. J Biol Chem 282: 29855-29865.
16. Goodkin HP, Yeh JL, Kapur J,. (2005) Status epilepticus increases the intracellular accumulation of GABAA receptors. J Neurosci 25: 5511-5520.
17. Goodkin HP, Joshi S, Mtchedlishvili Z, Brar J, Kapur J,. (2008) Subunit-specific trafficking of GABA(A) receptors during status epilepticus. J Neurosci 28: 2527-2538.
18. Grosshans DR, Clayton DA, Coultrap SJ, Browning MD,. (2002) Analysis of glutamate receptor surface expression in acute hippocampal slices. Sci STKE 2002: pl8.
19. Herman ST,. (2002) Epilepsy after brain insult: targeting epileptogenesis. Neurology 59: S21-S26.
20. Holman D, Henley JM,. (2007) A novel method for monitoring the cell surface expression of heteromeric protein complexes in dispersed neurons and acute hippocampal slices. J Neurosci Methods 160: 302-308.
21. Houser CR, Esclapez M,. (2003) Downregulation of the alpha5 subunit of the GABA(A) receptor in the pilocarpine model of temporal lobe epilepsy. Hippocampus 13: 633-645.
22. Jacob TC, Bogdanov YD, Magnus C, Saliba RS, Kittler JT, Haydon PG, Moss SJ,. (2005) Gephyrin regulates the cell surface dynamics of synaptic GABAA receptors. J Neurosci 25: 10469-10478.
23. Jacob TC, Moss SJ, Jurd R,. (2008) GABA(A) receptor trafficking and its role in the dynamic modulation of neuronal inhibition. Nat Rev Neurosci 9: 331-343.
24. Kapur J, Macdonald RL,. (1997) Rapid seizure-induced reduction of benzodiazepine and Zn2+ sensitivity of hippocampal dentate granule cell GABAA receptors. J Neurosci 17: 7532-7540.
25. Kneussel M, Loebrich S,. (2007) Trafficking and synaptic anchoring of ionotropic inhibitory neurotransmitter receptors. Biol Cell 99: 297-309.
26. Kneussel M, Brandstatter JH, Laube B, Stahl S, Muller U, Betz H,. (1999) Loss of postsynaptic GABA(A) receptor clustering in gephyrin-deficient mice. J Neurosci 19: 9289-9297.
27. Kneussel M, Haverkamp S, Fuhrmann JC, Wang H, Wassle H, Olsen RW, Betz H,. (2000) The gamma-aminobutyric acid type A receptor (GABAAR)-associated protein GABARAP interacts with gephyrin but is not involved in receptor anchoring at the synapse. Proc Natl Acad Sci U S A 97: 8594-8599.
28. Leidenheimer NJ,. (2008) Regulation of excitation by GABA(A) receptor internalization. Results Probl Cell Differ 44: 1-28.
29. Leroy C, Poisbeau P, Keller AF, Nehlig A,. (2004) Pharmacological plasticity of GABA(A) receptors at dentate gyrus synapses in a rat model of temporal lobe epilepsy. J Physiol 557: 473-487.
30. Li RW, Yu W, Christie S, Miralles CP, Bai J, Loturco JJ, De Blas AL,. (2005) Disruption of postsynaptic GABA receptor clusters leads to decreased GABAergic innervation of pyramidal neurons. J Neurochem 95: 756-770.
31. Löscher W, Brandt C,. (2010) Prevention or modification of epileptogenesis after brain insults: experimental approaches and translational research. Pharmacol Rev 62: 668-700.
32. Lund IV, Hu Y, Raol YH, Benham RS, Faris R, Russek SJ, Brooks-Kayal AR,. (2008) BDNF selectively regulates GABAA receptor transcription by activation of the JAK/STAT pathway. Sci Signal 1: ra9.
33. Luscher B, Keller CA,. (2004) Regulation of GABAA receptor trafficking, channel activity, and functional plasticity of inhibitory synapses. Pharmacol Ther 102: 195-221.
34. Luscher B, Fuchs T, Kilpatrick CL,. (2011) GABAA receptor trafficking-mediated plasticity of inhibitory synapses. Neuron 70: 385-409.
35. Macdonald RL, Olsen RW,. (1994) GABAA receptor channels. Annu Rev Neurosci 17: 569-602.
36. McNamara JO, Huang YZ, Leonard AS,. (2006) Molecular signaling mechanisms underlying epileptogenesis. Sci STKE 2006: re12.
37. Michels G, Moss SJ,. (2007) GABAA receptors: properties and trafficking. Crit Rev Biochem Mol Biol 42: 3-14.
38. Mukherjee J, Kretschmannova K, Gouzer G, Maric HM, Ramsden S, Tretter V, Harvey K, Davies PA, Triller A, Schindelin H, Moss SJ,. (2011) The residence time of GABA(A)Rs at inhibitory synapses is determined by direct binding of the receptor alpha1 subunit to gephyrin. J Neurosci 31: 14677-14687.
39. Naylor DE, Liu H, Wasterlain CG,. (2005) Trafficking of GABA(A) receptors, loss of inhibition, and a mechanism for pharmacoresistance in status epilepticus. J Neurosci 25: 7724-7733.
40. Schwarzer C, Sperk G,. (1995) Hippocampal granule cells express glutamic acid decarboxylase-67 after limbic seizures in the rat. Neuroscience 69: 705-709.
41. Schwarzer C, Tsunashima K, Wanzenbock C, Fuchs K, Sieghart W, Sperk G,. (1997) GABA(A) receptor subunits in the rat hippocampus II: altered distribution in kainic acid-induced temporal lobe epilepsy. Neuroscience 80: 1001-1017.
42. Scorza FA, Arida RM, Naffah-Mazzacoratti Mda G, Scerni DA, Calderazzo L, Cavalheiro EA,. (2009) The pilocarpine model of epilepsy: what have we learned? An Acad Bras Cienc 81: 345-365.
43. Sharma AK, Reams RY, Jordan WH, Miller MA, Thacker HL, Snyder PW,. (2007) Mesial temporal lobe epilepsy: pathogenesis, induced rodent models and lesions. Toxicol Pathol 35: 984-999.
44. Sieghart W, Fuchs K, Tretter V, Ebert V, Jechlinger M, Hoger H, Adamiker D,. (1999) Structure and subunit composition of GABA(A) receptors. Neurochem Int 34: 379-385.
45. Silva AP, Carvalho AP, Carvalho CM, Malva JO,. (2001) Modulation of intracellular calcium changes and glutamate release by neuropeptide Y1 and Y2 receptors in the rat hippocampus: differential effects in CA1, CA3 and dentate gyrus. J Neurochem 79: 286-296.
46. Terunuma M, Xu J, Vithlani M, Sieghart W, Kittler J, Pangalos M, Haydon PG, Coulter DA, Moss SJ,. (2008) Deficits in phosphorylation of GABA(A) receptors by intimately associated protein kinase C activity underlie compromised synaptic inhibition during status epilepticus. J Neurosci 28: 376-384.
47. Thind KK, Yamawaki R, Phanwar I, Zhang G, Wen X, Buckmaster PS,. (2010) Initial loss but later excess of GABAergic synapses with dentate granule cells in a rat model of temporal lobe epilepsy. J Comp Neurol 518: 647-667.
48. Tretter V, Jacob TC, Mukherjee J, Fritschy JM, Pangalos MN, Moss SJ,. (2008) The clustering of GABA(A) receptor subtypes at inhibitory synapses is facilitated via the direct binding of receptor alpha 2 subunits to gephyrin. J Neurosci 28: 1356-1365.
49. Wang H, Bedford FK, Brandon NJ, Moss SJ, Olsen RW,. (1999) GABA(A)-receptor-associated protein links GABA(A) receptors and the cytoskeleton. Nature 397: 69-72.
50. Yu W, Jiang M, Miralles CP, Li RW, Chen G, de Blas AL,. (2007) Gephyrin clustering is required for the stability of GABAergic synapses. Mol Cell Neurosci 36: 484-500.
51. Yu W, Charych EI, Serwanski DR, Li RW, Ali R, Bahr BA, De Blas AL,. (2008) Gephyrin interacts with the glutamate receptor interacting protein 1 isoforms at GABAergic synapses. J Neurochem 105: 2300-2314.