Coactivation of GABA receptors inhibits the JNK3 apoptotic pathway via disassembly of GluR6-PSD-95-MLK3 signaling module in KA-induced seizure

Epilepsia

Volumn 51, Issue 3, 2010, Pages 391-403

  Li, Chong ^a   Xu, Bo ^a   Wang, Wei Wei ^a   Yu, Xiu Ju ^a   Zhu, Jie ^a   Yu, Hong Min ^a   Han, Dong ^a   Pei, Dong Sheng ^a   Zhang, Guang Yi ^a  

^a XUZHOU MEDICAL UNIVERSITY   (China)

Author keywords

Baclofen; GABA; JNK pathway; Kainic acid; Muscimol; Neuroprotection

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; BACLOFEN; CYTOCHROME C; FAS LIGAND; GLUTAMATE RECEPTOR 6; GLUTAMIC ACID; KAINIC ACID; MITOGEN ACTIVATED PROTEIN KINASE KINASE 3; MIXED LINEAGE KINASE 3; MUSCIMOL; POSTSYNAPTIC DENSITY PROTEIN 95; PROTEIN BAX; STRESS ACTIVATED PROTEIN KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVATION; HISTOPATHOLOGY; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MALE; MOLECULAR MECHANICS; NERVE CELL NECROSIS; NERVE INJURY; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PYRAMIDAL NERVE CELL; RAT; SEIZURE; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; BACLOFEN; DISEASE MODELS, ANIMAL; GABA AGONISTS; HUMANS; IMMUNOHISTOCHEMISTRY; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; KAINIC ACID; MALE; MAP KINASE KINASE KINASES; MEMBRANE PROTEINS; MITOGEN-ACTIVATED PROTEIN KINASE 10; MUSCIMOL; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA; RECEPTORS, GABA-A; RECEPTORS, KAINIC ACID; SEIZURES;

EID: 77749270495     PISSN: 00139580     EISSN: 15281167     Source Type: Journal    
DOI: 10.1111/j.1528-1167.2009.02270.x     Document Type: Article

References (59)

1. Attwell D, Barbour B, Szatkowski M. (1993) Nonvesicular release of neurotransmitter. Neuron 11:401-407.
2. Balasubramanian S, Teissere JA, Raju DV, Hall RA. (2004) Hetero-oligomerization between GABAA and GABAB receptors regulates GABAB receptor trafficking. J Biol Chem 279:18840-18850.
3. Barila B, Cupello A, Robello M. (1999) GABA(B) receptor activation protects GABA(A) receptor from cyclic AMP-dependent down-regulation in rat cerebellar granule cells. Neuroscience 93:1077-1082.
4. Borsello T, Forloni G. (2007) JNK signalling: a possible target to prevent neurodegeneration. Curr Pharm Des 13:1875-1886.
5. Costa C, Leone G, Saulle E, Pisani F, Bernardi G, Calabresi P. (2004) Coactivation of GABA(A) and GABA(B) receptor results in neuroprotection during in vitro ischemia. Stroke 35:596-600.
6. Davis RJ. (2000) Signal transduction by the JNK group of MAP kinases. Cell 103:239-252.
7. Dingledine R, Borges K, Bowie D, Traynelis SF. (1999) The glutamate receptor ion channels. Pharmacol Rev 51:7-61.
8. Erdo SL, Michler A. (1990) GABA does not protect cerebro-cortical cultures against excitotoxic cell death. Eur J Pharmacol 182: 203-206.
9. Faris M, Latinis KM, Kempiak SJ, Koretzky GA, Nel A. (1998) Stress-induced Fas ligand expression in T cells is mediated through a MEK kinase 1-regulated response element in the Fas ligand promoter. Mol Cell Biol 18:5414-5424.
10. Fujiyama F, Fritschy JM, Stephenson FA, Bolam JP. (2000) Synaptic localization of GABA(A) receptor subunits in the striatum of the rat. J Comp Neurol 416:158-172.
11. Goodkin HP, Sun C, Yeh JL, Mangan PS, Kapur J. (2007) GABA(A) receptor internalization during seizures. Epilepsia 48(Suppl. 5): 109-113.
12. Henshall DC, Araki T, Schindler CK, Lan JQ, Tiekoter KL, Taki W, Simon RP. (2002) Activation of Bcl-2-associated death protein and counter-response of Akt within cell populations during seizureinduced neuronal death. J Neurosci 22:8458-8465.
13. Jackson-Friedman C, Lyden PD, Nunez S, Jin A, Zweifler R. (1997) High dose baclofen is neuroprotective but also causes intracerebral hemorrhage: a quantal bioassay study using the intraluminal suture occlusion method. Exp Neurol 147:346-352.
14. Kaminska B, Filipkowski RK, Biedermann IW, Konopka D, Nowicka D, Hetman M, Dabrowski M, Gorecki DC, Lukasiuk K, Szklarczyk AW, Kaczmarek L. (1997) Kainate-evoked modulation of gene expression in rat brain. Acta Biochim Pol 44:781-789.
15. Kardos J, Elster L, Damgaard I, Krogsgaard-Larsen P, Schousboe A. (1994) Role of GABAB receptors in intracellular Ca2+ homeostasis and possible interaction between GABAA and GABAB receptors in regulation of transmitter release in cerebellar granule neurons. J Neurosci Res 39:646-655.
16. Kardos J. (1999) Recent advances in GABA research. Neurochem Int 34:353-358.
17. Kew JN, Kemp JA. (2005) Ionotropic and metabotropic glutamate receptor structure and pharmacology. Psychopharmacology (Berl) 179: 4-29.
18. Knudson CM, Tung KS, Tourtellotte WG, Brown GA, Korsmeyer SJ. (1995) Bax-deficient mice with lymphoid hyperplasia and male germ cell death. Science 270:96-99.
19. Kulinskii VI, Mikhel'son GV. (2000) Additivity and independence of neuroprotective effects of GABAA and GABAB receptor agonists in complete global cerebral ischemia. Bull Exp Biol Med 130:772-774.
20. Kuwana T, Mackey MR, Perkins G, Ellisman MH, Latterich M, Schneiter R, Green DR, Newmeyer DD. (2002) Bid, Bax, and lipids cooperate to form supramolecular openings in the outer mitochondrial membrane. Cell 111:331-342.
21. Lilliu V, Perrone-Capano C, Pernas-Alonso R, Diaz Trelles R, Luca Colucci d'Amato G, Zuddas A, di Porzio U. (2002) Ontogeny of kainate receptor gene expression in the developing rat midbrain and striatum. Brain Res Mol Brain Res 104:1-10.
22. Lindsten T, Ross AJ, King A, Zong WX, Rathmell JC, Shiels HA, Ulrich E, Waymire KG, Mahar P, Frauwirth K, Chen Y, Wei M, Eng VM, Adelman DM, Simon MC, Ma A, Golden JA, Evan G, Korsmeyer SJ, MacGregor GR, Thompson CB. (2000) The combined functions of proapoptotic Bcl-2 family members bak and bax are essential for normal development of multiple tissues. Mol Cell 6:1389-1399.
23. Liu X, Kim CN, Yang J, Jemmerson R, Wang X. (1996) Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86:147-157.
24. Liu XM, Pei DS, Guan QH, Sun YF, Wang XT, Zhang QX, Zhang GY. (2006) Neuroprotection of Tat-GluR6-9c against neuronal death induced by kainate in rat hippocampus via nuclear and non-nuclear pathways. J Biol Chem 281:17432-17445.
25. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265-275.
26. Luscher C, Jan LY, Stoffel M, Malenka RC, Nicoll RA. (1997) G protein-coupled inwardly rectifying K+ channels (GIRKs) mediate postsynaptic but not presynaptic transmitter actions in hippocampal neurons. Neuron 19:687-695.
27. Lyden PD. (1997) GABA and neuroprotection. Int Rev Neurobiol 40:233-258.
28. Mayer ML, Armstrong N. (2004) Structure and function of glutamate receptor ion channels. Annu Rev Physiol 66:161-181.
29. Meldrum BS, Rogawski MA. (2007) Molecular targets for antiepileptic drug development. Neurotherapeutics 4:18-61.
30. Moldavan MG, Irwin RP, Allen CN. (2006) Presynaptic GABA(B) receptors regulate retinohypothalamic tract synaptic transmission by inhibiting voltage-gated Ca2+ channels. J Neurophysiol 95:3727-3741.
31. Muir JK, Lobner D, Monyer H, Choi DW. (1996) GABAA receptor activation attenuates excitotoxicity but exacerbates oxygen-glucose deprivation-induced neuronal injury in vitro. J Cereb Blood Flow Metab 16:1211-1218.
32. Mulle C, Sailer A, Perez-Otano I, Dickinson-Anson H, Castillo PE, Bureau I, Maron C, Gage FH, Mann JR, Bettler B, Heinemann SF. (1998) Altered synaptic physiology and reduced susceptibility to kainateinduced seizures in GluR6-deficient mice. Nature 392: 601-605.
33. Nomura M, Shimizu S, Sugiyama T, Narita M, Ito T,Matsuda H, Tsujimoto Y. (2003) 14-3-3 Interacts directly with and negatively regulates proapoptotic Bax. J Biol Chem 278:2058-2065.
34. Obrietan K, van den Pol AN. (1998) GABAB receptor-mediated inhibition of GABAA receptor calcium elevations in developing hypothalamic neurons. J Neurophysiol 79:1360-1370.
35. Ohkuma S, Chen SH, Katsura M, Chen DZ, Kuriyama K. (1994) Muscimol prevents neuronal injury induced by NMDA. Jpn J Pharmacol 64:125-128.
36. Pan J, Zhang QG, Zhang GY (2005) The neuroprotective effects of K252a through inhibiting MLK3/MKK7/JNK3 signaling pathway on ischemic brain injury in rat hippocampal CA1 region. Neuroscience 131:147-159.
37. Pei DS, Guan QH, Sun YF, Zhang QX, Xu TL, Zhang GY. (2005) Neuroprotective effects of GluR6 antisense oligodeoxynucleotides on transient brain ischemia/reperfusion-induced neuronal death in rat hippocampal CA1 region. J Neurosci Res 82:642-649.
38. Pei DS, Wang XT, Liu Y, Sun YF, Guan QH, Wang W, Yan JZ, Zong YY, Xu TL, Zhang GY. (2006) Neuroprotection against ischaemic brain injury by a GluR6-9c peptide containing the TAT protein transduction sequence. Brain 129:465-479.
39. Peng Z, Huang CS, Stell BM, Mody I, Houser CR. (2004) Altered expression of the delta subunit of the GABAA receptor in a mouse model of temporal lobe epilepsy. J Neurosci 24:8629-8639.
40. Porter RH, Eastwood SL, Harrison PJ. (1997) Distribution of kainate receptor subunit mRNAs in human hippocampus, neocortex and cerebellum, and bilateral reduction of hippocampal GluR6 and KA2 transcripts in schizophrenia. Brain Res 751:217-231.
41. Porter BE, Zhang G, Celix J, Hsu FC, Raol YH, Telfeian A, Gallagher PR, Coulter DA, Brooks-Kayal AR. (2005) Heterogeneous GABAA receptor subunit expression in pediatric epilepsy patients. Neurobiol Dis 18:484-491.
42. Racine RJ. (1972) Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol 32:281-294.
43. Raol YH, Zhang G, Lund IV, Porter BE, Maronski MA, Brooks-Kayal AR. (2006) Increased GABA(A)-receptor alpha1-subunit expression in hippocampal dentate gyrus after early-life status epilepticus. Epilepsia 47:1665-1673.
44. Saito M, Korsmeyer SJ, Schlesinger PH. (2000) BAX-dependent transport of cytochrome c reconstituted in pure liposomes. Nat Cell Biol 2:553-555.
45. Savinainen A, Garcia EP, Dorow D, Marshall J, Liu YF. (2001) Kainate receptor activation induces mixed lineage kinase-mediated cellular signaling cascades via post-synaptic density protein 95. J Biol Chem 276:11382-11386.
46. Shibuya I, Kongsamut S, Douglas WW. (1997) Both GABAA and GABAB receptors participate in suppression of [CA2+]i pulsing in toad melanotrophs. Eur J Pharmacol 321:241-246.
47. Shimizu S, Narita M, Tsujimoto Y. (1999) Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC. Nature 399:483-487.
48. Slee EA, Harte MT, Kluck RM, Wolf BB, Casiano CA, Newmeyer DD, Wang HG, Reed JC, Nicholson DW, Alnemri ES, Green DR, Martin SJ. (1999) Ordering the cytochrome c-initiated caspase cascade: hierarchical activation of caspases-2, -3, -6, -7, -8, and -10 in a caspase-9-dependent manner. J Cell Biol 144:281-292.
49. Smith Y, Charara A, Hanson JE, Paquet M, Levey AI. (2000) GABA(B) and group I metabotropic glutamate receptors in the striatopallidal complex in primates. J Anat 196(Pt 4):555-576.
50. Stafstrom CE. (2006) Epilepsy: a review of selected clinical syndromes and advances in basic science. J Cereb Blood Flow Metab 26:983-1004.
51. Tian H, Zhang G, Li H, Zhang Q. (2003) Antioxidant NAC and AMPA/KA receptor antagonist DNQX inhibited JNK3 activation following global ischemia in rat hippocampus. Neurosci Res 46:191-197.
52. Tian H, Zhang QG, Zhu GX, Pei DS, Guan QH, Zhang GY. (2005) Activation of c-Jun NH2-terminal kinase 3 is mediated by the GluR6.PSD-95.MLK3 signaling module following cerebral ischemia in rat hippocampus. Brain Res 1061:57-66.
53. Wang Q, Yu S, Simonyi A, Sun GY, Sun AY. (2005) Kainic acid-mediated excitotoxicity as a model for neurodegeneration. Mol Neurobiol 31:3-16.
54. Wei MC, Zong WX, Cheng EH, Lindsten T, Panoutsakopoulou V, Ross AJ, Roth KA, MacGregor GR, Thompson CB, Korsmeyer SJ. (2001) Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 292:727-730.
55. Whitmarsh AJ, Cavanagh J, Tournier C, Yasuda J, Davis RJ. (1998) A mammalian scaffold complex that selectively mediates MAP kinase activation. Science 281:1671-1674.
56. Wong BR, Rho J, Arron J, Robinson E, Orlinick J, Chao M, Kalachikov S, Cayani E, Bartlett FS III, Frankel WN, Lee SY, Choi Y. (1997) TRANCE is a novel ligand of the tumor necrosis factor receptor family that activates c-Jun N-terminal kinase in T cells. J Biol Chem 272:25190-25194.
57. Zagulska-Szymczak S, Filipkowski RK, Kaczmarek L. (2001) Kainateinduced genes in the hippocampus: lessons from expression patterns. Neurochem Int 38:485-501.
58. Zhang F, Li C, Wang R, Han D, Zhang QG, Zhou C, Yu HM, Zhang GY. (2007) Activation of GABA receptors attenuates neuronal apoptosis through inhibiting the tyrosine phosphorylation of NR2A by Src after cerebral ischemia and reperfusion. Neuroscience 150:938-949.
59. Zong WX, Lindsten T, Ross AJ, MacGregor GR, Thompson CB. (2001) BH3-only proteins that bind pro-survival Bcl-2 family members fail to induce apoptosis in the absence of Bax and Bak. Genes Dev 15:1481-1486.