Deficits in phosphorylation of GABAA receptors by intimately associated protein kinase C activity underlie compromised synaptic inhibition during status epilepticus

Journal of Neuroscience

Volumn 28, Issue 2, 2008, Pages 376-384

  Terunuma, Miho ^a   Xu, Jianwei ^b   Vithlani, Mansi ^a,c   Sieghart, Werner ^d   Kittler, Josef ^c   Pangalos, Menelas ^e   Haydon, Philip G ^a   Coulter, Douglas A ^b   Moss, Stephen J ^a,c  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d Neuroscience Discovery ^*  (Austria)

^e PFIZER INC   (United States)

Author keywords

Endocytosis; GABAA receptor; Phosphorylation; Protein kinase C; Status epilepticus; Synaptic inhibition

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; ADAPTOR PROTEIN; CLATHRIN; ISOENZYME; PROTEIN KINASE C; PROTEIN SUBUNIT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE; CELL SURFACE; CONTROLLED STUDY; ENDOCYTOSIS; ENZYME ACTIVITY; EPILEPTIC STATE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SYNAPTIC INHIBITION;

ANIMALS; BIOTINYLATION; DISEASE MODELS, ANIMAL; ENDOCYTOSIS; ENZYME INHIBITORS; HIPPOCAMPUS; IMMUNOPRECIPITATION; INHIBITORY POSTSYNAPTIC POTENTIALS; MALE; MICE; NEURONS; PATCH-CLAMP TECHNIQUES; PHORBOL 12,13-DIBUTYRATE; PHOSPHOPROTEIN PHOSPHATASES; PHOSPHORYLATION; PILOCARPINE; PROTEIN KINASE C; PROTEIN SUBUNITS; RECEPTORS, GABA-A; SERINE; STATUS EPILEPTICUS; TIME FACTORS;

EID: 38349004774     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4346-07.2008     Document Type: Article

References (39)

1. Alldredge BK, Lowenstein DH (1999) Status epilepticus: new concepts. Curr Opin Neurol 12:183-190.
2. Blanchet C, Sollini M, Luscher C (2003) Two distinct forms of desensitization of G-protein coupled inwardly rectifying potassium currents evoked by alkaloid and peptide mu-opioid receptor agonists. Mol Cell Neurosci 24:517-523.
3. Bogdanov Y, Michels G, Armstrong-Gold C, Haydon PG, Lindstrom J, Pangalos M, Moss SJ (2006) Synaptic GABAA receptors are directly recruited from their extrasynaptic counterparts. EMBO J 25:4381-4389.
4. Brandon NJ, Uren JM, Kittler JT, Wang H, Olsen R, Parker PJ, Moss SJ (1999) Subunit-specific association of protein kinase C and the receptor for activated C kinase with GABA type A receptors. J Neurosci 19:9228-9234.
5. Brandon NJ, Delmas P, Kittler JT, McDonald BJ, Sieghart W, Brown DA, Smart TG, Moss SJ (2000) GABAA receptor phosphorylation and functional modulation in cortical neurons by a protein kinase C-dependent pathway. J Biol Chem 275:38856-38862.
6. Brandon N, Jovanovic J, Moss S (2002a) Multiple roles of protein kinases in the modulation of gamma-aminobutyric acid(A) receptor function and cell surface expression. Pharmacol Ther 94:113-122.
7. A receptors with the activation of G-protein-coupled receptors. J Neurosci 22:6353-6361.
8. Brandon NJ, Jovanovic JN, Colledge M, Kittler JT, Brandon JM, Scott JD, Moss SJ (2003) A-kinase anchoring protein 79/150 facilitates the phosphorylation of GABA(A) receptors by cAMP-dependent protein kinase via selective interaction with receptor beta subunits. Mol Cell Neurosci 22:87-97.
9. Brooks-Kayal AR, Shumate MD, Jin H, Rikhter TY, Coulter DA (1999) Selective changes in single cell GABA(A) receptor subunit expression and function in temporal lobe epilepsy. Nat Med 1998 10:1166-1172.
10. A receptor function through a phospho-dependent endocytosis mechanism in nucleus accumbens. J Neurosci 26:2513-2521.
11. Coulter DA (2001) Epilepsy-associated plasticity in gamma-aminobutyric acid receptor expression, function, and inhibitory synaptic properties. Int Rev Neurobiol 45:237-252.
12. 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.
13. Farrant M, Nusser Z (2005) Variations on an inhibitory theme: phasic and tonic activation of GABA(A) receptors. Nat Rev Neurosci 6:215-229.
14. A receptors. J Neurosci 25:5511-5520.
15. Haucke V (2006) Cargo takes control of endocytosis. Cell 127:35-37.
16. Haucke V, Wenk MR, Chapman ER, Farsad K, De Camilli P (2000) Dual interaction of synaptotagmin with mu2- and alpha-adaptin facilitates clathrin-coated pit nucleation. EMBO J 19:6011-6019.
17. A receptor currents. J Neurosci 23:11698-11710.
18. A receptor phosphorylation, activity, and cell-surface stability. J Neurosci 24:522-530.
19. Kapur J, Coulter DA (1995) Experimental status epilepticus alters gammaaminobutyric acid type A receptor function in CA1 pyramidal neurons. Ann Neurol 38:893-900.
20. Kittler JT, Moss SJ (2003) Modulation of GABAA receptor activity by phosphorylation and receptor trafficking: implications for the efficacy of synaptic inhibition. Curr Opin Neurobiol 13:341-347.
21. A receptors by an association with the adaptin AP2 complex modulates inhibitory synaptic currents in hippocampal neurons. J Neurosci 20:7972-7977.
22. Kittler JT, Thomas P, Tretter V, Bogdanov YD, Haucke V, Smart TG, Moss SJ (2004) Huntingtin-associated protein 1 regulates inhibitory synaptic transmission by modulating gamma-aminobutyric acid type A receptor membrane trafficking. Proc Natl Acad Sci USA 101:12736-12741.
23. Kittler JT, Chen G, Honing S, Bogdanov Y, McAinsh K, Arancibia-Carcamo IL, Jovanovic JN, Pangalos MN, Haucke V, Yan Z, Moss SJ (2005) Phospho-dependent binding of the clathrin AP2 adaptor complex to GABAA receptors regulates the efficacy of inhibitory synaptic transmission. Proc Natl Acad Sci USA 102:14871-14876.
24. Lowenstein DH, Alldredge BK (1998) Status epilepticus. N Engl J Med 338:970-976.
25. Luscher B, Keller CA (2004) Regulation of GABAA receptor trafficking, channel activity, and functional plasticity of inhibitory synapses. Pharmacol Ther 102:195-221.
26. Nathanson NM (1987) Molecular properties of the muscarinic acetylcholine receptor. Annu Rev Neurosci 10:195-236.
27. A receptors, loss of inhibition, and a mechanism for pharmacoresistance in status epilepticus. J Neurosci 25:7724-7733.
28. Niimura M, Moussa R, Bissoon N, Ikeda-Douglas C, Milgram NW, Gurd JW (2005) Changes in phosphorylation of the NMDA receptor in the rat hippocampus induced by status epilepticus. J Neurochem 92:1377-1385.
29. Parker PJ (2003) Protein kinase C phosphorylation: an introduction. Methods Mol Biol 233:159-162.
30. 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 10:1665-1673.
31. Rudolph U, Mohler H (2004) Analysis of GABAA receptor function and dissection of the pharmacology of benzodiazepines and general anesthetics through mouse genetics. Annu Rev Pharmacol Toxicol 44:475-498.
32. Rudolph U, Mohler H (2006) GABA-based therapeutic approaches: GABAA receptor subtype functions. Curr Opin Pharmacol 6:18-23.
33. Sieghart W, Sperk G (2002) Subunit composition, distribution and function of GABA(A) receptor subtypes. Curr Top Med Chem 2:795-816.
34. Staley KJ (2004) Role of the depolarizing GABA response in epilepsy. Adv Exp Med Biol 548:104-109.
35. A receptor phosphodependent modulation is regulated by phospholipase C-related inactive protein type 1, a novel protein phosphatase 1 anchoring protein. J Neurosci 24:70747084.
36. Treiman DM (1990) The role of benzodiazepines in the management of status epilepticus. Neurology 40:32-42.
37. van Rijnsoever C, Sidler C, Fritschy JM (2005) Internalized GABA-receptor subunits are transferred to an intracellular pool associated with the postsynaptic density. Eur J Neurosci 21:327-338.
38. Wang Q, Liu L, Pei L, Ju W, Ahmadian G, Lu J, Wang Y, Liu F, Wang YT (2003) Control of synaptic strength, a novel function of Akt. Neuron 38:915-928.
39. Wess J (2004) Muscarinic acetylcholine receptor knockout mice: novel phenotypes and clinical implications. Annu Rev Pharmacol Toxicol 44:423-450.