GABAA receptor regulation after experimental traumatic brain injury

Journal of Neurotrauma

Volumn 29, Issue 16, 2012, Pages 2548-2554

  Raible, Daniel J ^a   Frey, Lauren C ^b   Cruz Del Angel, Yasmin ^a   Russek, Shelley J ^c   Brooks Kayal, Amy R ^a,b,d  

^a Children's Hospital Colorado   (United States)

^b UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^c BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d CHILDREN S HOSPITAL COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR ALPHA1; 4 AMINOBUTYRIC ACID A RECEPTOR ALPHA4; CYCLIC AMP; JANUS KINASE; STAT3 PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; MALE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; TRAUMATIC BRAIN INJURY;

ANIMALS; BLOTTING, WESTERN; BRAIN INJURIES; DISEASE MODELS, ANIMAL; EARLY GROWTH RESPONSE PROTEIN 3; GENE EXPRESSION REGULATION; JANUS KINASES; MALE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-A; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STAT TRANSCRIPTION FACTORS;

EID: 84869001151     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2012.2483     Document Type: Article

References (46)

1. Sosin, D.M., Sniezek, J.E., and Thurman, D.J. (1996). Incidence of mild and moderate brain injury in the United States, 1991. Brain Inj. 10, 47-54. (Pubitemid 26093550)
2. Thurman, D.J., Alverson, C., Dunn, K.A., Guerrero, J., and Sniezek, J.E. (1999). Traumatic brain injury in the United States: A public health perspective. J. Head Trauma Rehabil. 14, 602-615 (Pubitemid 30027268)
3. Salazar, A.M., Jabbari, B., Vance, S.C., Grafman, J., Amin, D., and Dillon, J.D. (1985). Epilepsy after penetrating head injury. I. Clinical correlates: a report of the Vietnam Head Injury Study. Neurology 35, 1406-1414 (Pubitemid 15242412)
4. Marcikic, M., Melada, A., and Kovacevic, R. (1998). Management of war penetrating craniocerebral injuries during the war in Croatia. Injury 29, 613-618 (Pubitemid 28508543)
5. Diaz-Arrastia, R., Agostini, M.A., Frol, A.B., Mickey, B., Fleckenstein, J., Bigio, E., and Van Ness, P.C. (2000). Neurophysiologic and neuroradiologic features of intractable epilepsy after traumatic brain injury in adults. Arch. Neurol. 57, 1611-1616
6. Hudak, A.M., Trivedi, K., Harper, C.R., Booker, K., Caesar, R.R., Agostini, M., Van Ness, P.C., and Diaz-Arrastia, R. (2004). Evaluation of seizure-like episodes in survivors of moderate and severe traumatic brain injury. J. Head Trauma Rehabil. 19, 290-295 (Pubitemid 38938194)
7. Oliva, A.A., Jr., Kang, Y., Sanchez-Molano, J., Furones, C., and Atkins, C.M. (2011). STAT3 signaling after traumatic brain injury. J. Neurochem. 120, 710-720
8. Zhao, J., Li, G., Zhang, Y., Su, X., and Hang, C. (2011a). The potential role of JAK2/STAT3 pathway on the anti-apoptotic effect of recombinant human erythropoietin (rhEPO) after experimental traumatic brain injury of rats. Cytokine 56, 343-350
9. Zhao, J.B., Zhang, Y., Li, G.Z., Su, X.F., and Hang, C.H. (2011b). Activation of JAK2/STAT pathway in cerebral cortex after experimental traumatic brain injury of rats. Neurosci. Lett. 498, 147-152
10. Planas, A.M., Soriano, M.A., Berruezo, M., Justicia, C., Estrada, A., Pitarch, S., and Ferrer, I. (1996). Induction of Stat3, a signal transducer and transcription factor, in reactive microglia following transient focal cerebral ischaemia. Eur. J. Neurosci. 8, 2612-2618 (Pubitemid 27011338)
11. Suzuki, S., Tanaka, K., Nogawa, S., Dembo, T., Kosakai, A., and Fukuuchi, Y. (2001). Phosphorylation of signal transducer and activator of transcription-3 (Stat3) after focal cerebral ischemia in rats. Exp. Neurol. 170, 63-71 (Pubitemid 32641774)
12. Choi, J.S., Kim, S.Y., Park, H.J., Cha, J.H., Choi, Y.S., Kang, J.E., Chung, J.W., Chun, M.H., and Lee, M.Y. (2003). 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. 119, 10-18 (Pubitemid 37324793)
13. Lund, I.V., Hu, Y., Raol, Y.H., Benham, R.S., Faris, R., Russek, S.J., and Brooks-Kayal, A.R. (2008). BDNF selectively regulates GABAA receptor transcription by activation of the JAK/STAT pathway. Sci. Signal 1, ra9
14. Brooks-Kayal, A.R., Shumate, M.D., Jin, H., Rikhter, T.Y., and 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 (Pubitemid 28468830)
15. Peng, Z., Huang, C.S., Stell, B.M., Mody, I., and Houser, C.R. (2004). Altered expression of the delta subunit of the GABAA receptor in a mouse model of temporal lobe epilepsy. J. Neurosci. 24, 8629-8639 (Pubitemid 39313785)
16. Zhang, G., Raol, Y.H., Hsu, F.C., Coulter, D.A., and Brooks-Kayal, A.R. (2004). Effects of status epilepticus on hippocampal GABAA receptors are age-dependent. Neuroscience 125, 299-303 (Pubitemid 38446737)
17. Raol, Y.H., Lund, I.V., Bandyopadhyay, S., Zhang, G., Roberts, D.S., Wolfe, J.H., Russek, S.J., and 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 (Pubitemid 44772163)
18. Gibson, C.J., Meyer, R.C., and Hamm, R.J. (2010). Traumatic brain injury and the effects of diazepam, diltiazem, and MK-801 on GABAA receptor subunit expression in rat hippocampus. J. Biomed. Sci. 17, 38
19. Sun, C., Mtchedlishvili, Z., Erisir, A., and Kapur, J. (2007). Diminished neurosteroid sensitivity of synaptic inhibition and altered location of the alpha4 subunit of GABA(A) receptors in an animal model of epilepsy. J. Neurosci. 27, 12641-12650 (Pubitemid 350127828)
20. Zhang, N., Wei, W., Mody, I., and 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 (Pubitemid 47066583)
21. Lowenstein, D.H., Thomas, M.J., Smith, D.H., and McIntosh, T.K. (1992). Selective vulnerability of dentate hilar neurons following traumatic brain injury: a potential mechanistic link between head trauma and disorders of the hippocampus. J. Neurosci. 12, 4846-4853
22. Toth, Z., Hollrigel, G.S., Gorcs, T., and Soltesz, I. (1997). Instantaneous perturbation of dentate interneuronal networks by a pressure wave-transient delivered to the neocortex. J. Neurosci. 17, 8106-8117 (Pubitemid 27461035)
23. Gupta, A., Elgammal, F.S., Proddutur, A., Shah, S., and Santhakumar, V. (2012). Decrease in tonic inhibition contributes to increase in dentate semilunar granule cell excitability after brain injury. J. Neurosci. 32, 2523-2537
24. D'Ambrosio, R., Fairbanks, J.P., Fender, J.S., Born, D.E., Doyle, D.L., and Miller, J.W. (2004). Post-traumatic epilepsy following fluid percussion injury in the rat. Brain 127, 304-314 (Pubitemid 38160315)
25. Kharatishvili, I., Nissinen, J.P., McIntosh, T.K., and Pitkanen, A. (2006). A model of posttraumatic epilepsy induced by lateral fluidpercussion brain injury in rats. Neuroscience 140, 685-697
26. Frey, L.C., Hellier, J., Unkart, C., Lepkin, A., Howard, A., Hasebroock, K., Serkova, N., Liang, L., Patel, M., Soltesz, I., and Staley, K. (2009). A novel apparatus for lateral fluid percussion injury in the rat. J. Neurosci. Methods 177, 267-272
27. Roberts, D.S., Hu, Y., Lund, I.V., Brooks-Kayal, A.R., and Russek, S.J. (2006). 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. 281, 29431-29435 (Pubitemid 44536950)
28. Sur, C., Wafford, K.A., Reynolds, D.S., Hadingham, K.L., Bromidge, F., Macaulay, A., Collinson, N., O'Meara, G., Howell, O., Newman, R., Myers, J., Atack, J.R., Dawson, G.R., McKernan, R.M., Whiting, P.J., and Rosahl, T.W. (2001). Loss of the major GABA(A) receptor subtype in the brain is not lethal in mice. J. Neurosci. 21, 3409-3418 (Pubitemid 32422806)
29. Kralic, J.E., Sidler, C., Parpan, F., Homanics, G.E., Morrow, A.L., and Fritschy, J.M. (2006). Compensatory alteration of inhibitory synaptic circuits in cerebellum and thalamus of gamma-aminobutyric acid type A receptor alpha1 subunit knockout mice. J. Comp. Neurol. 495, 408-421 (Pubitemid 43375814)
30. Schneider Gasser, E.M., Duveau, V., Prenosil, G.A., and Fritschy, J.M. (2007). Reorganization of GABAergic circuits maintains GABAA receptor-mediated transmission onto CA1 interneurons in alpha1- subunit-null mice. Eur. J. Neurosci. 25, 3287-3304 (Pubitemid 46872760)
31. Liang, J., Suryanarayanan, A., Chandra, D., Homanics, G.E., Olsen, R.W., and Spigelman, I. (2008). Functional consequences of GABAA receptor alpha 4 subunit deletion on synaptic and extrasynaptic currents in mouse dentate granule cells. Alcoholism Clin. Exper. Res. 32, 19-26 (Pubitemid 350293909)
32. Pavlov, I., Huusko, N., Drexel, M., Kirchmair, E., Sperk, G., Pitkanen, A., and Walker, M.C. (2011). Progressive loss of phasic, but not tonic, GABAA receptor-mediated inhibition in dentate granule cells in a model of post-traumatic epilepsy in rats. Neuroscience 194, 208-219
33. Kharlamov, E.A., Lepsveridze, E., Meparishvili, M., Solomonia, R.O., Lu, B., Miller, E.R., Kelly, K.M., and Mtchedlishvili, Z. (2011). Alterations of GABA(A) and glutamate receptor subunits and heat shock protein in rat hippocampus following traumatic brain injury and in posttraumatic epilepsy. Epilepsy Res. 95, 20-34
34. Mtchedlishvili, Z., Lepsveridze, E., Xu, H., Kharlamov, E.A., Lu, B., and Kelly, K.M. (2010). Increase of GABAA receptor-mediated tonic inhibition in dentate granule cells after traumatic brain injury. Neurobiol. Dis. 38, 464-475
35. Somogyi, P., Fritschy, J.M., Benke, D., Roberts, J.D., and Sieghart, W. (1996). The gamma 2 subunit of the GABAA receptor is concentrated in synaptic junctions containing the alpha 1 and beta 2/3 subunits in hippocampus, cerebellum and globus pallidus. Neuropharmacology 35, 1425-1444 (Pubitemid 27013878)
36. Nusser, Z., Sieghart, W., and Somogyi, P. (1998). Segregation of different GABAA receptors to synaptic and extrasynaptic membranes of cerebellar granule cells. J. Neurosci. 18, 1693-1703 (Pubitemid 28103077)
37. Sur, C., Farrar, S.J., Kerby, J., Whiting, P.J., Atack, J.R., and McKernan, R.M. (1999). Preferential coassembly of alpha4 and delta subunits of the gamma-aminobutyric acidA receptor in rat thalamus. Mol. Pharmacol. 56, 110-115 (Pubitemid 29309818)
38. Sassoe-Pognetto, M., Panzanelli, P., Sieghart, W., and Fritschy, J.M. (2000). Colocalization of multiple GABA(A) receptor subtypes with gephyrin at postsynaptic sites. J. Comp. Neurol. 420, 481-498 (Pubitemid 30235932)
39. Wei, W., Zhang, N., Peng, Z., Houser, C.R., and Mody, I. (2003). Perisynaptic localization of delta subunit-containing GABA(A) receptors and their activation by GABA spillover in the mouse dentate gyrus. J. Neurosci. 23, 10650-10661 (Pubitemid 37485279)
40. Semyanov, A., Walker, M.C., Kullmann, D.M., and Silver, R.A. (2004). Tonically active GABA A receptors: modulating gain and maintaining the tone. Trends Neurosci. 27, 262-269 (Pubitemid 38529954)
41. Sun, C., Sieghart, W., and Kapur, J. (2004). Distribution of alpha1, alpha4, gamma2, and delta subunits of GABAA receptors in hippocampal granule cells. Brain Res. 1029, 207-216 (Pubitemid 39470177)
42. Jia, F., Pignataro, L., Schofield, C.M., Yue, M., Harrison, N.L., and Goldstein, P.A. (2005). An extrasynaptic GABAA receptor mediates tonic inhibition in thalamic VB neurons. J. Neurophysiol. 94, 4491-4501 (Pubitemid 41691802)
43. Liang, J., Zhang, N., Cagetti, E., Houser, C.R., Olsen, R.W., and Spigelman, I. (2006). Chronic intermittent ethanol-induced switch of ethanol actions from extrasynaptic to synaptic hippocampal GABAA receptors. J. Neurosci. 26, 1749-1758 (Pubitemid 43236987)
44. Goodkin, H.P., Joshi, S., Mtchedlishvili, Z., Brar, J., and Kapur, J. (2008). Subunit-specific trafficking of GABA(A) receptors during status epilepticus. J. Neurosci. 28, 2527-2538 (Pubitemid 351348210)
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., and Russek, S.J. (2005). 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. USA 102, 11894-11899 (Pubitemid 41170821)
46. Gangisetty, O., and Reddy, D.S. (2010). Neurosteroid withdrawal regulates GABA-A receptor alpha4-subunit expression and seizure susceptibility by activation of progesterone receptor-independent early growth response factor-3 pathway. Neuroscience 170, 865-880