Alterations of A-type potassium channels in hippocampal neurons after traumatic brain injury

Journal of Neurotrauma

Volumn 29, Issue 2, 2012, Pages 235-245

  Lei, Zhigang ^a   Deng, Ping ^a   Li, Jinqing ^a   Xu, Zao C ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

controlled cortical impact; hyperexcitability; IA; K v4.2; Kv4.3; post traumatic epilepsy

Indexed keywords

BICUCULLINE; POTASSIUM CHANNEL; POTASSIUM CHANNEL A; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN ELECTROPHYSIOLOGY; CONTROLLED STUDY; DISEASE SEVERITY; DOWN REGULATION; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MALE; NERVE CELL EXCITABILITY; NERVE CELL NECROSIS; NONHUMAN; POTASSIUM CURRENT; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; RAT; SEIZURE; TRAUMATIC BRAIN INJURY; WESTERN BLOTTING;

ANIMALS; BRAIN INJURIES; DISEASE MODELS, ANIMAL; EPILEPSY; HIPPOCAMPUS; MALE; NERVE DEGENERATION; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; SHAL POTASSIUM CHANNELS;

EID: 84863012439     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2010.1537     Document Type: Article

References (51)

1. Agrawal, A., Timothy, J., Pandit, L., and Manju, M. (2006). Post-traumatic epilepsy: an overview. Clin. Neurol. Neurosurg. 108, 433-439.
2. An, W.F., Bowlby, M.R., Betty, M., Cao, J., Ling, H.P., Mendoza, G., Hinson, J.W., Mattsson, K.I., Strassle, B.W., Trimmer, J.S., and Rhodes, K.J. (2000). Modulation of A-type potassium channels by a family of calcium sensors. Nature 403, 553-556. (Pubitemid 30082201)
3. Andrasfalvy, B.K., Makara, J.K., Johnston, D., and Magee, J.C. (2008). Altered synaptic and non-synaptic properties of CA1 pyramidal neurons in Kv4.2 knockout mice. J. Physiol. 586, 3881-3892.
4. Arundine, M., and Tymianski, M. (2004). Molecular mechanisms of glutamate-dependent neurodegeneration in ischemia and traumatic brain injury. Cell Mol. Life Sci. 61, 657-668. (Pubitemid 38446410)
5. Bales, J.W., Wagner, A.K., Kline, A.E., and Dixon, C.E. (2009). Persistent cognitive dysfunction after traumatic brain injury: a dopamine hypothesis. Neurosci. Biobehav. Rev. 33, 981-1003.
6. Barnwell, L.F., Lugo, J.N., Lee, W.L., Willis, S.E., Gertz, S.J., Hrachovy, R.A., and Anderson, A.E. (2009). Kv4.2 knockout mice demonstrate increased susceptibility to convulsant stimulation. Epilepsia 50, 1741-1751.
7. Bernard, C., Anderson, A., Becker, A., Poolos, N.P., Beck, H., and Johnston, D. (2004). Acquired dendritic channelopathy in temporal lobe epilepsy. Science 305, 532-535. (Pubitemid 38971346)
8. Bruns, J., Jr., and Hauser, W.A. (2003). The epidemiology of traumatic brain injury: a review. Epilepsia 44, Suppl. 10, 2-10. (Pubitemid 37280386)
9. Cai, X., Liang, C.W., Muralidharan, S., Kao, J.P., Tang, C.M., and Thompson, S.M. (2004). Unique roles of SK and Kv4.2 potas-sium channels in dendritic integration. Neuron 44, 351-364. (Pubitemid 39346257)
10. Chen, X., Yuan, L.L., Zhao, C., Birnbaum, S.G., Frick, A., Jung, W.E., Schwarz, T.L., Sweatt, J.D., and Johnston, D. (2006). Deletion of Kv4.2 gene eliminates dendritic A-type K+ cur-rent and enhances induction of long-term potentiation in hippocampal CA1 pyramidal neurons. J. Neurosci. 26, 12,143-12,151. (Pubitemid 44808381)
11. D'Ambrosio, R., Hakimian, S., Stewart, T., Verley, D.R., Fender, J.S., Eastman, C.L., Sheerin, A.H., Gupta, P., Diaz-Arrastia, R., Ojemann, J., and Miller, J.W. (2009). Functional definition of seizure provides new insight into post-traumatic epilepto-genesis. Brain 132, 2805-2821.
12. D'Ambrosio, R., Maris, D.O., Grady, M.S., Winn, H.R., and Ja-nigro, D. (1999). Impaired K( + ) homeostasis and altered electrophysiological properties of post-traumatic hippocampal glia. J. Neurosci. 19, 8152-8162. (Pubitemid 30225811)
13. D'Ambrosio, R., and Perucca, E. (2004). Epilepsy after head in-jury. Curr. Opin. Neurol. 17, 731-735.
14. Deng, P., Pang, Z., Zhang, Y., and Xu, Z.C. (2004). Develop-mental changes of transient potassium currents in large aspiny neurons in the neostriatum. Brain Res. Dev. Brain Res. 153, 97-107. (Pubitemid 39298881)
15. Deng, P., Pang, Z.P., Lei, Z., and Xu, Z.C. (2009). Excitatory roles of protein kinase C in striatal cholinergic interneurons. J. Neurophysiol. 102, 2453-2461.
16. Diaz-Arrastia, R., Agostini, M.A., Frol, A.B., Mickey, B., Fleckenstein, J., Bigio, E., and Van Ness, P.C. (2000). Neuro-physiologic and neuroradiologic features of intractable epi-lepsy after traumatic brain injury in adults. Arch. Neurol. 57, 1611-1616.
17. Dixon, C.E., Clifton, G.L., Lighthall, J.W., Yaghmai, A.A., and Hayes, R.L. (1991). A controlled cortical impact model of traumatic brain injury in the rat. J. Neurosci. Methods. 39, 253-262.
18. Francis, J., Jugloff, D.G., Mingo, N.S., Wallace, M.C., Jones, O.T., Burnham, W.M., and Eubanks, J.H. (1997). Kainic acid-induced generalized seizures alter the regional hippocampal expression of the rat Kv4.2 potassium channel gene. Neurosci. Lett. 232, 91-94. (Pubitemid 27394493)
19. Frick, A., Magee, J., and Johnston, D. (2004). LTP is accompanied by an enhanced local excitability of pyramidal neuron den-drites. Nat. Neurosci. 7, 126-135. (Pubitemid 38129788)
20. Gandolfo, G., Gottesmann, C., Bidard, J.N., and Lazdunski, M. (1989). Subtypes of K+ channels differentiated by the effect of K+ channel openers upon K+ channel blocker-induced sei-zures. Brain Res. 495, 189-192. (Pubitemid 19195701)
21. Golarai, G., Greenwood, A.C., Feeney, D.M., and Connor, J.A. (2001). Physiological and structural evidence for hippocampal involvement in persistent seizure susceptibility after traumatic brain injury. J. Neurosci. 21, 8523-8537. (Pubitemid 33051451)
22. Goll, D.E., Thompson, V.F., Li, H., Wei, W., and Cong, J. (2003). The calpain system. Physiol. Rev. 83, 731-801. (Pubitemid 36828925)
23. Griesemer, D., and Mautes, A.M. (2007). Closed head injury causes hyperexcitability in rat hippocampal CA1 but not in CA3 pyramidal cells. J. Neurotrauma 24, 1823-1832.
24. Guo, W., Jung, W.E., Marionneau, C., Aimond, F., Xu, H., Ya-mada, K.A., Schwarz, T.L., Demolombe, S., and Nerbonne, J.M. (2005). Targeted deletion of Kv4.2 eliminates I(to,f) and results in electrical and molecular remodeling, with no evi-dence of ventricular hypertrophy or myocardial dysfunction. Circ. Res. 97, 1342-1350.
25. Hicks, R., Soares, H., Smith, D., and McIntosh, T. (1996). Tem-poral and spatial characterization of neuronal injury following lateral fluid-percussion brain injury in the rat. Acta Neuro-pathol. 91, 236-246. (Pubitemid 26042215)
26. 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)
27. Jerng, H.H., Pfaffinger, P.J., and Covarrubias, M. (2004). Mole-cular physiology and modulation of somatodendritic A-type potassium channels. Mol. Cell Neurosci. 27, 343-369. (Pubitemid 39539991)
28. Kharatishvili, I., Nissinen, J.P., McIntosh, T.K., and Pitkanen, A. (2006). A model of posttraumatic epilepsy induced by lat-eral fluid-percussion brain injury in rats. Neuroscience 140, 685-697
29. Kharatishvili, I., and Pitkanen, A. (2010). Association of the se-verity of cortical damage with the occurrence of spontaneous seizures and hyperexcitability in an animal model of post-traumatic epilepsy. Epilepsy Res. 90, 47-59.
30. Kim, J., Wei, D.S., and Hoffman, D.A. (2005). Kv4 potassium channel subunits control action potential repolarization and frequency-dependent broadening in rat hippocampal CA1 pyramidal neurones. J. Physiol. 569, 41-57. (Pubitemid 41701375)
31. Lei, Z., Deng, P., Li, Y., and Xu, Z.C. (2010). Downregulation of Kv4.2 channels mediated by NR2B-containing NMDA re-ceptors in cultured hippocampal neurons. Neuroscience 165, 350-362.
32. Lei, Z., Deng, P., and Xu, Z.C. (2008). Regulation of Kv4.2 channels by glutamate in cultured hippocampal neurons. J. Neurochem. 106, 182-192. (Pubitemid 351840205)
33. 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.
34. Lugo, J.N., Barnwell, L.F., Ren, Y., Lee, W.L., Johnston, L.D., Kim, R., Hrachovy, R.A., Sweatt, J.D., and Anderson, A.E. (2008). Altered phosphorylation and localization of the A-type channel, Kv4.2 in status epilepticus. J. Neurochem. 106, 1929-1940.
35. McKinney, R.A., Debanne, D., Gahwiler, B.H., and Thompson, S.M. (1997). Lesion-induced axonal sprouting and hyperex-citability in the hippocampus in vitro: implications for the genesis of posttraumatic epilepsy. Nat. Med. 3, 990-996. (Pubitemid 27391953)
36. Millis, S.R., Rosenthal, M., Novack, T.A., Sherer, M., Nick, T.G., Kreutzer, J.S., High, W.M., Jr., and Ricker, J.H. (2001). Long-term neuropsychological outcome after traumatic brain injury. J. Head Trauma Rehabil. 16, 343-355. (Pubitemid 32730343)
37. Monaghan, M.M., Menegola, M., Vacher, H., Rhodes, K.J., and Trimmer, J.S. (2008). Altered expression and localization of hippocampal A-type potassium channel subunits in the pilo-carpine-induced model of temporal lobe epilepsy. Neu-roscience 156, 550-562.
38. Nadal, M.S., Ozaita, A., Amarillo, Y., Vega-Saenz de Miera, E., Ma, Y., Mo, W., Goldberg, E.M., Misumi, Y., Ikehara, Y., Neubert, T.A., and Rudy, B. (2003). The CD26-related di-peptidyl aminopeptidase-like protein DPPX is a critical com-ponent of neuronal A-type K+ channels. Neuron 37, 449-461. (Pubitemid 36183366)
39. Nadler, V., Biegon, A., Beit-Yannai, E., Adamchik, J., and Sho-hami, E. (1995). 45Ca accumulation in rat brain after closed head injury; attenuation by the novel neuroprotective agent HU-211. Brain Res. 685, 1-11.
40. Nilsson, P., Ronne-Engstrom, E., Flink, R., Ungerstedt, U., Carlson, H., and Hillered, L. (1994). Epileptic seizure activity in the acute phase following cortical impact trauma in rat. Brain Res. 637, 227-232. (Pubitemid 24061052)
41. Pike, B.R., Zhao, X., Newcomb, J.K., Posmantur, R.M., Wang, K.K., and Hayes, R.L. (1998). Regional calpain and caspase-3 proteolysis of alpha-spectrin after traumatic brain injury. Neuroreport 9, 2437-2442. (Pubitemid 28387126)
42. Rettig, J., Heinemann, S.H., Wunder, F., Lorra, C., Parcej, D.N., Dolly, J.O., and Pongs, O. (1994). Inactivation properties of voltage-gated K+ channels altered by presence of beta-sub-unit. Nature 369, 289-294. (Pubitemid 24159535)
43. Santhakumar, V., Ratzliff, A.D., Jeng, J., Toth, Z., and Soltesz, I. (2001). Long-term hyperexcitability in the hippocampus after experimental head trauma. Ann. Neurol. 50, 708-717. (Pubitemid 33116130)
44. Santhakumar, V., Voipio, J., Kaila, K., and Soltesz, I. (2003). Post-traumatic hyperexcitability is not caused by impaired buffer-ing of extracellular potassium. J. Neurosci. 23, 5865-5876. (Pubitemid 36807866)
45. Schindler, C.J., Slamberova, R., and Vathy, I. (2004). Cholera toxin B decreases bicuculline seizures in prenatally morphine-and saline-exposed male rats. Pharmacol. Biochem. Behav. 77, 509-515. (Pubitemid 38296810)
46. Serodio, P., Kentros, C., and Rudy, B. (1994). Identification of molecular components of A-type channels activating at sub-threshold potentials. J. Neurophysiol. 72, 1516-1529. (Pubitemid 24325082)
47. Serodio, P., and Rudy, B. (1998). Differential expression of Kv4 K+ channel subunits mediating subthreshold transient K + (A-type) currents in rat brain. J. Neurophysiol. 79, 1081-1091. (Pubitemid 28095919)
48. Serodio, P., Vega-Saenz de Miera, E., and Rudy, B. (1996). Cloning of a novel component of A-type K+ channels oper-ating at subthreshold potentials with unique expression in heart and brain. J. Neurophysiol. 75, 2174-2179. (Pubitemid 26159051)
49. Singh, B., Ogiwara, I., Kaneda, M., Tokonami, N., Mazaki, E., Baba, K., Matsuda, K., Inoue, Y., and Yamakawa, K. (2006). A Kv4.2 truncation mutation in a patient with temporal lobe epilepsy. Neurobiol. Dis. 24, 245-253. (Pubitemid 44572745)
50. Tsaur, M.L., Sheng, M., Lowenstein, D.H., Jan, Y.N., and Jan, LY. (1992). Differential expression of K+ channel mRNAs in the rat brain and down-regulation in the hippocampus fol-lowing seizures. Neuron 8, 1055-1067.
51. van den Pol, A.N., Obrietan, K., and Chen, G. (1996). Excitatory actions of GABA after neuronal trauma. J. Neurosci. 16, 4283-4292. (Pubitemid 26192423)