Chronic dysfunction of astrocytic inwardly rectifying K+ channels specific to the neocortical epileptic focus after fluid percussion injury in the rat

Journal of Neurophysiology

Volumn 104, Issue 6, 2010, Pages 3345-3360

  Stewart, Tessandra H ^a,b   Eastman, Clifford L ^a   Groblewski, Peter A ^a   Fender, Jason S ^a   Verley, Derek R ^a   Cook, David G ^c,d   D'Ambrosio, Raimondo ^a,b,e,f,g  

^a Department of Neurological Surgery ^*  (United States)

^b Graduate Program in Neurobiology and Behavior   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

^d Departments of Medicine and Pharmacology   (United States)

^e Regional Epilepsy Center   (United States)

^f UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^g UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALBUMIN; INWARDLY RECTIFYING POTASSIUM CHANNEL; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR4.1; THROMBIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CHRONIC DISEASE; CONTROLLED STUDY; EPILEPTIC FOCUS; FEMALE; FOCAL EPILEPSY; HEAD INJURY; HIPPOCAMPUS; IMMUNOREACTIVITY; MEMBRANE CURRENT; NEOCORTEX; NONHUMAN; PATHOPHYSIOLOGY; PERCUSSION; PRIORITY JOURNAL; RAT; ROSTRAL PARASAGGITAL FLUID PERCUSSION INJURY;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ANIMALS; ASTROCYTES; BRAIN INJURIES; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; ELECTROENCEPHALOGRAPHY; EPILEPSIES, PARTIAL; EXUDATES AND TRANSUDATES; MALE; MICROSCOPY, CONFOCAL; NEOCORTEX; PATCH-CLAMP TECHNIQUES; POTASSIUM CHANNELS, INWARDLY RECTIFYING; RATS; RATS, SPRAGUE-DAWLEY; SERUM; THROMBIN; VIDEO RECORDING;

EID: 78650899612     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00398.2010     Document Type: Article

References (73)

1. Abrahám H, Losonczy A, Czéh G, Lázár G. Rapid activation of microglial cells by hypoxia, kainic acid, and potassium ions in slice preparations of the rat hippocampus. Brain Res 906: 115-126, 2001.
2. Albensi BC, Janigro D. Traumatic brain injury and its effects on synaptic plasticity. Brain Inj 17: 653-663, 2003.
3. Alexander JS, Patton WF, Christman BW, Cuiper LL, Haselton FR. Platelet-derived lysophosphatidic acid decreases endothelial permeability in vitro Am J Physiol Heart Circ Physiol 274: H115-H122, 1998.
4. Annegers JF, Hauser WA, Coan SP, Rocca WA. A population-based study of seizures after traumatic brain injuries. N Engl J Med 338: 20-24, 1998.
5. Ballanyi K, Grafe P, ten Bruggencate G. Ion activities and potassium uptake mechanisms of glial cells in guinea-pig olfactory cortex slices. J Physiol 382: 159-174, 1987.
6. Bordey A, Sontheimer H. Properties of human glial cells associated with epileptic seizure foci. Epilepsy Res 32: 286-303, 1998.
7. Bordey A, Spencer DD. Chemokine modulation of high-conductance Ca(2+)-sensitive K(+) currents in microglia from human hippocampi. Eur J Neurosci 18: 2893-2898, 2003.
8. Bordey A, Spencer DD. Distinct electrophysiological alterations in dentate gyrus versus CA1 glial cells from epileptic humans with temporal lobe sclerosis. Epilepsy Res 59: 107-122, 2004.
9. Boucsein C, Kettenmann H, Nolte C. Electrophysiological properties of microglial cells in normal and pathologic rat brain slices. Eur J Neurosci 12: 2049-2058, 2000.
10. Brew H, Attwell D. Electrogenic glutamate uptake is a major current carrier in the membrane of axolotl retinal glial cells. Nature 327: 707-709, 1987.
11. Bünemann M, Pott L. Membrane-delimited activation of muscarinic K current by an albumin-associated factor in guinea-pig atrial myocytes. Pfluegers 425: 329-334, 1993. (Pubitemid 23338851)
12. Buono RJ, Lohoff FW, Sander T, Sperling MR, O'Connor MJ, Dlugos DJ, Ryan SG, Golden GT, Zhao H, Scattergood TM, Berrettini WH, Ferraro TN. Association between variation in the human KCNJ10 potassium ion channel gene and seizure susceptibility. Epilepsy Res 58: 175-183, 2004.
13. Butt AM, Kalsi A. Inwardly rectifying potassium channels (Kir) in central nervous system glia: A special role for Kir4.1 in glial functions. J Cell Mol Med 10: 33-44, 2006.
14. Cacheaux LP, Ivens S, David Y, Lakhter AJ, Bar-Klein G, Shapira M, Heinemann U, Friedman A, Kaufer D. Transcriptome profiling reveals TGF-beta signaling involvement in epileptogenesis. J Neurosci 29: 8927-8935, 2009.
15. Cohen A, Pfister BJ, Schwarzbach E, Grady MS, Goforth PB, Satin LS. Injury-induced alterations in CNS electrophysiology. Prog Brain Res 161: 143-169, 2007.
16. D'Ambrosio R. The role of glial membrane ion channels in seizures and epileptogenesis. Pharmacol Ther 103: 95-108, 2004.
17. D'Ambrosio R, Fairbanks JP, Fender JS, Born DE, Doyle DL, Miller JW. Post-traumatic epilepsy following fluid percussion injury in the rat. Brain 127: 304-314, 2004.
18. D'Ambrosio R, Fender JS, Fairbanks JP, Simon EA, Born DE, Doyle DL, Miller JW. Progression from frontal-parietal to mesial-temporal epilepsy after fluid percussion injury in the rat. Brain 128: 174-188, 2005.
19. + in rat hippocampus. J Neurophysiol 87: 87-102, 2002.
20. D'Ambrosio R, Hakimian S, Stewart T, Verley DR, Fender JS, Eastman CL, Sheerin AH, Gupta P, Diaz-Arrastia R, Ojemann J, Miller JW. Functional definition of seizure provides new insight into post-traumatic epileptogenesis. Brain 132: 2805-2821, 2009.
21. D'Ambrosio R, Maris DO, Grady MS, Winn HR, Janigro D. Impaired K(+) homeostasis and altered electrophysiological properties of post-traumatic hippocampal glia. J Neurosci 19: 8152-8162, 1999.
22. D'Ambrosio R, Perucca E. Epilepsy after head injury. Curr Opin Neurol 17: 731-735, 2004.
23. D'Ambrosio R, Wenzel J, Schwartzkroin PA, McKhann GM II, Janigro D. Functional specialization and topographic segregation of hippocampal astrocytes. J Neurosci 18: 4425-4438, 1998.
24. Dawson M, Polito A, Levine JM, Reynolds R. NG2-expressing glial progenitor cells: An abundant and widespread population of cycling cells in the adult rat CNS. Mol Cell Neurosci 24: 476-488, 2003.
25. Dietzel I, Heinemann U, Lux HD. Relations between slow extracellular potential changes, glial potassium buffering, and electrolyte and cellular volume changes during neuronal hyperactivity in cat brain. Glia 2: 25-44, 1989.
26. DiFrancesco D, Ferroni A, Visentin S. Barium-induced blockade of the inward rectifier in calf Purkinje fibres. Pfluegers 402: 446-453, 1984.
27. Delgado-Escueta AV, Wilson WA, Olsen RW, Porter RJ. Glia and epilepsy. In: Jasper's Basic Mechanisms of the Epilepsies, (3rd ed.) edited by Delgado-Escueta Av and Jasper HH. Philadelphia, PA: Lippincott Williams and Wilkins, 1999, p. 561-591.
28. Djukic B, Caspe KB, Philpot BD, Chin LS, McCarthy KD. Conditional knock-out of Kir4.1 leads to glial membrane depolarization, inhibition of potassium and glutamate uptake, and enhanced short-term synaptic potentiation. J Neurosci 27: 11354-11365, 2007.
29. Dudek FE, Snow RW, Taylor CP. Role of electrical interactions in synchronization of epileptiform burst. In: Basic Mechanisms of the Epilepsies: Molecular and Cellular Approachs, edited by Delgado-Escueta AV, Ward AA, Woodbury DM, Porter RJ. New York: Raven Press, 1986.
30. Ferraro TN, Golden GT, Smith GG, Martin JF, Lohoff FW, Gieringer TA, Zamboni D, Schwebel CL, Press DM, Kratzer SO, Zhao H, Berrettini WH, Buono RJ. Fine mapping of a seizure susceptibility locus on mouse Chromosome 1: Nomination of Kcnj10 as a causative gene. Mamm Genome 15: 239-251, 2004.
31. Grundfest H, Magnes J. Excitability changes in dorsal roots produced by electrotonic effects from adjacent afferent activity. Am J Physiol 164: 502-508, 1951.
32. Hagiwara S, Takahashi K. The anomalous rectification and cation selectivity of the membrane of a starfish egg cell. J Membr Biol 18: 61-80, 1974.
33. + channel subunits, Kir4.1 and Kir5. 1, in brain astrocytes. J Biol Chem 279: 44065-44073, 2004.
34. Higashi K, Fujita A, Inanobe A, Tanemoto M, Doi K, Kubo T, Kurachi Y. An inwardly rectifying K(+) channel, Kir4.1, expressed in astrocytes surrounds synapses and blood vessels in brain. Am J Physiol Cell Physiol 281: C922-C931, 2001.
35. Hille B. Ionic Channels of Excitable Membranes. Sunderland, MA: Sinauer Associates, 2001.
36. Hill-Felberg SJ, McIntosh TK, Oliver DL, Raghupathi R, Barbarese E. Concurrent loss and proliferation of astrocytes following lateral fluid percussion brain injury in the adult rat. J Neurosci Res 57: 271-279, 1999.
37. Hinterkeuser S, Schröder W, Hager G, Seifert G, Blümcke I, Elger CE, Schramm J, Steinhäuser C. Astrocytes in the hippocampus of patients with temporal lobe epilepsy display changes in potassium conductances. Eur J Neurosci 12: 2087-2096, 2000.
38. Hochman DW, Baraban SC, Owens JW, Schwartzkroin PA. Dissociation of synchronization and excitability in furosemide blockade of epileptiform activity. Science 270: 99-102, 1995.
39. Hoshino S, Kobayashi S, Nakazawa S. Prolonged and extensive IgG immunoreactivity after severe fluid-percussion injury in rat brain. Brain Res 711: 73-83, 1996.
40. Ivens S, Kaufer D, Flores LP, Bechmann I, Zumsteg D, Tomkins O, Seiffert E, Heinemann U, Friedman A. TGF-beta receptor-mediated albumin uptake into astrocytes is involved in neocortical epileptogenesis. Brain 130: 535-547, 2007.
41. Jansen LA, Uhlmann EJ, Crino PB, Gutmann DH, Wong M. Epileptogenesis and reduced inward rectifier potassium current in tuberous sclerosis complex-1-deficient astrocytes. Epilepsia 46: 1871-1880, 2005.
42. Jauch R, Windmüller O, Lehmann TN, Heinemann U, Gabriel S. Effects of barium, furosemide, ouabaine and 4,4=-diisothiocyanatostilbene-2,2=- disulfonic acid (DIDS) on ionophoretically-induced changes in extracellular potassium concentration in hippocampal slices from rats and from patients with epilepsy. Brain Res 925: 18-27, 2002.
43. Karwoski CJ, Lu HK, Newman EA. Spatial buffering of light-evoked potassium increases by retinal Müller (glial) cells. Science 244: 578-580, 1989.
44. Katayama Y, Becker DP, Tamura T, Hovda DA. Massive increases in extracellular potassium and the indiscriminate release of glutamate following concussive brain injury. J Neurosurg 73: 889-900, 1990.
45. Kofuji P, Ceelen P, Zahs KR, Surbeck LW, Lester HA, Newman EA, et al. Genetic inactivation of an inwardly rectifying potassium channel (Kir4.1 subunit) in mice: Phenotypic impact in retina. J Neurosci 20: 5733-5740, 2000.
46. Kofuji P, Newman EA. Potassium buffering in the central nervous system. Neuroscience 129: 1045-1056, 2004.
47. Kreps DM, Whittle SM, Hoffman JM, Toews ML. Lysophosphatidic acid mimics seruminduced sensitization of cyclic AMP accumulation. FASEB J 7: 1376-1380, 1993.
48. Kucheryavykh YV, Shuba YM, Antonov SM, Inyushin MY, Cubano L, Pearson WL, Kurata H, Reichenbach A, Veh RW, Nichols CG, Eaton MJ, Skatchkov SN. Complex rectification of Müller cell Kir currents. Glia 56: 775-790, 2008.
49. Lee KR, Drury I, Vitarbo E, Hoff JT. Seizures induced by intracerebral injection of thrombin: A model of intracerebral hemorrhage. J Neurosurg 87: 73-78, 1997.
50. + channel with a novel structure. EMBO J 15: 1004-1011, 1996.
51. Maggio N, Shavit E, Chapman J, Segal M. Thrombin induces long-term potentiation of reactivity to afferent stimulation and facilitates epileptic seizures in rat hippocampal slices: Toward understanding the functional consequences of cerebrovascular insults. J Neurosci 28: 732-736, 2008.
52. Marrero H, Astion ML, Coles JA, Orkand RK. Facilitation of voltage-gated ion channels in frog neuroglia by nerve impulses. Nature 339: 378-380, 1989.
53. Messori A, Polonara G, Carle F, Gesuita R, Salvolini U. Predicting posttraumatic epilepsy with MRI: Prospective longitudinal morphologic study in adults. Epilepsia 46: 1472-1481, 2005.
54. Nadal A, Fuentes E, Pastor J, McNaughton PA. Plasma albumin induces calcium waves in rat cortical astrocytes. Glia 19: 343-351, 1997.
55. + regulation. J Neurophysiol 95: 1843-1852, 2006.
56. Newman EA. Regional specialization of retinal glial cell membrane. Nature 309: 155-157, 1984.
57. + siphoning. Science 225: 1174-1175, 1984.
58. + buffering to cell differentiation. J Neurochem 107: 589-601, 2008.
59. Orkand RK, Nicholls JG, Kuffler SW. Effect of nerve impulses on the membrane potential of glial cells in the central nervous system of amphibia. J Neurophysiol 29: 788-806, 1966.
60. + channel. J Biol Chem 275: 28722-28730, 2000.
61. Pollen DA, Trachtenberg MC. Neuroglia: Gliosis and focal epilepsy. Science 167: 1252-1253, 1970.
62. + Channel density increases selectively in the endfoot of retinal glial cells during development of Rana catesbiana. Glia 25: 199-203, 1999.
63. Schröder W, Hinterkeuser S, Seifert G, Schramm J, Jabs R, Wilkin GP, Steinhäuser C. Functional and molecular properties of human astrocytes in acute hippocampal slices obtained from patients with temporal lobe epilepsy. Epilepsia 41 Suppl. 6: S181-S184, 2000.
64. Seiffert E, Dreier JP, Ivens S, Bechmann I, Tomkins O, Heinemann U, Friedman A. Lasting blood-brain barrier disruption induces epileptic focus in the rat somatosensory cortex. J Neurosci 24: 7829-7836, 2004.
65. + currents by tamoxifen. J Membr Biol 181: 125-135, 2001.
66. Soltys Z, Orzylowska-Sliwinska O, Zaremba M, Orlowski D, Piechota M, Fiedorowicz A, Janeczko K, Oderfeld-Nowak B. Quantitative morphological study of microglial cells in the ischemic rat brain using principal component analysis. J Neurosci Methods 146: 50-60, 2005.
67. Tanno H, Nockels RP, Pitts LH, Noble LJ. Breakdown of the blood-brain barrier after fluid percussive brain injury in the rat. Part 1. Distribution and time course of protein extravasation. J Neurotrauma 9: 21-32, 1992.
68. Temkin NR. Risk factors for posttraumatic seizures in adults. Epilepsia 44 Suppl. 10: 18-20, 2003.
69. Thompson HJ, Lifshitz J, Marklund N, Grady MS, Graham DI, Hovda DA, McIntosh TK. Lateral fluid percussion injury: A 15-year review and evaluation. J Neurotrauma 22: 42-75, 2005.
70. Thomzig A, Wenzel M, Karschin C, Eaton MJ, Skatchkov SN, Karschin A, Veh RW. Kir6.1 is the principal pore-forming subunit of astrocyte but not neuronal plasma membrane K-ATP channels. Mol Cell Neurosci 18: 671-690, 2001.
71. Uhlmann EJ, Wong M, Baldwin RL, Bajenaru ML, Onda H, Kwiatkowski DJ, Yamada K, Gutmann DH. Astrocyte-specific TSC1 conditional knockout mice exhibit abnormal neuronal organization and seizures. Ann Neurol 52: 285-296, 2002.
72. Verrecchia F, Herve J. Reversible inhibition of gap junctional communication by tamoxifen in cultured cardiac myocytes. Pfluegers 434: 113-116, 1997. (Pubitemid 27190441)
73. Zha XM, Green SH, Dailey ME. Regulation of hippocampal synapse remodeling by epileptiform activity. Mol Cell Neurosci 29: 494-506, 2005.