Contributions of astrocytes to epileptogenesis following status epilepticus: Opportunities for preventive therapy?

Neurochemistry International

Volumn 63, Issue 7, 2013, Pages 660-669

  Gibbons, M B ^a   Smeal, R M ^b   Takahashi, D K ^c   Vargas, J R ^a   Wilcox, K S ^a,b  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF UTAH   (United States)

^c STANFORD UNIVERSITY   (United States)

Author keywords

Epilepsy; Epileptogenesis; Gliosis; Inflammation; Reactive astrocyte; Review; Seizure; Status Epilepticus

Indexed keywords

ADENOSINE TRIPHOSPHATE; ANTICONVULSIVE AGENT; AQUAPORIN; BELNACASAN; CARBAMAZEPINE; CONNEXIN 43; CYTOKINE; FERROUS CHLORIDE; GAP JUNCTION PROTEIN; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMATE TRANSPORTER; GLUTAMIC ACID; INTERLEUKIN 1BETA; INTERMEDIATE FILAMENT PROTEIN; INWARDLY RECTIFYING POTASSIUM CHANNEL; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR4.1; ION CHANNEL; JANUS KINASE; KAINIC ACID; LIPOPOLYSACCHARIDE; NEUROTRANSMITTER RECEPTOR; PHENYTOIN; PILOCARPINE; POTASSIUM; REACTIVE OXYGEN METABOLITE; STAT PROTEIN; TETANUS TOXIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; UNINDEXED DRUG; VALPROIC ACID;

ALZHEIMER DISEASE; ANTICONVULSANT THERAPY; ASTROCYTE; ASTROCYTOSIS; BLOOD BRAIN BARRIER; BRAIN METABOLISM; BRAIN REGION; CALCIUM SIGNALING; CELL FUNCTION; CENTRAL NERVOUS SYSTEM; CEREBROVASCULAR ACCIDENT; COMPLEX PARTIAL SEIZURE; CYTOKINE PRODUCTION; DENSITOMETRY; DRUG TRANSPORT; ELECTROSTIMULATION; EPILEPTIC STATE; EPILEPTOGENESIS; EXCITOTOXICITY; GAP JUNCTION; GLIA CELL; GLIOSIS; HIPPOCAMPUS; HUMAN; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INFLAMMATION; LOW DRUG DOSE; MOLECULAR IMAGING; NERVE CELL EXCITABILITY; NERVE CELL NETWORK; NERVE FIBER DEGENERATION; NEUROPATHOLOGY; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; RODENT; SEIZURE; SIGNAL TRANSDUCTION; SYNAPSE; SYNAPTIC TRANSMISSION; TEMPORAL LOBE EPILEPSY; TISSUE SECTION; TRAUMATIC EPILEPSY; WESTERN BLOTTING;

ANIMALIA;

EPILEPSY; EPILEPTOGENESIS; GLIOSIS; INFLAMMATION; REACTIVE ASTROCYTE; REVIEW; SEIZURE; STATUS EPILEPTICUS;

ANTICONVULSANTS; ASTROCYTES; BLOOD-BRAIN BARRIER; CALCIUM SIGNALING; EPILEPSY; HUMANS; RECEPTORS, GLUTAMATE; STATUS EPILEPTICUS;

EID: 84888202767     PISSN: 01970186     EISSN: 18729754     Source Type: Journal    
DOI: 10.1016/j.neuint.2012.12.008     Document Type: Review

References (131)

1. F. Aguado, J.F. Espinosa-Parrilla, M.A. Carmona, and E. Soriano Neuronal activity regulates correlated network properties of spontaneous calcium transients in astrocytes in situ J. Neurosci. 22 2002 9430 9444 (Pubitemid 35356186)
2. A. Araque, R.P. Sanzgiri, V. Parpura, and P.G. Haydon Calcium elevation in astrocytes causes an NMDA receptor-dependent increase in the frequency of miniature synaptic currents in cultured hippocampal neurons J. Neurosci. 18 1998 6822 6829 (Pubitemid 28388013)
3. E. Aronica, T. Ravizza, E. Zurolo, and A. Vezzani Astrocyte immune responses in epilepsy Glia 60 2012 1258 1268
4. E. Aronica, E.A. van Vliet, O.A. Mayboroda, D. Troost, F.H. da Silva, and J.A. Gorter Upregulation of metabotropic glutamate receptor subtype mGluR3 and mGluR5 in reactive astrocytes in a rat model of mesial temporal lobe epilepsy Eur. J. Neurosci. 12 2000 2333 2344 (Pubitemid 30497031)
5. A.M. Benediktsson, G.S. Marrs, J.C. Tu, P.F. Worley, J.D. Rothstein, D.E. Bergles, and M.E. Dailey Neuronal activity regulates glutamate transporter dynamics in developing astrocytes Glia 60 2012 175 188
6. M. Bialer, and H.S. White Key factors in the discovery and development of new antiepileptic drugs Nat. Rev. Drug Discov. 9 2010 68 82
7. D.K. Binder, and C. Steinhauser Functional changes in astroglial cells in epilepsy Glia 54 2006 358 368 (Pubitemid 44422938)
8. L.P. Bjornsen, T. Eid, S. Holmseth, N.C. Danbolt, D.D. Spencer, and N.C. de Lanerolle Changes in glial glutamate transporters in human epileptogenic hippocampus: inadequate explanation for high extracellular glutamate during seizures Neurobiol. Dis. 25 2007 319 330 (Pubitemid 46124012)
9. D. Boison Adenosine and epilepsy: from therapeutic rationale to new therapeutic strategies Neuroscientist 11 2005 25 36 (Pubitemid 40223088)
10. A.V. Bumanglag, and R.S. Sloviter Minimal latency to hippocampal epileptogenesis and clinical epilepsy after perforant pathway stimulation-induced status epilepticus in awake rats J. Comp. Neurol. 510 2008 561 580
11. A.C. Charles, J.E. Merrill, E.R. Dirksen, and M.J. Sanderson Intercellular signaling in glial cells: calcium waves and oscillations in response to mechanical stimulation and glutamate Neuron 6 1991 983 992
12. F. Chen, and J. LoTurco A method for stable transgenesis of radial glia lineage in rat neocortex by piggyBac mediated transposition J. Neurosci. Methods 207 2012 172 180
13. F. Collignon, N.M. Wetjen, A.A. Cohen-Gadol, G.D. Cascino, J. Parisi, F.B. Meyer, W.R. Marsh, P. Roche, and S.D. Weigand Altered expression of connexin subtypes in mesial temporal lobe epilepsy in humans J. Neurosurg. 105 2006 77 87 (Pubitemid 43979101)
14. A.H. Cornell-Bell, S.M. Finkbeiner, M.S. Cooper, and S.J. Smith Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling Science 247 1990 470 473
15. G. Curia, D. Longo, G. Biagini, R.S. Jones, and M. Avoli The pilocarpine model of temporal lobe epilepsy J. Neurosci. Methods 172 2008 143 157
16. S. D'Antoni, A. Berretta, C.M. Bonaccorso, V. Bruno, E. Aronica, F. Nicoletti, and M.V. Catania Metabotropic glutamate receptors in glial cells Neurochem. Res. 33 2008 2436 2443
17. N.C. Danbolt Glutamate uptake Prog. Neurobiol. 65 2001 1 105 (Pubitemid 32479155)
18. M.G. De Simoni, C. Perego, T. Ravizza, D. Moneta, M. Conti, F. Marchesi, A. De Luigi, S. Garattini, and A. Vezzani Inflammatory cytokines and related genes are induced in the rat hippocampus by limbic status epilepticus Eur. J. Neurosci. 12 2000 2623 2633 (Pubitemid 30497055)
19. J.S. Diamond Deriving the glutamate clearance time course from transporter currents in CA1 hippocampal astrocytes: transmitter uptake gets faster during development J. Neurosci. 25 2005 2906 2916 (Pubitemid 40389248)
20. J.S. Diamond, and C.E. Jahr Synaptically released glutamate does not overwhelm transporters on hippocampal astrocytes during high-frequency stimulation J. Neurophysiol. 83 2000 2835 2843 (Pubitemid 30321474)
21. + in the transition from the interictal state to seizures Brain Res. 48 1972 173 183
22. 2+ signals contribute to neuronal excitotoxicity after status epilepticus J. Neurosci. 27 2007 10674 10684 (Pubitemid 47535867)
23. B. Djukic, K.B. Casper, B.D. Philpot, L.S. Chin, and K.D. McCarthy 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 2007 11354 11365 (Pubitemid 47621304)
24. A.L. do Nascimento, N.F. Dos Santos, F. Campos Pelagio, S. Aparecida Teixeira, E.A. de Moraes Ferrari, and F. Langone Neuronal degeneration and gliosis time-course in the mouse hippocampal formation after pilocarpine-induced status epilepticus Brain Res. 1470 2012 98 110
25. K. Elisevich, S.A. Rempel, B. Smith, and N. Allar Connexin 43 mRNA expression in two experimental models of epilepsy Mol. Chem. Neuropathol. 32 1997 75 88 (Sponsored by the International Society for Neurochemistry and the World Federation of Neurology and research groups on neurochemistry and cerebrospinal fluid) (Pubitemid 28028114)
26. K. Elisevich, S.A. Rempel, B.J. Smith, and K. Edvardsen Hippocampal connexin 43 expression in human complex partial seizure disorder Exp. Neurol. 145 1997 154 164 (Pubitemid 27244289)
27. J. Engel Jr. Clinical evidence for the progressive nature of epilepsy Epilepsy Res. 12 1996 9 20
28. D.E. Fedele, N. Gouder, M. Guttinger, L. Gabernet, L. Scheurer, T. Rulicke, F. Crestani, and D. Boison Astrogliosis in epilepsy leads to overexpression of adenosine kinase, resulting in seizure aggravation Brain 128 2005 2383 2395 (Pubitemid 41407977)
29. T. Fellin, O. Pascual, S. Gobbo, T. Pozzan, P.G. Haydon, and G. Carmignoto Neuronal synchrony mediated by astrocytic glutamate through activation of extrasynaptic NMDA receptors Neuron 43 2004 729 743 (Pubitemid 39179731)
30. I. Fernaud-Espinosa, M. Nieto-Sampedro, and P. Bovolenta Differential activation of microglia and astrocytes in aniso- and isomorphic gliotic tissue Glia 8 1993 277 291
31. F. Ferraguti, C. Corti, E. Valerio, S. Mion, and J. Xuereb Activated astrocytes in areas of kainate-induced neuronal injury upregulate the expression of the metabotropic glutamate receptors 2/3 and 5 Exp. Brain Res. 137 2001 1 11 (Pubitemid 32186610)
32. S. Finkbeiner Calcium waves in astrocytes-filling in the gaps Neuron 8 1992 1101 1108
33. C.G. Fonseca, C.R. Green, and L.F. Nicholson Upregulation in astrocytic connexin 43 gap junction levels may exacerbate generalized seizures in mesial temporal lobe epilepsy Brain Res. Mol. Brain Res. 929 2002 105 116 (Pubitemid 34164415)
34. S. Gabriel, A. Eilers, A. Kivi, R. Kovacs, K. Schulze, T.N. Lehmann, and U. Heinemann Effects of barium on stimulus induced changes in extracellular potassium concentration in area CA1 of hippocampal slices from normal and pilocarpine-treated epileptic rats Neurosci. Lett. 242 1998 9 12 (Pubitemid 28122696)
35. V. Garcia-Marin, P. Garcia-Lopez, and M. Freire Cajal's contributions to glia research Trends Neurosci. 30 2007 479 487 (Pubitemid 47374835)
36. Gee, J.M., Flood, K.P., Morris, S.C., Smeal, R.M., Economo, M.N., Capecchi, M.R., Tvrdik, P., Wilcox, K.S., White, J.A., 2011. A toolset for targeting GCaMP3 to cytosol, membrane or mitochondria with in utero electroporation. Society for Neuroscience Annual Meeting, vol. 709.02. Washington, DC.
37. O. Glushakova, A. Jeromin, J. Martinez, D. Johnson, N.D. Denslow, J. Streeter, R. Hayes, and S. Mondello CSF protein biomarker panel for assessment of neurotoxicity induced by kainic acid in rats Toxicol. Sci 130 2012 158 167
38. J.A. Gorter, E.A. van Vliet, E. Aronica, T. Breit, H. Rauwerda, F.H. Lopes da Silva, and W.J. Wadman Potential new antiepileptogenic targets indicated by microarray analysis in a rat model for temporal lobe epilepsy J. Neurosci. 26 2006 11083 11110 (Pubitemid 44772198)
39. M. Gottlieb, and C. Matute Expression of ionotropic glutamate receptor subunits in glial cells of the hippocampal CA1 area following transient forebrain ischemia J. Cereb. Blood Flow Metab. 17 1997 290 300 (Pubitemid 27161372)
40. N. Gouder, L. Scheurer, J.M. Fritschy, and D. Boison Overexpression of adenosine kinase in epileptic hippocampus contributes to epileptogenesis J. Neurosci. 24 2004 692 701 (Pubitemid 38166495)
41. M.M. Halassa, T. Fellin, and P.G. Haydon The tripartite synapse: roles for gliotransmission in health and disease Trends Mol. Med. 13 2007 54 63 (Pubitemid 46186152)
42. M.M. Halassa, and P.G. Haydon Integrated brain circuits: astrocytic networks modulate neuronal activity and behavior Annu. Rev. Physiol. 72 2010 335 355
43. K. Higashi, A. Fujita, A. Inanobe, M. Tanemoto, K. Doi, T. Kubo, and Y. Kurachi An inwardly rectifying K(+) channel, Kir4.1, expressed in astrocytes surrounds synapses and blood vessels in brain Am. J. Physiol. Cell Physiol. 281 2001 C922 931
44. S. Hinterkeuser, W. Schroder, G. Hager, G. Seifert, I. Blumcke, C.E. Elger, J. Schramm, and C. Steinhauser Astrocytes in the hippocampus of patients with temporal lobe epilepsy display changes in potassium conductances Eur. J. Neurosci. 12 2000 2087 2096 (Pubitemid 30348846)
45. D.W. Hochman The extracellular space and epileptic activity in the adult brain: explaining the antiepileptic effects of furosemide and bumetanide Epilepsia 53 Suppl. 1 2012 18 25
46. M.Z. Hossain, M.A. Sawchuk, L.J. Murphy, E.L. Hertzberg, and J.I. Nagy Kainic acid induced alterations in antibody recognition of connexin43 and loss of astrocytic gap junctions in rat brain Glia 10 1994 250 265 (Pubitemid 2077430)
47. S. Ivens, D. Kaufer, L.P. Flores, I. Bechmann, D. Zumsteg, O. Tomkins, E. Seiffert, U. Heinemann, and A. Friedman TGF-beta receptor-mediated albumin uptake into astrocytes is involved in neocortical epileptogenesis Brain 130 2007 535 547 (Pubitemid 46181106)
48. + currents in glial cells of mouse hippocampal slices Pflugers Arch. 426 1994 310 319
49. M. Kálmán Glia reaction and reactive glia Adv. Mol. Cell Biol. 31 2003 787 835
50. T. Kielian Glial connexins and gap junctions in CNS inflammation and disease J. Neurochem. 106 2008 1000 1016
51. H.K. Kimelberg Receptors on astrocytes: what possible functions? Neurochem. Int. 26 1995 27 40
52. +]o in human epileptic non-sclerotic and sclerotic hippocampal area CA1 Eur. J. Neurosci. 12 2000 2039 2048 (Pubitemid 30348841)
53. C. Krebs, H.B. Fernandes, C. Sheldon, L.A. Raymond, and K.G. Baimbridge Functional NMDA receptor subtype 2B is expressed in astrocytes after ischemia in vivo and anoxia in vitro J. Neurosci. 23 2003 3364 3372 (Pubitemid 36531978)
54. N. Kuga, T. Sasaki, Y. Takahara, N. Matsuki, and Y. Ikegaya Large-scale calcium waves traveling through astrocytic networks in vivo J. Neurosci. 31 2011 2607 2614
55. D.W. Laird, K.L. Puranam, and J.P. Revel Turnover and phosphorylation dynamics of connexin43 gap junction protein in cultured cardiac myocytes Biochem. J. 273 Pt 1 1991 67 72
56. U. Lalo, Y. Pankratov, V. Parpura, and A. Verkhratsky Ionotropic receptors in neuronal-astroglial signalling: what is the role of "excitable" molecules in non-excitable cells Biochim. Biophys. Acta 1813 2010 992 1002
57. F. Lauritzen, N.C. de Lanerolle, T.S. Lee, D.D. Spencer, J.H. Kim, L.H. Bergersen, and T. Eid Monocarboxylate transporter 1 is deficient on microvessels in the human epileptogenic hippocampus Neurobiol. Dis. 41 2011 577 584
58. F. Lauritzen, K. Heuser, N.C. de Lanerolle, T.S. Lee, D.D. Spencer, J.H. Kim, A. Gjedde, T. Eid, and L.H. Bergersen Redistribution of monocarboxylate transporter 2 on the surface of astrocytes in the human epileptogenic hippocampus Glia 60 2012 1172 1181
59. F. Lauritzen, E.L. Perez, E.R. Melillo, J.M. Roh, H.P. Zaveri, T.S. Lee, Y. Wang, L.H. Bergersen, and T. Eid Altered expression of brain monocarboxylate transporter 1 in models of temporal lobe epilepsy Neurobiol. Dis. 45 2012 165 176
60. D.J. Lee, M.S. Hsu, M.M. Seldin, J.L. Arellano, and D.K. Binder Decreased expression of the glial water channel aquaporin-4 in the intrahippocampal kainic acid model of epileptogenesis Exp. Neurol. 235 2012 246 255
61. S.H. Lee, S. Magge, D.D. Spencer, H. Sontheimer, and A.H. Cornell-Bell Human epileptic astrocytes exhibit increased gap junction coupling Glia 15 1995 195 202
62. M.J. Lehmkuhle, K.E. Thomson, P. Scheerlinck, W. Pouliot, B. Greger, and F.E. Dudek A simple quantitative method for analyzing electrographic status epilepticus in rats J. Neurophysiol. 101 2009 1660 1670
63. K.P. Lehre, L.M. Levy, O.P. Ottersen, J. Storm-Mathisen, and N.C. Danbolt Differential expression of two glial glutamate transporters in the rat brain: quantitative and immunocytochemical observations J. Neurosci. 15 1995 1835 1853
64. T. Li, G. Ren, T. Lusardi, A. Wilz, J.Q. Lan, T. Iwasato, S. Itohara, R.P. Simon, and D. Boison Adenosine kinase is a target for the prediction and prevention of epileptogenesis in mice J. Clin. Invest. 118 2008 571 582 (Pubitemid 351206547)
65. W. Loscher Drug transporters in the epileptic brain Epilepsia 48 Suppl. 1 2007 8 13 (Pubitemid 46280513)
66. W. Loscher, and H. Potschka Drug resistance in brain diseases and the role of drug efflux transporters Nat. Rev. Neurosci. 6 2005 591 602 (Pubitemid 41059334)
67. J. LoTurco, J.B. Manent, and F. Sidiqi New and improved tools for in utero electroporation studies of developing cerebral cortex Cereb. Cortex 19 Suppl. 1 2009 i120 125
68. D.H. Lowenstein, T. Bleck, and R.L. Macdonald It's time to revise the definition of status epilepticus Epilepsia 40 1999 120 122 (Pubitemid 29031765)
69. I.V. Lund, Y. Hu, Y.H. Raol, R.S. Benham, R. Faris, S.J. Russek, and A.R. Brooks-Kayal BDNF selectively regulates GABAA receptor transcription by activation of the JAK/STAT pathway Sci. Signal. 1 2008 ra9
70. P. Marcaggi, and D. Attwell Role of glial amino acid transporters in synaptic transmission and brain energetics Glia 47 2004 217 225 (Pubitemid 39121066)
71. G.W. Mathern, D. Mendoza, A. Lozada, J.K. Pretorius, Y. Dehnes, N.C. Danbolt, N. Nelson, J.P. Leite, L. Chimelli, D.E. Born, A.C. Sakamoto, J.A. Assirati, I. Fried, W.J. Peacock, G.A. Ojemann, and P.D. Adelson Hippocampal GABA and glutamate transporter immunoreactivity in patients with temporal lobe epilepsy Neurology 52 1999 453 472 (Pubitemid 29075589)
72. Y. Murabe, Y. Ibata, and Y. Sano Morphological studies on neuroglia. IV. Proliferative response of non-neuronal elements in the hippocampus of the rat to kainic acid-induced lesions Cell Tissue Res. 222 1982 223 226 (Pubitemid 12134198)
73. A. Nadal, E. Fuentes, J. Pastor, and P.A. McNaughton Plasma albumin is a potent trigger of calcium signals and DNA synthesis in astrocytes Proc. Natl. Acad. Sci. USA 92 1995 1426 1430
74. J.I. Nagy, and J.E. Rash Connexins and gap junctions of astrocytes and oligodendrocytes in the CNS Brain Res. Brain Res. Rev. 32 2000 29 44 (Pubitemid 30177308)
75. T. Nakase, and C.C. Naus Gap junctions and neurological disorders of the central nervous system Biochim. Biophys. Acta 1662 2004 149 158 (Pubitemid 38372103)
76. C.C. Naus, J.F. Bechberger, and D.L. Paul Gap junction gene expression in human seizure disorder Exp. Neurol. 111 1991 198 203
77. C. Nicholson, and E. Sykova Extracellular space structure revealed by diffusion analysis Trends Neurosci. 21 1998 207 215 (Pubitemid 28191815)
78. J. Niquet, Y. Ben-Ari, and A. Represa Glial reaction after seizure induced hippocampal lesion: immunohistochemical characterization of proliferating glial cells J. Neurocytol. 23 1994 641 656 (Pubitemid 24375924)
79. B.A. Norwood, A.V. Bumanglag, F. Osculati, A. Sbarbati, P. Marzola, E. Nicolato, P.F. Fabene, and R.S. Sloviter Classic hippocampal sclerosis and hippocampal-onset epilepsy produced by a single "cryptic" episode of focal hippocampal excitation in awake rats J. Comp. Neurol. 518 2010 3381 3407
80. R.G. Notenboom, D.R. Hampson, G.H. Jansen, P.C. van Rijen, C.W. van Veelen, O. van Nieuwenhuizen, and P.N. de Graan Up-regulation of hippocampal metabotropic glutamate receptor 5 in temporal lobe epilepsy patients Brain 129 2006 96 107 (Pubitemid 43063762)
81. N.A. Oberheim, T. Takano, X. Han, W. He, J.H. Lin, F. Wang, Q. Xu, J.D. Wyatt, W. Pilcher, J.G. Ojemann, B.R. Ransom, S.A. Goldman, and M. Nedergaard Uniquely hominid features of adult human astrocytes J. Neurosci. 29 2009 3276 3287
82. N.A. Oberheim, G.F. Tian, X. Han, W. Peng, T. Takano, B. Ransom, and M. Nedergaard Loss of astrocytic domain organization in the epileptic brain J. Neurosci. 28 2008 3264 3276 (Pubitemid 351469330)
83. P.I. Ortinski, J. Dong, A. Mungenast, C. Yue, H. Takano, D.J. Watson, P.G. Haydon, and D.A. Coulter Selective induction of astrocytic gliosis generates deficits in neuronal inhibition Nat. Neurosci. 13 2010 584 591
84. U. Pannasch, L. Vargova, J. Reingruber, P. Ezan, D. Holcman, C. Giaume, E. Sykova, and N. Rouach Astroglial networks scale synaptic activity and plasticity Proc. Natl. Acad. Sci. USA 108 2011 8467 8472
85. V. Parpura, and P.G. Haydon Physiological astrocytic calcium levels stimulate glutamate release to modulate adjacent neurons Proc. Natl. Acad. Sci. USA 97 2000 8629 8634 (Pubitemid 30639724)
86. L. Pasti, A. Volterra, T. Pozzan, and G. Carmignoto Intracellular calcium oscillations in astrocytes: a highly plastic, bidirectional form of communication between neurons and astrocytes in situ J. Neurosci. 17 1997 7817 7830 (Pubitemid 27426219)
87. + channels via phospholipase C and protein kinase C-delta in reactive astrocytes from adult rat brain J. Biol. Chem. 277 2002 1974 1980 (Pubitemid 34968777)
88. Z.A. Peterlin, J. Kozloski, B.Q. Mao, A. Tsiola, and R. Yuste Optical probing of neuronal circuits with calcium indicators Proc. Natl. Acad. Sci. USA 97 2000 3619 3624 (Pubitemid 30183352)
89. O. Peters, C.G. Schipke, A. Philipps, B. Haas, U. Pannasch, L.P. Wang, B. Benedetti, A.E. Kingston, and H. Kettenmann Astrocyte function is modified by Alzheimer's disease-like pathology in aged mice J. Alzheimers Dis. 18 2009 177 189
90. S. Poopalasundaram, C. Knott, O.G. Shamotienko, P.G. Foran, J.O. Dolly, C.A. Ghiani, V. Gallo, and G.P. Wilkin Glial heterogeneity in expression of the inwardly rectifying K(+) channel, Kir4.1, in adult rat CNS Glia 30 2000 362 372 (Pubitemid 30334337)
91. E.A. Proper, G. Hoogland, S.M. Kappen, G.H. Jansen, M.G. Rensen, L.H. Schrama, C.W. van Veelen, P.C. van Rijen, O. van Nieuwenhuizen, W.H. Gispen, and P.N. de Graan Distribution of glutamate transporters in the hippocampus of patients with pharmaco-resistant temporal lobe epilepsy Brain 125 2002 32 43 (Pubitemid 34084035)
92. Y.H. Raol, I.V. Lund, S. Bandyopadhyay, G. Zhang, D.S. Roberts, J.H. Wolfe, S.J. Russek, and A.R. Brooks-Kayal 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 2006 11342 11346 (Pubitemid 44772163)
93. J.E. Rash, T. Yasumura, K.G. Davidson, C.S. Furman, F.E. Dudek, and J.I. Nagy Identification of cells expressing Cx43, Cx30, Cx26, Cx32 and Cx36 in gap junctions of rat brain and spinal cord Cell Commun. Adhes. 8 2001 315 320
94. T. Ravizza, F. Noe, D. Zardoni, V. Vaghi, M. Sifringer, and A. Vezzani Interleukin converting enzyme inhibition impairs kindling epileptogenesis in rats by blocking astrocytic IL-1beta production Neurobiol. Dis. 31 2008 327 333
95. A.M. Reeves, E. Shigetomi, and B.S. Khakh Bulk loading of calcium indicator dyes to study astrocyte physiology: key limitations and improvements using morphological maps J. Neurosci. 31 2011 9353 9358
96. J.L. Ridet, S.K. Malhotra, A. Privat, and F.H. Gage Reactive astrocytes: cellular and molecular cues to biological function Trends Neurosci. 20 1997 570 577 (Pubitemid 27508969)
97. M.B. Robinson Regulated trafficking of neurotransmitter transporters: common notes but different melodies J. Neurochem. 80 2002 1 11 (Pubitemid 34614572)
98. N. Rouach, A. Koulakoff, V. Abudara, K. Willecke, and C. Giaume Astroglial metabolic networks sustain hippocampal synaptic transmission Science 322 2008 1551 1555
99. S. Sarac, S. Afzal, H. Broholm, F.F. Madsen, T. Ploug, and H. Laursen Excitatory amino acid transporters EAAT-1 and EAAT-2 in temporal lobe and hippocampus in intractable temporal lobe epilepsy APMIS 117 2009 291 301
100. + channels in astrocytes of mouse hippocampus Mol. Cell. Neurosci. 19 2002 447 458 (Pubitemid 34293465)
101. G. Seifert, K. Huttmann, J. Schramm, and C. Steinhauser Enhanced relative expression of glutamate receptor 1 flip AMPA receptor subunits in hippocampal astrocytes of epilepsy patients with Ammon's horn sclerosis J. Neurosci. 24 2004 1996 2003 (Pubitemid 38292813)
102. G. Seifert, L. Rehn, M. Weber, and C. Steinhauser AMPA receptor subunits expressed by single astrocytes in the juvenile mouse hippocampus Brain Res. Mol. Brain Res. 47 1997 286 294 (Pubitemid 27284486)
103. A. Serrano, R. Robitaille, and J.C. Lacaille Differential NMDA-dependent activation of glial cells in mouse hippocampus Glia 56 2008 1648 1663
104. E. Shigetomi, D.N. Bowser, M.V. Sofroniew, and B.S. Khakh Two forms of astrocyte calcium excitability have distinct effects on NMDA receptor-mediated slow inward currents in pyramidal neurons J. Neurosci. 28 2008 6659 6663
105. E. Shigetomi, S. Kracun, and B.S. Khakh Monitoring astrocyte calcium microdomains with improved membrane targeted GCaMP reporters Neuron Glia Biol. 2011 1 9
106. Smeal, R.M., Economo, M.N., Lillis, K.P., Wilcox, K.S., White, J.A., in press. Targeted path scanning: an emerging method for recording fast changing network dynamics across large distances. J. Bioeng. Biomed. Sci.
107. M.V. Sofroniew Molecular dissection of reactive astrogliosis and glial scar formation Trends Neurosci. 32 2009 638 647
108. G. Sohl, M. Guldenagel, H. Beck, B. Teubner, O. Traub, R. Gutierrez, U. Heinemann, and K. Willecke Expression of connexin genes in hippocampus of kainate-treated and kindled rats under conditions of experimental epilepsy Brain Res. Mol. Brain Res. 83 2000 44 51
109. G.G. Somjen Nervenkitt: notes on the history of the concept of neuroglia Glia 1 1988 2 9
110. C. Steinhauser, R. Jabs, and H. Kettenmann Properties of GABA and glutamate responses in identified glial cells of the mouse hippocampal slice Hippocampus 4 1994 19 35 (Pubitemid 24168377)
111. D.K. Takahashi, J.R. Vargas, and K.S. Wilcox Increased coupling and altered glutamate transport currents in astrocytes following kainic-acid-induced status epilepticus Neurobiol. Dis. 40 2010 573 585
112. K. Tanaka, K. Watase, T. Manabe, K. Yamada, M. Watanabe, K. Takahashi, H. Iwama, T. Nishikawa, N. Ichihara, T. Kikuchi, S. Okuyama, N. Kawashima, S. Hori, M. Takimoto, and K. Wada Epilepsy and exacerbation of brain injury in mice lacking the glutamate transporter GLT-1 Science 276 1997 1699 1702 (Pubitemid 27421977)
113. S. Tessler, N.C. Danbolt, R.L. Faull, J. Storm-Mathisen, and P.C. Emson Expression of the glutamate transporters in human temporal lobe epilepsy Neuroscience 88 1999 1083 1091 (Pubitemid 28546991)
114. M. Theis, R. Jauch, L. Zhuo, D. Speidel, A. Wallraff, B. Doring, C. Frisch, G. Sohl, B. Teubner, C. Euwens, J. Huston, C. Steinhauser, A. Messing, U. Heinemann, and K. Willecke Accelerated hippocampal spreading depression and enhanced locomotory activity in mice with astrocyte-directed inactivation of connexin43 J. Neurosci. 23 2003 766 776 (Pubitemid 36206167)
115. M. Theis, G. Sohl, J. Eiberger, and K. Willecke Emerging complexities in identity and function of glial connexins Trends Neurosci. 28 2005 188 195 (Pubitemid 40445525)
116. P. Theofilas, S. Brar, K.A. Stewart, H.Y. Shen, U.S. Sandau, D. Poulsen, and D. Boison Adenosine kinase as a target for therapeutic antisense strategies in epilepsy Epilepsia 52 2011 589 601
117. C.G. Thomas, H. Tian, and J.S. Diamond The relative roles of diffusion and uptake in clearing synaptically released glutamate change during early postnatal development J. Neurosci. 31 2011 4743 4754
118. A.V. Tzingounis, and J.I. Wadiche Glutamate transporters: confining runaway excitation by shaping synaptic transmission Nat. Rev. Neurosci. 8 2007 935 947 (Pubitemid 350146934)
119. Y. Ueda, T. Doi, J. Tokumaru, H. Yokoyama, A. Nakajima, Y. Mitsuyama, H. Ohya-Nishiguchi, H. Kamada, and L.J. Willmore Collapse of extracellular glutamate regulation during epileptogenesis: down-regulation and functional failure of glutamate transporter function in rats with chronic seizures induced by kainic acid J. Neurochem. 76 2001 892 900 (Pubitemid 32126089)
120. J. Ulas, T. Satou, K.J. Ivins, J.P. Kesslak, C.W. Cotman, and R. Balazs Expression of metabotropic glutamate receptor 5 is increased in astrocytes after kainate-induced epileptic seizures Glia 30 2000 352 361 (Pubitemid 30334336)
121. E.A. van Vliet, S. da Costa Araujo, S. Redeker, R. van Schaik, E. Aronica, and J.A. Gorter Blood-brain barrier leakage may lead to progression of temporal lobe epilepsy Brain 130 2007 521 534 (Pubitemid 46181105)
122. E.A. van Vliet, S. Redeker, E. Aronica, P.M. Edelbroek, and J.A. Gorter Expression of multidrug transporters MRP1, MRP2, and BCRP shortly after status epilepticus, during the latent period, and in chronic epileptic rats Epilepsia 46 2005 1569 1580 (Pubitemid 44921930)
123. Vargas, J.R., Takahashi, D.K., Wilcox, K.S., 2006. Kainate Receptor Expression in Astrocytes in a Model of Temporal Lobe Epilepsy Society for Neuroscience Annual Meeting, Atlanta, GA.
124. A. Verkhratsky Patching the glia reveals the functional organisation of the brain Pflugers Arch. 453 2006 411 420 (Pubitemid 44764242)
125. A. Vezzani, J. French, T. Bartfai, and T.Z. Baram The role of inflammation in epilepsy Nat. Rev. Neurol. 7 2011 31 40
126. L.P. Wang, G. Cheung, G. Kronenberg, K. Gertz, S. Ji, G. Kempermann, M. Endres, and H. Kettenmann Mild brain ischemia induces unique physiological properties in striatal astrocytes Glia 56 2008 925 934
127. H.S. White, M.D. Smith, and K.S. Wilcox Mechanisms of action of antiepileptic drugs Int. Rev. Neurobiol. 81 2007 85 110
128. U. Wilhelmsson, E.A. Bushong, D.L. Price, B.L. Smarr, V. Phung, M. Terada, M.H. Ellisman, and M. Pekny Redefining the concept of reactive astrocytes as cells that remain within their unique domains upon reaction to injury Proc. Natl. Acad. Sci. USA 103 2006 17513 17518 (Pubitemid 44789000)
129. P.A. Williams, A.M. White, S. Clark, D.J. Ferraro, W. Swiercz, K.J. Staley, and F.E. Dudek Development of spontaneous recurrent seizures after kainate-induced status epilepticus J. Neurosci. 29 2009 2103 2112
130. I.R. Winship, N. Plaa, and T.H. Murphy Rapid astrocyte calcium signals correlate with neuronal activity and onset of the hemodynamic response in vivo J. Neurosci. 27 2007 6268 6272 (Pubitemid 46890012)
131. J.L. Zamanian, L. Xu, L.C. Foo, N. Nouri, L. Zhou, R.G. Giffard, and B.A. Barres Genomic analysis of reactive astrogliosis J. Neurosci. 32 2012 6391 6410