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Neural Plasticity
Volume 2011 (2011), Article ID 527605, 16 pages
doi:10.1155/2011/527605
Review Article

Altered GABA Signaling in Early Life Epilepsies

Stephen W. Briggs and Aristea S. Galanopoulou

Saul R. Korey Department of Neurology, Dominick P. Purpura Department of Neuroscience, Albert Einstein College of Medicine, 1410 Pelham Parkway South, Kennedy Center Rm 306, Bronx, NY 10461, USA

Received 7 February 2011; Revised 4 May 2011; Accepted 27 May 2011

Academic Editor: Laura Cancedda

Copyright © 2011 Stephen W. Briggs and Aristea S. Galanopoulou. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. T. Berg, S. F. Berkovic, M. J. Brodie et al., “Revised terminology and concepts for organization of seizures and epilepsies: report of the ILAE Commission on Classification and Terminology, 2005–2009,” Epilepsia, vol. 51, no. 4, pp. 676–685, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  2. R. S. Fisher, W. van Emde Boas, W. Blume et al., “Epileptic seizures and epilepsy: definitions proposed by the International League Against Epilepsy (ILAE) and the International Bureau for Epilepsy (IBE),” Epilepsia, vol. 46, no. 4, pp. 470–472, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  3. W. A. Hauser, J. F. Annegers, and L. T. Kurland, “Incidence of epilepsy and unprovoked seizures in Rochester, Minnesota: 1935–1984,” Epilepsia, vol. 34, no. 3, pp. 453–468, 1993. View at Scopus
  4. I. A. W. Kotsopoulos, T. van Merode, F. G. H. Kessels, M. C. T. F. M. de Krom, and J. A. Knottnerus, “Systematic review and meta-analysis of incidence studies of epilepsy and unprovoked seizures,” Epilepsia, vol. 43, no. 11, pp. 1402–1409, 2002. View at Publisher · View at Google Scholar · View at Scopus
  5. A. S. Galanopoulou, J. Vidaurre, and S. L. Moshé, “Under what circumstances can seizures produce hippocampal injury: evidence for age-specific effects,” Developmental Neuroscience, vol. 24, no. 5, pp. 355–363, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  6. F. Pisani, C. Cerminara, C. Fusco, and L. Sisti, “Neonatal status epilepticus vs recurrent neonatal seizures: clinical findings and outcome,” Neurology, vol. 69, no. 23, pp. 2177–2185, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  7. C. L. Padgett and P. A. Slesinger, “GABAB receptor coupling to G-proteins and ion channels,” Advances in Pharmacology, vol. 57, pp. 123–147, 2010. View at Publisher · View at Google Scholar · View at Scopus
  8. K. M. McClellan, A. R. Calver, and S. A. Tobet, “GABAB receptors role in cell migration and positioning within the ventromedial nucleus of the hypothalamus,” Neuroscience, vol. 151, no. 4, pp. 1119–1131, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  9. J. H. White, R. A. J. McIllhinney, A. Wise et al., “The GABAB receptor interacts directly with the related transcription factors CREB2 and ATFx,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 25, pp. 13967–13972, 2000. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  10. R. B. Nehring, H. P. M. Horikawa, O. El Far et al., “The metabotropic GABAB receptor directly interacts with the activating transcription factor 4,” Journal of Biological Chemistry, vol. 275, no. 45, pp. 35185–35191, 2000. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  11. A. S. Galanopoulou, “GABAA receptors in normal development and seizures: friends or foes?” Current Neuropharmacology, vol. 6, no. 1, pp. 1–20, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  12. M. Farrant and K. Kaila, “The cellular, molecular and ionic basis of GABAA receptor signalling,” Progress in Brain Research, vol. 160, pp. 59–87, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  13. R. W. Olsen and G. D. Li, “GABAA receptors as molecular targets of general anesthetics: identification of binding sites provides clues to allosteric modulation,” Canadian Journal of Anesthesia, pp. 1–10, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  14. P. Blaesse, M. S. Airaksinen, C. Rivera, and K. Kaila, “Cation-chloride cotransporters and neuronal function,” Neuron, vol. 61, no. 6, pp. 820–838, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  15. J. M. Russell, “Sodium-potassium-chloride cotransport,” Physiological Reviews, vol. 80, no. 1, pp. 211–276, 2000. View at Scopus
  16. M. D. Plotkin, E. Y. Snyder, S. C. Hebert, and E. Delpire, “Expression of the Na-K-2Cl cotransporter is developmentally regulated in postnatal rat brains: a possible mechanism underlying GABA's excitatory role in immature brain,” Journal of Neurobiology, vol. 33, no. 6, pp. 781–795, 1997. View at Publisher · View at Google Scholar · View at Scopus
  17. Y. Ben-Ari, E. Cherubini, R. Corradetti, and J. L. Gaiarsa, “Giant synaptic potentials in immature rat CA3 hippocampal neurones,” Journal of Physiology, vol. 416, pp. 303–325, 1989. View at Scopus
  18. X. Leinekugel, I. Khalilov, H. McLean et al., “GABA is the principal fast-acting excitatory transmitter in the neonatal brain,” Advances in Neurology, vol. 79, pp. 189–201, 1999. View at Scopus
  19. C. Rivera, J. Voipio, J. A. Payne et al., “The K+/Cl− co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation,” Nature, vol. 397, no. 6716, pp. 251–255, 1999. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  20. L. A. Jansen, L. D. Peugh, W. H. Roden, and J. G. Ojemann, “Impaired maturation of cortical GABAA receptor expression in pediatric epilepsy,” Epilepsia, vol. 51, no. 8, pp. 1456–1467, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  21. V. I. Dzhala, D. M. Talos, D. A. Sdrulla et al., “NKCC1 transporter facilitates seizures in the developing brain,” Nature Medicine, vol. 11, no. 11, pp. 1205–1213, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  22. C. Wang, C. Shimizu-Okabe, K. Watanabe et al., “Developmental changes in KCC1, KCC2, and NKCC1 mRNA expressions in the rat brain,” Developmental Brain Research, vol. 139, no. 1, pp. 59–66, 2002. View at Publisher · View at Google Scholar · View at Scopus
  23. V. Stein, I. Hermans-Borgmeyer, T. J. Jentsch, and C. A. Hübner, “Expression of the KCl cotransporter KCC2 parallels neuronal maturation and the emergence of low intracellular chloride,” Journal of Comparative Neurology, vol. 468, no. 1, pp. 57–64, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  24. K. Kaila, J. Voipio, P. Paalasmaa, M. Pasternack, and R. A. Deisz, “The role of bicarbonate in GABAA receptor-mediated IPSPs of rat neocortical neurones,” Journal of Physiology, vol. 464, pp. 273–289, 1993. View at Scopus
  25. C. Rivera, J. Voipio, and K. Kaila, “Two developmental switches in GABAergic signalling: the K+-Cl− cotransporter KCC2 and carbonic anhydrase CAVII,” Journal of Physiology, vol. 562, no. 1, pp. 27–36, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  26. E. Ruusuvuori, H. Li, K. Huttu et al., “Carbonic anhydrase isoform VII acts as a molecular switch in the development of synchronous gamma-frequency firing of hippocampal CA1 pyramidal cells,” Journal of Neuroscience, vol. 24, no. 11, pp. 2699–2707, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  27. M. H. Scantlebury, A. S. Galanopoulou, L. Chudomelova, E. Raffo, D. Betancourth, and S. L. Moshé, “A model of symptomatic infantile spasms syndrome,” Neurobiology of Disease, vol. 37, no. 3, pp. 604–612, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  28. S. Vanhatalo, J. Matias Palva, S. Andersson, C. Rivera, J. Voipio, and K. Kaila, “Slow endogenous activity transients and developmental expression of K+-Cl− cotransporter 2 in the immature human cortex,” European Journal of Neuroscience, vol. 22, no. 11, pp. 2799–2804, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  29. A. S. Galanopoulou, “Sexually dimorphic expression of KCC2 and GABA function,” Epilepsy Research, vol. 80, no. 2-3, pp. 99–113, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  30. A. S. Galanopoulou, “Dissociated gender-specific effects of recurrent seizures on GABA signaling in CA1 pyramidal neurons: role of GABAA receptors,” Journal of Neuroscience, vol. 28, no. 7, pp. 1557–1567, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  31. A. S. Galanopoulou, A. Kyrozis, O. I. Claudio, P. K. Stanton, and S. L. Moshé, “Sex-specific KCC2 expression and GABAA receptor function in rat substantia nigra,” Experimental Neurology, vol. 183, no. 2, pp. 628–637, 2003. View at Publisher · View at Google Scholar · View at Scopus
  32. J. L. Nuñez and M. M. McCarthy, “Evidence for an extended duration of GABA-mediated excitation in the developing male versus female hippocampus,” Developmental Neurobiology, vol. 67, no. 14, pp. 1879–1890, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  33. Y. Ben-Ari, “Excitatory actions of GABA during development: the nature of the nurture,” Nature Reviews Neuroscience, vol. 3, no. 9, pp. 728–739, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  34. M. A. Montenegro, M. M. Guerreiro, J. P. S. Caldas, M. V. L. Moura-Ribeiro, and C. A. M. Guerreiro, “Epileptic manifestations induced by midazolam in the neonatal period,” Arquivos de Neuro-Psiquiatria, vol. 59, no. 2A, pp. 242–243, 2001. View at Scopus
  35. J. Connell, R. Oozeer, L. de Vries, L. M. S. Dubowitz, and V. Dubowitz, “Clinical and EEG response to anticonvulsants in neonatal seizures,” Archives of Disease in Childhood, vol. 64, no. 4, pp. 459–464, 1989. View at Scopus
  36. D. Booth and D. J. Evans, “Anticonvulsants for neonates with seizures,” Cochrane Database of Systematic Reviews, no. 4, Article ID CD004218, 2004. View at Scopus
  37. C. Chiron, O. Dulac, D. Beaumont, L. Palacios, N. Pajot, and J. Mumford, “Therapeutic trial of vigabatrin in refractory infantile spasms,” Journal of Child Neurology, vol. 6, no. 2, pp. S52–S59, 1991. View at Scopus
  38. A. L. Lux, S. W. Edwards, E. Hancock et al., “The United Kingdom Infantile Spasms Study (UKISS) comparing hormone treatment with vigabatrin on developmental and epilepsy outcomes to age 14 months: a multicentre randomised trial,” The Lancet Neurology, vol. 4, no. 11, pp. 712–717, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  39. V. I. Dzhala, A. C. Brumback, and K. J. Staley, “Bumetanide enhances phenobarbital efficacy in a neonatal seizure model,” Annals of Neurology, vol. 63, no. 2, pp. 222–235, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  40. K. Staley, “Enhancement of the excitatory actions of GABA by barbiturates and benzodiazepines,” Neuroscience Letters, vol. 146, no. 1, pp. 105–107, 1992. View at Publisher · View at Google Scholar · View at Scopus
  41. J. M. Fritschy, J. Paysan, A. Enna, and H. Mohler, “Switch in the expression of rat GABAA-receptor subtypes during postnatal development: an immunohistochemical study,” Journal of Neuroscience, vol. 14, no. 9, pp. 5302–5324, 1994. View at Scopus
  42. O. Chudomel, H. Herman, K. Nair, S. L. Moshé, and A. S. Galanopoulou, “Age- and gender-related differences in GABAA receptor-mediated postsynaptic currents in GABAergic neurons of the substantia nigra reticulata in the rat,” Neuroscience, vol. 163, no. 1, pp. 155–167, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  43. S. L. Moshé, E. F. Sperber, L. L. Brown, and A. Tempel, “Age-dependent changes in substantia nigra GABA-mediated seizure suppression,” Epilepsy Research. Supplement, vol. 8, pp. 97–106, 1992. View at Scopus
  44. J. Velikova and S. L. Moshe, “Sexual dimorphism and developmental regulation of substantia nigra function,” Annals of Neurology, vol. 50, no. 5, pp. 596–601, 2001. View at Publisher · View at Google Scholar · View at Scopus
  45. E. F. Sperber, J. Velísková, I. M. Germano, L. K. Friedman, and S. L. Moshé, “Age-dependent vulnerability to seizures,” Advances in Neurology, vol. 79, pp. 161–169, 1999.
  46. A. Kyrozis, O. Chudomel, S. L. Moshé, and A. S. Galanopoulou, “Sex-dependent maturation of GABAA receptor-mediated synaptic events in rat substantia nigra reticulata,” Neuroscience Letters, vol. 398, no. 1-2, pp. 1–5, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  47. P. Cossette, L. Liu, K. Brisebois et al., “Mutation of GABRA1 in an autosomal dominant form of juvenile myoclonic epilepsy,” Nature Genetics, vol. 31, no. 2, pp. 184–189, 2002. View at Publisher · View at Google Scholar · View at PubMed
  48. L. Ding, H. J. Feng, R. L. Macdonald, E. J. Botzolakis, N. Hu, and M. J. Gallagher, “GABAA receptor α1 subunit mutation A322D associated with autosomal dominant juvenile myoclonic epilepsy reduces the expression and alters the composition of wild type GABAA receptors,” Journal of Biological Chemistry, vol. 285, no. 34, pp. 26390–26405, 2010. View at Publisher · View at Google Scholar · View at PubMed
  49. L. M. Dibbens, L. A. Harkin, M. Richards et al., “The role of neuronal GABAA receptor subunit mutations in idiopathic generalized epilepsies,” Neuroscience Letters, vol. 453, no. 3, pp. 162–165, 2009. View at Publisher · View at Google Scholar · View at PubMed
  50. L. Urak, M. Feucht, N. Fathi, K. Hornik, and K. Fuchs, “A GABRB3 promoter haplotype associated with childhood absence epilepsy impairs transcriptional activity,” Human Molecular Genetics, vol. 15, no. 16, pp. 2533–2541, 2006. View at Publisher · View at Google Scholar · View at PubMed
  51. M. Feucht, K. Fuchs, E. Pichlbauer et al., “Possible association between childhood absence epilepsy and the gene encoding GABRB3,” Biological Psychiatry, vol. 46, no. 7, pp. 997–1002, 1999. View at Publisher · View at Google Scholar
  52. M. Tanaka, R. W. Olsen, M. T. Medina et al., “Hyperglycosylation and reduced GABA currents of mutated GABRB3 polypeptide in remitting childhood absence epilepsy,” American Journal of Human Genetics, vol. 82, no. 6, pp. 1249–1261, 2008. View at Publisher · View at Google Scholar · View at PubMed
  53. L. M. Dibbens, H. J. Feng, M. C. Richards et al., “GABRD encoding a protein for extra- or peri-synaptic GABAA receptors is susceptibility locus for generalized epilepsies,” Human Molecular Genetics, vol. 13, no. 13, pp. 1315–1319, 2004. View at Publisher · View at Google Scholar · View at PubMed
  54. S. Baulac, G. Huberfeld, I. Gourfinkel-An et al., “First genetic evidence of GABAA receptor dysfunction in epilepsy: a mutation in the γ2-subunit gene,” Nature Genetics, vol. 28, no. 1, pp. 46–48, 2001. View at Publisher · View at Google Scholar · View at PubMed
  55. H. Sun, Y. Zhang, J. Liang et al., “SCN1A, SCN1B, and GABRG2 gene mutation analysis in Chinese families with generalized epilepsy with febrile seizures plus,” Journal of Human Genetics, vol. 53, no. 8, pp. 769–774, 2008. View at Publisher · View at Google Scholar · View at PubMed
  56. L. A. Harkin, D. N. Bowser, L. M. Dibbens et al., “Truncation of the GABAA-receptor γ2 subunit in a family with generalized epilepsy with febrile seizures plus,” American Journal of Human Genetics, vol. 70, no. 2, pp. 530–536, 2002. View at Publisher · View at Google Scholar · View at PubMed
  57. J. Q. Kang, W. Shen, and R. L. Macdonald, “The GABRG2 mutation, Q351X, associated with generalized epilepsy with febrile seizures plus, has both loss of function and dominant-negative suppression,” Journal of Neuroscience, vol. 29, no. 9, pp. 2845–2856, 2009. View at Publisher · View at Google Scholar · View at PubMed
  58. S. Hirose, “A new paradigm of channelopathy in epilepsy syndromes: intracellular trafficking abnormality of channel molecules,” Epilepsy Research, vol. 70, pp. S206–S217, 2006.
  59. D. Audenaert, E. Schwartz, K. G. Claeys et al., “A novel GABRG2 mutation associated with febrile seizures,” Neurology, vol. 67, no. 4, pp. 687–690, 2006. View at Publisher · View at Google Scholar · View at PubMed
  60. S. F. Kash, R. S. Johnson, L. H. Tecott et al., “Epilepsy in mice deficient in the 65-kDa isoform of glutamic acid decarboxylase,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 25, pp. 14060–14065, 1997. View at Publisher · View at Google Scholar
  61. H. Asada, Y. Kawamura, K. Maruyama et al., “Mice lacking the 65 kDa isoform of glutamic acid decarboxylase (GAD65) maintain normal levels of GAD67 and GABA in their brains but are susceptible to seizures,” Biochemical and Biophysical Research Communications, vol. 229, no. 3, pp. 891–895, 1996. View at Publisher · View at Google Scholar
  62. M. Kato, “A new paradigm for West syndrome based on molecular and cell biology,” Epilepsy Research, vol. 70, supplement 1, pp. S87–S95, 2006.
  63. M. Kato, S. Das, K. Petras et al., “Mutations of ARX are associated with striking pleiotropy and consistent genotype-phenotype correlation,” Human Mutation, vol. 23, no. 2, pp. 147–159, 2004. View at Publisher · View at Google Scholar · View at PubMed
  64. E. Marsh, C. Fulp, E. Gomez et al., “Targeted loss of Arx results in a developmental epilepsy mouse model and recapitulates the human phenotype in heterozygous females,” Brain, vol. 132, no. 6, pp. 1563–1576, 2009. View at Publisher · View at Google Scholar · View at PubMed
  65. M. Kato, N. Koyama, M. Ohta, K. Miura, and K. Hayasaka, “Frameshift mutations of the ARX gene in familial Ohtahara syndrome,” Epilepsia, vol. 51, no. 9, pp. 1679–1684, 2010. View at Publisher · View at Google Scholar · View at PubMed
  66. M. G. Price, J. W. Yoo, D. L. Burgess et al., “A triplet repeat expansion genetic mouse model of infantile spasms syndrome, Arx(GCG)10+7, with interneuronopathy, spasms in infancy, persistent seizures, and adult cognitive and behavioral impairment,” Journal of Neuroscience, vol. 29, no. 27, pp. 8752–8763, 2009. View at Publisher · View at Google Scholar · View at PubMed
  67. M. G. Frei, H. P. Zaveri, S. Arthurs et al., “Controversies in epilepsy: debates held during the Fourth International Workshop on Seizure Prediction,” Epilepsy and Behavior, vol. 19, no. 1, pp. 4–16, 2010. View at Publisher · View at Google Scholar · View at PubMed
  68. D. G. Margineanu, “Epileptic hypersynchrony revisited,” NeuroReport, vol. 21, no. 15, pp. 963–967, 2010. View at Publisher · View at Google Scholar · View at PubMed
  69. A. Klaassen, J. Glykys, J. Maguire, C. Labarca, I. Mody, and J. Boulter, “Seizures and enhanced cortical GABAergic inhibition in two mouse models of human autosomal dominant nocturnal frontal lobe epilepsy,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 50, pp. 19152–19157, 2006. View at Publisher · View at Google Scholar · View at PubMed
  70. E. O. Mann and I. Mody, “The multifaceted role of inhibition in epilepsy: seizure-genesis through excessive GABAergic inhibition in autosomal dominant nocturnal frontal lobe epilepsy,” Current Opinion in Neurology, vol. 21, no. 2, pp. 155–160, 2008. View at Publisher · View at Google Scholar · View at PubMed
  71. L. Danober, C. Deransart, A. Depaulis, M. Vergnes, and C. Marescaux, “Pathophysiological mechanisms of genetic absence epilepsy in the rat,” Progress in Neurobiology, vol. 55, no. 1, pp. 27–57, 1998. View at Publisher · View at Google Scholar
  72. L. Cancedda, H. Fiumelli, K. Chen, and M. M. Poo, “Excitatory GABA action is essential for morphological maturation of cortical neurons in vivo,” Journal of Neuroscience, vol. 27, no. 19, pp. 5224–5235, 2007. View at Publisher · View at Google Scholar · View at PubMed
  73. K. Nakanishi, J. Yamada, C. Takayama, A. Oohira, and A. Fukuda, “NKCC1 activity modulates formation of functional inhibitory synapses in cultured neocortical neurons,” Synapse, vol. 61, no. 3, pp. 138–149, 2007. View at Publisher · View at Google Scholar · View at PubMed
  74. D. D. Wang and A. R. Kriegstein, “Blocking early GABA depolarization with bumetanide results in permanent alterations in cortical circuits and sensorimotor gating deficits,” Cerebral Cortex, vol. 21, no. 3, pp. 574–587, 2011. View at Publisher · View at Google Scholar · View at PubMed
  75. S. Maljevic, K. Krampfl, J. Cobilanschi et al., “A mutation in the GABAA receptor α1-subunit is associated with absence epilepsy,” Annals of Neurology, vol. 59, no. 6, pp. 983–987, 2006. View at Publisher · View at Google Scholar · View at PubMed
  76. J. Q. Kang, W. Shen, M. Lee, M. J. Gallagher, and R. L. Macdonald, “Slow degradation and aggregation in vitro of mutant GABAA receptor γ2(Q351X) subunits associated with epilepsy,” Journal of Neuroscience, vol. 30, no. 41, pp. 13895–13905, 2010. View at Publisher · View at Google Scholar · View at PubMed
  77. A. S. Galanopoulou, “Mutations affecting GABAergic signaling in seizures and epilepsy,” Pflügers Archiv European Journal of Physiology, vol. 460, no. 2, pp. 505–523, 2010. View at Publisher · View at Google Scholar · View at PubMed
  78. R. L. Macdonald, J. Q. Kang, and M. J. Gallagher, “Mutations in GABAA receptor subunits associated with genetic epilepsies,” Journal of Physiology, vol. 588, no. 11, pp. 1861–1869, 2010. View at Publisher · View at Google Scholar · View at PubMed
  79. C. Chiu, C. A. Reid, H. O. Tan et al., “Developmental impact of a familial GABAA receptor epilepsy mutation,” Annals of Neurology, vol. 64, no. 3, pp. 284–293, 2008. View at Publisher · View at Google Scholar · View at PubMed
  80. D. L. Kaufman, C. R. Houser, and A. J. Tobin, “Two forms of the γ-aminobutyric acid synthetic enzyme glutamate decarboxylase have distinct intraneuronal distributions and cofactor interactions,” Journal of Neurochemistry, vol. 56, no. 2, pp. 720–723, 1991. View at Publisher · View at Google Scholar · View at Scopus
  81. A. B. Walls, E. M. Eyjolfsson, O. B. Smeland et al., “Knockout of GAD65 has major impact on synaptic GABA synthesized from astrocyte-derived glutamine,” Journal of Cerebral Blood Flow and Metabolism, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  82. A. B. Walls, L. H. Nilsen, E. M. Eyjolfsson et al., “GAD65 is essential for synthesis of GABA destined for tonic inhibition regulating epileptiform activity,” Journal of Neurochemistry, vol. 115, no. 6, pp. 1398–1408, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  83. S. Kure, Y. Sakata, S. Miyahayashi et al., “Mutation and polymorphic marker analyses of 65K- and 67K-glutamate decarboxylase genes in two families with pyridoxine-dependent epilepsy,” Journal of Human Genetics, vol. 43, no. 2, pp. 128–131, 1998. View at Scopus
  84. S. M. Gospe Jr., “Pyridoxine-dependent seizures: new genetic and biochemical clues to help with diagnosis and treatment,” Current Opinion in Neurology, vol. 19, no. 2, pp. 148–153, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  85. S. M. Gospe Jr., K. L. Olin, and C. L. Keen, “Reduced GABA synthesis in pyridoxine-dependent seizures,” The Lancet, vol. 343, no. 8906, pp. 1133–1134, 1994. View at Publisher · View at Google Scholar · View at Scopus
  86. H. Asada, Y. Kawamura, K. Maruyama et al., “Cleft palate and decreased brain γ-aminobutyric acid in mice lacking the 67-kDa isoform of glutamic acid decarboxylase,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 12, pp. 6496–6499, 1997. View at Publisher · View at Google Scholar · View at Scopus
  87. F. Ji, N. Kanbara, and K. Obata, “GABA and histogenesis in fetal and neonatal mouse brain lacking both the isoforms of glutamic acid decarboxylase,” Neuroscience Research, vol. 33, no. 3, pp. 187–194, 1999. View at Publisher · View at Google Scholar · View at Scopus
  88. P. Kwan, G. J. Sills, K. Kelly, E. Butler, and M. J. Brodie, “Glutamic acid decarboxylase autoantibodies in controlled and uncontrolled epilepsy: a pilot study,” Epilepsy Research, vol. 42, no. 2-3, pp. 191–195, 2000. View at Publisher · View at Google Scholar · View at Scopus
  89. T. Yoshimoto, M. Doi, N. Fukai et al., “Type 1 diabetes mellitus and drug-resistant epilepsy: presence of high titer of anti-glutamic acid decarboxylase autoantibodies in serum and cerebrospinal fluid,” Internal Medicine, vol. 44, no. 11, pp. 1174–1177, 2005. View at Publisher · View at Google Scholar · View at Scopus
  90. D. A. Pearce, M. Atkinson, and D. A. Tagle, “Glutamic acid decarboxylase autoimmunity in Batten disease and other disorders,” Neurology, vol. 63, no. 11, pp. 2001–2005, 2004. View at Scopus
  91. K. McKnight, Y. Jiang, Y. Hart et al., “Serum antibodies in epilepsy and seizure-associated disorders,” Neurology, vol. 65, no. 11, pp. 1730–1736, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  92. M. B. Rust, S. L. Alper, Y. Rudhard et al., “Disruption of erythroid K-Cl cotransporters alters erythrocyte volume and partially rescues erythrocyte dehydration in SAD mice,” Journal of Clinical Investigation, vol. 117, no. 6, pp. 1708–1717, 2007. View at Publisher · View at Google Scholar · View at PubMed
  93. C. A. Hübner, V. Stein, I. Hermans-Borgmeyer, T. Meyer, K. Ballanyi, and T. J. Jentsch, “Disruption of KCC2 reveals an essential role of K-Cl cotransport already in early synaptic inhibition,” Neuron, vol. 30, no. 2, pp. 515–524, 2001. View at Publisher · View at Google Scholar
  94. N. S. Woo, J. Lu, R. England et al., “Hyperexcitability and epilepsy associated with disruption of the mouse neuronal-specific K-Cl cotransporter gene,” Hippocampus, vol. 12, no. 2, pp. 258–268, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  95. J. Tornberg, V. Voikar, H. Savilahti, H. Rauvala, and M. S. Airaksinen, “Behavioural phenotypes of hypomorphic KCC2-deficient mice,” European Journal of Neuroscience, vol. 21, no. 5, pp. 1327–1337, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  96. L. Zhu, N. Polley, G. C. Mathews, and E. Delpire, “NKCC1 and KCC2 prevent hyperexcitability in the mouse hippocampus,” Epilepsy Research, vol. 79, no. 2-3, pp. 201–212, 2008. View at Publisher · View at Google Scholar · View at PubMed
  97. N. Dupré, H. C. Howard, J. Mathieu et al., “Hereditary motor and sensory neuropathy with agenesis of the corpus callosum,” Annals of Neurology, vol. 54, no. 1, pp. 9–18, 2003. View at Publisher · View at Google Scholar · View at PubMed
  98. J. Mathieu, F. Bedard, C. Prevost, and P. Langevin, “Hereditary motor and sensory neuropathy with or without agenesis of the corpus callosum. Radiological and clinical study of 64 cases,” Canadian Journal of Neurological Sciences, vol. 17, no. 2, pp. 103–108, 1990.
  99. H. C. Howard, D. B. Mount, D. Rochefort et al., “The K-Cl cotransporter KCC3 is mutant in a severe peripheral neuropathy associated with agenesis of the corpus callosum,” Nature Genetics, vol. 32, no. 3, pp. 384–392, 2002. View at Publisher · View at Google Scholar · View at PubMed
  100. T. Boettger, M. B. Rust, H. Maier et al., “Loss of K-Cl co-transporter KCC3 causes deafness, neurodegeneration and reduced seizure threshold,” The EMBO Journal, vol. 22, no. 20, pp. 5422–5434, 2003. View at Publisher · View at Google Scholar · View at PubMed
  101. T. Boettger, C. A. Hübner, H. Maier, M. B. Rust, F. X. Beck, and T. J. Jentsch, “Deafness and renal tubular acidosis in mice lacking the K-Cl co-transporter Kcc4,” Nature, vol. 416, no. 6883, pp. 874–878, 2002. View at Publisher · View at Google Scholar · View at PubMed
  102. M. J. Dixon, J. Gazzard, S. S. Chaudhry, N. Sampson, B. A. Schulte, and K. P. Steel, “Mutation of the Na-K-Cl co-transporter gene Slc12a2 results in deafness in mice,” Human Molecular Genetics, vol. 8, no. 8, pp. 1579–1584, 1999. View at Publisher · View at Google Scholar
  103. A. J. Pace, V. J. Madden, O. W. Henson, B. H. Koller, and M. M. Henson, “Ultrastructure of the inner ear of NKCC1-deficient mice,” Hearing Research, vol. 156, no. 1-2, pp. 17–30, 2001. View at Publisher · View at Google Scholar
  104. E. Delpire, J. Lu, R. England, C. Dull, and T. Thorne, “Deafness and imbalance associated with inactivation of the secretory Na-K-2Cl co-transporter,” Nature Genetics, vol. 22, no. 2, pp. 192–195, 1999. View at Publisher · View at Google Scholar · View at PubMed
  105. D. B. Simon, F. E. Karet, J. M. Hamdan, A. Di Pietro, S. A. Sanjad, and R. P. Lifton, “Bartter's syndrome, hypokalaemic alkalosis with hypercalciuria, is caused by mutations in the Na-K-2CI cotransporter NKCC2,” Nature Genetics, vol. 13, no. 2, pp. 183–188, 1996.
  106. P. Uvarov, A. Ludwig, M. Markkanen et al., “A novel N-terminal isoform of the neuron-specific K-Cl cotransporter KCC2,” Journal of Biological Chemistry, vol. 282, no. 42, pp. 30570–30576, 2007. View at Publisher · View at Google Scholar · View at PubMed
  107. K. J. Staley and I. Mody, “Shunting of excitatory input to dentate gyrus granule cells by a depolarizing GABAA receptor-mediated postsynaptic conductance,” Journal of Neurophysiology, vol. 68, no. 1, pp. 197–212, 1992.
  108. H. Li, S. Khirug, C. Cai et al., “KCC2 interacts with the dendritic cytoskeleton to promote spine development,” Neuron, vol. 56, no. 6, pp. 1019–1033, 2007. View at Publisher · View at Google Scholar · View at PubMed
  109. T. Viitanen, E. Ruusuvuori, K. Kaila, and J. Voipio, “The K+-Cl− cotransporter KCC2 promotes GABAergic excitation in the mature rat hippocampus,” Journal of Physiology, vol. 588, no. 9, pp. 1527–1540, 2010. View at Publisher · View at Google Scholar · View at PubMed
  110. D. D. Wang and A. R. Kriegstein, “GABA regulates excitatory synapse formation in the neocortex via NMDA receptor activation,” Journal of Neuroscience, vol. 28, no. 21, pp. 5547–5558, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  111. A. T. Berg, S. N. Smith, D. Frobish et al., “Special education needs of children with newly diagnosed epilepsy,” Developmental Medicine and Child Neurology, vol. 47, no. 11, pp. 749–753, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  112. K. Kitamura, M. Yanazawa, N. Sugiyama et al., “Mutation of ARX causes abnormal development of forebrain and testes in mice and X-linked lissencephaly with abnormal genitalia in humans,” Nature Genetics, vol. 32, no. 3, pp. 359–369, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  113. G. Friocourt, K. Poirier, S. Rakić, J. G. Parnavelas, and J. Chelly, “The role of ARX in cortical development,” European Journal of Neuroscience, vol. 23, no. 4, pp. 869–876, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  114. P. Strømme, M. E. Mangelsdorf, I. E. Scheffer, and J. Gécz, “Infantile spasms, dystonia, and other X-linked phenotypes caused by mutations in Aristaless related homeobox gene, ARX,” Brain and Development, vol. 24, no. 5, pp. 266–268, 2002. View at Publisher · View at Google Scholar · View at Scopus
  115. G. Turner, M. Partington, B. Kerr, M. Mangelsdorf, and J. Gecz, “Variable expression of mental retardation, autism, seizures, and dystonic hand movements in two families with an identical ARX gene mutation,” American Journal of Medical Genetics, vol. 112, no. 4, pp. 405–411, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  116. M. W. Partington, G. Turner, J. Boyle, and J. Gécz, “Three new families with X-linked mental retardation caused by the 428-451dup(24bp) mutation in ARX,” Clinical Genetics, vol. 66, no. 1, pp. 39–45, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  117. G. Friocourt and J. G. Parnavelas, “Mutations in ARX result in several defects involving GABAergic neurons,” Frontiers in Cellular Neuroscience, vol. 4, p. 4, 2010.
  118. B. A. Minassian, T. M. DeLorey, R. W. Olsen et al., “Angelman syndrome: correlations between epilepsy phenotypes and genotypes,” Annals of Neurology, vol. 43, no. 4, pp. 485–493, 1998. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  119. G. E. Homanics, T. M. DeLorey, L. L. Firestone et al., “Mice devoid of γ-aminobutyrate type A receptor β3 subunit have epilepsy, cleft palate, and hypersensitive behavior,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 8, pp. 4143–4148, 1997. View at Publisher · View at Google Scholar
  120. S. F. Berkovic, L. Harkin, J. M. McMahon et al., “De-novo mutations of the sodium channel gene SCN1A in alleged vaccine encephalopathy: a retrospective study,” The Lancet Neurology, vol. 5, no. 6, pp. 488–492, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  121. L. A. Harkin, J. M. McMahon, X. Iona et al., “The spectrum of SCN1A-related infantile epileptic encephalopathies,” Brain, vol. 130, no. 3, pp. 843–852, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  122. S. E. Heron, I. E. Scheffer, X. Iona et al., “De novo SCN1A mutations in Dravet syndrome and related epileptic encephalopathies are largely of paternal origin,” Journal of Medical Genetics, vol. 47, no. 2, pp. 137–141, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  123. R. H. Wallace, B. L. Hodgson, B. E. Grinton et al., “Sodium channel α1-subunit mutations in severe myoclonic epilepsy of infancy and infantile spasms,” Neurology, vol. 61, no. 6, pp. 765–769, 2003. View at Scopus
  124. M. S. Martin, K. Dutt, L. A. Papale et al., “Altered function of the SCN1A voltage-gated sodium channel leads to γ-aminobutyric acid-ergic (GABAergic) interneuron abnormalities,” Journal of Biological Chemistry, vol. 285, no. 13, pp. 9823–9834, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  125. H. Prüss, J. Dalmau, L. Harms et al., “Retrospective analysis of NMDA receptor antibodies in encephalitis of unknown origin,” Neurology, vol. 75, no. 19, pp. 1735–1739, 2010. View at Publisher · View at Google Scholar · View at PubMed
  126. T. Iizuka and F. Sakai, “Anti-NMDA receptor encephalitis—clinical manifestations and pathophysiology,” Brain and Nerve, vol. 60, no. 9, pp. 1047–1060, 2008. View at Scopus
  127. E. Aronica, K. Boer, S. Redeker et al., “Differential expression patterns of chloride transporters, Na+-K+-2Cl−-cotransporter and K+-Cl−-cotransporter, in epilepsy-associated malformations of cortical development,” Neuroscience, vol. 145, no. 1, pp. 185–196, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  128. C. Cepeda, V. M. André, N. Wu et al., “Immature neurons and GABA networks may contribute to epileptogenesis in pediatric cortical dysplasia,” Epilepsia, vol. 48, supplement 5, pp. 79–85, 2007. View at Publisher · View at Google Scholar · View at PubMed
  129. C. Shimizu-Okabe, A. Okabe, W. Kilb, K. Sato, H. J. Luhmann, and A. Fukuda, “Changes in the expression of cation-Cl− cotransporters, NKCC1 and KCC2, during cortical malformation induced by neonatal freeze-lesion,” Neuroscience Research, vol. 59, no. 3, pp. 288–295, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  130. O. Peters, C. Redecker, G. Hagemann, C. Bruehl, H. J. Luhmann, and O. W. Witte, “Impaired synaptic plasticity in the surround of perinatally aquired dysplasia in rat cerebral cortex,” Cerebral Cortex, vol. 14, no. 10, pp. 1081–1087, 2004. View at Publisher · View at Google Scholar · View at PubMed
  131. J. J. Hablitz and R. A. DeFazio, “Altered receptor subunit expression in rat neocortical malformations,” Epilepsia, vol. 41, no. 6, pp. S82–S85, 2000. View at Scopus
  132. E. A. Benardete and A. R. Kriegstein, “Increased excitability and decreased sensitivity to GABA in an animal model of dysplastic cortex,” Epilepsia, vol. 43, no. 9, pp. 970–982, 2002. View at Publisher · View at Google Scholar · View at Scopus
  133. J. Nabekura, T. Ueno, A. Okabe et al., “Reduction of KCC2 expression and GABAA receptor-mediated excitation after in vivo axonal injury,” Journal of Neuroscience, vol. 22, no. 11, pp. 4412–4417, 2002. View at Scopus
  134. H. Toyoda, K. Ohno, J. Yamada et al., “Induction of NMDA and GABAA receptor-mediated Ca2+ oscillations with KCC2 mRNA downregulation in injured facial motoneurons,” Journal of Neurophysiology, vol. 89, no. 3, pp. 1353–1362, 2003. View at Publisher · View at Google Scholar · View at PubMed
  135. A. Shulga, J. Thomas-Crusells, T. Sigl et al., “Posttraumatic GABAA-mediated [Ca2+]i increase is essential for the induction of brain-derived neurotrophic factor-dependent survival of mature central neurons,” Journal of Neuroscience, vol. 28, no. 27, pp. 6996–7005, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  136. X. Jin, J. R. Huguenard, and D. A. Prince, “Impaired Cl− extrusion in layer V pyramidal neurons of chronically injured epileptogenic neocortex,” Journal of Neurophysiology, vol. 93, no. 4, pp. 2117–2126, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  137. X. Jin, J. R. Huguenard, and D. A. Prince, “Reorganization of inhibitory synaptic circuits in rodent chronically injured epileptogenic neocortex,” Cerebral Cortex, vol. 21, no. 5, pp. 1094–1104, 2011. View at Publisher · View at Google Scholar · View at PubMed
  138. P. G. Ochalski, W. Fellows-Mayle, L. B. Hsieh et al., “Flumazenil administration attenuates cognitive impairment in immature rats after controlled cortical impact,” Journal of Neurotrauma, vol. 27, no. 3, pp. 647–651, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  139. H. P. Goodkin, S. Joshi, Z. Mtchedlishvili, J. Brar, and J. Kapur, “Subunit-specific trafficking of GABAA receptors during status epilepticus,” Journal of Neuroscience, vol. 28, no. 10, pp. 2527–2538, 2008. View at Publisher · View at Google Scholar · View at PubMed
  140. D. E. Naylor, H. Liu, and C. G. Wasterlain, “Trafficking of GABAA receptors, loss of inhibition, and a mechanism for pharmacoresistance in status epilepticus,” Journal of Neuroscience, vol. 25, no. 34, pp. 7724–7733, 2005. View at Publisher · View at Google Scholar · View at PubMed
  141. E. Isaeva, D. Isaev, R. Khazipov, and G. L. Holmes, “Selective impairment of GABAergic synaptic transmission in the flurothyl model of neonatal seizures,” European Journal of Neuroscience, vol. 23, no. 6, pp. 1559–1566, 2006. View at Publisher · View at Google Scholar · View at PubMed
  142. E. Isaeva, D. Isaev, R. Khazipov, and G. L. Holmes, “Long-term suppression of GABAergic activity by neonatal seizures in rat somatosensory cortex,” Epilepsy Research, vol. 87, no. 2-3, pp. 286–289, 2009. View at Publisher · View at Google Scholar · View at PubMed
  143. H. Ni, Y. W. Jiang, T. Bo, J. M. Wang, and X. R. Wu, “c-Fos, N-methyl-D-aspartate receptor 2C, GABA-A-α1 immonoreactivity, seizure latency and neuronal injury following single or recurrent neonatal seizures in hippocampus of Wistar rat,” Neuroscience Letters, vol. 380, no. 1-2, pp. 149–154, 2005. View at Publisher · View at Google Scholar · View at PubMed
  144. H. B. Laurén, F. R. Lopez-Picon, E. R. Korpi, and I. E. Holopainen, “Kainic acid-induced status epilepticus alters GABAA receptor subunit mRNA and protein expression in the developing rat hippocampus,” Journal of Neurochemistry, vol. 94, no. 5, pp. 1384–1394, 2005. View at Publisher · View at Google Scholar · View at PubMed
  145. G. Zhang, Y. H. Raol, F. C. Hsu, D. A. Coulter, and A. R. Brooks-Kayal, “Effects of status epilepticus on hippocampal GABAA receptors are age-dependent,” Neuroscience, vol. 125, no. 2, pp. 299–303, 2004. View at Publisher · View at Google Scholar · View at PubMed
  146. Y. H. Raol, G. Zhang, I. V. Lund, B. E. Porter, M. A. Maronski, and A. R. Brooks-Kayal, “Increased GABAA-receptor α1-subunit expression in hippocampal dentate gyrus after early-life status epilepticus,” Epilepsia, vol. 47, no. 10, pp. 1665–1673, 2006. View at Publisher · View at Google Scholar · View at PubMed
  147. N. S. Abend, A. M. Gutierrez-Colina, and D. J. Dlugos, “Medical treatment of pediatric status epilepticus,” Seminars in Pediatric Neurology, vol. 17, no. 3, pp. 169–175, 2010. View at Publisher · View at Google Scholar · View at PubMed
  148. P. Shearer and J. Riviello, “Generalized convulsive status epilepticus in adults and children: treatment guidelines and protocols,” Emergency Medicine Clinics of North America, vol. 29, no. 1, pp. 51–64, 2011. View at Publisher · View at Google Scholar · View at PubMed
  149. H. D. Lux and U. Heinemann, “Ionic changes during experimentally induced seizure activity,” Electroencephalography and Clinical Neurophysiology. Supplement, no. 34, pp. 289–297, 1978.
  150. V. I. Dzhala, K. V. Kuchibhotla, J. C. Glykys et al., “Progressive NKCC1-dependent neuronal chloride accumulation during neonatal seizures,” Journal of Neuroscience, vol. 30, no. 35, pp. 11745–11761, 2010. View at Publisher · View at Google Scholar · View at PubMed
  151. C. Rivera, J. Voipio, J. Thomas-Crusells et al., “Mechanism of activity-dependent downregulation of the neuron-specific K-Cl cotransporter KCC2,” Journal of Neuroscience, vol. 24, no. 19, pp. 4683–4691, 2004. View at Publisher · View at Google Scholar · View at PubMed
  152. U. Sayin, S. Osting, J. Hagen, P. Rutecki, and T. Sutula, “Spontaneous seizures and loss of axo-axonic and axo-somatic inhibition induced by repeated brief seizures in kindled rats,” Journal of Neuroscience, vol. 23, no. 7, pp. 2759–2768, 2003.
  153. A. Obenaus, M. Esclapez, and C. R. Houser, “Loss of glutamate decarboxylase mRNA-containing neurons in the rat dentate gyrus following pilocarpine-induced seizures,” Journal of Neuroscience, vol. 13, no. 10, pp. 4470–4485, 1993.
  154. L. Wang, Y. H. Liu, Y. G. Huang, and L. W. Chen, “Time-course of neuronal death in the mouse pilocarpine model of chronic epilepsy using Fluoro-Jade C staining,” Brain Research, vol. 1241, pp. 157–167, 2008. View at Publisher · View at Google Scholar · View at PubMed
  155. J. P. Leite, T. L. Babb, J. K. Pretorius, P. A. Kuhlman, K. M. Yeoman, and G. W. Mathern, “Neuron loss, mossy fiber sprouting, and interictal spikes after intrahippocampal kainate in developing rats,” Epilepsy Research, vol. 26, no. 1, pp. 219–231, 1996. View at Publisher · View at Google Scholar
  156. R. S. Sloviter, C. A. Zappone, B. D. Harvey, A. V. Bumanglag, R. A. Bender, and M. Frotscher, ““Dormant basket cell” hypothesis revisited: relative vulnerabilities of dentate gyrus mossy cells and inhibitory interneurons after hippocampal status epilepticus in the rat,” Journal of Comparative Neurology, vol. 459, no. 1, pp. 44–76, 2003. View at Publisher · View at Google Scholar · View at PubMed
  157. J. M. Fritschy, T. Kiener, V. Bouilleret, and F. Loup, “GABAergic neurons and GABAA-receptors in temporal lobe epilepsy,” Neurochemistry International, vol. 34, no. 5, pp. 435–445, 1999. View at Publisher · View at Google Scholar
  158. K. Z. Haas, E. F. Sperber, L. A. Opanashuk, P. K. Stanton, and S. L. Moshé, “Resistance of immature hippocampus to morphologic and physiologic alterations following status epilepticus or kindling,” Hippocampus, vol. 11, no. 6, pp. 615–625, 2001. View at Publisher · View at Google Scholar · View at PubMed
  159. C. E. Stafstrom, J. L. Thompson, and G. L. Holmes, “Kainic acid seizures in the developing brain: status epilepticus and spontaneous recurrent seizures,” Developmental Brain Research, vol. 65, no. 2, pp. 227–236, 1992. View at Publisher · View at Google Scholar
  160. L. Nitecka, E. Tremblay, and G. Charton, “Maturation of kainic acid seizure-brain damage syndrome in the rat. II. Histopathological sequelae,” Neuroscience, vol. 13, no. 4, pp. 1073–1094, 1984.
  161. D. J. Laurie, W. Wisden, and P. H. Seeburg, “The distribution of thirteen GABAA receptor subunit mRNAs in the rat brain. III. Embryonic and postnatal development,” Journal of Neuroscience, vol. 12, no. 11, pp. 4151–4172, 1992.
  162. Y. H. Raol, I. V. Lund, S. Bandyopadhyay et al., “Enhancing GABAA receptor α1 subunit levels in hippocampal dentate gyrus inhibits epilepsy development in an animal model of temporal lobe epilepsy,” Journal of Neuroscience, vol. 26, no. 44, pp. 11342–11346, 2006. View at Publisher · View at Google Scholar · View at PubMed
  163. I. Cohen, V. Navarro, S. Clemenceau, M. Baulac, and R. Miles, “On the origin of interictal activity in human temporal lobe epilepsy in vitro,” Science, vol. 298, no. 5597, pp. 1418–1421, 2002. View at Publisher · View at Google Scholar · View at PubMed
  164. G. Huberfeld, L. Wittner, S. Clemenceau et al., “Perturbed chloride homeostasis and GABAergic signaling in human temporal lobe epilepsy,” Journal of Neuroscience, vol. 27, no. 37, pp. 9866–9873, 2007. View at Publisher · View at Google Scholar · View at PubMed
  165. W. G. Reiss and K. S. Oles, “Acetazolamide in the treatment of seizures,” Annals of Pharmacotherapy, vol. 30, no. 5, pp. 514–518, 1996.
  166. X. Li, J. Zhou, Z. Chen, S. Chen, F. Zhu, and L. Zhou, “Long-term expressional changes of Na+-K+-Cl− co-transporter 1 (NKCC1) and K+-Cl− co-transporter 2 (KCC2) in CA1 region of hippocampus following lithium-pilocarpine induced status epilepticus (PISE),” Brain Research, vol. 1221, pp. 141–146, 2008. View at Publisher · View at Google Scholar · View at PubMed
  167. A. Muñoz, P. Méndez, J. Defelipe, and F. J. Alvarez-Leefmans, “Cation-chloride cotransporters and GABA-ergic innervation in the human epileptic hippocampus,” Epilepsia, vol. 48, no. 4, pp. 663–673, 2007. View at Publisher · View at Google Scholar · View at PubMed
  168. E. Palma, M. Amici, F. Sobrero et al., “Anomalous levels of Cl− transporters in the hippocampal subiculum from temporal lobe epilepsy patients make GABA excitatory,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 22, pp. 8465–8468, 2006. View at Publisher · View at Google Scholar · View at PubMed
  169. A. Sen, L. Martinian, M. Nikolic, M. C. Walker, M. Thom, and S. M. Sisodiya, “Increased NKCC1 expression in refractory human epilepsy,” Epilepsy Research, vol. 74, no. 2-3, pp. 220–227, 2007. View at Publisher · View at Google Scholar · View at PubMed
  170. M. Munakata, M. Watanabe, T. Otsuki et al., “Altered distribution of KCC2 in cortical dysplasia in patients with intractable epilepsy,” Epilepsia, vol. 48, no. 4, pp. 837–844, 2007. View at Publisher · View at Google Scholar · View at PubMed
  171. S. Khirug, F. Ahmad, M. Puskarjov, R. Afzalov, K. Kaila, and P. Blaesse, “A single seizure episode leads to rapid functional activation of KCC2 in the neonatal rat hippocampus,” Journal of Neuroscience, vol. 30, no. 36, pp. 12028–12035, 2010. View at Publisher · View at Google Scholar · View at PubMed
  172. F. Aguado, M. A. Carmona, E. Pozas et al., “BDNF regulates spontaneous correlated activity at early developmental stages by increasing synaptogenesis and expression of the K+/Cl− co-transporter KCC2,” Development, vol. 130, no. 7, pp. 1267–1280, 2003. View at Publisher · View at Google Scholar
  173. C. Rivera, H. Li, J. Thomas-Crusells et al., “BDNF-induced TrkB activation down-regulates the K+-Cl− cotransporter KCC2 and impairs neuronal Cl− extrusion,” Journal of Cell Biology, vol. 159, no. 5, pp. 747–752, 2002. View at Publisher · View at Google Scholar · View at PubMed
  174. W. Wang, N. Gong, and T. -L. Xu, “Downregulation of KCC2 following LTP contributes to EPSP-spike potentiation in rat hippocampus,” Biochemical and Biophysical Research Communications, vol. 343, no. 4, pp. 1209–1215, 2006. View at Publisher · View at Google Scholar · View at PubMed
  175. W. Wang, H. Wang, N. Gong, and T. L. Xu, “Changes of K+-Cl− cotransporter 2 (KCC2) and circuit activity in propofol-induced impairment of long-term potentiation in rat hippocampal slices,” Brain Research Bulletin, vol. 70, no. 4-6, pp. 444–449, 2006. View at Publisher · View at Google Scholar · View at PubMed
  176. C. J. McBain and J. A. Kauer, “Presynaptic plasticity: targeted control of inhibitory networks,” Current Opinion in Neurobiology, vol. 19, no. 3, pp. 254–262, 2009. View at Publisher · View at Google Scholar · View at PubMed
  177. H. T. Chao, H. Chen, R. C. Samaco et al., “Dysfunction in GABA signalling mediates autism-like stereotypies and Rett syndrome phenotypes,” Nature, vol. 468, no. 7321, pp. 263–269, 2010. View at Publisher · View at Google Scholar · View at PubMed
  178. G. Di Cristo, “Development of cortical GABAergic circuits and its implications for neurodevelopmental disorders,” Clinical Genetics, vol. 72, no. 1, pp. 1–8, 2007. View at Publisher · View at Google Scholar · View at PubMed
  179. A. L. Collins, D. Ma, P. L. Whitehead et al., “Investigation of autism and GABA receptor subunit genes in multiple ethnic groups,” Neurogenetics, vol. 7, no. 3, pp. 167–174, 2006. View at Publisher · View at Google Scholar · View at PubMed
  180. I. A. J. van Kooten, P. R. Hof, H. van Engeland, H. W. M. Steinbusch, P. H. Patterson, and C. Schmitz, “Autism: neuropathology, alterations of the GABAergic system, and animal models,” International Review of Neurobiology, vol. 71, pp. 1–26, 2005. View at Publisher · View at Google Scholar
  181. C. D'Hulst, I. Heulens, J. R. Brouwer et al., “Expression of the GABAergic system in animal models for fragile X syndrome and fragile X associated tremor/ataxia syndrome (FXTAS),” Brain Research, vol. 1253, pp. 176–183, 2009. View at Publisher · View at Google Scholar · View at PubMed
  182. T. M. DeLorey and R. W. Olsen, “GABA and epileptogenesis: comparing gabrb3 gene-deficient mice with Angelman syndrome in man,” Epilepsy Research, vol. 36, no. 2-3, pp. 123–132, 1999. View at Publisher · View at Google Scholar
  183. E. Lemonnier and Y. Ben-Ari, “The diuretic bumetanide decreases autistic behaviour in five infants treated during 3 months with no side effects,” Acta Paediatrica, vol. 99, no. 12, pp. 1885–1888, 2010. View at Publisher · View at Google Scholar · View at PubMed
  184. I. Khalilov, G. L. Holmes, and Y. Ben-Ari, “In vitro formation of a secondary epileptogenic mirror focus by interhippocampal propagation of seizures,” Nature Neuroscience, vol. 6, no. 10, pp. 1079–1085, 2003. View at Publisher · View at Google Scholar · View at PubMed
  185. A. S. Galanopoulou, “Developmental patterns in the regulation of chloride homeostasis and GABAA receptor signaling by seizures,” Epilepsia, vol. 48, no. 5, pp. 14–18, 2007. View at Publisher · View at Google Scholar · View at PubMed
  186. R. Nardou, Y. Ben-Ari, and I. Khalilov, “Bumetanide, an NKCC1 antagonist, does not prevent formation of epileptogenic focus but blocks epileptic focus seizures in immature rat hippocampus,” Journal of Neurophysiology, vol. 101, no. 6, pp. 2878–2888, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  187. P. Mares, “Age-and dose-specific anticonvulsant action of bumetanide in immature rats,” Physiological Research, vol. 58, no. 6, pp. 927–930, 2009. View at Scopus
  188. C. Brandt, M. Nozadze, N. Heuchert, M. Rattka, and W. Löscher, “Disease-modifying effects of phenobarbital and the NKCC1 inhibitor bumetanide in the pilocarpine model of temporal lobe epilepsy,” Journal of Neuroscience, vol. 30, no. 25, pp. 8602–8612, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  189. A. Mazarati, D. Shin, and R. Sankar, “Bumetanide inhibits rapid kindling in neonatal rats,” Epilepsia, vol. 50, no. 9, pp. 2117–2122, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  190. K. T. Kahle, S. M. Barnett, K. C. Sassower, and K. J. Staley, “Decreased seizure activity in a human neonate treated with bumetanide, an inhibitor of the Na+-K+-2Cl− cotransporter NKCC1,” Journal of Child Neurology, vol. 24, no. 5, pp. 572–576, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  191. W. Kilb, A. Sinning, and H. J. Luhmann, “Model-specific effects of bumetanide on epileptiform activity in the in-vitro intact hippocampus of the newborn mouse,” Neuropharmacology, vol. 53, no. 4, pp. 524–533, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  192. A. S. Galanopoulou and S. L. Moshé, “Role of sex hormones in the sexually dimorphic expression of KCC2 in rat substantia nigra,” Experimental Neurology, vol. 184, no. 2, pp. 1003–1009, 2003. View at Publisher · View at Google Scholar · View at PubMed
  193. F. C. Hsu, G. J. Zhang, Y. S. H. Raol, R. J. Valentino, D. A. Coulter, and A. R. Brooks-Kayal, “Repeated neonatal handling with maternal separation permanently alters hippocampal GABAA receptors and behavioral stress responses,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 21, pp. 12213–12218, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  194. K. Ganguly, A. F. Schinder, S. T. Wong, and M. M. Poo, “GABA itself promotes the developmental switch of neuronal GABAergic responses from excitation to inhibition,” Cell, vol. 105, no. 4, pp. 521–532, 2001. View at Publisher · View at Google Scholar · View at Scopus
  195. M. Ceanga, A. Spataru, and A. M. Zagrean, “Oxytocin is neuroprotective against oxygen-glucose deprivation and reoxygenation in immature hippocampal cultures,” Neuroscience Letters, vol. 477, no. 1, pp. 15–18, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  196. R. Khazipov, R. Tyzio, and Y. Ben-Ari, “Effects of oxytocin on GABA signalling in the foetal brain during delivery,” Progress in Brain Research, vol. 170, pp. 243–257, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus