KCC2 was downregulated in small neurons localized in epileptogenic human focal cortical dysplasia

Aronica, 2007, Differential expression patterns of chloride transporters, Na+–K+–2Cl−-cotransporter and K+–Cl−-cotransporter, in epilepsy-associated malformations of cortical development, Neuroscience, 145, 185, 10.1016/j.neuroscience.2006.11.041 Avoli, 1999, Epileptiform discharges in the human dysplastic neocortex: in vitro physiology and pharmacology, Ann. Neurol., 46, 816, 10.1002/1531-8249(199912)46:6<816::AID-ANA3>3.0.CO;2-O Avoli, 2005, Cellular and molecular mechanisms of epilepsy in the human brain, Prog. Neurobiol., 77, 166, 10.1016/j.pneurobio.2005.09.006 Ben-Ari, 1989, Giant synaptic potentials in immature rat CA3 hippocampal neurons, J. Physiol., 416, 303, 10.1113/jphysiol.1989.sp017762 Ben-Ari, 2005, The multiple facets of gamma-aminobutyric acid dysfunction in epilepsy, Curr. Opin. Neurol., 18, 141, 10.1097/01.wco.0000162855.75391.6a Cepeda, 2006, Epileptogenesis in pediatric cortical dysplasia: the dysmature cerebral developmental hypothesis, Epilepsy Behav., 9, 219, 10.1016/j.yebeh.2006.05.012 Cohen, 2003, Mesial temporal lobe epilepsy: a pathological replay of developmental mechanisms?, Biol. Cell, 95, 329, 10.1016/S0248-4900(03)00081-9 Crino, 2001, Differential expression of glutamate and GABA-A receptor subunit mRNA in cortical dysplasia, Neurology, 56, 906, 10.1212/WNL.56.7.906 D’Antuono, 2004, GABAA receptor-dependent synchronization leads to ictogenesis in the human dysplastic cortex, Brain, 127, 1626, 10.1093/brain/awh181 Dzhala, 2005, NKCC1 transporter facilitates seizures in the developing brain, Nat. Med., 11, 1205, 10.1038/nm1301 Fujiwara-Tsukamoto, 2003, Excitatory GABA input directly drives seizure-like rhythmic synchronization in mature hippocampal CA1 pyramidal cells, Neuroscience, 119, 265, 10.1016/S0306-4522(03)00102-7 Fukuda, 1998, Changes in intracellular Ca2+ induced by GABAA receptor activation and reduction in Cl− gradient in neonatal rat neocortex, J. Neurophysiol., 79, 439, 10.1152/jn.1998.79.1.439 Fukuda, 2005, Diuretic soothes seizures in newborns, Nat. Med., 11, 1153, 10.1038/nm1105-1153 Guerrini, 1999, Cortical dysplasias, genetics, and epileptogenesis, Adv. Neurol., 79, 95 Hubner, 2001, Disruption of KCC2 reveals an essential role of K–Cl cotransport already in early synaptic inhibition, Neuron, 30, 515, 10.1016/S0896-6273(01)00297-5 Isomura, 2003, Synaptically activated Cl− accumulation responsible for depolarizing GABAergic responses in mature hippocampal neurons, J. Neurophysiol., 90, 2752, 10.1152/jn.00142.2003 Jacobs, 1999, Focal epileptogenesis in a rat model of polymicrogyria, J. Neurophysiol., 81, 159, 10.1152/jn.1999.81.1.159 Kanaka, 2001, The differential expression patterns of messenger RNAs encoding K–Cl cotransporters (KCC1,2) and Na–K–2Cl cotransporter (NKCC1) in the rat nervous system, Neuroscience, 104, 933, 10.1016/S0306-4522(01)00149-X Khirug, 2005, Distinct properties of functional KCC2 expression in immature mouse hippocampal neurons in culture and in acute slices, Eur. J. Neurosci., 21, 899, 10.1111/j.1460-9568.2005.03886.x Lee, 2007, Direct protein kinase C-dependent phosphorylation regulates the cell surface stability and activity of the potassium chloride cotransporter KCC2, J. Biol. Chem., 282, 29777, 10.1074/jbc.M705053200 Luhmann, 1991, Postnatal maturation of the GABAergic system in rat neocortex, J. Neurophysiol., 65, 247, 10.1152/jn.1991.65.2.247 Lytle, 1995, Distribution and diversity of Na–K–Cl cotransport proteins: a study with monoclonal antibodies, Am. J. Physiol., 269, C1496, 10.1152/ajpcell.1995.269.6.C1496 Munakata, 2007, Altered distribution of KCC2 in cortical dysplasia in patients with intractable epilepsy, Epilepsia, 48, 837, 10.1111/j.1528-1167.2006.00954.x Muñoz, 2007, Cation-chloride cotransporters and GABA-ergic innervation in the human epileptic hippocampus, Epilepsia, 48, 663, 10.1111/j.1528-1167.2007.00986.x Nabekura, 2002, Reduction of KCC2 expression and GABAA receptor-mediated excitation after in vivo axonal injury, J. Neurosci., 22, 4412, 10.1523/JNEUROSCI.22-11-04412.2002 Okabe, 2002, Amygdala kindling induces upregulation of mRNA for NKCC1, a Na(+), K(+)–2Cl(−) cotransporter, in the rat piriform cortex, Neurosci. Res., 44, 225, 10.1016/S0168-0102(02)00093-7 Okabe, 2003, Changes in chloride homeostasis-regulating gene expressions in the rat hippocampus following amygdala kindling, Brain Res., 990, 221, 10.1016/S0006-8993(03)03528-5 Palmini, 1991, Focal neuronal migration disorders and intractable partial epilepsy: results of surgical treatment, Ann. Neurol., 30, 750, 10.1002/ana.410300603 Palmini, 2004, Terminology and classification of the cortical dysplasia, Neurology, 62, S2, 10.1212/01.WNL.0000114507.30388.7E Payne, 2003, Cation-chloride co-transporters in neuronal communication, development and trauma, Trends Neurosci., 26, 199, 10.1016/S0166-2236(03)00068-7 Payne, 1996, Molecular characterization of a putative K–Cl cotransporter in rat brain. A neuronal-specific isoform, J. Biol. Chem., 271, 16245, 10.1074/jbc.271.27.16245 Raymond, 1995, Abnormalities of gyration, heterotopias, tuberous sclerosis, focal cortical dysplasia, microdysgenesis, dysembryoplastic neuroepithelial tumor and dysgenesis of the archicortex in epilepsy. Clinical, EEG and neuroimaging features in 100 adult patients, Brain, 118, 629, 10.1093/brain/118.3.629 Rivera, 2002, BDNF-induced TrkB activation down-regulates the K+–Cl− cotransporter KCC2 and impairs neuronal Cl− extrusion, J. Cell Biol., 159, 747, 10.1083/jcb.200209011 Rivera, 1999, The K+/Cl− co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation, Nature, 397, 251, 10.1038/16697 Rivera, 2003, Mechanism of activity-dependent downregulation of the neuron-specific K–Cl cotransporter KCC2, J. Neurosci., 24, 4683, 10.1523/JNEUROSCI.5265-03.2004 Sen, 2007, Increased NKCC1 expression in refractory human epilepsy, Epilepsy Res., 74, 220, 10.1016/j.eplepsyres.2007.01.004 Shimizu-Okabe, 2007, Changes in the expression of cation-Cl− cotransporters, NKCC1 and KCC2, during cortical malformation induced by freeze-lesion, Neurosci. Res., 59, 288, 10.1016/j.neures.2007.07.010 Shimizu-Okabe, 2004, KCC2 expression is downregulated in human epileptogenic cortical dysplasia, Soc. Neurosci. Abstr., 30, 27222 Sugimoto, 2003, Regaining of gaba- and glycine-induced calcium influxes during formation of the microgyrus in an experimental model of cortical malformations, Soc. Neurosci. Abstr., 29 Toyoda, 2003, Induction of NMDA and GABAA receptor-mediated Ca2+ oscillations with KCC2 mRNA downregulation in injured facial motoneurons, J. Neurophysiol., 89, 1353, 10.1152/jn.00721.2002 Ueno, 2002, Diversity of neuron-specific K+–Cl− cotransporter expression and inhibitory postsynaptic potential depression in rat motoneurons, J. Biol. Chem., 277, 4945, 10.1074/jbc.M109439200 van den Pol, 1996, Exitatory actions of GABA after neuronal trauma, J. Neurosci., 16, 4283, 10.1523/JNEUROSCI.16-13-04283.1996 Wake, 2007, Early changes in KCC2 phosphorylation in response to neuronal stress result in functional downregulation, J. Neurosci., 27, 1642, 10.1523/JNEUROSCI.3104-06.2007 Woo, 2002, Hyperexcitability and epilepsy associated with disruption of the mouse neuronal-specific K–Cl cotransporter gene, Hippocampus, 12, 258, 10.1002/hipo.10014 Yamada, 2004, Cl− uptake promoting depolarizing GABA actions in immature rat neocortical neurons is mediated by NKCC1, J. Physiol., 15, 829, 10.1113/jphysiol.2004.062471