Cation-Chloride Cotransporters and Neuronal Function

Neuron

Volumn 61, Issue 6, 2009, Pages 820-838

  Blaesse, Peter ^a   Airaksinen, Matti S ^a   Rivera, Claudio ^b   Kaila, Kai ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ANALGESIC AGENT; ANTICONVULSIVE AGENT; BUMETANIDE; CHLORIDE ION; FUROSEMIDE; GLUTAMIC ACID; GLYCINE RECEPTOR; OPIATE; POTASSIUM CHLORIDE COTRANSPORTER; SODIUM CHLORIDE COTRANSPORTER; SODIUM POTASSIUM CHLORIDE COTRANSPORTER;

ANTICONVULSANT ACTIVITY; BRAIN DEVELOPMENT; CELL FUNCTION; CELL STRUCTURE; CELL VOLUME; CHANNELOPATHY; CHLORIDE TRANSPORT; CORPUS CALLOSUM AGENESIS; EPILEPSY; HEREDITARY MOTOR SENSORY NEUROPATHY; HUMAN; NERVE CELL; NERVE CELL LESION; NERVE CELL PLASTICITY; NEURAL STEM CELL; NEUROPATHIC PAIN; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; SYNAPTOGENESIS;

ANIMALS; CATIONS; CHLORIDES; EVOLUTION; GENE EXPRESSION; HUMANS; NERVOUS SYSTEM DISEASES; NEURONAL PLASTICITY; NEURONS; SYMPORTERS; SYNAPSES;

EID: 62549109964     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2009.03.003     Document Type: Review

References (235)

1. Achilles K., Okabe A., Ikeda M., Shimizu-Okabe C., Yamada J., Fukuda A., Luhmann H.J., and Kilb W. Kinetic properties of Cl uptake mediated by Na+-dependent K+-2Cl cotransport in immature rat neocortical neurons. J. Neurosci. 27 (2007) 8616-8627
2. Aickin C.C., Deisz R.A., and Lux H.D. Ammonium action on post-synaptic inhibition in crayfish neurones: implications for the mechanism of chloride extrusion. J. Physiol. 329 (1982) 319-339
3. Akerman C.J., and Cline H.T. Depolarizing GABAergic conductances regulate the balance of excitation to inhibition in the developing retinotectal circuit in vivo. J. Neurosci. 26 (2006) 5117-5130
4. Akerman C.J., and Cline H.T. Refining the roles of GABAergic signaling during neural circuit formation. Trends Neurosci. 30 (2007) 382-389
5. Amiry-Moghaddam M., and Ottersen O.P. The molecular basis of water transport in the brain. Nat. Rev. Neurosci. 4 (2003) 991-1001
6. Andang M., Hjerling-Leffler J., Moliner A., Lundgren T.K., Castelo-Branco G., Nanou E., Pozas E., Bryja V., Halliez S., Nishimaru H., et al. Histone H2AX-dependent GABA(A) receptor regulation of stem cell proliferation. Nature 451 (2008) 460-464
7. Auger A.P., Perrot-Sinal T.S., and McCarthy M.M. Excitatory versus inhibitory GABA as a divergence point in steroid-mediated sexual differentiation of the brain. Proc. Natl. Acad. Sci. USA 98 (2001) 8059-8064
8. Avoli M., Louvel J., Pumain R., and Kohling R. Cellular and molecular mechanisms of epilepsy in the human brain. Prog. Neurobiol. 77 (2005) 166-200
9. Balakrishnan V., Becker M., Löhrke S., Nothwang H.G., Güresir E., and Friauf E. Expression and function of chloride transporters during development of inhibitory neurotransmission in the auditory brainstem. J. Neurosci. 23 (2003) 4134-4145
10. Banke T.G., and Gegelashvili G. Tonic activation of group I mGluRs modulates inhibitory synaptic strength by regulating KCC2 activity. J. Physiol. 586 (2008) 4925-4934
11. Bartho P., Payne J.A., Freund T.F., and Acsady L. Differential distribution of the KCl cotransporter KCC2 in thalamic relay and reticular nuclei. Eur. J. Neurosci. 20 (2004) 965-975
12. Bayatti N., Moss J.A., Sun L., Ambrose P., Ward J.F.H., Lindsay S., and Clowry G.J. A molecular neuroanatomical study of the developing human neocortex from 8 to 17 postconceptional weeks revealing the early differentiation of the subplate and subventricular zone. Cereb. Cortex 18 (2008) 1536-1548
13. Becker M., Nothwang H.G., and Friauf E. Differential expression pattern of chloride transporters NCC, NKCC2, KCC1, KCC3, KCC4, and AE3 in the developing rat auditory brainstem. Cell Tissue Res. 312 (2003) 155-165
14. Ben Ari Y., and Holmes G.L. Effects of seizures on developmental processes in the immature brain. Lancet Neurol. 5 (2006) 1055-1063
15. Ben-Ari Y., Cherubini E., Corradetti R., and Gaiarsa J.L. Giant synaptic potentials in immature rat CA3 hippocampal neurons. J. Physiol. 416 (1989) 303-325
16. Ben-Ari Y., Gaiarsa J.L., Tyzio R., and Khazipov R. GABA: a pioneer transmitter that excites immature neurons and generates primitive oscillations. Physiol. Rev. 87 (2007) 1215-1284
17. Bergeron M.J., Gagnon E., Caron L., and Isenring P. Identification of key functional domains in the C terminus of the K+-Cl- cotransporters. J. Biol. Chem. 281 (2006) 15959-15969
18. Berglund K., Schleich W., Krieger P., Loo L., Wang D., Cant N., Feng G., Augustine G., and Kuner T. Imaging synaptic inhibition in transgenic mice expressing the chloride indicator, Clomeleon. Brain Cell Biol. 35 (2006) 207-228
19. Blackburn-Munro G., and Erichsen H.K. Antiepileptics and the treatment of neuropathic pain: Evidence from animal models. Curr. Pharm. Des. 11 (2005) 2961-2976
20. Blaesse P., Guillemin I., Schindler J., Schweizer M., Delpire E., Khiroug L., Friauf E., and Nothwang H.G. Oligomerization of KCC2 correlates with development of inhibitory neurotransmission. J. Neurosci. 26 (2006) 10407-10419
21. Boettger T., Hübner C.A., Maier H., Rust M.B., Beck F.X., and Jentsch T.J. Deafness and renal tubular acidosis in mice lacking the K-Cl co-transporter Kcc4. Nature 416 (2002) 874-878
22. Boettger T., Rust M.B., Maier H., Seidenbecher T., Schweizer M., Keating D.J., Faulhaber J., Ehmke H., Pfeffer C., Scheel O., et al. Loss of K-Cl co-transporter KCC3 causes deafness, neurodegeneration and reduced seizure threshold. EMBO J. 22 (2003) 5422-5434
23. Bonislawski D.P., Schwarzbach E.P., and Cohen A.S. Brain injury impairs dentate gyrus inhibitory efficacy. Neurobiol. Dis. 25 (2007) 163-169
24. Brumback A.C., and Staley K.J. Thermodynamic regulation of NKCC1-mediated Cl- cotransport underlies plasticity of GABAA signaling in neonatal neurons. J. Neurosci. 28 (2008) 1301-1312
25. Buzsaki G., Kaila K., and Raichle M. Inhibition and brain work. Neuron 56 (2007) 771-783
26. Byun N., and Delpire E. Axonal and periaxonal swelling precede peripheral neurodegeneration in KCC3 knockout mice. Neurobiol. Dis. 28 (2007) 39-51
27. Cancedda L., Fiumelli H., Chen K., and Poo M.M. Excitatory GABA action is essential for morphological maturation of cortical neurons in vivo. J. Neurosci. 27 (2007) 5224-5235
28. Carmosino M., Gimenez I., Caplan M., and Forbush B. Exon loss accounts for differential sorting of Na-K-Cl cotransporters in polarized epithelial cells. Mol. Biol. Cell 19 (2008) 4341-4351
29. Casula S., Shmukler B.E., Wilhelm S., Stuart-Tilley A.K., Su W., Chernova M.N., Brugnara C., and Alper S.L. A dominant negative mutant of the KCC1 K-Cl cotransporter: both N- and C-terminal cytoplasmic domains are required for K-Cl cotransport activity. J. Biol. Chem. 276 (2001) 41870-41878
30. Chen H., Luo J., Kintner D.B., Shull G.E., and Sun D. Na+-dependent chloride transporter (NKCC1)-null mice exhibit less gray and white matter damage after focal cerebral ischemia. J. Cereb. Blood Flow Metab. 25 (2005) 54-66
31. Chesler M. Regulation and modulation of pH in the brain. Physiol. Rev. 83 (2003) 1183-1221
32. Chudotvorova I., Ivanov A., Rama S., Hübner C.A., Pellegrino C., Ben Ari Y., and Medina I. Early expression of KCC2 in rat hippocampal cultures augments expression of functional GABA synapses. J. Physiol. 566 (2005) 671-679
33. Clarkson J., and Herbison A.E. Development of GABA and glutamate signaling at the GnRH neuron in relation to puberty. Mol. Cell. Endocrinol. 254 (2006) 32-38
34. Clayton G.H., Owens G.C., Wolff J.S., and Smith R.L. Ontogeny of cation-Cl- cotransporter expression in rat neocortex. Brain Res. Dev. Brain Res. 109 (1998) 281-292
35. Cohen I., Navarro V., Clemenceau S., Baulac M., and Miles R. On the origin of interictal activity in human temporal lobe epilepsy in vitro. Science 298 (2002) 1418-1421
36. Colmenero-Flores J.M., Martinez G., Gamba G., Vazquez N., Iglesias D.J., Brumos J., and Talon M. Identification and functional characterization of cation-chloride cotransporters in plants. Plant J. 50 (2007) 278-292
37. Coull J.A., Boudreau D., Bachand K., Prescott S.A., Nault F., Sik A., De Koninck P., and De Koninck Y. Trans-synaptic shift in anion gradient in spinal lamina I neurons as a mechanism of neuropathic pain. Nature 424 (2003) 938-942
38. Coull J.A.M., Beggs S., Boudreau D., Boivin D., Tsuda M., Inoue K., Gravel C., Salter M.W., and De Koninck Y. BDNF from microglia causes the shift in neuronal anion gradient underlying neuropathic pain. Nature 438 (2005) 1017-1021
39. De Koninck Y. Altered chloride homeostasis in neurological disorders: a new target. Curr. Opin. Pharmacol. 7 (2007) 93-99
40. Delpire E., and Mount D.B. Human and murine phenotypes associated with defects in cation-chloride cotransport. Annu. Rev. Physiol. 64 (2002) 803-843
41. Delpire E., and Gagnon K.B.E. SPAK and OSR1: STE20 kinases involved in the regulation of ion homoeostasis and volume control in mammalian cells. Biochem. J. 409 (2008) 321-331
42. Delpire E., Lu J.M., England R., Dull C., and Thorne T. Deafness and imbalance associated with inactivation of the secretory Na-K-2Cl co-transporter. Nat. Genet. 22 (1999) 192-195
43. Delpire E., Days E., Lewis M., Mi D., Kim K., Lindsley C.W., and Weaver C.D. Small molecule screen identifies inhibitors for the neuronal K-Cl cotransporter KCC2. Proc. Natl. Acad. Sci. USA (2009) 10.1073/pnas.0812756106 in press
44. Demarque M., Represa A., Becq H., Khalilov I., Ben Ari Y., and Aniksztejn L. Paracrine intercellular communication by a Ca2+- and SNARE-independent release of GABA and glutamate prior to synapse formation. Neuron 36 (2002) 1051-1061
45. Denker S.P., and Barber D.L. Ion transport proteins anchor and regulate the cytoskeleton. Curr. Opin. Cell Biol. 14 (2002) 214-220
46. Dixon M.J., Gazzard J., Chaudhry S.S., Sampson N., Schulte B.A., and Steel K.P. Mutation of the Na-K-Cl co-transporter gene Slc12a2 results in deafness in mice. Hum. Mol. Genet. 8 (1999) 1579-1584
47. Duebel J., Haverkamp S., Schleich W., Feng G., Augustine G.J., Kuner T., and Euler T. Two-photon imaging reveals somatodendritic chloride gradient in retinal ON-type bipolar cells expressing the biosensor clomeleon. Neuron 49 (2006) 81-94
48. Dzhala V.I., Talos D.M., Sdrulla D.A., Brumback A.C., Mathews G.C., Benke T.A., Delpire E., Jensen F.E., and Staley K.J. NKCC1 transporter facilitates seizures in the developing brain. Nat. Med. 11 (2005) 1205-1213
49. Dzhala V.I., Brumback A.C., and Staley K.J. Bumetanide enhances phenobarbital efficacy in a neonatal seizure model. Ann. Neurol. 63 (2008) 222-235
50. Esposito M.S., Piatti V.C., Laplagne D.A., Morgenstern N.A., Ferrari C.C., Pitossi F.J., and Schinder A.F. Neuronal differentiation in the adult hippocampus recapitulates embryonic development. J. Neurosci. 25 (2005) 10074-10086
51. Farrant M., and Kaila K. The cellular, molecular and ionic basis of GABAA receptor signalling. Prog. Brain Res. 160 (2007) 59-87
52. Fiumelli H., and Woodin M.A. Role of activity-dependent regulation of neuronal chloride homeostasis in development. Curr. Opin. Neurol. 17 (2007) 81-86
53. Fiumelli H., Cancedda L., and Poo M.M. Modulation of GABAergic transmission by activity via postsynaptic Ca2+-dependent regulation of KCC2 function. Neuron 48 (2005) 773-786
54. Flagella M., Clarke L.L., Miller M.L., Erway L.C., Giannella R.A., Andringa A., Gawenis L.R., Kramer J., Duffy J.J., Doetschman T., et al. Mice lacking the basolateral Na-K-2Cl cotransporter have impaired epithelial chloride secretion and are profoundly deaf. J. Biol. Chem. 274 (1999) 26946-26955
55. Flatman P.W. Cotransporters, WNKs and hypertension: an update. Curr. Opin. Nephrol. Hypertens. 17 (2008) 186-192
56. Flemmer A.W., Gimenez I., Dowd B.F.X., Darman R.B., and Forbush B. Activation of the Na-K-Cl cotransporter NKCC1 detected with a phospho-specific antibody. J. Biol. Chem. 277 (2002) 37551-37558
57. Freund T.F., and Buzsaki G. Interneurons of the hippocampus. Hippocampus 6 (1996) 347-470
58. Fukuda A., Muramatsu K., Okabe A., Shimano Y., Hida H., Fujimoto I., and Nishino H. Changes in intracellular Ca2+ induced by GABAA receptor activation and reduction in Cl- gradient in neonatal rat neocortex. J. Neurophysiol. 79 (1998) 439-446
59. Galanopoulou A.S. Dissociated gender-specific effects of recurrent seizures on GABA signaling in CA1 pyramidal neurons: role of GABAA receptors. J. Neurosci. 28 (2008) 1557-1567
60. Gamba G. Molecular physiology and pathophysiology of electroneutral cation-chloride cotransporters. Physiol. Rev. 85 (2005) 423-493
61. Ganguly K., Schinder A.F., Wong S.T., and Poo M.M. GABA itself promotes the developmental switch of neuronal GABAergic responses from excitation to inhibition. Cell 105 (2001) 521-532
62. Gao X.B., Chen G., and van den Pol A.N. GABA-dependent firing of glutamate-evoked action potentials at AMPA/kainate receptors in developing hypothalamic neurons. J. Neurophysiol. 79 (1998) 716-726
63. Gavrikov K.E., Dmitriev A.V., Keyser K.T., and Mangel S.C. Cation-chloride cotransporters mediate neural computation in the retina. Proc. Natl. Acad. Sci. USA 100 (2003) 16047-16052
64. Ge S., Goh E.L.K., Sailor K.A., Kitabatake Y., Ming G.L., and Song H. GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 439 (2006) 589-593
65. Gerelsaikhan T., and Turner R.J. Transmembrane topology of the secretory Na+-K+-2Cl- cotransporter NKCC1 studied by in vitro translation. J. Biol. Chem. 275 (2000) 40471-40477
66. Glickfeld L.L., Roberts J.D., Somogyi P., and Scanziani M. Interneurons hyperpolarize pyramidal cells along their entire somatodendritic axis. Nat. Neurosci. 12 (2009) 21-23
67. Gonzalez-Islas C.E., Chub N.L., and Wenner P. NKCC1 and AE3 appear to accumulate chloride in embryonic motoneurons. J. Neurophysiol. 101 (2008) 507-518
68. Gulledge A.T., and Stuart G.J. Excitatory actions of GABA in the cortex. Neuron 37 (2003) 299-309
69. Gulyas A.I., Sik A., Payne J.A., Kaila K., and Freund T.F. The KCI cotransporter, KCC2, is highly expressed in the vicinity of excitatory synapses in the rat hippocampus. Eur. J. Neurosci. 13 (2001) 2205-2217
70. Haglund M.M., and Hochman D.W. Furosemide and mannitol suppression of epileptic activity in the human brain. J. Neurophysiol. 94 (2005) 907-918
71. Heck N., Kilb W., Reiprich P., Kubota H., Furukawa T., Fukuda A., and Luhmann H.J. GABA-A receptors regulate neocortical neuronal migration in vitro and in vivo. Cereb. Cortex 17 (2007) 138-148
72. Hekmat-Scafe D.S., Lundy M.Y., Ranga R., and Tanouye M.A. Mutations in the K+/Cl- cotransporter gene kazachoc (kcc) increase seizure susceptibility in Drosophila. J. Neurosci. 26 (2006) 8943-8954
73. Hennou S., Khalilov I., Diabira D., Ben Ari Y., and Gozlan H. Early sequential formation of functional GABA(A) and glutamatergic synapses on CA1 interneurons of the rat foetal hippocampus. Eur. J. Neurosci. 16 (2002) 197-208
74. Hensch T.K. Critical period plasticity in local cortical circuits. Nat. Rev. Neurosci. 6 (2005) 877-888
75. Hentschke M., Wiemann M., Hentschke S., Kurth I., Hermans-Borgmeyer I., Seidenbecher T., Jentsch T.J., Gal A., and Hübner C.A. Mice with a targeted disruption of the Cl-/HCO3- exchanger AE3 display a reduced seizure threshold. Mol. Cell. Biol. 26 (2006) 182-191
76. Hilgenberg L.G.W., Su H., Gu H., O'Dowd D.K., and Smith M.A. [alpha]3Na+/K+-ATPase is a neuronal receptor for agrin. Cell 125 (2006) 359-369
77. Hochman D.W., Baraban S.C., Owens J.W., and Schwartzkroin P.A. Dissociation of synchronization and excitability in furosemide blockade of epileptiform activity. Science 270 (1995) 99-102
78. Howard H.C., Mount D.B., Rochefort D., Byun N., Dupre N., Lu J., Fan X., Song L., Riviere J.B., Prevost C., et al. The K-Cl cotransporter KCC3 is mutant in a severe peripheral neuropathy associated with agenesis of the corpus callosum. Nat. Genet. 32 (2002) 384-392
79. Huberfeld G., Wittner L., Clemenceau S., Baulac M., Kaila K., Miles R., and Rivera C. Perturbed chloride homeostasis and GABAergic signaling in human temporal lobe epilepsy. J. Neurosci. 27 (2007) 9866-9873
80. Hübner C.A., Lorke D.E., and Hermans-Borgmeyer I. Expression of the Na-K-2Cl-cotransporter NKCC1 during mouse development. Mech. Dev. 102 (2001) 267-269
81. Hübner C.A., Stein V., Hermans-Borgmeyer I., Meyer T., Ballanyi K., and Jentsch T.J. Disruption of KCC2 reveals an essential role of K-Cl cotransport already in early synaptic inhibition. Neuron 30 (2001) 515-524
82. Ikeda K., Onimaru H., Yamada J., Inoue K., Ueno S., Onaka T., Toyoda H., Arata A., Ishikawa T., Taketo M.M., et al. Malfunction of respiratory-related neuronal activity in Na+, K+-ATPase alpha 2 subunit-deficient mice is attributable to abnormal Cl- homeostasis in brainstem neurons. J. Neurosci. 24 (2004) 10693-10701
83. Inoue K., Yamada J., Ueno S., and Fukuda A. Brain-type creatine kinase activates neuron-specific K+-Cl- co-transporter KCC2. J. Neurochem. 96 (2006) 598-608
84. Jang I.S., Jeong H.J., and Akaike N. Contribution of the Na-K-Cl cotransporter on GABAA receptor-mediated presynaptic depolarization in excitatory nerve terminals. J. Neurosci. 21 (2001) 5962-5972
85. Jang I.S., Nakamura M., Ito Y., and Akaike N. Presynaptic GABAA receptors facilitate spontaneous glutamate release from presynaptic terminals on mechanically dissociated rat CA3 pyramidal neurons. Neuroscience 138 (2006) 25-35
86. Jarolimek W., Lewen A., and Misgeld U. A furosemide-sensitive K+-Cl- cotransporter counteracts intracellular Cl- accumulation and depletion in cultured rat midbrain neurons. J. Neurosci. 19 (1999) 4695-4704
87. Jean-Xavier C., Mentis G.Z., O'Donovan M.J., Cattaert D., and Vinay L. Dual personality of GABA/glycine-mediated depolarizations in immature spinal cord. Proc. Natl. Acad. Sci. USA 104 (2007) 11477-11482
88. Jensen T.S. Anticonvulsants in neuropathic pain: rationale and clinical evidence. Eur. J. Pain 6 (2002) 61-68
89. Jin Y., Jorgensen E., Hartwieg E., and Horvitz H.R. The Caenorhabditis elegans gene unc-25 encodes glutamic acid decarboxylase and is required for synaptic transmission but not synaptic development. J. Neurosci. 19 (1999) 539-548
90. Jin X., Huguenard J.R., and Prince D.A. Impaired Cl- extrusion in layer V pyramidal neurons of chronically injured epileptogenic neocortex. J. Neurophysiol. 93 (2005) 2117-2126
91. Kahle K.T., Staley K.J., Nahed B.V., Gamba G., Hebert S.C., Lifton R.P., and Mount D.B. Roles of the cation-chloride cotransporters in neurological disease. Nat. Clin. Pract. Neurol. 4 (2008) 490-503
92. Kahle K.T., Ring A.M., and Lifton R.P. Molecular physiology of the WNK kinases. Annu. Rev. Physiol. 70 (2008) 329-355
93. Kaila K. Ionic basis of GABA(A) receptor channel function in the nervous system. Prog. Neurobiol. 42 (1994) 489-537
94. Kaila K., and Voipio J. Postsynaptic fall in intracellular pH induced by GABA-activated bicarbonate conductance. Nature 330 (1987) 163-165
95. Kaila K., Voipio J., Paalasmaa P., Pasternack M., and Deisz R.A. The role of bicarbonate in GABAA receptor-mediated IPSPs of rat neocortical neurones. J. Physiol. 464 (1993) 273-289
96. Kaila K., Lamsa K., Smirnov S., Taira T., and Voipio J. Long-lasting GABA-mediated depolarization evoked by high- frequency stimulation in pyramidal neurons of rat hippocampal slice is attributable to a network-driven, bicarbonate-dependent K+ transient. J. Neurosci. 17 (1997) 7662-7672
97. Kakazu Y., Akaike N., Komiyama S., and Nabekura J. Regulation of intracellular chloride by cotransporters in developing lateral superior olive neurons. J. Neurosci. 19 (1999) 2843-2851
98. Kakazu Y., Uchida S., Nakagawa T., Akaike N., and Nabekura J. Reversibility and cation selectivity of the K+-Cl- cotransport in rat central neurons. J. Neurophysiol. 84 (2000) 281-288
99. Kanaka C., Ohno K., Okabe A., Kuriyama K., Itoh T., Fukuda A., and Sato K. 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 (2001) 933-946
100. Kandler K., and Gillespie D.C. Developmental refinement of inhibitory sound-localization circuits. Trends Neurosci. 28 (2005) 290-296
101. Kaneko H., Putzier I., Frings S., Kaupp U.B., and Gensch T. Chloride accumulation in mammalian olfactory sensory neurons. J. Neurosci. 24 (2004) 7931-7938
102. Kanold P.O., and Shatz C.J. Subplate neurons regulate maturation of cortical inhibition and outcome of ocular dominance plasticity. Neuron 51 (2006) 627-638
103. Karadsheh M.F., and Delpire E. Neuronal restrictive silencing element is found in the KCC2 gene: molecular basis for KCC2-specific expression in neurons. J. Neurophysiol. 85 (2001) 995-997
104. Katchman A.N., Vicini S., and Hershkowitz N. Mechanism of early anoxia-induced suppression of the GABAA- mediated inhibitory postsynaptic current. J. Neurophysiol. 71 (1994) 1128-1138
105. Katz B. Nerve, Muscle and Synapse (1966), McGraw-Hill, New York
106. Katz L.C., and Shatz C.J. Synaptic activity and the construction of cortical circuits. Science 274 (1996) 1133-1138
107. Khalilov I., Dzhala V., Ben Ari Y., and Khazipov R. Dual role of GABA in the neonatal rat hippocampus. Dev. Neurosci. 21 (1999) 310-319
108. Khazipov R., Sirota A., Leinekugel X., Holmes G.L., Ben Ari Y., and Buzsaki G. Early motor activity drives spindle bursts in the developing somatosensory cortex. Nature 432 (2004) 758-761
109. Khirug S., Huttu K., Ludwig A., Smirnov S., Voipio J., Rivera C., Kaila K., and Khiroug L. Distinct properties of functional KCC2 expression in immature mouse hippocampal neurons in culture and in acute slices. Eur. J. Neurosci. 21 (2005) 899-904
110. Khirug S., Yamada J., Afzalov R., Voipio J., Khiroug L., and Kaila K. GABAergic depolarization of the axon initial segment in cortical principal neurons is caused by the Na-K-2Cl cotransporter NKCC1. J. Neurosci. 28 (2008) 4635-4639
111. Kilb W., Ikeda M., Uchida K., Okabe A., Fukuda A., and Luhmann H.J. Depolarizing glycine responses in Cajal-Retzius cells of neonatal rat cerebral cortex. Neuroscience 112 (2002) 299-307
112. Kilb W., Sinning A., and Luhmann H.J. Model-specific effects of bumetanide on epileptiform activity in the in-vitro intact hippocampus of the newborn mouse. Neuropharmacology 53 (2007) 524-533
113. Kohling R., Lucke A., Straub H., Speckmann E.J., Tuxhorn I., Wolf P., Pannek H., and Oppel F. Spontaneous sharp waves in human neocortical slices excised from epileptic patients. Brain 121 (1998) 1073-1087
114. Kyrozis A., and Reichling D.B. Perforated-patch recording with gramicidin avoids artifactual changes in intracellular chloride concentration. J. Neurosci. Methods 57 (1995) 27-35
115. Lamsa K., Palva J.M., Ruusuvuori E., Kaila K., and Taira T. Synaptic GABA(A) activation inhibits AMPA-kainate receptor-mediated bursting in the newborn (P0-P2) rat hippocampus. J. Neurophysiol. 83 (2000) 359-366
116. Laplagne D.A., Kamienkowski J.E., Esposito M.S., Piatti V.C., Zhao C., Gage F.H., and Schinder A.F. Similar GABAergic inputs in dentate granule cells born during embryonic and adult neurogenesis. Eur. J. Neurosci. 25 (2007) 2973-2981
117. Le Rouzic P., Ivanov T.R., Stanley P.J., Baudoin F.M.H., Chan F., Pinteaux E., Brown P.D., and Luckman S.M. KCC3 and KCC4 expression in rat adult forebrain. Brain Res. 1110 (2006) 39-45
118. Lee H.H.C., Walker J.A., Williams J.R., Goodier R.J., Payne J.A., and Moss S.J. Direct protein kinase C-dependent phosphorylation regulates the cell surface stability and activity of the potassium chloride cotransporter KCC2. J. Biol. Chem. 282 (2007) 29777-29784
119. Leitch E., Coaker J., Young C., Mehta V., and Sernagor E. GABA type-A activity controls its own developmental polarity switch in the maturing retina. J. Neurosci. 25 (2005) 4801-4805
120. Lessmann V., Gottmann K., and Malcangio M. Neurotrophin secretion: current facts and future prospects. Prog. Neurobiol. 69 (2003) 341-374
121. Li H., Tornberg J., Kaila K., Airaksinen M.S., and Rivera C. Patterns of cation-chloride cotransporter expression during embryonic rodent CNS development. Eur. J. Neurosci. 16 (2002) 2358-2370
122. Li H., Khirug S., Cai C., Ludwig A., Blaesse P., Kolikova J., Afzalov R., Coleman S.K., Lauri S., Airaksinen M.S., et al. KCC2 interacts with the dendritic cytoskeleton to promote spine development. Neuron 56 (2007) 1019-1033
123. Li B.Q., McKernan K., and Shen W. Spatial and temporal distribution patterns of Na-K-2C1 cotransporter in adult and developing mouse retinas. Vis. Neurosci. 25 (2008) 109-123
124. Liu X.X., Wang Q., Haydar T.F., and Bordey A. Nonsynaptic GABA signaling in postnatal subventricular zone controls proliferation of GFAP-expressing progenitors. Nat. Neurosci. 8 (2005) 1179-1187
125. Liu Z., Neff R.A., and Berg D.K. Sequential interplay of nicotinic and GABAergic signaling guides neuronal development. Science 314 (2006) 1610-1613
126. LoTurco J.J., Owens D.F., Heath M.J.S., Davis M.B.E., and Kriegstein A.R. GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis. Neuron 15 (1995) 1287-1298
127. Ludwig A., Li H., Saarma M., Kaila K., and Rivera C. Developmental up-regulation of KCC2 in the absence of GABAergic and glutamatergic transmission. Eur. J. Neurosci. 18 (2003) 3199-3206
128. Lytle C., and Forbush B. The Na-K-Cl cotransport protein of shark rectal gland. II. Regulation by direct phosphorylation. J. Biol. Chem. 267 (1992) 25438-25443
129. Lytle C., Xu J.C., Biemesderfer D., and Forbush B. Distribution and diversity of Na-K-Cl cotransport proteins: a study with monoclonal antibodies. Am. J. Physiol. 269 (1995) C1496-C1505
130. Martina M., Royer S., and Pare D. Cell-type-specific GABA responses and chloride homeostasis in the cortex and amygdala. J. Neurophysiol. 86 (2001) 2887-2895
131. Marty A., and Llano I. Excitatory effects of GABA in established brain networks. Trends Neurosci. 28 (2005) 284-289
132. Marty S., Berninger B., Carroll P., and Thoenen H. GABAergic stimulation regulates the phenotype of hippocampal interneurons through the regulation of brain-derived neurotrophic factor. Neuron 16 (1996) 565-570
133. Marty S., Wehrle R., and Sotelo C. Neuronal activity and brain-derived neurotrophic factor regulate the density of inhibitory synapses in organotypic slice cultures of postnatal hippocampus. J. Neurosci. 20 (2000) 8087-8095
134. Mercado A., Mount D.B., and Gamba G. Electroneutral cation-chloride cotransporters in the central nervous system. Neurochem. Res. 29 (2004) 17-25
135. Mikawa S., Wang C., Shu F., Wang T., Fukuda A., and Sato K. Developmental changes in KCC1, KCC2 and NKCC1 mRNAs in the rat cerebellum. Brain Res. Dev. Brain Res. 136 (2002) 93-100
136. Minlebaev M., Ben Ari Y., and Khazipov R. Network mechanisms of spindle-burst oscillations in the neonatal rat barrel cortex in vivo. J. Neurophysiol. 97 (2007) 692-700
137. Misgeld U., Deisz R.A., Dodt H.U., and Lux H.D. The role of chloride transport in postsynaptic inhibition of hippocampal neurons. Science 232 (1986) 1413-1415
138. Mulley J.C., Scheffer I.E., Petrou S., and Berkovic S.F. Channelopathies as a genetic cause of epilepsy. Curr. Opin. Neurol. 16 (2003) 171-176
139. Mulley J.C., Scheffer I.E., Harkin L.A., Berkovic S.F., and Dibbens L.M. Susceptibility genes for complex epilepsy. Hum. Mol. Genet. 14 (2005) R243-R249
140. Munoz A., Mendez P., DeFelipe J., and Alvarez-Leefmans F.J. Cation-chloride cotransporters and GABA-ergic innervation in the human epileptic hippocampus. Epilepsia 48 (2007) 663-673
141. Nabekura J., Ueno T., Okabe A., Furuta A., Iwaki T., Shimizu-Okabe C., Fukuda A., and Akaike N. Reduction of KCC2 expression and GABA(A) receptor-mediated excitation after in vivo axonal injury. J. Neurosci. 22 (2002) 4412-4417
142. O'Donovan M.J. The origin of spontaneous activity in developing networks of the vertebrate nervous system. Curr. Opin. Neurol. 9 (1999) 94-104
143. Obata K., Oide M., and Tanaka H. Excitatory and inhibitory actions of GABA and glycine on embryonic chick spinal neurons in culture. Brain Res. 144 (1978) 179-184
144. Owens D.F., and Kriegstein A.R. Is there more to GABA than synaptic inhibiton?. Nat. Rev. Neurosci. 3 (2002) 715-727
145. Owens D.F., Liu X.L., and Kriegstein A.R. Changing properties of GABA(A) receptor-mediated signaling during early neocortical development. J. Neurophysiol. 82 (1999) 570-583
146. Pace A.J., Lee E., Athirakul K., Coffman T.M., O'Brien D.A., and Koller B.H. Failure of spermatogenesis in mouse lines deficient in the Na+-K+-2Cl(-) cotransporter. J. Clin. Invest. 105 (2000) 441-450
147. Papp E., Rivera C., Kaila K., and Freund T.F. Relationship between neuronal vulnerability and potassium-chloride cotransporter 2 immunoreactivity in hippocampus following transient forebrain ischemia. Neuroscience 154 (2008) 677-689
148. Pathak H.R., Weissinger F., Terunuma M., Carlson G.C., Hsu F.C., Moss S.J., and Coulter D.A. Disrupted dentate granule cell chloride regulation enhances synaptic excitability during development of temporal lobe epilepsy. J. Neurosci. 27 (2007) 14012-14022
149. Payne J.A. Functional characterization of the neuronal-specific K-Cl cotransporter - implications for [K+](o) regulation. Am. J. Physiol. 42 (1997) C1516-C1525
150. Payne J.A., Stevenson T.J., and Donaldson L.F. Molecular characterization of a putative K-Cl cotransporter in rat brain. A neuronal-specific isoform. J. Biol. Chem. 271 (1996) 16245-16252
151. Payne J.A., Rivera C., Voipio J., and Kaila K. Cation-chloride co-transporters in neuronal communication, development and trauma. Trends Neurosci. 26 (2003) 199-206
152. Pearson M.M., Lu J., Mount D.B., and Delpire E. Localization of the K-Cl-cotransporter, KCC3, in the central and peripheral nervous systems: expression in the choroid plexus, large neurons and white matter tracts. Neuroscience 103 (2001) 481-491
153. Pedersen S.F., O'Donnell M.E., Anderson S.E., and Cala P.M. Physiology and pathophysiology of Na+/H+ exchange and Na+-K+-2Cl- cotransport in the heart, brain, and blood. Am. J. Physiol. 291 (2006) R1-R25
154. Pedersen M., Carmosino M., and Forbush B. Intramolecular and intermolecular fluorescence resonance energy transfer in fluorescent protein-tagged Na-K-Cl cotransporter (NKCC1): sensitivity to regulatory conformational change and cell volume. J. Biol. Chem. 283 (2008) 2663-2674
155. Perrot-Sinal T.S., Sinal C.J., Reader J.C., Speert D.B., and McCarthy M.M. Sex differences in the chloride cotransporters, NKCC1 and KCC2, in the developing hypothalamus. J. Neuroendocrinol. 19 (2007) 302-308
156. Pieraut S., Laurent-Matha V., Sar C., Hubert T., Mechaly I., Hilaire C., Mersel M., Delpire E., Valmier J., and Scamps F. NKCC1 phosphorylation stimulates neurite growth of injured adult sensory neurons. J. Neurosci. 27 (2007) 6751-6759
157. Plotkin M.D., Snyder E.Y., Hebert S.C., and Delpire E. 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. J. Neurobiol. 33 (1997) 781-795
158. Pond B.B., Berglund K., Kuner T., Feng G.P., Augustine G.J., and Schwartz-Bloom R.D. The chloride transporter Na+-K+-Cl- cotransporter isoform-1 contributes to intracellular chloride increases after in vitro ischemia. J. Neurosci. 26 (2006) 1396-1406
159. Praetorius J. Water and solute secretion by the choroid plexus. Pflugers Arch. 454 (2007) 1-18
160. Price G.D., and Trussell L.O. Estimate of the chloride concentration in a central glutamatergic terminal: a gramicidin perforated-patch study on the Calyx of Held. J. Neurosci. 26 (2006) 11432-11436
161. Price T.J., Cervero F., and De Koninck Y. Role of cation-chloride-cotransporters (CCC) in pain and hyperalgesia. Curr. Top. Med. Chem. 5 (2005) 547-555
162. Pylova S.I., Majkowska J., Hilgier W., Kapuscinski A., and Albrecht J. Rapid decrease of high-affinity ouabain binding-sites in hippocampal CA1 region following short-term global cerebral-ischemia in rat. Brain Res. 490 (1989) 170-173
163. Randall J., Thorne T., and Delpire E. Partial cloning and characterization of Slc12a2: the gene encoding the secretory Na+-K+-2Cl- cotransporter. Am. J. Physiol. 273 (1997) C1267-C1277
164. Reisert J., Lai J., Yau K.W., and Bradley J. Mechanism of the excitatory Cl- response in mouse olfactory receptor neurons. Neuron 45 (2005) 553-561
165. Rennie J., and Boylan G. Treatment of neonatal seizures. Arch. Dis. Child. 92 (2007) F148-F150
166. Represa A., and Ben Ari Y. Trophic actions of GABA on neuronal development. Trends Neurosci. 28 (2005) 278-283
167. Reynolds A., Brustein E., Liao M., Mercado A., Babilonia E., Mount D.B., and Drapeau P. Neurogenic role of the depolarizing chloride gradient revealed by global overexpression of KCC2 from the onset of development. J. Neurosci. 28 (2008) 1588-1597
168. Rheims S., Minlebaev M., Ivanov A., Represa A., Khazipov R., Holmes G.L., Ben Ari Y., and Zilberter Y. Excitatory GABA in rodent developing neocortex in vitro. J. Neurophysiol. 100 (2008) 609-619
169. Riekki R., Pavlov I., Tornberg J., Lauri S.E., Airaksinen M.S., and Taira T. Altered Synaptic Dynamics and Hippocampal Excitability but Normal Long-Term Plasticity in Mice Lacking Hyperpolarizing GABAA Receptor-Mediated Inhibition in CA1 Pyramidal Neurons. J. Neurophysiol. 99 (2008) 3075-3089
170. Rivera C., Voipio J., Payne J.A., Ruusuvuori E., Lahtinen H., Lamsa K., Pirvola U., Saarma M., and Kaila K. The K+/Cl- co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 397 (1999) 251-255
171. Rivera C., Li H., Thomas-Crusells J., Lahtinen H., Viitanen T., Nanobashvili A., Kokaia Z., Airaksinen M.S., Voipio J., Kaila K., and Saarma M. BDNF-induced TrkB activation down-regulates the K+-Cl- cotransporter KCC2 and impairs neuronal Cl- extrusion. J. Cell Biol. 159 (2002) 747-752
172. Rivera C., Voipio J., Thomas-Crusells J., Li H., Emri Z., Sipilä S., Payne J.A., Minichiello L., Saarma M., and Kaila K. Mechanism of activity-dependent downregulation of the neuron-specific K-Cl cotransporter KCC2. J. Neurosci. 24 (2004) 4683-4691
173. Rocha-Gonzalez H.I., Mao S., and Alvarez-Leefmans F.J. Na+, K+, 2Cl(-) cotransport and intracellular chloride regulation in rat primary sensory neurons: Thermodynamic and kinetic aspects. J. Neurophysiol. 100 (2008) 169-184
174. Rogawski M.A., and Loscher W. The neurobiology of antiepileptic drugs for the treatment of nonepileptic conditions. Nat. Med. 10 (2004) 685-692
175. Rohrbough J., and Spitzer N.C. Regulation of intracellular Cl- levels by Na(+)-dependent Cl- cotransport distinguishes depolarizing from hyperpolarizing GABAA receptor-mediated responses in spinal neurons. J. Neurosci. 16 (1996) 82-91
176. Romero M.F., Fulton C.M., and Boron W.F. The SLC4 family of HCO3- transporters. Pflugers Arch. 447 (2004) 495-509
177. Romo-Parra H., Trevino M., Heinemann U., and Gutierrez R. GABA actions in hippocampal area CA3 during postnatal development: Differential shift from depolarizing to hyperpolarizing in somatic and dendritic compartments. J. Neurophysiol. 99 (2008) 1523-1534
178. Ross S.T., and Soltesz I. Selective depolarization of interneurons in the early posttraumatic dentate gyrus: involvement of the Na(+)/K(+)-ATPase. J. Neurophysiol. 83 (2000) 2916-2930
179. Rudomin P., and Schmidt R.F. Presynaptic inhibition in the vertebrate spinal cord revisited. Exp. Brain Res. 129 (1999) 1-37
180. Russell J.M. Sodium-potassium-chloride cotransport. Physiol. Rev. 80 (2000) 211-276
181. Rust M.B., Faulhaber J., Budack M.K., Pfeffer C., Maritzen T., Didie M., Beck F.X., Boettger T., Schubert R., Ehmke H., et al. Neurogenic mechanisms contribute to hypertension in mice with disruption of the K-Cl cotransporter KCC3. Circ. Res. 98 (2006) 549-556
182. Rust M.B., Alper S.L., Rudhard Y., Shmukler B.E., Vicente R., Brugnara C., Trudel M., Jentsch T.J., and Hübner C.A. Disruption of erythroid K-Cl cotransporters alters erythrocyte volume and partially rescues erythrocyte dehydration in SAD mice. J. Clin. Invest. 117 (2007) 1708-1717
183. Saier M.H. Tracing pathways of transport protein evolution. Mol. Microbiol. 48 (2003) 1145-1156
184. Salin-Cantegrel A., Shekarabi M., Holbert S., Dion P., Rochefort D., Laganiere J., Dacal S., Hince P., Karemera L., Gaspar C., et al. HMSN/ACC truncation mutations disrupt brain-type creatine kinase-dependant activation of K+/Cl- cotransporter 3. Hum. Mol. Genet. 17 (2008) 2703-2711
185. Serafini R., Valeyev A.Y., Barker J.L., and Poulter M.O. Depolarizing GABA-activated Cl- channels in embryonic rat spinal and olfactory bulb cells. J. Physiol. 488 (1995) 371-386
186. Shulga A., Thomas-Crusells J., Sigl T., Blaesse A., Mestres P., Meyer M., Yan Q., Kaila K., Saarma M., Rivera C., and Giehl K.M. Posttraumatic GABAA-mediated [Ca2+]i increase is essential for the induction of brain-derived neurotrophic factor-dependent survival of mature central neurons. J. Neurosci. 28 (2008) 6996-7005
187. Simard C.F., Bergeron M.J., Frenette-Cotton R., Carpentier G.A., Pelchat M.E., Caron L., and Isenring P. Homooligomeric and heterooligomeric associations between K+-Cl- Cotransporter isoforms and between K+-Cl- and Na+-K+-Cl- cotransporters. J. Biol. Chem. 282 (2007) 18083-18093
188. Simat M., Ambrosetti L., Lardi-Studler B., and Fritschy J.M. GABAergic synaptogenesis marks the onset of differentiation of basket and stellate cells in mouse cerebellum. Eur. J. Neurosci. 26 (2007) 2239-2256
189. Sipilä S.T., Huttu K., Soltesz I., Voipio J., and Kaila K. Depolarizing GABA acts on intrinsically bursting pyramidal neurons to drive giant depolarizing potentials in the immature hippocampus. J. Neurosci. 25 (2005) 5280-5289
190. Sipilä S.T., Schuchmann S., Voipio J., Yamada J., and Kaila K. The cation-chloride cotransporter NKCC1 promotes sharp waves in the neonatal rat hippocampus. J. Physiol. 573 (2006) 765-773
191. Spitzer N.C. Electrical activity in early neuronal development. Nature 444 (2006) 707-712
192. Staley K.J. Diuretics as antiepileptic drugs: should we go with the flow?. Epilepsy Curr. 2 (2002) 35-38
193. Stein V., Hermans-Borgmeyer I., Jentsch T.J., and Hübner C.A. Expression of the KC1 cotransporter KCC2 parallels neuronal maturation and the emergence of low intracellular chloride. J. Comp. Neurol. 468 (2004) 57-64
194. Stell B.M., Rostaing P., Triller A., and Marty A. Activation of presynaptic GABAA receptors induces glutamate release from parallel fiber synapses. J. Neurosci. 27 (2007) 9022-9031
195. Szabadics J., Varga C., Molnar G., Olah S., Barzo P., and Tamas G. Excitatory effect of GABAergic axo-axonic cells in cortical microcircuits. Science 311 (2006) 233-235
196. Thompson S.M., and Gähwiler B.H. Activity-dependent disinhibition. II. Effects of extracellular potassium, furosemide, and membrane potential on ECl- in hippocampal CA3 neurons. J. Neurophysiol. 61 (1989) 512-523
197. Titz S., Hans M., Kelsch W., Lewen A., Swandulla D., and Misgeld U. Hyperpolarizing inhibition develops without trophic support by GABA in cultured rat midbrain neurons. J. Physiol. 550 (2003) 719-730
198. Toni N., Laplagne D.A., Zhao C., Lombardi G., Ribak C.E., Gage F.H., and Schinder A.F. Neurons born in the adult dentate gyrus form functional synapses with target cells. Nat. Neurosci. 11 (2008) 901-907
199. Tornberg J., Voikar V., Savilahti H., Rauvala H., and Airaksinen M.S. Behavioural phenotypes of hypomorphic KCC2-deficient mice. Eur. J. Neurosci. 21 (2005) 1327-1337
200. Tozuka Y., Fukuda S., Namba T., Seki T., and Hisatsune T. GABAergic excitation promotes neuronal differentiation in adult hippocampal progenitor cells. Neuron 47 (2005) 803-815
201. Trevino M., and Gutierrez R. The GABAergic projection of the dentate gyrus to hippocampal area CA3 of the rat: pre- and postsynaptic actions after seizures. J. Physiol. 567 (2005) 939-949
202. Tyzio R., Cossart R., Khalilov I., Minlebaev M., Hübner C.A., Represa A., Ben Ari Y., and Khazipov R. Maternal oxytocin triggers a transient inhibitory switch in GABA signaling in the fetal brain during delivery. Science 314 (2006) 1788-1792
203. Tyzio R., Minlebaev M., Rheims S., Ivanov A., Jorquera I., Holmes G.L., Zilberter Y., Ben Ari Y., and Khazipov R. Postnatal changes in somatic gamma-aminobutyric acid signalling in the rat hippocampus. Eur. J. Neurosci. 27 (2008) 2515-2528
204. Uvarov P., Pruunsild P., Timmusk T., and Airaksinen M.S. Neuronal K+/Cl- co-transporter (KCC2) transgenes lacking neurone restrictive silencer element recapitulate CNS neurone-specific expression and developmental up-regulation of endogenous KCC2 gene. J. Neurochem. 95 (2005) 1144-1155
205. Uvarov P., Ludwig A., Markkanen M., Rivera C., and Airaksinen M.S. Upregulation of the neuron-specific K+/Cl- cotransporter expression by transcription factor early growth response 4. J. Neurosci. 26 (2006) 13463-13473
206. Uvarov P., Ludwig A., Markkanen M., Pruunsild P., Kaila K., Delpire E., Timmusk T., Rivera C., and Airaksinen M.S. A novel N-terminal isoform of the neuron-specific K-Cl cotransporter KCC2. J. Biol. Chem. 282 (2007) 30570-30576
207. Vale C., Caminos E., Martinez-Galan J.R., and Juiz J.M. Expression and developmental regulation of the K+-Cl- cotransporter KCC2 in the cochlear nucleus. Hear. Res. 206 (2005) 107-115
208. van den Pol A.N., Obrietan K., and Chen G. Excitatory actions of GABA after neuronal trauma. J. Neurosci. 16 (1996) 4283-4292
209. Vanhatalo S., Palva J.M., Andersson S., Rivera C., Voipio J., and Kaila K. Slow endogenous activity transients and developmental expression of K+-Cl- cotransporter 2 in the immature human cortex. Eur. J. Neurosci. 22 (2005) 2799-2804
210. Vardi N., Zhang L.L., Payne J.A., and Sterling P. Evidence that different cation chloride cotransporters in retinal neurons allow opposite responses to GABA. J. Neurosci. 20 (2000) 7657-7663
211. Varoqueaux F., Sigler A., Rhee J.S., Brose N., Enk C., Reim K., and Rosenmund C. Total arrest of spontaneous and evoked synaptic transmission but normal synaptogenesis in the absence of Munc13-mediated vesicle priming. Proc. Natl. Acad. Sci. USA 99 (2002) 9037-9042
212. Verhage M., Maia A.S., Plomp J.J., Brussaard A.B., Heeroma J.H., Vermeer H., Toonen R.F., Hammer R.E., van den Berg T.K., Missler M., et al. Synaptic assembly of the brain in the absence of neurotransmitter secretion. Science 287 (2000) 864-869
213. Verkman A.S. Development and biological applications of chloride-sensitive fluorescent indicators. Am. J. Physiol. 259 (1990) C375-C388
214. Vibat C.R.T., Holland M.J., Kang J.J., Putney L.K., and O'Donnell M.E. Quantitation of Na+-K+-2Cl(-) cotransport splice variants in human tissues using kinetic polymerase chain reaction. Anal. Biochem. 298 (2001) 218-230
215. Vinay L., and Jean-Xavier C. Plasticity of spinal cord locomotor networks and contribution of cation-chloride cotransporters. Brain Res. Brain Res. Rev. 57 (2008) 103-110
216. Voipio J., and Kaila K. GABAergic excitation and K(+)-mediated volume transmission in the hippocampus. Prog. Brain Res. 125 (2000) 329-338
217. Wake H., Watanabe M., Moorhouse A.J., Kanematsu T., Horibe S., Matsukawa N., Asai K., Ojika K., Hirata M., and Nabekura J. Early changes in KCC2 phosphorylation in response to neuronal stress result in functional downregulation. J. Neurosci. 27 (2007) 1642-1650
218. Wang D.D., and Kriegstein A.R. GABA regulates excitatory synapse formation in the neocortex via NMDA receptor activation. J. Neurosci. 28 (2008) 5547-5558
219. Wang D.D., and Kriegstein A.R. Defining the Role of GABA in Cortical Development. J. Physiol. (2009) in press. Published online January 19, 2009. jphysiol.2008.167635v1
220. Wang C., Shimizu-Okabe C., Watanabe K., Okabe A., Matsuzaki H., Ogawa T., Mori N., Fukuda A., and Sato K. Developmental changes in KCC1, KCC2, and NKCC1 mRNA expressions in the rat brain. Brain Res. Dev. Brain Res. 139 (2002) 59-66
221. Wardle R.A., and Poo M.M. Brain-derived neurotrophic factor modulation of GABAergic synapses by postsynaptic regulation of chloride transport. J. Neurosci. 23 (2003) 8722-8732
222. Waxman S.G. Channel, neuronal and clinical function in sodium channelopathies: from genotype to phenotype. Nat. Neurosci. 10 (2007) 405-409
223. Williams J.R., and Payne J.A. Cation transport by the neuronal K+-Cl- cotransporter KCC2: thermodynamics and kinetics of alternate transport modes. Am. J. Physiol. 287 (2004) C919-C931
224. Williams J.R., Sharp J.W., Kumari V.G., Wilson M., and Payne J.A. The neuron-specific K-Cl cotransporter, KCC2. Antibody development and initial characterization of the protein. J. Biol. Chem. 274 (1999) 12656-12664
225. Wojcik S.M., Katsurabayashi S., Guillemin I., Friauf E., Rosenmund C., Brose N., and Rhee J.S. A shared vesicular carrier allows synaptic corelease of GABA and glycine. Neuron 50 (2006) 575-587
226. Woo N.S., Lu J.M., England R., McClellan R., Dufour S., Mount D.B., Deutch A.Y., Lovinger D.M., and Delpire E. Hyperexcitability and epilepsy associated with disruption of the mouse neuronal-specific K-Cl cotransporter gene. Hippocampus 12 (2002) 258-268
227. Woodin M.A., Ganguly K., and Poo M.M. Coincident pre- and postsynaptic activity modifies GABAergic synapses by postsynaptic changes in Cl- transporter activity. Neuron 39 (2003) 807-820
228. Xu J.C., Lytle C., Zhu T.T., Payne J.A., Benz E.J., and Forbush B. Molecular cloning and functional expression of the bumetanide-sensitive Na-K-Cl cotransporter. Proc. Natl. Acad. Sci. USA 91 (1994) 2201-2205
229. Yamada J., Okabe A., Toyoda H., Kilb W., Luhmann H.J., and Fukuda A. Cl- uptake promoting depolarizing GABA actions in immature rat neocortical neurones is mediated by NKCC1. J. Physiol. 557 (2004) 829-841
230. Yan Y., Dempsey R.J., and Sun D. Expression of Na+-K+-Cl- cotransporter in rat brain during development and its localization in mature astrocytes. Brain Res. 911 (2001) 43-55
231. Yan Y.P., Dempsey R.J., and Sun D. Na+-K+-Cl- cotransporter in rat focal cerebral ischemia. J. Cereb. Blood Flow Metab. 21 (2001) 711-721
232. Zhang L.L., Fina M.E., and Vardi N. Regulation of KCC2 and NKCC during development: Membrane insertion and differences between cell types. J. Comp. Neurol. 499 (2006) 132-143
233. Zhang L.L., Delpire E., and Vardi N. NKCC1 does not accumulate chloride in developing retinal neurons. J. Neurophysiol. 98 (2007) 266-277
234. Zheng J.J., Lee S., and Zhou Z.J. A transient network of intrinsically bursting starburst cells underlies the generation of retinal waves. Nat. Neurosci. 9 (2006) 363-371
235. Zhu L., Lovinger D., and Delpire E. Cortical neurons lacking KCC2 expression show impaired regulation of intracellular chloride. J. Neurophysiol. 93 (2005) 1557-1568