Cortical neurons lacking KCC2 expression show impaired regulation of intracellular chloride

Journal of Neurophysiology

Volumn 93, Issue 3, 2005, Pages 1557-1568

  Zhu, Lei ^a   Lovinger, David ^b   Delpire, Eric ^a  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^b NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); CATION; CHLORIDE; CHLORIDE CHANNEL; COTRANSPORTER; GLYCINE RECEPTOR; LIGAND; PROTEIN KCC2; UNCLASSIFIED DRUG;

ACTION POTENTIAL; ANIMAL CELL; ARTICLE; BRAIN CELL; CHLORIDE TRANSPORT; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENZYME ACTIVITY; HYPERPOLARIZATION; ION TRANSPORT; MEMBRANE CHANNEL; MEMBRANE DEPOLARIZATION; MEMBRANE POTENTIAL; MOUSE; NERVE CELL EXCITABILITY; NONHUMAN; POTASSIUM TRANSPORT; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; SYNAPTIC TRANSMISSION;

ANIMALS; ANIMALS, NEWBORN; CELLS, CULTURED; CEREBRAL CORTEX; CHLORIDES; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; EXTRACELLULAR SPACE; FLUORESCENT ANTIBODY TECHNIQUE; FUROSEMIDE; GAMMA-AMINOBUTYRIC ACID; HOMOZYGOTE; MEMBRANE POTENTIALS; MICE; MICE, KNOCKOUT; MICROTUBULE-ASSOCIATED PROTEINS; NEURONS; PATCH-CLAMP TECHNIQUES; POTASSIUM; SYMPORTERS; TIME FACTORS;

EID: 14144253198     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.00616.2004     Document Type: Article

References (56)

1. Alvarez-Leefmans FJ, Gamiño SM, Giraldez F, and Nogueron I. Intracellular chloride regulation in amphibian dorsal root ganglion neurons studied with ion-selective microelectrodes. J Physiol 406: 225-246, 1988.
2. Balakrishnan V, Becker M, Lohrke S, Nothwang HG, Guresir E, and Friauf E. Expression and function of chloride transporters during development of inhibitory neurotransmission in the auditory brainstem. J Neurosci 23: 4134-4145, 2003.
3. Baughman RW, Huettner JE, Jones KA, and Khan AA. Cell culture of neocortex and basal forebrain from postnatal rats. In: Culturing Nerve Cells, edited by Banker G and Goslin K. Cambridge, MA: MIT Press, 1991, p. 227-249.
4. Ben-Ari Y, Cherubini E, Corradetti R, and Gaiarsa JL. Giant synaptic potentials in immature rat CA3 hippocampal neurones. J Physiol 416: 303-325, 1989.
5. Ben-Ari Y, Tseeb V, Raggozzino D, Khazipov R, and Gaiarsa JL. g-Aminobutyric acid (GABA): a fast excitatory transmitter which may regulate the development of hippocampal neurones in early postnatal life. Prog Brain Res 102: 261-273, 1994.
6. - co-transporter expression in rat neocortex. Brain Res Dev Brain Res 109: 281-292, 1998.
7. Coull JA, Boudreau D, Bachand K, Prescott SA, 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: 938-942, 2003.
8. BeFazio RA, Keros S, Quick MW, and Hablitz JJ. Potassium-coupled chloride co-transport controls intracellular chloride in rat neocortical pyramidal neurons. J Neurosci 20: 8069-8076, 2000.
9. Delpire E, Lu J, England R, Dull C, and Thorne T. Deafness and imbalance associated with inactivation of the secretory Na-K-2Cl co-transporter. Nat Genet 22: 192-195, 1999.
10. Ehrlich I, Lohrke S, and Friauf E. Shift from depolarizing to hyperpolarizing glycine action in rat auditory neurones is due to age-dependent CP regulation. J Physiol 520: 121-137, 1999.
11. A receptor activation and reduction in Cl- gradient in neonatal rat neocortex. J Neurophysiol 79: 439-446, 1998.
12. Ganguly K, Schinder AF, Wong ST, and Poo M. GABA itself promotes the developmental switch of neuronal GABAergic responses from excitation to inhibition. Cell 105: 521-532, 2001.
13. Gulyas AI, Sik A, Payne JA, Kaila K, and Freund TF. The KCl co-transporter, KCC2, is highly expressed in the vicinity of excitatory synapses in the rat hippocampus. Eur J Neurosci 13: 2205-2217, 2001.
14. Hubner CA, Stein V, Hermans-Borgmeyer I, Meyer T, Ballanyi K, and Jentsch TJ. Disruption of KCC2 reveals an essential role of K-Cl co-transport already in early synaptic inhibition. Neuron 30: 515-524, 2001.
15. Huettner JE and Baughman RW. Primary culture of identified neurons from the visual cortex of postnatal rats. J Neurosci 6: 3044-3060, 1986.
16. Janigro D and Schwartzkroin PA. Effects of GABA and baclofen on pyramidal cells in the developing rabbit hippocampus: an in vitro study. Dev Brain Res 41: 171-184, 1988.
17. Kakazu Y, Uchida S, Nakagawa T, Akaike N, and Nabekura J. Reversibility and cation selectivity of the K(+)-Cl(-) co-transport in rat central neurons. J Neurophysiol 84: 281-288, 2000.
18. Kandler K and Friauf E. Development of glycinergic and glutamatergic synaptic transmission in the auditory brainstem of perinatal rats. J Neurosci 15: 6890-6904, 1995.
19. Karadsheh MF, Byun N, Mount DB, and Delpire E. Localization of the KCC4 potassium-chloride co-transporter in the nervous system. Neuroscience 123: 381-391, 2003.
20. Karadsheh MF and Delpire E. A neuronal restrictive silencing element is found in the KCC2 gene: molecular basis for KCC2 specific expression in neurons. J Neurophysiol 85: 995-997, 2001.
21. Li H, Tornberg J, Kaila K, Airaksinen MS, and Rivera C. Patterns of cation-chloride co-transporter expression during embryonic rodent CNS development. Eur J Neurosci 16: 2358-2370, 2002.
22. LoTurco JJ, Owens DF, Heath MJS, Davis MBE, and Kriegstein AR. GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis. Neuron 15: 1287-1298, 1995.
23. Lu J, Karadsheh M, and Delpire E. Developmental regulation of the neuronal-specific isoform of K-Cl co-transporter KCC2 in postnatal rat brains. J Neurobiol 39: 558-568, 1999.
24. 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: 3199-3206, 2003.
25. Luhmann HJ and Prince DA. Postnatal maturation of the GABAergic system in rat neocortex. J Neurophysiol 65: 247-263, 1991.
26. +-Cl-co-transporters KCC1 and KCC4. J Biol Chem 275: 30326-30334, 2000.
27. Mienville JM and Pesold C. Low resting potential and postnatal upregulation of NMDA receptors may cause Cajal-Retzius cell death. J Neurosci 19: 1636-1646, 1999.
28. Misgeld U, Deisz RA, Dodt HU, and Lux HD. The role of chloride transport in postsynaptic inhibition of hippocampal neurons. Science 232: 1413-1415, 1986.
29. Mount DB, Mercado A, Song L, Xu J, George JAL, Delpire E, and Gamba G. Cloning and characterization of KCC3 and KCC4, new members of the cation-chloride co-transporter gene family. J Biol Chem 274: 16355-16362, 1999.
30. Mueller AL, Chesnut RM, and Schwartzkroin PA. Actions of gaba in developing rabbit hippocampus: an in vitro study. Neurosci Lett 39: 193-198, 1983.
31. Muller D, Oliver M, and Lynch G. Developmental changes in synaptic properties in hippocampus of neonatal rats. Dev Brain Res 49: 105-114, 1989.
32. Owens DF, Boyce LH, Davis MBE, and Kriegstein AR. Excitatory GABA responses in embryonic and neonatal cortical slices demonstrated by gramicidin perforated-patch recordings and calcium imaging. J Neurosci 16: 6414-6423, 1996.
33. o regulation. Am J Physiol 273: C1516-C1525, 1997.
34. Payne JA, Stevenson TJ, and Bonaldson LF. Molecular characterization of a putative K-Cl co-transporter in rat brain. A neuronal-specific isoform. J Biol Chem 271: 16245-16252, 1996.
35. Pearson M, Lu J, Mount DB, and Delpire E. Localization of the K-Cl co-transporter, KCC3, in the central and peripheral nervous systems: expression in choroid plexus, large neurons, and white matter tracts. Neuroscience 103: 483-493, 2001.
36. - co-transporter BSC2 in the nervous system. Am J Physiol 272: C173-C183, 1997a.
37. Plotkin MD, Snyder EY, Hebert SC, and Delpire E. Expression of the Na-K-2Cl co-transporter is developmentally regulated in postnatal rat brains: a possible mechanism underlying GABA's excitatory role in immature brain. J Neurobiol 33: 781-795, 1997b.
38. +-Cl- co-transporter KCC2 and impairs neuronal Cl- extrusion. J Cell Biol 159: 747-752, 2002.
39. +/CP co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 397: 251-255, 1999.
40. A receptor-mediated responses in spinal neurons. J Neurosci 16: 82-91, 1996.
41. Schoenherr CJ and Anderson DJ. The neuron-restrictive silencer factor (NRSF): a coordinate repressor of multiple neuron-specific genes. Science 267: 1360-1363, 1995.
42. -. J Neurophysiol 89: 159-167, 2003.
43. Song L, Mercado A, Vazquez N, Xie Q, Desai R, Jr. GAL, Gamba G, and Mount DB. Molecular, functional, and genomic characterization of human KCC2, the neuronal K-Cl co-transporter. Brain Res Mol Brain Res 103: 91-105, 2002.
44. Staley K. The role of an inwardly rectifying chloride conductance in postsynaptic inhibition. J Neurophysiol 72: 273-284, 1994.
45. A receptor function following gene transfer of the CLC-2 chloride channel. Neuron 17: 543-551, 1996.
46. A receptors. Science 269: 977-981, 1995.
47. Stein V, Hermans-Borgmeyer I, Jentsch TJ, and Hubner CA. Expression of the KCl co-transporter KCC2 parallels neuronal maturation and the emergence of low intracellular chloride. J Comp Neurol 468: 57-64, 2004.
48. Strange K, Singer TD, Morrison R, and Delpire E. Dependence of KCC2 K-Cl co-transporter activity on a conserved carboxy terminus tyrosine residue. Am J Physiol 279: C860-C867, 2000.
49. A-receptor mediated currents in dorsal root ganglion neurons isolated from Na-K-2Cl cotransporter null mice. J Neurosci 20: 7531-7538, 2000.
50. Thompson SM, Deisz RA, and Prince DA. Outward chloride/cation co-transport in mammalian cortical neurons. Neurosci Lett 89: 49-54, 1988.
51. 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: 719-730, 2003.
52. Tyzio R, Ivanov A, Bernard C, Holmes GL, Ben-Ari Y, and Khazipov R. Membrane potential of CA3 hippocampal pyramidal cells during postnatal development. J Neurophysiol 90: 2964-2972, 2003.
53. Vu TQ, Payne JA, and Copenhagen DR. Localization and developmental expression patterns of the neuronal K-Cl co-transporter (KCC2) in the rat retina. J Neurosci 20: 1414-1423, 2000.
54. Woo N-S, Lu J, England R, McClellan R, Dufour S, Mount DB, Deutch AY, Lovinger DM, and Delpire E. Hyper-excitability and epilepsy associated with disruption of the mouse neuronal-specific K-Cl co-transporter gene. Hippocampus 12: 258-268, 2002.
55. Wu WL, Ziskind-Conhaim L, and Sweet MA. Early development of glycine- and GABA-mediated synapses in rat spinal cord. J Neurosci 12: 3935-3945, 1992.
56. Zhou FM and Hablitz JJ. Postnatal development of membrane properties of layer I neurons in rat neocortex. J Neurosci 16: 1131-1139, 1996.