Expression of the KCl Cotransporter KCC2 Parallels Neuronal Maturation and the Emergence of Low Intracellular Chloride

Journal of Comparative Neurology

Volumn 468, Issue 1, 2004, Pages 57-64

  Stein, Valentin ^a,c   Hermans Borgmeyer, Irm ^a   Jentsch, Thomas J ^a   Hübner, Christian A ^a,b  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b UNIVERSITY OF HAMBURG   (Germany)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Development; Expression; GABA; K+Cl cotransport; Synaptic inhibition

Indexed keywords

4 AMINOBUTYRIC ACID; CHLORIDE ION; COTRANSPORTER; GLYCINE; POTASSIUM ION; PROTEIN KCC2; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CELL MATURATION; CHLORIDE TRANSPORT; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; HIPPOCAMPUS; IMMUNOPRECIPITATION; IN SITU HYBRIDIZATION; MEMBRANE POTENTIAL; MOTONEURON; MOUSE; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEWBORN; NONHUMAN; PATCH CLAMP; POSTNATAL DEVELOPMENT; POTASSIUM TRANSPORT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PYRAMIDAL NERVE CELL; SPINAL CORD; TRANSCRIPTION REGULATION; WESTERN BLOTTING;

EID: 0348042110     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.10983     Document Type: Article

References (42)

1. Baulac S, Huberfeld G, Gourfinkel-An I, Mitropoulou G, Beranger A, Prud'homme JF, Baulac M, Brice A, Bruzzone R, LeGuern E. 2001. First genetic evidence of GABA(A) receptor dysfunction in epilepsy: a mutation in the gamma2-subunit gene. Nat Genet 28:46-48.
2. Ben-Ari Y. 2002. Excitatory actions of gaba during development: the nature of the nurture. Nat Rev Neurosci 3:728-739.
3. Ben-Ari Y, Cherubini E, Corradetti R, Gaiarsa JL. 1989. Giant synaptic potentials in immature rat CA3 hippocampal neurones. J Physiol 416:303-325.
4. A, NMDA and AMPA receptors: a developmentally regulated 'menage à trois'. Trends Neurosci 20:523-529.
5. Boettger T, Hübner CA, Maier H, Rust MB, Beck FX, Jentsch TJ. 2002. Deafness and renal tubular acidosis in mice lacking the K-Cl cotransporter Kcc4. Nature 416:874-878.
6. Cherubini E, Gaiarsa JL, Ben-Ari Y. 1991. GABA: an excitatory transmitter in early postnatal life. Trends Neurosci 14:515-519.
7. Clayton GH, Owens GC, Wolff JS, Smith RL. 1998. Ontogeny of cation-Cl-cotransporter expression in rat neocortex. Brain Res Dev Brain Res 109:281-292.
8. Cossette P, Liu L, Brisebois K, Dong H, Lortie A, Vanasse M, Saint-Hilaire JM, Carmant L, Verner A, Lu WY, Wang YT, Rouleau GA. 2002. Mutation of GABRA1 in an autosomal dominant form of juvenile myoclonic epilepsy. Nat Genet 31:184-189.
9. Delpire E, Lu J, England R, Dull C, Thorne T. 1999. Deafness and imbalance associated with inactivation of the secretory Na-K-2Cl cotransporter. Nat Genet 22:192-195.
10. Ehrlich I, Lohrke S, Friauf E. 1999. Shift from depolarizing to hyperpolarizing glycine action in rat auditory neurones is due to age-dependent Cl-regulation. J Physiol 520:121-137.
11. Flagella M, Clarke LL, Miller ML, Erway LC, Giannella RA, Andringa A, Gawenis LR, Kramer J, Duffy JJ, Doetschman T, Lorenz JN, Yamoah EN, Cardell EL, Shull GE. 1999. Mice lacking the basolateral Na-K-2Cl cotransporter have impaired epithelial chloride secretion and are profoundly deaf. J Biol Chem 274:26946-26955.
12. Gao BX, Ziskind-Conhaim L. 1995. Development of glycine- and GABA-gated currents in rat spinal motoneurons. J Neurophysiol 74:113-121.
13. Hatten ME, Alder J, Zimmerman K, Heintz N. 1997. Genes involved in cerebellar cell specification and differentiation. Curr Opin Neurobiol 7:40-47.
14. Hübner CA, Lorke DE, Hermans-Borgmeyer I. 2001a. Expression of the Na-K-2Cl-cotransporter NKCC1 during mouse development. Mech Dev 102:267-269.
15. Hübner CA, Stein V, Hermans-Borgmeyer I, Meyer T, Ballanyi K, Jentsch TJ. 2001b. Disruption of KCC2 reveals an essential role of K-Cl cotransport already in early synaptic inhibition. Neuron 30:515-524.
16. Kakazu Y, Akaike N, Komiyama S, Nabekura J. 1999. Regulation of intracellular chloride by cotransporters in developing lateral superior olive neurons. J Neurosci 19:2843-2851.
17. Kaufman MH, Bard JBL. 1999. The anatomical basis of mouse development. New York: Academic Press. p 179-184.
18. Kelsch W, Hormuzdi S, Straube E, Lewen A, Monyer H, Misgeld U. 2001. Insulin-like growth factor 1 and a cytosolic tyrosine kinase activate chloride outward transport during maturation of hippocampal neurons. J Neurosci 21:8339-8347.
19. LoTurco JJ, Owens DF, Heath MJ, Davis MB, Kriegstein AR. 1995. GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis. Neuron 15:1287-1298.
20. Lu J, Karadsheh M, Delpire E. 1999. Developmental regulation of the neuronal-specific isoform of K-Cl cotransporter KCC2 in postnatal rat brains. J Neurobiol 39:558-568.
21. Maric D, Liu QY, Maric I, Chaudry S, Chang YH, Smith SV, Sieghart W, Fritschy JM, Barker JL. 2001. GABA expression dominates neuronal lineage progression in the embryonic rat neocortex and facilitates neurite outgrowth via GABA(A) autoreceptor/Cl-channels. J Neurosci 21:2343-2360.
22. Misgeld U, Deisz RA, Dodt HU, Lux HD. 1986. The role of chloride transport in postsynaptic inhibition of hippocampal neurons. Science 232:1413-1415.
23. Niimi K, IHarada I, Kusaka Y, Kishi S. 1962. The ontogenetic development of the diencephalon of the mouse. Tokushima J Exp Med 8:203-208.
24. Obata K, Oide M, Tanaka H. 1978. Excitatory and inhibitory actions of GABA and glycine on embryonic chick spinal neurons in culture. Brain Res 144:179-184.
25. Onimaru H, Homma I. 1987. Respiratory rhythm generator neurons in medulla of brainstem-spinal cord preparation from newborn rat. Brain Res 403:380-384.
26. Owens DF, Boyce LH, Davis MB, Kriegstein AR. 1996. Excitatory GABA responses in embryonic and neonatal cortical slices demonstrated by gramicidin perforated-patch recordings and calcium imaging. J Neurosci 16:6414-6423.
27. . cotransporter. J Clin Invest 105:441-450.
28. Paxinos G. 1995. The rat nervous system, 2nd ed. New York: Academic Press.
29. Payne JA. 1997. Functional characterization of the neuronal-specific K-Cl cotransporter: implications for [K+]o regulation. Am J Physiol 273: C1516-1525.
30. Payne JA, Stevenson TJ, Donaldson LF. 1996. Molecular characterization of a putative K-Cl cotransporter in rat brain. A neuronal-specific isoform. J Biol Chem 271:16245-16252.
31. - co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 397:251-255.
32. Russell JM. 2000. Sodium-potassium-chloride cotransport. Physiol Rev 80:211-276.
33. Shiang R, Ryan SG, Zhu YZ, Hahn AF, O'Connell P, Wasmuth JJ. 1993. Mutations in the alpha 1 subunit of the inhibitory glycine receptor cause the dominant neurologic disorder, hyperekplexia. Nat Genet 5:351-358.
34. Strange K, Singer TD, Morrison R, Delpire E. 2000. Dependence of KCC2 K-Cl cotransporter activity on a conserved carboxy terminus tyrosine residue. Am J Physiol Cell Physiol 279:C860-C867.
35. A receptor-mediated currents in dorsal root ganglion neurons isolated from Na-K-2Cl cotransporter null mice. J Neurosci 20:7531-7538.
36. Suzue T. 1984. Respiratory rhythm generation in the in vitro brain stem-spinal cord preparation of the neonatal rat. J Physiol (Lond) 354:173-183.
37. Wallace RH, Marini C, Petrou S, Harkin LA, Bowser DN, Panchal RG, Williams DA, Sutherland GR, Mulley JC, Scheffer IE, Berkovic SF. 2001. Mutant GABA(A) receptor gamma2-subunit in childhood absence epilepsy and febrile seizures. Nat Genet 28:49-52.
38. Woo NS, Lu J, England R, McClellan R, Dufour S, Mount DB, Deutch AY, Lovinger DM, Delpire E. 2002. Hyperexcitability and epilepsy associated with disruption of the mouse neuronal-specific K-Cl cotransporter gene. Hippocampus 12:258-268.
39. Wu WL, Ziskind-Conhaim L, Sweet MA. 1992. Early development of glycine- and GABA-mediated synapses in rat spinal cord. J Neurosci 12:3935-3945.
40. 2+ influx in developing neocortex by excitatory and inhibitory neurotransmitters. Neuron 6:333-344.
41. Zhang SJ, Jackson MB. 1993. GABA-activated chloride channels in secretory nerve endings. Science 259:531-534.
42. Zhang L, Spigelman I, Carlen PL. 1990. Whole-cell patch study of GABAergic inhibition in CA1 neurons of immature rat hippocampal slices. Brain Res Dev Brain Res 56:127-130.