Expression and developmental regulation of the K+-Cl- cotransporter KCC2 in the cochlear nucleus

Hearing Research

Volumn 206, Issue 1-2, 2005, Pages 107-115

  Vale, Carmen ^a,b   Caminos, Elena ^a   Martinez Galán, Juan R ^a   Juiz, José M ^a  

^a UNIVERSITY OF CASTILLA LA MANCHA   (Spain)

^b UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

Author keywords

Auditory; Brain stem; Chloride transport; Development; GABA; Glycine; Inhibition

Indexed keywords

CHLORIDE ION; COTRANSPORTER; KCC2 PROTEIN; POTASSIUM ION; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AUDITORY SYSTEM; CELL MEMBRANE; CHLORIDE TRANSPORT; COCHLEAR NUCLEUS; CONTROLLED STUDY; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RAT; REGULATORY MECHANISM; SYNAPTOGENESIS; UPREGULATION;

ANIMALS; BLOTTING, WESTERN; CHLORIDES; COCHLEAR NUCLEUS; GAMMA-AMINOBUTYRIC ACID; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLYCINE; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; NEURAL INHIBITION; POTASSIUM; RATS; RATS, WISTAR; RECEPTORS, GABA; SYMPORTERS;

EID: 23144443153     PISSN: 03785955     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.heares.2005.03.012     Document Type: Article

References (53)

1. F.J. Alvarez-Leefmans Intracellular chloride regulation N. Sperelakis Cell physiology sourcebook: a molecular approach 2001 Academic Press San Diego 301 318
2. V. Balakrishnan, M. Becker, H.G. Löhrke, E. Güresir, and E. Friauf Expression and function of chloride transporters during development of inhibitory neurotransmission in the auditory brainstem J. Neurosci. 23 2003 4134 4145
3. Y. Ben-Ari, R. Khazipov, X. Leinekugel, O. Caillard, and J.L. Gaiarsa GABAA, NMDA and AMPA receptors: a developmentally regulated "menage à trois" Trends Neurosci. 20 1997 523 529
4. Y. Ben-Ari Excitatory actions of GABA during development: the nature of the nurture Nat. Rev. Neurosci. 3 2002 728 739
5. Blaesse, P., Nothwang, H.G., Loh, C., Friauf, E., 2004. Subcellular localization of KCC2 in immature neurons in the rat lateral superior olive. In: Third Symposium on Molecular Mechanisms of Central Auditory Palasticity and Development. p. 24
6. J. Bormann, O.P. Hamill, and B. Sakmann Mechanism of anion permeation trough channels gated by glycine and γ-aminobutyric acid in mouse cultured spinal neurons J. Physiol. (Lond) 385 1987 243 286
7. M.L. Campos, C. de Cabo, W. Wisden, J.M. Juiz, and D. Merlo Expression of GABA(A) receptor subunits in rat brainstem auditory pathways: cochlear nuclei, superior olivary complex and nucleus of the lateral lemniscus Neuroscience 102 2001 625 638
8. D.M. Caspary, D.S. Palombi, P.M. Backoff, R.H. Helfert, and P.G. Finlayson GABA and glycine inputs control discharge rate within the excitatory response area of primary-like and phase-locked AVCN neurons M.A. Merchan J.M. Juiz D.A. Godfrey E. Mugnaini The mammalian cochlear nuclei: organization and function 1993 Plenum Press New York 239 252
9. G. Chen, P.Q. Trombley, and A.N. van den Pol Excitatory actions of GABA in developing rat hypothalamic neurones J. Physiol. (Lond) 494 1996 451 464
10. E. Cherubini, C. Rovira, J.L. Gaiarsa, R. Corradetti, and Y. Ben-Ari GABA mediated excitation in inmature CA3 hippocampal neurons Int. J. Dev. Neurosci. 8 1990 481 490
11. E. Cherubini, J.L. Gaiarsa, and Y. Ben-Ari GABA: an excitatory neurotransmitter in early postnatal life Trends Neurosci. 14 1991 515 519
12. R.A. DeFazio, S. Keros, M.W. Quick, and J.J. Hablitz Potassium-coupled chloride cotransport controls intracellular chloride in rat neocortical pyramidal neurons J. Neurosci. 20 2000 8069 8076
13. E. Delpire, M.I. Rauchman, D.R. Beier, S.C. Hebert, and S.R. Gullans Molecular cloning and chromosome localization of a putative basolateral Na(+)-K(+)-2Cl(-) cotransporter from mouse inner medullary collecting duct (mIMCD-3) cells J. Biol. Chem. 269 1994 25677 25683
14. E. Delpire, and D.B. Mount Human and murine phenotypes associated with defects in cation-chloride cotransport Annu Rev. Physiol. 64 2002 803 843
15. J.C. Eccles The ionic mechanisms of inhibitory and excitatory synaptic action Ann NY Acad. Sci. 137 1966 473 494
16. I. Ehrlich, S. Löhrke, and E. Friauf Shift from depolarising to hyperpolarizing glycine actions in rat auditory neurons is due to age-dependent Cl- regulation J. Physiol. (Lond) 520 1999 131 137
17. A.I. Gulyás, A. Sik, J.A. Payne, K. Kaila, and T.F. Freund The KCl cotransporter, KCC2, is highly expressed in the vicinity of excitatory synapses in the rat hippocampus Eur. J. Neurosci. 13 2001 2205 2217
18. J.A. Hirsch, and D. Oertel Synaptic connections in the dorsal cochlear nucleus of mice, in vitro J. Physiol. 396 1988 549 562
19. 2+]I in retinal neurons of postnatal rabbits Vis. Neurosci. 13 1996 441 447
20. 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 30 2001 515 524
21. - accumulation and depletion in cultured rat midbrain neurons J. Neurosci. 19 1999 4695 4704
22. J.M. Juiz, R.H. Helfert, J. Bonneau, R.A. Wenthold, and R.A. Altschuler Three classes of inhibitory amino acid terminals in the cochlear nucleus of the guinea pig J. Comp. Neurol. 373 1996 11 26
23. + transient J. Neurosci. 17 1997 7662 7672
24. Y. Kakazu, N. Akaike, S. Komiyama, and J. Nabekura Regulation of intracellular chloride by cotransporter in developing lateral superior olive neurons J. Neurosci. 19 1999 2843 2851
25. K. Kandler, and E. Friauf Development of glycinergic and glutamatergic synaptic transmission in the auditory brainstem of perinatal rats J. Neurosci. 15 1995 6804 6890
26. W. Kelsch, S. Hormuzdi, E. Straube, A. Lewen, H. Monyer, and U. Misgeld Insulin-like growth factor 1 and a cytosolic tyrosine kinase activate chloride outward transport during maturation of hippocampal neurons J. Neurosci. 21 2001 8339 8347
27. K. Krnjevic Chemical nature of synaptic transmission in vertebrates Physiol. Rev. 54 1974 418 540
28. P.H.M. Kullmann, F.A. Ene, and K. Kandler Glycinergic and GABAergic calcium responses in the developing lateral superior olive Eur. J. Neurosci. 15 2002 1093 2004
29. J.J. LoTurco, D.F. Owens, M.J. Heath, M.B. Davis, and A.R. Kriegstein GABA and glutamate depolarise cortical progenitor cells and inhibit DNA synthesis Neuron 15 1995 1287 1298
30. J. Lu, M. Karadhed, and E. Delpire Developmental regulation of the neuronal-specific isoform of K-Cl cotranspoter KCC2 in postnatal rat brains J. Neurobiol. 39 1999 558 568
31. H.J. Luhmann, and D.A. Prince Postnatal maturation of the GABAergic system in rat neocortex J. Neurophysiol. 65 1991 247 263
32. D.F. Owens, L.H. Boyce, M.B. Davis, and A.R. Kriegstein Excitatory GABA responses in embryonic and neonatal cortical slices demonstrated by gramicidin perforated-patch recordings and calcium imaging J. Neurosci. 16 1996 6414 6423
33. J.A. Payne, T.J. Stevenson, and L.F. Donaldson Molecular characterization of a putative K-Cl cotransporter in rat brain J. Biol. Chem. 27 1996 16245 16252
34. +]o regulation Am. J. Physiol. 273 1997 C1516 C1525
35. J.A. Payne, C. Rivera, J. Voipio, and K. Kaila Cation-chloride co-transporters in neuronal communication, development and trauma Trends Neurosci. 26 2003 199 206
36. D.B. Reichling, A. Kyrozis, J. Wang, and A.B. MacDermott Mechanisms of GABA and glycine depolarisation-induced calcium transients in rat dorsal horn neurons J. Physiol. (Lond) 476 1994 411 421
37. - cotransporter KCC2 renders GABA hyperpolarizing during neuronal maturation Nature 397 1999 251 255
38. M.E. Rubio Differential distribution of synaptic endings containing glutamate, glycine, and GABA in the rat dorsal cochlear nucleus J. Comp. Neurol. 477 2004 253 272
39. - regulation in developing auditory neurons Neurosci. Res. 48 2004 211 220
40. J.H. Singer, E.M. Talley, D.A. Bayliss, and A.J. Berger Development of glycinergic synaptic transmission to rat brain stem motoneurons J. Neurophysiol. 80 1998 2608 2620
41. 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 J. Comp. Neurol. 468 2004 57 64
42. K. Strange, T.D. Singer, R. Morrison, and E. Delpire Dependence of KCC2 K-Cl cotransporter activity on a conserved carboxy terminus tyrosine residue Am. J. Physiol. Cell Physiol. 279 2000 860 867
43. S.M. Thompson, and B.H. Gähwiler Activity-dependent disinhibition I. Repetitive stimulation reduces IPSP driving force and conductance in the hippocampus in vitro J. Neurophysiol. 61 1989 501 511
44. C. Vale, and D.H. Sanes Afferent regulation of inhibitory synaptic transmission in the developing auditory midbrain J. Neurosci. 20 2000 1912 1921
45. C. Vale, and D,H. Sanes The effect of bilateral deafness on excitatory and inhibitory synaptic strength in the inferior colliculus Eur. J. Neurosci. 16 2002 2394 2404
46. C. Vale, J. Schoorlemmer, and D.H. Sanes Deafness disrupts chloride transporter function and inhibitory synaptic transmission J. Neurosci. 23 2003 7516 7524
47. C. Vale, J.M. Juiz, D.R. Moore, and D.H. Sanes Unilateral cochlear ablation produces greater loss of inhibition in the contralateral inferior colliculus Eur. J. Neurosci. 20 2004 2133 2140
48. 2+ transients in embryonic rat dorsal horn neurons in culture Eur. J. Neurosci. 6 1994 1275 1280
49. R.J. Wenthold Neurotransmitters of brainstem auditory nuclei R.A. Altschuler R.P. Bobbin B.M. Clopton D.W. Hoffman Neurobiology of hearing: the central auditory system 1991 Raven Press New York 121 140
50. J.R. Williams, J.W. Sharp, V.G. Kumari, M. Wilson, and J.A. Payne The neuron-specific K-Cl cotransporter KCC2. Antibody development and initial characterization of the protein J. Biol. Chem. 274 1999 12656 12664
51. S.H. Wu, and D. Oertel Inhibitory circuitry in the ventral cochlear nucleus is probably mediated by glycine J. Neurosci. 6 1986 2691 2706
52. W.I. Wu, L. Ziskind-Conhaim, and M.A. Sweet Early development of glycine- and GABA-mediated synapses in rat spinal cord J. Neurosci. 12 1992 3935 3945
53. 2+ influx in control of postsynaptic developing neocortex by excitatory and inhibitory neurotransmitters Neuron 6 1991 333 344