Differential expression pattern of chloride transporters NCC, NKCC2, KCC1, KCC3, KCC4, and AE3 in the developing rat auditory brainstem

Cell and Tissue Research

Volumn 312, Issue 2, 2003, Pages 155-165

  Becker, Michael ^a   Nothwang, Hans Gerd ^a   Friauf, Eckhard ^a  

^a Rheinland Pfälzische Technische Universität Kaiserslautern Landau   (Germany)

Author keywords

Brain development; In situ hybridization; Inhibitory synapses; Rat (Sprague Dawley); Superior olivary complex

Indexed keywords

NEUROTRANSMITTER; RNA;

ANIMAL TISSUE; ARTICLE; AUDITORY NERVOUS SYSTEM; BRAIN DEVELOPMENT; BRAIN STEM; CHLORIDE TRANSPORT; CONTROLLED STUDY; IN SITU HYBRIDIZATION; MOLECULAR DYNAMICS; NERVE CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SUPERIOR OLIVARY NUCLEUS;

ANIMALIA; MAMMALIA;

EID: 0037663842     PISSN: 0302766X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00441-003-0713-5     Document Type: Article

References (55)

1. Aickin CC (1990) Chloride transport across the sarcolemma of vertebrate smooth and skeletal muscle. In: Alvarez-Leefmans FJ, Russell JM (eds) Chloride channels and carriers in nerve, muscle and glial cells. Plenum, New York, pp 209-249
2. - regulation and synaptic inhibition in vertebrate and invertebrate neurons. In: Alvarez-Leefmans FJ, Russell JM (eds) Chloride channels and carriers in nerve, muscle and glial cells. Plenum, New York, pp 109-158
3. Alvarez-Leefmans FJ (2001) Intracellular chloride regulation. In: Sperelakis N (ed) Cell physiology sourcebook: a molecular approach. Academic, New York, pp 301-318
4. Balakrishnan V, Becker M, Löhrke S, Nothwang HG, Güresir E, Friauf E (2003) Expression and function of chloride transporters during development of inhibitory neurotransmission in the auditory brainstem. J Neurosci (in press)
5. Ben-Ari Y (2001) Developing networks play a similar melody. Trends Neurosci 24:353-360
6. Ben-Ari Y (2002) Excitatory actions of GABA during development: the nature of the nurture. Nat Rev Neurosci 3:728-739
7. Ben-Ari Y, Cherubini E, Corradetti R, Galarsa J-L (1989) Giant synaptic potentials in immature rat CA3 hippocampal neurones. J Physiol (Lond) 416:303-325
8. Boguski MS (1995) The turning point in genome research. Trends Biochem Sci 20:295-296
9. Brazy PC, Gunn RB (1976) Furosemide inhibition of chloride transport in human red blood cells. J Gen Physiol 68:583-599
10. Cherubini E, Rovira C, Gaiarsa JL, Corradetti R, Ben-Ari Y (1990) GABA mediated excitation in immature rat CA3 hippocampal neurons. Int J Dev Neurosci 8:481-490
11. Cherubini E, Gaiarsa JL, Ben-Ari Y (1991) GABA: an excitatory transmitter in early postnatal life. Trends Neurosci 14:515-519
12. Clayton GH, Owens GC, Wolff JS, Smith RL (1998) Ontogeny of cation-Cl-cotransporter expression in rat neocortex. Brain Res 109:281-292
13. Delpire E (2000) Cation-chloride cotransporters in neuronal communication. News Physiol Sci 15:309-312
14. Delpire E, Mount DB (2002) Human and murine phenotypes associated with defects in cation-chloride cotransport. Annu Rev Physiol 64:803-843
15. - regulation. J Physiol 520:121-137
16. Gamba G, Saltzberg SN, Lombardi M, Miyanoshita A, Lytton J, Hediger MA, Brenner BM, Hebert SC (1993) Primary structure and functional expression of a cDNA encoding the thiazide-sensitive, electroneutral sodium-chloride cotransporter. Proc Natl Acad Sci U S A 90:2749-2753
17. Gamba G, Miyanoshita A, Lombardi M, Lytton J, Lee WS, Hediger MA, Hebert SC (1994) Molecular cloning, primary structure, and characterization of two members of the mammalian electroneutral sodium-(potassium)-chloride cotransporter family expressed in kidney. J Biol Chem 269:17713-17722
18. Garon L, Rousseau F, Gagnon E, Isenring P (2000) Cloning and functional characterization of a cation-Cl-cotransporter-interacting protein. J Biol Chem 275:32027-32036
19. Gillen CM, Brill S, Payne JA, Forbush BI (1996) Molecular cloning and functional expression of the K-Cl cotransporter from rabbit, rat and human. A new member of the cation-chloride cotransporter family. J Biol Chem 271:16236-16244
20. Grothe B (2000) The evolution of temporal processing in the medial superior olive, an auditory brainstem structure. Prog Neurobiol 61:581-610
21. Gunn RB (1985) Bumetanide inhibition of anion exchange in human red blood cells. Biophys J 47:326a
22. Helfert RH, Snead CR, Altschuler RA (1991) The ascending auditory pathways. In: Altschuler RA, Bobbin RP, Clopton BM, Hoffman DW (eds) Neurobiology of hearing: the central auditory system. Raven, New York, pp 1-25
23. - cotransporter. J Biol Chem 274:10661-10667
24. Hübner CA, Stein V, Hermans-Borgmeyer I, Meyer T, Ballanyi K, Jentsch TJ (2001) Disruption of KCC2 reveals an essential role of K-Cl cotransport already in early synaptic inhibition. Neuron 30:515-524
25. 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
26. Kanaka C, Ohno K, Okabe A, Kuriyama K, Itoh T, Fukuda A, Sato K (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 104:933-946
27. Kandler K, Friauf E (1995) Development of glycinergic and glutamatergic synaptic transmission in the auditory brainstem of perinatal rats. J Neurosci 15:6890-6904
28. Klinke R, Silbernagl S (2001) Lehrbuch der Physiologie, 3rd edn. Thieme, Stuttgart
29. Kopito RR, Lee BS, Simmons DM, Lindsey AE, Morgans CW, Schneider .K (1989) Regulation of intracellular pH by a neuronal homolog of the erythrocyte anion exchanger. Cell 59:927-937
30. - exchanger. J Biol Chem 265:462-471
31. Kullmann PHM, Kandler K (2001) Glycinergic/GABAergic synapses in the lateral superior olive are excitatory in neonatal C57B1/6J mice. Brain Res 131:143-147
32. Legendre P (2001) The glycinergic inhibitory synapse. Cell Mol Life Sci 58:760-793
33. - exchanger. Cloning of a cardiac AE3 cDNA, organization of the AE3 gene, and identification of an alternative transcription initiation site. J Biol Chem 267:7927-7935
34. Lo Turco JJ, Owens DF, Heath MJS, Davis MBE, Kriegstein AR (1995) GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis. Neuron 15:1287-1298
35. 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
36. Luhmann HJ, Prince DA (1991) Postnatal maturation of the GABAergic system in rat neocortex. J Neurophysiol 65:247-263
37. - cotransporter expression and inhibitory synaptogenesis in the rat hippocampus: an immunocytochemical analysis. Eur J Neurosci 15:233-245
38. Mehta AK, Ticku MK (1999) An update on GABA(A) receptors. Brain Res Rev 29:196-217
39. Mount DB, Mercado A, Song LY, Xu J, George AL, Delpire E, Gamba G (1999) Cloning and characterization of KCC3 and KCC4, new members of the cation-chloride cotransporter gene family. J Biol Chem 274:16355-16362
40. 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
41. Payne JA, Forbush B III (1994) Alternatively spliced isoforms of the putative renal Na-K-Cl cotransporter are differentially distributed within the rabbit kidney. Proc Natl Acad Sci U S A 91:4544-4548
42. Pearson MM, Lu J, Mount DB, Delpire E (2001) 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 103:481-491
43. Plotkin MD, Snyder EY, Hebert SC, Delpire E (1997) 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 33:781-795
44. Race JE, Makhlouf FN, Logue PJ, Wilson FH, Dunham PB, Holtzman EJ (1999) Molecular cloning and functional characterization of KCC3, a new K-Cl cotransporter. Am J Physiol-Cell Physiol 277:C1210-C1219
45. - exchange function differs in adult and fetal rat hippocampal neurons. Brain Res 614:308-314
46. - co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 397:251-255
47. Russell JM (2000) Sodium-potassium-chloride cotransport. Physiol Rev 80:211-276
48. Shen MR, Chou CY, Hsu KF, Liu HS, Dunham PB, Holtzman EJ, Ellory JC (2001) The KCl cotransporter isoform KCC3 can play an important role in cell growth regulation. Proc Natl Acad Sci U S A 98:14714-14719
49. Singer JH, Talley EM, Bayliss DA, Berger AJ (1998) Development of glycinergic synaptic transmission to rat brain stem motoneurons. J Neurophysiol 80:2608-2620
50. Spitzer NC, Kingston PA, Manning TJ Jr, Conklin MW (2002) Outside and in: development of neuronal excitability. Curr Opin Neurobiol 12:315-323
51. Sung KW, Kirby M, McDonald MP, Lovinger DM, Delpire E (2000) Abnormal GABAA receptor-mediated currents in dorsal root ganglion neurons isolated from Na-K-2Cl cotransporter null mice. J Neurosci 20:7531-7538
52. - cotransporter expression and inhibitory postsynaptic potential depression in rat motoneurons. J Biol Chem 277:4945-4950
53. Vaughan-Jones RD (1986) An investigation of chloride-bicarbonate exchange in the sheep cardiac Purkinje fibre. J Physiol (Lond) 379:377-406
54. Wisden W, Morris BJ, Hunt SP (1991) In situ hybridization with synthetic DNA probes. In: Chad J, Wheal H (eds) Molecular neurobiology - a practical approach. IRL, Oxford, pp 205-225
55. Wu WI, Ziskind-Conhaim L, Sweet MA (1992) Early development of glycine- and GABA-mediated synapses in rat spinal cord. J Neurosci 12:3935-3945