Chloride transport in the kidney: Lessons from human disease and knockout mice

Journal of the American Society of Nephrology

Volumn 16, Issue 6, 2005, Pages 1549-1561

  Jentsch, Thomas J ^a  

^a UNIVERSITY OF HAMBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; CHLORIDE; CHLORIDE CHANNEL; POTASSIUM CHLORIDE; PROTEIN C1C 5; PROTEIN C1C K; PROTEIN CLC C; PROTEIN KCC K; PROTEIN KCC3; PROTEIN KCC4; SODIUM CHLORIDE; UNCLASSIFIED DRUG; BSND PROTEIN, HUMAN; COTRANSPORTER; MEMBRANE PROTEIN; POTASSIUM CHLORIDE SYMPORTERS; POTASSIUM-CHLORIDE SYMPORTERS;

ACID SECRETION; ANION EXCHANGE; CELL SECRETION; CHLORIDE TRANSPORT; CONFERENCE PAPER; DISEASE ASSOCIATION; ENDOCYTOSIS; HUMAN; HYPERCALCIURIA; KIDNEY METABOLISM; KIDNEY TUBULE ABSORPTION; KIDNEY TUBULE ACIDOSIS; KNOCKOUT MOUSE; NEPHROLITHIASIS; NONHUMAN; PRIORITY JOURNAL; ANIMAL; ANIMAL MODEL; ARTICLE; ION TRANSPORT; KIDNEY; KIDNEY DISEASE; KIDNEY PROXIMAL TUBULE; METABOLISM; MOUSE; MOUSE MUTANT; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; CHLORIDE CHANNELS; CHLORIDES; ENDOCYTOSIS; HUMANS; ION TRANSPORT; KIDNEY; KIDNEY DISEASES; KIDNEY TUBULES, PROXIMAL; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; MODELS, ANIMAL; SYMPORTERS;

EID: 24144439165     PISSN: 10466673     EISSN: None     Source Type: Journal    
DOI: 10.1681/ASN.2005020207     Document Type: Conference Paper

References (101)

1. Jentsch TJ, Steinmeyer K, Schwarz G: Primary structure of Torpedo marmorata chloride channel isolated by expression cloning in Xenopus oocytes. Nature 348: 510-514, 1990
2. Steinmeyer K, Ortland C, Jentsch TJ: Primary structure and functional expression of a developmentally regulated skeletal muscle chloride channel. Nature 354: 301-304, 1991
3. Miller C: Open-state substructure of single chloride channels from Torpedo electroplax. Philos Trans R Soc Lond B Biol Sci 299: 401-411, 1982
4. Ludewig U, Pusch M, Jentsch TJ: Two physically distinct pores in the dimeric ClC-0 chloride channel. Nature 383: 340-343, 1996
5. Middleton RE, Pheasant DJ, Miller C: Homodimeric architecture of a ClC-type chloride ion channel. Nature 383: 337-340, 1996
6. Weinreich F, Jentsch TJ: Pores formed by single subunits in mixed dimers of different CLC chloride channels. J Biol Chem 276: 2347-2353, 2001
7. Dutzler R, Campbell EB, Cadene M, Chait BT, MacKinnon R: X-ray structure of a ClC chloride channel at 3.0 A reveals the molecular basis of anion selectivity. Nature 415: 287-294, 2002
8. Dutzler R, Campbell EB, MacKinnon R: Gating the selectivity filter in ClC chloride channels. Science 300: 108-112, 2003
9. Mindell JA, Maduke M, Miller C, Grigorieff N: Projection structure of a ClC-type chloride channel at 6.5 A resolution. Nature 409: 219-223, 2001
10. Lorenz C, Pusch M, Jentsch TJ: Heteromultimeric CLC chloride channels with novel properties. Proc Natl Acad Sci U S A 93: 13362-13366, 1996
11. Mohammad-Panah R, Harrison R, Dhani S, Ackerley C, Huan LJ, Wang Y, Bear CE: The chloride channel ClC-4 contributes to endosomal acidification and trafficking. J Biol Chem 278: 29267-29277, 2003
12. +-secretion. Nature 414: 558-561, 2001
13. Waldegger S, Jentsch TJ: Functional and structural analysis of ClC-K chloride channels involved in renal disease. J Biol Chem 275: 24527-24533, 2000
14. Pusch M, Ludewig U, Rehfeldt A, Jentsch TJ: Gating of the voltage-dependent chloride channel ClC-0 by the permeant anion. Nature 373: 527-531, 1995
15. - channels. Nature 427: 803-807, 2004
16. Brandt S, Jentsch TJ: ClC-6 and ClC-7 are two novel broadly expressed members of the CLC chloride channel family. FEBS Lett 377: 15-20, 1995
17. Friedrich T, Breiderhoff T, Jentsch TJ: Mutational analysis demonstrates that ClC-4 and ClC-5 directly mediate plasma membrane currents. J Biol Chem 274: 896-902, 1999
18. Li X, Shimada K, Showalter LA, Weinman SA: Biophysical properties of ClC-3 differentiate it from swelling- activated chloride channels in Chinese hamster ovary-K1 cells. J Biol Chem 275: 35994-35998, 2000
19. Steinmeyer K, Schwappach B, Bens M, Vandewalle A, Jentsch TJ: Cloning and functional expression of rat CLC-5, a chloride channel related to kidney disease. J Biol Chem 270: 31172-31177, 1995
20. Kieferle S, Fong P, Bens M, Vandewalle A, Jentsch TJ: Two highly homologous members of the ClC chloride channel family in both rat and human kidney. Proc Natl Acad Sci U S A 91: 6943-6947, 1994
21. Uchida S, Sasaki S, Furukawa T, Hiraoka M, Imai T, Hirata Y, Marumo F: Molecular cloning of a chloride channel that is regulated by dehydration and expressed predominantly in kidney medulla. J Biol Chem 268: 3821-3824, 1993
22. [published erratum appears in J Biol Chem 269: 19192, 1994]
23. Sage CL, Marcus DC: Immunolocalization of ClC-K chloride channel in strial marginal cells and vestibular dark cells. Hear Res 160: 1-9, 2001
24. Simon DB, Bindra RS, Mansfield TA, Nelson-Williams C, Mendonca E, Stone R, Schurman S, Nayir A, Alpay H, Bakkaloglu A, Rodriguez-Soriano J, Morales JM, Sanjad SA, Taylor CM, Pilz D, Brem A, Trachtman H, Griswold W, Richard GA, John E, Lifton RP: Mutations in the chloride channel gene, CLCNKB, cause Bartter's syndrome type III. Nat Genet 17: 171-178, 1997
25. Adachi S, Uchida S, Ito H, Hata M, Hiroe M, Marumo F, Sasaki S: Two isoforms of a chloride channel predominantly expressed in thick ascending limb of Henle's loop and collecting ducts of rat kidney. J Biol Chem 269: 17677-17683, 1994
26. Uchida S, Sasaki S, Nitta K, Uchida K, Horita S, Nihei H, Marumo F: Localization and functional characterization of rat kidney-specific chloride channel, ClC-K1. J Clin Invest 95: 104-113, 1995
27. Matsumura Y, Uchida S, Kondo Y, Miyazaki H, Ko SB, Hayama A, Morimoto T, Liu W, Arisawa M, Sasaki S, Marumo F: Overt nephrogenic diabetes insipidus in mice lacking the CLC-K1 chloride channel. Nat Genet 21: 95-98, 1999
28. Nissant A, Lourdel S, Baillet S, Paulais M, Marvao P, Teulon J, Imbert-Teboul M: Heterogeneous distribution of chloride channels along the distal convoluted tubule probed by single-cell RT-PCR and patch clamp. Am J Physiol Renal Physiol 287: F1233-F1243, 2004
29. Yoshikawa M, Uchida S, Yamauchi A, Miyai A, Tanaka Y, Sasaki S, Marumo F: Localization of rat CLC-K2 chloride channel mRNA in the kidney. Am J Physiol 276: F552-F558, 1999
30. Mejia R, Wade JB: Immunomorphometric study of rat renal inner medulla. Am J Physiol Renal Physiol 282: F553-F557, 2002
31. Vandewalle A, Cluzeaud F, Bens M, Kieferle S, Steinmeyer K, Jentsch TJ: Localization and induction by dehydration of ClC-K chloride channels in the rat kidney. Am J Physiol 272: F678-F688, 1997
32. Kobayashi K, Uchida S, Mizutani S, Sasaki S, Marumo F: Intrarenal and cellular localization of CLC-K2 protein in the mouse kidney. J Am Soc Nephrol 12: 1327-1334, 2001
33. Kobayashi K, Uchida S, Okamura HO, Marumo F, Sasaki S: Human CLC-KB gene promoter drives the EGFP expression in the specific distal nephron segments and inner ear. J Am Soc Nephrol 13: 1992-1998, 2002
34. Simon DB, Karet FE, Hamdan JM, DiPietro A, Sanjad SA, Lifton RP: Bartter's syndrome, hypokalaemic alkalosis with hypercalciuria, is caused by mutations in the Na-K-2Cl cotransporter NKCC2. Nat Genet 13: 183-188, 1996
35. + channel, ROMK. Nat Genet 14: 152-156, 1996
36. Birkenhäger R, Otto E, Schürmann MJ, Vollmer M, Ruf EM, Maier-Lutz I, Beekmann F, Fekete A, Omran H, Feldmann D, Milford DV, Jeck N, Konrad M, Landau D, Knoers NVAM, Antignac C, Sudbrack R, Kispert A, Hildebrandt F: Mutation of BSND causes Bartter syndrome with sensorineural deafness and kidney failure. Nat Genet 29: 310-314, 2001
37. Vargas-Poussou R, Huang C, Hulin P, Houillier P, Jeunemaitre X, Paillard M, Planelles G, Dechaux M, Miller RT, Antignac C: Functional characterization of a calcium-sensing receptor mutation in severe autosomal dominant hypocalcemia with a Bartter-like syndrome. J Am Soc Nephrol 13: 2259-2266, 2002
38. Watanabe S, Fukumoto S, Chang H, Takeuchi Y, Hasegawa Y, Okazaki R, Chikatsu N, Fujita T: Association between activating mutations of calcium-sensing receptor and Bartter's syndrome. Lancet 360: 692-694, 2002
39. Fukuyama S, Hiramatsu M, Akagi M, Higa M, Ohta T: Novel mutations of the chloride channel Kb gene in two Japanese patients clinically diagnosed as Bartter syndrome with hypocalciuria. J. Clin Endocrinol Metab 89: 5847-5850, 2004
40. Jeck N, Konrad M, Peters M, Weber S, Bonzel KE, Seyberth HW: Mutations in the chloride channel gene, CLCNKB, leading to a mixed Bartter-Gitelman phenotype. Pediatr Res 48: 754-758, 2000
41. Zelikovic I, Szargel R, Hawash A, Labay V, Hatib I, Cohen N, Nakhoul F: A novel mutation in the chloride channel gene, CLCNKB, as a cause of Gitelman and Bartter syndromes. Kidney Int 63: 24-32, 2003
42. Simon DB, Nelson-Williams C, Bia MJ, Ellison D, Karet FE, Molina AM, Vaara I, Iwata F, Cushner HM, Koolen M, Gainza FJ, Gitleman HJ, Lifton RP: Gitelman's variant of Bartter's syndrome, inherited hypokalaemic alkalosis, is caused by mutations in the thiazide-sensitive Na-Cl cotransporter. Nat Genet 12: 24-30, 1996
43. Liapis H, Nag M, Kaji DM: K-Cl cotransporter expression in the human kidney. Am J Physiol 275: C1432-C1437, 1998
44. Liu W, Morimoto T, Kondo Y, Iinuma K, Uchida S, Sasaki S, Marumo F, Imai M: Analysis of NaCl transport in thin ascending limb of Henle's loop in CLC-Kl null mice. Am J Physiol Renal Physiol 282: F451-F457, 2002
45. -/- mice kidney. Am J Physiol 280: F79-F87, 2001
46. Waldegger S, Jeck N, Barth P, Peters M, Vitzthum H, Wolf K, Kurtz A, Konrad M, Seyberth HW: Barttin increases surface expression and changes current properties of ClC-K channels. Pflügers Arch 444: 411-418, 2002
47. Lourdel S, Paulais M, Marvao P, Nissant A, Teulon J: A chloride channel at the basolateral membrane of the distal-convoluted tubule: a candidate ClC-K channel. J Gen Physiol 121: 287-300, 2003
48. Schwake M, Friedrich T, Jentsch TJ: An internalization signal in ClC-5, an endosomal CP-channel mutated in Dent's disease. J Biol Chem 276: 12049-12054, 2001
49. + channel deleted in Liddle's syndrome. EMBO J 15: 2371-2380, 1996
50. Embark HM, Bohmer C, Palmada M, Rajamanickam J, Wyatt AW, Wallisch S, Capasso G, Waldegger P, Seyberth HW, Waldegger S, Lang F: Regulation of CLC-Ka/barttin by the ubiquitin ligase Nedd4-2 and the serum- and glucocorticoid-dependent kinases. Kidney Int 66: 1918-1925, 2004
51. Jeck N, Waldegger P, Doroszewicz J, Seyberth H, Waldegger S: A common sequence variation of the CLCNKB gene strongly activates ClC-Kb chloride channel activity. Kidney Int 65: 190-197, 2004
52. Jeck N, Waldegger S, Lampert A, Boehmer C, Waldegger P, Lang PA, Wissinger B, Friedrich B, Risler T, Moehle R, Lang UE, Zill P, Bondy B, Schaeffeler E, Asante-Poku S, Seyberth H, Schwab M, Lang F: Activating mutation of the renal epithelial chloride channel ClC-Kb predisposing to hypertension. Hypertension 43: 1175-1181, 2004
53. Geller DS: A genetic predisposition to hypertension? Hypertension 44: 27-28, 2004
54. Kokubo Y, Iwai N, Tago N, Inamoto N, Okayama A, Yamawaki H, Naraba H, Tomoike H: Association analysis between hypertension and CYBA, CLCNKB, and KCNMB1 functional polymorphisms in the Japanese population. Circ J 69: 138-142, 2005
55. Schlingmann KP, Konrad M, Jeck N, Waldegger P, Reinalter SC, Holder M, Seyberth HW, Waldegger S: Salt wasting and deafness resulting from mutations in two chloride channels. N Engl J Med 350: 1314-1319, 2004
56. Jeck N, Reinalter SC, Henne T, Marg W, Mallmann R, Pasel K, Vollmer M, Klaus G, Leonhardt A, Seyberth HW, Konrad M: Hypokalemic salt-losing tubulopathy with chronic renal failure and sensorineural deafness. Pediatrics 108: E5, 2001
57. Boettger T, Hübner C, Maier H, Rust MB, Beck FX, Jentsch TJ: Deafness and renal tubular acidosis in mice lacking the K-Cl cotransporter Kcc4. Nature 416: 874-878, 2002
58. Koch MC, Steinmeyer K, Lorenz C, Ricker K, Wolf F, Otto M, Zoll B, Lehmann-Horn F, Grzeschik KH, Jentsch TJ: The skeletal muscle chloride channel in dominant and recessive human myotonia. Science 257: 797-800, 1992
59. Pusch M, Steinmeyer K, Koch MC, Jentsch TJ: Mutations in dominant human myotonia congenita drastically alter the voltage dependence of the ClC-1 chloride channel. Neuron 15: 1455-1463, 1995
60. Steinmeyer K, Klocke R, Ortland C, Gronemeier M, Jockusch H, Gründer S, Jentsch TJ: Inactivation of muscle chloride channel by transposon insertion in myotonic mice. Nature 354: 304-308, 1991
61. Steinmeyer K, Lorenz C, Pusch M, Koch MC, Jentsch TJ: Multimeric structure of ClC-1 chloride channel revealed by mutations in dominant myotonia congenita (Thomsen). EMBO J 13: 737-743, 1994
62. Kornak U, Kasper D, Bösl MR, Kaiser E, Schweizer M, Schulz A, Friedrich W, Delling G, Jentsch TJ: Loss of the ClC-7 chloride channel leads to osteopetrosis in mice and man. Cell 104: 205-215, 2001
63. Cleiren E, Benichou O, Van Hul E, Gram J, Bollerslev J, Singer FR, Beaverson K, Aledo A, Whyte MP, Yoneyama T, deVernejoul MC, Van Hul W: Albers-Schönberg disease (autosomal dominant osteopetrosis, type II) results from mutations in the ClCN7 chloride channel gene. Hum Mol Genet 10: 2861-2867, 2001
64. Saviane C, Conti F, Pusch M: The muscle chloride channel ClC-1 has a double-barreled appearance that is differentially affected in dominant and recessive myotonia. J Gen Physiol 113: 457-468, 1999
65. --channel disruption impairs endocytosis in a mouse model for Dent's disease. Nature 408: 369-373, 2000
66. Lloyd SE, Pearce SH, Fisher SE, Steinmeyer K, Schwappach B, Scheinman SJ, Harding B, Bolino A, Devoto M, Goodyer P, Rigden SP, Wrong O, Jentsch TJ, Craig IW, Thakker RV: A common molecular basis for three inherited kidney stone diseases. Nature 379: 445-449, 1996
67. Duan D, Winter C, Cowley S, Hume JR, Horowitz B: Molecular identification of a volume-regulated chloride channel. Nature 390: 417-421, 1997
68. Stobrawa SM, Breiderhoff T, Takamori S, Engel D, Schweizer M, Zdebik AA, Bösl MR, Ruether K, Jahn H, Draguhn A, Jahn R, Jentsch TJ: Disruption of ClC-3, a chloride channel expressed on synaptic vesicles, leads to a loss of the hippocampus. Neuron 29: 185-196, 2001
69. Li X, Wang T, Zhao Z, Weinman SA: The ClC-3 chloride channel promotes acidification of lysosomes in CHO-K1 and Huh-7 cells. Am J Physiol Cell Physiol 282: C1483-C1491, 2002
70. Pirozzi G, McConnell SJ, Uveges AJ, Carter JM, Sparks AB, Kay BK, Fowlkes DM: Identification of novel human WW domain-containing proteins by cloning of ligand targets. J Biol Chem 272: 14611-14616, 1997
71. Hryciw DH, Ekberg J, Lee A, Lensink IL, Kumar S, Guggino WB, Cook DI, Pollock CA, Poronnik P: Nedd4-2 functionally interacts with ClC-5: Involvement in constitutive albumin endocytosis in proximal tubule cells. J Biol Chem 279: 54996-55007, 2004
72. Günther W, Lüchow A, Cluzeaud F, Vandewalle A, Jentsch TJ: ClC-5, the chloride channel mutated in Dent's disease, colocalizes with the proton pump in endocytotically active kidney cells. Proc Natl Acad Sci U S A 95: 8075-8080, 1998
73. Vandewalle A, Cluzeaud F, Peng KC, Bens M, Lüchow A, Günther W, Jentsch TJ: Tissue distribution and subcellular localization of the ClC-5 chloride channel in rat intestinal cells. Am J Physiol Cell Physiol 280: C373-C381, 2001
74. Devuyst O, Christie PT, Courtoy PJ, Beauwens R, Thakker RV: Intra-renal and subcellular distribution of the human chloride channel, CLC-5, reveals a pathophysiological basis for Dent's disease. Hum Mol Genet 8: 247-257, 1999
75. +-ATPase. Am J Physiol 277: F957-F965, 1999
76. Wrong OM, Norden AG, Feest TG: Dent's disease; a familial proximal renal tubular syndrome with low-molecular-weight proteinuria, hypercalciuria, nephrocalcinosis, metabolic bone disease, progressive renal failure and a marked male predominance. QJM 87: 473-493, 1994
77. Günther W, Piwon N, Jentsch TJ: The ClC-5 chloride channel knock-out mouse-An animal model for Dent's disease. Pflügers Arch 445: 456-462, 2003
78. Wang SS, Devuyst O, Courtoy PJ, Wang XT, Wang H, Wang Y, Thakker RV, Guggino S, Guggino WB: Mice lacking renal chloride channel, CLC-5, are a model for Dent's disease, a nephrolithiasis disorder associated with defective receptor-mediated endocytosis. Hum Mol Genet 9: 2937-2945, 2000
79. Leheste JR, Rolinski B, Vorum H, Hilpert J, Nykjaer A, Jacobsen C, Aucouturier P, Moskaug JO, Otto A, Christensen EI, Willnow TE: Megalin knockout mice as an animal model of low molecular weight proteinuria. Am J Pathol 155: 1361-1370, 1999
80. Christensen EI, Devuyst O, Dom G, Nielsen R, Van der Smissen P, Verroust P, Leruth M, Guggino WB, Courtoy PJ: Loss of chloride channel ClC-5 impairs endocytosis by defective trafficking of megalin and cubilin in kidney proximal tubules. Proc Natl Acad Sci U S A 100: 8472-8477, 2003
81. Hilpert J, Nykjaer A, Jacobsen C, Wallukat G, Nielsen R, Moestrup SK, Haller H, Luft FC, Christensen EI, Willnow TE: Megalin antagonizes activation of the parathyroid hormone receptor. J Biol Chem 274: 5620-5625, 1999
82. Nykjaer A, Dragun D, Walther D, Vorum H, Jacobsen C, Herz J, Melsen F, Christensen EI, Willnow TE: An endocytic pathway essential for renal uptake and activation of the steroid 25-(OH) vitamin D3. Cell 96: 507-515, 1999
83. Norden AG, Lapsley M, Lee PJ, Pusey CD, Scheinman SJ, Tam FW, Thakker RV, Unwin RJ, Wrong O: Glomerular protein sieving and implications for renal failure in Fanconi syndrome. Kidney Int 60: 1885-1892, 2001
84. Kaufmann M, Muff R, Stieger B, Biber J, Murer H, Fischer JA: Apical and basolateral parathyroid hormone receptors in rat renal cortical membranes. Endocrinology 134: 1173-1178, 1994
85. Traebert M, Völkl H, Biber J, Murer H, Kaissling B: Luminal and contraluminal action of 1-34 and 3-34 PTH peptides on renal type IIa Na-Pi cotransporter. Am J Physiol 278: F792-F798, 2000
86. Murer H, Forster I, Hernando N, Lambert G, Traebert M, Biber J: Posttranscriptional regulation of the proximal tubule NaPi-II transporter in response to PTH and dietary Pi. Am J Physiol 277: F676-F684, 1999
87. 3-1α-hydroxylase gene promoter. Proc Natl Acad Sci U S A 95: 1387-1391, 1998
88. 3 in intact animals. Endocrinology 140: 2224-2231, 1999
89. Scheinman SJ: X-linked hypercalciuric nephrolithiasis: Clinical syndromes and chloride channel mutations. Kidney Int 53: 3-17, 1998
90. Silva IV, Cebotaru V, Wang H, Wang XT, Wang SS, Guo G, Devuyst O, Thakker RV, Guggino WB, Guggino SE: The ClC-5 knockout mouse model of Dent's disease has renal hypercalciuria and increased bone turnover. J Bone Miner Res 18: 615-623, 2003
91. Aniento F, Gu F, Parton RG, Gruenberg J: An endosomal βCOP is involved in the pH-dependent formation of transport vesicles destined for late endosomes. J Cell Biol 133: 29-41, 1996
92. Maranda B, Brown D, Bourgoin S, Casanova JE, Vinay P, Ausiello DA, Marshansky V: Intra-endosomal pH-sensitive recruitment of the Arf-nucleotide exchange factor ARNO and Arf6 from cytoplasm to proximal tubule endosomes. J Biol Chem 276: 18540-18550, 2001
93. Hara-Chikuma M, Yang B, Sonawane ND, Sasaki S, Uchida S, Verkman AS: ClC-3 chloride channels facilitate endosomal acidification and chloride accumulation. J Biol Chem 280: 1241-1247, 2005
94. Kasper D, Planells-Cases R, Fuhrmann JC, Scheel O, Zeitz O, Ruether K, Schmitt A, Poet M, Steinfeld R, Schweizer M, Kornak U, Jentsch TJ: Loss of the chloride channel ClC-7 leads to lysosomal storage disease and neurodegeneration. EMBO J 2005 24: 1079-1091
95. Wang T, Weinman SA: Involvement of chloride channels in hepatic copper metabolism: ClC4 promotes copper incorporation into ceruloplasmin. Gastroenterology 126: 1157-1166, 2004
96. + exchange impairs receptor-mediated albumin endocytosis in renal proximal tubule-derived epithelial cells from opossum. J Physiol 520: 709-721, 1999
97. + exchanger supports proximal tubular protein reabsorption in vivo. Am J Physiol Renal Physiol 287: F469-F473, 2004
98. Lauf PK, Adragna NC: K-Cl cotransport: Properties and molecular mechanism. Cell Physiol Biochem 10: 341-354, 2000
99. Boettger T, Rust MB, Maier H, Seidenbecher T, Schweizer M, Keating DJ, Faulhaber J, Ehmke H, Pfeffer C, Scheel O, Lemcke B, Horst J, Leuwer R, Pape HC, Völkl H, Hübner CA, Jentsch TJ: Loss of K-Cl co-transporter KCC3 causes deafness, neurodegeneration and reduced seizure threshold. EMBO J 22: 5422-5434, 2003
100. Hübner C, Stein V, Hermanns-Borgmeyer I, Meyer T, Ballanyi K, Jentsch TJ: Disruption of KCC2 reveals an essential role of K-Cl-cotransport already in early synaptic inhibition. Neuron 30: 515-524, 2001
101. Howard HC, Mount DB, Rochefort D, Byun N, Dupre N, Lu J, Fan X, Song L, Riviere JB, Prevost C, Horst J, Simonati A, Lemcke B, Welch R, England R, Zhan FQ, Mercado A, Siesser WB, George AL Jr, McDonald MP, Bouchard JP, Mathieu J, Delpire E, Rouleau GA: The K-Cl cotransporter KCC3 is mutant in a severe peripheral neuropathy associated with agenesis of the corpus callosum. Nat Genet 32: 384-392, 2002