Direct endosomal acidification by the outwardly rectifying CLC-5 Cl-/H+ exchanger

Journal of Physiology

Volumn 588, Issue 12, 2010, Pages 2033-2045

  Smith, Andrew J ^a   Lippiat, Jonathan D ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BAFILOMYCIN A1; CHLORIDE; HYDROGEN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL; VOLTAGE GATED CALCIUM CHANNEL 5; CHLORIDE CHANNEL; CLC-5 CHLORIDE CHANNEL; ENZYME INHIBITOR; HYBRID PROTEIN; MACROLIDE; PHOTOPROTEIN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; CHLORIDE HYDROGEN EXCHANGER PROTEIN; CHLORIDE ION; MEMBRANE PROTEIN; PROTON; VOLTAGE GATED CHLORIDE CHANNEL; VOLTAGE GATED CHLORIDE CHANNEL 5;

ACIDIFICATION; ARTICLE; CALCIUM CURRENT; CELL LINE; CHLORIDE TRANSPORT; CONTROLLED STUDY; CYTOPLASM; EMBRYO; ENDOSOME; ENZYME INHIBITION; HUMAN; HUMAN CELL; ION EXCHANGE; KIDNEY TUBULE CELL; MUTATION; PATCH CLAMP; PH; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTON TRANSPORT; WHOLE CELL; ANTAGONISTS AND INHIBITORS; CONFOCAL MICROSCOPY; DRUG EFFECTS; GENETIC TRANSFECTION; GENETICS; MEMBRANE POTENTIAL; METABOLISM; PATCH CLAMP TECHNIQUE; RNA INTERFERENCE; ANIMAL CELL; ANION EXCHANGE; CELL LEVEL; CELL PH; CHLORIDE CONDUCTANCE; CHLORIDE CURRENT; CLC 5 GENE; ENDOSOMAL ACIDIFICATION; GENE; NONHUMAN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVERSAL POTENTIAL; WHOLE CELL PATCH CLAMP;

CELL LINE; CHLORIDE CHANNELS; CHLORIDES; ENDOSOMES; ENZYME INHIBITORS; HUMANS; HYDROGEN-ION CONCENTRATION; LUMINESCENT PROTEINS; MACROLIDES; MEMBRANE POTENTIALS; MICROSCOPY, CONFOCAL; MUTATION; PATCH-CLAMP TECHNIQUES; RECOMBINANT FUSION PROTEINS; RNA INTERFERENCE; TRANSFECTION; VACUOLAR PROTON-TRANSLOCATING ATPASES;

EID: 77954643733     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2010.188540     Document Type: Article

References (39)

1. Accardi A, Miller C. Secondary active transport mediated by a prokaryotic homologue of CLC Cl- channels. Nature 2004, 427:803-807.
2. Accardi A, Walden M, Nguitragool W, Jayaram H, Williams C, Miller C. Separate ion pathways in a Cl-/H+ exchanger. J Gen Physiol 2005, 126:563-570.
3. 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 2003, 100:8472-8477.
4. 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 1999, 8:247-257.
5. Disbrow GL, Hanover JA, Schlegel R. Endoplasmic reticulum-localized human papillomavirus type 16 E5 protein alters endosomal pH but not trans-Golgi pH. J Virol 2005, 79:5839-5846.
6. Friedrich T, Breiderhoff T, Jentsch TJ. Mutational analysis demonstrates that ClC-4 and ClC-5 directly mediate plasma membrane currents. J Biol Chem 1999, 274:896-902.
7. 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 1998, 95:8075-8080.
8. Günther W, Piwon N, Jentsch TJ. The ClC-5 chloride channel knock-out mouse - an animal model for Dent's disease. Pflugers Arch 2003, 445:456-462.
9. Hara-Chikuma M, Wang Y, Guggino SE, Guggino WB, Verkman AS. Impaired acidification in early endosomes of ClC-5 deficient proximal tubule. Biochem Biophys Res Commun 2005, 329:941-946.
10. Hryciw DH, Ekberg J, Ferguson C, Lee A, Wang D, Parton RG, Pollock CA, Yun CC, Poronnik P. Regulation of albumin endocytosis by PSD95/Dlg/ZO-1 (PDZ) scaffolds. Interaction of Na+-H+ exchange regulatory factor-2 with ClC-5. J Biol Chem 2006a, 281:16068-16077.
11. Hryciw DH, Ekberg J, Pollock CA, Poronnik P. ClC-5: a chloride channel with multiple roles in renal tubular albumin uptake. Int J Biochem Cell Biol 2006b, 38:1036-1042.
12. Jentsch TJ. Chloride and the endosomal-lysosomal pathway: emerging roles of CLC chloride transporters. J Physiol 2007, 578:633-640.
13. Jentsch TJ, Neagoe I, Scheel O. CLC chloride channels and transporters. Curr Opin Neurobiol 2005, 15:319-325.
14. Jouret F, Bernard A, Hermans C, Dom G, Terryn S, Leal T, Lebecque P, Cassiman JJ, Scholte BJ, de Jonge HR, Courtoy PJ, Devuyst O. Cystic fibrosis is associated with a defect in apical receptor-mediated endocytosis in mouse and human kidney. J Am Soc Nephrol 2007, 18:707-718.
15. Mankouri J, Taneja TK, Smith AJ, Ponnambalam S, Sivaprasadarao A. Kir6.2 mutations causing neonatal diabetes prevent endocytosis of ATP-sensitive potassium channels. EMBO J 2006, 25:4142-4151.
16. Marshansky V, Ausiello DA, Brown D. Physiological importance of endosomal acidification: potential role in proximal tubulopathies. Curr Opin Nephrol Hypertens 2002, 11:527-537.
17. Matsuda JJ, Filali MS, Volk KA, Collins MM, Moreland JG, Lamb FS. Overexpression of CLC-3 in HEK293T cells yields novel currents that are pH dependent. Am J Physiol Cell Physiol 2008, 294:C251-C262.
18. Miesenböck G, De Angelis DA, Rothman JE. Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 1998, 394:192-195.
19. Miller FJ, Filali M, Huss GJ, Stanic B, Chamseddine A, Barna TJ, Lamb FS. Cytokine activation of nuclear factor κB in vascular smooth muscle cells requires signaling endosomes containing Nox1 and CLC-3. Circ Res 2007, 101:663-671.
20. Moulin P, Igarashi T, Van Der Smissen P, Cosyns JP, Verroust P, Thakker RV, Scheinman SJ, Courtoy PJ, Devuyst O. Altered polarity and expression of H+-ATPase without ultrastructural changes in kidneys of Dent's disease patients. Kidney Int 2003, 63:1285-1295.
21. Picollo A, Pusch M. Chloride/proton antiporter activity of mammalian CLC proteins ClC-4 and ClC-5. Nature 2005, 436:420-423.
22. Piwon N, Günther W, Schwake M, Bosl MR, Jentsch TJ. ClC-5 Cl- channel disruption impairs endocytosis in a mouse model for Dent's disease. Nature 2000, 408:369-373.
23. Pusch M, Jordt SE, Stein V, Jentsch TJ. Chloride dependence of hyperpolarization-activated chloride channel gates. J Physiol 1999, 515:341-353.
24. Pusch M, Ludewig U, Rehfeldt A, Jentsch TJ. Gating of the voltage-dependent chloride channel CIC-0 by the permeant anion. Nature 1995, 373:527-531.
25. Rychkov GY, Pusch M, Astill DS, Roberts ML, Jentsch TJ, Bretag AH. Concentration and pH dependence of skeletal muscle chloride channel ClC-1. J Physiol 1996, 497:423-435.
26. Sabolic I, Burckhardt G. Characteristics of the proton pump in rat renal cortical endocytotic vesicles. Am J Physiol Renal Physiol 1986, 250:F817-F826.
27. Saito M, Hanson PI, Schlesinger P. Luminal chloride-dependent activation of endosome calcium channels: patch clamp study of enlarged endosomes. J Biol Chem 2007, 282:27327-27333.
28. Scheel O, Zdebik AA, Lourdel S, Jentsch TJ. Voltage-dependent electrogenic chloride/proton exchange by endosomal CLC proteins. Nature 2005, 436:424-427.
29. Schmid A, Burckhardt G, Gögelein H. Single chloride channels in endosomal vesicle preparations from rat kidney cortex. J Membr Biol 1989, 111:265-275.
30. Smith AJ, Lippiat JD. Voltage-dependent charge movement associated with activation of the CLC-5 2Cl-/1H+ exchanger. FASEB J 2010
31. Smith AJ, Reed AA, Loh NY, Thakker RV, Lippiat JD. Characterization of Dent's disease mutations of CLC-5 reveals a correlation between functional and cell biological consequences and protein structure. Am J Physiol Renal Physiol 2009, 296:F390-F397.
32. Sonawane ND, Thiagarajah JR, Verkman AS. Chloride concentration in endosomes measured using a ratioable fluorescent Cl- indicator: evidence for chloride accumulation during acidification. J Biol Chem 2002, 277:5506-5513.
33. Sonawane ND, Verkman AS. Determinants of [Cl-] in recycling and late endosomes and Golgi complex measured using fluorescent ligands. J Cell Biol 2003, 160:1129-1138.
34. Stanfield PR, Davies NW, Shelton PA, Khan IA, Brammar WJ, Standen NB, Conley EC. The intrinsic gating of inward rectifier K+ channels expressed from the murine IRK1 gene depends on voltage, K+ and Mg2+. J Physiol 1994, 475:1-7.
35. Ulmasov B, Bruno J, Woost PG, Edwards JC. Tissue and subcellular distribution of CLIC1. BMC Cell Biol 2007, 8:8.
36. Van Dyke RW. Proton pump-generated electrochemical gradients in rat liver multivesicular bodies. Quantitation and effects of chloride. J Biol Chem 1988, 263:2603-2611.
37. 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 2000, 9:2937-2945.
38. Zdebik AA, Zifarelli G, Bergsdorf EY, Soliani P, Scheel O, Jentsch TJ, Pusch M. Determinants of anion-proton coupling in mammalian endosomal CLC proteins. J Biol Chem 2008, 283:4219-4227.
39. Zifarelli G, Pusch M. Conversion of the 2 Cl-/1 H+ antiporter ClC-5 in a NO3-/H+ antiporter by a single point mutation. EMBO J 2009, 10:1111-1116.