N-glycosylation of the Xenopus laevis ClC-5 protein plays a role in cell surface expression, affecting transport activity at the plasma membrane

Journal of Cellular Physiology

Volumn 210, Issue 2, 2007, Pages 479-488

  Schmieder, Sandra ^a   Bogliolo, Stéphanie ^a   Ehrenfeld, Jordi ^a  

^a UNIVERSITÉ CÔTE D'AZUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIPORTER; ASPARAGINE; BREFELDIN A; CHLORIDE; CHLORIDE CHANNEL; HYDROGEN; PROTEASOME; PROTEIN CLC 5; TUNICAMYCIN; XENOPUS PROTEIN;

ANIMAL CELL; ARTICLE; BIOCHEMISTRY; CELL MEMBRANE; CELL SURFACE; CLINICAL FEATURE; CONDUCTANCE; CONTROLLED STUDY; ENDOCYTOSIS; FUNCTIONAL PROTEOMICS; GENE EXPRESSION SYSTEM; GENE MUTATION; HYPERCALCIURIA; IMMUNOCYTOCHEMISTRY; KIDNEY PROXIMAL TUBULE; KIDNEY TUBULE CELL; NEPHROLITHIASIS; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE; PHOSPHATURIA; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN TRANSPORT; PROTEINURIA; UBIQUITINATION; VOLTAGE CLAMP; WILD TYPE; X LINKED HYPERCALCIURIC NEPHROLITHIASIS; XENOPUS LAEVIS;

ANIMALS; ASPARAGINE; CELL MEMBRANE; CHLORIDE CHANNELS; CHLORIDES; FEMALE; GLYCOSYLATION; INTRACELLULAR FLUID; MACROMOLECULAR SUBSTANCES; MEMBRANE POTENTIALS; MUTATION; OOCYTES; PATCH-CLAMP TECHNIQUES; POLYSACCHARIDES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN SYNTHESIS INHIBITORS; PROTEIN TRANSPORT; TIME FACTORS; XENOPUS LAEVIS; XENOPUS PROTEINS;

XENOPUS LAEVIS;

EID: 33845641027     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcp.20882     Document Type: Article

References (49)

1. Accardi A, Miller C. 2004. Secondary active transport mediated by a prokaryotic homologue of ClC Cl- channels. Nature 427:803-807.
2. Bolino A, Devoto M, Enia G, Zoccali C, Weissenbach J, Romeo G. 1993. Genetic mapping in the Xp11.2 region of a new form of X-linked hypophosphatemic rickets. Eur J Hum Genet 1:269-279.
3. Christensen EI, Devuyst O, Dom G, Nielsen R, Van der Smissen P, Verroust P, Leruth M, Guggino WB, Courtoy PJ. 2003. Loss of chloride channel ClC-5 impairs endocytosis by defective trafficking of megalin and cubilin in kidney proximal tubules. Proc Natl Acad Sci USA 100:8472-8477.
4. Devuyst O, Christie PT, Courtoy PJ, Beauwens R, Thakker RV. 1999. 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.
5. Dowland LK, Luyckx VA, Enck AH, Leclercq B, Yu AS. 2000. Molecular cloning and characterization of an intracellular chloride channel in the proximal tubule cell line, LLC-PK1. J Biol Chem 275:37765-37773.
6. Dutzler R, Campbell EB, Cadene M, Chait BT, MacKinnon R. 2002. X-ray structure of a ClC chloride channel at 3.0 A reveals the molecular basis of anion selectivity. Nature 415:287-294.
7. Estevez R, Boettger T, Stein V, Birkenhager R, Otto E, Hildebrandt F, Jentsch TJ. 2001. Barttin is a Cl- channel beta-subunit crucial for renal Cl-reabsorption and inner ear K+ secretion. Nature 414:558-561.
8. Fahlke C, Rhodes TH, Desai RR, George AL, Jr. 1998. Pore stoichiometry of a voltage-gated chloride channel. Nature 394:687-690.
9. Günther W, Lüchow A, Cluzeaud F, Vandewalle A, Jentsch TJ. 1998. ClC-5, the chloride channel mutated in Dent's disease, colocalizes with the proton pump in endocytotically active kidney cells. Proc Natl Acad Sci USA 95:8075-8080.
10. Günther W, Piwon N, Jentsch TJ. 2003. The ClC-5 chloride channel knock-out mouse-An animal model for Dent's disease. Pflugers Arch 445:456-462.
11. Gut A, Rappeler F, Hyka N, Balda MS, Hauri HP, Matter K. 1998. Carbohydrate-mediated Golgi to cell surface transport and apical targeting of membrane proteins. EMBO J 17:1919-1929.
12. Hampton RY. 2002. ER-associated degradation in protein quality control and cellular regulation. Curr Opin Cell Biol 14:476-482.
13. Hara-Chikuma M, Wang Y, Guggino SE, Guggino WB, Verkman AS. 2005. Impaired acidification in early endosomes of ClC-5 deficient proximal tubule. Biochem Biophys Res Commun 329:941-946.
14. Helenius A, Aebi M. 2001. Intracellular functions of N-linked glycans. Science 291:2364-2369.
15. Hilpert J, Nykjaer A, Jacobsen C, Wallukat G, Nielsen R, Moestrup SK, Haller H, Luft FC, Christensen EI, Willnow TE. 1999. Megalin antagonizes activation of the parathyroid hormone receptor. J Biol Chem 274:5620-5625.
16. Hryciw DH, Wang Y, Devuyst O, Pollock CA, Poronnik P, Guggino WB. 2003. Cofilin interacts with ClC-5 and regulates albumin uptake in proximal tubule cell lines. J Biol Chem 278:40169-40176.
17. Hryciw DH, Ekberg J, Lee A, Lensink IL, Kumar S, Guggino WB, Cook DI, Pollock CA, Poronnik P, 2004. Nedd4-2 functionally interacts with ClC-5: Involvement in constitutive albumin endocytosis in proximal tubule cells. J Biol Chem 279:54996-55007.
18. Hryciw DH, Ekberg J, Pollock CA, Poronnik P. 2006a. ClC-5: A chloride channel with multiple roles in renal tubular albumin uptake. Int J Biochem Cell Biol 38:1036-1042.
19. Hryciw DH, Ekberg J, Ferguson C, Lee A, Wang D, Parton RG, Pollock CA, Yun CC, Poronnik P. 2006b. Regulation of albumin endocytosis by PSD95/Dlg/ZO-1(PDZ) scaffolds: Interaction of Na+-H+ exchange regulatory factor-2 (NHERF2) with ClC-5. J Biol Chem. 281:16068-16077.
20. Klausner RD, Donaldson JG, Lippincott-Schwartz J. 1992. Brefeldin A: Insights into the control of membrane traffic and organelle structure. J Cell Biol 116:1071-1080.
21. Lin DH, Sterling H, Wang Z, Babilonia E, Yang B, Dong K, Hebert SC, Giebisch G, Wang WH. 2005. ROMK1 channel activity is regulated by monoubiquitination. Proc Natl Acad Sci USA 102:4306-4311.
22. Lippincott-Schwartz J, Yuan L, Tipper C, Amherdt M, Orci L, Klausner RD. 1991. Brefeldin A's effects on endosomes, lysosomes, and the TGN suggest a general mechanism for regulating organelle structure and membrane traffic. Cell 67:601-616.
23. 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. 1996. A common molecular basis for three inherited kidney stone diseases. Nature 379:445-449.
24. Lorenz C, Pusch M, Jentsch TJ. 1996. Heteromultimeric CLC chloride channels with novel properties. Proc Natl Acad Sci USA 93:13362-13366.
25. Luyckx VA, Goda FO, Mount DB, Nishio T, Hall A, Hebert SC, Hammond TG, Yu AS. 1998. Intrarenal and subcellular localization of rat CLC5. Am J Physiol 275:F761-F769.
26. Maulet Y, Lambert RC, Mykita S, Mouton J, Partisani M, Bailly Y, Bombarde G, Feltz A. 1999, Expression and targeting to the plasma membrane of xClC-K, a chloride channel specifically expressed in distinct tubule segments of Xenopus laevis kidney. Biochem J 340:737-743.
27. Moulin P, Igarashi T, Van der Smissen P, Cosyns JP, Verroust P, Thakker RV, Scheinman SJ, Courtoy PJ, Devuyst O. 2003. Altered polarity and expression of H-r-ATPase without ultrastructural changes in kidneys of Dent's disease patients. Kidney Int 63:1285-1295.
28. Opdenakker G, Rudd PM, Ponting CP, Dwek RA. 1993. Concepts and principles of glycobiology. FASEB J 7:1330-1337.
29. Picollo A, Pusch M. 2005. Chloride/proton antiporter activity of mammalian CLC proteins ClC-4 and ClC-5. Nature 436:420-423.
30. Piwon N, Günther W, Schwake M, Bösl MR, Jentsch TJ. 2000. ClC-5 Cl- channel disruption impairs endocytosis in a mouse model for Dent's disease. Nature 408:369-373.
31. Ramjeesingh M, Li C, Huan LJ, Garami E, Wang Y, Bear CE. 2000. Quaternary structure of the chloride channel ClC-2, Biochemistry 39:13838-13847.
32. Ratcliff FG, Ehrenfeld J. 1994. Activation of osmotically-activated potassium transporters after injection of mRNA from A6 cells in Xenopus oocytes. Biochim Biophys Acta 1190:248-256.
33. Robinson MS. 2004. Adaptable adaptors for coated vesicles. Trends Cell Biol 14:167-174.
34. Sakamoto H, Sado Y, Naito I, Kwon TH, Inoue S, Endo K, Kawasaki M, Uchida S, Nielsen S, Sasaki S, Marumo F. 1999. Cellular and subcellular immunolocalization of ClC-5 channel in mouse kidney: Colocalization with H+-ATPase. Am J Physiol 277:F957-F965.
35. Salazar G, Love R, Styers ML, Werner E, Peden A, Rodriguez S, Gearing M, Wainer BH, Faundez V. 2004. AP-3-dependent mechanisms control the targeting of a chloride channel (ClC-3) in neuronal and non-neuronal cells. J Biol Chem 279:25430-25439.
36. Scheel O, Zdebik AA, Lourdel S, Jentsch TJ. 2005. Voltage-dependent electrogenic chloride/proton exchange by endosomal CLC proteins. Nature 436:424-427.
37. Scheinman SJ. 1998. X-linked hypercalciuric nephrolithiasis: Clinical syndromes and chloride channel mutations. Kidney Int 53:3-17.
38. Schmieder S, Lindenthal S, Banderali U, Ehrenfeld J. 1998. Characterization of the putative chloride channel xClC-5 expressed in Xenopus laevis oocytes and comparison with endogenous chloride currents. J Physiol 511:379-393.
39. Schmieder S, Lindenthal S, Ehrenfeld J. 2001. Tissue-specific N-glycosylation of the ClC-3 Chloride channel. Biochem Biophys Res Commun 286:635-640.
40. Schmieder S, Lindenthal S, Ehrenfeld J. 2002. Cloning and characterisation of amphibian ClC-3 and ClC-5 chloride channels. Biochim Biophys Acta 1566:55-66.
41. Schnell JD, Hicke L. 2003. Non-traditional functions of ubiquitin and ubiquitin-binding proteins. J Biol Chem 278:35857-35860.
42. Schwake M, Friedrich T, Jentsch TJ. 2001. An internalization signal in ClC-5, an endosomal Cl-channel mutated in dent's disease. J Biol Chem 276:12049-12054.
43. Staub O, Gautschi I, Ishikawa T, Breitschopf K, Ciechanover A, Schild L, Rotin D. 1997. Regulation of stability and function of the epithelial Na+ channel (ENaC) by ubiquitination. EMBO J 16:6325-6336.
44. Steinmeyer K, Schwappach B, Bens M, Vandewalle A, Jentseh TJ. 1995. Cloning and functional expression of rat CLC-5, a chloride channel related to kidney disease. J Biol Chem 270:31172-31177.
45. Suzuki T, Rai T, Hayama A, Sohara E, Suda S, Itoh T, Sasaki S, Uchida S. 2006. Intraeellular localization of ClC chloride channels and their ability to form hetero-oligomers. J Cell Physiol 206:792-798.
46. van den Hove MF, Croizet-Berger K, Jouret F, Guggino SE, Guggino WB, Devuyst O, Courtoy PJ. 2006. The loss of the chloride channel, ClC-5, delays apical iodide efflux and induces a euthyroid goiter in the mouse thyroid gland. Endocrinology 147:1287-1296.
47. Vandewalle A, Cluzeaud F, Peng KC, Bens M, Lüehow A, Günther W, Jentsch TJ. 2001. Tissue distribution and subcellular localization of the ClC-5 chloride channel in rat intestinal cells. Am J Physiol Cell Physiol 280:C373-C381.
48. Wallace RA, Opresko L, Wiley HS, Selman K, 1983. The oocyte as an endocytic cell. Ciba Found Symp 98:228-248.
49. Wang Y, Cai H, Cebotaru L, Hryciw DH, Weinman EJ, Donowitz M, Guggino SE, Guggino WB. 2005. ClC-5: Role in endocytosis in the proximal tubule. Am J Physiol Renal Physiol 289:F850-F862.