Conformational defects underlie proteasomal degradation of Dent's disease-causing mutants of ClC-5

Biochemical Journal

Volumn 452, Issue 3, 2013, Pages 391-400

  D'Antonio, Christina ^a,b   Molinski, Steven ^a,b   Ahmadi, Saumel ^a,b   Huan, Ling Jun ^a   Wellhauser, Leigh ^a,b   Bear, Christine E ^a,b  

^a HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Misfolded membrane protein; Polyubiquitination; Proteasome; Unfolded protein response

Indexed keywords

CHLORIDE; PROTEASOME; PROTEINASE; VOLTAGE GATED CHLORIDE CHANNEL;

ARTICLE; DENT DISEASE; ENZYME DEGRADATION; EPITHELIUM CELL; GENE MUTATION; HUMAN; HUMAN CELL; MUTANT; PRIORITY JOURNAL; PROTEIN DEGRADATION;

ANIMALS; CHLORIDE CHANNELS; CODON, NONSENSE; DENT DISEASE; ENDOPLASMIC RETICULUM; HEK293 CELLS; HUMANS; MUTATION, MISSENSE; OPOSSUMS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN CONFORMATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOSTASIS DEFICIENCIES;

DIDELPHIDAE; EUKARYOTA;

EID: 84878402423     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20121848     Document Type: Article

References (31)

1. Gunther, W., Piwon, N. and Jentsch, T. J. (2003) The ClC-5 chloride channel knock-out mouse: an animal model for Dent's disease. Pflugers Arch. 445, 456-462 (Pubitemid 36222992)
2. - channel disruption impairs endocytosis in a mouse model for Dent's disease. Nature 408, 369-373
3. Lloyd, S. E., Gunther, W., Pearce, S. H., Thomson, A., Bianchi, M. L., Bosio, M., Craig, I. W., Fisher, S. E., Scheinman, S. J., Wrong, O. et al. (1997) Characterisation of renal chloride channel, CLCN5, mutations in hypercalciuric nephrolithiasis (kidney stones) disorders. Hum. Mol. Genet. 6, 1233-1239 (Pubitemid 27351062)
4. Christensen, E. I., Devuyst, O., Dom, G., Nielsen, R., Van der Smissen, P., Verroust, P., Leruth, M., Guggino, W. B. and Courtoy, P. J. (2003) 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 (Pubitemid 36842569)
5. Devuyst, O., Jouret, F., Auzanneau, C. and Courtoy, P. J. (2005) Chloride channels and endocytosis: new insights from Dent's disease and ClC-5 knockout mice. Nephron Physiol. 99, 69-73
6. Grand, T., L'Hoste, S., Mordasini, D., Defontaine, N., Keck, M., Pennaforte, T., Genete, M., Laghmani, K., Teulon, J. and Lourdel, S. (2011) Heterogeneity in the processing of CLCN5 mutants related to Dent disease. Hum. Mutat. 32, 476-483
7. Grand, T., Mordasini, D., L'Hoste, S., Pennaforte, T., Genete, M., Biyeyeme, M. J., Vargas-Poussou, R., Blanchard, A., Teulon, J. and Lourdel, S. (2009) Novel CLCN5 mutations in patients with Dent's disease result in altered ion currents or impaired exchanger processing. Kidney Int. 76, 999-1005
8. Dutzler, R., Campbell, E. B., Cadene, M., Chait, B. T. and MacKinnon, R. (2002) X-ray structure of a ClC chloride channel at 3.0 Å reveals the molecular basis of anion selectivity. Nature 415, 287-294 (Pubitemid 34087544)
9. Dutzler, R., Campbell, E. B. and MacKinnon, R. (2003) Gating the selectivity filter in ClC chloride channels. Science 300, 108-112 (Pubitemid 36423038)
10. Feng, L., Campbell, E. B., Hsiung, Y. and MacKinnon, R. (2010) Structure of a eukaryotic CLC transporter defines an intermediate state in the transport cycle. Science 330, 635-641
11. Lourdel, S., Grand, T., Burgos, J., Gonzalez, W., Sepulveda, F. V. and Teulon, J. (2012) ClC-5 mutations associated with Dent's disease: a major role of the dimer interface. Pflugers Arch. 463, 247-256
12. Mohammad-Panah, R., Harrison, R., Dhani, S., Ackerley, C., Huan, L. J., Wang, Y. and Bear, C. E. (2003) The chloride channel ClC-4 contributes to endosomal acidification and trafficking. J. Biol. Chem. 278, 29267-29277 (Pubitemid 36935843)
13. Smith, A. J., Reed, A. A., Loh, N. Y., Thakker, R. V. and Lippiat, J. D. (2009) 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. 296, F390-F397
14. Gelman, M. S. and Kopito, R. R. (2003) Cystic fibrosis: premature degradation of mutant proteins as a molecular disease mechanism. Methods Mol. Biol. 232, 27-37
15. Kiser, G. L., Gentzsch, M., Kloser, A. K., Balzi, E., Wolf, D. H., Goffeau, A. and Riordan, J. R. (2001) Expression and degradation of the cystic fibrosis transmembrane conductance regulator in Saccharomyces cerevisiae. Arch. Biochem. Biophys. 390, 195-205 (Pubitemid 32568481)
16. Kubota, K., Niinuma, Y., Kaneko, M., Okuma, Y., Sugai, M., Omura, T., Uesugi, M., Uehara, T., Hosoi, T. and Nomura, Y. (2006) Suppressive effects of 4-phenylbutyrate on the aggregation of Pael receptors and endoplasmic reticulum stress. J. Neurochem. 97, 1259-1268 (Pubitemid 43725566)
17. Rubenstein, R. C. and Zeitlin, P. L. (2000) Sodium 4-phenylbutyrate downregulates Hsc70: implications for intracellular trafficking of ΔF508-CFTR. Am. J. Physiol. Cell Physiol. 278, C259-C267 (Pubitemid 30131142)
18. Denning, G. M., Anderson, M. P., Amara, J. F., Marshall, J., Smith, A. E. and Welsh, M. J. (1992) Processing of mutant cystic fibrosis transmembrane conductance regulator is temperature-sensitive. Nature 358, 761-764
19. Yuzaki, M. (2010) Snapin snaps into the dynein complex for late endosome-lysosome trafficking and autophagy. Neuron 68, 4-6
20. Yoshida, Y., Chiba, T., Tokunaga, F., Kawasaki, H., Iwai, K., Suzuki, T., Ito, Y., Matsuoka, K., Yoshida, M., Tanaka, K. and Tai, T. (2002) E3 ubiquitin ligase that recognizes sugar chains. Nature 418, 438-442 (Pubitemid 34826846)
21. - channel mutated in Dent's disease. J. Biol. Chem. 276, 12049-12054
22. Thelen, M., Damumue, M., Schweizer, M., Hagel, C., Wong, A. M., Cooper, J. D., Braulke, T. and Galliciotti, G. (2012) Disruption of the autophagy-lysosome pathway is involved in neuropathology of the nclf mouse model of neuronal ceroid lipofuscinosis. PLoS ONE 7, e35493
23. Vij, N., Fang, S. and Zeitlin, P. L. (2006) Selective inhibition of endoplasmic reticulum-associated degradation rescues ΔF508-cystic fibrosis transmembrane regulator and suppresses interleukin-8 levels: therapeutic implications. J. Biol. Chem. 281, 17369-17378
24. Pearse, B. R. and Hebert, D. N. (2006) Cotranslocational degradation: utilitarianism in the ER stress response. Mol. Cell 23, 773-775 (Pubitemid 44344526)
25. Witte, I. and Horke, S. (2011) Assessment of endoplasmic reticulum stress and the unfolded protein response in endothelial cells. Methods Enzymol. 489, 127-146
26. Yan, W., Frank, C. L., Korth, M. J., Sopher, B. L., Novoa, I., Ron, D. and Katze, M. G. (2002) Control of PERK eIF2α kinase activity by the endoplasmic reticulum stress-induced molecular chaperone P58IPK. Proc. Natl. Acad. Sci. U.S.A. 99, 15920-15925 (Pubitemid 35462724)
27. Meyer, S., Savaresi, S., Forster, I. C. and Dutzler, R. (2007) Nucleotide recognition by the cytoplasmic domain of the human chloride transporter ClC-5. Nat. Struct. Mol. Biol. 14, 60-67 (Pubitemid 46067424)
28. Bouchecareilh, M. and Balch, W. E. (2012) Proteostasis, an emerging therapeutic paradigm for managing inflammatory airway stress disease. Curr. Mol. Med. 12, 815-826
29. Hutt, D. M., Olsen, C. A., Vickers, C. J., Herman, D., Chalfant, M., Montero, A., Leman, L. J., Burkle, R., Maryanoff, B. E., Balch, W. E. and Ghadiri, M. R. (2011) Potential agents for treating cystic fibrosis: cyclic tetrapeptides that restore trafficking and activity of ΔF508-CFTR. ACS Med. Chem. Lett. 2, 703-707
30. Hutt, D. M., Herman, D., Rodrigues, A. P., Noel, S., Pilewski, J. M., Matteson, J., Hoch, B., Kellner, W., Kelly, J. W., Schmidt, A. et al. (2010) Reduced histone deacetylase 7 activity restores function to misfolded CFTR in cystic fibrosis. Nat. Chem. Biol. 6, 25-33
31. + antiporter. Biophys. J. 102, 2060-2069