Lysosomal degradation of endocytosed proteins depends on the chloride transport protein ClC-7

FASEB Journal

Volumn 23, Issue 12, 2009, Pages 4056-4068

  Wartosch, Lena ^a,b   Fuhrmann, Jens C ^a,d   Schweizer, Michaela ^c   Stauber, Tobias ^a   Jentsch, Thomas J ^a  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

^c UNIVERSITY OF HAMBURG   (Germany)

^d Metanomics GmbH   (Germany)

Author keywords

Lysosomal storage disease; NCL; Neurodegeneration; Neuronal ceroid lipofuscinosis

Indexed keywords

CARRIER PROTEIN; CHLORIDE TRANSPORT PROTEIN CIC7; PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; BRAIN REGION; CELL ACTIVATION; CELL CULTURE; CHIMERA; CONTROLLED STUDY; ENDOCYTOSIS; FEMALE; GENE DELETION; GENE DISRUPTION; GENE MUTATION; GENOTYPE; GLIA; HALF LIFE TIME; IN VIVO STUDY; KIDNEY PROXIMAL TUBULE; KIDNEY TUBULE CELL; KNOCKOUT MOUSE; LYSOSOME; MALE; MOUSE; NERVE CELL; NERVE CELL NECROSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; TISSUE SPECIFICITY;

MUS;

EID: 72749119040     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.09-130880     Document Type: Article

References (45)

1. Brandt, S., and Jentsch, T. J. (1995) ClC-6 and ClC-7 are two novel broadly expressed members of the CLC chloride channel family. FEBS Lett. 377, 15-20 (Pubitemid 26008977)
2. Jentsch, T. J. (2007) Chloride and the endosomal-lysosomal pathway: emerging roles of CLC chloride transporters. J. Physiol. 578, 633-640
3. Accardi, A., and Miller, C. (2004) Secondary active transport mediated by a prokaryotic homologue of ClC Cl- channels. Nature 427, 803-807 (Pubitemid 38297735)
4. Picollo, A., and Pusch, M. (2005) Chloride/proton antiporter activity of mammalian CLC proteins ClC-4 and ClC-5. Nature 436, 420-423 (Pubitemid 41059054)
5. Scheel, O., Zdebik, A. A., Lourdel, S., and Jentsch, T. J. (2005) Voltage-dependent electrogenic chloride/proton exchange by endosomal CLC proteins. Nature 436, 424-427 (Pubitemid 41059055)
6. Kasper, D., Planells-Cases, R., Fuhrmann, J. C., Scheel, O., Zeitz, O., Ruether, K., Schmitt, A., Poët, M., Steinfeld, R., Schweizer, M., Kornak, U., and Jentsch, T. J. (2005) Loss of the chloride channel ClC-7 leads to lysosomal storage disease and neurodegeneration. EMBO J. 24, 1079-1091 (Pubitemid 40470155)
7. Kornak, U., Kasper, D., Bösl, M. R., Kaiser, E., Schweizer, M., Schulz, A., Friedrich, W., Delling, G., and Jentsch, T. J. (2001) Loss of the ClC-7 chloride channel leads to osteopetrosis in mice and man. Cell 104, 205-215 (Pubitemid 32174837)
8. Lange, P. F., Wartosch, L., Jentsch, T. J., and Fuhrmann, J. C. (2006) ClC-7 requires Ostm1 as a beta-subunit to support bone resorption and lysosomal function. Nature 440, 220-223 (Pubitemid 43372100)
9. Graves, A. R., Curran, P. K., Smith, C. L., and Mindell, J. A. (2008) The Cl-/H+ antiporter ClC-7 is the primary chloride permeation pathway in lysosomes. Nature 453, 788-792
10. Mellman, I., Fuchs, R., and Helenius, A. (1986) Acidification of the endocytic and exocytic pathways. Annu. Rev. Biochem. 55, 663-700
11. Piwon, N., Günther, W., Schwake, M., Bösl, M. R., and Jentsch, T. J. (2000) ClC-5 Cl- -channel disruption impairs endocytosis in a mouse model for Dent's disease. Nature 408, 369-373
12. Lloyd, S. E., Pearce, S. H., Fisher, S. E., Steinmeyer, K., Schwappach, B., Scheinman, S. J., Harding, B., Bolino, A., Devoto, M., Goodyer, P., Rigden, S. P., Wrong, O., Jentsch, T. J., Craig, I. W., and Thakker, R. V. (1996) A common molecular basis for three inherited kidney stone diseases. Nature 379, 445-449 (Pubitemid 26039523)
13. Wang, S. S., Devuyst, O., Courtoy, P. J., Wang, X. T., Wang, H., Wang, Y., Thakker, R. V., Guggino, S., and Guggino, W. B. (2000) 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 (Pubitemid 32000767)
14. Stobrawa, S. M., Breiderhoff, T., Takamori, S., Engel, D., Schweizer, M., Zdebik, A. A., Bösl, M. R., Ruether, K., Jahn, H., Draguhn, A., Jahn, R., and Jentsch, T. J. (2001) Disruption of ClC-3, a chloride channel expressed on synaptic vesicles, leads to a loss of the hippocampus. Neuron 29, 185-196 (Pubitemid 32108731)
15. Chalhoub, N., Benachenhou, N., Rajapurohitam, V., Pata, M., Ferron, M., Frattini, A., Villa, A., and Vacher, J. (2003) Grey-lethal mutation induces severe malignant autosomal recessive osteopetrosis in mouse and human. Nat. Med. 9, 399-406 (Pubitemid 36460073)
16. Frattini, A., Pangrazio, A., Susani, L., Sobacchi, C., Mirolo, M., Abinun, M., Andolina, M., Flanagan, A., Horwitz, E. M., Mihci, E., Notarangelo, L. D., Ramenghi, U., Teti, A., Van Hove, J., Vujic, D., Young, T., Albertini, A., Orchard, P. J., Vezzoni, P., and Villa, A. (2003) Chloride channel ClCN7 mutations are responsible for severe recessive, dominant, and intermediate osteopetrosis. J. Bone Miner. Res. 18, 1740-1747 (Pubitemid 37322549)
17. Pangrazio, A., Poliani, P. L., Megarbane, A., Lefranc, G., Lanino, E., Di Rocco, M., Rucci, F., Lucchini, F., Ravanini, M., Facchetti, F., Abinun, M., Vezzoni, P., Villa, A., and Frattini, A. (2006) Mutations in OSTM1 (grey lethal) define a particularly severe form of autosomal recessive osteopetrosis with neural involvement. J. Bone Miner. Res. 21, 1098-1105 (Pubitemid 43962838)
18. Iwasato, T., Datwani, A., Wolf, A. M., Nishiyama, H., Taguchi, Y., Tonegawa, S., Knopfel, T., Erzurumlu, R. S., and Itohara, S. (2000) Cortex-restricted disruption of NMDAR1 impairs neuronal patterns in the barrel cortex. Nature 406, 726-731 (Pubitemid 30671225)
19. Leheste, J. R., Melsen, F., Wellner, M., Jansen, P., Schlichting, U., Renner-Muller, I., Andreassen, T. T., Wolf, E., Bachmann, S., Nykjaer, A., and Willnow, T. E. (2003) Hypocalcemia and osteopathy in mice with kidney-specific megalin gene defect. FASEB J. 17, 247-249
20. Schwenk, F., Baron, U., and Rajewsky, K. (1995) A Cre-transgenic mouse strain for the ubiquitous deletion of loxP-flanked gene segments including deletion in germ cells. Nucl. Acids Res. 23, 5080-5081 (Pubitemid 26012492)
21. Günther, W., Luchow, A., Cluzeaud, F., Vandewalle, A., and Jentsch, T. J. (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. U. S. A. 95, 8075-8080 (Pubitemid 28326068)
22. Maritzen, T., Keating, D. J., Neagoe, I., Zdebik, A. A., and Jentsch, T. J. (2008) Role of the vesicular chloride transporter ClC-3 in neuroendocrine tissue. J. Neurosci. 28, 10587-10598
23. Kobayashi, T., Stang, E., Fang, K. S., de Moerloose, P., Parton, R. G., and Gruenberg, J. (1998) A lipid associated with the antiphospholipid syndrome regulates endosome structure and function. Nature 392, 193-197 (Pubitemid 28162794)
24. Rubinsztein, D. C., Cuervo, A. M., Ravikumar, B., Sarkar, S., Korolchuk, V., Kaushik, S., and Klionsky, D. J. (2009) In search of an " autophagomometer." Autophagy 5, 585-589
25. Estévez, R., Boettger, T., Stein, V., Birkenhäger, R., Otto, E., Hildebrandt, F., and Jentsch, T. J. (2001) Barttin is a Cl- channel beta-subunit crucial for renal Cl- reabsorption and inner ear K+ secretion. Nature 414, 558-561
26. Suzuki, T., Rai, T., Hayama, A., Sohara, E., Suda, S., Itoh, T., Sasaki, S., and Uchida, S. (2006) Intracellular localization of ClC chloride channels and their ability to form hetero-oligomers. J. Cell. Physiol. 206, 792-798 (Pubitemid 43191054)
27. Kreutzberg, G. W. (1996) Microglia: a sensor for pathological events in the CNS. Trends Neurosci. 19, 312-318
28. Pekny, M., and Nilsson, M. (2005) Astrocyte activation and reactive gliosis. Glia 50, 427-434
29. Cooper, J. D., Russell, C., and Mitchison, H. M. (2006) Progress towards understanding disease mechanisms in small vertebrate models of neuronal ceroid lipofuscinosis. Biochim. Biophys. Acta. 1762, 873-889 (Pubitemid 44740126)
30. Christensen, E. I., and Birn, H. (2002) Megalin and cubilin: multifunctional endocytic receptors. Nat. Rev. Mol. Cell. Biol. 3, 256-266 (Pubitemid 34619261)
31. Gieselmann, V. (1995) Lysosomal storage diseases. Biochim. Biophys. Acta. 1270, 103-136
32. Hara-Chikuma, M., Yang, B., Sonawane, N. D., Sasaki, S., Uchida, S., and Verkman, A. S. (2005) ClC-3 chloride channels facilitate endosomal acidification and chloride accumulation. J. Biol. Chem. 280, 1241-1247
33. Cigič, B., and Pain, R. H. (1999) Location of the binding site for chloride ion activation of cathepsin C. Eur. J. Biochem. 264, 944-951 (Pubitemid 29437226)
34. Faundez, V., and Hartzell, H. C. (2004) Intracellular chloride channels: determinants of function in the endosomal pathway. Sci. STKE 2004, re8
35. De Angeli, A., Monachello, D., Ephritikhine, G., Frachisse, J. M., Thomine, S., Gambale, F., and Barbier-Brygoo, H. (2006) The nitrate/proton antiporter AtCLCa mediates nitrate accumulation in plant vacuoles. Nature 442, 939-942 (Pubitemid 44285951)
36. Günther, W., Piwon, N., and Jentsch, T. J. (2003) The ClC-5 chloride channel knock-out mouse - an animal model for Dent's disease. Pflügers Arch. 445, 456-462 (Pubitemid 36222992)
37. Nielsen, R., Courtoy, P. J., Jacobsen, C., Dom, G., Lima, W. R., Jadot, M., Willnow, T. E., Devuyst, O., and Christensen, E. I. (2007) Endocytosis provides a major alternative pathway for lysosomal biogenesis in kidney proximal tubular cells. Proc. Natl. Acad. Sci. U. S. A. 104, 5407-5412 (Pubitemid 47175693)
38. Aniento, F., Gu, F., Parton, R. G., and Gruenberg, J. (1996) An endosomal beta COP is involved in the pH-dependent formation of transport vesicles destined for late endosomes. J. Cell Biol. 133, 29-41 (Pubitemid 126618595)
39. Zeuzem, S., Feick, P., Zimmermann, P., Haase, W., Kahn, R. A., and Schulz, I. (1992) Intravesicular acidification correlates with binding of ADP-ribosylation factor to microsomal membranes. Proc. Natl. Acad. Sci. U. S. A. 89, 6619-6623
40. Maranda, B., Brown, D., Bourgoin, S., Casanova, J. E., Vinay, P., Ausiello, D. A., and Marshansky, V. (2001) 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 (Pubitemid 37411433)
41. Clague, M. J., Urbe, S., Aniento, F., and Gruenberg, J. (1994) Vacuolar ATPase activity is required for endosomal carrier vesicle formation. J. Biol. Chem. 269, 21-24 (Pubitemid 24026612)
42. Van Weert, A. W., Dunn, K. W., Gueze, H. J., Maxfield, F. R., and Stoorvogel, W. (1995) Transport from late endosomes to lysosomes, but not sorting of integral membrane proteins in endosomes, depends on the vacuolar proton pump. J. Cell Biol. 130, 821-834
43. Saito, M., Hanson, P. I., and Schlesinger, P. (2007) Luminal chloride-dependent activation of endosome calcium channels: patch clamp study of enlarged endosomes. J. Biol. Chem. 282, 27327-27333 (Pubitemid 47501953)
44. Luzio, J. P., Bright, N. A., and Pryor, P. R. (2007) The role of calcium and other ions in sorting and delivery in the late endocytic pathway. Biochem. Soc. Trans. 35, 1088-1091
45. Poët, M., Kornak, U., Schweizer, M., Zdebik, A. A., Scheel, O., Hoelter, S., Wurst, W., Schmitt, A., Fuhrmann, J. C., Planells-Cases, R., Mole, S. E., Hübner, C. A., and Jentsch, T. J. (2006) Lysosomal storage disease upon disruption of the neuronal chloride transport protein ClC-6. Proc. Natl. Acad. Sci. U. S. A. 103, 13854-13859