Syntaxin 8 impairs trafficking of cystic fibrosis transmembrane conductance regulator (CFTR) and inhibits its channel activity

Journal of Cell Science

Volumn 117, Issue 10, 2004, Pages 1923-1935

  Bilan, Frédéric ^a   Thoreau, Vincent ^a   Nacfer, Magali ^a   Dérand, Renaud ^b   Norez, Caroline ^b   Cantereau, Anne ^b   Garcia, Martine ^b   Becq, Frédéric ^b   Kitzis, Alain ^a  

^a POITIERS UNIVERSITY HOSPITAL   (France)

^b UNIVERSITÉ DE POITIERS   (France)

Author keywords

CFTR; Recycling endosome; SNARE; Syntaxin 8; Trafficking

Indexed keywords

CHLORIDE; CHLORIDE CHANNEL; CYCLIC AMP; GREEN FLUORESCENT PROTEIN; IODIDE; MEMBRANE PROTEIN; MONOCLONAL ANTIBODY; RAB PROTEIN; SNARE PROTEIN; SYNTAXIN; TRANSMEMBRANE CONDUCTANCE REGULATOR;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL STRAIN COS7; CELL STRAIN HT29; CELL SURFACE; CELL VACUOLE; CHANNEL GATING; CHLORIDE CURRENT; CHO CELL; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYSTIC FIBROSIS; ELECTROLYTE TRANSPORT; ENDOSOME; EPITHELIUM CELL; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; IN VITRO STUDY; INHIBITION KINETICS; MEMBRANE FUSION; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN INTERACTION; PROTEIN TRANSPORT; REGULATORY MECHANISM;

ANIMALS; ANTIGENS, CD; ANTIGENS, SURFACE; CELL LINE; CHO CELLS; COS CELLS; CRICETINAE; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; DNA, COMPLEMENTARY; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENDOSOMES; GLUTATHIONE TRANSFERASE; HUMANS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; IODIDES; LYSOSOME-ASSOCIATED MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; NERVE TISSUE PROTEINS; PATCH-CLAMP TECHNIQUES; PROTEIN BINDING; PROTEIN TRANSPORT; QA-SNARE PROTEINS; RAB GTP-BINDING PROTEINS; RECEPTORS, TRANSFERRIN; SIGNAL TRANSDUCTION; SYNTAXIN 1; TIME FACTORS; TRANSFECTION;

ANIMALIA; CRICETINAE; CRICETULUS GRISEUS;

EID: 2942601325     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.01070     Document Type: Article

References (50)

1. Antonin, W., Holroyd, C., Fasshauer, D., Pabst, S., von Mollard, G. F. and Jahn, R. (2000). A SNARE complex mediating fusion of late endosomes defines conserved properties of SNARE structure and function. EMBO J. 19, 6453-6464.
2. Antonin, W., Fasshauer, D., Becker, S., Jahn, R. and Schneider, T. R. (2002). Crystal structure of the endosomal SNARE complex reveals common structural principles of all SNAREs. Nat. Struct. Biol. 9, 107-111.
3. Bezprozvanny, I., Scheller, R. H. and Tsien, R. W. (1995). Functional impact of syntaxin on gating of N-type and Q-type calcium channels. Nature 378, 623-626.
4. Chen, Y. A. and Scheller, R. H. (2001). SNARE-mediated membrane fusion. Nat. Rev. Mol. Cell. Biol. 2, 98-106.
5. Cheng, J., Moyer, B. D., Milewski, M., Loffing, J., Ikeda, M., Mickle, J. E., Cutting, G. G., Li, M., Stanton, B. A. and Guggino, W. B. (2002). A Golgi associated PDZ domain protein modulates cystic fibrosis transmembrane conductance regulator plasma membrane expression. J. Biol. Chem. 277, 3520-3529.
6. Cormet-Boyaka, E., Di, A., Chang, S. Y., Naren, A. P., Tousson, A., Nelson, D. J. and Kirk, K. L. (2002). CFTR chloride channels are regulated by a SNAP-23/syntaxin 1 A complex. Proc. Natl. Acad. Sci. USA 99, 12477-12482.
7. Dascher, C. and Balch, W. E. (1996). Mammalian Sly1 regulates syntaxin 5 function in endoplasmic reticulum to Golgi transport. J. Biol. Chem. 271, 15866-15869.
8. Delgrossi, M. H., Breuza, L., Mirre, C., Chavrier, P. and le Bivic, A. (1997). Human syntaxin 3 is localized apically in human intestinal cells. J. Cell Sci. 110, 2207-2214.
9. Dérand, R., Bulteau-Pignoux, L., Mettey, Y., Zegarra-Moran, O., Howell, L. D., Randak, C., Galietta, L. J., Cohn, J. A., Norez, C., Romio, L. et al. (2001). Activation of G551D CFTR channel with MPB-91: regulation by ATPase activity and phosphorylation. Am. J. Physiol. Cell Physiol. 281, 1657-1666.
10. Dormer, R. L., Dérand, R., McNeilly, C. M., Mettey, Y., Bulteau-Pignoux, L., Metaye, T., Vierfond, J. M., Gray, M. A., Galietta, L. J., Morris, M. R. et al. (2001). Correction of delF508-CFTR activity with benzo(c)quinolizinium compounds through facilitation of its processing in cystic fibrosis airway cells. J. Cell Sci. 114, 4073-4081.
11. Gabriel, S. E., Clarke, L. L., Boucher, R. C. and Stutts, M. J. (1993). CFTR and outward rectifying chloride channels are distinct proteins with a regulatory relationship. Nature 363, 263-266.
12. Gruenberg, J. (2001). The endocytic pathway: a mosaic of domains. Nat. Rev. Mol. Cell. Biol. 2, 721-730.
13. Jarvis, S. E., Magga, J. M., Beedle, A. M., Braun, J. E. A. and Zamponi, G. W. (2000). G protein modulation of N-type calcium channels is facilitated by physical interactions between syntaxin 1A and Gβγ. J. Biol. Chem. 275, 6388-6394.
14. Ji, H. L., Chalfant, M. L., Jovov, B., Lockhart, J. P., Parker, S. B., Fuller, C. M., Stanton, B. A. and Benos, D. J. (2000). The cytosolic termini of the β- an γ-ENaC subunits are involved in the functional interactions between cystic fibrosis transmembrane conductance regulator and epithelial sodium channel. J. Biol. Chem. 275, 27947-27956.
15. Kasai, K. and Akagawa, K. (2001). Roles of the cytoplasmic and transmembrane domains of syntaxins in intracellular localization and trafficking. J. Cell Sci. 114, 31115-31124.
16. Laëmmli, U. K. and Favre, M. (1973). Maturation of the head of bacteriophage T4. I. DNA packaging events. J. Mol. Biol. 80, 575-599.
17. 2+ exchanger. J. Biol. Chem. 269, 17434-17439.
18. Low, S. H., Chapin, S. J., Wimmer, C., Whiteheart, S. W., Komuves, L. G., Mostov, K. E. and Weimbs, T. (1998). The SNARE machinery is involved in apical plasma membrane trafficking in MDCK cells. J Cell Biol. 141, 1503-1513.
19. Moyer, B. D., Loffing, J., Schwiebert, E. M., Loffing-Cueni, D., Halpin, P. A., Karlson, K. H., Ismailov, I. I., Guggino, W. B., Langford, G. M. and Stanton, B. A. (1998). Membrane trafficking of the cystic fibrosis gene product, cystic fibrosis transmembrane conductance regulator, tagged with green fluorescent protein in madin-darby canine kidney cells. J. Biol. Chem. 273, 21759-21768.
20. Mullock, B. M., Smith, C. W., Ihrke, G., Bright, N. A., Lindsay, M., Parkinson, E. J., Brooks, D. A., Parton, R. G., James, D. E., Luzio, J. P. et al. (2000). Syntaxin 7 is localized to late endosome compartments, associates with Vamp8, and is required for late endosome-lysosome fusion. Mol. Biol. Cell 11, 3137-3153.
21. Naren, A. P., Nelson, D. J., Xie, W., Jovov, B., Pevsner, J., Bennett, M. K., Benos, D. J., Quick, M. W. and Kirk, K. L. (1997). Regulation of CFTR chloride channels by syntaxin and Munc 18 isoforms. Nature 390, 302-305.
22. Naren, A. P., Quick, M. W., Collawn, J. F., Nelson, D. J. and Kirk, K. L. (1998). Syntaxin 1A inhibits CFTR chloride channels by means of domain-specific protein-protein interactions. Proc. Natl. Acad. Sci. USA 95, 10972-10977.
23. Naren, A. P., Di, A., Cormet-Boyaka, E., Boyaka, P. N., McGhee, J. R., Zhou, W., Akagawa, K., Fujiwara, T., Thorne, U., Engelhardt, J. F. et al. (2000). Syntaxin 1A is expressed in airway epithelial cells, where it modulates CFTR Cl- currents. J Clin. Invest. 105, 377-386.
24. - channel by its R domain. J Biol. Chem. 276, 7689-7692.
25. Peters, K. W., Qi, J., Watkins, S. C. and Frizzell, R. A. (1999). Syntaxin 1A inhibits regulated CFTR trafficking in Xenopus oocytes. Am. J. Physiol. 277, 174-180.
26. Poschet, J. F., Skidmore, J., Boucher, J. C., Firoved, A. M., van Dyke, R. W. and Deretic, V. (2002). Hyperacidification of cellulobrevin endocytic compartments and defective endosomal recycling in cystic fibrosis respiratory epithelial cells. J Biol. Chem. 277, 13959-13965.
27. Prekeris, R., Klumperman, J., Chen, Y. A. and Scheller, R. H. (1998). Syntaxin 13 mediates cycling of plasma membrane proteins via tubulovesicular recycling endosomes. J. Cell Biol. 143, 957-971.
28. Prekeris, R., Yang, B., Oorschot, V., Klumperman, J. and Scheller, R. H. (1999). Differential roles of syntaxin 7 and syntaxin 8 in endosomal trafficking. Mol. Biol. Cell 10, 3891-3908.
29. Raghuram, V., Mak, D. O. D. and Foskett, J. K. (2001). Regulation of cystic fibrosis transmembrane conductance regulator single-channel gating by bivalent PDZ-domain-mediated interaction. Proc. Natl. Acad. Sci. USA 98, 1300-1305.
30. Riordan, J. R., Rommens, J. M., Kerem, B. S., Alon, N., Rozmahel, R., Grzelczak, Z., Zielenski, J., Lok, S., Plavsic, N., Chou, J. L. et al. (1989). Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science 245, 1066-1073.
31. Rommens, J. M., Iannuzzi, C., Kerem, B. S., Drumm, M. L., Melmer, G., Dean, M., Rozmahel, R., Cole, J. L., Kennedy, D., Hidaka, N. et al. (1989). Identification of the cystic fibrosis gene: chromosome walking and jumping. Science 245, 1059-1065.
32. Saxena, S., Quick, M. W., Tousson, A., Oh, Y. and Warnock, D. G. (1999). Interaction of syntaxins with the amiloride-sensitive epithelial sodium channel. J Biol. Chem. 274, 20812-20817.
33. Sheng, Z. H., Rettig, J., Cook, T. and Catterall, W. A. (1996). Calcium-dependent interaction of N-type calcium channels with the synaptic core complex. Nature 379, 451-454.
34. Short, D. B., Trotter, K. W., Reczek, D., Kreda, S. M., Bretscher, A., Boucher, R. C., Stutts, M. J. and Milgram, S. L. (1998). An apical PDZ protein anchors the cystic fibrosis transmembrane conductance regulator to the cytoskeleton. J. Biol. Chem. 273, 19797-19801.
35. Stutts, M. J., Canessa, C. M., Olsen, J. C., Hamrick, M., Cohn, J. A., Rossier, B. C. and Boucher, R. C. (1995). CFTR as a cAMP-dependent regulator of sodium channels. Science 269, 847-850.
36. Subramaniam, V. N., Loh, E., Horstmann, H., Habermann, A., Xu, Y., Coe, J., Griffiths, G. and Hong, W. (2000). Preferential association of syntaxin 8 with the early endosome. J. Cell Sci. 113, 997-1008.
37. - associated ATP channel: distinct pores regulated by common gates. EMBO J. 17, 898-908.
38. - channel in CHO cells stably expressing the cystic fibrosis gene. Nature 352, 628-631.
39. Tang, B. L., Tan, A. E. H., Lim, L. K., Lee, S. S., Low, D. Y. H. and Hong, W. (1998). Syntaxin 12, a member of the syntaxin family localized to the endosome. J. Biol. Chem. 273, 6944-6950.
40. Thoreau, V., Bergès, T., Callebaut, L, Gencik, Z. G., Gressin, L., Bernheim, A., Karst, F., Mornon, J. P., Kitzis, A. and Chomel, J. C. (1999). Molecular cloning, expression analysis, and chromosomal localization of human syntaxin 8 (STX8). Biochem. Biophys. Res. Commun. 257, 577-583.
41. Ullrich, O., Reinsch, S., Urbe, S., Zerial, M. and Parton, R. (1996). Rab11 regulates recycling through the pericentriolar recycling endosome. J. Cell Biol. 135, 913-924.
42. Urbe, S., Huber, L. A., Zerial, M., Tooze, S. A. and Parton, R. G. (1993). Rab11, a small GTPase associated with both constitutive and regulated secretory pathways in PC12 cells. FEBS Lett. 334, 175-182.
43. Valdez, A. C., Cabaniols, J. P., Brown, M. J. and Roche, P. A. (1999). Syntaxin 11 is associated with SNAP-23 on late endosomes and the trans-Golgi network. J. Cell Sci. 112, 845-854.
44. Venglarik, C. J., Bridges, R. J. and Frizzell, R. A. (1990). A simple assay for agonist-regulated Cl And K conductances in salt-secreting epithelial cells. Am. J. Physiol. 259, 358-364.
45. Wang, S., Raab, R. W., Schatz, P. J., Guggino, W. B. and Li, M. (1998). Peptide binding consensus of the NHE-RF-PDZ1 domain matches the C-terminal sequence of the cystic fibrosis transmembrane conductance regulator (CFTR). FEBS Lett. 427, 103-108.
46. Wang, S., Yue, H., Derin, R. B., Guggino, W. B. and Li, M. (2000). Accessory protein facilitated CFTR-CFTR interaction, a molecular mechanism to potentiate the chloride channel activity. Cell 103, 169-179.
47. Weimbs, T., Low, S. H., Chapin, S. J., Mostov, K. E., Bucher, P. and Hofmann, K. (1997). A conserved domain is present in different families of vesicular fusion proteins: a new superfamily. Proc. Natl. Acad. Sci. USA 94, 3046-3051.
48. Weixel, K. M. and Bradbury, N. A. (2000). The carboxyl terminus of the cystic fibrosis transmembrane conductance regulator binds to AP-2 clathrin adaptators. J. Biol. Chem. 275, 3655-3660.
49. Wilcke, M., Johannes, L., Galli, T., Mayau, V., Goud, B. and Salamero, J. (2000). Rab11 regulates the compartmentalization of early endosomes required for efficient transport from early endosomes to the trans-Golgi network. J. Cell Biol. 151, 1207-1220.
50. Wong, S. H., Xu, Y., Zhang, T. and Hong, W. (1998). Syntaxin 7, a novel syntaxin member associated with the early endosomal compartments. J. Biol. Chem. 273, 375-380.