Deletion of phenylalanine 508 causes attenuated phosphorylation-dependent activation of CFTR chloride channels

Journal of Physiology

Volumn 524, Issue 3, 2000, Pages 637-648

  Wang, Fei ^a   Zeltwanger, Shawn ^a   Hu, Shenghui ^a   Hwang, Tzyh Chang ^a,b  

^a University of Missouri   (United States)

^b UNIVERSITY OF MISSOURI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHLORIDE CHANNEL; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; FORSKOLIN; GENISTEIN; PHENYLALANINE; TRANSMEMBRANE CONDUCTANCE REGULATOR; ADENOSINE TRIPHOSPHATE; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR;

ARTICLE; CELL STRAIN 3T3; CHANNEL GATING; CYSTIC FIBROSIS; GENE DELETION; GENE MUTATION; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; ANIMAL CELL; ANIMAL TISSUE; CELL DENSITY; CELL MEMBRANE; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME ACTIVATION; FIBROBLAST; MOUSE; NONHUMAN; PROTEIN DEFECT; PROTEIN EXPRESSION; SINGLE CHANNEL PATCH CLAMP; WHOLE CELL PATCH CLAMP;

EID: 0034192547     PISSN: 00223751     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1469-7793.2000.00637.x     Document Type: Article

References (36)

1. AL-NAKKASH, L. & HWANG, T.-C. (1999). Activation of wild-type and ΔF508-CFTR by phosphodiesterase inhibitors through cAMP-dependent and -independent mechanisms. Pflügers Archiv 437, 553-561.
2. ARMSTRONG, S., TABERNERO, R. L., ZHANG, H., HERMODSON, M. & STAUFFACHER, C. V. (1998). Powering the ABC transporter: The 2.5 A crystallographic structure of the ABC domain of RBSA. Pediatric Pulmonology Supplement 17, 91-92.
3. BERGER, H. A., ANDERSON, M. P., GREGORY, R. J., THOMPSON, S., HOWARD, P. W., MAURER, R. A., SMITH, A. K. & WELSH, M. J. (1991). Identification and regulation of the cystic fibrosis transmembrane conductance regulator-generated chloride channel. Journal of Clinical Investigation 88, 1422-1431.
4. CHANG, X.-B., HOU, Y.-X., JENSEN, T. J. & RIORDAN, J. R. (1994). Mapping of cystic fibrosis transmembrane conductance regulator membrane topology by glycosylation site insertion. Journal of Biological Chemistry 269, 18572-18575.
5. CHENG, S. H., GREGORY, R. J., MARSHALL, J., PAUL, S., SOUZA, D. W., WHITE, G. A., O'RIORDAN, C. R. & SMITH, A. L. (1990). Defective intrucellular transport and processing of CFTR is the molecular basis of most cystic fibrosis. Cell 65, 827-834.
6. CHENG, S. H., RICH, D. P., MARSHALL, J., GREGORY, R. J., WELSH, M. J. & SMITH, A. E. (1991). Phosphorylation of the R domain by cAMP-dependent protein kinase regulates the CFTR chloride channel. Cell 66, 1027-1036.
7. DALEMANS, W., BARBRY, P., CHAMPIGNY, G., JALLAT, S., DOTT, K., DREYER, D., CRYSTAL, R. G., PAVIRANI, A., LECOCQ, J.-P. & LAZDUNSKI, M. (1991). Altered chloride ion channel kinetics associated with the ΔF508 cystic fibrosis mutation. Nature 354, 526-528.
8. DENNING, G. M., ANDERSON, M. P., AMARA, J. F., MARSHALL, J., SMITH, A. E. & WELSH, M. J. (1992). Processing of mutant cystic fibrosis transmembrane conductance regulator is temperature-sensitive. Nature 358, 761-764.
9. DRUMM, M. L., WILKINSON, D. J., SMIT, L. S., WORRELL, R. T., STRONG, T. V., FRIZZELL, R. A., DAWSON, D. C. & COLLINS, F. S. (1991). Chloride conductance expressed by ΔF508 and other mutant CFTRs in Xenopus oocytes. Science 254, 1797-1799.
10. FLOCKHART, D. A. & CORBIN, J. D. (1984). Preparation of the catalytic subunit of cAMP-dcpendent protein kinase. In Brain Receptor Methodologies: Amino Acids, Psychoactive Drugs. Part A: General Methods and Concepts. Amines and Acetylcholine, ed. MARANGOS, P. J., CAMPBELL, I. C. & COHEN, R. M., pp. 209-215. Academic Press, Orlando, FL, USA.
11. GADSBY, D. C., NAGEL, G. & HWANG, T.-C. (1995). The CFTR chloride channel of mammalian heart. Annual Review of Physiology 57, 387-416.
12. GADSBY, D. C. & NAIRN, A. C. (1999). Control of CFTR gating by phosphorylation and nucleotide hydrolysis. Physiological Reviews 79, S77-107.
13. HAWS, C. M., NEPOMUCENO, I. B., KROUSE, M. E., WAKELEE, H., LAW, T, NIA, Y., NGUYEN, H. & WINE, J. J. (1996). ΔF508-CFTR channels: kinetics, activation by forskolin, and potentiation by xanthines. American Journal of Physiology 270, C1544-1555.
14. HE, Z., RAMAN, S., GUO, Y. & REENSTRA, W. W. (1998). Cystic fbrosis transmembrane conductance regulator activation by cAMP-independent mechanisms. American Journal of Physiology 275, C958-966.
15. HUNG, L.-W., WANG, I. X., NIKAIDO, K., LIU, P.-Q., AMES, G. F. & KIM, S.-H. (1998). Crystal structure of the ATP-binding subunit of an ABC transporter. Nature 396, 703-707.
16. HWANG, T.-C., HORIE, M. & GADSBY, D. C. (1993). Functionally distinct phospho-forms underlie incremental activation of protein kinase-regulated Cl conductance in mammalian heart. Journal of General Physiology 101, 629-650.
17. HWANg, T.-C., NAGEL, G., NAIRN, A. C. & GADSBY, D. C. (1994). Regulation of the gating of cystic fibrosis transmembrane conductance regulator Cl channels by phosphorylation and ATP hydrolysis. Proceedings of the National Academy of Sciences of the USA 91, 4698-4702.
18. HWANG, T.-C., WANG, F., YANG, I. C.-H. & REENSTRA, W. W. (1997). Genistein potentiates wild-type and ΔF508-CFTR channel activity. American Journal of Physiology 273, C988-998.
19. KÄLIN, N., CLAAß, A., SOMMER, M., PUCHELLE, E. & TÜMMLER, B. (1999). ΔF508 CFTK protein expression in tissues from patients with cystic fibrosis. Journal of Clinical Investigation 103, 1379-1389.
20. KELLEY, T. J., AL-NAKKASH, L., COTTON, C. U. & DRUMM, M. L. (1996). Activation of endogenous ΔF508 cystic fibrosis transmembrane conductance regulator by phosphodiesterase inhibition. Journal of Clinical Investigation 98, 513-520.
21. LI, C., RAMJEESINGH, M., REYES, E., JENSEN. T., CHANG, X., ROMMENS, J. M. & BEAR, C. E. (1993). The cystic fibrosis mutation (ΔF508) does not influence the chloride channel activity of CFTR. Nature Genetics 3, 311-316.
22. LUKACS, G. L., MOHAMED, A., KARTNER, N., CHANG, X.-B., RIORDAN, J. R. & GRINSTEIN, S. (1994). Conformational maturation of CFTR but not its mutant counterpart (delta F508) occurs in the endoplasmic reticulum and requires ATP. EMBO Journal 13, 6076-6086.
23. MATHEWS, C. J., TABCHARANI, J. A., CHANG, X.-B., JENSEN, T. J., RIORDAN, J. R. & HANRAHAN, J. W. (1998). Dibasic protein kinase A sites regulate bursting rate and nucleotide sensitivity of the cystic fibrosis transmembrane conductance regulator chloride channel. Journal of Physiology 508, 365-377.
24. RICH, D. P., BERGER, H. A., CHENG, S. H., TRAVIS, S. M., SAXENA, M., SMITH, A. E. & WELSH, M. J. (1993). Regulation of the cystic fibrosis transmembrane conductance regulator Cl channel by negative charge in the R domain. Journal of Biological Chemistry 268, 20259-20267.
25. RIORDAN, J. R., ROMMENS, J. M., KEREM, B.-S., ALON, N., ROZMAHEL, R., GRZELCZAK, Z., ZIELENSKI, J., LOK, S., PLAVSIC, N., CHOU, J.-L., DRUMM, M. L., IANNUZZI, M. C., COLLINS, F. S. & TSUI, L.-C. (1989). Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science 245, 1066-1073.
26. SATO, S., WARD, C. L., KROUSE, M. E., WINE, J. J. & KOPITO, R. R. (1996). Glycerol reverses the misfolding phenotype of the most common cystic fibrosis mutation. Journal of Biological Chemistry 271, 635-638.
27. SCHULTZ, B. D., FRIZZELL, R. A. & BRIDGES, R. J. (1999). Rescue of dysfunctional ΔF508-CFTR chloride channel activity by IBMX. Journal of Membrane Biology 170, 51-66.
28. SEIBERT, F. S., JIA, Y., MATHEWS, C. J., HANRAHAN, J. W., RIORDAN, J. R., LOO, R. W. & CLARKE, D. M. (1997). Disease-associated mutations in cytoplasmic loops 1 and 2 of cystic fibrosis transmembrane conductance regulator impede processing or opening of the channel. Biochemistry 36, 11966-11974.
29. SHEPPARD, D. N. & WELSH, M. J. (1999). Structure and function of the CFTR chloride channel. Physiological Reviews 79, S23-43.
30. WANG, F., ZELTWANGER, S., YANG, I. C.-H., NAIRN, A. C. & HWANG, T.-C. (1998). Actions of genistein on cystic fibrosis transmembrane conductance regulator channel gating: evidence for two binding sites with opposite effects. Journal of General Physiology 111, 477-490.
31. WARD, C. L., OMURA, S. & KOPITO, R. R. (1995). Degradation of CFTR by the ubiquitin-proteasome pathway. Cell 83, 121-127.
32. WEINREICH, F., RIORDAN, J. R. & NAGEL, G. (1999). Dual effects of ADP and adenylylimidodiphosphate on CFTR channel kinetics show binding to two different nucleotide binding sites. Journal of General Physiology 114, 55-70.
33. WILKINSON, D. J., STRONG, T. V., MANSOURA, M. K., WOOD, D. L., SMITH, S. S., COLLINS, F. S. & DAWSON, D. C. (1997). CFTR activation: additive effects of stimulatory and inhibitory phosphorylation sites in the R domain. American Journal of Physiology 273, L127-133.
34. WINTER, M. C. & WELSH, M. J. (1997). Stimulation of CFTR activity by its phosphorylated R domain. Nature 389, 294-296.
35. YAMAMOTO, T., YAMAMOTO, S., OSBORNE, J. C., MANGANIELLO, V. C., VAUGHAN, M. & HIKAIDA, H. (1983). Complex effects of inhibitors on cyclic GMP-stimulated cyclic nucleotide phosphodiesterase. Journal of Biological Chemistry 258, 14173-14177.
36. ZELTWANGER, S., WANG, F, WANG, G. T., GILLIS, K. & HWANG, T.-C. (1999). Gating of CFTR chloride channels by ATP hydrolysis: quantitative analysis of a cyclic gating scheme. Journal of General Physiology 113, 541-554.