Defective adenosine-stimulated cAMP production in cystic fibrosis airway epithelia: A novel role for CFTR in cell signaling

FASEB Journal

Volumn 25, Issue 9, 2011, Pages 2996-3003

  Watson, Michael J ^a   Worthington, Erin N ^a   Clunes, Lucy A ^a   Rasmussen, Julia E ^a   Jones, Lisa ^a   Tarran, Robert ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

2nd messenger; Chloride; G protein coupled receptor; Ion channel

Indexed keywords

ADENOSINE; ADENOSINE A2B RECEPTOR; ADENYLATE CYCLASE; BETA 2 ADRENERGIC RECEPTOR; CHLORIDE ION; CYCLIC AMP; CYTOKINE; FORSKOLIN; INTERLEUKIN 8; ISOPRENALINE; NEUROMODULIN; TRANSMEMBRANE CONDUCTANCE REGULATOR;

ANIMAL CELL; APICAL MEMBRANE; ARTICLE; BRONCHUS MUCOSA; CELL MEMBRANE; CELL SPECIFICITY; CILIARY MOTILITY; CONTROLLED STUDY; CYSTIC FIBROSIS; CYTOKINE RELEASE; EPITHELIUM CELL; FLUORESCENCE RESONANCE ENERGY TRANSFER; HAMSTER; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOPRECIPITATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION;

ADENOSINE; ANIMALS; CELL COMMUNICATION; CELLS, CULTURED; CILIA; CYCLIC AMP; CYSTIC FIBROSIS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMANS; INTERLEUKIN-8; RECEPTOR, ADENOSINE A2B; RESPIRATORY MUCOSA; SIGNAL TRANSDUCTION;

EID: 80052666226     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-186080     Document Type: Article

References (44)

1. Com, G., and Clancy, J. P. (2009) Adenosine receptors, cystic fibrosis, and airway hydration. Handb. Exp. Pharmacol. 363-381
2. Rollins, B. M., Burn, M., Coakley, R. D., Chambers, L. A., Hirsh, A. J., Clunes, M. T., Lethem, M. I., Donaldson, S. H., and Tarran, R. (2008) A2B adenosine receptors regulate the mucus clearance component of the lung's innate defense system. Am. J. Respir. Cell Mol. Biol. 39, 190-197
3. Tarran, R., Button, B., and Boucher, R. C. (2006) Regulation of normal and cystic fibrosis airway surface liquid volume by phasic shear stress. Annu. Rev. Physiol. 68, 543-561
4. Bucheimer, R. E., and Linden, J. (2004) Purinergic regulation of epithelial transport. J. Physiol. 555, 311-321 (Pubitemid 38379992)
5. Burnstock, G. (2006) Pathophysiology and therapeutic potential of purinergic signaling. Pharmacol. Rev. 58, 58-86
6. Brunton, L. L. (2003) PDE4: arrested at the border. Sci. STKE. 2003, PE44
7. Fredholm, B. B., Arslan, G., Halldner, L., Kull, B., Schulte, G., and Wasserman, W. (2000) Structure and function of adenosine receptors and their genes. Naunyn Schmiedebergs Arch. Pharmacol. 362, 364-374
8. McConnachie, G., Langeberg, L. K., and Scott, J. D. (2006) AKAP signaling complexes: getting to the heart of the matter. Trends Mol. Med. 12, 317-323 (Pubitemid 44110003)
9. Cooper, D. M., and Crossthwaite, A. J. (2006) Higher-order organization and regulation of adenylyl cyclases. Trends Pharmacol. Sci. 27, 426-431 (Pubitemid 44069584)
10. Li, C., Krishnamurthy, P. C., Penmatsa, H., Marrs, K. L., Wang, X. Q., Zaccolo, M., Jalink, K., Li, M., Nelson, D. J., Schuetz, J. D., and Naren, A. P. (2007) Spatiotemporal coupling of cAMP transporter to CFTR chloride channel function in the gut epithelia. Cell 131, 940-951 (Pubitemid 350138082)
11. Anderson, M. P., Sheppard, D. N., Berger, H. A., and Welsh, M. J. (1992) Chloride channels in the apical membrane of normal and cystic fibrosis airway and intestinal epithelia. Am. J. Physiol. 263, L1-L14
12. Antonioli, L., Fornai, M., Colucci, R., Ghisu, N., Tuccori, M., Del Tacca, M., and Blandizzi, C. (2008) Regulation of enteric functions by adenosine: pathophysiological and pharmacological implications. Pharmacol. Ther. 120, 233-253
13. Harris, A., and Argent, B. E. (1993) The cystic fibrosis gene and its product CFTR. Semin. Cell Biol. 4, 37-44
14. Skach, W. R. (2000) Defects in processing and trafficking of the cystic fibrosis transmembrane conductance regulator. Kidney Int. 57, 825-831
15. Dalemans, W., Barbry, P., Champigny, G., Jallat, S., Dott, K., Dreyer, D., Crystal, R. G., Pavirani, A., Lecocq, J. P., and Lazdunski, M. (1991) Altered chloride ion channel kinetics associated with the delta F508 cystic fibrosis mutation. Nature 354, 526-528 (Pubitemid 21896832)
16. Cholon, D. M., O'Neal, W. K., Randell, S. H., Riordan, J. R., and Gentzsch, M. Modulation of endocytic trafficking and apical stability of CFTR in primary human airway epithelial cultures. Am. J. Physiol. Lung Cell. Mol. Physiol. 298, L304-L314
17. Chmiel, J. F., and Davis, P. B. (2003) State of the art: why do the lungs of patients with cystic fibrosis become infected and why can't they clear the infection? Respir. Res. 4, 8
18. Campodonico, V. L., Gadjeva, M., Paradis-Bleau, C., Uluer, A., and Pier, G. B. (2008) Airway epithelial control of Pseudomonas aeruginosa infection in cystic fibrosis. Trends Mol. Med. 14, 120-133
19. Nichols, D., Chmiel, J., and Berger, M. (2008) Chronic inflammation in the cystic fibrosis lung: alterations in inter- and intracellular signaling. Clin. Rev. Allergy Immunol. 34, 146-162
20. Quinton, P. M. (2008) Cystic fibrosis: impaired bicarbonate secretion and mucoviscidosis. Lancet 372, 415-417
21. Naren, A. P., Cobb, B., Li, C., Roy, K., Nelson, D., Heda, G. D., Liao, J., Kirk, K. L., Sorscher, E. J., Hanrahan, J., and Clancy, J. P. (2003) A macromolecular complex of beta 2 adrenergic receptor, CFTR, and ezrin/radixin/moesin-binding phosphoprotein 50 is regulated by PKA. Proc. Natl. Acad. Sci. U. S. A. 100, 342-346 (Pubitemid 36078076)
22. + conductance by the cystic fibrosis transmembrane conductance regulator. Pflügers Arch. 440, 193-201
23. Berdiev, B. K., Cormet-Boyaka, E., Tousson, A., Qadri, Y. J., Oosterveld-Hut, H. M., Hong, J. S., Gonzales, P. A., Fuller, C. M., Sorscher, E. J., Lukacs, G. L., and Benos, D. J. (2007) Molecular proximity of cystic fibrosis transmembrane conductance regulator and epithelial sodium channel assessed by fluorescence resonance energy transfer. J. Biol. Chem. 282, 36481-36488
24. Ho, K. (1998) The ROMK-cystic fibrosis transmembrane conductance regulator connection: new insights into the relationship between ROMK and cystic fibrosis transmembrane conductance regulator channels. Curr. Opin. Nephrol. Hypertens. 7, 49-58
25. Penmatsa, H., Zhang, W., Yarlagadda, S., Li, C., Conoley, V. G., Yue, J., Bahouth, S. W., Buddington, R. K., Zhang, G., Nelson, D. J., Sonecha, M. D., Manganiello, V., Wine, J. J., and Naren, A. P. (2010) Compartmentalized cyclic adenosine 3′,5′-monophosphate at the plasma membrane clusters PDE3A and cystic fibrosis transmembrane conductance regulator into microdomains. Mol. Biol. Cell. 21, 1097-1110
26. Sitaraman, S. V., Wang, L., Wong, M., Bruewer, M., Hobert, M., Yun, C. H., Merlin, D., and Madara, J. L. (2002) The adenosine 2b receptor is recruited to the plasma membrane and associates with E3KARP and Ezrin upon agonist stimulation. J. Biol. Chem. 277, 33188-33195 (Pubitemid 34984837)
27. Sitaraman, S. V., Si-Tahar, M., Merlin, D., Strohmeier, G. R., and Madara, J. L. (2000) Polarity of A2b adenosine receptor expression determines characteristics of receptor desensitization. Am. J. Physiol. Cell Physiol. 278, C1230-C1236 (Pubitemid 30432407)
28. 2+-activated Cl- channel Ano1/TMEM16A. J. Biol. Chem. 286, 1381-1388
29. Liu, Y., Fisher, D. A., and Storm, D. R. (1993) Analysis of the palmitoylation and membrane targeting domain of neuromodulin (GAP-43) by site-specific mutagenesis. Biochemistry 32, 10714-10719 (Pubitemid 23327805)
30. Cui, L., Aleksandrov, L., Chang, X. B., Hou, Y. X., He, L., Hegedus, T., Gentzsch, M., Aleksandrov, A., Balch, W. E., and Riordan, J. R. (2007) Domain interdependence in the biosynthetic assembly of CFTR. J. Mol. Biol. 365, 981-994 (Pubitemid 46014191)
31. Gentzsch, M., Chang, X. B., Cui, L., Wu, Y., Ozols, V. V., Choudhury, A., Pagano, R. E., and Riordan, J. R. (2004) Endocytic trafficking routes of wild type and DeltaF508 cystic fibrosis transmembrane conductance regulator. Mol. Biol. Cell 15, 2684-2696 (Pubitemid 38691858)
32. Gentzsch, M., Choudhury, A., Chang, X. B., Pagano, R. E., and Riordan, J. R. (2007) Misassembled mutant DeltaF508 CFTR in the distal secretory pathway alters cellular lipid trafficking. J. Cell Sci. 120, 447-455 (Pubitemid 46332508)
33. Turnbull, E. L., Rosser, M. F., and Cyr, D. M. (2007) The role of the UPS in cystic fibrosis. BMC Biochem. 8(Suppl. 1), S11
34. Bradbury, N. A., Jilling, T., Berta, G., Sorscher, E. J., Bridges, R. J., and Kirk, K. L. (1992) Regulation of plasma membrane recycling by CFTR. Science 256, 530-532
35. Wang, L., Kolachala, V., Walia, B., Balasubramanian, S., Hall, R. A., Merlin, D., and Sitaraman, S. V. (2004) Agonist-induced polarized trafficking and surface expression of the adenosine 2b receptor in intestinal epithelial cells: role of SNARE proteins. Am. J. Physiol. Gastrointest. Liver Physiol. 287, G1100-G1107 (Pubitemid 39423703)
36. 2. Am. J. Physiol. Lung Cell. Mol. Physiol. 282, L12-L25
37. Vilardaga, J. P., Bunemann, M., Krasel, C., Castro, M., and Lohse, M. J. (2003) Measurement of the millisecond activation switch of G protein-coupled receptors in living cells. Nat. Biotechnol. 21, 807-812 (Pubitemid 36791401)
38. Guggino, W. B. (2004) The cystic fibrosis transmembrane regulator forms macromolecular complexes with PDZ domain scaffold proteins. Proc. Am. Thorac. Soc. 1, 28-32
39. Li, C., and Naren, A. P. (2005) Macromolecular complexes of cystic fibrosis transmembrane conductance regulator and its interacting partners. Pharmacol. Ther. 108, 208-223 (Pubitemid 41527085)
40. Haggie, P. M., Kim, J. K., Lukacs, G. L., and Verkman, A. S. (2006) Tracking of quantum dot-labeled CFTR shows near immobilization by C-terminal PDZ interactions. Mol. Biol. Cell 17, 4937-4945 (Pubitemid 44907340)
41. Haggie, P. M., Stanton, B. A., and Verkman, A. S. (2004) Increased diffusional mobility of CFTR at the plasma membrane after deletion of its C-terminal PDZ binding motif. J. Biol. Chem. 279, 5494-5500 (Pubitemid 38220574)
42. Thelin, W. R., Chen, Y., Gentzsch, M., Kreda, S. M., Sallee, J. L., Scarlett, C. O., Borchers, C. H., Jacobson, K., Stutts, M. J., and Milgram, S. L. (2007) Direct interaction with filamins modulates the stability and plasma membrane expression of CFTR. J. Clin. Invest. 117, 364-374 (Pubitemid 46203965)
43. Sun, Y., Wu, F., Sun, F., and Huang, P. (2008) Adenosine promotes IL-6 release in airway epithelia. J. Immunol. 180, 4173-4181
44. Gray, T., Coakley, R., Hirsh, A., Thornton, D., Kirkham, S., Koo, J. S., Burch, L., Boucher, R., and Nettesheim, P. (2004) Regulation of MUC5AC mucin secretion and airway surface liquid metabolism by IL-1β in human bronchial epithelia. Am. J. Physiol. Lung Cell. Mol. Physiol. 286, L320-L330 (Pubitemid 38129513)