CFTR regulation in human airway epithelial cells requires integrity of the actin cytoskeleton and compartmentalized cAMP and PKA activity

Journal of Cell Science

Volumn 125, Issue 5, 2012, Pages 1106-1117

  Monterisi, Stefania ^a   Favia, Maria ^a   Guerra, Lorenzo ^a   Cardone, Rosa A ^a   Marzulli, Domenico ^b   Reshkin, Stephan J ^a   Casavola, Valeria ^a   Zaccolo, Manuela ^c  

^a UNIVERSITY OF BARI   (Italy)

^b CNR   (Italy)

^c UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

Airways cells; cAMP; Cystic fibrosis; FRET; NHERF1; PKA

Indexed keywords

CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE ANCHORING PROTEIN; TRANSMEMBRANE CONDUCTANCE REGULATOR;

ACTIN FILAMENT; ARTICLE; CELL COMPARTMENTALIZATION; CELL FRACTIONATION; CELL MEMBRANE; CELL SURFACE; CONTROLLED STUDY; CYSTIC FIBROSIS; CYTOSKELETON; CYTOSOL; EPITHELIUM CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION;

ACTIN CYTOSKELETON; CELL LINE; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; CYTOPLASM; CYTOSKELETAL PROTEINS; EPITHELIAL CELLS; HUMANS; PHOSPHOPROTEINS; RESPIRATORY MUCOSA; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SODIUM-HYDROGEN ANTIPORTER;

EID: 84861362217     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.089086     Document Type: Article

References (57)

1. Al-Nkkash, L. and Hwang, T. C. (1999). Activation of wild-type and deltaF508-CFTR by phosphodiesterase inhibitors through cAMP-dependent and -independent mechanisms. Pflugers Arch. 437, 553-561.
2. Allen, M. D. and Zhang, J. (2006). Subcellular dynamics of protein kinase A activity visualized by FRET-based reporters. Biochem. Biophys. Res. Commun. 348, 716-721.
3. Barnes, A. P., Livera, G., Huang, P., Sun, C., O'Neal, W. K., Conti, M., Stutts, M. J. and Milgram, S. L. (2005). Phosphodiesterase 4D forms a cAMP diffusion barrier at the apical membrane of the airway epithelium. J. Biol. Chem. 280, 7997-8003.
4. Bear, C. E., Li, C., Kartner, N., Bridges, R. D., Jensen, T. J., Ramjeesingh, M. and Riordan, J. R. (1992). Purification and functional reconstitution of the cystic fibrosis transmembrane conductance regulator (CFTR). Cell 68, 809-818.
5. Bossard, F., Robay, A., Toumaniantz, G., Dahimene, S., Becq, F., Merot, J. and Gauthier, C. (2007). NHE-RF1 protein rescues DeltaF508-CFTR function. Am. J. Physiol. Lung Cell Mol. Physiol. 292, L1085-L1094.
6. Brown, C. R., Hong-Brown, L. Q., Biwersi, J., Verkman, A. S. and Welch, W. J. (1996). Chemical chaperones correct the mutant phenotype of the delta F508 cystic fibrosis transmembrane conductance regulator protein. Cell Stress Chaperones 1, 117-125.
7. Cantiello, H. F. (2001). Role of actin filament organization in CFTR activation. Pflugers Arch. 443 Suppl. 1, S75-S80.
8. Cardone, R. A., Bagorda, A., Bellizzi, A., Busco, G., Guerra, L., Paradiso, A., Casavola, V., Zaccolo, M. and Reshkin, S. J. (2005). Protein kinase A gating of a pseudopodial-located RhoA/ROCK/p38/NHE1 signal module regulates invasion in breast cancer cell lines. Mol. Biol. Cell 16, 3117-3127.
9. Cheng, S. H., Rich, D. P., Marshall, J., Gregory, R. J., Welsh, M. J. and Smith, A. E. (1991). Phosphorylation of the R domain by cAMP-dependent protein kinase regulates the CFTR chloride channel. Cell 66, 1027-1036.
10. Clements, R. T., Minnear, F. L., Singer, H. A., Keller, R. S. and Vincent, P. A. (2005). RhoA and Rho-kinase dependent and independent signals mediate TGF-betainduced pulmonary endothelial cytoskeletal reorganization and permeability. Am. J. Physiol. Lung Cell Mol. Physiol. 288, L294-L306.
11. 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.
12. Di Benedetto, G., Zoccarato, A., Lissandron, V., Terrin, A., Li, X., Houslay, M. D., Baillie, G. S. and Zaccolo, M. (2008). Protein kinase A type I and type II define distinct intracellular signaling compartments. Circ. Res. 103, 836-844.
13. Favia, M., Guerra, L., Fanelli, T., Cardone, R. A., Monterisi, S., Di Sole, F., Castellani, S., Chen, M., Seidler, U., Reshkin, S. J. et al. (2010). Na+/H+ exchanger regulatory factor 1 overexpression-dependent increase of cytoskeleton organization is fundamental in the rescue of F508del cystic fibrosis transmembrane conductance regulator in human airway CFBE41o- cells. Mol. Biol. Cell 21, 73-86.
14. Gadsby, D. C. and Nairn, A. C. (1999). Control of CFTR channel gating by phosphorylation and nucleotide hydrolysis. Physiol. Rev. 79, S77-S107.
15. Galietta, L. J., Springsteel, M. F., Eda, M., Niedzinski, E. J., By, K., Haddadin, M. J., Kurth, M. J., Nantz, M. H. and Verkman, A. S. (2001). Novel CFTR chloride channel activators identified by screening of combinatorial libraries based on flavone and benzoquinolizinium lead compounds. J. Biol. Chem. 276, 19723-19728.
16. Ganeshan, R., Nowotarski, K., Di, A., Nelson, D. J. and Kirk, K. L. (2007). CFTR surface expression and chloride currents are decreased by inhibitors of N-WASP and actin polymerization. Biochim. Biophys. Acta 1773, 192-200.
17. Gelman, M. S., Kannegaard, E. S. and Kopito, R. R. (2002). A principal role for the proteasome in endoplasmic reticulum-associated degradation of misfolded intracellular cystic fibrosis transmembrane conductance regulator. J. Biol. Chem. 277, 11709-11714.
18. + exchanger regulatory factor isoform 1 overexpression modulates cystic fibrosis transmembrane conductance regulator (CFTR) expression and activity in human airway 16HBE14o- cells and rescues DeltaF508 CFTR functional expression in cystic fibrosis cells. J. Biol. Chem. 280, 40925-40933.
19. 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.
20. Houslay, M. D., Schafer, P. and Zhang, K. Y. (2005). Keynote review: phosphodiesterase-4 as a therapeutic target. Drug Discov. Today 10, 1503-1519.
21. Huang, P., Lazarowski, E. R., Tarran, R., Milgram, S. L., Boucher, R. C. and Stutts, M. J. (2001). Compartmentalized autocrine signaling to cystic fibrosis transmembrane conductance regulator at the apical membrane of airway epithelial cells. Proc. Natl. Acad. Sci. USA 98, 14120-14125.
22. Hwang, T. C., Wang, F., Yang, I. C. and Reenstra, W. W. (1997). Genistein potentiates wild-type and delta F508-CFTR channel activity. Am. J. Physiol. 273, C988-C998.
23. Jin, S., Haggie, P. M. and Verkman, A. S. (2007). Single-particle tracking of membrane protein diffusion in a potential: simulation, detection, and application to confined diffusion of CFTR Cl- channels. Biophys. J. 93, 1079-1088.
24. Klussmann, E., Maric, K., Wiesner, B., Beyermann, M. and Rosenthal, W. (1999). Protein kinase A anchoring proteins are required for vasopressin-mediated translocation of aquaporin-2 into cell membranes of renal principal cells. J. Biol. Chem. 274, 4934-4938.
25. Konstan, M.W. and Davis, P. B. (2002). Pharmacological approaches for the discovery and development of new anti-inflammatory agents for the treatment of cystic fibrosis. Adv. Drug Deliv. Rev. 54, 1409-1423.
26. Li, C. and Naren, A. P. (2010). CFTR chloride channel in the apical compartments: spatiotemporal coupling to its interacting partners. Integr. Biol. 2, 161-177.
27. Li, C., Ramjeesingh, M., Reyes, E., Jensen, T., Chang, X., Rommens, J. M. and Bear, C. E. (1993). The cystic fibrosis mutation (delta F508) does not influence the chloride channel activity of CFTR. Nat. Genet. 3, 311-316.
28. Liedtke, C. M., Yun, C. H., Kyle, N. and Wang, D. (2002). Protein kinase C epsilondependent regulation of cystic fibrosis transmembrane regulator involves binding to a receptor for activated C kinase (RACK1) and RACK1 binding to Na+/H+ exchange regulatory factor. J. Biol. Chem. 277, 22925-22933.
29. Ma, T., Thiagarajah, J. R., Yang, H., Sonawane, N. D., Folli, C., Galietta, L. J. and Verkman, A. S. (2002). Thiazolidinone CFTR inhibitor identified by high-throughput screening blocks cholera toxin-induced intestinal fluid secretion. J. Clin. Invest. 110, 1651-1658.
30. Machen, T. E. (2006). Innate immune response in CF airway epithelia: hyperinflammatory? Am. J. Physiol. Cell Physiol. 291, C218-C230.
31. McCarty, N. A., Standaert, T. A., Teresi, M., Tuthill, C., Launspach, J., Kelley, T. J., Milgram, L. J., Hilliard, K. A., Regelmann, W. E., Weatherly, M. R. et al. (2002). A phase I randomized, multicenter trial of CPX in adult subjects with mild cystic fibrosis. Pediatr. Pulmonol. 33, 90-98.
32. Mohler, P. J., Kreda, S. M., Boucher, R. C., Sudol, M., Stutts, M. J. and Milgram, S. L. (1999). Yes-associated protein 65 localizes p62(c-Yes) to the apical compartment of airway epithelia by association with EBP50. J. Cell Biol. 147, 879-890.
33. Moyer, B. D., Duhaime, M., Shaw, C., Denton, J., Reynolds, D., Karlson, K. H., Pfeiffer, J., Wang, S., Mickle, J. E., Milewski, M. et al. (2000). The PDZ-interacting domain of cystic fibrosis transmembrane conductance regulator is required for functional expression in the apical plasma membrane. J. Biol. Chem. 275, 27069-27074.
34. Okiyoneda, T. and Lukacs, G. L. (2007). Cell surface dynamics of CFTR: the ins and outs. Biochim. Biophys. Acta 1773, 476-479.
35. Oliveira, R. F., Terrin, A., Di Benedetto, G., Cannon, R. C., Koh, W., Kim, M., Zaccolo, M. and Blackwell, K. T. (2010). The role of type 4 phosphodiesterases in generating microdomains of cAMP: large scale stochastic simulations. PLoS ONE 5, e11725.
36. Pedemonte, N., Sonawane, N. D., Taddei, A., Hu, J., Zegarra-Moran, O., Suen, Y. F., Robins, L. I., Dicus, C. W., Willenbring, D., Nantz, M. H. et al. (2005). Phenylglycine and sulfonamide correctors of defective delta F508 and G551D cystic fibrosis transmembrane conductance regulator chloride-channel gating. Mol. Pharmacol. 67, 1797-1807.
37. Pedemonte, N., Tomati, V., Sondo, E. and Galietta, L. J. (2010). Influence of cell background on pharmacological rescue of mutant CFTR. Am. J. Physiol. Cell Physiol. 298, C866-C874.
38. Penmatsa, H., Zhang, W., Yarlagadda, S., Li, C., Conoley, V. G., Yue, J., Bahouth, S. W., Buddington, R. K., Zhang, G., Nelson, D. J. et al. (2010). Compartmentalized cyclic adenosine 39,59-monophosphate at the plasma membrane clusters PDE3A and cystic fibrosis transmembrane conductance regulator into microdomains. Mol. Biol. Cell 21, 1097-1110.
39. Ponsioen, B., Zhao, J., Riedl, J., Zwartkruis, F., van der Krogt, G., Zaccolo, M., Moolenaar, W. H., Bos, J. L. and Jalink, K. (2004). Detecting cAMP-induced Epac activation by fluorescence resonance energy transfer: Epac as a novel cAMP indicator. EMBO Rep. 5, 1176-1180.
40. Quinton, P. M. (1983). Chloride impermeability in cystic fibrosis. Nature 301, 421-422.
41. Rich, T. C., Fagan, K. A., Nakata, H., Schaack, J., Cooper, D. M. and Karpen, J. W. (2000). Cyclic nucleotide-gated channels colocalize with adenylyl cyclase in regions of restricted cAMP diffusion. J. Gen. Physiol. 116, 147-161.
42. Riordan, J. R. (1993). The cystic fibrosis transmembrane conductance regulator. Annu. Rev. Physiol. 55, 609-630.
43. Rowe, S. M., Pyle, L. C., Jurkevante, A., Varga, K., Collawn, J., Sloane, P. A., Woodworth, B., Mazur, M., Fulton, J., Fan, L. et al. (2010). DeltaF508 CFTR processing correction and activity in polarized airway and non-airway cell monolayers. Pulm. Pharmacol. Ther. 23, 268-278.
44. Rubenstein, R. C. and Zeitlin, P. L. (1998). A pilot clinical trial of oral sodium 4-phenylbutyrate (Buphenyl) in deltaF508-homozygous cystic fibrosis patients: partial restoration of nasal epithelial CFTR function. Am. J. Respir. Crit. Care Med. 157, 484-490.
45. 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.
46. Sloane, P. A. and Rowe, S. M. (2010). Cystic fibrosis transmembrane conductance regulator protein repair as a therapeutic strategy in cystic fibrosis. Curr. Opin. Pulm. Med. 16, 591-597.
47. Sun, F., Hug, M. J., Bradbury, N. A. and Frizzell, R. A. (2000a). Protein kinase A associates with cystic fibrosis transmembrane conductance regulator via an interaction with ezrin. J. Biol. Chem. 275, 14360-14366.
48. Sun, F., Hug, M. J., Lewarchik, C. M., Yun, C. H., Bradbury, N. A. and Frizzell, R. A. (2000b). E3KARP mediates the association of ezrin and protein kinase A with the cystic fibrosis transmembrane conductance regulator in airway cells. J. Biol. Chem. 275, 29539-29546.
49. Swiatecka-Urban, A., Duhaime, M., Coutermarsh, B., Karlson, K. H., Collawn, J., Milewski, M., Cutting, G. R., Guggino, W. B., Langford, G. and Stanton, B. A. (2002). PDZ domain interaction controls the endocytic recycling of the cystic fibrosis transmembrane conductance regulator. J. Biol. Chem. 277, 40099-40105.
50. Taddei, A., Folli, C., Zegarra-Moran, O., Fanen, P., Verkman, A. S. and Galietta, L. J. (2004). Altered channel gating mechanism for CFTR inhibition by a highaffinity thiazolidinone blocker. FEBS Lett. 558, 52-56.
51. Terrin, A., Di Benedetto, G., Pertegato, V., Cheung, Y. F., Baillie, G., Lynch, M. J., Elvassore, N., Prinz, A., Herberg, F. W., Houslay, M. D. et al. (2006). PGE(1) stimulation of HEK293 cells generates multiple contiguous domains with different [cAMP]: role of compartmentalized phosphodiesterases. J. Cell Biol. 175, 441-451.
52. Wang, F., Zeltwanger, S., Yang, I. C., Nairn, A. C. and Hwang, T. C. (1998). Actions of genistein on cystic fibrosis transmembrane conductance regulator channel gating. Evidence for two binding sites with opposite effects. J. Gen. Physiol. 111, 477-490.
53. Ward, C. L. and Kopito, R. R. (1994). Intracellular turnover of the cystic fibrosis transmembrane conductance regulator. J. Biol. Chem. 41, 25710-25718.
54. Ward, C. L., Omura, S. and Kopito, R. R. (1995). Degradation of CFTR by the ubiquitin-proteasome pathway. Cell 83, 121-127.
55. Zaccolo, M., De Giorgi, F., Cho, C. Y., Feng, L., Knapp, T., Negulescu, P. A., Taylor, S. S., Tsien, R. Y. and Pozzan, T. (2000). A genetically encoded, fluorescent indicator for cyclic AMP in living cells. Nat. Cell Biol. 2, 25-29.
56. Zeitlin, P. L. (2000). Pharmacologic restoration of delta F508 CFTR-mediated chloride current. Kidney Int. 57, 832-837.
57. Zhong, H., Voll, R. E. and Ghosh, S. (1998). Phosphorylation of NF-kappa B p65 by PKA stimulates transcriptional activity by promoting a novel bivalent interaction with the coactivator CBP/p300. Mol. Cell 1, 661-671.