Correctors of mutant CFTR enhance subcortical cAMP-PKA signaling through modulating ezrin phosphorylation and cytoskeleton organization

Journal of Cell Science

Volumn 129, Issue 6, 2016, Pages 1128-1140

  Abbattiscianni, Anna C ^a   Favia, Maria ^a   Mancini, Maria T ^a   Cardone, Rosa A ^a   Guerra, Lorenzo ^a   Monterisi, Stefania ^b   Castellani, Stefano ^c   Laselva, Onofrio ^a   Di Sole, Francesca ^d   Conese, Massimo ^c   Zaccolo, Manuela ^b   Casavola, Valeria ^a  

^a UNIVERSITY OF BARI   (Italy)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF FOGGIA   (Italy)

^d DES MOINES UNIVERSITY   (United States)

Author keywords

Airway cells; cAMP; Correctors; Cystic fibrosis; FRET; PKA

Indexed keywords

ACTIN; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; EZRIN; LATRUNCULIN B; LUMACAFTOR; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; CHLORIDE; CYTOSKELETON PROTEIN;

ACTIN FILAMENT; APICAL MEMBRANE; ARTICLE; CELL COMPARTMENTALIZATION; CONTROLLED STUDY; CYTOSKELETON; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; SUBCORTEX; ANIMAL; CYSTIC FIBROSIS; ENZYMOLOGY; GENE DELETION; GENETICS; METABOLISM; PHOSPHORYLATION;

ACTINS; ANIMALS; CHLORIDES; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYSTIC FIBROSIS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; CYTOSKELETAL PROTEINS; CYTOSKELETON; HUMANS; PHOSPHORYLATION; RATS; SEQUENCE DELETION; SIGNAL TRANSDUCTION;

EID: 84961203476     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.177907     Document Type: Article

References (53)

1. Arora, K., Moon, C., Zhang, W., Yarlagadda, S., Penmatsa, H., Ren, A., Sinha, C. and Naren, A. P. (2014). Stabilizing rescued surface-localized deltaF508 CFTR by potentiation of its interaction with Na(+)/H(+) exchanger regulatory factor 1. Biochemistry 53, 4169-4179.
2. Auvinen, E., Kivi, N. and Vaheri, A. (2007). Regulation of ezrin localization by Rac1 and PIPK in human epithelial cells. Exp. Cell Res. 313, 824-833.
3. Babich, V. and Di Sole, F. (2015). The Na+/H+ Exchanger-3 (NHE3) activity requires ezrin binding to phosphoinositide and its phosphorylation. PLoS ONE 10, e0129306.
4. Blanchard, E., Zlock, L., Lao, A., Mika, D., Namkung, W., Xie, M., Scheitrum, C., Gruenert, D. C., Verkman, A. S., Finkbeiner, W. E. et al. (2014). Anchored PDE4 regulates chloride conductance in wild-type and DeltaF508-CFTR human airway epithelia. FASEB J. 28, 791-801.
5. Bosk, S., Braunger, J. A., Gerke, V. and Steinem, C. (2011). Activation of F-actin binding capacity of ezrin: synergism of PIP(2) interaction and phosphorylation. Biophys. J. 100, 1708-1717.
6. Bretscher, A., Edwards, K. and Fehon, R. G. (2002). ERM proteins and merlin: integrators at the cell cortex. Nat. Rev. Mol. Cell Biol. 3, 586-599.
7. Cai, Z.-W., Liu, J., Li, H.-Y. and Sheppard, D. N. (2011). Targeting F508del-CFTR to develop rational new therapies for cystic fibrosis. Acta Pharmacol. Sin. 32, 693-701.
8. Cholon, D. M., O'Neal, W. K., Randell, S. H., Riordan, J. R. and Gentzsch, M. (2010). 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.
9. Cholon, D. M., Quinney, N. L., Fulcher, M. L., Esther, C. R., Jr., Das, J., Dokholyan, N. V., Randell, S. H., Boucher, R. C. and Gentzsch, M. (2014). Potentiator ivacaftor abrogates pharmacological correction of DeltaF508 CFTR in cystic fibrosis. Sci. Transl. Med. 6, 246ra96.
10. Clunes, M. T. and Boucher, R. C. (2011). Introduction to section I: overview of approaches to study cystic fibrosis pathophysiology. Methods Mol. Biol. 742, 3-14.
11. 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.
12. Di Sole, F., Babich, V. and Moe, O.W. (2009). The calcineurin homologous protein-1 increases Na(+)/H(+) -exchanger 3 trafficking via ezrin phosphorylation. J. Am. Soc. Nephrol. 20, 1776-1786.
13. Eckford, P. D.W., Ramjeesingh, M., Molinski, S., Pasyk, S., Dekkers, J. F., Li, C., Ahmadi, S., Ip, W., Chung, T. E., Du, K. et al. (2014). VX-809 and related corrector compounds exhibit secondary activity stabilizing active F508del-CFTR after its partial rescue to the cell surface. Chem. Biol. 21, 666-678.
14. 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.
15. Favia, M., Mancini, M. T., Bezzerri, V., Guerra, L., Laselva, O., Abbattiscianni, A. C., Debellis, L., Reshkin, S. J., Gambari, R., Cabrini, G. et al. (2014). Trimethylangelicin promotes the functional rescue of mutant F508del CFTR protein in cystic fibrosis airway cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 307, L48-L61.
16. Fievet, B. T., Gautreau, A., Roy, C., Del Maestro, L., Mangeat, P., Louvard, D. and Arpin, M. (2004). Phosphoinositide binding and phosphorylation act sequentially in the activation mechanism of ezrin. J. Cell Biol. 164, 653-659.
17. Guerra, L., Fanelli, T., Favia, M., Riccardi, S. M., Busco, G., Cardone, R. A., Carrabino, S., Weinman, E. J., Reshkin, S. J., Conese, M. et al. (2005). Na+/H+ 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.
18. Guggino, W. B. and Stanton, B. A. (2006). New insights into cystic fibrosis: molecular switches that regulate CFTR. Nat. Rev. Mol. Cell Biol. 7, 426-436.
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. 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.
21. Hao, J.-J., Liu, Y., Kruhlak, M., Debell, K. E., Rellahan, B. L. and Shaw, S. (2009). Phospholipase C-mediated hydrolysis of PIP2 releases ERM proteins from lymphocyte membrane. J. Cell Biol. 184, 451-462.
22. Janke, M., Herrig, A., Austermann, J., Gerke, V., Steinem, C. and Janshoff, A. (2008). Actin binding of ezrin is activated by specific recognition of PIP2-functionalized lipid bilayers. Biochemistry 47, 3762-3769.
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. Jurkuvenaite, A., Chen, L., Bartoszewski, R., Goldstein, R., Bebok, Z., Matalon, S. and Collawn, J. F. (2010). Functional stability of rescued delta F508 cystic fibrosis transmembrane conductance regulator in airway epithelial cells. Am. J. Respir. Cell Mol. Biol. 42, 363-372.
25. Li, C. and Naren, A. P. (2005). Macromolecular complexes of cystic fibrosis transmembrane conductance regulator and its interacting partners. Pharmacol. Ther. 108, 208-223.
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, J., Dai, Z., Jana, D., Callaway, D. J. E. and Bu, Z. (2005). Ezrin controls the macromolecular complexes formed between an adapter protein Na+/H+ exchanger regulatory factor and the cystic fibrosis transmembrane conductance regulator. J. Biol. Chem. 280, 37634-37643.
28. Loureiro, C. A., Matos, A. M., Dias-Alves, A., Pereira, J. F., Uliyakina, I., Barros, P., Amaral, M. D. and Matos, P. (2015). A molecular switch in the scaffold NHERF1 enables misfolded CFTR to evade the peripheral quality control checkpoint. Sci. Signal. 8, ra48.
29. Lukacs, G. L., Chang, X. B., Bear, C., Kartner, N., Mohamed, A., Riordan, J. R. and Grinstein, S. (1993). The delta F508 mutation decreases the stability of cystic fibrosis transmembrane conductance regulator in the plasma membrane. Determination of functional half-lives on transfected cells. J. Biol. Chem. 268, 21592-21598.
30. Monterisi, S., Favia, M., Guerra, L., Cardone, R. A., Marzulli, D., Reshkin, S. J., Casavola, V. and Zaccolo, M. (2012). CFTR regulation in human airway epithelial cells requires integrity of the actin cytoskeleton and compartmentalized cAMP and PKA activity. J. Cell Sci. 125, 1106-1117.
31. 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 PDZinteracting domain of cystic fibrosis transmembrane conductance regulator is required for functional expression in the apical plasma membrane. J. Biol. Chem. 275, 27069-27074.
32. Neuberger, T., Burton, B., Clark, H. and Van Goor, F. (2011). Use of primary cultures of human bronchial epithelial cells isolated from cystic fibrosis patients for the pre-clinical testing of CFTR modulators. Methods Mol. Biol. 741, 39-54.
33. Okiyoneda, T., Barriere, H., Bagdany, M., Rabeh, W. M., Du, K., Hohfeld, J., Young, J. C. and Lukacs, G. L. (2010). Peripheral protein quality control removes unfolded CFTR from the plasma membrane. Science 329, 805-810.
34. Pedemonte, N., Tomati, V., Sondo, E. and Galietta, L. J. V. (2010). Influence of cell background on pharmacological rescue of mutant CFTR. Am. J. Physiol. Cell Physiol. 298, C866-C874.
35. Ponsioen, B., Zhao, J., Riedl, J., Zwartkruis, F. J., 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.
36. Pyle, L. C., Ehrhardt, A., Mitchell, L. H., Fan, L., Ren, A., Naren, A. P., Li, Y., Clancy, J. P., Bolger, G. B., Sorscher, E. J. et al. (2011). Regulatory domain phosphorylation to distinguish the mechanistic basis underlying acute CFTR modulators. Am. J. Physiol. Lung Cell. Mol. Physiol. 301, L587-L597.
37. Randell, S. H., Fulcher, M. L., O'Neal, W. and Olsen, J. C. (2011). Primary epithelial cell models for cystic fibrosis research. Methods Mol. Biol. 742, 285-310.
38. Rowe, S. M. and Verkman, A. S. (2013). Cystic fibrosis transmembrane regulator correctors and potentiators. Cold Spring Harb. Perspect. Med. 3, 1-15.
39. Scudieri, P., Caci, E., Bruno, S., Ferrera, L., Schiavon, M., Sondo, E., Tomati, V., Gianotti, A., Zegarra-Moran, O., Pedemonte, N. et al. (2012). Association of TMEM16A chloride channel overexpression with airway goblet cell metaplasia. J. Physiol. 590, 6141-6155.
40. Sharma, M., Pampinella, F., Nemes, C., Benharouga, M., So, J., Du, K., Bache, K. G., Papsin, B., Zerangue, N., Stenmark, H. et al. (2004). Misfolding diverts CFTR from recycling to degradation: quality control at early endosomes. J. Cell Biol. 164, 923-933.
41. 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.
42. Soderberg, O., Gullberg, M., Jarvius, M., Ridderstrale, K., Leuchowius, K.-J., Jarvius, J., Wester, K., Hydbring, P., Bahram, F., Larsson, L.-G. et al. (2006). Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat. Methods 3, 995-1000.
43. Sun, F., Hug, M. J., Bradbury, N. A. and Frizzell, R. A. (2000). Protein kinase A associates with cystic fibrosis transmembrane conductance regulator via an interaction with ezrin. J. Biol. Chem. 275, 14360-14366.
44. 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.
45. Tamanini, A., Borgatti, M., Finotti, A., Piccagli, L., Bezzerri, V., Favia, M., Guerra, L., Lampronti, I., Bianchi, N., Dall'acqua, F. et al. (2011). Trimethylangelicin Reduces IL-8 Transcription and Potentiates CFTR Function. Am. J. Physiol. Lung Cell. Mol. Physiol. 300, L380-L390.
46. 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.
47. Valentine, C. D., Lukacs, G. L., Verkman, A. S. and Haggie, P. M. (2012). Reduced PDZ Interactions of rescued DeltaF508CFTR increases its cell surface mobility. J. Biol. Chem. 287, 43630-43638.
48. Van Goor, F., Hadida, S., Grootenhuis, P. D. J., Burton, B., Stack, J. H., Straley, K. S., Decker, C. J., Miller, M., McCartney, J., Olson, E. R. et al. (2011). Correction of the F508del-CFTR protein processing defect in vitro by the investigational drug VX-809. Proc. Natl. Acad. Sci. USA 108, 18843-18848.
49. Veit, G., Avramescu, R. G., Perdomo, D., Phuan, P.-W., Bagdany, M., Apaja, P. M., Borot, F., Szollosi, D., Wu, Y.-S., Finkbeiner, W. E. et al. (2014). Some gating potentiators, including VX-770, diminish DeltaF508-CFTR functional expression. Sci. Transl. Med. 6, 246ra97.
50. Welsh, M. J. and Smith, A. E. (1993). Molecular mechanisms of CFTR chloride channel dysfunction in cystic fibrosis. Cell 73, 1251-1254.
51. Yonemura, S., Matsui, T. and Tsukita, S. (2002). Rho-dependent and -independent activation mechanisms of ezrin/radixin/moesin proteins: an essential role for polyphosphoinositides in vivo. J. Cell Sci. 115, 2569-2580.
52. Zegarra-Moran, O., Romio, L., Folli, C., Caci, E., Becq, F., Vierfond, J.-M., Mettey, Y., Cabrini, G., Fanen, P. and Galietta, L. J. V. (2002). Correction of G551D-CFTR transport defect in epithelial monolayers by genistein but not by CPX or MPB-07. Br. J. Pharmacol. 137, 504-512.
53. Zhang, W., Fujii, N. and Naren, A. P. (2012). Recent advances and new perspectives in targeting CFTR for therapy of cystic fibrosis and enterotoxin-induced secretory diarrheas. Future Med. Chem. 4, 329-345.