EPAC1 activation by cAMP stabilizes CFTR at the membrane by promoting its interaction with NHERF1

Journal of Cell Science

Volumn 129, Issue 13, 2016, Pages 2599-2612

  Lobo, Miguel J ^a,b   Amaral, Margarida D ^a   Zaccolo, Manuela ^b   Farinha, Carlos M ^a  

^a UNIVERSITY OF LISBON   (Portugal)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

CAMP; CFTR; EPAC1; Membrane stability; Protein trafficking

Indexed keywords

ADAPTOR PROTEIN; ANTIPORTER; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; EPAC1 PROTEIN; NHERF1 PROTEIN; UNCLASSIFIED DRUG; GUANINE NUCLEOTIDE EXCHANGE FACTOR; PHOSPHOPROTEIN; PROTEIN BINDING; RAPGEF3 PROTEIN, HUMAN; SODIUM PROTON EXCHANGE PROTEIN; SODIUM-HYDROGEN EXCHANGER REGULATORY FACTOR;

ANCHORING JUNCTION; ARTICLE; BIOGENESIS; CELL MEMBRANE; CELL MIGRATION; CHANNEL GATING; CONTROLLED STUDY; ENDOCYTOSIS; EPITHELIUM CELL; HUMAN; HUMAN CELL; ION TRANSPORT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; REGULATORY MECHANISM; A-549 CELL LINE; CYSTIC FIBROSIS; GENETICS; METABOLISM; PATHOLOGY; PHOSPHORYLATION; RESPIRATORY SYSTEM; SIGNAL TRANSDUCTION;

A549 CELLS; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYSTIC FIBROSIS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; ENDOCYTOSIS; EPITHELIAL CELLS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN INTERACTION MAPS; RESPIRATORY SYSTEM; SIGNAL TRANSDUCTION; SODIUM-HYDROGEN ANTIPORTER;

EID: 84977605019     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.185629     Document Type: Article

References (57)

1. Almaca, J., Dahimene, S., Appel, N., Conrad, C., Kunzelmann, K., Pepperkok, R. and Amaral, M. D. (2011). Functional genomics assays to study CFTR traffic and ENaC function. Methods Mol. Biol. 742, 249-264.
2. Amaral, M. D. and Farinha, C. M. (2013). Rescuing mutant CFTR: a multi-task approach to a better outcome in treating cystic fibrosis. Curr. Pharm. Des. 19, 3497-3508.
3. Bebok, Z., Collawn, J. F., Wakefield, J., Parker, W., Li, Y., Varga, K., Sorscher, E. J. and Clancy, J. P. (2005). Failure of cAMP agonists to activate rescued deltaF508 CFTR in CFBE41o-airway epithelial monolayers. J. Physiol. 569, 601-615.
4. Boucher, R. C. (2004). New concepts of the pathogenesis of cystic fibrosis lung disease. Eur. Respir. J. 23, 146-158.
5. Castellani, S., Guerra, L., Favia, M., Di Gioia, S., Casavola, V. and Conese, M. (2012). NHERF1 and CFTR restore tight junction organisation and function in cystic fibrosis airway epithelial cells: role of ezrin and the RhoA/ROCK pathway. Lab. Invest. 92, 1527-1540.
6. Chang, S. Y., Di, A., Naren, A. P., Palfrey, H. C., Kirk, K. L. and Nelson, D. J. (2002). Mechanisms of CFTR regulation by syntaxin 1A and PKA. J. Cell Sci. 115, 783-791.
7. Christensen, A. E., Selheim, F., de Rooij, J., Dremier, S., Schwede, F., Dao, K. K., Martinez, A., Maenhaut, C., Bos, J. L., Genieser, H.-G. et al. (2003). cAMP analog mapping of Epac1 and cAMP kinase: discriminating analogs demonstrate that Epac and cAMP kinase act synergistically to promote PC-12 cell neurite extension. J. Biol. Chem. 278, 35394-35402.
8. Cihil, K. M., Ellinger, P., Fellows, A., Stolz, D. B., Madden, D. R. and Swiatecka-Urban, A. (2012). Disabled-2 protein facilitates assembly polypeptide-2-independent recruitment of cystic fibrosis transmembrane conductance regulator to endocytic vesicles in polarized human airway epithelial cells. J. Biol. Chem. 287, 15087-15099.
9. Clancy, J. P., Rowe, S. M., Accurso, F. J., Aitken, M. L., Amin, R. S., Ashlock, M. A., Ballmann, M., Boyle, M. P., Bronsveld, I., Campbell, P. W. et al. (2012). Results of a phase IIa study of VX-809, an investigational CFTR corrector compound, in subjects with cystic fibrosis homozygous for the F508del-CFTR mutation. Thorax 67, 12-18.
10. Conrotto, P., Yakymovych, I., Yakymovych, M. and Souchelnytskyi, S. (2007). Interactome of transforming growth factor-beta type I receptor (TbetaRI): inhibition of TGFbeta signaling by Epac1. J. Proteome Res. 6, 287-297.
11. Consonni, S. V., Gloerich, M., Spanjaard, E. and Bos, J. L. (2012). cAMP regulates DEP domain-mediated binding of the guanine nucleotide exchange factor Epac1 to phosphatidic acid at the plasma membrane. Proc. Natl. Acad. Sci. USA 109, 3814-3819.
12. de Rooij, J., Rehmann, H., van Triest, M., Cool, R. H., Wittinghofer, A. and Bos, J. L. (2000). Mechanism of regulation of the Epac family of cAMP-dependent RapGEFs. J. Biol. Chem. 275, 20829-20836.
13. DiPilato, L. M., Cheng, X. and Zhang, J. (2004). Fluorescent indicators of cAMP and Epac activation reveal differential dynamics of cAMP signaling within discrete subcellular compartments. Proc. Natl. Acad. Sci. USA 101, 16513-16518.
14. Farinha, C. M., Nogueira, P., Mendes, F., Penque, D. and Amaral, M. D. (2002). The human DnaJ homologue (Hdj)-1/heat-shock protein (Hsp) 40 co-chaperone is required for the in vivo stabilization of the cystic fibrosis transmembrane conductance regulator by Hsp70. Biochem. J. 366, 797-806.
15. Farinha, C. M., King-Underwood, J., Sousa, M., Correia, A. R., Henriques, B. J., Roxo-Rosa, M., Da Paula, A. C., Williams, J., Hirst, S., Gomes, C. M. et al. (2013a). Revertants, low temperature, and correctors reveal the mechanism of F508del-CFTR rescue by VX-809 and suggest multiple agents for full correction. Chem. Biol. 20, 943-955.
16. Farinha, C. M., Matos, P. and Amaral, M. D. (2013b). Control of cystic fibrosis transmembrane conductance regulator membrane trafficking: not just from the endoplasmic reticulum to the Golgi. FEBS J. 280, 4396-4406.
17. 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.
18. Fogh, J., Wright, W. C. and Loveless, J. D. (1977). Absence of HeLa cell contamination in 169 cell lines derived from human tumors. J. Natl. Cancer Inst. 58, 209-214.
19. Franke, B., Akkerman, J.-W. N. and Bos, J. L. (1997). Rapid Ca2+-mediated activation of Rap1 in human platelets. EMBO J. 16, 252-259.
20. Gloerich, M. and Bos, J. L. (2010). Epac: defining a new mechanism for cAMP action. Annu. Rev. Pharmacol. Toxicol. 50, 355-375.
21. Gloerich, M., Ponsioen, B., Vliem, M. J., Zhang, Z., Zhao, J., Kooistra, M. R., Price, L. S., Ritsma, L., Zwartkruis, F. J., Rehmann, H. et al. (2010). Spatial regulation of cyclic AMP-Epac1 signaling in cell adhesion by ERM proteins. Mol. Cell. Biol. 30, 5421-5431.
22. Gruenert, D. C., Finkbeiner, W. E. and Widdicombe, J. H. (1995). Culture and transformation of human airway epithelial cells. Am. J. Physiol. 268, L347-L360.
23. 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.
24. Hoque, K. M., Woodward, O. M., van Rossum, D. B., Zachos, N. C., Chen, L., Leung, G. P. H., Guggino, W. B., Guggino, S. E. and Tse, C.-M. (2010). Epac1 mediates protein kinase A-independent mechanism of forskolin-activated intestinal chloride secretion. J. Gen. Physiol. 135, 43-58.
25. Ivonnet, P., Salathe, M. and Conner, G. E. (2015). Hydrogen peroxide stimulation of CFTR reveals an Epac-mediated, soluble AC-dependent cAMP amplification pathway common to GPCR signalling. Br. J. Pharmacol. 172, 173-184.
26. Kooistra, M. R. H., Corada, M., Dejana, E. and Bos, J. L. (2005). Epac1 regulates integrity of endothelial cell junctions through VE-cadherin. FEBS Lett. 579, 4966-4972.
27. Lefkimmiatis, K., Leronni, D. and Hofer, A. M. (2013). The inner and outer compartments of mitochondria are sites of distinct cAMP/PKA signaling dynamics. J. Cell Biol. 202, 453-462.
28. 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.
29. Liu, S., Zhang, J. and Xiang, Y. K. (2011). FRET-based direct detection of dynamic protein kinase A activity on the sarcoplasmic reticulum in cardiomyocytes. Biochem. Biophys. Res. Commun. 404, 581-586.
30. 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.
31. Macia, E., Ehrlich, M., Massol, R., Boucrot, E., Brunner, C. and Kirchhausen, T. (2006). Dynasore, a cell-permeable inhibitor of dynamin. Dev. Cell 10, 839-850.
32. Mendes, A. I., Matos, P., Moniz, S., Luz, S., Amaral, M. D., Farinha, C. M. and Jordan, P. (2011). Antagonistic regulation of cystic fibrosis transmembrane conductance regulator cell surface expression by protein kinases WNK4 and spleen tyrosine kinase. Mol. Cell. Biol. 31, 4076-4086.
33. Mochizuki, N., Yamashita, S., Kurokawa, K., Ohba, Y., Nagai, T., Miyawaki, A. and Matsuda, M. (2001). Spatio-temporal images of growth-factor-induced activation of Ras and Rap1. Nature 411, 1065-1068.
34. 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.
35. Monterisi, S., Casavola, V. and Zaccolo, M. (2013). Local modulation of cystic fibrosis conductance regulator: cytoskeleton and compartmentalized cAMP signalling. Br. J. Pharmacol. 169, 1-9.
36. Morales, F. C., Takahashi, Y., Momin, S., Adams, H., Chen, X. and Georgescu, M.-M. (2007). NHERF1/EBP50 head-to-tail intramolecular interaction masks association with PDZ domain ligands. Mol. Cell. Biol. 27, 2527-2537.
37. 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.
38. Nakamura, T., Kurokawa, K., Kiyokawa, E. and Matsuda, M. (2006). Analysis of the spatiotemporal activation of rho GTPases using Raichu probes. Methods Enzymol. 406, 315-332.
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. Ponsioen, B., Gloerich, M., Ritsma, L., Rehmann, H., Bos, J. L. and Jalink, K. (2009). Direct spatial control of Epac1 by cyclic AMP. Mol. Cell. Biol. 29, 2521-2531.
41. Reczek, D., Berryman, M. and Bretscher, A. (1997). Identification of EBP50: a PDZ-containing phosphoprotein that associates with members of the ezrinradixin-moesin family. J. Cell Biol. 139, 169-179.
42. Riordan, J. R. (2008). CFTR function and prospects for therapy. Annu. Rev. Biochem. 77, 701-726.
43. Roscioni, S. S., Kistemaker, L. E. M., Menzen, M. H., Elzinga, C. R. S., Gosens, R., Halayko, A. J., Meurs, H. and Schmidt, M. (2009). PKA and Epac cooperate to augment bradykinin-induced interleukin-8 release from human airway smooth muscle cells. Respir. Res. 10, 88.
44. Schmidt, M., Dekker, F. J. and Maarsingh, H. (2013). Exchange protein directly activated by cAMP (epac): a multidomain cAMP mediator in the regulation of diverse biological functions. Pharmacol. Rev. 65, 670-709.
45. Schwede, F.,Bertinetti, D., Langerijs,C.N., Hadders, M. A.,Wienk,H., Ellenbroek, J. H., de Koning, E. J. P., Bos, J. L., Herberg, F.W.,Genieser, H.-G. et al. (2015). Structure-guided design of selective Epac1 and Epac2 agonists. PLoS Biol. 13, e1002038.
46. Sheppard, D. N. and Welsh, M. J. (1999). Structure and function of the CFTR chloride channel. Physiol. Rev. 79, S23-S45.
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. C., 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. Tkachenko, E., Sabouri-Ghomi, M., Pertz, O., Kim, C., Gutierrez, E., Machacek, M., Groisman, A., Danuser, G. and Ginsberg, M. H. (2011). Protein kinase A governs a RhoA-RhoGDI protrusion-retraction pacemaker in migrating cells. Nat. Cell Biol. 13, 661-668.
51. Ulucan, C., Wang, X., Baljinnyam, E., Bai, Y., Okumura, S., Sato, M., Minamisawa, S., Hirotani, S. and Ishikawa, Y. (2007). Developmental changes in gene expression of Epac and its upregulation in myocardial hypertrophy. Am. J. Physiol. Heart Circ. Physiol. 293, H1662-H1672.
52. 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.
53. Voltz, J. W., Weinman, E. J. and Shenolikar, S. (2001). Expanding the role of NHERF, a PDZ-domain containing protein adapter, to growth regulation. Oncogene 20, 6309-6314.
54. Wainwright, C. E., Elborn, J. S., Ramsey, B. W., Marigowda, G., Huang, X., Cipolli, M., Colombo, C., Davies, J. C., De Boeck, K., Flume, P. A. et al. (2015). Lumacaftor-Ivacaftor in patients with cystic fibrosis homozygous for Phe508del CFTR. N. Engl. J. Med. 373, 220-231.
55. 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 cystic fibrosis transmembrane conductance regulator (CFTR). FEBS Lett. 427, 103-108.
56. Young, A., Gentzsch, M., Abban, C. Y., Jia, Y., Meneses, P. I., Bridges, R. J. and Bradbury, N. A. (2009). Dynasore inhibits removal of wild-type and DeltaF508 cystic fibrosis transmembrane conductance regulator (CFTR) from the plasma membrane. Biochem. J. 421, 377-385.
57. Zinchuk, V. and Zinchuk, O. (2008). Quantitative colocalization analysis of confocal fluorescence microscopy images. Curr. Protoc. Cell Biol. 39, 4.19, 4.19.1-4.19.16.