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

Molecular Biology of the Cell

Volumn 21, Issue 1, 2010, Pages 73-86

  Favia, Maria ^a   Guerra, Lorenzo ^a   Fanelli, Teresa ^a   Cardone, Rosa Angela ^a   Monterisi, Stefania ^a   Di Sole, Francesca ^b   Castellani, Stefano ^c   Chen, Mingmin ^d   Seidler, Ursula ^d   Reshkin, Stephan Joel ^a   Conese, Massimo ^c   Casavola, Valeria ^a  

^a UNIVERSITY OF BARI   (Italy)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c UNIVERSITY OF FOGGIA   (Italy)

^d HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CHLORIDE; EZRIN; F ACTIN; PHENYLALANINE; RADIXIN; RHO KINASE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SODIUM HYDROGEN EXCHANGER REGULATORY FACTOR 1; SODIUM PROTON EXCHANGE PROTEIN; TRANSMEMBRANE CONDUCTANCE REGULATOR; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ARTICLE; CONTROLLED STUDY; CYTOSKELETON; ENZYME INHIBITION; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; WILD TYPE;

ACTINS; ANIMALS; BRONCHI; CELL LINE; CHLORIDES; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; CYTOSKELETAL PROTEINS; CYTOSKELETON; ENDOCYTOSIS; EPITHELIAL CELLS; HUMANS; KINETICS; MEMBRANE PROTEINS; MICE; MICROFILAMENT PROTEINS; PHOSPHOPROTEINS; PROTEIN BINDING; PROTEIN TRANSPORT; RHO-ASSOCIATED KINASES; RHOA GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION; SODIUM-HYDROGEN ANTIPORTER;

EID: 75649086188     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E09-03-0185     Document Type: Article

References (58)

1. Arber, S., Barbayannis, F. A., Hanser, H., Schneider, C., Stanyon, C. A., Bernard, O., and Caroni, P. (1998). Regulation of actin dynamics through phosphorylation of cofilin by LIM-kinase. Nature 393, 805-809.
2. Bates, I. R., Hebert, B., Luo, Y., Liao, J., Bachir, A. I., Kolin, D. L., Wiseman, P. W., and Hanrahan, J. W. (2006). Membrane lateral diffusion and capture of CFTR within transient confinement zones. Biophys. J. 91, 1046-1058.
3. Benharouga, M., Sharma, M., So, J., Haardt, M., Drzymala, L., Popov, M., Schwapach, B., Grinstein, S., Du, K., and Lukacs, G. L. (2003). The role of the C terminus and Na+/H+ exchanger regulatory factor in the functional expression of cystic fibrosis transmembrane conductance regulator in nonpolarized cells and epithelia. J. Biol. Chem. 278, 22079-22089.
4. 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.
5. Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
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. Bretscher, A., Reczek, D., and Berryman, M. (1997). Ezrin: a protein requiring conformational activation to link microfilaments to the plasma membrane in the assembly of cell surface structures. J. Cell Sci. 110, 3011-3018.
8. Bronsveld, I., et al. (2000). Residual chloride secretion in intestinal tissue of deltaF508 homozygous twins and siblings with cystic fibrosis. The European CF Twin and Sibling Study Consortium. Gastroenterology 119, 32-40.
9. 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.
10. Cheng, J., Moyer, B. D., Milewski, M., Loffing, J., Ikeda, M., Mickle, J. E., Cutting, G. R., Li, M., Stanton, B. A., and Guggino, W. B. (2002). A Golgiassociated PDZ domain protein modulates cystic fibrosis transmembrane regulator plasma membrane expression. J. Biol. Chem. 277, 3520-3529.
11. 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.
12. 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.
13. Gautreau, A., Louvard, D., and Arpin, M. (2000). Morphogenic effects of ezrin require a phosphorylation-induced transition from oligomers to monomers at the plasma membrane. J. Cell Biol. 150, 193-203.
14. Guerra, L., 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.
15. 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.
16. 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.
17. 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.
18. Hall, R. A., Ostedgaard, L. S., Premont, R. T., Blitzer, J. T., Rahman, N., Welsh, M. J., and Lefkowitz, R. J. (1998). A C-terminal motif found in the beta2-adrenergic receptor, P2Y1 receptor and cystic fibrosis transmembrane conductance regulator determines binding to the Na+/H+ exchanger regulatory factor family of PDZ proteins. Proc. Natl. Acad. Sci. USA 95, 8496-8501.
19. Hayashi, K., Yonemura, S., Matsui, T., and Tsukita, S. (1999). Immunofluorescence detection of ezrin/radixin/moesin (ERM) proteins with their carboxyl-terminal threonine phosphorylated in cultured cells and tissues. J. Cell Sci. 112, 1149-1158.
20. Howard, M., Jiang, X., Stolz, D. B., Hill, W. G., Johnson, J. A., Watkins, S. C., Frizzell, R. A., Bruton, C. M., Robbins, P. D., and Weisz, O. A. (2000). Forskolin-induced apical membrane insertion of virally expressed, epitopetagged CFTR in polarized MDCK cells. Am. J. Physiol. Cell Physiol. 279, C375-C382.
21. Ivetic, A., and Ridley, A. J. (2004). Ezrin/radixin/moesin proteins and Rho GTPase signalling in leucocytes. Immunology 112, 165-176.
22. Kalin, N., Claass, A., Sommer, M., Puchelle, E., and Tummler, B. (1999). DeltaF508 CFTR protein expression in tissues from patients with cystic fibrosis. J. Clin. Invest. 103, 1379-1389.
23. Kimura, K., et al. (1996). Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase). Science 273, 245-248.
24. Korichneva, I., and Hammerling, U. (1999). F-actin as a functional target for retro-retinoids: a potential role in anhydroretinol-triggered cell death. J. Cell Sci. 112, 2521-2528.
25. - exchange in developing neonatal rat cardiac cells. Biochemical identification and immunolocalization of band 3-like proteins. Circ. Res. 77, 556-564.
26. Kwon, S. H., Pollard, H., and Guggino, W. B. (2007). Knockdown of NHERF1 enhances degradation of temperature rescued DeltaF508 CFTR from the cell surface of human airway cells. Cell Physiol. Biochem. 20, 763-772.
27. Li, C., and Naren, A. P. (2005). Macromolecular complexes of cystic fibrosis transmembrane conductance regulator and its interacting partners. Pharmacol. Ther. 108, 208-223.
28. Lukacs, G. L., Chang, X., Bear, C., Kartner, N., Mohamed, A., Riordan, J. R., and Grinstein, S. (1993). The DF508 mutation decreases the stability of cystic fibrosis transmembrane conductance regulator in the plasma membrane. J. Biol. Chem. 268, 21592-21598.
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. Mackay, D. J., and Hall, A. (1998). Rho GTPases. J. Biol. Chem. 273, 20685-20688.
31. Matsui, T., Maeda, M., Doi, Y., Yonemura, S., Amano, M., Kaibuchi, K., and Tsukita, S. (1998). Rho-kinase phosphorylates COOH-terminal threonines of ezrin/radixin/moesin (ERM) proteins and regulates their head-to-tail association. J. Cell Biol. 140, 647-657.
32. Matsui, T., Yonemura, S., and Tsukita, S. (1999). Activation of ERM proteins in vivo by Rho involves phosphatidyl-inositol 4-phosphate 5-kinase and not ROCK kinases. Curr. Biol. 9, 1259-1262.
33. 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.
34. Morales, F. C., Takahashi, Y., Kreimann, E. L., and Georgescu, M. M. (2004). Ezrin-radixin-moesin (ERM)-binding phosphoprotein 50 organizes ERM proteins at the apical membrane of polarized epithelia. Proc. Natl. Acad. Sci. USA 101, 17705-17710.
35. Moyer, B. D., et al. (1999). A PDZ-interacting domain in CFTR is an apical membrane polarization signal. J. Clin. Invest. 104, 1353-1361.
36. Moyer, B. D., et al. (2000). The PDZ-interacting domain of cystic fibrosis transmembrane conductance regulator is required for functional expression in the apical membrane. J. Biol. Chem. 275, 27069-27074.
37. Nakano, M., Okamoto, Y., Ohzeki, J., and Masumoto, H. (2003). Epigenetic assembly of centromeric chromatin at ectopic alpha-satellite sites on human chromosomes. J. Cell Sci. 116, 4021-4034.
38. Okiyoneda, T., and Lukacs, G. L. (2007). Cell surface dynamics of CFTR: the ins and outs. Biochim. Biophys. Acta 1773, 476-479.
39. Paradiso, A., Cardone, R. A., Bellizzi, A., Bagorda, A., Guerra, L., Tommasino, M., Casavola, V., and Reshkin, S. J. (2004). The Na+-H+ exchanger-1 induces cytoskeletal changes involving reciprocal RhoA and Rac1 signaling, resulting in motility and invasion in MDA-MB-435 cells. Breast Cancer Res. 6, R616-R628.
40. Prat, A. G., Xiao, Y. F., Ausiello, D. A., and Cantiello, H. F. (1995). cAMPindependent regulation of CFTR by the actin cytoskeleton. Am. J. Physiol. 268, C1552-C1561.
41. Raghuram, V., Mak, D. D., and Foskett, J. K. (2001). Regulation of cystic fibrosis transmembrane conductance regulator single-channel gating by bivalent PDZ-domain-mediated interaction. Proc. Natl. Acad. Sci. USA 98, 1300-1305.
42. Schmieder, S., Nagai, M., Orlando, R. A., Takeda, T., and Farquhar, M. G. (2004). Podocalyxin activates RhoA and induces actin reorganization through NHERF1 and Ezrin in MDCK cells. J. Am. Soc. Nephrol. 15, 2289-2298.
43. Sharma, M., Benharouga, M., Hu, W., and Lukacs, G. L. (2001). Conformational and temperature-sensitive stability defects of the delta F508 cystic fibrosis transmembrane conductance regulator in post-endoplasmic reticulum compartments. J. Biol. Chem. 276, 8942-8950.
44. Sheppard, D. N., and Welsh, M. J. (1999). Structure and function of the CFTR chloride channel. Physiol. Rev. 79, S23-S45.
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. Silvis, M. R., Bertrand, C. A., Ameen, N., Golin-Bisello, F., Butterworth, M. B., Frizzell, R. A., and Bradbury, N. A. (2009). Rab11b regulates the apical recycling of the cystic fibrosis transmembrane conductance regulator in polarized intestinal epithelial cells. Mol. Biol. Cell 20, 2337-2350.
47. Stanasila, L., Abuin, L., Diviani, D., and Cotecchia, S. (2006). Ezrin directly interacts with the alpha1b-adrenergic receptor and plays a role in receptor recycling. J. Biol. Chem. 281, 4354-4363.
48. 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.
49. Swiatecka-Urban, A., et al. (2005). The short apical membrane half-life of rescued {Delta}F508-cystic fibrosis transmembrane conductance regulator (CFTR) results from accelerated endocytosis of {Delta}F508-CFTR in polarized human airway epithelial cells. J. Biol. Chem. 280, 36762-36772.
50. 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.
51. 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 high-affinity thiazolidinone blocker. FEBS Lett. 558, 52-56.
52. Tapon, N., and Hall, A. (1997). Rho, Rac and Cdc42 GTPases regulate the organization of the actin cytoskeleton. Curr. Opin. Cell Biol. 9, 86-92.
53. Tominaga, T., Sahai, E., Chardin, P., McCormick, F., Courtneidge, S. A., and Alberts, A. S. (2000). Diaphanous-related formins bridge Rho GTPase and Src tyrosine kinase signaling. Mol. Cell 5, 13-25.
54. Uehata, M., Ishizaki, T., Satoh, H., Ono, T., Kawahara, T., Morishita, T., Tamakawa, H., Yamagami, K., Inui, J., Maekawa, M., and Narumiya, S. (1997). Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature 389, 990-994.
55. Wang, S., Yue, H., Derin, R. B., Guggino, W. B., and Li, M. (2000). Accessory protein facilitated CFTR-CFTR interaction, a molecular mechanism to potentiate the chloride channel activity. Cell 103, 169-179.
56. Watanabe, N., Madaule, P., Reid, T., Ishizaki, T., Watanabe, G., Kakizuka, A., Saito, Y., Nakao, K., Jockusch, B. M., and Narumiya, S. (1997). p140mDia, a mammalian homolog of Drosophila diaphanous, is a target protein for Rho small GTPase and is a ligand for profilin. EMBO J. 16, 3044-3056.
57. 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.
58. Yoshizaki, H., Ohba, Y., Parrini, M. C., Dulyaninova, N. G., Bresnick, A. R., Mochizuki, N., and Matsuda, M. (2004). Cell type-specific regulation of RhoA activity during cytokinesis. J. Biol. Chem. 279, 44756-44762.