Local modulation of cystic fibrosis conductance regulator: Cytoskeleton and compartmentalized cAMP signalling

British Journal of Pharmacology

Volumn 169, Issue 1, 2013, Pages 1-9

  Monterisi, Stefania ^a   Casavola, Valeria ^b   Zaccolo, Manuela ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF BARI   (Italy)

Author keywords

cAMP; CFTR; compartmentalization; cystic fibrosis; cytoskeleton; PKA

Indexed keywords

CYCLIC AMP; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; EZRIN; IVACAFTOR;

ACTIN FILAMENT; APICAL MEMBRANE; BINDING AFFINITY; CYSTIC FIBROSIS; CYTOSKELETON; DRUG EFFICACY; DRUG MECHANISM; HUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; REVIEW; TREATMENT RESPONSE;

ANIMALS; CHLORIDE CHANNELS; CYCLIC AMP; CYSTIC FIBROSIS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; CYTOSKELETON; DRUG DESIGN; EPITHELIAL CELLS; HUMANS; MOLECULAR TARGETED THERAPY; MUTATION; SIGNAL TRANSDUCTION;

EID: 84876269644     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.12017     Document Type: Review

References (79)

1. Barnes AP, Livera G, Huang P, Sun C, O'Neal WK, Conti M, et al. (2005). Phosphodiesterase 4D forms a cAMP diffusion barrier at the apical membrane of the airway epithelium. J Biol Chem 280: 7997-8003.
2. Bates IR, Hebert B, Luo Y, Liao J, Bachir AI, Kolin DL, et al. (2006). Membrane lateral diffusion and capture of CFTR within transient confinement zones. Biophys J 91: 1046-1058.
3. Bebok Z, Collawn JF, Wakefield J, Parker W, Li Y, Varga K, et al. (2005). Failure of cAMP agonists to activate rescued deltaF508 CFTR in CFBE41o- airway epithelial monolayers. J Physiol 569: 601-615.
4. Becq F, Mall MA, Sheppard DN, Conese M, Zegarra-Moran O, (2011). Pharmacological therapy for cystic fibrosis: from bench to bedside. J Cyst Fibros 10 (Suppl. 2): S129-S145.
5. Beene DL, Scott JD, (2007). A-kinase anchoring proteins take shape. Curr Opin Cell Biol 19: 192-198.
6. Boucher RC, (2007). Cystic fibrosis: a disease of vulnerability to airway surface dehydration. Trends Mol Med 13: 231-240.
7. Bretscher A, Edwards K, Fehon RG, (2002). ERM proteins and merlin: integrators at the cell cortex. Nat Rev Mol Cell Biol 3: 586-599.
8. Brown CR, Hong-Brown LQ, Biwersi J, Verkman AS, Welch WJ, (1996). Chemical chaperones correct the mutant phenotype of the delta F508 cystic fibrosis transmembrane conductance regulator protein. Cell Stress Chaperones 1: 117-125.
9. Cai ZW, Liu J, Li HY, Sheppard DN, (2011). Targeting F508del-CFTR to develop rational new therapies for cystic fibrosis. Acta Pharmacol Sin 32: 693-701.
10. Cholon DM, O'Neal WK, Randell SH, Riordan JR, 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.
11. Cuthbert AW, (2011). New horizons in the treatment of cystic fibrosis. Br J Pharmacol 163: 173-183.
12. Davis PB, Drumm M, Konstan MW, (1996). Cystic fibrosis. Am J Respir Crit Care Med 154: 1229-1256.
13. Denning GM, Anderson MP, Amara JF, Marshall J, Smith AE, et al. (1992). Processing of mutant cystic fibrosis transmembrane conductance regulator is temperature-sensitive. Nature 358: 761-764.
14. Di Benedetto G, Zoccarato A, Lissandron V, Terrin A, Li X, Houslay MD, et al. (2008). Protein kinase A type I and type II define distinct intracellular signaling compartments. Circ Res 103: 836-844.
15. Dransfield DT, Bradford AJ, Smith J, Martin M, Roy C, Mangeat PH, et al. (1997). Ezrin is a cyclic AMP-dependent protein kinase anchoring protein. EMBO J 16: 35-43.
16. Favia M, Guerra L, Fanelli T, Cardone RA, Monterisi S, Di Sole F, 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.
17. Fehon RG, McClatchey AI, Bretscher A, (2010). Organizing the cell cortex: the role of ERM proteins. Nat Rev Mol Cell Biol 11: 276-287.
18. Fievet BT, Gautreau A, Roy C, Del Maestro L, Mangeat P, Louvard D, et al. (2004). Phosphoinositide binding and phosphorylation act sequentially in the activation mechanism of ezrin. J Cell Biol 164: 653-659.
19. Flume PA, Van Devanter DR, (2012). State of progress in treating cystic fibrosis respiratory disease. BMC Med 10: 88. doi: 10.1186/1741-7015-10-88
20. Gadsby DC, Dousmanis AG, Nairn AC, (1998). ATP hydrolysis cycles and the gating of CFTR Cl- channels. Acta Physiol Scand Suppl 643: 247-256.
21. Galietta LJ, Springsteel MF, Eda M, Niedzinski EJ, By K, Haddadin MJ, et al. (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.
22. Ganeshan R, Nowotarski K, Di A, Nelson DJ, Kirk KL, (2007). CFTR surface expression and chloride currents are decreased by inhibitors of N-WASP and actin polymerization. Biochim Biophys Acta 1773: 192-200.
23. Gentzsch M, Chang XB, Cui L, Wu Y, Ozols VV, Choudhury A, et al. (2004). Endocytic trafficking routes of wild type and DeltaF508 cystic fibrosis transmembrane conductance regulator. Mol Biol Cell 15: 2684-2696.
24. Griesenbach U, Alton EW, (2011). Current status and future directions of gene and cell therapy for cystic fibrosis. BioDrugs 25: 77-88.
25. Grove DE, Rosser MF, Ren HY, Naren AP, Cyr DM, (2009). Mechanisms for rescue of correctable folding defects in CFTRDelta F508. Mol Biol Cell 20: 4059-4069.
26. Guerra L, Fanelli T, Favia M, Riccardi SM, Busco G, Cardone RA, 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.
27. Guggino WB, Stanton BA, (2006). New insights into cystic fibrosis: molecular switches that regulate CFTR. Nat Rev Mol Cell Biol 7: 426-436.
28. Haggie PM, Kim JK, Lukacs GL, Verkman AS, (2006). Tracking of quantum dot-labeled CFTR shows near immobilization by C-terminal PDZ interactions. Mol Biol Cell 17: 4937-4945.
29. Huang P, Lazarowski ER, Tarran R, Milgram SL, Boucher RC, Stutts MJ, (2001). Compartmentalized autocrine signaling to cystic fibrosis transmembrane conductance regulator at the apical membrane of airway epithelial cells. Proc Natl Acad Sci U S A 98: 14120-14125.
30. Huang P, Gilmore E, Kultgen P, Barnes P, Milgram S, Stutts MJ, (2004). Local regulation of cystic fibrosis transmembrane regulator and epithelial sodium channel in airway epithelium. Proc Am Thorac Soc 1: 33-37.
31. Joo NS, Irokawa T, Robbins RC, Wine JJ, (2006). Hyposecretion, not hyperabsorption, is the basic defect of cystic fibrosis airway glands. J Biol Chem 281: 7392-7398.
32. Krauss RD, Bubien JK, Drumm ML, Zheng T, Peiper SC, Collins FS, et al. (1992). Transfection of wild-type CFTR into cystic fibrosis lymphocytes restores chloride conductance at G1 of the cell cycle. EMBO J 11: 875-883.
33. Kwon SH, Pollard H, Guggino WB, (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.
34. Li C, Dandridge KS, Di A, Marrs KL, Harris EL, Roy K, et al. (2005). Lysophosphatidic acid inhibits cholera toxin-induced secretory diarrhea through CFTR-dependent protein interactions. J Exp Med 202: 975-986.
35. Li C, Krishnamurthy PC, Penmatsa H, Marrs KL, Wang XQ, Zaccolo M, et al. (2007). Spatiotemporal coupling of cAMP transporter to CFTR chloride channel function in the gut epithelia. Cell 131: 940-951.
36. Li C, Naren AP, (2010). CFTR chloride channel in the apical compartments: spatiotemporal coupling to its interacting partners. Integr Biol (Camb) 2: 161-177.
37. Li C, Ramjeesingh M, Reyes E, Jensen T, Chang X, Rommens JM, et al. (1993). The cystic fibrosis mutation (delta F508) does not influence the chloride channel activity of CFTR. Nat Genet 3: 311-316.
38. Liu S, Veilleux A, Zhang L, Young A, Kwok E, Laliberte F, et al. (2005). Dynamic activation of cystic fibrosis transmembrane conductance regulator by type 3 and type 4D phosphodiesterase inhibitors. J Pharmacol Exp Ther 314: 846-854.
39. Lukacs GL, Verkman AS, (2012). CFTR: folding, misfolding and correcting the DeltaF508 conformational defect. Trends Mol Med 18: 81-91.
40. Lukacs GL, Segal G, Kartner N, Grinstein S, Zhang F, (1997). Constitutive internalization of cystic fibrosis transmembrane conductance regulator occurs via clathrin-dependent endocytosis and is regulated by protein phosphorylation. Biochem J 328 (Pt 2): 353-361.
41. Matsui H, Grubb BR, Tarran R, Randell SH, Gatzy JT, Davis CW, et al. (1998). Evidence for periciliary liquid layer depletion, not abnormal ion composition, in the pathogenesis of cystic fibrosis airways disease. Cell 95: 1005-1015.
42. Mongillo M, McSorley T, Evellin S, Sood A, Lissandron V, Terrin A, et al. (2004). Fluorescence resonance energy transfer-based analysis of cAMP dynamics in live neonatal rat cardiac myocytes reveals distinct functions of compartmentalized phosphodiesterases. Circ Res 95: 67-75.
43. Mongillo M, Tocchetti CG, Terrin A, Lissandron V, Cheung YF, Dostmann WR, et al. (2006). Compartmentalized phosphodiesterase-2 activity blunts beta-adrenergic cardiac inotropy via an NO/cGMP-dependent pathway. Circ Res 98: 226-234.
44. Monterisi S, Favia M, Guerra L, Cardone RA, Marzulli D, Reshkin SJ, et al. (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.
45. Moyer BD, Duhaime M, Shaw C, Denton J, Reynolds D, Karlson KH, 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.
46. Naren AP, Cobb B, Li C, Roy K, Nelson D, Heda GD, et al. (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.
47. Oliveira RF, Terrin A, Di Benedetto G, Cannon RC, Koh W, Kim M, et al. (2010). The role of type 4 phosphodiesterases in generating microdomains of cAMP: large scale stochastic simulations. Plos ONE 5: e11725.
48. Pedemonte N, Sonawane ND, Taddei A, Hu J, Zegarra-Moran O, Suen YF, 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.
49. Pedemonte N, Tomati V, Sondo E, Galietta LJ, (2010). Influence of cell background on pharmacological rescue of mutant CFTR. Am J Physiol Cell Physiol 298: C866-C874.
50. Powers ET, Morimoto RI, Dillin A, Kelly JW, Balch WE, (2009). Biological and chemical approaches to diseases of proteostasis deficiency. Annu Rev Biochem 78: 959-991.
51. Prat AG, Xiao YF, Ausiello DA, Cantiello HF, (1995). cAMP-independent regulation of CFTR by the actin cytoskeleton. Am J Physiol 268: C1552-C1561.
52. Prat AG, Cunningham CC, Jackson GR, JR, Borkan SC, Wang Y, Ausiello DA, et al. (1999). Actin filament organization is required for proper cAMP-dependent activation of CFTR. Am J Physiol 277: C1160-C1169.
53. Proesmans M, Vermeulen F, De Boeck K, (2008). What's new in cystic fibrosis? From treating symptoms to correction of the basic defect. Eur J Pediatr 167: 839-849.
54. Rich TC, Fagan KA, Nakata H, Schaack J, Cooper DM, Karpen JW, (2000). Cyclic nucleotide-gated channels colocalize with adenylyl cyclase in regions of restricted cAMP diffusion. J Gen Physiol 116: 147-161.
55. Rich TC, Fagan KA, Tse TE, Schaack J, Cooper DM, Karpen JW, (2001). A uniform extracellular stimulus triggers distinct cAMP signals in different compartments of a simple cell. Proc Natl Acad Sci U S A 98: 13049-13054.
56. Riordan JR, Rommens JM, Kerem B, Alon N, Rozmahel R, Grzelczak Z, et al. (1989). Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science 245: 1066-1073. [Erratum, Science 1989;245:1437.].
57. Rowe SM, Pyle LC, Jurkevante A, Varga K, Collawn J, Sloane PA, et al. (2010). DeltaF508 CFTR processing correction and activity in polarized airway and non-airway cell monolayers. Pulm Pharmacol Ther 23: 268-278.
58. Schreiber R, Nitschke R, Greger R, Kunzelmann K, (1999). The cystic fibrosis transmembrane conductance regulator activates aquaporin 3 in airway epithelial cells. J Biol Chem 274: 11811-11816.
59. Sharma M, Benharouga M, Hu W, Lukacs GL, (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.
60. Sharma M, Pampinella F, Nemes C, Benharouga M, So J, Du K, et al. (2004). Misfolding diverts CFTR from recycling to degradation: quality control at early endosomes. J Cell Biol 164: 923-933.
61. Singh AK, Riederer B, Krabbenhoft A, Rausch B, Bonhagen J, Lehmann U, et al. (2009). Differential roles of NHERF1, NHERF2, and PDZK1 in regulating CFTR-mediated intestinal anion secretion in mice. J Clin Invest 119: 540-550.
62. Sun F, Hug MJ, Bradbury NA, Frizzell RA, (2000). Protein kinase A associates with cystic fibrosis transmembrane conductance regulator via an interaction with ezrin. J Biol Chem 275: 14360-14366.
63. Swiatecka-Urban A, Boyd C, Coutermarsh B, Karlson KH, Barnaby R, Aschenbrenner L, et al. (2004). Myosin VI regulates endocytosis of the cystic fibrosis transmembrane conductance regulator. J Biol Chem 279: 38025-38031.
64. Swiatecka-Urban A, Brown A, Moreau-Marquis S, Renuka J, Coutermarsh B, Barnaby R, 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.
65. Taouil K, Hinnrasky J, Hologne C, Corlieu P, Klossek JM, Puchelle E, (2003). Stimulation of beta 2-adrenergic receptor increases cystic fibrosis transmembrane conductance regulator expression in human airway epithelial cells through a cAMP/protein kinase A-independent pathway. J Biol Chem 278: 17320-17327.
66. Terrin A, Di Benedetto G, Pertegato V, Cheung YF, Baillie G, Lynch MJ, 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.
67. Thelin WR, Kesimer M, Tarran R, Kreda SM, Grubb BR, Sheehan JK, et al. (2005). The cystic fibrosis transmembrane conductance regulator is regulated by a direct interaction with the protein phosphatase 2A. J Biol Chem 280: 41512-41520.
68. Tousson A, Fuller CM, Benos DJ, (1996). Apical recruitment of CFTR in T-84 cells is dependent on cAMP and microtubules but not Ca2+ or microfilaments. J Cell Sci 109 (Pt 6): 1325-1334.
69. Van Goor F, Straley KS, Cao D, Gonzalez J, Hadida S, Hazlewood A, et al. (2006). Rescue of DeltaF508-CFTR trafficking and gating in human cystic fibrosis airway primary cultures by small molecules. Am J Physiol Lung Cell Mol Physiol 290: L1117-L1130.
70. Van Goor F, Hadida S, Grootenhuis PD, Burton B, Stack JH, Straley KS, et al. (2011). Correction of the F508del-CFTR protein processing defect in vitro by the investigational drug VX-809. Proc Natl Acad Sci U S A 108: 18843-18848.
71. Wang F, Zeltwanger S, Hu S, Hwang TC, (2000). Deletion of phenylalanine 508 causes attenuated phosphorylation-dependent activation of CFTR chloride channels. J Physiol 524: 637-648.
72. Weinman EJ, Minkoff C, Shenolikar S, (2000). Signal complex regulation of renal transport proteins: NHERF and regulation of NHE3 by PKA. Am J Physiol Renal Physiol 279: F393-F399.
73. Wong W, Scott JD, (2004). AKAP signalling complexes: focal points in space and time. Nat Rev Mol Cell Biol 5: 959-970.
74. Yang H, Shelat AA, Guy RK, Gopinath VS, Ma T, Du K, et al. (2003). Nanomolar affinity small molecule correctors of defective Delta F508-CFTR chloride channel gating. J Biol Chem 278: 35079-35085.
75. Yonemura S, Matsui T, 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.
76. Zaccolo M, (2009). cAMP signal transduction in the heart: understanding spatial control for the development of novel therapeutic strategies. Br J Pharmacol 158: 50-60.
77. Zaccolo M, (2011). Spatial control of cAMP signalling in health and disease. Curr Opin Pharmacol 11: 649-655.
78. Zaccolo M, Pozzan T, (2002). Discrete microdomains with high concentration of cAMP in stimulated rat neonatal cardiac myocytes. Science 295: 1711-1715.
79. Zeitlin PL, (2000). Pharmacologic restoration of delta F508 CFTR-mediated chloride current. Kidney Int 57: 832-837.