VIP-dependent increase in f508del-CFTR membrane localization is mediated by PKCε

American Journal of Physiology - Cell Physiology

Volumn 301, Issue 1, 2011, Pages

  Alcolado, Nicole ^a   Conrad, Dustin J ^a   Rafferty, Sara ^a   Chappe, Frédéric G ^a   Chappe, Valérie M ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Cystic fibrosis; Cystic fibrosis transmembrane conductance regulator chloride channel; Membrane insertion; Protein kinase c

Indexed keywords

CARNITINE PALMITOYLTRANSFERASE; MUTANT PROTEIN; PROTEIN KINASE C; PROTEIN KINASE C ALPHA; PROTEIN KINASE C BETA; PROTEIN KINASE C BETA1; PROTEIN KINASE C BETA2; PROTEIN KINASE C DELTA; PROTEIN KINASE C EPSILON; PROTEIN KINASE C ETA; PROTEIN KINASE C GAMMA; PROTEIN KINASE C INHIBITOR; PROTEIN KINASE C IOTA; PROTEIN KINASE C MU; PROTEIN KINASE C NU; PROTEIN KINASE C THETA; PROTEIN KINASE C ZETA; SMALL INTERFERING RNA; TRANSMEMBRANE CONDUCTANCE REGULATOR; UNCLASSIFIED DRUG; VASOACTIVE INTESTINAL POLYPEPTIDE; VASOACTIVE INTESTINAL POLYPEPTIDE RECEPTOR;

ARTICLE; BIOASSAY; BIOTINYLATION; CELL MEMBRANE TRANSPORT; CELL STRAIN BHK; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYSTIC FIBROSIS; GENE DELETION; HUMAN; HUMAN CELL; IC 50; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; INHIBITION KINETICS; MEMBRANE BIOLOGY; MEMBRANE INSERTION; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SENSITIVITY ANALYSIS; WILD TYPE;

ANIMALS; BIOTINYLATION; CELL LINE; CELL MEMBRANE; CRICETINAE; CYSTIC FIBROSIS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; EPITHELIAL CELLS; HUMANS; IMMUNOBLOTTING; IODIDES; MICROSCOPY, CONFOCAL; MUTATION; POLYMERASE CHAIN REACTION; PROTEIN ISOFORMS; PROTEIN KINASE C-EPSILON; RECEPTORS, VASOACTIVE INTESTINAL PEPTIDE; RNA INTERFERENCE; RNA, SMALL INTERFERING; TETRADECANOYLPHORBOL ACETATE; VASOACTIVE INTESTINAL PEPTIDE;

CRICETINAE;

EID: 79959832527     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00568.2009     Document Type: Article

References (60)

1. Ameen NA, Marino C, Salas PJ. cAMP-dependent exocytosis and vesicle traffic regulate CFTR and fluid transport in rat jejunum in vivo. Am J Physiol Cell Physiol 284: C429-C438, 2003.
2. Auerbach M, Liedtke CM. Role of the scaffold protein RACK1 in apical expression of CFTR. Am J Physiol Cell Physiol 293: C294-C304, 2007.
3. Bajnath RB, Dekker K, De Jonge HR, Groot JA. Chloride secretion induced by phorbol dibutyrate and forskolin in the human colonic carcinoma cell line HT-29Cl.19A is regulated by different mechanisms. Pflügers Arch 430: 705-712, 1995.
4. Bajnath RB, Groot JA, De Jonge HR, Kansen M, Bijman J. Synergistic activation of non-rectifying small-conductance chloride channels by forskolin and phorbol esters in cell-attached patches of the human colon carcinoma cell line HT-29cl.19A. Pflügers Arch 425: 100-108, 1993.
5. Bajnath RB, van den Berghe N, De Jonge HR, Groot JA. Activation of ion transport by combined effects of ionomycin, forskolin and phorbol ester on cultured HT-29cl.19A human colonocytes. Pflügers Arch 425: 90-99, 1993.
6. Barthelson RA, Jacoby DB, Widdicombe JH. Regulation of chloride secretion in dog tracheal epithelium by protein kinase C. Am J Physiol Cell Physiol 253: C802-C808, 1987.
7. Becq F, Auzanneau C, Norez C, Dérand R, Bulteau-Pignoux L. Radiotracer flux method to study CFTR channel activity: regulation, pharmacology and drug discovery. European Working Group on CFTR Expression D5: 1-13, 2003.
8. Bradbury NA, Bridges RJ. Role of membrane trafficking in plasma membrane solute transport. Am J Physiol Cell Physiol 267: C1-C24, 1994.
9. Bradbury NA, Cohn JA, Venglarik CJ, Bridges RJ. Biochemical and biophysical identification of cystic fibrosis transmembrane conductance regulator chloride channels as components of endocytic clathrin-coated vesicles. J Biol Chem 269: 8296-8302, 1994.
10. Bradbury NA, Jilling T, Kirk KL, Bridges RJ. Regulated endocytosis in a chloride secretory epithelial cell line. Am J Physiol Cell Physiol 262: C752-C759, 1992.
11. Chappe FG, Loewen ME, Hanrahan JW, Chappe VM. VIP increases CFTR levels in the apical membrane of Calu-3 cells through a PKCdependent mechanism. J Pharmacol Exp Ther 327: 226-238, 2008.
12. Chappe V, Hinkson DA, Howell LD, Evagelidis A, Liao J, Chang XB, Riordan JR, Hanrahan JW. Stimulatory and inhibitory protein kinase C consensus sequences regulate the cystic fibrosis transmembrane conductance regulator. Proc Natl Acad Sci USA 101: 390-395, 2004.
13. Chappe V, Hinkson DA, Zhu T, Chang XB, Riordan JR, Hanrahan JW. Phosphorylation of protein kinase C sites in NBD1 and the R domain control CFTR channel activation by PKA. J Physiol 548: 39-52, 2003.
14. Cheng SH, Gregory RJ, Marshall J, Paul S, Souza DW, White GA, O'Riordan CR, Smith AE. Defective intracellular transport and processing of CFTR is the molecular basis of most cystic fibrosis. Cell 63: 827-834, 1990.
15. Dechecchi MC, Rolfini R, Tamanini A, Gamberi C, Berton G, Cabrini G. Effect of modulation of protein kinase C on the cAMP-dependent chloride conductance in T84 cells. FEBS Lett 311: 25-28, 1992.
16. Dempsey EC, Newton AC, Mochly-Rosen D, Fields AP, Reyland ME, Insel PA, Messing RO. Protein kinase C isozymes and the regulation of diverse cell responses. Am J Physiol Lung Cell Mol Physiol 279: L429-L438, 2000.
17. Derand R, Montoni A, Bulteau-Pignoux L, Janet T, Moreau B, Muller JM, Becq F. Activation of VPAC1 receptors by VIP and PACAP-27 in human bronchial epithelial cells induces CFTR-dependent chloride secretion. Br J Pharmacol 141: 698-708, 2004.
18. Fondacaro JD, Henderson LS. Evidence for protein kinase C as a regulator of intestinal electrolyte transport. Am J Physiol Gastrointest Liver Physiol 249: G422-G426, 1985.
19. Gadsby DC, Vergani P, Csanady L. The ABC protein turned chloride channel whose failure causes cystic fibrosis. Nature 440: 477-483, 2006.
20. Seavilleklein G, Amer N, Evagelidis A, Chappe F, Hanrahan JW, Chappe V. PKC phosphorylation modulates PKA-dependent binding of the R domain to other domains of CFTR. Am J Physiol Cell Physiol 295: C1366-C1375, 2008.
21. Gallegos LL, Newton AC. Spatiotemporal dynamics of lipid signaling: protein kinase C as a paradigm. IUBMB Life 60: 782-789, 2008.
22. Groneberg DA, Rabe KF, Fischer A. Novel concepts of neuropeptidebased drug therapy: vasoactive intestinal polypeptide and its receptors. Eur J Pharmacol 533: 182-194, 2006.
23. Hanrahan JW, Gentzsch M, Riordan JR. The cystic fibrosis transmembrane conductance regulator [ABCC7]. In: ABC Proteins, edited by Holland B, Higgins CF, Kuchler K, and Cole SPC, New York: Elsevier Science, 2003, p. 589-618.
24. Heinz-Erian P, Dey RD, Flux M, Said SI. Deficient vasoactive intestinal peptide innervation in the sweat glands of cystic fibrosis patients. Science 229: 1407-1408, 1985.
25. Helenius A, Aebi M. Roles of N-linked glycans in the endoplasmic reticulum. Annu Rev Biochem 73: 1019-1049, 2004.
26. Ianowski JP, Choi JY, Wine JJ, Hanrahan JW. Mucus secretion by single tracheal submucosal glands from normal and cystic fibrosis transmembrane conductance regulator knockout mice. J Physiol 580: 301-314, 2007.
27. Jefferson DM, Valentich JD, Marini FC, Grubman SA, Iannuzzi MC, Dorkin HL, Li M, Klinger KW, Welsh MJ. Expression of normal and cystic fibrosis phenotypes by continuous airway epithelial cell lines. Am J Physiol Lung Cell Mol Physiol 259: L496-L505, 1990.
28. Jia Y, Mathews CJ, Hanrahan JW. Phosphorylation by protein kinase C is required for acute activation of cystic fibrosis transmembrane conductance regulator by protein kinase A. J Biol Chem 272: 4978-4984, 1997.
29. Kartner N, Augustinas O, Jensen TJ, Naismith AL, Riordan JR. Mislocalization of delta F508 CFTR in cystic fibrosis sweat gland. Nat Genet 1: 321-327, 1992.
30. Koh DS, Moody MW, Nguyen TD, Hille B. Regulation of exocytosis by protein kinases and Ca(2) in pancreatic duct epithelial cells. J Gen Physiol 116: 507-520, 2000.
31. Laburthe M, Couvineau A, Tan V. Class II G protein-coupled receptors for VIP and PACAP: structure, models of activation and pharmacology. Peptides 28: 1631-1639, 2007.
32. Lehrich RW, Aller SG, Webster P, Marino CR, Forrest JN, Jr. Vasoactive intestinal peptide, forskolin, and genistein increase apical CFTR trafficking in the rectal gland of the spiny dogfish, Squalus acanthias. Acute regulation of CFTR trafficking in an intact epithelium. J Clin Invest 101: 737-745, 1998.
33. Liedtke CM, Cody D, Cole TS. Differential regulation of Cl- transport proteins by PKC in Calu-3 cells. Am J Physiol Lung Cell Mol Physiol 280: L739-L747, 2001.
34. Liedtke CM, Cole TS. Antisense oligonucleotide to PKC-epsilon alters cAMP-dependent stimulation of CFTR in Calu-3 cells. Am J Physiol Cell Physiol 275: C1357-C1364, 1998.
35. Liedtke CM, Raghuram V, Yun CC, Wang X. Role of a PDZ1 domain of NHERF1 in the binding of airway epithelial RACK1 to NHERF1. Am J Physiol Cell Physiol 286: C1037-C1044, 2004.
36. Lu Z, Liu D, Hornia A, Devonish W, Pagano M, Foster DA. Activation of protein kinase C triggers its ubiquitination and degradation. Mol Cell Biol 18: 839-845, 1998.
37. Lukacs GL, Chang XB, Bear C, Kartner N, Mohamed A, Riordan JR, Grinstein S. 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, 1993.
38. Lukacs GL, Segal G, Kartner N, Grinstein S, Zhang F. Constitutive internalization of cystic fibrosis transmembrane conductance regulator occurs via clathrin-dependent endocytosis and is regulated by protein phosphorylation. Biochem J 328: 353-361, 1997.
39. Nishizuka Y. Intracellular signaling by hydrolysis of phospholipids and activation of protein kinase C. Science 258: 607-614, 1992.
40. Prince LS, Tousson A, Marchase RB. Cell surface labeling of CFTR in T84 cells. Am J Physiol Cell Physiol 264: C491-C498, 1993.
41. Prince LS, Workman RB, Jr, Marchase RB. Rapid endocytosis of the cystic fibrosis transmembrane conductance regulator chloride channel. Proc Natl Acad Sci USA 91: 5192-5196, 1994.
42. Quinton PM. Cystic fibrosis: a disease in electrolyte transport. FASEB J 4: 2709-2717, 1990.
43. Rafferty S, Alcolado N, Norez C, Chappe F, Pelzer S, Becq F, Chappe V. Rescue of functional F508del-CFTR by VIP in the human nasal epithelial cell line JME/CF15. J Pharmacol Exp Ther 331: 2-13, 2009.
44. Reubi JC. In vitro evaluation of VIP/PACAP receptors in healthy and diseased human tissues. Clinical implications. Ann NY Acad Sci 921: 1-25, 2000.
45. Reyland ME. Protein kinase C isoforms: multi-functional regulators of cell life and death. Front Biosci 14: 2386-2399, 2009.
46. Rommens JM, Zengerling-Lentes S, Kerem B, Melmer G, Buchwald M, Tsui LC. Physical localization of two DNA markers closely linked to the cystic fibrosis locus by pulsed-field gel electrophoresis. Am J Hum Genet 45: 932-941, 1989.
47. Said SI. The vasoactive intestinal peptide gene is a key modulator of pulmonary vascular remodeling and inflammation. Ann NY Acad Sci 1144: 148-153, 2008.
48. Said SI. The discovery of VIP: initially looked for in the lung, isolated from intestine, and identified as a neuropeptide. Peptides 28: 1620-1621, 2007.
49. Said SI. Vasoactive intestinal polypeptide (VIP) in asthma. Ann NY Acad Sci 629: 305-318, 1991.
50. Said SI. Vasoactive intestinal polypeptide (VIP) in lung function and disease. Nihon Kyobu Shikkan Gakkai Zasshi 29: 1525-1531, 1991.
51. Said SI. VIP as a modulator of lung inflammation and airway constriction. Am Rev Respir Dis 143: S22-S24, 1991.
52. Savage MV, Brengelmann GL, Buchan AM, Freund PR. Cystic fibrosis, vasoactive intestinal polypeptide, and active cutaneous vasodilation. J Appl Physiol 69: 2149-2154, 1990.
53. Sharma M, Benharouga M, Hu W, Lukacs GL. 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, 2001.
54. Sullivan SK, Swamy K, Field M. cAMP-activated C1 conductance is expressed in Xenopus oocytes by injection of shark rectal gland mRNA. Am J Physiol Cell Physiol 260: C664-C669, 1991.
55. Tabcharani JA, Chang XB, Riordan JR, Hanrahan JW. Phosphorylation-regulated Cl- channel in CHO cells stably expressing the cystic fibrosis gene. Nature 352: 628-631, 1991.
56. Ward CL, Kopito RR. Intracellular turnover of cystic fibrosis transmembrane conductance regulator. Inefficient processing and rapid degradation of wild-type and mutant proteins. J Biol Chem 269: 25710-25718, 1994.
57. Webster P, Vanacore L, Nairn AC, Marino CR. Subcellular localization of CFTR to endosomes in a ductal epithelium. Am J Physiol Cell Physiol 267: C340-C348, 1994.
58. Welsh MJ, Smith AE. Molecular mechanisms of CFTR chloride channel dysfunction in cystic fibrosis. Cell 73: 1251-1254, 1993.
59. Wine JJ, Joo NS. Submucosal glands and airway defense. Proc Am Thorac Soc 1: 47-53, 2004.
60. Winpenny JP, McAlroy HL, Gray MA, Argent BE. Protein kinase C regulates the magnitude and stability of CFTR currents in pancreatic duct cells. Am J Physiol Cell Physiol 268: C823-C828, 1995.