Vasoactive intestinal peptide increases cystic fibrosis transmembrane conductance regulator levels in the apical membrane of Calu-3 cells through a protein kinase C-dependent mechanism

Journal of Pharmacology and Experimental Therapeutics

Volumn 327, Issue 1, 2008, Pages 226-238

  Chappe, Frédéric ^a   Loewen, Matthew E ^b,c   Hanrahan, John W ^b   Chappe, Valérie ^a,d  

^a DALHOUSIE UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^d Department of Physiology and Biophysics ^*  (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BISINDOLYLMALEIMIDE; BISINDOLYLMALEIMIDE X; CHELERYTHRINE; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE INHIBITOR; FORSKOLIN; N [2 (4 BROMOCINNAMYLAMINO)ETHYL] 5 ISOQUINOLINESULFONAMIDE; PHORBOL ESTER; PROTEIN KINASE C; PROTEIN KINASE C INHIBITOR; TANNIN; TRANSMEMBRANE CONDUCTANCE REGULATOR; UNCLASSIFIED DRUG; VASOACTIVE INTESTINAL POLYPEPTIDE;

ARTICLE; BIOTINYLATION; CELL LYSATE; CELL MEMBRANE; CONTROLLED STUDY; ENDOCYTOSIS; ENZYME MECHANISM; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

1-METHYL-3-ISOBUTYLXANTHINE; BENZOPHENANTHRIDINES; CELLS, CULTURED; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; ENDOCYTOSIS; HUMANS; INDOLES; MALEIMIDES; PROTEIN KINASE C; TETRADECANOYLPHORBOL ACETATE; VASOACTIVE INTESTINAL PEPTIDE;

EID: 52649179496     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.108.141143     Document Type: Article

References (38)

1. Abdullah LH, Bundy JT, Ehre C, and Davis CW (2003) Mucin secretion and PKC isoforms in SPOC1 goblet cells: differential activation by purinergic agonist and PMA. Am J Physiol Lung Cell Mol Physiol 285:L149-L160.
2. Ameen N and Apodaca G (2007) Defective CFTR apical endocytosis and enterocyte brush border in myosin VI-deficient mice. Traffic 8:998-1006.
3. Bajnath RB, Dekker K, De Jonge HR, and Groot JA (1995) Chloride secretion induced by phorbol dibutyrate and forskolin in the human colonic carcinoma cell line HT-29Cl.19A is regulated by different mechanisms. Pflugers Arch 430:705-712.
4. Bajnath RB, Groot JA, De Jonge HR, Kansen M, and Bijman J (1993) 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. Pflugers Arch 425:100-108.
5. Barthelson RA, Jacoby DB, and Widdicombe JH (1987) Regulation of chloride secretion in dog tracheal epithelium by protein kinase C. Am J Physiol Cell Physiol 253:C802-C808.
6. Becq F, Auzanneau C, Norez C, Dérand R, and Bulteau-Pignoux L (text citation) (2003) Radiotracer flux method to study CFTR channel activity: regulation, pharmacology and drug discovery. European Working Group on CFTR Expression Online Forum D. 5. EFFLUX ASSAYS:1-13.
7. Berger JT, Voynow JA, Peters KW, and Rose MC (1999) Respiratory carcinoma cell lines. MUC genes and glycoconjugates. Am J Respir Cell Mol Biol 20:500-510.
8. Bertrand CA and Frizzell RA (2003) The role of regulated CFTR trafficking in epithelial secretion. Am J Physiol Cell Physiol 285:C1-C18.
9. Bradbury NA and Bridges RJ (1992) Endocytosis is regulated by protein kinase A, but not protein kinase C in a secretory epithelial cell line. Biochem Biophys Res Commun 184:1173-1180.
10. Bradbury NA, Cohn JA, Venglarik CJ, and Bridges RJ (1994) 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.
11. Bradbury NA, Jilling T, Kirk KL, and Bridges RJ (1992) Regulated endocytosis in a chloride secretory epithelial cell line. Am J Physiol Cell Physiol 262:C752-C759.
12. Chappe F, Loewen ME, Hanrahan JW, and Chappe V (2006) VIP increases insertion of active CFTR channels in the apical membrane of Calu-3 cells by stimulating PKC signaling pathway. Pediatr Pulmonol 41(S29):210.
13. Chappe V, Hinkson DA, Howell LD, Evagelidis A, Liao J, Chang XB, Riordan JR, and Hanrahan JW (2004) Stimulatory and inhibitory protein kinase C consensus sequences regulate the cystic fibrosis transmembrane conductance regulator. Proc Natl Acad Sci U S A 101:390-395.
14. Chappe V, Hinkson DA, Zhu T, Chang XB, Riordan JR, and Hanrahan JW (2003) Phosphorylation of protein kinase C sites in NBD1 and the R domain control CFTR channel activation by PKA. J Physiol 548:39-52.
15. Chappe V, Irvine T, Liao J, Evagelidis A, and Hanrahan JW (2005) Phosphorylation of CFTR by PKA promotes binding of the regulatory domain. EMBO J 24:2730-2740.
16. Chen P, Hwang TC, and Gillis KD (2001) The relationship between cAMP, Ca(2)+, and transport of CFTR to the plasma membrane. J Gen Physiol 118:135-144.
17. Choi JY, Joo NS, Krouse ME, Wu JV, Robbins RC, Ianowski JP, Hanrahan JW, and Wine JJ (2007) Synergistic airway gland mucus secretion in response to vasoactive intestinal peptide and carbachol is lost in cystic fibrosis. J Clin Invest 117:3118-3127.
18. Davies SP, Reddy H, Caivano M, and Cohen P (2000) Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J 351:95-105.
19. DérandR, Montoni A, Bulteau-Pignoux L, Janet T, Moreau B, Muller JM, and Becq F (2004) 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.
20. Gadsby DC, Vergani P, and Csana'dy L (2006) The ABC protein turned chloride channel whose failure causes cystic fibrosis. Nature 440:477-483.
21. Ganeshan R, Nowotarski K, Di A, Nelson DJ, and 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.
22. Ianowski JP, Choi JY, Wine JJ, and Hanrahan JW (2007) Mucus secretion by single tracheal submucosal glands from normal and cystic fibrosis transmembrane conductance regulator knockout mice. J Physiol 580:301-314.
23. Jia Y, Mathews CJ, and Hanrahan JW (1997) 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.
24. Kazanietz MG (2002) Novel "nonkinase" phorbol ester receptors: The C1 domain connection. Mol Pharmacol 61:759-767.
25. Koh DS, Moody MW, Nguyen TD, and Hille B (2000) Regulation of exocytosis by protein kinases and Ca(2+) in pancreatic duct epithelial cells. J Gen Physiol 116:507-520.
26. Laburthe M, Couvineau A, and Tan V (2007) Class II G protein-coupled receptors for VIP and PACAP: structure, models of activation and pharmacology. Peptides 28:1631-1639.
27. - secretion via CFTR in Calu-3 airway epithelial cells. Am J Physiol Cell Physiol 275:C913-C920.
28. Lukacs GL, Segal G, Kartner N, Grinstein S, and 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.
29. Prince LS, Workman RB Jr, and Marchase RB (1994) Rapid endocytosis of the cystic fibrosis transmembrane conductance regulator chloride channel. Proc Natl Acad Sci U S A 91:5192-5196.
30. Rhee JS, Betz A, Pyott S, Reim K, Varoqueaux F, Augustin I, Hesse D, Südhof TC, Takahashi M, Rosenmund C, et al. (2002) Beta phorbol ester- and diacylglycerol-induced augmentation of transmitter release is mediated by Munc13s and not by PKCs. Cell 108:121-133.
31. Riordan JR, Rommens JM, Kerem B, Alon N, Rozmahel R, Grzelczak Z, Zielenski J, Lok S, Plavsic N, and Chou JL (1989) Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science 245:1066-1073.
32. Sullivan SK, Swamy K, and Field M (1991) cAMP-activated C1 conductance is expressed in Xenopus oocytes by injection of shark rectal gland mRNA. Am J Physiol Cell Physiol 260:C664-C669.
33. - channel in CHO cells stably expressing the cystic fibrosis gene. Nature 352:628-631.
34. Thelin WR, Chen Y, Gentzsch M, Kreda SM, Sallee JL, Scarlett CO, Borchers CH, Jacobson K, Stutts MJ, and Milgram SL (2007) Direct interaction with filamins modulates the stability and plasma membrane expression of CFTR. J Clin Invest 117:364-374.
35. Thiagarajah JR and Verkman AS (2003) CFTR pharmacology and its role in intestinal fluid secretion. Curr Opin Pharmacol 3:594-599.
36. Varga K, Jurkuvenaite A, Wakefield J, Hong JS, Guimbellot JS, Venglarik CJ, Niraj A, Mazur M, Sorscher EJ, Collawn JF, et al. (2004) Efficient intracellular processing of the endogenous cystic fibrosis transmembrane conductance regulator in epithelial cell lines. J Biol Chem 279:22578-22584.
37. Wine JJ and Joo NS (2004) Submucosal glands and airway defense. Proc Am Thorac Soc 1:47-53.
38. Winpenny JP, McAlroy HL, Gray MA, and Argent BE (1995) Protein kinase C regulates the magnitude and stability of CFTR currents in pancreatic duct cells. Am J Physiol Cell Physiol 268:C823-C828.