Purinergic regulation of CFTR and Ca2+-activated Cl-channels and K+ channels in human pancreatic duct epithelium

American Journal of Physiology - Cell Physiology

Volumn 304, Issue 7, 2013, Pages

  Wang, Jing ^a   Haanes, Kristian A ^a   Novak, Ivana ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

ANO1; HCO3 transport; IK; KCa3.1; K+transport; P2Y2; TMEM16A

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM ACTIVATED CHLORIDE CHANNEL; CLOTRIMAZOLE; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; NIFLUMIC ACID; POTASSIUM CHANNEL; PURINERGIC RECEPTOR; CALCIUM; CALCIUM ACTIVATED POTASSIUM CHANNEL; CHLORIDE CHANNEL; PURINERGIC P2X RECEPTOR; PURINERGIC P2Y RECEPTOR; URIDINE TRIPHOSPHATE;

ARTICLE; CHLORIDE TRANSPORT; CONTROLLED STUDY; EPITHELIUM; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; INHIBITION KINETICS; MEMBRANE CONDUCTANCE; PANCREAS DUCT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; REAL TIME POLYMERASE CHAIN REACTION; RNA ANALYSIS; SIGNAL TRANSDUCTION; CELL LINE; CYTOLOGY; DRUG EFFECT; EPITHELIUM CELL; GENE EXPRESSION REGULATION; GENETICS; METABOLISM;

RODENTIA;

ADENOSINE TRIPHOSPHATE; CALCIUM; CELL LINE; CHLORIDE CHANNELS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; HUMANS; PANCREATIC DUCTS; POTASSIUM CHANNELS, CALCIUM-ACTIVATED; RECEPTORS, PURINERGIC P2X; RECEPTORS, PURINERGIC P2Y; URIDINE TRIPHOSPHATE;

MLCS; MLOWN;

EID: 84878219975     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00196.2012     Document Type: Article

References (60)

1. Abbracchio MP, Burnstock G, Boeynaems JM, Barnard EA, Boyer JL, Kennedy C, Knight GE, Fumagalli M, Gachet C, Jacobson KA, Weisman GA. International Union of Pharmacology LVIII: update on the P2Y G protein-coupled nucleotide receptors: from molecular mechanisms and pathophysiology to therapy. Pharmacol Rev 58: 281-341, 2006.
2. Accurso FJ, Moss RB, Wilmott RW, Anbar RD, Schaberg AE, Dur-ham TA, Ramsey BW, TIGER-1 Investigator Study Group. Denufosol tetrasodium in patients with cystic fibrosis and normal to mildly impaired lung function. Am J Respir Crit Care Med 183: 627-634, 2011.
3. Burnstock G. Pathophysiology and therapeutic potential of purinergic signaling. Pharmacol Rev 58: 58-86, 2006.
4. Caputo A, Caci E, Ferrera L, Pedemonte N, Barsanti C, Sondo E, Pfeffer U, Ravazzolo R, Zegarra-Moran O, Galietta LJ. TMEM16A, a membrane protein associated with calcium-dependent chloride channel activity. Science 322: 590-594, 2008.
5. Chan HC, Cheung WT, Leung PY, Wu LJ, Chew SB, Ko WH, Wong PY. Purinergic regulation of anion secretion by cystic fibrosis pancreatic duct cells. Am J Physiol Cell Physiol 271: C469-C477, 1996.
6. -secretion in a human pancreatic duct cell line (CAPAN-1). J Membr Biol 164: 155-167, 1998.
7. Cuthbert AW. New horizons in the treatment of cystic fibrosis. Br J Pharmacol 163: 173-183, 2011.
8. Deterding R, Retsch-Bogart G, Milgram L, Gibson R, Daines C, Zeitlin PL, Milla C, Marshall B, LaVange L, Engels J, Mathews D, Gorden J, Schaberg A, Williams J, Ramsey B. Safety and tolerability of denufosol tetrasodium inhalation solution, a novel P2Y2 receptor agonist: results of a phase 1/phase 2 multicenter study in mild to moderate cystic fibrosis. Pediatr Pulmonol 39: 339-348, 2005.
9. -secretion by benzimidazolones. II. Coordinate regulation of apical GCl and basolateral GK. Am J Physiol Lung Cell Mol Physiol 271: L785-L795, 1996.
10. Duran C, Thompson CH, Xiao Q, Hartzell HC. Chloride channels: often enigmatic HC, rarely predictable. Annu Rev Physiol 72: 95-121, 2010.
11. Faria D, Schreiber R, Kunzelmann K. CFTR is activated through stimu-lation of purinergic P2Y2 receptors. Pflügers Arch 457: 1373-1380, 2009.
12. Fong P, Argent BE, Guggino WB, Gray MA. Characterization of vectorial chloride transport pathways in the human pancreatic duct ade-nocarcinoma cell line HPAF. Am J Physiol Cell Physiol 285: C433-C445, 2003.
13. -currents by UTP and ATP in CFPAC-1 cells. Pflügers Arch 426: 534-541, 1994.
14. Gray MA, Greenwell JR, Garton AJ, Argent BE. Regulation of maxi-K?channels on pancreatic duct cells by cyclic AMP-dependent phosphorylation. J Membr Biol 115: 203-215, 1990.
15. Gray MA, Winpenny JP, Porteous DJ, Dorin JR, Argent BE. CFTR and calcium-activated chloride currents in pancreatic duct cells of a transgenic CF mouse. Am J Physiol Cell Physiol 266: C213-C221, 1994.
16. Haanes KA, Novak I. ATP storage and uptake by isolated pancreatic zymogen granules. Biochem J 429: 303-311, 2010.
17. -secretion in the mouse jejunum. Am J Physiol Cell Physiol 290: C152-C164, 2006.
18. Hansen MR, Krabbe S, Novak I. Purinergic receptors and calcium signalling in human pancreatic duct cell lines. Cell Physiol Biochem 22: 157-168, 2008.
19. + channel is important for secretion in pancreatic duct cells. Am J Physiol Cell Physiol 303: C151-C159, 2012.
20. Hede SE, Amstrup J, Christoffersen BC, Novak I. Purinoceptors evoke different electrophysiological responses in pancreatic ducts. P2Y inhibits K?conductance, and P2X stimulates cation conductance. J Biol Chem 274: 31784-31791, 1999.
21. +channels differently. Pflügers Arch 450: 429-436, 2005.
22. -reab-sorption in rat submandibular gland. Am J Physiol Regul Integr Comp Physiol 294: R1729-R1736, 2008.
23. -secretion in guinea-pig pancreatic duct. J Physiol 519: 551-558, 1999.
24. Jung J, Nam JH, Park HW, Oh U, Yoon JH, Lee MG. Dynamic modulation of ANO1/TMEM16A. Proc Natl Acad Sci USA 110: 360-365, 2013.
25. 2+ increase determines the type of secretory mechanism activated in dog pancreatic duct epithelial cells. J Physiol 576: 163-178, 2006.
26. Kellerman D, Rossi Mospan A, Engels J, Schaberg A, Gorden J, Smiley L. Denufosol: A review of studies with inhaled P2Y2 agonists that led to Phase 3. Pulm Pharmacol Ther 21: 600-607, 2008.
27. Lazarowski ER, Boucher RC. Purinergic receptors in airway epithelia. Curr Opin Pharmacol 9: 262-267, 2009.
28. -(Ct)method. Methods 25: 402-408, 2001.
29. Luo X, Zheng W, Yan M, Lee MG, Muallem S. Multiple functional P2X and P2Y receptors in the luminal and basolateral membranes of pancreatic duct cells. Am J Physiol Cell Physiol 277: C205-C215, 1999.
30. Marsey LL, Winpenny JP. Bestrophin expression and function in the human pancreatic duct cell line, CFPAC-1. J Physiol 587: 2211-2224, 2009.
31. 2+ -activated Cl?channels by gallotannins as a possible molecular basis for health benefits of red wine and green tea. FASEB J 24: 4178-4186, 2010.
32. -transport in pancreatic duct cells. J Biol Chem 278: 200-207, 2003.
33. Nguyen TD, Meichle S, Kim US, Wong T, Moody MW. P2Y11, a purinergic receptor acting via cAMP, mediates secretion by pancreatic duct epithelial cells. Am J Physiol Gastrointest Liver Physiol 280: G795-G804, 2001.
34. Nguyen TD, Moody MW, Savard CE, Lee SP. Secretory effects of ATP on nontransformed dog pancreatic duct epithelial cells. Am J Physiol Gastrointest Liver Physiol 275: G104-G113, 1998.
35. Nichols KK, Yerxa B, Kellerman DJ. Diquafosol tetrasodium: a novel dry eye therapy. Expert Opin Investig Drugs 13: 47-54, 2004.
36. Novak I. Purinergic receptors in the endocrine and exocrine pancreas. Purinergic Signal 4: 237-253, 2008.
37. Novak I. Purinergic signalling in epithelial ion transport: regulation of secretion and absorption. Acta Physiol (Oxf) 202: 501-522, 2011.
38. Novak I, Greger R. Effect of bicarbonate on potassium conductance of isolated perfused rat pancreatic ducts. Pflügers Arch 419: 76-83, 1991.
39. Novak I, Hede SE, Hansen MR. Adenosine receptors in rat and human pancreatic ducts stimulate chloride transport. Pflügers Arch 456: 437-447, 2008.
40. 2+ -dependent chloride transport. J Biol Chem 284: 28698-28703, 2009.
41. -]i and its role in pancreatic bicarbonate secretion. Gastroenterology 139: 620-631, 2010.
42. Pascua P, Garcia M, Fernandez-Salazar MP, Hernandez-Lorenzo MP, Calvo JJ, Colledge WH, Case RM, Steward MC, San Roman JI. Ducts isolated from the pancreas of CFTR-null mice secrete fluid. Pflügers Arch 459: 203-214, 2009.
43. +channel opener 1-EBIO potentiates residual function of mutant CFTR in rectal biopsies from cystic fibrosis patients. PLos One 6: e24445, 2011.
44. Schoumacher RA, Ram J, Iannuzzi MC, Bradbury NA, Wallace RW, Hon CT, Kelly DR, Schmid SM, Gelder FB, Rado TA. A cystic fibrosis pancreatic adenocarcinoma cell line. Proc Natl Acad Sci USA 87: 4012-4016, 1990.
45. Scudieri P, Caci E, Bruno S, Ferrera L, Schiavon M, Sondo E, Tomati V, Gianotti A, Zegarra-Moran O, Pedemonte N, Rea F, Ravazzolo R, Galietta LJ. Association of TMEM16A chloride channel overexpression with airway goblet cell metaplasia. J Physiol 590: 6141-6155, 2012.
46. Sewell WA, Young JA. Secretion of electrolytes by the pancreas of the anaestetized rat. J Physiol 252: 379-396, 1975.
47. Singh S, Syme CA, Singh AK, Devor DC, Bridges RJ. Benzimidazolone activators of chloride secretion: potential therapeutics for cystic fibrosis and chronic obstructive pulmonary disease. J Pharmacol Exp Ther 296: 600-611, 2001.
48. Sones WR, Davis AJ, Leblanc N, Greenwood IA. Cholesterol depletion alters amplitude and pharmacology of vascular calcium-activated chloride channels. Cardiovasc Res 87: 476-484, 2010.
49. Sorensen CE, Novak I. Visualization of ATP release in pancreatic acini in response to cholinergic stimulus. Use of fluorescent probes and confocal microscopy. J Biol Chem 276: 32925-32932, 2001.
50. Szucs A, Demeter I, Burghardt B, Ovari G, Case RM, Ste ward MC, Varga G. Vectorial bicarbonate transport by Capan-1 cells: a model for human pancreatic ductal secretion. Cell Physiol Biochem 18: 253-264, 2006.
51. -currents in cerebral artery smooth muscle cells. Am J Physiol Heart Circ Physiol 301: H1819-H1827, 2011.
52. Tian Y, Kongsuphol P, Hug M, Ousingsawat J, Witzgall R, Schreiber R, Kunzelmann K. Calmodulin-dependent activation of the epithelial calcium-dependent chloride channel TMEM16A. FASEB J 25: 1058-1068, 2011.
53. Wang J, Novak I. Ion transport in human pancreatic duct epithelium, Capan-1 cells, is regulated by secretin, vip, acetylcholine, and purinergic receptors. Pancreas 2012 Sep 13. [Epub ahead of print].
54. 2+ response to both UTP and ATP at human P2Y11 receptors: evidence for agonist-specific signaling. Mol Pharmacol 63: 1356-1363, 2003.
55. Winpenny JP, Verdon B, McAlroy HL, Colledge WH, Ratcliff R, Evans MJ, Gray MA, Argent BE. Calcium-activated chloride conduc-tance is not increased in pancreatic duct cells of CF mice. Pflügers Arch 430: 26-33, 1995.
56. Wong AM, Chow AW, Au SC, Wong CC, Ko WH. Apical versus basolateral P2Y6 receptor-mediated Cl?secretion in immortalized bron-chial epithelia. Am J Respir Cell Mol Biol 40: 733-745, 2009.
57. Wulff H, Gutman GA, Cahalan MD, Chandy KG. Delineation of the clotrimazole/TRAM-34 binding site on the intermediate conductance calcium-activated potassium channel, IKCa1. J Biol Chem 276: 32040-32045, 2001.
58. 2+ -activated Cl?channel TMEM16A. PLos One 7: e38030, 2012.
59. Yerxa BR, Sabater JR, Davis CW, Stutts MJ, Lang-Furr M, Picher M, Jones AC, Cowlen M, Dougherty R, Boyer J, Abraham WM, Boucher RC. Pharmacology of INS37217 [P1-(uridine 5=)-P4-(2=-deoxy-cytidine 5=)tetraphosphate, tetrasodium salt], a next-generation P2Y2 receptor agonist for the treatment of cystic fibrosis. J Pharmacol Exp Ther 302: 871-880, 2002.
60. -channels can substitute for CFTR in stimulation of pancreatic duct bicarbonate secre-tion. FASEB J 14: 2345-2356, 2000.