A role for two-pore K + channels in modulating Na + absorption and Cl - secretion in normal human bronchial epithelial cells

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 302, Issue 1, 2012, Pages

  Zhao, Ke Qing ^a,b   Xiong, Guoxiang ^c   Wilber, Morgan ^c   Cohen, Noam A ^b,d   Kreindler, James L ^b,c  

^a FUDAN UNIVERSITY   (China)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Chloride secretion; Cystic fibrosis; Ion transport

Indexed keywords

AMILORIDE; BUPIVACAINE; CHLORIDE ION; FORSKOLIN; POTASSIUM CHANNEL; POTASSIUM CHANNEL KCNK1; POTASSIUM CHANNEL KCNK2; POTASSIUM CHANNEL KCNK5; POTASSIUM CHANNEL KCNK6; QUINIDINE; SODIUM ION; TWO PORE POTASSIUM CHANNEL; UNCLASSIFIED DRUG;

ARTICLE; BRONCHUS MUCOSA; EPITHELIUM CELL; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ABSORPTION; AMILORIDE; BRONCHI; BUPIVACAINE; CELL LINE; CELL POLARITY; CHLORIDES; EPITHELIAL CELLS; FORSKOLIN; HUMANS; IMMUNOHISTOCHEMISTRY; ION TRANSPORT; POTASSIUM CHANNEL BLOCKERS; POTASSIUM CHANNELS, TANDEM PORE DOMAIN; QUINIDINE; RESPIRATORY MUCOSA; SODIUM;

EID: 83755173577     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00102.2011     Document Type: Article

References (34)

1. Anderson MP, Gregory RJ, Thompson S, Souza DW, Paul S, Mulligan RC, Smith AE, Welsh MJ. Demonstration that CFTR is a chloride channel by alteration of its anion selectivity. Science 253: 202-205, 1991.
2. Bardou O, Trinh NT, Brochiero E. Molecular diversity and function of K_ channels in airway and alveolar epithelial cells. Am J Physiol Lung Cell Mol Physiol 296: L145-L155, 2009.
3. Bernard K, Bogliolo S, Soriani O, Ehrenfeld J. Modulation of calciumdependent chloride secretion by basolateral SK4-like channels in a human bronchial cell line. J Membr Biol 196: 15, 2003.
4. Boucher RC. New concepts of the pathogenesis of cystic fibrosis lung disease. Eur Respir J 23: 146-158, 2004.
5. Chen JH, Stoltz DA, Karp PH, Ernst SE, Pezzulo AA, Moninger TO, Rector MV, Reznikov LR, Launspach JL, Chaloner K, Zabner J, Welsh MJ. Loss of anion transport without increased sodium absorption characterizes newborn porcine cystic fibrosis airway epithelia. Cell 143: 911-923, 2010.
6. Cook DI, Young JA. Effect of K_ channels in the apical plasma membrane on epithelial secretion based on secondary active Cl_ transport. J Membr Biol 110: 139-146, 1989.
7. Cowley EA, Linsdell P. Characterization of basolateral K_ channels underlying anion secretion in the human airway cell line Calu-3. J Physiol 538: 747-757, 2002.
8. Davis KA, Cowley EA. Two-pore-domain potassium channels support anion secretion from human airway Calu-3 epithelial cells. Pflügers Arch 451: 631-641, 2006.
9. Dawson DC, Richards NW. Basolateral K conductance: role in regulation of NaCl absorption and secretion. Am J Physiol Cell Physiol 259: C181-C195, 1990.
10. Devor DC, Bridges RJ, Pilewski JM. Pharmacological modulation of ion transport across wild-type and _F508 CFTR-expressing human bronchial epithelia. Am J Physiol Cell Physiol 279: C461-C479, 2000.
11. Devor DC, Singh AK, Bridges RJ, Frizzell RA. Modulation of Cl_ secretion by benzimidazolones. II. Coordinate regulation of apical GCl and basolateral GK. Am J Physiol Lung Cell Mol Physiol 271: L785-L795, 1996.
12. Gray TE, Guzman K, Davis CW, Abdullah LH, Nettesheim P. Mucociliary differentiation of serially passaged normal human tracheobronchial epithelial cells. Am J Respir Cell Mol Biol 14: 104-112, 1996.
13. Halm DR, Frizzell RA. Intestinal chloride secretion. In: Textbook of Secretory Diarrhea, edited by Lebenthal E, Duffey M. New York: Raven, 1990, p. 47-58.
14. Han DY, Nie HG, Gu X, Nayak RC, Su XF, Fu J, Chang Y, Rao V, Ji HL. K_ channel openers restore verapamil-inhibited lung fluid resolution and transepithelial ion transport. Respir Res 11: 65, 2010.
15. Inglis SK, Brown SG, Constable MJ, McTavish N, Olver RE, Wilson SM. A Ba2_-resistant, acid-sensitive K_ conductance in Na_-absorbing H441 human airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 292: L1304-L1312, 2007.
16. Joo NS, Irokawa T, Robbins RC, Wine JJ. Hyposecretion, not hyperabsorption, is the basic defect of cystic fibrosis airway glands. J Biol Chem 281: 7392-7398, 2006.
17. Kerem E, Bistritzer T, Hanukoglu A, Hofmann T, Zhou Z, Bennett W, MacLaughlin E, Barker P, Nash M, Quittell L, Boucher R, Knowles MR. Pulmonary epithelial sodium-channel dysfunction and excess airway liquid in pseudohypoaldosteronism. N Engl J Med 341: 156-162, 1999.
18. Kim D. Physiology and pharmacology of two-pore domain potassium channels. Curr Pharm Des 11: 2717-2736, 2005.
19. Kreindler JL, Bertrand CA, Lee RJ, Karasic T, Aujla S, Pilewski JM, Frizzell RA, Kolls JK. Interleukin-17A induces bicarbonate secretion in normal human bronchial epithelial cells. Am J Physiol Lung Cell Mol Physiol 296: L257-L266, 2009.
20. Kreindler JL, Jackson AD, Kemp PA, Bridges RJ, Danahay H. Inhibition of chloride secretion in human bronchial epithelial cells by cigarette smoke extract. Am J Physiol Lung Cell Mol Physiol 288: L894-L902, 2005.
21. Lotshaw D. Biophysical, pharmacological, and functional characteristics of cloned and native mammalian two-pore domain K_ channels. Cell Biochem Biophys 47: 209-256, 2007.
22. Mall M, Grubb BR, Harkema JR, O'Neal WK, Boucher RC. Increased airway epithelial Na_ absorption produces cystic fibrosis-like lung disease in mice. Nat Med 10: 487-493, 2004.
23. Matsui H, Grubb BR, Tarran R, Randell SH, Gatzy JT, Davis CW, Boucher RC. Evidence for periciliary liquid layer depletion, not abnormal ion composition, in the pathogenesis of cystic fibrosis airways disease. Cell 95: 1005-1015, 1998.
24. Moser SL, Harron SA, Crack J, Fawcett JP, Cowley EA. Multiple KCNQ potassium channel subtypes mediate basal anion secretion from the human airway epithelial cell line Calu-3. J Membr Biol 221: 153-163, 2008.
25. Namkung W, Song Y, Mills AD, Padmawar P, Finkbeiner WE, Verkman AS. Insitu measurement of airway surface liquid [K_] using a ratioable K_-sensitive fluorescent dye. J Biol Chem 284: 15916-15926, 2009.
26. Namkung W, Song Y, Mills AD, Padmawar P, Finkbeiner WE, Verkman AS. Insitu measurement of airway surface liquid [K_] using a ratioable K_-sensitive fluorescent dye. J Biol Chem 284: 15916-15926, 2009.
27. Rich DP, Anderson MP, Gregory RJ, Cheng SH, Paul S, Jefferson DM, McCann JD, Klinger KW, Smith AE, Welsh MJ. Expression of cystic fibrosis transmembrane conductance regulator corrects defective chloride channel regulation in cystic fibrosis airway epithelial cells. Nature 347: 358-363, 1990.
28. Savitski AN, Mesaros C, Blair IA, Cohen NA, Kreindler JL. Secondhand smoke inhibits both Cl_ and K_ conductances in normal human bronchial epithelial cells. Respir Res 10: 120, 2009.
29. Shah AS, Ben-Shahar Y, Moninger TO, Kline JN, Welsh MJ. Motile cilia of human airway epithelia are chemosensory. Science 325: 1131-1134, 2009.
30. Shen BQ, Finkbeiner WE, Wine JJ, Mrsny RJ, Widdicombe JH. Calu-3: a human airway epithelial cell line that shows cAMP-dependent Cl_ secretion. Am J Physiol Lung Cell Mol Physiol 266: L493-L501, 1994.
31. Smith PL, Frizzell RA. Chloride secretion by canine tracheal epithelium: IV. Basolateral membrane K permeability parallels secretion rate. J Membr Biol 77: 187-199, 1984.
32. Sood N, Bennett WD, Zeman K, Brown J, Foy C, Boucher RC, Knowles MR. Increasing concentration of inhaled saline with or without amiloride: effect on mucociliary clearance in normal subjects. Am J Respir Crit Care Med 167: 158-163, 2003.
33. Willumsen NJ, Davis CW, Boucher RC. Intracellular Cl_ activity and cellular Cl_ pathways in cultured human airway epithelium. Am J Physiol Cell Physiol 256: C1033-C1044, 1989.
34. Wu JV, Krouse ME, Rustagi A, Joo NS, Wine JJ. An inwardly rectifying potassium channel in apical membrane of Calu-3 cells. J Biol Chem 279: 46558-46565, 2004.