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Serous cells are the predominant site of cystic fibrosis transmembrane conductance regulator expression in the airways, and they make a significant contribution to the volume, composition, and consistency of the submucosal gland secretions. We have employed the human airway serous cell line Calu-3 as a model system to investigate the mechanisms of serous cell anion secretion. Forskolin-stimulated Calu-3 cells secrete HCO–3 by a Cl –-independent, serosal Na+-dependent, serosal bumetanide-insensitive, and serosal 4,4'-dinitrostilben-2,2'-disulfonic acid (DNDS)–sensitive, electrogenic mechanism as judged by transepithelial currents, isotopic fluxes, and the results of ion substitution, pharmacology, and pH studies. Similar studies revealed that stimulation of Calu-3 cells with 1-ethyl-2-benzimidazolinone (1-EBIO), an activator of basolateral membrane Ca2+-activated K+ channels, reduced HCO–3 secretion and caused the secretion of Cl – by a bumetanide-sensitive, electrogenic mechanism. Nystatin permeabilization of Calu-3 monolayers demonstrated 1-EBIO activated a charybdotoxin- and clotrimazole- inhibited basolateral membrane K+ current. Patch-clamp studies confirmed the presence of an intermediate conductance inwardly rectified K+ channel with this pharmacological profile. We propose that hyperpolarization of the basolateral membrane voltage elicits a switch from HCO–3 secretion to Cl – secretion because the uptake of HCO–3 across the basolateral membrane is mediated by a 4,4 '-dinitrostilben-2,2'-disulfonic acid (DNDS)–sensitive Na+:HCO–3 cotransporter. Since the stoichiometry reported for Na +:HCO–3 cotransport is 1:2 or 1:3, hyperpolarization of the basolateral membrane potential by 1-EBIO would inhibit HCO–3 entry and favor the secretion of Cl –. Therefore, differential regulation of the basolateral membrane K+ conductance by secretory agonists could provide a means of stimulating HCO–3 and Cl – secretion. In this context, cystic fibrosis transmembrane conductance regulator could serve as both a HCO–3 and a Cl – channel, mediating the apical membrane exit of either anion depending on basolateral membrane anion entry mechanisms and the driving forces that prevail. If these results with Calu-3 cells accurately reflect the transport properties of native submucosal gland serous cells, then HCO–3 secretion in the human airways warrants greater attention.
Key Words: submucosal glands • cystic fibrosis • cystic fibrosis transmembrane conductance regulator • sodium bicarbonate cotransporter • serous cells
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J. Loffing, B. D. Moyer, D. Reynolds, B. E. Shmukler, S. L. Alper, and B. A. Stanton Functional and molecular characterization of an anion exchanger in airway serous epithelial cells Am J Physiol Cell Physiol, October 1, 2000; 279(4): C1016 - C1023. [Abstract] [Full Text] [PDF]
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D. C. Devor, R. J. Bridges, and J. M. Pilewski Pharmacological modulation of ion transport across wild-type and Delta F508 CFTR-expressing human bronchial epithelia Am J Physiol Cell Physiol, August 1, 2000; 279(2): C461 - C479. [Abstract] [Full Text] [PDF]
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C. A. Syme, A. C. Gerlach, A. K. Singh, and D. C. Devor Pharmacological activation of cloned intermediate- and small-conductance Ca2+-activated K+ channels Am J Physiol Cell Physiol, March 1, 2000; 278(3): C570 - C581. [Abstract] [Full Text] [PDF]
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A. K. Singh, D. C. Devor, A. C. Gerlach, M. Gondor, J. M. Pilewski, and R. J. Bridges Stimulation of Cl- Secretion by Chlorzoxazone J. Pharmacol. Exp. Ther., February 1, 2000; 292(2): 778 - 787. [Abstract] [Full Text]
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A. C. Gerlach, N. N. Gangopadhyay, and D. C. Devor Kinase-dependent Regulation of the Intermediate Conductance, Calcium-dependent Potassium Channel, hIK1 J. Biol. Chem., January 7, 2000; 275(1): 585 - 598. [Abstract] [Full Text] [PDF]
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P. Pedarzani, J. Mosbacher, A. Rivard, L. A. Cingolani, D. Oliver, M. Stocker, J. P. Adelman, and B. Fakler Control of Electrical Activity in Central Neurons by Modulating the Gating of Small Conductance Ca2+-activated K+ Channels J. Biol. Chem., March 23, 2001; 276(13): 9762 - 9769. [Abstract] [Full Text] [PDF]
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W. J. Joiner, R. Khanna, L. C. Schlichter, and L. K. Kaczmarek Calmodulin Regulates Assembly and Trafficking of SK4/IK1 Ca2+-activated K+ Channels J. Biol. Chem., October 5, 2001; 276(41): 37980 - 37985. [Abstract] [Full Text] [PDF]
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H. Wulff, G. A. Gutman, M. D. Cahalan, and K. G. Chandy Delineation of the Clotrimazole/TRAM-34 Binding Site on the Intermediate Conductance Calcium-activated Potassium Channel, IKCa1 J. Biol. Chem., August 17, 2001; 276(34): 32040 - 32045. [Abstract] [Full Text] [PDF]
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X. C. Sun and J. A. Bonanno Expression, localization, and functional evaluation of CFTR in bovine corneal endothelial cells Am J Physiol Cell Physiol, April 1, 2002; 282(4): C673 - C683. [Abstract] [Full Text] [PDF]
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C. M. Liedtke, R. Papay, and T. S. Cole Modulation of Na-K-2Cl cotransport by intracellular Cl- and protein kinase C-delta in Calu-3 cells Am J Physiol Lung Cell Mol Physiol, May 1, 2002; 282(5): L1151 - L1159. [Abstract] [Full Text] [PDF]
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A. Lazrak, U. Thome, C. Myles, J. Ware, L. Chen, C. J. Venglarik, and S. Matalon Alveolar Epithelial Ion and Fluid Transport: cAMP regulation of Cl- and HCO3- secretion across rat fetal distal lung epithelial cells Am J Physiol Lung Cell Mol Physiol, April 1, 2002; 282(4): L650 - L658. [Abstract] [Full Text] [PDF]
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