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J. Biol. Chem., Vol. 281, Issue 32, 22992-23002, August 11, 2006
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Physiological Regulation of ATP Release at the Apical Surface of Human Airway Epithelia*
1
From the
Cystic Fibrosis/Pulmonary Research and Treatment Center, and the Department of Pharmacology, University of North Carolina, Chapel Hill, North Carolina 27599
Extracellular ATP and its metabolite adenosine regulate mucociliary clearance in airway epithelia. Little has been known, however, regarding the actual ATP and adenosine concentrations in the thin (
7 µm) liquid layer lining native airway surfaces and the link between ATP release/metabolism and autocrine/paracrine regulation of epithelial function. In this study, chimeric Staphylococcus aureus protein A-luciferase (SPA-luc) was bound to endogenous antigens on primary human bronchial epithelial (HBE) cell surface and ATP concentrations assessed in real-time in the thin airway surface liquid (ASL). ATP concentrations on resting cells were 1-10 nM. Inhibition of ecto-nucleotidases resulted in ATP accumulation at a rate of 250 fmol/min/cm2, reflecting the basal ATP release rate. Following hypotonic challenge to promote cell swelling, cell-surface ATP concentration measured by SPA-luc transiently reached 1 µM independent of ASL volume, reflecting a transient 3-log increase in ATP release rates. In contrast, peak ATP concentrations measured in bulk ASL by soluble luciferase inversely correlated with volume. ATP release rates were intracellular calcium-independent, suggesting that non-exocytotic ATP release from ciliated cells, which dominate our cultures, mediated hypotonicity-induced nucleotide release. However, the cystic fibrosis transmembrane conductance regulator (CFTR) did not participate in this function. Following the acute swelling phase, HBE cells exhibited regulatory volume decrease which was impaired by apyrase and facilitated by ATP or UTP. Our data provide the first evidence that ATP concentrations at the airway epithelial surface reach the range for P2Y2 receptor activation by physiological stimuli and identify a role for mucosal ATP release in airway epithelial cell volume regulation.
Received for publication, March 30, 2006 , and in revised form, June 2, 2006.
* This work was supported by the National Institutes of Health Grant NIH/NHLBI 5 P01 HL 34322-18 and Cystic Fibrosis Foundation Grant CFF R026-CR02 (both to R. C. B.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
This article was selected as a Paper of the Week.
1 To whom correspondence should be addressed. Tel.: 919-966-7045; Fax: 919-966-5178; E-mail: seiko_okada{at}med.unc.edu.
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