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J. Biol. Chem., Vol. 279, Issue 45, 46558-46565, November 5, 2004

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An Inwardly Rectifying Potassium Channel in Apical Membrane of Calu-3 Cells^*

Jin V. Wu, Mauri E. Krouse, Arjun Rustagi, Nam Soo Joo, and Jeffrey J. Wine

From the Cystic Fibrosis Research Laboratory, Stanford University, Stanford, California 94305-2130

Patch clamp methods and reverse transcription-polymerase chain reaction (RT-PCR) were used to characterize an apical K⁺ channel in Calu-3 cells, a widely used model of human airway gland serous cells. In cell-attached and excised apical membrane patches, we found an inwardly rectifying K⁺ channel (Kir). The permeability ratio was P_Na/P_K = 0.058. In 30 patches with both cystic fibrosis transmembrane conductance regulator and Kir present, we observed 79 cystic fibrosis transmembrane conductance regulator and 58 Kir channels. The average chord conductance was 24.4 ± 0.5 pS (n = 11), between 0 and –200 mV, and was 9.6 ± 0.7 pS (n = 8), between 0 and 50 mV; these magnitudes and their ratio of 2.5 are most similar to values for rectifying K⁺ channels of the Kir4.x subfamilies. We attempted to amplify transcripts for Kir4.1, Kir4.2, and Kir5.1; of these only Kir4.2 was present in Calu-3 lysates. The channel was only weakly activated by ATP and was relatively insensitive to internal pH. External Cs⁺ and Ba²⁺ blocked the channel with K_d values in the millimolar range. Quantitative modeling of Cl^– secreting epithelia suggests that secretion rates will be highest and luminal K⁺ will rise to 16–28 mM if 11–25% of the total cellular K⁺ conductance is placed in the apical membrane (Cook, D. I., and Young, J. A. (1989) J. Membr. Biol. 110, 139–146). Thus, we hypothesize that the K⁺ channel described here optimizes the rate of secretion and is involved in K⁺ recycling for the recently proposed apical H⁺-K⁺-ATPase in Calu-3 cells.

Received for publication, June 1, 2004 , and in revised form, August 20, 2004.

^* This work was supported by National Institutes of Health Grants DK-51817 and the Cystic Fibrosis Foundation. 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.

To whom correspondence should be addressed: Cystic Fibrosis Research Laboratory, Rm. 450, Bldg. 420, Main Quad, Stanford University, Stanford, CA 94305-2130. Tel.: 650-725-2462; Fax: 650-725-5699; E-mail: wine{at}stanford.edu.

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