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J Biol Chem, Vol. 275, Issue 18, 13266-13274, May 5, 2000

Epithelial Sodium Channels Regulate Cystic Fibrosis Transmembrane Conductance Regulator Chloride Channels in Xenopus Oocytes*

Qinshi JiangDagger §, Jinqing LiDagger §, Rachael DubroffDagger , Yoon J. AhnDagger §, J. Kevin Foskett, John Engelhardt||, and Thomas R. KleymanDagger **

From the Departments of Dagger  Medicine and  Physiology, University of Pennsylvania and Veterans Affairs Medical Center, Philadelphia, Pennsylvania 19104-6144 and the || Department of Anatomy, University of Iowa, Iowa City, Iowa 52242

The cystic fibrosis transmembrane conductance regulator (CFTR), in addition to its well defined Cl- channel properties, regulates other ion channels. CFTR inhibits epithelial Na+ channel (ENaC) currents in many epithelial and nonepithelial cells. Because modulation of net NaCl reabsorption has important implications in extracellular fluid volume homeostasis and airway fluid volume and composition, we investigated whether this regulation was reciprocal by examining whether ENaC regulates CFTR. Co-expression of human (h) CFTR and mouse (m) alpha beta gamma ENaC in Xenopus oocytes resulted in a significant, 3.7-fold increase in whole-cell hCFTR Cl- conductance compared with oocytes expressing hCFTR alone. The forskolin/3-isobutyl-1-methylxanthine-stimulated whole-cell conductance in hCFTR-mENaC co-injected oocytes was amiloride-insensitive, indicating an inhibition of mENaC following hCFTR activation, and it was blocked by DPC (diphenylamine-2-carboxylic acid) and was DIDS (4,4'-diisothiocyanatostilbene-2,2'-disulfonic acid)-insensitive. Enhanced hCFTR Cl- conductance was also observed when either the alpha - or beta -subunit of mENaC was co-expressed with hCFTR, but this was not seen when CFTR was co-expressed with the gamma -subunit of mENaC. Single Cl- channel analyses showed that both CFTR Cl- channel open probability and the number of CFTR Cl- channels detected per patch increased when hCFTR was co-expressed with alpha beta gamma mENaC. We conclude that in addition to acting as a regulator of ENaC, CFTR activity is regulated by ENaC.

* This work was supported in part by grants from the Cystic Fibrosis Foundation (to J. K. F. and T. R. K.) and by National Institutes of Health Grant DK56305.The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

§ Recipients of postdoctoral fellowship awards from the Cystic Fibrosis Foundation.

** To whom correspondence should be addressed: Renal Division, University of Pennsylvania, 700 CRB, 415 Curie Blvd., Philadelphia, PA 19104-6144. Tel.: 215-573-1848; Fax: 215-898-0189; E-mail: kleyman@mail.med.upenn.edu.

Copyright © 2000 by The American Society for Biochemistry and Molecular Biology, Inc.
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