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Originally published In Press as doi:10.1074/jbc.M002316200 on June 6, 2000

J. Biol. Chem., Vol. 275, Issue 35, 26906-26913, September 1, 2000
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myo-Inositol 3,4,5,6-Tetrakisphosphate Inhibits an Apical Calcium-activated Chloride Conductance in Polarized Monolayers of a Cystic Fibrosis Cell Line*

Mark A. CarewDagger §, Xiaonian YangDagger , Carsten Schultz, and Stephen B. ShearsDagger

From the Dagger  Inositide Signaling Section, Laboratory of Signal Transduction, NIEHS, National Institutes of Health, Research Triangle Park, North Carolina 27709 and the  Institut für Organische Chemie, Universität Bremen, UFT, 28359 Bremen, Germany

Does inositol 3,4,5,6-tetrakisphosphate (Ins(3,4,5,6)P4) inhibit apical Ca2+-activated Cl- conductance (CaCC)? We studied this question using human CFPAC-1 pancreatoma cells grown in polarized monolayers. Cellular Ins(3,4,5,6)P4 levels were acutely sensitive to purinergic receptor activation, rising 3-fold within 1 min of agonist addition. Intracellular Ins(3,4,5,6)P4 levels were therefore specifically elevated, independently of receptor activation, by incubating cells with a cell-permeant bioactivable analogue, 1,2-di-O-butyl-myo-inositol 3,4,5,6-tetrakisphosphate octakis(acetoxymethyl)ester (Bt2Ins (3,4,5,6)P4/AM). The latter inhibited Ca2+-activated Cl- secretion by 60%. We next used nystatin to selectively permeabilize the basolateral membrane to monovalent anions and cations, thereby preventing this membrane from electrochemically dominating ion movements through the apical membrane. Thus, we studied autonomous regulation of apical Cl- channels in situ. The properties of Cl- flux across the apical membrane were those expected of CaCC: niflumic acid sensitivity, outward rectification, and 2-fold greater permeability of I- over Cl-. Following nystatin-treatment, we elevated intracellular levels of Ins(3,4,5,6)P4 with either purinergic agonists or with Bt2Ins(3,4,5,6)P4/AM. Both protocols inhibited Ca2+-activated Cl- secretion (up to 70%). These studies provide the first demonstration that, in a physiologically relevant context of a polarized monolayer, there is an apical, Ins(3,4,5,6)P4-inhibited CaCC.

* 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.

§ To whom correspondence should be addressed. Tel.: 919-541-2630; Fax: 919-541-0559; E-mail: Carew@niehs.nih.gov.

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