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Volume 272, Number 52, Issue of December 26, 1997 pp. 32956-32965

Membrane-specific Regulation of Cl Channels by Purinergic Receptors in Rat Submandibular Gland Acinar and Duct Cells

(Received for publication, June 23, 1997, and in revised form, October 21, 1997)

From the Department of Physiology, University of Texas Southwestern Medical Center, Dallas, Texas 75235

Measurement of [Cl]_i and the Cl current in the rat salivary submandibular gland (SMG) acinar and duct cells was used to evaluate the role of Cl channels in the regulation of [Cl]_i during purinergic stimulation. Under resting conditions [Cl]_i averaged 56 ± 8 and 26 ± 7 mM in acinar and duct cells, respectively. In both cells, stimulation with 1 mM ATP resulted in Cl efflux and subsequent influx. Inhibition of NaKCl₂ cotransport had no effect on [Cl]_i changes in duct cells and inhibited only about 50% of Cl uptake in acinar cells. Accordingly, low levels of expression of NaKCl₂ cotransporter protein were found in duct cells. Acinar cells expressed high levels of the cotransporter. Measurement of Cl current under selective conditions revealed that acinar and duct cells express at least five distinct Cl channels; a ClCO-like, volume-sensitive, inward rectifying, Ca²⁺-activated and CFTR-like Cl currents. ATP acting on both cell types activated at least two channels, the Ca²⁺-activated Cl channel and a Ca²⁺-independent glibenclamide-sensitive Cl-current, possibly cystic fibrosis transmembrane regulator (CFTR). Of the many nucleotides tested only 2-3-benzoylbenzoyl (Bz)-ATP and UTP activated Cl channels in SMG cells. Despite their relative potency in increasing [Ca²⁺]_i, BzATP in both SMG cell types largely activated the Ca²⁺-independent, glibenclamide-sensitive Cl current, whereas UTP activated only the Ca²⁺-dependent Cl current. We interpret this to suggest that BzATP and UTP largely activate Cl channels residing in the membrane expressing the receptor for the active nucleotide. The present studies reveal a potentially new mechanism for transcellular Cl transport in a CFTR-expressing tissue, the SMG. Coordinated action of the P₂z (luminal) and P₂u (basolateral) receptors can mediate part of the transcellular Cl transport by acinar and duct cells to determine the final electrolyte composition of salivary fluid.

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