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Volume 272, Number 20, Issue of May 16, 1997 pp. 12984-12988
©1997 by The American Society for Biochemistry and Molecular Biology, Inc.

Secretin Promotes Osmotic Water Transport in Rat Cholangiocytes by Increasing Aquaporin-1 Water Channels in Plasma Membrane
EVIDENCE FOR A SECRETIN-INDUCED VESICULAR TRANSLOCATION OF AQUAPORIN-1

(Received for publication, December 24, 1996, and in revised form, March 6, 1997)

Raul A. Marinelli , Linh Pham , Peter Agre ^§ and Nicholas F. LaRusso

From the  Center for Basic Research in Digestive Diseases, Departments of Internal Medicine, Biochemistry, and Molecular Biology, Mayo Clinic and Foundation, Mayo Medical School, Rochester, Minnesota 55905 and the ^§ Departments of Biological Chemistry and Medicine, The Johns Hopkins University School of Medicine, Baltimore, Maryland 21205

Although secretin is known to stimulate ductal bile secretion by directly interacting with cholangiocytes, the precise cellular mechanisms accounting for this choleretic effect are unknown. We have previously shown that secretin stimulates exocytosis in cholangiocytes and that these cells transport water mainly via the water channel aquaporin-1 (AQP1). In this study, we tested the hypothesis that secretin promotes osmotic water movement in cholangiocytes by inducing the exocytic insertion of AQP1 into plasma membranes. Exposure of highly purified isolated rat cholangiocytes to secretin caused significant, dose-dependent increases in osmotic membrane water permeability (P_f) (e.g. increased by 60% with 10⁷ M secretin), which was reversibly inhibited by the water channel blocker HgCl₂. Immunoblotting analysis of cholangiocyte membrane fractions showed that secretin caused up to a 3-fold increase in the amount of AQP1 in plasma membranes and a proportional decrease in the amount of the water channel in microsomes, suggesting a secretin-induced redistribution of AQP1 from intracellular to plasma membranes. Both the secretin-induced increase in cholangiocyte P_f and AQP1 redistribution were blocked by two perturbations that inhibit secretin-stimulated exocytosis in cholangiocytes, i.e. treatment with colchicine and exposure at low temperatures (20 and 4 °C). Our results demonstrate that secretin increases AQP1-mediated P_f in cholangiocytes. Moreover, our studies implicate the microtubule-dependent vesicular translocation of AQP1 water channels to the plasma membrane, a mechanism that appears to be essential for secretin-induced ductal bile secretion and suggests that AQP1 can be regulated by membrane trafficking.

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