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NaCl and fluid secretion by the intestine of the teleost Fundulus heteroclitus: involvement of CFTR
Department of Biology, St Francis Xavier University, Antigonish, Nova Scotia, Canada B2G 2W5
*e-mail: bmarshal{at}stfx.ca
Accepted 9 January 2002
Sections of posterior intestine of the euryhaline killifish Fundulus heteroclitus adapted to sea water were stimulated by the calcium ionophore ionomycin (1 µmol l–1) in combination with agents to elevate intracellular cyclic AMP levels, 0.5 mmol l–1 dibutyryl-cyclic AMP (db-cAMP) with 0.1 mmol l–1 3-isobutyl-1-methylxanthine (IBMX). Intestinal bag preparations from recently fed animals (but not from overnight unfed animals) changed from fluid absorption (+18.9±8.30 µl cm–2 h–1 , N=8) in the untreated control period to net fluid secretion after stimulation (–7.43±1.30 µl cm–2 h–1, N=8, P<0.01; means ± S.E.M.), indicative of the capacity of teleost intestine to undergo secretion. Posterior intestinal pieces mounted in vitro in Ussing-style membrane chambers showed net Cl– uptake (+2.245±0.633 µequiv cm–2 h–1, N=7) that turned to net secretion following stimulation by ionomycin + db-cAMP + IBMX (–3.809±1.22 µequiv cm–2 h–1, N=7, P<0.01). Mucosal application of the anion channel blocker 1 mmol l–1 diphenylamine-2-carboxylate (DPC) after ionomycin + db-cAMP + IBMX treatment significantly reduced serosal-to-mucosal unidirectional Cl– flux (P<0.001), net Cl– flux (P<0.05), short-circuit current (Isc, P<0.001) and tissue conductance (Gt, P<0.001), while 0.1 mmol l–1 4,4'-diisothiocyano-2,2'-stilbene-disulphonic acid (DIDS, a blocker of anion exchange) was without effect. Stimulation by db-cAMP + IBMX (no ionomycin) significantly increased unidirectional fluxes, Isc and Gt but did not produce net Cl– secretion. Ionomycin alone produced a transient increase in Isc but had no effect on Gt and caused no significant changes in unidirectional or net Cl– fluxes. Addition of db-cAMP + IBMX after ionomycin treatment produced net secretion of Cl– and large increases in unidirectional fluxes and Gt. Cystic fibrosis transmembrane conductance regulator (CFTR) was immunocytochemically localized with a monoclonal mouse antibody to the carboxy terminus and found to be present in the cytoplasm and basolateral membranes of all enterocytes and in the brush-border membrane of some cells, whereas NKCC immunofluorescence, demonstrating the presence of the Na+/K+/2Cl– cotransporter, was present in the cytoplasm and brush-border membrane. We conclude that the teleost intestine is capable of salt and fluid secretion only if intracellular Ca2+ and cyclic AMP pathways are stimulated together and that this secretion appears to involve activation of CFTR ion channels in the apical membrane of a subpopulation of enterocytes.
Key words: epithelium, ion transport, cystic fibrosis transmembrane conductance regulator, immunocytochemistry, secretory diarrhoea, Na+/K+/2Cl– cotransporter, Na+/K+-ATPase, osmoregulation, ionomycin, cyclic AMP.
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