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The Journal of Experimental Biology 205, 745-758 (2002)
© 2002 The Company of Biologists Limited

NaCl and fluid secretion by the intestine of the teleost Fundulus heteroclitus: involvement of CFTR

W. S. Marshall^*, J. A. Howard, R. R. F. Cozzi and E. M. Lynch

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 (I_sc, P<0.001) and tissue conductance (G_t, 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, I_sc and G_t but did not produce net Cl^– secretion. Ionomycin alone produced a transient increase in I_sc but had no effect on G_t 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 G_t. 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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